Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 513518, 16 pages
http://dx.doi.org/10.1155/2015/513518
Review Article

Triggers, Inhibitors, Mechanisms, and Significance of Eryptosis: The Suicidal Erythrocyte Death

Department of Physiology, University of Tübingen, Gmelinstrasse 5, 72076 Tübingen, Germany

Received 16 June 2014; Revised 12 January 2015; Accepted 15 January 2015

Academic Editor: Ulrich Salzer

Copyright © 2015 Elisabeth Lang and Florian Lang. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Arese, F. Turrini, and E. Schwarzer, “Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes,” Cellular Physiology and Biochemistry, vol. 16, no. 4–6, pp. 133–146, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. G. J. C. G. M. Bosman, F. L. A. Willekens, and J. M. Werre, “Erythrocyte aging: a more than superficial resemblance to apoptosis?” Cellular Physiology and Biochemistry, vol. 16, no. 1–3, pp. 1–8, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. C. R. Kiefer and L. M. Snyder, “Oxidation and erythrocyte senescence,” Current Opinion in Hematology, vol. 7, no. 2, pp. 113–116, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. H. U. Lutz, “Innate immune and non-immune mediators of erythrocyte clearance,” Cellular and Molecular Biology, vol. 50, no. 2, pp. 107–116, 2004. View at Google Scholar
  5. F. Lang, K. S. Lang, P. A. Lang, S. M. Huber, and T. Wieder, “Mechanisms and significance of eryptosis,” Antioxidants & Redox Signaling, vol. 8, no. 7-8, pp. 1183–1192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Lang, S. M. Qadri, and F. Lang, “Killing me softly—suicidal erythrocyte death,” International Journal of Biochemistry and Cell Biology, vol. 44, no. 8, pp. 1236–1243, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Y. B. Çimen, “Free radical metabolism in human erythrocytes,” Clinica Chimica Acta, vol. 390, no. 1-2, pp. 1–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Föller, D. Bobbala, S. Koka, S. M. Huber, E. Gulbins, and F. Lang, “Suicide for survival—death of infected erythrocytes as a host mechanism to survive malaria,” Cellular Physiology and Biochemistry, vol. 24, no. 3-4, pp. 133–140, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. D. B. Nguyen, L. Wagner-Britz, S. Maia et al., “Regulation of phosphatidylserine exposure in red blood cells,” Cellular Physiology and Biochemistry, vol. 28, no. 5, pp. 847–856, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Lang and S. M. Qadri, “Mechanisms and significance of eryptosis, the suicidal death of erythrocytes,” Blood Purification, vol. 33, no. 1–3, pp. 125–130, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Lang, M. Abed, E. Lang, and M. Föller, “Oxidative stress and suicidal erythrocyte death,” Antioxidants & Redox Signaling, vol. 21, no. 1, pp. 138–153, 2014. View at Publisher · View at Google Scholar
  12. F. Lang, E. Lang, and M. Fller, “Physiology and pathophysiology of eryptosis,” Transfusion Medicine and Hemotherapy, vol. 39, no. 5, pp. 308–314, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. K. S. Lang, C. Duranton, H. Poehlmann et al., “Cation channels trigger apoptotic death of erythrocytes,” Cell Death and Differentiation, vol. 10, no. 2, pp. 249–256, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. B. A. Klarl, P. A. Lang, D. S. Kempe et al., “Protein kinase C mediates erythrocyte “programmed cell death” following glucose depletion,” The American Journal of Physiology—Cell Physiology, vol. 290, no. 1, pp. C244–C253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Kamp, T. Sieberg, and C. W. M. Haest, “Inhibition and stimulation of phospholipid scrambling activity. Consequences for lipid asymmetry, echinocytosis, and microvesiculation of erythrocytes,” Biochemistry, vol. 40, no. 31, pp. 9438–9446, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Foller, H. Mahmud, S. Gu et al., “Participation of leukotriene C4 in the regulation of suicidal erythrocyte death,” Journal of Physiology and Pharmacology, vol. 60, no. 3, pp. 135–143, 2009. View at Google Scholar · View at Scopus
  17. J. P. Nicolay, G. Liebig, O. M. Niemoeller et al., “Inhibition of suicidal erythrocyte death by nitric oxide,” Pflugers Archiv European Journal of Physiology, vol. 456, no. 2, pp. 293–305, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. D. M. Vota, R. L. Crisp, A. B. Nesse, and D. C. Vittori, “Oxidative stress due to aluminum exposure induces eryptosis which is prevented by erythropoietin,” Journal of Cellular Biochemistry, vol. 113, no. 5, pp. 1581–1589, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Myssina, S. M. Huber, C. Birka et al., “Inhibition of erythrocyte cation channels by erythropoietin,” Journal of the American Society of Nephrology, vol. 14, no. 11, pp. 2750–2757, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Ghashghaeinia, J. C. A. Cluitmans, A. Akel et al., “The impact of erythrocyte age on eryptosis,” British Journal of Haematology, vol. 157, no. 5, pp. 606–614, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Rice and C. P. Alfrey, “The negative regulation of red cell mass by neocytolysis: physiologic and pathophysiologic manifestations,” Cellular Physiology and Biochemistry, vol. 15, no. 6, pp. 245–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Hermle, E. Shumilina, P. Attanasio et al., “Decreased cation channel activity and blunted channel-dependent eryptosis in neonatal erythrocytes,” The American Journal of Physiology—Cell Physiology, vol. 291, no. 4, pp. C710–C717, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. S. K. Jain, “Presence of phosphatidylserine in the outer membrane bilayer of newborn human erythrocytes,” Biochemical and Biophysical Research Communications, vol. 136, no. 3, pp. 914–920, 1986. View at Publisher · View at Google Scholar · View at Scopus
  24. B. N. Y. Setty, S. Kulkarni, A. K. Rao, and M. J. Stuart, “Fetal hemoglobin in sickle cell disease: relationship to erythrocyte phosphatidylserine exposure and coagulation activation,” Blood, vol. 96, no. 3, pp. 1119–1124, 2000. View at Google Scholar · View at Scopus
  25. S. G. Bell, “An introduction to hemoglobin physiology,” Neonatal Network, vol. 18, no. 2, pp. 9–15, 1999. View at Google Scholar · View at Scopus
  26. M. Föller, R. S. Kasinathan, S. Koka et al., “TRPC6 contributes to the Ca2+ leak of human erythrocytes,” Cellular Physiology and Biochemistry, vol. 21, no. 1–3, pp. 183–192, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Föller, M. Sopjani, S. Koka et al., “Regulation of erythrocyte survival by AMP-activated protein kinase,” The FASEB Journal, vol. 23, no. 4, pp. 1072–1080, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Duranton, S. M. Huber, and F. Lang, “Oxidation induces a Cl-dependent cation conductance in human red blood cells,” Journal of Physiology, vol. 539, no. 3, pp. 847–855, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. P. A. Lang, D. S. Kempe, S. Myssina et al., “PGE2 in the regulation of programmed erythrocyte death,” Cell Death and Differentiation, vol. 12, no. 5, pp. 415–428, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Kaestner and I. Bernhardt, “Ion channels in the human red blood cell membrane: their further investigation and physiological relevance,” Bioelectrochemistry, vol. 55, no. 1-2, pp. 71–74, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Föller, I. S. Harris, A. Elia et al., “Functional significance of glutamate-cysteine ligase modifier for erythrocyte survival in vitro and in vivo,” Cell Death and Differentiation, vol. 20, no. 10, pp. 1350–1358, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Bilmen, T. A. Aksu, S. Gümüşlü, D. K. Korgun, and D. Canatan, “Antioxidant capacity of G-6-PD-deficient erythrocytes,” Clinica Chimica Acta, vol. 303, no. 1-2, pp. 83–86, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. I. Mavelli, M. R. Ciriolo, L. Rossi et al., “Favism: a hemolytic disease associated with increased superoxide dismutase and decreased glutathione peroxidase activities in red blood cells,” European Journal of Biochemistry, vol. 139, no. 1, pp. 13–18, 1984. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Damonte, L. Guida, A. Sdraffa et al., “Mechanisms of perturbation of erythrocyte calcium homeostasis in favism,” Cell Calcium, vol. 13, no. 10, pp. 649–658, 1992. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Gökkuşu and T. Mostafazadeh, “Changes of oxidative stress in various tissues by long-term administration of vitamin E in hypercholesterolemic rats,” Clinica Chimica Acta, vol. 328, no. 1-2, pp. 155–161, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Kobayashi, H. Moriya, K. Aso, and T. Ohtake, “Vitamin E-bonded hemodialyzer improves atherosclerosis associated with a rheological improvement of circulating red blood cells,” Kidney International, vol. 63, no. 5, pp. 1881–1887, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. S. K. Jain, “Vitamin E and stabilization of membrane lipid organization in red blood cells with peroxidative damage,” Biomedica Biochimica Acta, vol. 42, no. 11-12, pp. S43–S47, 1983. View at Google Scholar · View at Scopus
  38. U. J. Dumaswala, M. J. Wilson, Y. L. Wu et al., “Glutathione loading prevents free radical injury in red blood cells after storage,” Free Radical Research, vol. 33, no. 5, pp. 517–529, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. E. W. Qian, D. T. Ge, and S.-K. Kong, “Salidroside protects human erythrocytes against hydrogen peroxide-induced apoptosis,” Journal of Natural Products, vol. 75, no. 4, pp. 531–537, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. L. de Franceschi, F. Turrini, M. Honczarenko et al., “In vivo reduction of erythrocyte oxidant stress in a murine model of β-thalassemia,” Haematologica, vol. 89, no. 11, pp. 1287–1298, 2004. View at Google Scholar · View at Scopus
  41. R. M. Bookchin, O. E. Ortiz, and V. L. Lew, “Activation of calcium-dependent potassium channels in deoxygenated sickled red cells,” Progress in Clinical and Biological Research, vol. 240, pp. 193–200, 1987. View at Google Scholar · View at Scopus
  42. C. Brugnara, L. De Franceschi, and S. L. Alper, “Inhibition of Ca2+-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives,” Journal of Clinical Investigation, vol. 92, no. 1, pp. 520–526, 1993. View at Publisher · View at Google Scholar · View at Scopus
  43. P. A. Lang, S. Kaiser, S. Myssina, T. Wieder, F. Lang, and S. M. Huber, “Role of Ca2+-activated K+ channels in human erythrocyte apoptosis,” The American Journal of Physiology—Cell Physiology, vol. 285, no. 6, pp. C1553–C1560, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Myssina, P. A. Lang, D. S. Kempe et al., “Cl -channel blockers NPPB and niflumic acid blunt Ca2+-induced erythrocyte ‘apoptosis’,” Cellular Physiology and Biochemistry, vol. 14, no. 4–6, pp. 241–248, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. S. M. Huber, A.-C. Uhlemann, N. L. Gamper, C. Duranton, P. G. Kremsner, and F. Lang, “Plasmodium falciparum activates endogenous Cl channels of human erythrocytes by membrane oxidation,” The EMBO Journal, vol. 21, no. 1-2, pp. 22–30, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. V. Tanneur, C. Duranton, V. B. Brand et al., “Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes,” FASEB Journal, vol. 20, no. 1, pp. 133–135, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Lang, G. L. Busch, M. Ritter et al., “Functional significance of cell volume regulatory mechanisms,” Physiological Reviews, vol. 78, no. 1, pp. 247–306, 1998. View at Google Scholar · View at Scopus
  48. C. P. Berg, I. H. Engels, A. Rothbart et al., “Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis,” Cell Death and Differentiation, vol. 8, no. 12, pp. 1197–1206, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. M. S. E. Ahmed, H. Langer, M. Abed, J. Voelkl, and F. Lang, “The uremic toxin acrolein promotes suicidal erythrocyte death,” Kidney and Blood Pressure Research, vol. 37, no. 2-3, pp. 158–167, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. S. K. Bhavsar, D. Bobbala, N. T. Xuan, M. Föller, and F. Lang, “Stimulation of suicidal erythrocyte death by α-lipoic acid,” Cellular Physiology and Biochemistry, vol. 26, no. 6, pp. 859–868, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. O. M. Niemoeller, V. Kiedaisch, P. Dreischer, T. Wieder, and F. Lang, “Stimulation of eryptosis by aluminium ions,” Toxicology and Applied Pharmacology, vol. 217, no. 2, pp. 168–175, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Föller, C. Geiger, H. Mahmud, J. Nicolay, and F. Lang, “Stimulation of suicidal erythrocyte death by amantadine,” European Journal of Pharmacology, vol. 581, no. 1-2, pp. 13–18, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. J. P. Nicolay, P. J. Bentzen, M. Ghashghaeinia, T. Wieder, and F. Lang, “Stimulation of erythrocyte cell membrane scrambling by amiodarone,” Cellular Physiology and Biochemistry, vol. 20, no. 6, pp. 1043–1050, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Mahmud, D. Mauro, S. M. Qadri, M. Föller, and F. Lang, “Triggering of suicidal erythrocyte death by Amphotericin B,” Cellular Physiology and Biochemistry, vol. 24, no. 3-4, pp. 263–270, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. J. P. Nicolay, S. Gatz, G. Liebig, E. Gulbins, and F. Lang, “Amyloid induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 19, no. 1–4, pp. 175–184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. P. J. Bentzen and F. Lang, “Effect of anandamide on erythrocyte survival,” Cellular Physiology and Biochemistry, vol. 20, no. 6, pp. 1033–1042, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Attanasio, E. Shumilina, T. Hermle et al., “Stimulation of eryptosis by anti-A IgG antibodies,” Cellular Physiology and Biochemistry, vol. 20, no. 5, pp. 591–600, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Zbidah, A. Lupescu, K. Jilani et al., “Apigenin-induced suicidal erythrocyte death,” Journal of Agricultural and Food Chemistry, vol. 60, no. 1, pp. 533–538, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Malik, R. Bissinger, S. Calabrò, C. Faggio, K. Jilani, and F. Lang, “Aristolochic acid induced suicidal erythrocyte death,” Kidney and Blood Pressure Research, vol. 39, no. 5, pp. 408–419, 2014. View at Publisher · View at Google Scholar
  60. D. Biswas, M. Banerjee, G. Sen et al., “Mechanism of erythrocyte death in human population exposed to arsenic through drinking water,” Toxicology and Applied Pharmacology, vol. 230, no. 1, pp. 57–66, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Mahmud, M. Föller, and F. Lang, “Arsenic-induced suicidal erythrocyte death,” Archives of Toxicology, vol. 83, no. 2, pp. 107–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Alzoubi, S. Calabrò, R. Bissinger, M. Abed, C. Faggio, and F. Lang, “Stimulation of suicidal erythrocyte death by artesunate,” Cellular Physiology and Biochemistry, vol. 34, no. 6, pp. 2232–2244, 2014. View at Publisher · View at Google Scholar
  63. D. Bobbala, S. Koka, C. Geiger, M. Föller, S. M. Huber, and F. Lang, “Azathioprine favourably influences the course of malaria,” Malaria Journal, vol. 8, no. 1, article 102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Geiger, M. Föller, K. R. Herrlinger, and F. Lang, “Azathioprine-induced suicidal erythrocyte death,” Inflammatory Bowel Diseases, vol. 14, no. 8, pp. 1027–1032, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Ghashghaeinia, J. C. Cluitmans, M. Toulany et al., “Age sensitivity of NFκB abundance and programmed cell death in erythrocytes induced by NFκB inhibitors,” Cellular Physiology and Biochemistry, vol. 32, no. 4, pp. 801–813, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Ghashghaeinia, M. Toulany, M. Saki et al., “The NFκB pathway inhibitors bay 11-7082 and parthenolide induce programmed cell death in anucleated erythrocytes,” Cellular Physiology and Biochemistry, vol. 27, no. 1, pp. 45–54, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Shumilina, V. Kiedaisch, A. Akkel et al., “Stimulation of suicidal erythrocyte death by lipoxygenase inhibitor Bay-Y5884,” Cellular Physiology and Biochemistry, vol. 18, no. 4-5, pp. 233–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. S. M. Qadri, Y. Kucherenko, and F. Lang, “Beauvericin induced erythrocyte cell membrane scrambling,” Toxicology, vol. 283, no. 1, pp. 24–31, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. E. Lang, K. Jilani, C. Zelenak et al., “Stimulation of suicidal erythrocyte death by benzethonium,” Cellular Physiology and Biochemistry, vol. 28, no. 2, pp. 347–354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Gao, P. M. Lau, and S. K. Kong, “Mitochondrial toxin betulinic acid induces in vitro eryptosis in human red blood cells through membrane permeabilization,” Archives of Toxicology, vol. 88, no. 3, pp. 755–768, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Braun, M. Föller, E. Gulbins, and F. Lang, “Eryptosis triggered by bismuth,” BioMetals, vol. 22, no. 3, pp. 453–460, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Sopjani, M. Föller, P. Dreischer, and F. Lang, “Stimulation of eryptosis by cadmium ions,” Cellular Physiology and Biochemistry, vol. 22, no. 1–4, pp. 245–252, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Lang, S. M. Qadri, K. Jilani et al., “Carbon monoxide-sensitive apoptotic death of erythrocytes,” Basic and Clinical Pharmacology and Toxicology, vol. 111, no. 5, pp. 348–355, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Jilani and F. Lang, “Carmustine-induced phosphatidylserine translocation in the erythrocyte membrane,” Toxins, vol. 5, no. 4, pp. 703–716, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Lupescu, R. Bissinger, K. Jilani, and F. Lang, “Triggering of suicidal erythrocyte death by celecoxib,” Toxins, vol. 5, no. 9, pp. 1543–1554, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. K. S. Lang, S. Myssina, V. Brand et al., “Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes,” Cell Death and Differentiation, vol. 11, no. 2, pp. 231–243, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Akel, T. Hermle, O. M. Niemoeller et al., “Stimulation of erythrocyte phosphatidylserine exposure by chlorpromazine,” European Journal of Pharmacology, vol. 532, no. 1-2, pp. 11–17, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Lupescu, K. Jilani, C. Zelenak, M. Zbidah, S. M. Qadri, and F. Lang, “Hexavalent chromium-induced erythrocyte membrane phospholipid asymmetry,” BioMetals, vol. 25, no. 2, pp. 309–318, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. O. M. Niemoeller, H. Mahmud, M. Föller, T. Wieder, and F. Lang, “Ciglitazone and 15d-PGJ2 induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 22, no. 1–4, pp. 237–244, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Mahmud, M. Föller, and F. Lang, “Suicidal erythrocyte death triggered by cisplatin,” Toxicology, vol. 249, no. 1, pp. 40–44, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. P. A. Lang, M. Schenck, J. P. Nicolay et al., “Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide,” Nature Medicine, vol. 13, no. 2, pp. 164–170, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. J. C. K. Lui, J. W. Y. Wong, Y. K. Suen, T. T. Kwok, K. P. Fung, and S. K. Kong, “Cordycepin induced eryptosis in mouse erythrocytes through a Ca2+-dependent pathway without caspase-3 activation,” Archives of Toxicology, vol. 81, no. 12, pp. 859–865, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. R. Bissinger, A. Lupescu, C. Zelenak, K. Jilani, and F. Lang, “Stimulation of eryptosis by cryptotanshinone,” Cellular Physiology and Biochemistry, vol. 34, no. 2, pp. 432–442, 2014. View at Publisher · View at Google Scholar
  84. P. J. Bentzen, E. Lang, and F. Lang, “Curcumin induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 19, no. 1–4, pp. 153–164, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. D. Bobbala, S. Koka, C. Lang, K. M. Boini, S. M. Huber, and F. Lang, “Effect of cyclosporine on parasitemia and survival of Plasmodium berghei infected mice,” Biochemical and Biophysical Research Communications, vol. 376, no. 3, pp. 494–498, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. O. M. Niemoeller, A. Akel, P. A. Lang et al., “Induction of eryptosis by cyclosporine,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 374, no. 1, pp. 41–49, 2006. View at Publisher · View at Google Scholar
  87. D. Mandal, A. Mazumder, P. Das, M. Kundu, and J. Basu, “Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes,” Journal of Biological Chemistry, vol. 280, no. 47, pp. 39460–39467, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Abed, K. A. Zoubi, M. Theurer, and F. Lang, “Effect of dermaseptin on erythrocytes,” Basic and Clinical Pharmacology and Toxicology, vol. 113, no. 5, pp. 347–352, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. S. M. Qadri, Y. Kucherenko, C. Zelenak, K. Jilani, E. Lang, and F. Lang, “Dicoumarol activates Ca2+-permeable cation channels triggering erythrocyte cell membrane scrambling,” Cellular Physiology and Biochemistry, vol. 28, no. 5, pp. 857–864, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Ghashghaeinia, D. Bobbala, T. Wieder et al., “Targeting glutathione by dimethylfumarate protects against experimental malaria by enhancing erythrocyte cell membrane scrambling,” The American Journal of Physiology—Cell Physiology, vol. 299, no. 4, pp. C791–C804, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. K. Jilani, S. M. Qadri, E. Lang et al., “Stimulation of erythrocyte phospholipid scrambling by enniatin A,” Molecular Nutrition and Food Research, vol. 55, supplement 2, pp. S294–S302, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. R. Bissinger, P. Modicano, L. Frauenfeld et al., “Estramustine-induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 32, no. 5, pp. 1426–1436, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. M. Gao, S. Y. Wong, P. M. Lau, and S. K. Kong, “Ferutinin induces in vitro eryptosis/erythroptosis in human erythrocytes through membrane permeabilization and calcium influx,” Chemical Research in Toxicology, vol. 26, no. 8, pp. 1218–1228, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. K. Jilani, S. Enkel, R. Bissinger, A. Almilaji, M. Abed, and F. Lang, “Fluoxetine induced suicidal erythrocyte death,” Toxins, vol. 5, no. 7, pp. 1230–1243, 2013. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Eberhard, K. Ferlinz, K. Alizzi et al., “FTY720-induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 26, no. 4-5, pp. 761–766, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Zbidah, A. Lupescu, K. Jilani, and F. Lang, “Stimulation of suicidal erythrocyte death by fumagillin,” Basic and Clinical Pharmacology and Toxicology, vol. 112, no. 5, pp. 346–351, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Lupescu, K. Jilani, C. Zelenak, M. Zbidah, N. Shaik, and F. Lang, “Induction of programmed erythrocyte death by gambogic acid,” Cellular Physiology and Biochemistry, vol. 30, no. 2, pp. 428–438, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. A. Lupescu, R. Bissinger, J. Warsi, K. Jilani, and F. Lang, “Stimulation of erythrocyte cell membrane scrambling by gedunin,” Cellular Physiology and Biochemistry, vol. 33, no. 6, pp. 1838–1848, 2014. View at Publisher · View at Google Scholar
  99. K. Jilani, S. M. Qadri, and F. Lang, “Geldanamycin-induced phosphatidylserine translocation in the erythrocyte membrane,” Cellular Physiology and Biochemistry, vol. 32, no. 6, pp. 1600–1609, 2013. View at Google Scholar · View at Scopus
  100. Y. V. Kucherenko, S. K. Bhavsar, V. I. Grischenko, U. R. Fischer, S. M. Huber, and F. Lang, “Increased cation conductance in human erythrocytes artificially aged by glycation,” Journal of Membrane Biology, vol. 235, no. 3, pp. 177–189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. D. J. Head, Z. E. Lee, J. Poole, and N. D. Avent, “Expression of phosphatidylserine (PS) on wild-type and Gerbich variant erythrocytes following glycophorin-C (GPC) ligation,” British Journal of Haematology, vol. 129, no. 1, pp. 130–137, 2005. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Sopjani, M. Föller, and F. Lang, “Gold stimulates Ca2+ entry into and subsequent suicidal death of erythrocytes,” Toxicology, vol. 244, no. 2-3, pp. 271–279, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. I. P. Lau, H. Chen, J. Wang et al., “In vitro effect of CTAB-and PEG-coated gold nanorods on the induction of eryptosis/erythroptosis in human erythrocytes,” Nanotoxicology, vol. 6, no. 8, pp. 847–856, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Zbidah, A. Lupescu, N. Shaik, and F. Lang, “Gossypol-induced suicidal erythrocyte death,” Toxicology, vol. 302, no. 2-3, pp. 101–105, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. E. Böttger, G. Multhoff, J. F. J. Kun, and M. Esen, “Plasmodium falciparum-infected erythrocytes induce granzyme B by NK cells through expression of host-Hsp70,” PLoS ONE, vol. 7, no. 3, Article ID e33774, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. S. Gatidis, M. Föller, and F. Lang, “Hemin-induced suicidal erythrocyte death,” Annals of Hematology, vol. 88, no. 8, pp. 721–726, 2009. View at Publisher · View at Google Scholar · View at Scopus
  107. R. Zhang, Y. Xiang, Q. Ran et al., “Involvement of calcium, reactive oxygen species, and ATP in hexavalent chromium-induced damage in red blood cells,” Cellular Physiology and Biochemistry, vol. 34, no. 5, pp. 1780–1791, 2014. View at Publisher · View at Google Scholar
  108. P. A. Lang, S. Kaiser, S. Myssina et al., “Effect of Vibrio parahaemolyticus haemolysin on human erythrocytes,” Cellular Microbiology, vol. 6, no. 4, pp. 391–400, 2004. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Zbidah, A. Lupescu, T. Herrmann et al., “Effect of honokiol on erythrocytes,” Toxicology in Vitro, vol. 27, no. 6, pp. 1737–1745, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. M. S. E. Ahmed, M. Abed, J. Voelkl, and F. Lang, “Triggering of suicidal erythrocyte death by uremic toxin indoxyl sulfate,” BMC Nephrology, vol. 14, article 244, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. C. Zelenak, M. Föller, A. Velic et al., “Proteome analysis of erythrocytes lacking AMP-activated protein kinase reveals a role of PAK2 kinase in eryptosis,” Journal of Proteome Research, vol. 10, no. 4, pp. 1690–1697, 2011. View at Publisher · View at Google Scholar · View at Scopus
  112. N. Shaik, E. Alhourani, A. Bosc et al., “Stimulation of suicidal erythrocyte death by ipratropium bromide,” Cellular Physiology and Biochemistry, vol. 30, no. 6, pp. 1517–1525, 2012. View at Publisher · View at Google Scholar · View at Scopus
  113. D. S. Kempe, P. A. Lang, K. Eisele et al., “Stimulation of erythrocyte phosphatidylserine exposure by lead ions,” The American Journal of Physiology—Cell Physiology, vol. 288, no. 2, pp. C396–C402, 2005. View at Publisher · View at Google Scholar · View at Scopus
  114. K. Wang, H. Mahmud, M. Föller et al., “Lipopeptides in the triggering of erythrocyte cell membrane scrambling,” Cellular Physiology and Biochemistry, vol. 22, no. 5-6, pp. 381–386, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. M. Föller, E. Shumilina, R. S. Lam et al., “Induction of suicidal erythrocyte death by listeriolysin from Listeria monocytogenes,” Cellular Physiology and Biochemistry, vol. 20, no. 6, pp. 1051–1060, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. J. P. Nicolay, S. Gatz, F. Lang, and U. E. Lang, “Lithium-induced suicidal erythrocyte death,” Journal of Psychopharmacology, vol. 24, no. 10, pp. 1533–1539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. K. Alzoubi, B. Alktifan, G. Oswald, M. Fezai, M. Abed, and F. Lang, “Breakdown of phosphatidylserine asymmetry following treatment of erythrocytes with lumefantrine,” Toxins, vol. 6, no. 2, pp. 650–664, 2014. View at Publisher · View at Google Scholar · View at Scopus
  118. K. Eisele, P. A. Lang, D. S. Kempe et al., “Stimulation of erythrocyte phosphatidylserine exposure by mercury ions,” Toxicology and Applied Pharmacology, vol. 210, no. 1-2, pp. 116–122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. H. Mahmud, M. Föller, and F. Lang, “Stimulation of erythrocyte cell membrane scrambling by methyldopa,” Kidney and Blood Pressure Research, vol. 31, no. 5, pp. 299–306, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. J. P. Nicolay, J. Schneider, O. M. Niemoeller et al., “Stimulation of suicidal erythrocyte death by methylglyoxal,” Cellular Physiology and Biochemistry, vol. 18, no. 4-5, pp. 223–232, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. C. Munoz, K. Alzoubi, J. Jacobi, M. Abed, and F. Lang, “Effect of miltefosine on erythrocytes,” Toxicology in Vitro, vol. 27, no. 6, pp. 1913–1919, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. J. Jacobi, E. Lang, R. Bissinger et al., “Stimulation of erythrocyte cell membrane scrambling by mitotane,” Cellular Physiology and Biochemistry, vol. 33, no. 5, pp. 1516–1526, 2014. View at Publisher · View at Google Scholar · View at Scopus
  123. M. Arnold, R. Bissinger, and F. Lang, “Mitoxantrone-induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 34, no. 5, pp. 1756–1767, 2014. View at Publisher · View at Google Scholar
  124. S. K. Bhavsar, M. Eberhard, D. Bobbala, and F. Lang, “Monensin induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 25, no. 6, pp. 745–752, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. M. Arnold, E. Lang, P. Modicano et al., “Effect of nitazoxanide on erythrocytes,” Basic and Clinical Pharmacology and Toxicology, vol. 114, no. 5, pp. 421–426, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. A. Lupescu, R. Bissinger, T. Herrmann, G. Oswald, K. Jilani, and F. Lang, “Induction of suicidal erythrocyte death by novobiocin,” Cellular Physiology and Biochemistry, vol. 33, no. 3, pp. 670–680, 2014. View at Publisher · View at Google Scholar · View at Scopus
  127. A. Malik, R. Bissinger, K. Jilani, and F. Lang, “Stimulation of erythrocyte cell membrane scrambling by nystatin,” Basic & Clinical Pharmacology & Toxicology, vol. 116, no. 1, pp. 47–52, 2015. View at Publisher · View at Google Scholar
  128. K. Jilani, A. Lupescu, M. Zbidah, M. Abed, N. Shaik, and F. Lang, “Enhanced apoptotic death of erythrocytes induced by the mycotoxin ochratoxin A,” Kidney and Blood Pressure Research, vol. 36, no. 1, pp. 107–118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  129. K. Jilani, S. M. Qadri, C. Zelenak, and F. Lang, “Stimulation of suicidal erythrocyte death by oridonin,” Archives of Biochemistry and Biophysics, vol. 511, no. 1-2, pp. 14–20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  130. L. Tesoriere, A. Attanzio, M. Allegra, A. Cilla, C. Gentile, and M. A. Livrea, “Oxysterol mixture in hypercholesterolemia-relevant proportion causes oxidative stress-dependent eryptosis,” Cellular Physiology and Biochemistry, vol. 34, no. 4, pp. 1075–1089, 2014. View at Publisher · View at Google Scholar
  131. S. Koka, D. Bobbala, C. Lang, K. M. Boini, S. M. Huber, and F. Lang, “Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice,” Cellular Physiology and Biochemistry, vol. 23, no. 1–3, pp. 191–198, 2009. View at Publisher · View at Google Scholar · View at Scopus
  132. P. A. Lang, J. Huober, C. Bachmann et al., “Stimulation of erythrocyte phosphatidylserine exposure by paclitaxel,” Cellular Physiology and Biochemistry, vol. 18, no. 1–3, pp. 151–154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  133. P. A. Lang, D. S. Kempe, V. Tanneur et al., “Stimulation of erythrocyte ceramide formation by platelet-activating factor,” Journal of Cell Science, vol. 118, no. 6, pp. 1233–1243, 2005. View at Publisher · View at Google Scholar · View at Scopus
  134. A. Lupescu, K. Jilani, M. Zbidah, and F. Lang, “Patulin-induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 32, no. 2, pp. 291–299, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. K. Alzoubi, S. Honisch, M. Abed, and F. Lang, “Triggering of suicidal erythrocyte death by penta-O-galloyl-beta-D-glucose,” Toxins, vol. 6, no. 1, pp. 54–65, 2014. View at Google Scholar · View at Scopus
  136. M. Abed, S. T. Towhid, T. Pakladok et al., “Effect of bacterial peptidoglycan on erythrocyte death and adhesion to endothelial cells,” International Journal of Medical Microbiology, vol. 303, no. 4, pp. 182–189, 2013. View at Publisher · View at Google Scholar · View at Scopus
  137. M. Föller, R. Biswas, H. Mahmud et al., “Effect of peptidoglycans on erythrocyte survival,” International Journal of Medical Microbiology, vol. 299, no. 1, pp. 75–85, 2009. View at Publisher · View at Google Scholar · View at Scopus
  138. R. Bissinger, S. Fischer, K. Jilani, and F. Lang, “Stimulation of erythrocyte death by phloretin,” Cellular Physiology and Biochemistry, vol. 34, no. 6, pp. 2256–2265, 2014. View at Publisher · View at Google Scholar
  139. J. Voelkl, K. Alzoubi, A.-K. Mamar, M. S. E. Ahmed, M. Abed, and F. Lang, “Stimulation of suicidal erythrocyte death by increased extracellular phosphate concentrations,” Kidney and Blood Pressure Research, vol. 38, no. 1, pp. 42–51, 2014. View at Publisher · View at Google Scholar · View at Scopus
  140. M. Eberhard, M. Föller, and F. Lang, “Effect of phytic acid on suicidal erythrocyte death,” Journal of Agricultural and Food Chemistry, vol. 58, no. 3, pp. 2028–2033, 2010. View at Publisher · View at Google Scholar · View at Scopus
  141. M. Gao, K. L. Cheung, I. P. Lau et al., “Polyphyllin D induces apoptosis in human erythrocytes through Ca2+ rise and membrane permeabilization,” Archives of Toxicology, vol. 86, no. 5, pp. 741–752, 2012. View at Publisher · View at Google Scholar · View at Scopus
  142. N. Shaik, A. Lupescu, and F. Lang, “Inhibition of suicidal erythrocyte death by probucol,” Journal of Cardiovascular Pharmacology, vol. 61, no. 2, pp. 120–126, 2013. View at Publisher · View at Google Scholar · View at Scopus
  143. C. Zelenak, M. Eberhard, K. Jilani, S. M. Qadri, B. MacEk, and F. Lang, “Protein kinase CK1α regulates erythrocyte survival,” Cellular Physiology and Biochemistry, vol. 29, no. 1-2, pp. 171–180, 2012. View at Publisher · View at Google Scholar · View at Scopus
  144. Y. Kucherenko, C. Zelenak, M. Eberhard, S. M. Qadri, and F. Lang, “Effect of casein kinase 1alpha activator pyrvinium pamoate on erythrocyte ion channels,” Cellular Physiology and Biochemistry, vol. 30, no. 2, pp. 407–417, 2012. View at Publisher · View at Google Scholar · View at Scopus
  145. M. Föller, M. Sopjani, H. P. Schlemmer, C. D. Claussen, and F. Lang, “Triggering of suicidal erythrocyte death by radiocontrast agents,” European Journal of Clinical Investigation, vol. 39, no. 7, pp. 576–583, 2009. View at Publisher · View at Google Scholar · View at Scopus
  146. O. M. Niemoeller, M. Föller, C. Lang, S. M. Huber, and F. Lang, “Retinoic acid induced suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 21, no. 1–3, pp. 193–202, 2008. View at Publisher · View at Google Scholar · View at Scopus
  147. G. Oswald, K. Alzoubi, M. Abed, and F. Lang, “Stimulation of suicidal erythrocyte death by ribavirin,” Basic & Clinical Pharmacology & Toxicology, vol. 114, no. 4, pp. 311–317, 2014. View at Publisher · View at Google Scholar
  148. M. Abed, S. T. Towhid, N. Shaik, and F. Lang, “Stimulation of suicidal death of erythrocytes by rifampicin,” Toxicology, vol. 302, no. 2-3, pp. 123–128, 2012. View at Publisher · View at Google Scholar · View at Scopus
  149. A. Lupescu, K. Jilani, M. Zbidah, and F. Lang, “Induction of apoptotic erythrocyte death by rotenone,” Toxicology, vol. 300, no. 3, pp. 132–137, 2012. View at Publisher · View at Google Scholar · View at Scopus
  150. R. Bissinger, A. Malik, K. Jilani, and F. Lang, “Triggering of erythrocyte cell membrane scrambling by salinomycin,” Basic & Clinical Pharmacology & Toxicology, vol. 115, no. 5, pp. 396–402, 2014. View at Publisher · View at Google Scholar
  151. M. Sopjani, M. Föller, E. Gulbins, and F. Lang, “Suicidal death of erythrocytes due to selenium-compounds,” Cellular Physiology and Biochemistry, vol. 22, no. 5-6, pp. 387–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  152. M. Sopjani, M. Föller, J. Haendeler, F. Götz, and F. Lang, “Silver ion-induced suicidal erythrocyte death,” Journal of Applied Toxicology, vol. 29, no. 6, pp. 531–536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  153. A. Lupescu, N. Shaik, K. Jilani et al., “Enhanced erythrocyte membrane exposure of phosphatidylserine following sorafenib treatment: an in vivo and in vitro study,” Cellular Physiology and Biochemistry, vol. 30, no. 4, pp. 876–888, 2012. View at Publisher · View at Google Scholar · View at Scopus
  154. M. Abed, S. T. Towhid, S. Mia et al., “Sphingomyelinase-induced adhesion of eryptotic erythrocytes to endothelial cells,” American Journal of Physiology—Cell Physiology, vol. 303, no. 9, pp. C991–C999, 2012. View at Publisher · View at Google Scholar · View at Scopus
  155. S. M. Qadri, J. Bauer, C. Zelenak et al., “Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 28, no. 2, pp. 339–346, 2011. View at Publisher · View at Google Scholar · View at Scopus
  156. M. Zbidah, A. Lupescu, W. Yang et al., “Sulindac sulfde—induced stimulation of eryptosis,” Cellular Physiology and Biochemistry, vol. 30, no. 4, pp. 1072–1082, 2012. View at Publisher · View at Google Scholar · View at Scopus
  157. N. Shaik, A. Lupescu, and F. Lang, “Sunitinib-sensitive suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 30, no. 3, pp. 512–522, 2012. View at Publisher · View at Google Scholar · View at Scopus
  158. C. Zelenak, V. Pasham, K. Jilani et al., “Tanshinone IIA stimulates erythrocyte phosphatidylserine exposure,” Cellular Physiology and Biochemistry, vol. 30, no. 1, pp. 282–294, 2012. View at Publisher · View at Google Scholar · View at Scopus
  159. E. Lang, P. Modicano, M. Arnold et al., “Effect of thioridazine on erythrocytes,” Toxins, vol. 5, no. 10, pp. 1918–1931, 2013. View at Publisher · View at Google Scholar · View at Scopus
  160. D. J. Head, Z. E. Lee, M. M. Swallah, and N. D. Avent, “Ligation of CD47 mediates phosphatidylserine expression on erythrocytes and a concomitant loss of viability in vitro,” British Journal of Haematology, vol. 130, no. 5, pp. 788–790, 2005. View at Publisher · View at Google Scholar · View at Scopus
  161. S. M. Qadri, H. Mahmud, M. Föller, and F. Lang, “Thymoquinone-induced suicidal erythrocyte death,” Food and Chemical Toxicology, vol. 47, no. 7, pp. 1545–1549, 2009. View at Publisher · View at Google Scholar · View at Scopus
  162. T. T. Nguyen, M. Föller, and F. Lang, “Tin triggers suicidal death of erythrocytes,” Journal of Applied Toxicology, vol. 29, no. 1, pp. 79–83, 2009. View at Publisher · View at Google Scholar · View at Scopus
  163. M. Theurer, N. Shaik, and F. Lang, “Stimulation of suicidal erythrocyte death by trans-cinnamaldehyde,” Phytomedicine, vol. 20, no. 12, pp. 1119–1123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  164. L. Frauenfeld, K. Alzoubi, M. Abed, and F. Lang, “Stimulation of erythrocyte cell membrane scrambling by mushroom tyrosinase,” Toxins, vol. 6, no. 3, pp. 1096–1108, 2014. View at Publisher · View at Google Scholar · View at Scopus
  165. K. Jilani, M. Abed, C. Zelenak, E. Lang, S. M. Qadri, and F. Lang, “Triggering of erythrocyte cell membrane scrambling by ursolic acid,” Journal of Natural Products, vol. 74, no. 10, pp. 2181–2186, 2011. View at Publisher · View at Google Scholar · View at Scopus
  166. J. Schneider, J. P. Nicolay, M. Föller, T. Wieder, and F. Lang, “Suicidal erythrocyte death following cellular K+ loss,” Cellular Physiology and Biochemistry, vol. 20, no. 1–4, pp. 35–44, 2007. View at Publisher · View at Google Scholar · View at Scopus
  167. M. Föller, M. Sopjani, H. Mahmud, and F. Lang, “Vanadate-induced suicidal erythrocyte death,” Kidney and Blood Pressure Research, vol. 31, no. 2, pp. 87–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  168. S. M. Qadri, M. Eberhard, H. Mahmud, M. Föller, and F. Lang, “Stimulation of ceramide formation and suicidal erythrocyte death by vitamin K3 (menadione),” European Journal of Pharmacology, vol. 623, no. 1–3, pp. 10–13, 2009. View at Publisher · View at Google Scholar · View at Scopus
  169. K. Jilani, A. Lupescu, M. Zbidah, N. Shaik, and F. Lang, “Withaferin A-stimulated Ca2+ entry, ceramide formation and suicidal death of erythrocytes,” Toxicology in Vitro, vol. 27, no. 1, pp. 52–58, 2013. View at Publisher · View at Google Scholar · View at Scopus
  170. K. Jilani and F. Lang, “Ca2+-dependent suicidal erythrocyte death following zearalenone exposure,” Archives of Toxicology, vol. 87, no. 10, pp. 1821–1828, 2013. View at Publisher · View at Google Scholar · View at Scopus
  171. V. Kiedaisch, A. Akel, O. M. Niemoeller, T. Wieder, and F. Lang, “Zinc-induced suicidal erythrocyte death,” American Journal of Clinical Nutrition, vol. 87, no. 5, pp. 1530–1534, 2008. View at Google Scholar · View at Scopus
  172. O. M. Niemoeller, P. J. Bentzen, E. Lang, and F. Lang, “Adenosine protects against suicidal erythrocyte death,” Pflügers Archiv, vol. 454, no. 3, pp. 427–439, 2007. View at Publisher · View at Google Scholar · View at Scopus
  173. V. Brand, S. Koka, C. Lang et al., “Influence of amitriptyline on eryptosis, parasitemia and survival of Plasmodium berghei-infected mice,” Cellular Physiology and Biochemistry, vol. 22, no. 5-6, pp. 405–412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  174. E. Floride, M. Föller, M. Ritter, and F. Lang, “Caffeine inhibits suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 22, no. 1–4, pp. 253–260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  175. P. A. Lang, D. S. Kempe, A. Akel et al., “Inhibition of erythrocyte 'apoptosis' by catecholamines,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 372, no. 3, pp. 228–235, 2005. View at Publisher · View at Google Scholar · View at Scopus
  176. S. M. Huber, N. Gamper, and F. Lang, “Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts,” Pflugers Archiv, vol. 441, no. 4, pp. 551–558, 2001. View at Publisher · View at Google Scholar · View at Scopus
  177. K. S. Lang, S. Myssina, V. Tanneur et al., “Inhibition of erythrocyte cation channels and apoptosis by ethylisopropylamiloride,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 367, no. 4, pp. 391–396, 2003. View at Publisher · View at Google Scholar · View at Scopus
  178. D. M. Vota, R. E. Maltaneri, S. D. Wenker, A. B. Nesse, and D. C. Vittori, “Differential erythropoietin action upon cells induced to eryptosis by different agents,” Cell Biochemistry and Biophysics, vol. 65, no. 2, pp. 145–157, 2013. View at Publisher · View at Google Scholar · View at Scopus
  179. R. S. Kasinathan, M. Föller, S. Koka, S. M. Huber, and F. Lang, “Inhibition of eryptosis and intraerythrocytic growth of Plasmodium falciparum by flufenamic acid,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 374, no. 4, pp. 255–264, 2007. View at Publisher · View at Google Scholar · View at Scopus
  180. Y. V. Kucherenko and F. Lang, “Inhibitory effect of furosemide on non-selective voltage-independent cation channels in human erythrocytes,” Cellular Physiology and Biochemistry, vol. 30, no. 4, pp. 863–875, 2012. View at Publisher · View at Google Scholar · View at Scopus
  181. N. Shaik, M. Zbidah, and F. Lang, “Inhibition of Ca2+ entry and suicidal erythrocyte death by naringin,” Cellular Physiology and Biochemistry, vol. 30, no. 3, pp. 678–686, 2012. View at Publisher · View at Google Scholar · View at Scopus
  182. M. Föller, H. Mahmud, S. Gu et al., “Modulation of suicidal erythrocyte cation channels by an AMPA antagonist,” Journal of Cellular and Molecular Medicine, vol. 13, no. 9, pp. 3680–3686, 2009. View at Publisher · View at Google Scholar · View at Scopus
  183. S. Gatidis, C. Zelenak, A. Fajol et al., “P38 MAPK activation and function following osmotic shock of erythrocytes,” Cellular Physiology and Biochemistry, vol. 28, no. 6, pp. 1279–1286, 2011. View at Publisher · View at Google Scholar · View at Scopus
  184. S. M. Qadri, M. Föller, and F. Lang, “Inhibition of suicidal erythrocyte death by resveratrol,” Life Sciences, vol. 85, no. 1-2, pp. 33–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  185. K. S. Lang, S. Myssina, P. A. Lang et al., “Inhibition of erythrocyte phosphatidylserine exposure by urea and Cl,” American Journal of Physiology—Renal Physiology, vol. 286, no. 6, pp. F1046–F1053, 2004. View at Publisher · View at Google Scholar · View at Scopus
  186. S. M. Qadri, H. Mahmud, M. Föller, and F. Lang, “Inhibition of suicidal erythrocyte death by xanthohumol,” Journal of Agricultural and Food Chemistry, vol. 57, no. 16, pp. 7591–7595, 2009. View at Publisher · View at Google Scholar · View at Scopus
  187. Y. Kucherenko, C. Geiger, E. Shumilina, M. Föller, and F. Lang, “Inhibition of cation channels and suicidal death of human erythrocytes by zidovudine,” Toxicology, vol. 253, no. 1–3, pp. 62–69, 2008. View at Publisher · View at Google Scholar · View at Scopus
  188. M. Abed, M. Feger, K. Alzoubi et al., “Sensitization of erythrocytes to suicidal erythrocyte death following water deprivation,” Kidney and Blood Pressure Research, vol. 37, no. 6, pp. 567–578, 2013. View at Publisher · View at Google Scholar · View at Scopus
  189. E. Weiss, U. M. Cytlak, D. C. Rees, A. Osei, and J. S. Gibson, “Deoxygenation-induced and Ca2+ dependent phosphatidylserine externalisation in red blood cells from normal individuals and sickle cell patients,” Cell Calcium, vol. 51, no. 1, pp. 51–56, 2012. View at Publisher · View at Google Scholar · View at Scopus
  190. D. S. Kempe, P. A. Lang, C. Duranton et al., “Enhanced programmed cell death of iron-deficient erythrocytes,” The FASEB Journal, vol. 20, no. 2, pp. 368–370, 2006. View at Publisher · View at Google Scholar · View at Scopus
  191. D. Zappulla, “Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases?” Journal of the Cardiometabolic Syndrome, vol. 3, no. 1, pp. 30–34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  192. U. Fırat, S. Kaya, A. Çim et al., “Increased caspase-3 immunoreactivity of erythrocytes in STZ diabetic rats,” Experimental Diabetes Research, vol. 2012, Article ID 316384, 4 pages, 2012. View at Publisher · View at Google Scholar
  193. C. Birka, P. A. Lang, D. S. Kempe et al., “Enhanced susceptibility to erythrocyte ‘apoptosis’ following phosphate depletion,” Pflügers Archiv, vol. 448, no. 5, pp. 471–477, 2004. View at Google Scholar · View at Scopus
  194. D. Banerjee, S. Saha, S. Basu, and A. Chakrabarti, “Porous red cell ultrastructure and loss of membrane asymmetry in a novel case of hemolytic anemia,” European Journal of Haematology, vol. 81, no. 5, pp. 399–402, 2008. View at Publisher · View at Google Scholar · View at Scopus
  195. H. Mahmud, W. P. T. Ruifrok, B. D. Westenbrink et al., “Suicidal erythrocyte death, eryptosis, as a novel mechanism in heart failure-associated anaemia,” Cardiovascular Research, vol. 98, no. 1, pp. 37–46, 2013. View at Publisher · View at Google Scholar · View at Scopus
  196. D. Polak-Jonkisz and L. Purzyc, “Ca2+ influx versus efflux during eryptosis in uremic erythrocytes,” Blood Purification, vol. 34, no. 3-4, pp. 209–210, 2012. View at Publisher · View at Google Scholar
  197. M. Abed, F. Artunc, K. Alzoubi et al., “Suicidal erythrocyte death in end-stage renal disease,” Journal of Molecular Medicine, vol. 92, no. 8, pp. 871–879, 2014. View at Publisher · View at Google Scholar · View at Scopus
  198. P. A. Lang, O. Beringer, J. P. Nicolay et al., “Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome,” Journal of Molecular Medicine, vol. 84, no. 5, pp. 378–388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  199. D. S. Kempe, A. Akel, P. A. Lang et al., “Suicidal erythrocyte death in sepsis,” Journal of Molecular Medicine, vol. 85, no. 3, pp. 269–277, 2007. View at Publisher · View at Google Scholar · View at Scopus
  200. K. M. Felder, K. Hoelzle, M. Ritzmann et al., “Hemotrophic mycoplasmas induce programmed cell death in red blood cells,” Cellular Physiology and Biochemistry, vol. 27, no. 5, pp. 557–564, 2011. View at Publisher · View at Google Scholar · View at Scopus
  201. S. Koka, C. Lang, O. M. Niemoeller et al., “Influence of NO synthase inhibitor L-NAME on parasitemia and survival of Plasmodium berghei infected mice,” Cellular Physiology and Biochemistry, vol. 21, no. 5-6, pp. 481–488, 2008. View at Publisher · View at Google Scholar · View at Scopus
  202. P. R. R. Totino, C. T. Daniel-Ribeiro, and M. D. F. Ferreira-da-Cru, “Refractoriness of eryptotic red blood cells to plasmodium falciparum infection: a putative host defense mechanism limiting parasitaemia,” PLoS ONE, vol. 6, no. 10, Article ID e26575, 2011. View at Publisher · View at Google Scholar · View at Scopus
  203. K. S. Lang, B. Roll, S. Myssina et al., “Enhanced erythrocyte apoptosis in sickle cell anemia, thalassemia and glucose-6-phosphate dehydrogenase deficiency,” Cellular Physiology and Biochemistry, vol. 12, no. 5-6, pp. 365–372, 2002. View at Publisher · View at Google Scholar · View at Scopus
  204. K. Ayi, F. Turrini, A. Piga, and P. Arese, “Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait,” Blood, vol. 104, no. 10, pp. 3364–3371, 2004. View at Publisher · View at Google Scholar · View at Scopus
  205. K. de Jong, R. K. Emerson, J. Butler, J. Bastacky, N. Mohandas, and F. A. Kuypers, “Short survival of phosphatidylserine-exposing red blood cells in murine sickle cell anemia,” Blood, vol. 98, no. 5, pp. 1577–1584, 2001. View at Publisher · View at Google Scholar · View at Scopus
  206. L. S. Kean, L. E. Brown, J. W. Nichols, N. Mohandas, D. R. Archer, and L. L. Hsu, “Comparison of mechanisms of anemia in mice with sickle cell disease and beta-thalassemia: peripheral destruction, ineffective erythropoiesis, and phospholipid scramblase-mediated phosphatidylserine exposure,” Experimental Hematology, vol. 30, no. 5, pp. 394–402, 2002. View at Publisher · View at Google Scholar · View at Scopus
  207. J. A. Browning, H. C. Robinson, J. C. Ellory, and J. S. Gibson, “Deoxygenation-induced non-electrolyte pathway in red cells from sickle cell patients,” Cellular Physiology and Biochemistry, vol. 19, no. 1–4, pp. 165–174, 2007. View at Publisher · View at Google Scholar · View at Scopus
  208. B. L. Wood, D. F. Gibson, and J. F. Tait, “Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations,” Blood, vol. 88, no. 5, pp. 1873–1880, 1996. View at Google Scholar · View at Scopus
  209. P. Chadebech, A. Habibi, R. Nzouakou et al., “Delayed hemolytic transfusion reaction in sickle cell disease patients: evidence of an emerging syndrome with suicidal red blood cell death,” Transfusion, vol. 49, no. 9, pp. 1785–1792, 2009. View at Publisher · View at Google Scholar · View at Scopus
  210. F. A. Kuypers, J. Yuan, R. A. Lewis et al., “Membrane phospholipid asymmetry in human thalassemia,” Blood, vol. 91, no. 8, pp. 3044–3051, 1998. View at Google Scholar · View at Scopus
  211. S. Basu, D. Banerjee, S. Chandra, and A. Chakrabarti, “Eryptosis in hereditary spherocytosis and thalassemia: role of glycoconjugates,” Glycoconjugate Journal, vol. 27, no. 7–9, pp. 717–722, 2010. View at Publisher · View at Google Scholar · View at Scopus
  212. M. Cappadoro, G. Giribaldi, E. O'Brien et al., “Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency,” Blood, vol. 92, no. 7, pp. 2527–2534, 1998. View at Google Scholar · View at Scopus
  213. S. Ganesan, N. D. Chaurasiya, R. Sahu, L. A. Walker, and B. L. Tekwani, “Understanding the mechanisms for metabolism-linked hemolytic toxicity of primaquine against glucose 6-phosphate dehydrogenase deficient human erythrocytes: evaluation of eryptotic pathway,” Toxicology, vol. 294, no. 1, pp. 54–60, 2012. View at Publisher · View at Google Scholar · View at Scopus
  214. L. J. Bruce, H. C. Robinson, H. Guizouarn et al., “Monovalent cation leaks in human red cells caused by single amino-acid substitutions in the transport domain of the band 3 chloride-bicarbonate exchanger, AE1,” Nature Genetics, vol. 37, no. 11, pp. 1258–1263, 2005. View at Publisher · View at Google Scholar · View at Scopus
  215. Y. G. Weber, A. Storch, T. V. Wuttke et al., “GLUT1 mutations are a cause of paroxysmal exertion-induced dyskinesias and induce hemolytic anemia by a cation leak,” The Journal of Clinical Investigation, vol. 118, no. 6, pp. 2157–2168, 2008. View at Google Scholar · View at Scopus
  216. M. Abed, S. Balasaheb, S. T. Towhid, C. Daniel, K. Amann, and F. Lang, “Adhesion of annexin 7 deficient erythrocytes to endothelial cells,” PLoS ONE, vol. 8, no. 2, Article ID e56650, 2013. View at Publisher · View at Google Scholar · View at Scopus
  217. M. Föller, S. Feil, K. Ghoreschi et al., “Anemia and splenomegaly in cGKI-deficient mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 18, pp. 6771–6776, 2008. View at Publisher · View at Google Scholar · View at Scopus
  218. M. Abed, S. T. Towhid, M. Feger et al., “Adhesion of klotho-deficient eryptotic erythrocytes to endothelial cells,” Acta Physiologica, vol. 207, no. 3, pp. 485–493, 2013. View at Publisher · View at Google Scholar · View at Scopus
  219. D. S. Kempe, T. F. Ackermann, S. S. Fischer et al., “Accelerated suicidal erythrocyte death in Klotho-deficient mice,” Pflugers Archiv European Journal of Physiology, vol. 458, no. 3, pp. 503–512, 2009. View at Publisher · View at Google Scholar · View at Scopus
  220. M. Föller, R. S. Kasinathan, S. Koka et al., “Enhanced susceptibility to suicidal death of erythrocytes from transgenic mice overexpressing erythropoietin,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 293, no. 3, pp. R1127–R1134, 2007. View at Publisher · View at Google Scholar · View at Scopus
  221. A. Akel, C. A. Wagner, J. Kovacikova et al., “Enhanced suicidal death of erythrocytes from gene-targeted mice lacking the Cl/HCO3 exchanger AE1,” The American Journal of Physiology—Cell Physiology, vol. 292, no. 5, pp. C1759–C1767, 2007. View at Publisher · View at Google Scholar
  222. S. K. Bhavsar, S. Gu, D. Bobbala, and F. Lang, “Janus kinase 3 is expressed in erythrocytes, phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 27, no. 5, pp. 547–556, 2011. View at Publisher · View at Google Scholar · View at Scopus
  223. M. Föller, H. Mahmud, S. Koka, and F. Lang, “Reduced Ca2+ entry and suicidal death of erythrocytes in PDK1 hypomorphic mice,” Pflugers Archiv European Journal of Physiology, vol. 455, no. 5, pp. 939–949, 2008. View at Publisher · View at Google Scholar · View at Scopus
  224. E. Maellaro, S. Leoncini, D. Moretti et al., “Erythrocyte caspase-3 activation and oxidative imbalance in erythrocytes and in plasma of type 2 diabetic patients,” Acta Diabetologica, vol. 50, no. 4, pp. 489–495, 2013. View at Publisher · View at Google Scholar · View at Scopus
  225. D. Mandal, V. Baudin-Creuza, A. Bhattacharyya et al., “Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3),” Journal of Biological Chemistry, vol. 278, no. 52, pp. 52551–52558, 2003. View at Publisher · View at Google Scholar · View at Scopus
  226. D. Bratosin, J. Estaquier, F. Petit et al., “Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria,” Cell Death and Differentiation, vol. 8, no. 12, pp. 1143–1156, 2001. View at Publisher · View at Google Scholar · View at Scopus
  227. D. Mandal, P. K. Moitra, S. Saha, and J. Basu, “Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes,” FEBS Letters, vol. 513, no. 2-3, pp. 184–188, 2002. View at Publisher · View at Google Scholar · View at Scopus
  228. P. Matarrese, E. Straface, D. Pietraforte et al., “Peroxynitrite induces senescence and apoptosis of red blood cells through the activation of aspartyl and cysteinyl proteases,” The FASEB Journal, vol. 19, no. 3, pp. 416–418, 2005. View at Publisher · View at Google Scholar · View at Scopus
  229. M. Weil, M. D. Jacobson, and M. C. Raff, “Are caspases involved in the death of cells with a transcriptionally inactive nucleus? Sperm and chicken erythrocytes,” Journal of Cell Science, vol. 111, no. 18, pp. 2707–2715, 1998. View at Google Scholar · View at Scopus
  230. A. Das, A. Smolenski, S. M. Lohmann, and R. C. Kukreja, “Cyclic GMP-dependent protein kinase Iα attenuates necrosis and apoptosis following ischemia/reoxygenation in adult cardiomyocyte,” Journal of Biological Chemistry, vol. 281, no. 50, pp. 38644–38652, 2006. View at Publisher · View at Google Scholar · View at Scopus
  231. J. R. Li and T. R. Billiar, “The anti-apoptotic actions of nitric oxide in hepatocytes,” Cell Death and Differentiation, vol. 6, no. 10, pp. 952–955, 1999. View at Publisher · View at Google Scholar · View at Scopus
  232. A. Nagai-Kusuhara, M. Nakamura, H. Mukuno, A. Kanamori, A. Negi, and G. M. Seigel, “cAMP-responsive element binding protein mediates a cGMP/protein kinase G-deendent anti-apoptotic signal induced by nitric oxide in retinal neuro-glial progenitor cells,” Experimental Eye Research, vol. 84, pp. 152–162, 2007. View at Google Scholar
  233. J. Schlossmann, R. Feil, and F. Hofmann, “Insights into cGMP signalling derived from cGMP kinase knockout mice,” Frontiers in Bioscience, vol. 10, pp. 1279–1289, 2005. View at Publisher · View at Google Scholar · View at Scopus
  234. B. Y. Owusu, R. Stapley, and R. P. Patel, “Nitric oxide formation versus scavenging: the red blood cell balancing act,” Journal of Physiology (London), vol. 590, no. 20, pp. 4993–5000, 2012. View at Publisher · View at Google Scholar · View at Scopus
  235. M. J. Kahn, J. H. Maley, G. F. Lasker, and P. J. Kadowitz, “Updated role of nitric oxide in disorders of erythrocyte function,” Cardiovascular and Hematological Disorders—Drug Targets, vol. 13, no. 1, pp. 83–87, 2013. View at Publisher · View at Google Scholar · View at Scopus
  236. A. J. Gow, B. P. Luchsinger, J. R. Pawloski, D. J. Singel, and J. S. Stamler, “The oxyhemoglobin reaction of nitric oxide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 16, pp. 9027–9032, 1999. View at Publisher · View at Google Scholar · View at Scopus
  237. D. Malan, R. C. Levi, G. Alloatti, A. Marcantoni, I. Bedendi, and M. P. Gallo, “Cyclic AMP and cyclic GMP independent stimulation of ventricular calcium current by peroxynitrite donors in guinea pig myocytes,” Journal of Cellular Physiology, vol. 197, no. 2, pp. 284–296, 2003. View at Publisher · View at Google Scholar · View at Scopus
  238. M. William, J. Vien, E. Hamilton et al., “The nitric oxide donor sodium nitroprusside stimulates the Na+-K+ pump in isolated rabbit cardiac myocytes,” Journal of Physiology, vol. 565, no. 3, pp. 815–825, 2005. View at Publisher · View at Google Scholar · View at Scopus
  239. S. Dimmeler, J. Haendeler, M. Nehls, and A. M. Zeiher, “Suppression of apoptosis by nitric oxide via inhibition of interleukin- 1β-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases,” The Journal of Experimental Medicine, vol. 185, no. 4, pp. 601–607, 1997. View at Publisher · View at Google Scholar · View at Scopus
  240. L. Rössig, B. Fichtlscherer, K. Breitschopf et al., “Nitric oxide inhibits caspase-3 by S-nitrosation in vivo,” Journal of Biological Chemistry, vol. 274, no. 11, pp. 6823–6826, 1999. View at Publisher · View at Google Scholar · View at Scopus
  241. M. Benhar and J. S. Stamler, “A central role for S-nitrosylation in apoptosis,” Nature Cell Biology, vol. 7, no. 7, pp. 645–646, 2005. View at Publisher · View at Google Scholar · View at Scopus
  242. J. Haendeler, J. Hoffmann, V. Tischler, B. C. Berk, A. M. Zeiher, and S. Dimmeler, “Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69,” Nature Cell Biology, vol. 4, no. 10, pp. 743–749, 2002. View at Publisher · View at Google Scholar · View at Scopus
  243. J. Haendeler, J. Hoffmann, A. M. Zeiher, and S. Dimmeler, “Antioxidant effects of statins via S-nitrosylation and activation of thioredoxin in endothelial cells: a novel vasculoprotective function of statins,” Circulation, vol. 110, no. 7, pp. 856–861, 2004. View at Publisher · View at Google Scholar · View at Scopus
  244. J. Hoffmann, J. Haendeler, A. M. Zeiher, and S. Dimmeler, “TNF alpha and oxLDL reduce protein S-nitrosylation in endothelial cells,” Journal of Biological Chemistry, vol. 276, no. 44, pp. 41383–41387, 2001. View at Publisher · View at Google Scholar · View at Scopus
  245. G. Melino, F. Bernassola, R. A. Knight, M. T. Corasaniti, G. Nisticò, and A. Finazzi-Agrò, “S-nitrosylation regulates apoptosis,” Nature, vol. 388, no. 6641, pp. 432–433, 1997. View at Publisher · View at Google Scholar · View at Scopus
  246. S. S. Castillo, M. Levy, C. Wang, J. V. Thaikoottathil, E. Khan, and T. Goldkorn, “Nitric oxide-enhanced caspase-3 and acidic sphingomyelinase interaction: a novel mechanism by which airway epithelial cells escape ceramide-induced apoptosis,” Experimental Cell Research, vol. 313, no. 4, pp. 816–823, 2007. View at Publisher · View at Google Scholar · View at Scopus
  247. S. M. Davidson and M. R. Duchen, “Endothelial mitochondria: contributing to vascular function and disease,” Circulation Research, vol. 100, no. 8, pp. 1128–1141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  248. P. Pacher, J. S. Beckman, and L. Liaudet, “Nitric oxide and peroxynitrite in health and disease,” Physiological Reviews, vol. 87, no. 1, pp. 315–424, 2007. View at Publisher · View at Google Scholar · View at Scopus
  249. T. Dasgupta, M. E. Fabry, and D. K. Kaul, “Antisickling property of fetal hemoglobin enhances nitric oxide bioavailability and ameliorates organ oxidative stress in transgenic-knockout sickle mice,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 298, no. 2, pp. R394–R402, 2010. View at Publisher · View at Google Scholar · View at Scopus
  250. J. M. Salhany, “The oxidative denitrosylation mechanism and nitric oxide release from human fetal and adult hemoglobin, an experimentally based model simulation study,” Blood Cells, Molecules, and Diseases, vol. 50, no. 1, pp. 8–19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  251. D. K. Kaul, X.-D. Liu, H.-Y. Chang, R. L. Nagel, and M. E. Fabry, “Effect of fetal hemoglobin on microvascular regulation in sickle transgenic-knockout mice,” Journal of Clinical Investigation, vol. 114, no. 8, pp. 1136–1145, 2004. View at Publisher · View at Google Scholar · View at Scopus
  252. O. Borst, M. Abed, I. Alesutan et al., “Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX,” The American Journal of Physiology—Cell Physiology, vol. 302, no. 4, pp. C644–C651, 2012. View at Publisher · View at Google Scholar · View at Scopus
  253. S. G. Betal and B. N. Y. Setty, “Phosphatidylserine-positive erythrocytes bind to immobilized and soluble thrombospondin-1 via its heparin-binding domain,” Translational Research, vol. 152, no. 4, pp. 165–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  254. A. B. Manodori, G. A. Barabino, B. H. Lubin, and F. A. Kuypers, “Adherence of phosphatidylserine-exposing erythrocytes to endothelial matrix thrombospondin,” Blood, vol. 95, no. 4, pp. 1293–1300, 2000. View at Google Scholar · View at Scopus
  255. V. A. Fadok, D. L. Bratton, D. M. Rose, A. Pearson, R. A. B. Ezekewitz, and P. M. Henson, “A receptor for phosphatidylserine-specific clearance of apoptotic cells,” Nature, vol. 405, no. 6782, pp. 85–90, 2000. View at Publisher · View at Google Scholar · View at Scopus
  256. B. Walker, S. T. Towhid, E. Schmid et al., “Dynamic adhesion of eryptotic erythrocytes to immobilized platelets via platelet phosphatidylserine receptors,” The American Journal of Physiology—Cell Physiology, vol. 306, no. 3, pp. C291–C297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  257. D. A. Andrews and P. S. Low, “Role of red blood cells in thrombosis,” Current Opinion in Hematology, vol. 6, no. 2, pp. 76–82, 1999. View at Publisher · View at Google Scholar · View at Scopus
  258. E. Nagababu, S. Gulyani, C. J. Earley, R. Cutler, M. Mattson, and J. Rifkind, “Iron-deficiency anaemia enhances red blood cell oxidative stress,” Free Radical Research, vol. 42, no. 9, pp. 824–829, 2008. View at Publisher · View at Google Scholar · View at Scopus
  259. S. M. Qadri, H. Mahmud, E. Lang et al., “Enhanced suicidal erythrocyte death in mice carrying a loss-of-function mutation of the adenomatous polyposis coli gene,” Journal of Cellular and Molecular Medicine, vol. 16, no. 5, pp. 1085–1093, 2012. View at Publisher · View at Google Scholar · View at Scopus
  260. J. V. Calderón-Salinas, E. G. Muñoz-Reyes, J. F. Guerrero-Romero et al., “Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease,” Molecular and Cellular Biochemistry, vol. 357, no. 1-2, pp. 171–179, 2011. View at Publisher · View at Google Scholar · View at Scopus
  261. P. J. Thornalley, “Modification of the glyoxalase system in human red blood cells by glucose in vitro,” Biochemical Journal, vol. 254, no. 3, pp. 751–755, 1988. View at Google Scholar · View at Scopus
  262. E. U. Nwose, H. F. Jelinek, R. S. Richards, and R. G. Kerr, “Erythrocyte oxidative stress in clinical management of diabetes and its cardiovascular complications,” British Journal of Biomedical Science, vol. 64, no. 1, pp. 35–43, 2007. View at Google Scholar · View at Scopus
  263. S. D. M. Bandeira, G. D. S. Guedes, L. J. S. de Fonseca et al., “Characterization of blood oxidative stress in type 2 diabetes mellitus patients: increase in lipid peroxidation and SOD activity,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 819310, 13 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  264. O. Dmitrieva, S. de Lusignan, I. C. Macdougall et al., “Association of anaemia in primary care patients with chronic kidney disease: cross sectional study of quality improvement in chronic kidney disease (QICKD) trial data,” BMC Nephrology, vol. 14, article 24, 2013. View at Publisher · View at Google Scholar · View at Scopus
  265. M. Yang, C. H. Fox, J. Vassalotti, and M. Choi, “Complications of progression of CKD,” Advances in Chronic Kidney Disease, vol. 18, no. 6, pp. 400–405, 2011. View at Publisher · View at Google Scholar · View at Scopus
  266. J. W. Adamson, “Hyporesponsiveness to erythropoiesis stimulating agents in chronic kidney disease: the many faces of inflammation,” Advances in Chronic Kidney Disease, vol. 16, no. 2, pp. 76–82, 2009. View at Publisher · View at Google Scholar · View at Scopus
  267. M. A. Atkinson and S. L. Furth, “Anemia in children with chronic kidney disease,” Nature Reviews Nephrology, vol. 7, no. 11, pp. 635–641, 2011. View at Publisher · View at Google Scholar · View at Scopus
  268. P. Attanasio, C. Ronco, S. D. Anker, M. Cicoira, and S. von Haehling, “Role of iron deficiency and anemia in cardio-renal syndromes,” Seminars in Nephrology, vol. 32, no. 1, pp. 57–62, 2012. View at Publisher · View at Google Scholar · View at Scopus
  269. A. Besarab and D. W. Coyne, “Iron supplementation to treat anemia in patients with chronic kidney disease,” Nature Reviews Nephrology, vol. 6, no. 12, pp. 699–710, 2010. View at Publisher · View at Google Scholar · View at Scopus
  270. C. P. Kovesdy, “Iron and clinical outcomes in dialysis and non-dialysis-dependent chronic kidney disease patients,” Advances in Chronic Kidney Disease, vol. 16, no. 2, pp. 109–116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  271. C. Kwack and V. S. Balakrishnan, “Managing erythropoietin hyporesponsiveness,” Seminars in Dialysis, vol. 19, no. 2, pp. 146–151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  272. F. E. Vos, J. B. Schollum, C. V. Coulter, T. C. A. Doyle, S. B. Duffull, and R. J. Walker, “Red blood cell survival in long-term dialysis patients,” American Journal of Kidney Diseases, vol. 58, no. 4, pp. 591–598, 2011. View at Publisher · View at Google Scholar · View at Scopus
  273. M. H. Antonelou, A. G. Kriebardis, A. D. Velentzas, A. C. Kokkalis, S.-C. Georgakopoulou, and I. S. Papassideri, “Oxidative stress-associated shape transformation and membrane proteome remodeling in erythrocytes of end stage renal disease patients on hemodialysis,” Journal of Proteomics, vol. 74, no. 11, pp. 2441–2452, 2011. View at Publisher · View at Google Scholar · View at Scopus
  274. Q. Zhu, Z. Sun, Y. Jiang, F. Chen, and M. Wang, “Acrolein scavengers: reactivity, mechanism and impact on health,” Molecular Nutrition and Food Research, vol. 55, no. 9, pp. 1375–1390, 2011. View at Publisher · View at Google Scholar · View at Scopus
  275. G. Facorro, F. Aguirre, L. Florentin et al., “Oxidative stress and membrane fluidity in erythrocytes from patients with hemolytic uremic syndrome,” Acta Physiologica, Pharmacologica et Therapeutica Latinoamericana, vol. 47, no. 3, pp. 137–146, 1997. View at Google Scholar · View at Scopus
  276. S. A. Gomez, M. J. Abrey-Recalde, C. A. Panek et al., “The oxidative stress induced in vivo by Shiga toxin-2 contributes to the pathogenicity of haemolytic uraemic syndrome,” Clinical & Experimental Immunology, vol. 173, no. 3, pp. 463–472, 2013. View at Publisher · View at Google Scholar · View at Scopus
  277. H. F. Galley, “Oxidative stress and mitochondrial dysfunction in sepsis,” British Journal of Anaesthesia, vol. 107, no. 1, pp. 57–64, 2011. View at Publisher · View at Google Scholar · View at Scopus
  278. J. D. Gitlin, “Wilson Disease,” Gastroenterology, vol. 125, no. 6, pp. 1868–1877, 2003. View at Publisher · View at Google Scholar · View at Scopus
  279. S. Attri, N. Sharma, S. Jahagirdar, B. R. Thapa, and R. Prasad, “Erythrocyte metabolism and antioxidant status of patients with wilson disease with hemolytic anemia,” Pediatric Research, vol. 59, no. 4, pp. 593–597, 2006. View at Publisher · View at Google Scholar · View at Scopus
  280. H. Nagasaka, I. Inoue, A. Inui et al., “Relationship between oxidative stress and antioxidant systems in the liver of patients with Wilson disease: hepatic manifestation in wilson disease as a consequence of augmented oxidative stress,” Pediatric Research, vol. 60, no. 4, pp. 472–477, 2006. View at Publisher · View at Google Scholar · View at Scopus
  281. P. A. Lang, R. S. Kasinathan, V. B. Brand et al., “Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency,” Cellular Physiology and Biochemistry, vol. 24, no. 5-6, pp. 415–428, 2009. View at Publisher · View at Google Scholar · View at Scopus
  282. S. Basu, D. Banerjee, S. Chandra, and A. Chakrabarti, “Loss of phospholipid membrane asymmetry and sialylated glycoconjugates from erythrocyte surface in haemoglobin E β-thalassaemia,” British Journal of Haematology, vol. 141, no. 1, pp. 92–99, 2008. View at Publisher · View at Google Scholar · View at Scopus
  283. J. Haynes Jr., B. Obiako, J. A. King, R. B. Hester, and S. Ofori-Acquah, “Activated neutrophil-mediated sickle red blood cell adhesion to lung vascular endothelium: role of phosphatidylserine-exposed sickle red blood cells,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 291, no. 4, pp. H1679–H1685, 2006. View at Publisher · View at Google Scholar · View at Scopus
  284. D. K. Kaul, H. M. Tsai, X. D. Liu, M. T. Nakada, R. L. Nagel, and B. S. Coller, “Monoclonal antibodies to alpha V beta 3 (7E3 and LM609) inhibit sickle red blood cell-endothelium interactions induced by platelet-activating factor,” Blood, vol. 95, no. 2, pp. 368–374, 2000. View at Google Scholar · View at Scopus
  285. A. Kumar, J. R. Eckman, and T. M. Wick, “Inhibition of plasma-mediated adherence of sickle erythrocytes to microvascular endothelium by conformationally constrained RGD-containing peptides,” American Journal of Hematology, vol. 53, no. 2, pp. 92–98, 1996. View at Publisher · View at Google Scholar
  286. B. N. Y. Setty, S. Kulkarni, and M. J. Stuart, “Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion,” Blood, vol. 99, no. 5, pp. 1564–1571, 2002. View at Publisher · View at Google Scholar · View at Scopus
  287. J. Haynes, B. Obiako, R. B. Hester, B. S. Baliga, and T. Stevens, “Hydroxyurea attenuates activated neutrophil-mediated sickle erythrocyte membrane phosphatidylserine exposure and adhesion to pulmonary vascular endothelium,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 294, no. 1, pp. H379–H385, 2008. View at Publisher · View at Google Scholar · View at Scopus
  288. C. A. Hillery, M. C. Du, W. C. Wang, and J. P. Scott, “Hydroxyurea therapy decreases the in vitro adhesion of sickle erythrocytes to thrombospondin and laminin,” British Journal of Haematology, vol. 109, no. 2, pp. 322–327, 2000. View at Publisher · View at Google Scholar · View at Scopus
  289. B. N. Y. Setty, S. Kulkarni, C. D. Dampier, and M. J. Stuart, “Fetal hemoglobin in sickle cell anemia: relationship to erythrocyte adhesion markers and adhesion,” Blood, vol. 97, no. 9, pp. 2568–2573, 2001. View at Publisher · View at Google Scholar · View at Scopus
  290. Z. Yasin, S. Witting, M. B. Palascak, C. H. Joiner, D. L. Rucknagel, and R. S. Franco, “Phosphatidylserine externalization in sickle red blood cells: associations with cell age, density, and hemoglobin F,” Blood, vol. 102, no. 1, pp. 365–370, 2003. View at Publisher · View at Google Scholar · View at Scopus
  291. S. Charache, M. L. Terrin, R. D. Moore et al., “Effect of hydroxyurea on the frequency of painful crises in sickle-cell-anemia,” The New England Journal of Medicine, vol. 332, no. 20, pp. 1317–1322, 1995. View at Publisher · View at Google Scholar · View at Scopus
  292. K. Kirk, “Membrane transport in the malaria-infected erythrocyte,” Physiological Reviews, vol. 81, no. 2, pp. 495–537, 2001. View at Google Scholar · View at Scopus
  293. C. Duranton, S. M. Huber, V. Tanneur et al., “Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes,” Cellular Physiology and Biochemistry, vol. 13, no. 4, pp. 189–198, 2003. View at Publisher · View at Google Scholar · View at Scopus
  294. V. B. Brand, C. D. Sandu, C. Duranton et al., “Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte,” Cellular Physiology and Biochemistry, vol. 13, no. 6, pp. 347–356, 2003. View at Publisher · View at Google Scholar · View at Scopus
  295. F. Lang, P. A. Lang, K. S. Lang et al., “Channel-induced apoptosis of infected host cells—the case of malaria,” Pflugers Archiv, vol. 448, no. 3, pp. 319–324, 2004. View at Publisher · View at Google Scholar · View at Scopus
  296. S. M. Huber, C. Duranton, and F. Lang, “Patch-clamp analysis of the ‘new permeability pathways’ in malaria-infected erythrocytes,” International Review of Cytology, vol. 246, pp. 59–134, 2005. View at Publisher · View at Google Scholar · View at Scopus
  297. V. L. Lew, T. Tiffert, and H. Ginsburg, “Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells,” Blood, vol. 101, no. 10, pp. 4189–4194, 2003. View at Publisher · View at Google Scholar · View at Scopus
  298. P. Joshi and C. M. Gupta, “Abnormal membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes,” British Journal of Haematology, vol. 68, no. 2, pp. 255–259, 1988. View at Publisher · View at Google Scholar · View at Scopus
  299. R. S. Schwartz, J. A. Olson, C. Raventos-Suarez et al., “Altered plasma membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes,” Blood, vol. 69, no. 2, pp. 401–407, 1987. View at Google Scholar · View at Scopus
  300. K. Ayi, G. Giribaldi, A. Skorokhod, E. Schwarzer, P. T. Prendergast, and P. Arese, “16alpha-bromoepiandrosterone, an antimalarial analogue of the hormone dehydroepiandrosterone, enhances phagocytosis of ring stage parasitized erythrocytes: a novel mechanism for antimalarial activity,” Antimicrobial Agents and Chemotherapy, vol. 46, no. 10, pp. 3180–3184, 2002. View at Publisher · View at Google Scholar · View at Scopus
  301. F. Turrini, H. Ginsburg, F. Bussolino, G. P. Pescarmona, M. V. Serra, and P. Arese, “Phagocytosis of Plasmodium falciparum-infected human red blood cells by human monocytes: involvement of immune and nonimmune determinants and dependence on parasite developmental stage,” Blood, vol. 80, no. 3, pp. 801–808, 1992. View at Google Scholar · View at Scopus
  302. I. W. Sherman, S. Eda, and E. Winograd, “Erythrocyte aging and malaria,” Cellular and Molecular Biology, vol. 50, no. 2, pp. 159–169, 2004. View at Google Scholar · View at Scopus
  303. I. W. Sherman, S. Eda, and E. Winograd, “Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind,” Microbes and Infection, vol. 5, no. 10, pp. 897–909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  304. S. Koka, M. Föller, G. Lamprecht et al., “Iron deficiency influences the course of malaria in Plasmodium berghei infected mice,” Biochemical and Biophysical Research Communications, vol. 357, no. 3, pp. 608–614, 2007. View at Publisher · View at Google Scholar · View at Scopus
  305. S. Koka, S. M. Huber, K. M. Boini, C. Lang, M. Föller, and F. Lang, “Lead decreases parasitemia and enhances survival of Plasmodium berghei-infected mice,” Biochemical and Biophysical Research Communications, vol. 363, no. 3, pp. 484–489, 2007. View at Publisher · View at Google Scholar · View at Scopus