Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2018 (2018), Article ID 9405617, 10 pages
https://doi.org/10.1155/2018/9405617
Review Article

Eryptosis: An Erythrocyte’s Suicidal Type of Cell Death

Department of Physiology, School of Medicine, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa

Correspondence should be addressed to Anna Margaretha Joubert; az.ca.pu@trebuoj.einna

Received 16 October 2017; Accepted 14 December 2017; Published 3 January 2018

Academic Editor: Christophe Duranton

Copyright © 2018 Lisa Repsold and Anna Margaretha Joubert. 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. Baylor College of Medicine, “Erythropoiesis and Red Blood Cell Physiology,” http://www.bcm.edu/medicine/heme-onc/index.cfm?pmid=4536.
  2. K. S. Lang, P. A. Lang, C. Bauer et al., “Mechanisms of suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 15, no. 5, pp. 195–202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. 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
  4. 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
  5. 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 & Differentiation, vol. 8, no. 12, pp. 1197–1206, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. 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
  7. 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
  8. A. D. Maher and P. W. Kuchel, “The Gárdos channel: A review of the Ca2+-activated K+ channel in human erythrocytes,” The International Journal of Biochemistry & Cell Biology, vol. 35, no. 8, pp. 1182–1197, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Lang, S. M. Qadri, and F. Lang, “Killing me softly—suicidal erythrocyte death,” The International Journal of Biochemistry & Cell Biology, vol. 44, no. 8, pp. 1236–1243, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. F. E. Boas, L. Forman, and E. Beutler, “Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 95, no. 6, pp. 3077–3081, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Föller, S. M. Huber, and F. Lang, “Erythrocyte programmed cell death,” IUBMB Life, vol. 60, no. 10, pp. 661–668, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. Q. Zhou, J. Zhao, T. Wiedmer, and P. J. Sims, “Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1,” Blood, vol. 99, no. 11, pp. 4030–4038, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. 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
  14. F. Lang, S. M. Huber, I. Szabo, and E. Gulbins, “Plasma membrane ion channels in suicidal cell death,” Archives of Biochemistry and Biophysics, vol. 462, no. 2, pp. 189–194, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. 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 & Differentiation, vol. 8, no. 12, pp. 1143–1156, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Lang and F. Lang, “Triggers, inhibitors, mechanisms, and significance of eryptosis: The suicidal erythrocyte death,” BioMed Research International, vol. 2015, Article ID 513518, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Lang, E. Lang, and M. Föller, “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
  18. S. M. Qadri, R. Bissinger, Z. Solh, and P. Oldenborg, “Eryptosis in health and disease: A paradigm shift towards understanding the (patho)physiological implications of programmed cell death of erythrocytes,” Blood Reviews, vol. 31, no. 6, pp. 349–361, 2017. View at Publisher · View at Google Scholar
  19. M. Pagano and C. Faggio, “The use of erythrocyte fragility to assess xenobiotic cytotoxicity,” Cell Biochemistry & Function, vol. 33, no. 6, pp. 351–355, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. 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
  21. F. Lang, K. S. Lang, P. A. Lang, S. M. Huber, and T. Wieder, “Osmotic shock-induced suicidal death of erythrocytes,” Acta Physiologica, vol. 87, no. 1-2, pp. 191–198, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. 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
  23. 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
  24. 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
  25. F. Lang, E. Gulbins, P. A. Lang, D. Zappulla, and M. Föller, “Ceramide in suicidal death of erythrocytes,” Cellular Physiology and Biochemistry, vol. 26, no. 1, pp. 21–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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,” The Journal of Biological Chemistry, vol. 280, no. 47, pp. 39460–39467, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. 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
  41. 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
  42. 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
  43. D. S. Kempe, P. A. Lang, K. Eisele et al., “Stimulation of erythrocyte phosphatidylserine exposure by lead ions,” American Journal of Physiology-Cell Physiology, vol. 288, no. 2, pp. C396–C402, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. 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
  45. 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
  46. 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
  47. 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
  48. 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
  49. 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
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. 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
  56. 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
  57. 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
  58. O. M. Niemoeller, P. J. Bentzen, E. Lang, and F. Lang, “Adenosine protects against suicidal erythrocyte death,” Pflügers Archiv - European Journal of Physiology, vol. 454, no. 3, pp. 427–439, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. 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
  60. 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
  61. 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
  62. 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
  63. J. P. Nicolay, G. Liebig, O. M. Niemoeller et al., “Inhibition of suicidal erythrocyte death by nitric oxide,” Pflügers Archiv - European Journal of Physiology, vol. 456, no. 2, pp. 293–305, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. B. A. Klarl, P. A. Lang, D. S. Kempe et al., “Protein kinase C mediates erythrocyte “programmed cell death” following glucose depletion,” American Journal of Physiology-Cell Physiology, vol. 290, no. 1, pp. C244–C253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. 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
  66. 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
  67. C. Birka, P. A. Lang, D. S. Kempe et al., “Enhanced susceptibility to erythrocyte ‘apoptosis’ following phosphate depletion,” Pflügers Archiv - European Journal of Physiology, vol. 448, no. 5, pp. 471–477, 2004. View at Google Scholar · View at Scopus
  68. 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
  69. D. S. Kempe, A. Akel, P. A. Lang et al., “Suicidal erythrocyte death in sepsis,” Journal of Molecular Medicine, vol. 85, no. 3, pp. 273–281, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. 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
  71. 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
  72. S. Koka, C. Lang, K. M. Boini, D. Bobbala, S. M. Huber, and F. Lang, “Influence of chlorpromazine on eryptosis, parasitemia and survival of Plasmodium berghei infected mice,” Cellular Physiology and Biochemistry, vol. 22, no. 1-4, pp. 261–268, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. 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
  74. 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
  75. 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
  76. 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
  77. 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
  78. 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
  79. 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
  80. 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
  81. 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
  82. 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
  83. 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
  84. 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. 151–164, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. 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
  86. F. Lang, E. Gulbins, H. Lerche, S. M. Huber, D. S. Kempe, and M. Föller, “Eryptosis, a window to systemic disease,” Cellular Physiology and Biochemistry, vol. 22, no. 5-6, pp. 373–380, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Mahmud, D. Mauro, M. Föller, and F. Lang, “Inhibitory effect of thymol on suicidal erythrocyte death,” Cellular Physiology and Biochemistry, vol. 24, no. 5-6, pp. 407–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. 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
  89. R. Bissinger, C. Schumacher, S. M. Qadri et al., “Enhanced eryptosis contributes to anemia in lung cancer patients,” Oncotarget , vol. 7, no. 12, pp. 14002–14014, 2016. View at Publisher · View at Google Scholar · View at Scopus
  90. F. Lang, R. Bissinger, M. Abed, and F. Artunc, “Eryptosis - the Neglected Cause of Anemia in End Stage Renal Disease,” Kidney and Blood Pressure Research, vol. 42, no. 4, pp. 749–760, 2017. View at Publisher · View at Google Scholar
  91. N. Jermnim, D. Sagan, S. Tangvarasittichai, and O. Tangvarasittichai, “Insulin reduces eryptosis in thalassemic red blood cells,” Public Health Journal of Burapha University, vol. 6, pp. 124–127, 2011. View at Google Scholar
  92. 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
  93. 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
  94. T. Hermle, E. Shumilina, P. Attanasio et al., “Decreased cation channel activity and blunted channel-dependent eryptosis in neonatal erythrocytes,” American Journal of Physiology-Cell Physiology, vol. 291, no. 4, pp. C710–C717, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. T. Wieder, P. A. Lang, K. S. Lang et al., “Studying mechanisms of eryptosis,” Cytotechnology, vol. 49, no. 2-3, pp. 117–132, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. 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
  97. E. Lang, R. Bissinger, E. Gulbins, and F. Lang, “Ceramide in the regulation of eryptosis, the suicidal erythrocyte death,” Apoptosis, vol. 20, no. 5, pp. 758–767, 2015. View at Publisher · View at Google Scholar · View at Scopus
  98. 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
  99. M. Briglia, M. A. Rossi, and C. Faggio, “Eryptosis: Ally or Enemy,” Current Medicinal Chemistry, vol. 24, no. 9, pp. 937–942, 2017. View at Publisher · View at Google Scholar
  100. E. Lefrançais, G. Ortiz-Muñoz, A. Caudrillier et al., “The lung is a site of platelet biogenesis and a reservoir for haematopoietic progenitors,” Nature, vol. 544, no. 7648, pp. 105–109, 2017. View at Publisher · View at Google Scholar · View at Scopus