Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2015, Article ID 697193, 11 pages
http://dx.doi.org/10.1155/2015/697193
Review Article

Reconciling the IPC and Two-Hit Models: Dissecting the Underlying Cellular and Molecular Mechanisms of Two Seemingly Opposing Frameworks

1Laboratory of Biochemistry and Protein Chemistry, Department of Cell Biology, Institute of Biology, University of Brasilia, 70910-900 Brasilia, DF, Brazil
2Laboratory of Surgical Physiopathology (LIM-62), Faculty of Medicine, University of Sao Paulo, 01246-904 Sao Paulo, SP, Brazil

Received 3 September 2015; Revised 10 November 2015; Accepted 18 November 2015

Academic Editor: Carlos Rosales

Copyright © 2015 Carlos F. M. Morris et al. 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. T. A. Mare, D. F. Treacher, M. Shankar-Hari et al., “The diagnostic and prognostic significance of monitoring blood levels of immature neutrophils in patients with systemic inflammation,” Critical Care, vol. 19, no. 1, article 57, 2015. View at Publisher · View at Google Scholar
  2. D. Stubljar and M. Skvarc, “Effective strategies for diagnosis of Systemic Inflammatory Response Syndrome (SIRS) due to bacterial infection in surgical patients,” Infectious Disorders: Drug Targets, vol. 15, no. 1, pp. 53–56, 2015. View at Publisher · View at Google Scholar
  3. M. Bhatia, R. L. Zemans, and S. Jeyaseelan, “Role of chemokines in the pathogenesis of acute lung injury,” American Journal of Respiratory Cell and Molecular Biology, vol. 46, no. 5, pp. 566–572, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Fontes, W. Fontes, E. M. Utiyama, and D. Birolini, “The efficacy of loop colostomy for complete fecal diversion,” Diseases of the Colon & Rectum, vol. 31, no. 4, pp. 298–302, 1988. View at Publisher · View at Google Scholar · View at Scopus
  5. C. F. M. Morris, M. S. Castro, and W. Fontes, “Neutrophil proteome: lessons from different standpoints,” Protein and Peptide Letters, vol. 15, no. 9, pp. 995–1001, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. M. de Souza Castro, N. M. de Sá, R. P. Gadelha et al., “Proteome analysis of resting human neutrophils,” Protein and Peptide Letters, vol. 13, no. 5, pp. 481–487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. R. N. Garrison, D. A. Spain, M. A. Wilson, P. A. Keelen, and P. D. Harris, “Microvascular changes explain the “two-hit” theory of multiple organ failure,” Annals of Surgery, vol. 227, no. 6, pp. 851–860, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Matsuda and Y. Hattori, “Systemic inflammatory response syndrome (SIRS): molecular pathophysiology and gene therapy,” Journal of Pharmacological Sciences, vol. 101, no. 3, pp. 189–198, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Okubo, L. Xi, N. L. Bernardo, K.-I. Yoshida, and R. C. Kukreja, “Myocardial preconditioning: basic concepts and potential mechanisms,” Molecular and Cellular Biochemistry, vol. 196, no. 1-2, pp. 3–12, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. C. E. Murry, R. B. Jennings, and K. A. Reimer, “Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium,” Circulation, vol. 74, no. 5, pp. 1124–1136, 1986. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Lenz, G. A. Franklin, and W. G. Cheadle, “Systemic inflammation after trauma,” Injury, vol. 38, no. 12, pp. 1336–1345, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. M. J. Bown, M. L. Nicholson, P. R. F. Bell, and R. D. Sayers, “Cytokines and inflammatory pathways in the pathogenesis of multiple organ failure following abdominal aortic aneurysm repair,” European Journal of Vascular and Endovascular Surgery, vol. 22, no. 6, pp. 485–495, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. M. J. Bown, M. L. Nicholson, P. R. F. Bell, and R. D. Sayers, “The systemic inflammatory response syndrome, organ failure, and mortality after abdominal aortic aneurysm repair,” Journal of Vascular Surgery, vol. 37, no. 3, pp. 600–606, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Fan, J. C. Marshall, M. Jimenez, P. N. Shek, J. Zagorski, and O. D. Rotstein, “Hemorrhagic shock primes for increased expression of cytokine-induced neutrophil chemoattractant in the lung: role in pulmonary inflammation following lipopolysaccharide,” The Journal of Immunology, vol. 161, no. 1, pp. 440–447, 1998. View at Google Scholar · View at Scopus
  15. B. J. Czermak, M. Breckwoldt, Z. B. Ravage et al., “Mechanisms of enhanced lung injury during sepsis,” American Journal of Pathology, vol. 154, no. 4, pp. 1057–1065, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. J. A. Nemzek, D. R. Call, S. J. Ebong, D. E. Newcomb, G. L. Bolgos, and D. G. Remick, “Immunopathology of a two-hit murine model of acid aspiration lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 278, no. 3, pp. L512–L520, 2000. View at Google Scholar · View at Scopus
  17. M. Van Griensven, M. Kuzu, M. Breddin et al., “Polymicrobial sepsis induces organ changes due to granulocyte adhesion in a murine two hit model of trauma,” Experimental and Toxicologic Pathology, vol. 54, no. 3, pp. 203–209, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. A. E. Baue, R. Durham, and E. Faist, “Systemic Inflammatory Response Syndrome (SIRS), multiple organ dysfunction syndrome (MODS), multiple organ failure (MOF): are we winning the battle?” Shock, vol. 10, no. 2, pp. 79–89, 1998. View at Publisher · View at Google Scholar · View at Scopus
  19. C. J. Hauser, P. Joshi, Q. Jones, X. Zhou, D. H. Livingston, and R. F. Lavery, “Suppression of natural killer cell activity in patients with fracture/soft tissue injury,” Archives of Surgery, vol. 132, no. 12, pp. 1326–1330, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Hietbrink, L. Koenderman, G. T. Rijkers, and L. P. H. Leenen, “Trauma: the role of the innate immune system,” World Journal of Emergency Surgery, vol. 1, article 15, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Keel and O. Trentz, “Pathophysiology of polytrauma,” Injury, vol. 36, no. 6, pp. 691–709, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. D. H. Livingston, S. H. Appel, S. R. Wellhausen, G. Sonnenfeld, and H. C. Polk Jr., “Depressed interferon gamma production and monocyte HLA-DR expression after severe injury,” Archives of Surgery, vol. 123, no. 11, pp. 1309–1312, 1988. View at Publisher · View at Google Scholar · View at Scopus
  23. M. F. Osuchowski, K. Welch, J. Siddiqui, and D. G. Remick, “Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality,” The Journal of Immunology, vol. 177, no. 3, pp. 1967–1974, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Zedler and E. Faist, “The impact of endogenous triggers on trauma-associated inflammation,” Current Opinion in Critical Care, vol. 12, no. 6, pp. 595–601, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Jones, N. Hopkins, T. G. Bailey, D. J. Green, N. T. Cable, and D. H. J. Thijssen, “Seven-day remote ischemic preconditioning improves local and systemic endothelial function and microcirculation in healthy humans,” American Journal of Hypertension, vol. 27, no. 7, pp. 918–925, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. Z. Li and Z.-Q. Jin, “Ischemic preconditioning enhances integrity of coronary endothelial tight junctions,” Biochemical and Biophysical Research Communications, vol. 425, no. 3, pp. 630–635, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Yang, M. A. H. Talukder, S. Varadharaj, M. Velayutham, and J. L. Zweier, “Early ischaemic preconditioning requires Akt- and PKA-mediated activation of eNOS via serine1176 phosphorylation,” Cardiovascular Research, vol. 97, no. 1, pp. 33–43, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Brom and W. Konig, “Cytokine-induced (interleukins-3, -6 and -8 and tumour necrosis factor-beta) activation and deactivation of human neutrophils,” Immunology, vol. 75, no. 2, pp. 281–285, 1992. View at Google Scholar · View at Scopus
  29. W. Ertel, M. Keel, D. Marty et al., “Significance of systemic inflammation in 1,278 trauma patients],” Unfallchirurg, vol. 101, no. 7, pp. 520–526, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Schlag, H. Redl, and S. Bahrami, “SIRS (systemic inflammatory response syndrome) following trauma and during sepsis,” Anästhesiologie, Intensivmedizin, Notfallmedizin, Schmerztherapie, vol. 29, no. 1, pp. 37–41, 1994. View at Google Scholar
  31. L. M. Teles, E. N. Aquino, A. C. Neves et al., “Comparison of the neutrophil proteome in trauma patients and normal controls,” Protein and Peptide Ltters, vol. 19, no. 6, pp. 663–672, 2012. View at Google Scholar
  32. M. C. Carroll and V. M. Holers, “Innate autoimmunity,” Advances in Immunology, vol. 86, pp. 137–157, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. S. D. Fleming and G. C. Tsokos, “Complement, natural antibodies, autoantibodies and tissue injury,” Autoimmunity Reviews, vol. 5, no. 2, pp. 89–92, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Mastellos and J. D. Lambris, “Complement: more than a ‘guard’ against invading pathogens?” Trends in Immunology, vol. 23, no. 10, pp. 485–491, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. B. P. Morgan, K. J. Marchbank, M. P. Longhi, C. L. Harris, and A. M. Gallimore, “Complement: central to innate immunity and bridging to adaptive responses,” Immunology Letters, vol. 97, no. 2, pp. 171–179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Schlag and H. Redl, “Mediators of injury and inflammation,” World Journal of Surgery, vol. 20, no. 4, pp. 406–410, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. O. I. Schmidt, C. E. Heyde, W. Ertel, and P. F. Stahel, “Closed head injury—an inflammatory disease?” Brain Research Reviews, vol. 48, no. 2, pp. 388–399, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. B. J. Czermak, A. B. Lentsch, N. M. Bless, H. Schmal, H. P. Friedl, and P. A. Ward, “Synergistic enhancement of chemokine generation and lung injury by C5a or the membrane attack complex of complement,” The American Journal of Pathology, vol. 154, no. 5, pp. 1513–1524, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. J. A. Ember and T. E. Hugli, “Complement factors and their receptors,” Immunopharmacology, vol. 38, no. 1-2, pp. 3–15, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Mastellos, D. Morikis, S. N. Isaacs, M. C. Holland, C. W. Strey, and J. D. Lambris, “Complement: structure, functions, evolution, and viral molecular mimicry,” Immunologic Research, vol. 27, no. 2-3, pp. 367–386, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. R.-F. Guo and P. A. Ward, “Role of C5a in inflammatory responses,” Annual Review of Immunology, vol. 23, pp. 821–852, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. B.-M. Bellander, S. K. Singhrao, M. Ohlsson, P. Mattsson, and M. Svensson, “Complement activation in the human brain after traumatic head injury,” Journal of Neurotrauma, vol. 18, no. 12, pp. 1295–1311, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Gallinaro, W. G. Cheadle, K. Applegate, and H. C. Polk Jr., “The role of the complement system in trauma and infection,” Surgery Gynecology and Obstetrics, vol. 174, no. 5, pp. 435–440, 1992. View at Google Scholar · View at Scopus
  44. M. Heideman, “The role of complement in trauma,” Acta Chirurgica Scandinavica, Supplement, vol. 522, pp. 233–244, 1985. View at Google Scholar · View at Scopus
  45. M. Heideman and L.-E. Gelin, “The general and local response to injury related to complement activation,” Acta Chirurgica Scandinavica. Supplementum, vol. 145, no. 489, pp. 215–223, 1979. View at Google Scholar · View at Scopus
  46. P. F. Stahel, M. C. Morganti-Kossmann, and T. Kossmann, “The role of the complement system in traumatic brain injury,” Brain Research Reviews, vol. 27, no. 3, pp. 243–256, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. P. F. Stahel, M. C. Morganti-Kossmann, D. Perez et al., “Intrathecal levels of complement-derived soluble membrane attack complex (sC5b-9) correlate with blood-brain barrier dysfunction in patients with traumatic brain injury,” Journal of Neurotrauma, vol. 18, no. 8, pp. 773–781, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. M. E. Bianchi, “DAMPs, PAMPs and alarmins: all we need to know about danger,” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 1–5, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. L. O. Carvalho, E. N. Aquino, A. C. Neves, and W. Fontes, “The neutrophil nucleus and its role in neutrophilic function,” Journal of Cellular Biochemistry, vol. 116, no. 9, pp. 1831–1836, 2015. View at Publisher · View at Google Scholar
  50. D. Foell, H. Wittkowski, T. Vogl, and J. Roth, “S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules,” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 28–37, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. C. A. Janeway Jr. and R. Medzhitov, “Innate immune recognition,” Annual Review of Immunology, vol. 20, pp. 197–216, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. U. Felderhoff-Mueser, O. I. Schmidt, A. Oberholzer, C. Bührer, and P. F. Stahel, “IL-18: a key player in neuroinflammation and neurodegeneration?” Trends in Neurosciences, vol. 28, no. 9, pp. 487–493, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. F. Y. Liew and I. B. McInnes, “The role of innate mediators in inflammatory response,” Molecular Immunology, vol. 38, no. 12-13, pp. 887–890, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. I. B. McInnes and J. A. Gracie, “Interleukin-15: a new cytokine target for the treatment of inflammatory diseases,” Current Opinion in Pharmacology, vol. 4, no. 4, pp. 392–397, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Perl, C. Hohmann, S. Denk et al., “Role of activated neutrophils in chest trauma-induced septic acute lung injury,” Shock, vol. 38, no. 1, pp. 98–106, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. I. F. Charo and R. M. Ransohoff, “The many roles of chemokines and chemokine receptors in inflammation,” The New England Journal of Medicine, vol. 354, no. 6, pp. 610–621, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. T. S. Blackwell and J. W. Christman, “Sepsis and cytokines: current status,” British Journal of Anaesthesia, vol. 77, no. 1, pp. 110–117, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. W. L. Biffl, E. E. Moore, F. A. Moore, and V. M. Peterson, “Interleukin-6 in the injured patient: marker of injury or mediator of inflammation?” Annals of Surgery, vol. 224, no. 5, pp. 647–664, 1996. View at Publisher · View at Google Scholar · View at Scopus
  59. A. M. Condliffe, E. Kitchen, and E. R. Chilvers, “Neutrophil priming: pathophysiological consequences and underlying mechanisms,” Clinical Science, vol. 94, no. 5, pp. 461–471, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. W. L. Biffl, E. E. Moore, G. Zallen et al., “Neutrophils are primed for cytotoxicity and resist apoptosis in injured patients at risk for multiple organ failure,” Surgery, vol. 126, no. 2, pp. 198–202, 1999. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Zallen, E. E. Moore, J. L. Johnson et al., “Circulating postinjury neutrophils are primed for the release of proinflammatory cytokines,” The Journal of Trauma, vol. 46, no. 1, pp. 42–48, 1999. View at Google Scholar
  62. M. S. Libério, G. A. Joanitti, R. B. Azevedo et al., “Anti-proliferative and cytotoxic activity of pentadactylin isolated from Leptodactylus labyrinthicus on melanoma cells,” Amino Acids, vol. 40, no. 1, pp. 51–59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Nascimento, A. Chapeaurouge, J. Perales et al., “Purification, characterization and homology analysis of ocellatin 4, a cytolytic peptide from the skin secretion of the frog Leptodactylus ocellatus,” Toxicon, vol. 50, no. 8, pp. 1095–1104, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. M. M. Kapur, P. Jain, and M. Gidh, “The effect of trauma on serum C3 activation and its correlation with injury severity score in man,” The Journal of Trauma, vol. 26, no. 5, pp. 464–466, 1986. View at Publisher · View at Google Scholar · View at Scopus
  65. H. Redl, H. Gasser, G. Schlag, and I. Marzi, “Involvement of oxygen radicals in shock related cell injury,” British Medical Bulletin, vol. 49, no. 3, pp. 556–565, 1993. View at Google Scholar · View at Scopus
  66. W. L. Biffl, E. E. Moore, F. A. Moore, V. S. Carl, F. J. Kim, and R. J. Franciose, “Interleukin-6 potentiates neutrophil priming with platelet-activating factor,” Archives of Surgery, vol. 129, no. 11, pp. 1131–1139, 1994. View at Publisher · View at Google Scholar
  67. R. S. Friese, T. F. Rehring, M. Wollmering et al., “Trauma primes cells,” Shock, vol. 1, no. 5, pp. 388–394, 1994. View at Publisher · View at Google Scholar · View at Scopus
  68. D. A. Partrick, F. A. Moore, E. E. Moore, C. C. Barnett Jr., and C. C. Silliman, “Neutrophil priming and activation in the pathogenesis of postinjury multiple organ failure,” New Horizons, vol. 4, no. 2, pp. 194–210, 1996. View at Google Scholar · View at Scopus
  69. A. J. Botha, F. A. Moore, E. E. Moore, A. Sauaia, A. Banerjee, and V. M. Peterson, “Early neutrophil sequestration after injury: a pathogenic mechanism for multiple organ failure,” Journal of Trauma—Injury, Infection and Critical Care, vol. 39, no. 3, pp. 411–417, 1995. View at Google Scholar · View at Scopus
  70. H.-C. Pape, D. Remmers, M. Grotz et al., “Reticuloendothelial system activity and organ failure in patients with multiple injuries,” Archives of Surgery, vol. 134, no. 4, pp. 421–427, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. M. R. Rosengart, A. B. Nathens, S. Arbabi et al., “Mitogen-activated protein kinases in the intensive care unit: prognostic potential,” Annals of Surgery, vol. 237, no. 1, pp. 94–100, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Waydhas, D. Nast-Kolb, A. Trupka et al., “Posttraumatic inflammatory response, secondary operations, and late multiple organ failure,” Journal of Trauma, vol. 40, no. 4, pp. 624–630, 1996. View at Publisher · View at Google Scholar · View at Scopus
  73. A. J. Botha, F. A. Moore, E. E. Moore, F. J. Kim, A. Banerjee, and V. M. Peterson, “Postinjury neutrophil priming and activation: an early vulnerable window,” Surgery, vol. 118, no. 2, pp. 358–365, 1995. View at Publisher · View at Google Scholar · View at Scopus
  74. D. J. Ciesla, E. E. Moore, J. L. Johnson, J. M. Burch, C. C. Cothren, and A. Sauaia, “The role of the lung in postinjury multiple organ failure,” Surgery, vol. 138, no. 4, pp. 749–758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. M. C. Morganti-Kossmann, M. Rancan, V. I. Otto, P. F. Stahel, and T. Kossmann, “Role of cerebral inflammation after traumatic brain injury: a revisited concept,” Shock, vol. 16, no. 3, pp. 165–177, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. D. A. Partrick, E. E. Moore, F. A. Moore, W. L. Biffl, and C. C. Barnett Jr., “Release of anti-inflammatory mediators after major torso trauma correlates with the development of postinjury multiple organ failure,” The American Journal of Surgery, vol. 178, no. 6, pp. 564–569, 1999. View at Publisher · View at Google Scholar · View at Scopus
  77. R. J. Schoettle, P. M. Kochanek, M. J. Magargee, M. W. Uhl, and E. M. Nemoto, “Early polymorphonuclear leukocyte accumulation correlates with the development of posttraumatic cerebral edema in rats,” Journal of Neurotrauma, vol. 7, no. 4, pp. 207–217, 1990. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Scholz, J. Cinatl, M. Schädel-Höpfner, and J. Windolf, “Neutrophils and the blood-brain barrier dysfunction after trauma,” Medicinal Research Reviews, vol. 27, no. 3, pp. 401–416, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. A. W. Unterberg, J. Stover, B. Kress, and K. L. Kiening, “Edema and brain trauma,” Neuroscience, vol. 129, no. 4, pp. 1021–1029, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. E. Rahbar, J. C. Cardenas, G. Baimukanova et al., “Endothelial glycocalyx shedding and vascular permeability in severely injured trauma patients,” Journal of Translational Medicine, vol. 13, no. 1, article 117, 2015. View at Publisher · View at Google Scholar
  81. H. Kolářová, B. Ambrůzová, L. Švihálková Šindlerová, A. Klinke, and L. Kubala, “Modulation of endothelial glycocalyx structure under inflammatory conditions,” Mediators of Inflammation, vol. 2014, Article ID 694312, 17 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. Van Zandvoort, and M. G. A. Oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflügers Archiv, vol. 454, no. 3, pp. 345–359, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. H. H. Lipowsky, “The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases,” Annals of Biomedical Engineering, vol. 40, no. 4, pp. 840–848, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Khakpour, K. Wilhelmsen, and J. Hellman, “Vascular endothelial cell Toll-like receptor pathways in sepsis,” Innate Immunity, vol. 21, no. 8, pp. 827–846, 2015. View at Publisher · View at Google Scholar
  85. U. K. Sampson, M. M. Engelgau, E. K. Peprah, and G. A. Mensah, “Endothelial dysfunction: a unifying hypothesis for the burden of cardiovascular diseases in sub-Saharan Africa,” Cardiovascular Journal of Africa, vol. 26, no. 2, supplement 1, pp. S56–S60, 2015. View at Google Scholar
  86. S. Sukriti, M. Tauseef, P. Yazbeck, and D. Mehta, “Mechanisms regulating endothelial permeability,” Pulmonary Circulation, vol. 4, no. 4, pp. 535–551, 2014. View at Publisher · View at Google Scholar
  87. D. Mehta and A. B. Malik, “Signaling mechanisms regulating endothelial permeability,” Physiological Reviews, vol. 86, no. 1, pp. 279–367, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. G. Asimakopoulos and K. M. Taylor, “Effects of cardiopulmonary bypass on leukocyte and endothelial adhesion molecules,” Annals of Thoracic Surgery, vol. 66, no. 6, pp. 2135–2144, 1998. View at Publisher · View at Google Scholar · View at Scopus
  89. G. Matheis, M. Scholz, A. Simon, O. Dzemali, and A. Mortiz, “Leukocyte filtration in cardiac surgery: a review,” Perfusion, vol. 16, no. 5, pp. 361–370, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. D. Vestweber, “Molecular mechanisms that control endothelial cell contacts,” Journal of Pathology, vol. 190, no. 3, pp. 281–291, 2000. View at Google Scholar · View at Scopus
  91. T. M. Carlos and J. M. Harlan, “Leukocyte-endothelial adhesion molecules,” Blood, vol. 84, no. 7, pp. 2068–2101, 1994. View at Google Scholar · View at Scopus
  92. W. F. Westlin and M. A. Gimbrone Jr., “Neutrophil-mediated damage to human vascular endothelium. Role of cytokine activation,” The American Journal of Pathology, vol. 142, no. 1, pp. 117–128, 1993. View at Google Scholar · View at Scopus
  93. J. Varani and P. A. Ward, “Mechanisms of endothelial cell injury in acute inflammation,” Shock, vol. 2, no. 5, pp. 311–319, 1994. View at Publisher · View at Google Scholar · View at Scopus
  94. W. van Oeveren, C. R. H. Wildevuur, and M. D. Kazatchkine, “Biocompatibility of extracorporeal circuits in heart surgery,” Transfusion Science, vol. 11, no. 1, pp. 5–31, 1990. View at Publisher · View at Google Scholar · View at Scopus
  95. S. D. Marlin and T. A. Springer, “Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1),” Cell, vol. 51, no. 5, pp. 813–819, 1987. View at Publisher · View at Google Scholar · View at Scopus
  96. W. Fontes, R. B. Cunha, M. V. Sousa, and L. Morhy, “Improving the recovery of lysine in automated protein sequencing,” Analytical Biochemistry, vol. 258, no. 2, pp. 259–267, 1998. View at Publisher · View at Google Scholar · View at Scopus
  97. S. J. Weiss, “Tissue destruction by neutrophils,” The New England Journal of Medicine, vol. 320, no. 6, pp. 365–376, 1989. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Kitagawa, M. Matsumoto, M. Tagaya et al., “‘Ischemic tolerance’ phenomenon found in the brain,” Brain Research, vol. 528, no. 1, pp. 21–24, 1990. View at Publisher · View at Google Scholar · View at Scopus
  99. J. Moncayo, G. R. de Freitas, J. Bogousslavsky, M. Altieri, and G. Van Melle, “Do transient ischemic attacks have a neuroprotective effect?” Neurology, vol. 54, no. 11, pp. 2089–2094, 2000. View at Publisher · View at Google Scholar · View at Scopus
  100. Y. W. Li, P. Whittaker, and R. A. Kloner, “The transient nature of the effect of ischemic preconditioning on myocardial infarct size and ventricular arrhythmia,” American Heart Journal, vol. 123, no. 2, pp. 346–353, 1992. View at Publisher · View at Google Scholar · View at Scopus
  101. Y.-Z. Qian, J. E. Levasseur, K.-I. Yoshida, and R. C. Kukreja, “KATP channels in rat heart: blockade of ischemic and acetylcholine-mediated preconditioning by glibenclamide,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 271, no. 1, part 2, pp. H23–H28, 1996. View at Google Scholar · View at Scopus
  102. M. S. Marber, D. S. Latchman, J. M. Walker, and D. M. Yellon, “Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction,” Circulation, vol. 88, no. 3, pp. 1264–1272, 1993. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Ovize, K. Przyklenk, S. L. Hale, and R. A. Kloner, “Preconditioning does not attenuate myocardial stunning,” Circulation, vol. 85, no. 6, pp. 2247–2254, 1992. View at Publisher · View at Google Scholar · View at Scopus
  104. I. Laskowski, J. Pratschke, M. J. Wilhelm, M. Gasser, and N. L. Tilney, “Molecular and cellular events associated with ischemia/reperfusion injury,” Annals of Transplantation, vol. 5, no. 4, pp. 29–35, 2000. View at Google Scholar · View at Scopus
  105. I. E. Konstantinov, S. Arab, R. K. Kharbanda et al., “The remote ischemic preconditioning stimulus modifies inflammatory gene expression in humans,” Physiological Genomics, vol. 19, no. 1, pp. 143–150, 2004. View at Publisher · View at Google Scholar · View at Scopus
  106. N. Tapuria, Y. Kumar, M. M. Habib, M. A. Amara, A. M. Seifalian, and B. R. Davidson, “Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury—a review,” Journal of Surgical Research, vol. 150, no. 2, pp. 304–330, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. T. B. McClanahan, B. S. Nao, L. J. Wolke, B. J. Martin, T. E. Mertz, and K. P. Gallagher, “Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits,” The FASEB Journal, vol. 7, no. A118, pp. 682–683, 1993. View at Google Scholar
  108. B. C. G. Gho, R. G. Schoemaker, M. A. Van den Doel, D. J. Duncker, and P. D. Verdouw, “Myocardial protection by brief ischemia in noncardiac tissue,” Circulation, vol. 94, no. 9, pp. 2193–2200, 1996. View at Publisher · View at Google Scholar · View at Scopus
  109. K. R. Eberlin, M. C. McCormack, J. T. Nguyen, H. S. Tatlidede, M. A. Randolph, and W. G. Austen Jr., “Ischemic preconditioning of skeletal muscle mitigates remote injury and mortality,” Journal of Surgical Research, vol. 148, no. 1, pp. 24–30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  110. D. W. Harkin, A. A. B. D'Sa Barros, K. McCallion, M. Hoper, and F. C. Campbell, “Ischemic preconditioning before lower limb ischemia—reperfusion protects against acute lung injury,” Journal of Vascular Surgery, vol. 35, no. 6, pp. 1264–1273, 2002. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Tahir, S. Arshid, A. M. C. Heimbecker et al., “Evaluation of the effects of ischemic preconditioning on the hematological parameters of rats subjected to intestinal ischemia and reperfusion,” Clinics, vol. 70, no. 1, pp. 61–68, 2015. View at Publisher · View at Google Scholar · View at Scopus
  112. A. Zuk and J. V. Bonventre, “Acute kidney injury: can remote ischaemic preconditioning prevent AKI?” Nature Reviews Nephrology, vol. 11, no. 9, pp. 512–513, 2015. View at Publisher · View at Google Scholar
  113. K. Przyklenk, B. Bauer, M. Ovize, R. A. Kloner, and P. Whittaker, “Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion,” Circulation, vol. 87, no. 3, pp. 893–899, 1993. View at Publisher · View at Google Scholar · View at Scopus
  114. D. J. Hausenloy, E. Boston-Griffiths, and D. M. Yellon, “Cardioprotection during cardiac surgery,” Cardiovascular Research, vol. 94, no. 2, pp. 253–265, 2012. View at Publisher · View at Google Scholar · View at Scopus
  115. R. Gill, R. Kuriakose, Z. M. Gertz, F. N. Salloum, L. Xi, and R. C. Kukreja, “Remote ischemic preconditioning for myocardial protection: update on mechanisms and clinical relevance,” Molecular and Cellular Biochemistry, vol. 402, no. 1-2, pp. 41–49, 2015. View at Publisher · View at Google Scholar · View at Scopus
  116. P. J. Sullivan, K. J. Sweeney, K. M. Hirpara, C. B. Malone, W. Curtin, and M. J. Kerin, “Cyclical ischaemic preconditioning modulates the adaptive immune response in human limb ischaemia-reperfusion injury,” British Journal of Surgery, vol. 96, no. 4, pp. 381–390, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. T. J. Pell, G. F. Baxter, D. M. Yellon, and G. M. Drew, “Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 275, part 2, no. 5, pp. H1542–H1547, 1998. View at Google Scholar · View at Scopus
  118. R. G. Schoemaker and C. L. van Heijningen, “Bradykinin mediates cardiac preconditioning at a distance,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 278, no. 5, pp. H1571–H1576, 2000. View at Google Scholar · View at Scopus
  119. H. H. Patel, J. Moore, A. K. Hsu, and G. J. Gross, “Cardioprotection at a distance: mesenteric artery occlusion protects the myocardium via an opioid sensitive mechanism,” Journal of Molecular and Cellular Cardiology, vol. 34, no. 10, pp. 1317–1323, 2002. View at Publisher · View at Google Scholar · View at Scopus
  120. A. R. Hajrasouliha, S. Tavakoli, M. Ghasemi et al., “Endogenous cannabinoids contribute to remote ischemic preconditioning via cannabinoid CB2 receptors in the rat heart,” European Journal of Pharmacology, vol. 579, no. 1–3, pp. 246–252, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. S. Wolfrum, K. Schneider, M. Heidbreder, J. Nienstedt, P. Dominiak, and A. Dendorfer, “Remote preconditioning protects the heart by activating myocardial PKCε-isoform,” Cardiovascular Research, vol. 55, no. 3, pp. 583–589, 2002. View at Publisher · View at Google Scholar · View at Scopus
  122. D. Singh and K. Chopra, “Evidence of the role of angiotensin AT1 receptors in remote renal preconditioning of myocardium,” Methods and Findings in Experimental and Clinical Pharmacology, vol. 26, no. 2, pp. 117–122, 2004. View at Publisher · View at Google Scholar · View at Scopus
  123. C. Weinbrenner, M. Nelles, N. Herzog, L. Sárváry, and R. H. Strasser, “Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: a newly identified non-neuronal but PKC-dependent pathway,” Cardiovascular Research, vol. 55, no. 3, pp. 590–601, 2002. View at Publisher · View at Google Scholar · View at Scopus
  124. R. Bolli, S. Manchikalapudi, X.-L. Tang et al., “The protective effect of late preconditioning against myocardial stunning in conscious rabbits is mediated by nitric oxide synthase: evidence that nitric oxide acts both as a trigger and as a mediator of the late phase of ischemic preconditioning,” Circulation Research, vol. 81, no. 6, pp. 1094–1107, 1997. View at Publisher · View at Google Scholar · View at Scopus
  125. M. A. H. Talukder, F. Yang, H. Shimokawa, and J. L. Zweier, “eNOS is required for acute in vivo ischemic preconditioning of the heart: effects of ischemic duration and sex,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 299, no. 2, pp. H437–H445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  126. M. V. Cohen, C. P. Baines, and J. M. Downey, “Ischemic preconditioning: from adenosine receptor to KATP channel,” Annual Review of Physiology, vol. 62, pp. 79–109, 2000. View at Publisher · View at Google Scholar · View at Scopus
  127. M. J. Sisalli, L. Annunziato, and A. Scorziello, “Novel cellular mechanisms for neuroprotection in ischemic preconditioning: a view from inside organelles,” Frontiers in Neurology, vol. 6, p. 115, 2015. View at Publisher · View at Google Scholar
  128. A. P. Wojtovich, W. R. Urciuoli, S. Chatterjee, A. B. Fisher, K. Nehrke, and P. S. Brookes, “Kir6.2 is not the mitochondrial KATP channel but is required for cardioprotection by ischemic preconditioning,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 304, no. 11, pp. H1439–H1445, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. D. J. Hausenloy, “Cardioprotection techniques: preconditioning, postconditioning and remote conditioning (basic science),” Current Pharmaceutical Design, vol. 19, no. 25, pp. 4544–4563, 2013. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Duda, E. Czarnowska, M. Kurzelewski, A. Konior, and A. Beresewicz, “Ischemic preconditioning prevents endothelial dysfunction, P-selectin expression, and neutrophil adhesion by preventing endothelin and O2- generation in the post-ischemic guinea-pig heart,” Journal of Physiology and Pharmacology, vol. 57, no. 4, pp. 553–569, 2006. View at Google Scholar · View at Scopus
  131. G. Li, F. Labruto, A. Sirsjö, F. Chen, J. Vaage, and G. Valen, “Myocardial protection by remote preconditioning: the role of nuclear factor κ-B p105 and inducible nitric oxide synthase,” European Journal of Cardio-thoracic Surgery, vol. 26, no. 5, pp. 968–973, 2004. View at Publisher · View at Google Scholar · View at Scopus
  132. N. N. Petrishchev, T. D. Vlasov, V. G. Sipovsky, D. I. Kurapeev, and M. M. Galagudza, “Does nitric oxide generation contribute to the mechanism of remote ischemic preconditioning?” Pathophysiology, vol. 7, no. 4, pp. 271–274, 2001. View at Publisher · View at Google Scholar · View at Scopus
  133. C. C. Lai, C. Y. Tang, S. C. Chiang, K. W. Tseng, and C. H. Huang, “Ischemic preconditioning activates prosurvival kinases and reduces myocardial apoptosis,” Journal of the Chinese Medical Association, vol. 78, no. 8, pp. 460–468, 2015. View at Google Scholar
  134. M. Albrecht, K. Zitta, B. Bein et al., “Remote ischemic preconditioning regulates HIF-1alpha levels, apoptosis and inflammation in heart tissue of cardiosurgical patients: a pilot experimental study,” Basic Research in Cardiology, vol. 108, no. 1, article 314, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. T. Brandenburger, R. Huhn, A. Galas et al., “Remote ischemic preconditioning preserves Connexin 43 phosphorylation in the rat heart in vivo,” Journal of Translational Medicine, vol. 12, p. 228, 2014. View at Publisher · View at Google Scholar · View at Scopus
  136. S. K. Jain, R. B. Schuessler, and J. E. Saffitz, “Mechanisms of delayed electrical uncoupling induced by ischemic preconditioning,” Circulation Research, vol. 92, no. 10, pp. 1138–1144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  137. J. Li, S. Rohailla, N. Gelber et al., “MicroRNA-144 is a circulating effector of remote ischemic preconditioning,” Basic Research in Cardiology, vol. 109, no. 5, article 423, 2014. View at Publisher · View at Google Scholar · View at Scopus