The complement anaphylatoxin C5a induces apoptosis in adrenomedullary cells during experimental sepsis

PLoS ONE

Volumn 3, Issue 7, 2008, Pages

  Flierl, Michael A ^a   Rittirsch, Daniel ^a   Chen, Anthony J ^a   Nadeau, Brian A ^a   Day, Danielle E ^a   Sarma, J Vidya ^a   Huber Lang, Markus S ^b   Ward, Peter A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ULM MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHYLATOXIN; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5 INHIBITOR; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT COMPONENT C5L2; COMPLEMENT COMPONENT C5R; DOPAMINE; NORADRENALIN; CATECHOLAMINE; COMPLEMENT; LIPOCORTIN 5; PROPIDIUM IODIDE;

ADRENAL CELL; ADRENAL MEDULLA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL STRAIN; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; NICK END LABELING; NONHUMAN; PHEOCHROMOCYTOMA CELL; PROTEIN FUNCTION; RAT; RISK FACTOR; SEPSIS; SEPTIC SHOCK; ANIMAL; CHEMISTRY; METABOLISM; MOUSE; PATHOLOGY;

RATTUS;

ADRENAL MEDULLA; ANAPHYLATOXINS; ANIMALS; ANNEXIN A5; APOPTOSIS; CATECHOLAMINES; COMPLEMENT C5A; COMPLEMENT SYSTEM PROTEINS; IN SITU NICK-END LABELING; MICE; NOREPINEPHRINE; PC12 CELLS; PROPIDIUM; RATS; SEPSIS;

EID: 50149117225     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002560     Document Type: Article

References (46)

1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, et al. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29: 1303-1310.
2. Annane D, Aegerter P, Jars-Guincestre MC, Guidet B (2003) Current epidemiology of septic shock: the CUB-Rea Network. Am J Respir Crit Care Med 168: 165-172.
3. Dombrovskiy VY, Martin AA, Sunderram J, Paz HL (2007) Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003. Crit Care Med 35: 1244-1250.
4. Kochanek KD, Smith BL (2004) Deaths: preliminary data for 2002. Natl Vital Stat Rep 52: 1-47.
5. Remick DG (2007) Pathophysiology of sepsis. Am J Pathol 170: 1435-1444.
6. Rittirsch D, Flierl MA, Nadeau BA, Day DE, Huber-Lang M, et al. (2008) Functional roles for C5a receptors in sepsis. Nat Med 14: 551-557.
7. Tracey KJ (2002) The inflammatory reflex. Nature 420: 853-859.
8. Sternberg EM (2006) Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat Rev Immunol 6: 318-328.
9. Tracey KJ (2007) Physiology and immunology of the cholinergic antiinflammatory pathway. J Clin Invest 117: 289-296.
10. Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES (2000) The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 52: 595-638.
11. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, et al. (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405: 458-462.
12. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, et al. (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421: 384-388.
13. Flierl MA, Rittirsch D, Nadeau BA, Chen AJ, Sarma JV, et al. (2007) Phagocyte-derived catecholamines enhance acute inflammatory injury. Nature 449: 721-725.
14. Flierl MA, Rittirsch D, Huber-Lang M, Sarma JV, Ward PA (2008) Catecholamines-crafty weapons in the inflammatory arsenal of immune/ inflammatory cells or opening pandora's box? Mol Med 14: 195-204.
15. Baker CC, Chaudry IH, Gaines HO, Baue AE. (1983) Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 94: 331-335.
16. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73: 2424-2428.
17. Laudes IJ, Chu JC, Huber-Lang M, Guo RF, Riedemann NC, et al. (2002) Expression and function of C5a receptor in mouse microvascular endothelial cells. J Immunol 169: 5962-5970.
18. Hack CE, Nuijens JH, Felt-Bersma RJ, Schreuder WO, Eerenberg-Belmer AJ, et al. (1989) Elevated plasma levels of the anaphylatoxins C3a and C4a are associated with a fatal outcome in sepsis. Am J Med 86: 20-26.
19. Hecke F, Schmidt U, Kola A, Baunch W, Klos A, et al. (1997) Circulating complement proteins in multiple trauma patients-correlation with injury severity, development of sepsis, and outcome. Crit Care Med 25: 2015-2024.
20. Nakae H, Endo S, Inada K, Takakuwa T, Kasai T, et al. (1994) Serum complement levels and severity of sepsis. Res Commun Chem Pathol Pharmacol 81: 189-195.
21. Nakae H, Endo S, Inada K, Yoshida M (1996) Chronological changes in the complement system in sepsis. Surg Today 26: 225-229.
22. Guo RF, Ward PA (2005) Role of C5a in inflammatory responses. Annu Rev Immunol 23: 821-852.
23. Riedemann NC, Guo RF, Ward PA (2003) The enigma of sepsis. J Clin Invest 112: 460-467.
24. Huber-Lang M, Sarma VJ, Lu KT, McGuire SR, Padgaonkar VA, et al. (2001) Role of C5a in multiorgan failure during sepsis. J Immunol 166: 1193-1199.
25. Huber-Lang MS, Younkin EM, Sarma JV, McGuire SR, Lu KT, et al. (2002) Complement-induced impairment of innate immunity during sepsis. J Immunol 169: 3223-3231.
26. Niederbichler AD, Hoesel LM, Westfall MV, Gao H, Ipaktchi KR, et al. (2006) An essential role for complement C5a in the pathogenesis of septic cardiac dysfunction. J Exp Med 203: 53-61.
27. Laudes IJ, Chu JC, Sikranth S, Huber-Lang M, Guo RF, et al. (2002) Anti-c5a ameliorates coagulation/fibrinolytic protein changes in a rat model of sepsis. Am J Pathol 160: 1867-1875.
28. Riedemann NC, Guo RF, Bernacki KD, Reuben JS, Laudes IJ, et al. (2003) Regulation by C5a of neutrophil activation during sepsis. Immunity 19: 193-202.
29. Gerard C (2003) Complement C5a in the sepsis syndrome too much of a good thing? N Engl J Med 348: 167-169.
30. Ward PA (2004) The dark side of C5a in sepsis. Nat Rev Immunol 4: 133-142.
31. Bardakhch'ian EA, Kirichenko Iu G (1986) [Changes in the ultrastructure of the adrenal medulla and cortex during endotoxic shock]. Biull Eksp Biol Med 102: 97-100.
32. Tracey KJ, Lowry SF, Fahey TJ, 3rd, Albert JD, Fong Y, et al. (1987) Cachectin/tumor necrosis factor induces lethal shock and stress hormone responses in the dog. Surg Gynecol Obstet 164: 415-422.
33. Hoffmann R (1977) Adrenal lesions in calves dying from endotoxin shock, with special reference to the Waterhouse-Friderichsen syndrome. J Comp Pathol 87: 231-239.
34. Hotchkiss RS, Nicholson DW (2006) Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol 6: 813-822.
35. Papathanassoglou ED, Moynihan JA, Ackerman MH (2000) Does programmed cell death (apoptosis) play a role in the development of multiple organ dysfunction in critically ill patients? A review and a theoretical framework. Crit Care Med 28: 537-519.
36. Ayala A, Chaudry IH (1996) Immune dysfunction in murine polymicrobial sepsis: mediators, macrophages, lymphocytes and apoptosis. Shock 6 Suppl 1: S27-38.
37. Mahidhara R, Billiar TR (2000) Apoptosis in sepsis. Crit Care Med 28: N105-113.
38. Guo RF, Huber-Lang M, Wang X, Sarma V, Padgaonkar VA, et al. (2000) Protective effects of anti-C5a in sepsis-induced thymocyte apoptosis. J Clin Invest 106: 1271-1280.
39. Hotchkiss RS, Swanson PE, Freeman BD, Tinsley KW, Cobb JP, et al. (1999) Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 27: 1230-1251.
40. Tinsley KW, Graysons MH, Swanson PE, Drewry AM, Chang KC, et al. (2003) Sepsis induces apoptosis and profound depletion of splenic interdigitating and follicular dendritic cells. J Immunol 171: 909-914.
41. Cheadle WG, Pemberton RM, Robinson D, Livingston DH, Rodriguez JL, et al. (1993) Lymphocyte subset responses to trauma and sepsis. J Trauma 35: 844-849.
42. Le Tulzo Y, Pangault C, Gacouin A, Guilloux V, Tribut O, et al. (2002) Early circulating lymphocyte apoptosis in human septic shock is associated with poor outcome. Shock 18: 487-494.
43. Hotchkiss RS, Tinsley KW, Swanson PE, Chang KC, Cobb JP, et al, (1999) Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc Natl Acad Sci U S A 96: 14541-14516.
44. Gao H, Neff TA, Guo RF, Speyer CL, Sarma JV, et al. (2005) Evidence for a functional role of the second C5a receptor C5L2. Faseb J 19: 1003-1005.
45. Huber-Lang MS, Sarma JV, Rittirsch D, Schreiber H, Weiss M, et al. (2005) Changes in the novel orphan C5a receptor (C5L2) during experimental sepsis and sepsis in humans. J Immunol 174: 1104-1110.
46. Huber-Lang MS, Sarma JV, McGuire SR, Lu KT, Guo RF, et al. (2001) Protective effects of anti-C5a peptide antibodies in experimental sepsis. Faseb J 15: 568-570.