Neutrophils - A key component of ischemia-reperfusion injury

Shock

Volumn 40, Issue 6, 2013, Pages 463-470

  Schofield, Zoe Victoria ^a   Woodruff, Trent Martin ^a   Halai, Reena ^a   Wu, Mike Chia Lun ^a   Cooper, Matthew Allister ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

cytokines; Inflammation; migration; multiple organ failure

Indexed keywords

DISEASE SEVERITY; HEART MUSCLE ISCHEMIA; HUMAN; INFLAMMATION; INTESTINE ISCHEMIA; KIDNEY ISCHEMIA; LIVER ISCHEMIA; LUNG INJURY; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; REPERFUSION INJURY; REVIEW; TISSUE INJURY;

ANIMALS; CYTOKINES; HUMANS; MOLECULAR TARGETED THERAPY; NEUTROPHIL ACTIVATION; NEUTROPHIL INFILTRATION; NEUTROPHILS; REPERFUSION INJURY;

EID: 84888131816     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0000000000000044     Document Type: Review

References (107)

1. Feinberg H, Levitsky S: Postbypass treatment. Ann Thorac Surg 20(1): 106-113, 1975.
2. Widgerow AD: Ischemia-reperfusion injury: influencing the microcirculatory and cellular environment. Ann Plast Surg 2012 Dec 13. [Epub ahead of print]
3. Linfert D, Chowdhry T, Rabb H: Lymphocytes and ischemia-reperfusion injury. Transplant Rev 23(1):1-10, 2009.
4. Boros P, Bromberg JS: New cellular and Mol immune pathways in ischemia/ reperfusion injury. Am J Transplant 6(4):652-658, 2006.
5. Arslan F, Keogh B, McGuirk P, Parker a E: TLR2 and TLR4 in ischemia reperfusion injury. Mediat Inflamm 2010:704202, 2010.
6. Yoshiya K, Lapchak PH, Thai T-H, Kannan L, Rani P, Dalle Lucca JJ, Tsokos GC: Depletion of gut commensal bacteria attenuates intestinal ischemia/ reperfusion injury. Am J Physiol Gastrointest Liver Physiol 301(6):G1020Y G1030, 2011.
7. Cerqueira NF, Hussni CA, Yoshida WB: PathoPhysiol of mesenteric ischemia/ reperfusion: a review. Acta Cir Bras 20(4):336-343, 2005.
8. Jin R, Yang G, Li G: Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 87(5):779-789, 2010.
9. Grootjans J, Lenaerts K, Derikx JPM, Matthijsen RA, de BruBne AP, Van Bijnen AA, van Dam, RM, Dejong, CHC, Buurman, WA: Human intestinal ischemia-reperfusionYinduced inflammation characterized: experiences from a new translational model. Am J Pathol 176(5):2283-2291, 2010.
10. Braunersreuther V, Jaquet V: Reactive oxygen species in myocardial reperfusion injury: from physiopathololgy to therapeutic approaches. Curr Pharm Biotechnol 13(1):97-114, 2012.
11. Farrar CA, Asgari E, Schwaeble WJ, Sacks SH: Which pathways trigger the role of complement in ischaemia/reperfusion injury? Front Immunol 3(341): 1-6, 2012.
12. Rodrigues SF, Granger DN: Role of blood cells in ischaemia-reperfusion induced endothelial barrier failure. Cardiovasc Res 87(2):291-299, 2010.
13. Sivarajah A, Collino M, Yasin M, Benetti E, Gallicchio M, Mazzon E, Cuzzocrea S, Fantozzi R, Thiemermann C: Anti-apoptotic and anti-inflammatory effects of hydrogen sulfide in a rat model of regional myocardial I/R. Shock 31(3): 267-274, 2009.
14. WangWZ, Fang X-H, Stephenson LL, Khiabani KT, Zamboni WA: Ischemia/ reperfusionYinduced necrosis and apoptosis in the cells isolated from rat skeletal muscle. J Orthop Res 26(3):351-356, 2008.
15. Dzieciatkowska M, Wohlauer M V, Moore EE, Damle S, Peltz E, Campsen J, Kelher M, Silliman C, Banerjee A, Hansen KC: Proteomic analysis of human mesenteric lymph. Shock 35(4):331-338, 2011.
16. Chen L-W, Chang W-J, Chen P-H, Liu W-C, Hsu C-M: TLR ligand decreases mesenteric ischemia and reperfusion injuryYinduced gut damage through TNF-alpha signaling. Shock 30(5):563-570, 2008.
17. Alverdy JC, Chang EB: The re-emerging role of the intestinal microflora in critical illness and inflammation: why the gut hypothesis of sepsis syndrome will not go away. J Leukoc Biol 83(3):461-466, 2008.
18. Pope MR, Bukovnik U, Tomich JM, Fleming SD: Small "2-glycoprotein I peptides protect from intestinal ischemia reperfusion injury. J Immunol 189(10): 5047-5056, 2012.
19. Hernandez LA, Grisham MB, Twohig B, Arfors KE, Harlan JM, Granger DN: Role of neutrophils in ischemia-reperfusionYinduced microvascular injury. Am J Physiol 253:H699YH703, 1987.
20. Arumugam T V, Shiels IA,Woodruff TM, Granger DN, Taylor SM: The role of the complement system in ischemia-reperfusion injury. Shock 21(5):401-409, 2004.
21. Arumugam T V, Okun E, Tang S-C, Thundyil J, Taylor SM, Woodruff TM: Toll-like receptors in ischemia-reperfusion injury. Shock 32(1):4-16, 2009.
22. Soares AL, Coelho FR, Guabiraba R, Kamal M, Vargaftig BB, Li L, Li J, Tavaresde-Lima W, Ryffel B: Tumor necrosis factor is not associated with intestinal ischemia/reperfusionYinduced lung inflammation. Shock 34(3):306-313, 2010.
23. Wu MCL, Brennan FH, Lynch JPL, Mantovani S, Phipps S, Wetsel RA, Ruitenberg MJ, Taylor S, Woodruff TM: The receptor for complement component C3a mediates protection from intestinal ischemia-reperfusion injuries by inhibiting neutrophil mobilization. PNAS 1-6, 2013.
24. Ramaiah SK, Jaeschke H: Role of neutrophils in the pathogenesis of acute inflammatory liver injury. Toxicol Pathol 35(6):757-766, 2007.
25. Bolisetty S, Agarwal A: Neutrophils in acute kidney injury: not neutral any more. Kidney Int 75(7):674-676, 2009.
26. Grommes J, Soehnlein O: Contribution of neutrophils to acute lung injury. Mol Med 17(3-4):293-307, 2011.
27. El-Benna J, Dang PM-C, Gougerot-Pocidalo M-A: Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol 30(3):279-289, 2008.
28. Fialkow L, Wang Y, Downey GP: Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 42(2): 153-164, 2007.
29. Kolaczkowska E, Kubes P: Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13(3):159-175, 2013.
30. Mathers CD, Loncar D: Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3(11):2011-2030, 2006.
31. Vinten-Johansen J: Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovasc Res 61(3):481-497, 2004.
32. Duilio C, Ambrosio G, Kuppusamy P, DiPaula A, Becker LC, Zweier JL: Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. Am J Physiol Heart Circ 280(6):H2649YH2657, 2001.
33. Kakkar AK, Lefer DJ: Leukocyte and endothelial adhesion molecule studies in knockout mice. Curr Opin Pharmacol 4(2):154-158, 2004.
34. Fan H, Sun B, Gu Q, Lafond-Walker A, Cao S, Becker LC: Oxygen radicals trigger activation of NF-kappaB and AP-1 and upregulation of ICAM-1 in reperfused canine heart. Am J Physiol Heart Circ 282(5):H1778YH1786, 2002.
35. Litt MR, Jeremy RW, Weisman HF, Winkelstein JA, Becker LC: Neutrophil depletion limited to reperfusion reduces myocardial infarct size after 90 minutes of ischemia. Evidence for neutrophil-mediated reperfusion injury. Circulation 80(6):1816-1827, 1989.
36. Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA., Lucchesi BR: Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 67(5):1016-1023, 1983.
37. Budde JM, Morris CD, Velez DA, Muraki S, Wang N-P, Guyton RA, Zhao ZQ: Reduction of infarct size and preservation of endothelial function by multidose intravenous adenosine during extended reperfusion. J Surg Res 116(1): 104-115, 2004.
38. Chandrasekar B, Colston JT, Geimer J, Cortez D, Freeman GL: Induction of nuclear factor kB but not kB-responsive cytokine expression during myocardial reperfusion injury after neutropenia. Free Radic Biol Med 28(11):1579-1588, 2000.
39. Palazzo AJ, Jones SP, Anderson DC, Granger DN, Lefer DJ: Coronary endothelial P-selectin in pathogenesis of myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ 275(5):H1865YH1872, 1998.
40. Jones SP, Trocha SD, Strange MB, Granger DN, Kevil CG, Bullard DC, Lefer DJ: Leukocyte and endothelial cell adhesion molecules in a chronic murine model of myocardial reperfusion injury. Am J Physiol Heart Circ 279(5): H2196YH2201, 2000.
41. Entman ML, Michael L, Rossen RD, Dreyer WJ, Anderson DC, Taylor AA, Smith CW: Inflammation in the course of early myocardial ischemia. FASEB J 5(11):2529-2537, 1991.
42. Jang HR, Rabb H: The innate immune response in ischemic acute kidney injury. Clin Immunol 130(1):41-50, 2009.
43. Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, Linden J, Okusa MD: Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury. Kidney Int 75(7):689-698, 2009.
44. Bajwa, A. ; Kinsey, G. R. ; Okusa MD: Immune mechanisms and novel pharmacological therapies of acute kidney injury. Curr Drug Targets 10(12): 1196-1204, 2009.
45. Jang HR, Ko GJ, Wasowska BA, Rabb H: The interaction between ischemiareperfusion and immune responses in the kidney. JMolMed 87(9):859-864, 2009.
46. Lauriat S, Linas SL: The role of neutrophils in acute renal failure. Semin Nephrol 18(5):498-504, 1998.
47. Arumugam T V, Shiels IA, Woodruff TM, Granger DN, Taylor SM: The role of the complement system in ischemia-reperfusion injury. Shock 21(5):401-409, 2004.
48. Den Hengst WA, Gielis JF, Lin JY, Van Schil PE, De Windt LJ, Moens AL: Lung ischemia-reperfusion injury: a Mol and clinical view on a complex pathophysiological process. Am J Physiol Heart Circ 299(5):H1283YH1299, 2010.
49. Schmeling DJ, Caty MG, Oldham KT, Guice KS, Hinshaw DB: Evidence for neutrophil-related acute lung injury after intestinal ischemia-reperfusion. Surgery 106(2):195-202, 1989.
50. Eppinger M, Jones M, DeebM, Bolling S, Ward P: Pattern of injury and the role of neutrophils in reperfusion injury of rat lung. J Surg Res 58:713-718, 1995.
51. Seekamp A, Mulligan MS, Till GO, Ward PA: Requirements for neutrophil products and L-arginine in ischemia-reperfusion injury. Am J Pathol 142(4): 1217-1226, 1993.
52. Vlahopoulos S, Boldogh I, Casola A and Brasier AR: Nuclear factor-kappaBdependent induction of interleukin-8 gene expression by tumor necrosis factor alpha: evidence for an antioxidant sensitive activating pathway distinct from nuclear translocation. Blood 94:1878-1889, 1999.
53. Jaeschke H, Farhood A, Smith CW: Neutrophil-induced liver cell injury in endotoxin shock is a CD11b/CD18Ydependent mechanism neutrophil-induced liver cell injury in endotoxin is a CD11b/CDWYdependent mechanism shock. Am J Physiol Gastrointest Liver Physiol 261:G1051YG1056, 1991.
54. Kubes P, Mehal WZ: Sterile inflammation in the liver. Gastroenterology 143(5): 1158-1172, 2012.
55. Jaeschke H, Woolbright BL: Current strategies to minimize hepatic ischemiaYreperfusion injury by targeting reactive oxygen species. Transplant Rev 26(2): 103-114, 2012.
56. Gujral JS, Farhood A, Bajt ML, Jaeschke H: Neutrophils aggravate acute liver injury during obstructive cholestasis in bile ductYligated mice. Hepatology 38(2): 355-363, 2003.
57. Gujral JS, Liu J, Farhood A, Hinson JA, Jaeschke H: Functional importance of ICAM-1 in the mechanism of neutrophil-induced liver injury in bile ductY ligated mice. Am J Physiol Gastrointest Liver Physiol 286(3):G499YG507, 2004.
58. Simpson R, Alon R, Kobzik L, Valeri CR, Shepro D, Hechtman HB: Neutrophil and nonneutrophilYmediated injury in intestinal ischemia reperfusion. Ann Surg 218(4):444-453, 1993.
59. Langdale LA, Flaherty LC, Liggit DH, Harlan JM, Rice CL, Winn RK: Neutrophils contribute to hepatic ischemia reperfusion injury by a CD18-independent. J Leukoc Biol 53:511-517, 1993.
60. Stallion A, Kou TD, Latifi SQ, Miller KA, Dahms BB, Dudgeon DL, Levine AD: Ischemia/reperfusion: a clinically relevant model of intestinal injury yielding systemic inflammation. J Pediatr Surg 40(3):470-477, 2005.
61. Panes J, Kurose I, Rodriguez-Vaca MD, Anderson DC, Miyasaka M, Tso P: Diabetes exacerbates inflammatory responses to ischemia-reperfusion. Circulation 93(1):161-167, 1996.
62. Shigematsu T, Wolf RE, Granger DN: T-lymphocytes modulate the microvascular and inflammatory responses to intestinal ischemia-reperfusion. Microcirculation 9(2):99-109, 2002.
63. Yu LC-H: Protective mechanism against gut barrier dysfunction in mesenteric ischemia/reperfusion clinical aspects of intestinal I/R. Adapt Med 2(1): 11-22, 2010.
64. Kaneko H, Tamura A, Ishii T, Maeda T, Katagiri T, Ishii J, Kubota Y, Suzuki T, Tsuchiya M, Otsuka Y, et al. : Bacterial translocation in small intestinal ischemia-reperfusion injury and efficacy of anti-CINC antibody treatment. Eur Surg Res 39(3):153-159, 2007.
65. Tsuruma T, Yagihashi A, Tarumi K, Hirata K: AntiYrat IL-8 (CINC) monoclonal antibody administration reduces ischemia-reperfusion injury in small intestine. Transplant Proc 30(6):2644-2645, 1998.
66. Yagihashi A, Tsuruma T, Tarumi K, Kameshima T, Yajima T, Yanai Y, Watanabe N, Hirata K: Prevention of small intestinal ischemia-reperfusion injury in rat by antiYcytokine-induced neutrophil chemoattractant monoclonal antibody. J Surg Res 78(2):92-96, 1998.
67. Usatyuk P V, Natarajan V: Regulation of reactive oxygen species-induced endothelial cell-cell and cell-matrix contacts by focal adhesion kinase and adherens junction proteins. Am J Physiol-Lung C 289(6):L999YL1010, 2005.
68. Arumugam TV, Shiels IA, Woodruff TM, Reid RC, Fairlie DP, Taylor SM: Protective effect of a new C5a receptor antagonist against ischemia-reperfusion injury in the rat small intestine. J Surg Res 103(2):260-267, 2002.
69. Arslan F, de Kleijn DPV, Timmers L, Doevendans PA, Pasterkamp G: Bridging innate immunity and myocardial ischemia/reperfusion injury: the search for therapeutic targets. Curr Pharm Design 14(12):1205-1216, 2008.
70. Xu D, Zaets SB, Chen R, Lu Q, Rajan H, Yang X: Elimination of C5aR prevents intestinal mucosal damage and attenuates neutrophil infiltration in local and remote organs. Shock 31(5):493-499, 2009.
71. Ortolano GA, Capetandes A, Wenz B: A review of leukofiltration therapy for decreasing the morbidity associated with cardiopulmonary bypass and acute inflammatory bowel disease. Ther Apher 6(2):119-129, 2002.
72. Collard C, Gelman S: PathoPhysiolology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology 94(6):1133-1138, 2001.
73. Mumy KL, McCormick BA: The role of neutrophils in the event of intestinal inflammation. Curr Opin Pharmacol 9(6):697-701, 2009.
74. Kucharzik T, Hudson JT, Lügering A, Abbas JA, Bettini M, Lake JG, Evans ME, Ziegler TR, Merlin D, Madara JL, et al. : Acute induction of human IL-8 production by intestinal epithelium triggers neutrophil infiltration without mucosal injury. Gut 54(11):1565-1572, 2005.
75. Hansen PR: Role of neutrophils in myocardial ischemia and reperfusion. Circulation 91(6):1872-1885, 1995.
76. Angus DC, Barnato AE, Linde-Zwirble WT, Weissfeld LA, Watson RS, Rickert T, Rubenfeld GD: Use of intensive care at the end of life in the United States: an epidemiologic study. Crit Care Med 32(3):638-643, 2004.
77. WoodfinA, VoisinM, BeyrauM, Colom B, Caille D, Diapouli F, Diapouli F-M, Nash GB, Chavakis T, Albelda SM, et al. : Junctional adhesion molecule-C (JAM-C) regulates polarized neutrophil transendothelial cell migration in vivo. Nat Immunol 12(8): 761-769, 2012.
78. Goldsmith JR, Perez-Chanona E, Yadav PN, Whistler J, Roth B, Jobin C: Intestinal epithelial cellYderived 2-opioid signaling protects against ischemia reperfusion injury through PI3K Signaling. Am J Pathol 1-11, 2013.
79. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, Hussain P, Vecoli C, Paolocci N, Ambs S, et al. : The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 45(1):18-31, 2008.
80. Sonoda A, Nitta N, Seko A, Ohta S, Takemura S, Miyagawa Y, Takahashi M, Murata M: Edaravone prevents bowel infarction after acute superior mesenteric artery thromboembolism using autologous fibrin clots in a rabbit model. Br J Radiol 82(981):711-715, 2009.
81. Mallick IH, Yang W, Winslet MC, Seifalian AM: Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 49(9): 1359-1377, 2004.
82. Suzuki T: Additional lung-protective perfusion techniques during cardiopulmonary bypass. Ann Thorac Surg 16(3):150-155, 2010.
83. Tsujita K, Shimomura H, Kawano H, Hokamaki J, Fukuda M, Yamashita T, Hida S, Nakamura Y, Nagayoshi Y, Sakamoto M, et al. : Effects of edaravone on reperfusion injury in patients with acute myocardial infarction. Am J Cardiol 94(4):481-484, 2004.
84. Zanardo RCO, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL: Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20(12):2118-2120, 2006.
85. Tajra LC, Martin X, Margonari J, Blanc-Brunat N, Ishibashi M, Vivier G, Panaye G, Steghens JP, Kawashima H, Miyasaka M, Treille-Ritouet D, Dubernard JM, Revillard JP. In vivo effects of monoclonal antibodies against rat beta(2) integrins on kidney ischemia-reperfusion injury. J Surg Res 87(1):32-38, 1999.
86. Gardinali M, Borrelli E, Chiara O, Lundberg C, Padalino P, Conciato L, Cafaro C, Lazzi S, Luzi P, Giomarelli PP, et al. : Inhibition of CD11-CD18 complex prevents acute lung injury and reduces mortality after peritonitis in rabbits. Am J Respir Crit Care 161(3 Pt 1):1022-1029, 2000.
87. Zhang ZG, Chopp M, Tang WX, Jiang N, Zhang RL: Postischemic treatment (2-4 h) with anti-CD11b and anti-CD18 monoclonal antibodies are neuroprotective after transient (2 h) focal cerebral ischemia in the rat. Brain Res 698(1-2):79-85, 1995.
88. Faxon DP, Gibbons RJ, Chronos N a F, Gurbel PA, Sheehan F: The effect of blockade of the CD11/CD18 integrin receptor on infarct size in patients with acute myocardial infarction treated with direct angioplasty: the results of the HALT-MI study. J Am Coll Cardiol 40(7):1199-1204, 2002.
89. Rusnak JM, Kopecky SL, Clements IP, Gibbons RJ, Holland AE, Peterman HS, Martin JS, Saoud JB, Feldman RL, Breisblatt WM, et al. : Antibody in patients with acute percutaneous transluminal coronary angioplasty (the FESTIVAL study). Am J Cardiol 88:482-487, 2001.
90. Heilker R, Wolff M, Tautermann CS, Bieler M: G-proteinYcoupled receptorfocused drug discovery using a target class platform approach. Drug Discov Today 14(5-6):231-240, 2009.
91. Ulven T: Short-chain free fatty acid receptors FFA2/GPR43 and FFA3/GPR41 as new potential therapeutic targets. Front Endocrinol 3:111, 2012.
92. Baba AA, Srinivas M, Shariff A, Nazir T: Role of short chain fatty acids in mesenteric ischemia reperfusion injury in rats. Eur J Paediatr Surg 20:98-101, 2010.
93. Lasley RD, Jahania MS, Mentzer RM: Beneficial effects of adenosine A2a agonist CGS-21680 in infarcted and stunned porcine myocardium. Am J Physiol Heart Circ 280:H1660YH1666, 2001.
94. Okusa MD, Linden J, Huang L, Rieger JM, Macdonald TL, Huynh LP: A2A adenosine receptor-mediated inhibition of renal injury and neutrophil adhesion. Am J Physiol-Renal 279:F809YF818, 2000.
95. Fleming SD, Mastellos D, Karpel-Massler G, Shea-Donohue T, Lambris JD, Tsokos GC: C5a causes limited, polymorphonuclear cell-independent, mesenteric ischemia/reperfusionYinduced injury. Clin Immunol 108(3):263-273, 2003.
96. Stahl GL, Xu Y, Hao L, Miller M, Buras JA, Fung M, Zhao H: Role for the alternative complement pathway in ischemia/reperfusion injury. Am J Pathol 162(2):449-455, 2003.
97. Arumugam T V, Shiels IA, Strachan AJ, Abbenante G, Fairlie DP, Taylor SM: A small molecule C5a receptor antagonist protects kidneys from ischemia/ reperfusion injury in rats. Kidney Int 63(1):134-142, 2003.
98. Arumugam T V, Woodruff TM, Stocks SZ, Proctor LM, Pollitt S, Shiels IA, Reid RC, Fairlie DP, Taylor SM: Protective effect of a human C5a receptor antagonist against hepatic ischaemia-reperfusion injury in rats. J Hepatol 40(6): 934-941, 2004.
99. Woodruff TM, Arumugam T V, Shiels IA, Reid RC, Fairlie DP, Taylor SM: Protective effects of a potent C5a receptor antagonist on experimental acute limb ischemia-reperfusion in rats. J Surg Res 116(1):81-90, 2004.
100. Pavlovski D, Thundyil J, Monk PN, Wetsel RA, Taylor SM, Woodruff TM: Generation of complement component C5a by ischemic neurons promotes neuronal apoptosis. FASEB J 26(9):3680-3690, 2012.
101. Wagner E, Frank MM: Therapeutic potential of complement modulation. Nat Rev Drug Discov 9(1):43-56, 2010.
102. Woodruff TM, Nandakumar KS, Tedesco F: Inhibiting the C5-C5a receptor axis. Mol Immunol 48(14):1631-1642, 2011.
103. Martel C, Granger CB, Ghitescu M, Stebbins A, Fortier A, Armstrong PW, Bonnefoy A, Theroux P: Pexelizumab fails to inhibit assembly of the terminal complement complex in patients with ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention. Insight from a substudy of the Assessment of Pexelizumab in Acute Myocardia. Am Heart J 164(1):43-51, 2012.
104. Arumugam T V, Magnus T, Woodruff TM, Proctor LM, Shiels IA, Taylor SM: Complement mediators in ischemia-reperfusion injury. Clin Chim Acta 374(1-2):33-45, 2006.
105. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker H V, Xu W, Richards DR, McDonald-Smith GP, Gao H, Hennessy L, et al. : Genomic responses in mouse models poorly mimic human inflammatory diseases. PNAS 1-6, 2013.
106. Woodcock J, Woosley R: The FDA critical path initiative and its influence on new drug development. Annu Rev Med 59:1-12, 2008.
107. Hayday AC, Peakman M: The habitual, diverse and surmountable obstacles to human immunology research. Nat Immunol 9(6):575-580, 2008.