The complement system in ischemia-reperfusion injuries

Immunobiology

Volumn 217, Issue 11, 2012, Pages 1026-1033

  Gorsuch, William B ^a   Chrysanthou, Elvina ^b   Schwaeble, Wilhelm J ^b   Stahl, Gregory L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Gastrointestinal; Inflammation; Inhibitor; Lectin; Myocardial

Indexed keywords

CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C1S INHIBITOR; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C4D; COMPLEMENT RECEPTOR; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; LECTIN; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE 2; MANNOSE BINDING LECTIN; PEXELIZUMAB; PLACEBO; TP 10; UNCLASSIFIED DRUG;

ACUTE HEART INFARCTION; CARDIOPULMONARY BYPASS; COMPLEMENT ACTIVATION; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT DEPOSITION; COMPLEMENT LECTIN PATHWAY; COMPLEMENT SYSTEM; CORONARY ARTERY BYPASS SURGERY; GENOMICS; HEART MUSCLE ISCHEMIA; HUMAN; HYPERGLYCEMIA; INTESTINE ISCHEMIA; ISCHEMIA; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; LEUKOCYTE ACTIVATION; NEUTROPHIL CHEMOTAXIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW;

EID: 84866006658     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.07.024     Document Type: Review

References (117)

1. Amsterdam E.A., Stahl G.L., Pan H.-L., Rendig S.V., Fletcher M.P., Longhurst J.C. Limitation of reperfusion injury by a monoclonal antibody to C5a during myocardial infarction in pigs. Am. J. Physiol. Heart Circ. Physiol. 1995, 268:H448-H457.
2. Armstrong P.W., Mahaffey K.W., Chang W.C., Weaver W.D., Hochman J.S., Theroux P., Rollins S., Todaro T.G., Granger C.B. COMMA investigators concerning the mechanism of pexelizumab's benefit in acute myocardial infarction. Am. Heart J. 2006, 151:787-790.
3. Arnold J.N., Wormald M.R., Suter D.M., Radcliffe C.M., Harvey D.J., Dwek R.A., Rudd P.M., Sim R.B. Human serum IgM glycosylation: identification of glycoforms that can bind to mannan-binding lectin. J. Biol. Chem. 2005, 280:29080-29087.
4. Arumugam T.V., Shiels I.A., Woodruff T.M., Granger D.N., Taylor S.M. The role of the complement system in ischemia-reperfusion injury. Shock 2004, 21:401-409.
5. Bauernschmitt R., Bohrer H., Hagl S. Rescue therapy with C1-esterase inhibitor concentrate after emergency coronary surgery for failed PTCA. Intensive Care Med. 1998, 24:635-638.
6. Botto M., Kirschfink M., Macor P., Pickering M.C., Wurzner R., Tedesco F. Complement in human diseases: lessons from complement deficiencies. Mol. Immunol. 2009, 46:2774-2783.
7. Brock R.W., Nie R.G., Harris K.A., Potter R.F. Kupffer cell-initiated remote hepatic injury following bilateral hindlimb ischemia is complement dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280:G279-G284.
8. Buerke M., Murohara T., Lefer A.M. Cardioprotective effects of a C1 esterase inhibitor in myocardial ischemia and reperfusion. Circulation 1995, 91:393-402.
9. Burke S.E., Wright C.D., Potoczak R.E., Boucher D.M., Dodd G.D., Taylor D.G., Kaplan H.R. Reduction of canine myocardial infarct size by CI-959, an inhibitor of inflammatory cell activation. J. Cardiovasc. Pharmacol. 1992, 20:619-629.
10. Busche M.N., Pavlov V., Takahashi K., Stahl G.L. Myocardial ischemia and reperfusion injury is dependent on both IgM and mannose-binding lectin. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H1853-H1859.
11. Busche M.N., Stahl G.L. Role of the complement components C5 and C3a in a mouse model of myocardial ischemia and reperfusion injury. Ger. Med. Sci. 2010, 8.
12. Busche M.N., Walsh M.C., McMullen M.E., Guikema B.J., Stahl G.L. Mannose-binding lectin plays a critical role in myocardial ischaemia and reperfusion injury in a mouse model of diabetes. Diabetologia 2008, 51:1544-1551.
13. Cedzynski M., Madalinski K., Gregorek H., Swierzko A.S., Nowicka E., Obtulowicz K., Dzierzanowska-Fangrat K., Wojda U., Rabczenko D., Kawakami M. Possible disease-modifying factors: the mannan-binding lectin pathway and infections in hereditary angioedema of children and adults. Arch. Immunol. Ther. Exp. (Warsz.) 2008, 56:69-75.
14. Cervera A., Planas A.M., Justicia C., Urra X., Jensenius J.C., Torres F., Lozano F., Chamorro A. Genetically-defined deficiency of mannose-binding lectin is associated with protection after experimental stroke in mice and outcome in human stroke. PLoS ONE 2010, 5:e8433.
15. Chan R.K., Ibrahim S.I., Takahashi K., Kwon E., McCormack M., Ezekowitz A., Carroll M.C., Moore F.D., Austen W.G. The differing roles of the classical and mannose-binding lectin complement pathways in the events following skeletal muscle ischemia-reperfusion. J. Immunol. 2006, 177:8080-8085.
16. Collard C.D., Lekowski R., Jordan J.E., Agah A., Stahl G.L. Complement activation following oxidative stress. Mol. Immunol. 1999, 36:941-948.
17. Collard C.D., Montalto M.C., Reenstra W.R., Buras J.A., Stahl G.L. Endothelial oxidative stress activates the lectin complement pathway: role of cytokeratin 1. Am. J. Pathol. 2001, 159:1045-1054.
18. Collard C.D., Vakeva A., Bukusoglu C., Zund G., Sperati C.J., Colgan S.P., Stahl G.L. Reoxygenation of hypoxic human umbilical vein endothelial cells (HUVECs) activates the classic complement pathway. Circulation 1997, 96:326-333.
19. Collard C.D., Vakeva A., Morrissey M.A., Agah A., Rollins S.A., Reenstra W.R., Buras J.A., Meri S., Stahl G.L. Complement activation following oxidative stress: role of the lectin complement pathway. Am. J. Pathol. 2000, 156:1549-1556.
20. Collins C., Tsui F.W., Shulman M.J. Differential activation of human and guinea pig complement by pentameric and hexameric IgM. Eur. J. Immunol. 2002, 32:1802-1810.
21. Davis A.E. Biological effects of C1 inhibitor. Drug News Perspect. 2004, 17:439-446.
22. Degn S.E., Hansen A.G., Steffensen R., Jacobsen C., Jensenius J.C., Thiel S. MAp44, a human protein associated with pattern recognition molecules of the complement system and regulating the lectin pathway of complement activation. J. Immunol. 2009, 183:7371-7378.
23. Degn S.E., Jensenius J.C., Thiel S. Disease-causing mutations in genes of the complement system. Am. J. Hum. Genet. 2011, 88:689-705.
24. Eror A.T., Stojadinovic A., Starnes B.W., Makrides S.C., Tsokos G.C., Shea-Donohue T. Antiinflammatory effects of soluble complement receptor type 1 promote rapid recovery of ischemia/reperfusion injury in rat small intestine. Clin. Immunol. 1999, 90:266-275.
25. Farrar C.A., Asgari E., Lynch N.J., Roschen S., Stover C.M., Schwaeble W.J. Mannan binding lectin associated serine protease-2 (MASP-2) is a critical player in the pathophysiology of renal ischaemia reperfusion (I/R) injury and mediates tissue injury in absence of complement C4. Mol. Immunol. 2009, 46:2832.
26. Fattouch K., Bianco G., Speziale G., Sampognaro R., Lavalle C., Guccione F., Dioguardi P., Ruvolo G. Beneficial effects of C1 esterase inhibitor in ST-elevation myocardial infarction in patients who underwent surgical reperfusion: a randomised double-blind study. Eur. J. Cardiothorac. Surg. 2007, 32:326-332.
27. Fleming S.D., Shea-Donohue T., Guthridge J.M., Kulik L., Waldschmidt T.J., Gipson M.G., Tsokos G.C., Holers V.M. Mice deficient in complement receptors 1 and 2 lack a tissue injury-inducing subset of the natural antibody repertoire. J. Immunol. 2002, 169:2126-2133.
28. Fortpied J., Vertommen D., Van S.E. Binding of mannose-binding lectin to fructosamines: a potential link between hyperglycaemia and complement activation in diabetes. Diabetes Metab. Res. Rev. 2010, 26:254-260.
29. Fruchterman T.M., Spain D.A., Wilson M.A., Harris P.D., Garrison R.N. Complement inhibition prevents gut ischemia and endothelial cell dysfunction after hemorrhage/resuscitation. Surgery 1998, 124:782-791.
30. Fujita T. Evolution of the lectin-complement pathway and its role in innate immunity. Nat. Rev. Immunol. 2002, 2:346-353.
31. Fujita T., Matsushita M., Endo Y. The lectin-complement pathway-its role in innate immunity and evolution. Immunol. Rev. 2004, 198:185-202.
32. Fujita T., Ohi H., Endo M., Ohsawa I., Kanmatsuse K. Complement activation accelerates glomerular injury in diabetic rats. Nephron 1999, 81:208-214.
33. Gesuete R., Storini C., Fantin A., Stravalaci M., Zanier E.R., Orsini F., Vietsch H., Mannesse M.L., Ziere B., Gobbi M., De Simoni M.G. Recombinant C1 inhibitor in brain ischemic injury. Ann. Neurol. 2009, 66:332-342.
34. Gorsuch W.B., Guikema B.J., Fritzinger D.C., Vogel C.-W., Stahl G.L. Humanized cobra venom factor decreases myocardial ischemia-reperfusion injury. Mol. Immunol. 2009, 47:506-510.
35. Goulet J.L., Snouwaert J.N., Latour A.M., Coffman T.M., Koller B.H. Altered inflammatory responses in leukotriene-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:12852-12856.
36. Granger C.B., Mahaffey K.W., Weaver W.D., Theroux P., Hochman J.S., Filloon T.G., Rollins S., Todaro T.G., Nicolau J.C., Ruzyllo W., Armstrong P.W. Pexelizumab, an anti-C5 complement antibody, as adjunctive therapy to primary percutaneous coronary intervention in acute myocardial infarction: the COMplement inhibition in myocardial infarction treated with Angioplasty (COMMA) trial. Circulation 2003, 108:1184-1190.
37. Hansen T.K., Tarnow L., Thiel S., Steffensen R., Stehouwer C.D., Schalkwijk C.G., Parving H.H., Flyvbjerg A. Association between mannose-binding lectin and vascular complications in type 1 diabetes. Diabetes 2004, 53:1570-1576.
38. Hansen T.K., Thiel S., Knudsen S.T., Gravholt C.H., Christiansen J.S., Mogensen C.E., Poulsen P.L. Elevated levels of mannan-binding lectin in patients with type 1 diabetes. J. Clin. Endocrinol. Metab. 2003, 88:4857-4861.
39. Hart M.L., Ceonzo K.A., Shaffer L.A., Takahashi K., Rother R.P., Reenstra W.R., Buras J.A., Stahl G.L. Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J. Immunol. 2005, 174:6373-6380.
40. Hill J., Lindsay T.F., Ortiz F., Yeh C.G., Hechtman H.B., Moore F.D. Soluble complement receptor type 1 ameliorates the local and remote organ injury after intestinal ischemia-reperfusion in the rat. J. Immunol. 1992, 149:1723-1728.
41. Hill J.H., Ward P.A. The phlogistic role of C3 leukotactic fragments in myocardial infarcts in rats. J. Exp. Med. 1971, 133:885-900.
42. Horstick G., Berg O., Heimann A., Gotze O., Loos M., Hafner G., Bierbach B., Petersen S., Bhakdi S., Darius H., Horstick M., Meyer J., Kempski O. Application of C1-esterase inhibitor during reperfusion of ischemic myocardium: dose-related beneficial versus detrimental effects. Circulation 2001, 104:3125-3131.
43. Horstick G., Heimann A., Gotze O., Hafner G., Berg O., Boehmer P., Becker P., Darius H., Rupprecht H.-J., Loos M., Bhakdi S., Meyer J., Kempski O. Intracoronary application of C1 esterase inhibitor improves cardiac function and reduces myocardial necrosis in an experimental model of ischemia and reperfusion. Circulation 1997, 95:701-708.
44. Horstick G., Kempf T., Lauterbach M., Bhakdi S., Kopacz L., Heimann A., Malzahn M., Horstick M., Meyer J., Kempski O. C1-esterase-inhibitor treatment at early reperfusion of hemorrhagic shock reduces mesentry leukocyte adhesion and rolling. Microcirculation 2001, 8:427-433.
45. Hovind P., Hansen T.K., Tarnow L., Thiel S., Steffensen R., Flyvbjerg A., Parving H.H. Mannose-binding lectin as a predictor of microalbuminuria in type 1 diabetes: an inception cohort study. Diabetes 2005, 54:1523-1527.
46. Hughey C.T., Brewer J.W., Colosia A.D., Rosse W.F., Corley R.B. Production of IgM hexamers by normal and autoimmune B cells: implications for the physiologic role of hexameric IgM. J. Immunol. 1998, 161:4091-4097.
47. Jordan J.E., Montalto M.C., Stahl G.L. Inhibition of mannose-binding lectin reduces postischemic myocardial reperfusion injury. Circulation 2001, 104:1413-1418.
48. Karpel-Massler G., Fleming S.D., Kirschfink M., Tsokos G.C. Human C1 esterase inhibitor attenuates murine mesenteric ischemia/reperfusion induced local organ injury. J. Surg. Res. 2003, 115:247-256.
49. Krijnen P.A., Ciurana C., Cramer T., Hazes T., Meijer C.J., Visser C.A., Niessen H.W., Hack C.E. IgM colocalises with complement and C reactive protein in infarcted human myocardium. J. Clin. Pathol. 2005, 58:382-388.
50. Kyriakides C., Austen W., Wang Y., Favuzza J., Kobzik L., Moore F.D., Hechtman H.B. Skeletal muscle reperfusion injury is mediated by neutrophils and the complement membrane attack complex. Am. J. Physiol. 1999, 277:C1263-C1268.
51. Kyriakides C., Wang Y., Austen W.G., Favuzza J., Kobzik L., Moore F.D., Hechtman H.B. Moderation of skeletal muscle reperfusion injury by a sLe(x)-glycosylated complement inhibitory protein. Am. J. Physiol. Cell Physiol. 2001, 281:C224-C230.
52. La Bonte L.R., Davis-Gorman G., Stahl G.L., McDonagh P.F. Complement inhibition reduces injury in the type 2 diabetic heart following ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H1282-H1290.
53. La Bonte L.R., Dokken B., Davis-Gorman G., Stahl G.L., McDonagh P.F. The mannose-binding lectin pathway is a significant contributor to reperfusion injury in the type 2 diabetic heart. Diab. Vasc. Dis. Res. 2009, 6:172-180.
54. Lazar H.L., Bokesch P.M., van L.F., Fitzgerald C., Emmett C., Marsh H.C., Ryan U. Soluble human complement receptor 1 limits ischemic damage in cardiac surgery patients at high risk requiring cardiopulmonary bypass. Circulation 2004, 110:II274-II279.
55. Lefer A.M., Weyrich A.S., Buerke M. Role of selectins, a new family of adhesion molecules, in ischaemia-reperfusion injury. Cardiovasc. Res. 1994, 28:289-294.
56. Lehr H.-A., Olofsson A.M., Carew T.E., Vajkoczy P., Von Andrian U.H., Hübner C., Berndt M.C., Steinberg D., Messmer K., Arfors K.E. P-selectin mediates the interaction of circulating leukocytes with platelets and microvascular endothelium in response to oxidized lipoprotein in vivo. Lab. Invest. 1994, 71:380-386.
57. Lekowski R., Collard C.D., Reenstra W.R., Stahl G.L. Ulex europaeus agglutinin II (UEA-II) is a novel, potent inhibitor of complement activation. Protein Sci. 2001, 10:277-284.
58. Li J.S., Sanders S.P., Perry A.E., Stinnett S.S., Jaggers J., Bokesch P., Reynolds L., Nassar R., Anderson P.A. Pharmacokinetics and safety of TP10, soluble complement receptor 1, in infants undergoing cardiopulmonary bypass. Am. Heart J. 2004, 147:173-180.
59. Liangos O., Domhan S., Schwager C., Zeier M., Huber P.E., Addabbo F., Goligorsky M.S., Hlatky L., Jaber B.L., Abdollahi A. Whole blood transcriptomics in cardiac surgery identifies a gene regulatory network connecting ischemia reperfusion with systemic inflammation. PLoS ONE 2010, 5:e13658.
60. Lin T., Zhou W., Farrar C.A., Hargreaves R.E., Sheerin N.S., Sacks S.H. Deficiency of C4 from donor or recipient mouse fails to prevent renal allograft rejection. Am. J. Pathol. 2006, 168:1241-1248.
61. MacLean D., Fishbein M.C., Braunwald E., Maroko P.R. Long-term preservation of ischemic myocardium after experimental coronary artery occlusion. J. Clin. Invest. 1978, 61:541-551.
62. Maroko P.R., Carpenter C.B., Chiariello M., Fishbein M.C., Radvany P., Knostman J.D., Hale S.L. Reduction by cobra venom factor of myocardial necrosis after coronary artery occlusion. J. Clin. Invest. 1978, 61:661-670.
63. McMullen M.E., Hart M.L., Walsh M.C., Buras J., Takahashi K., Stahl G.L. Mannose-binding lectin binds IgM to activate the lectin complement pathway in vitro and in vivo. Immunobiology 2006, 211:759-766.
64. Montalto M.C., Collard C.D., Buras J.A., Reenstra W.R., McClaine R., Gies D.R., Rother R.P., Stahl G.L. A keratin peptide inhibits mannose-binding lectin. J. Immunol. 2001, 166:4148-4153.
65. Montalto M.C., Hart M.L., Jordan J.E., Wada K., Stahl G.L. Role for complement in mediating intestinal nitric oxide synthase-2 and superoxide dismutase expression. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:G197-G206.
66. Mulligan M.S., Yeh C.G., Rudolph A.R., Ward P.A. Protective effects of soluble CR1 in complement- and neutrophil-mediated tissue injury. J. Immunol. 1992, 148:1479-1485.
67. Murata K., Fox-Talbot K., Qian Z., Takahashi K., Stahl G.L., Baldwin W.M., Wasowska B.A. Synergistic deposition of C4d by complement-activating and nonactivating antibodies in cardiac transplants. Am. J. Transplant. 2007, 7:2605-2614.
68. Nevens J.R., Mallia A.K., Wendt M.W., Smith P.K. Affinity chromatographic purification of immunoglobulin M antibodies utilizing immobilized mannan binding protein. J. Chromatogr. 1992, 597:247-256.
69. Nolte D., Lehr H.-A., Messmer K. Adenosine inhibits postischemic leukocyte-endothelium interaction in postcapillary venules of the hamster. Am. J. Physiol. Heart Circ. Physiol. 1991, 261:H651-H655.
70. Ogawa S., Clauss M., Kuwabara K., Shreeniwas R., Butura C., Koga S., Stern D. Hypoxia induces endothelial cell synthesis of membrane-associated proteins. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:9897-9901.
71. Orsini, F., Villa, P., Parrella, S., Zangari, R., Zanier, E.R., Gesuete, R., Stravalaci, M., Fumagalli, S., Ottria, R., Reina, J.J., Paladini, A., Micotti, E., Ribeiro-Viana, R., Rojo, J., Pavlov, V.I., Stahl, G.L., Bernardi, A., Gobbi, M., De Simoni, M.-G., 2012. Targeting mannose binding lectin confers long lasting protection with a surprisingly wide therapeutic window in cerebral ischemia. Circulation, in press.
72. Pavlov V.I., La Bonte L.R., Baldwin W.M., Markiewski M., Lambris J., Stahl G.L. Absence of mannose-binding lectin prevents hyperglycemic cardiovascular complications. Am. J. Pathol. 2012, 180:104-112.
73. Peng T., Hao L., Madri J.A., Su X., Elias J.A., Stahl G.L., Squinto S., Wang Y. Role of C5 in the development of airway inflammation, airway hyperresponsiveness, and ongoing airway response. J. Clin. Invest. 2005, 115:1590-1600.
74. Pinckard R.N., O'Rourke R.A., Crawford M.H., Grover F.S., McManus L.M., Ghidoni J.J., Storrs S.B., Olson M.S. Complement localization and mediation of ischemic injury in baboon myocardium. J. Clin. Invest. 1980, 66:1050-1056.
75. Prasad M.R., Popescu L.M., Moraru I.I., Liu X.K., Maity S., Engelman R.M., Das D.K. Role of phospholipases A2 and C in myocardial ischemic reperfusion injury. Am. J. Physiol. 1991, 260:H877-H883.
76. Pratt J.R., Hibbs M.J., Laver A.J., Smith R.A., Sacks S.H. Effects of complement inhibition with soluble complement receptor-1 on vascular injury and inflammation during renal allograft rejection in the rat. Am. J. Pathol. 1996, 149:2055-2066.
77. Renner B., Strassheim D., Amura C.R., Kulik L., Ljubanovic D., Glogowska M.J., Takahashi K., Carroll M.C., Holers V.M., Thurman J.M. B cell subsets contribute to renal injury and renal protection after ischemia/reperfusion. J. Immunol. 2010, 185:4393-4400.
78. Ricklin D., Lambris J.D. Complement-targeted therapeutics. Nat. Biotechnol. 2007, 25:1265-1275.
79. Riedemann N.C., Ward P.A. Complement in ischemia reperfusion injury. Am. J. Pathol. 2003, 162:363-367.
80. Rioux P. TP-10 (AVANT Immunotherapeutics). Curr. Opin. Investig. Drugs 2001, 2:364-371.
81. Rossi V., Cseh S., Bally I., Thielens N.M., Jensenius J.C., Arlaud G.J. Substrate specificities of recombinant mannan-binding lectin-associated serine proteases-1 and-2. J. Biol. Chem. 2001, 276:40880-40887.
82. Rossi V., Teillet F., Thielens N.M., Bally I., Arlaud G.J. Functional characterization of complement proteases C1s/mannan-binding lectin-associated serine protease-2 (MASP-2) chimeras reveals the higher C4 recognition efficacy of the MASP-2 complement control protein modules. J. Biol. Chem. 2005, 280:41811-41818.
83. Schwaeble W.J., Lynch N.J., Clark J.E., Marber M., Samani N.J., Ali Y.M., Dudler T., Parent B., Lhotta K., Wallis R., Farrar C.A., Sacks S., Lee H., Zhang M., Iwaki D., Takahashi M., Fujita T., Tedford C.E., Stover C.M. Targeting of mannan-binding lectin-associated serine protease-2 confers protection from myocardial and gastrointestinal ischemia/reperfusion injury. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7523-7528.
84. Shernan S.K., Fitch J.C., Nussmeier N.A., Chen J.C., Rollins S.A., Mojcik C.F., Malloy K.J., Todaro T.G., Filloon T., Boyce S.W., Gangahar D.M., Goldberg M., Saidman L.J., Mangano D.T. Impact of pexelizumab, an anti-C5 complement antibody, on total mortality and adverse cardiovascular outcomes in cardiac surgical patients undergoing cardiopulmonary bypass. Ann. Thorac. Surg. 2004, 77:942-949.
85. Skjoedt M.O., Hummelshoj T., Palarasah Y., Honore C., Koch C., Skjodt K., Garred P. A novel MBL/ficolin associated protein is highly expressed in heart and skeletal muscle tissues and inhibits complement activation. J. Biol. Chem. 2010, 285:8234-8243.
86. Skjoedt, M.-O., Pavlov, V.I., Tan, Y.S., Rosbjerg, A., Garred, P., Stahl, G.L., 2012. Endogenous and natural complement inhibitor attenuates myocardial injury and arterial thrombogenesis. Immunobiology, in press.
87. Smith P.K., Shernan S.K., Chen J.C., Carrier M., Verrier E.D., Adams P.X., Todaro T.G., Muhlbaier L.H., Levy J.H. Effects of C5 complement inhibitor pexelizumab on outcome in high-risk coronary artery bypass grafting: combined results from the PRIMO-CABG I and II trials. J. Thorac. Cardiovasc. Surg. 2011, 142:89-98.
88. Spain D.A., Fruchterman T.M., Matheson P.J., Wilson M.A., Martin A.W., Garrison R.N. Complement activation mediates intestinal injury after resuscitation from hemorrhagic shock. J. Trauma 1999, 46:224-233.
89. Stahl G.L., Xu Y., Hao L., Miller M., Buras J.A., Fung M., Zhao H. Role for the alternative complement pathway in ischemia/reperfusion injury. Am. J. Pathol. 2003, 162:449-455.
90. Stotland M.A., Kerrigan C.L. E- and L-selectin adhesion molecules in musculocutaneous flap reperfusion injury. Plast. Reconstr. Surg. 1997, 99:2010-2020.
91. Theroux P., Armstrong P.W., Mahaffey K.W., Hochman J.S., Rollins S.A., Malloy K.J., Parish T., Nicolau J.C., Lavoie J., Granger C.B. Markers of inflammation predict mortality and are reduced by pexelizumab in patients with acute myocardial infarction: insights from the Complement Inhibition in Myocardial Infarction Treated with Angioplasty (COMMA) trial. J. Am. Coll. Cardiol. 2004, 43:287A.
92. Thurman J.M., Ljubanovic D., Edelstein C.L., Gilkeson G.S., Holers V.M. Lack of a functional alternative complement pathway ameliorates ischemic acute renal failure in mice. J. Immunol. 2003, 170:1517-1523.
93. Thurman J.M., Royer P.A., Ljubanovic D., Dursun B., Lenderink A.M., Edelstein C.L., Holers V.M. Treatment with an inhibitory monoclonal antibody to mouse factor B protects mice from induction of apoptosis and renal ischemia/reperfusion injury. J. Am. Soc. Nephrol. 2006, 17:707-715.
94. Tofukuji M., Metais C., Collard C.D., Morse D.S., Stahl G.L., Nelson D.P., Li J., Simons M., Sellke F.W. Effect of sialyl Lewis(x) oligosaccharide on myocardial and cerebral injury in the pig. Ann. Thorac. Surg. 1999, 67:112-119.
95. Tofukuji M., Stahl G.L., Metais C., Tomita M., Agah A., Bianchi C., Fink M.P., Sellke F.W. Mesenteric dysfunction after cardiopulmonary bypass: role of complement C5a. Ann. Thorac. Surg. 2000, 69:799-807.
96. Toomayan G.A., Chen L.E., Jiang H.X., Qi W.N., Seaber A.V., Frank M.M., Urbaniak J.R. C1-esterase inhibitor and a novel peptide inhibitor improve contractile function in reperfused skeletal muscle. Microsurgery 2003, 23:561-567.
97. Vakeva A., Meri S. Complement activation and regulator expression after anoxic injury of human endothelial cells. APMIS 1998, 106:1149-1156.
98. Vakeva A.P., Agah A., Rollins S.A., Matis L.A., Li L., Stahl G.L. Myocardial infarction and apoptosis after myocardial ischemia and reperfusion: role of the terminal complement components and inhibition by anti-C5 therapy. Circulation 1998, 97:2259-2267.
99. van de Pol P., Schlagwein N., Van Gijlswijk-Janssen D.J., Berger S.P., Roos A., Bajema I.M., de Boer H.C., de Fijter J.W., Stahl G.L., Daha M.R., Van Kooten C. A crucial role for mannan-binding lectin in renal ischemia/reperfusion injury. Am. J. Transplant. 2012, 12:877-887.
100. Vogel C.W., Fritzinger D.C. Humanized cobra venom factor: experimental therapeutics for targeted complement activation and complement depletion. Curr. Pharm. Des. 2007, 13:2916-2926.
101. Wada K., Montalto M.C., Stahl G.L. Inhibition of complement C5 reduces local and remote organ injury after intestinal ischemia/reperfusion in the rat. Gastroenterology 2001, 120:126-133.
102. Walport M.J. Complement. First of two parts. N. Engl. J. Med. 2001, 344:1058-1066.
103. Walport M.J. Complement. Second of two parts. N. Engl. J. Med. 2001, 344:1140-1144.
104. Walsh M.C., Bourcier T., Takahashi K., Shi L., Busche M.N., Rother R.P., Solomon S.D., Ezekowitz R.A., Stahl G.L. Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J. Immunol. 2005, 175:541-546.
105. Weiser M.R., Williams J.P., Moore F.D., Kobzik L., Ma M.H., Hechtman H.B., Carroll M.C. Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement. J. Exp. Med. 1996, 183:2343-2348.
106. Weisman H.F., Bartow T., Leppo M.K., Marsh H.C.J., Carson G.R., Concino M.F., Boyle M.P., Roux K.H., Weisfeldt M.L., Fearon D.T. Soluble human complement receptor type 1: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 1990, 249:146-151.
107. Williams J.P., Pechet T.T., Weiser M.R., Reid R., Kobzik L., Moore F.D., Carroll M.C., Hechtman H.B. Intestinal reperfusion injury is mediated by IgM and complement. J. Appl. Physiol. 1999, 86:938-942.
108. Wong N.K., Kojima M., Dobo J., Ambrus G., Sim R.B. Activities of the MBL-associated serine proteases (MASPs) and their regulation by natural inhibitors. Mol. Immunol. 1999, 36:853-861.
109. Woodruff T.M., Nandakumar K.S., Tedesco F. Inhibiting the C5-C5a receptor axis. Mol. Immunol. 2011, 48:1631-1642.
110. Xiao F., Eppihimer M.J., Willis B.H., Carden D.L. Complement-mediated lung injury and neutrophil retention after intestinal ischemia-reperfusion. J. Appl. Physiol. 1997, 82:1459-1465.
111. Zhang M., Hou Y.J., Cavusoglu E., Lee D.C., Steffensen R., Yang L., Bashari D., Villamil J., Moussa M., Fernaine G., Jensenius J.C., Marmur J.D., Ko W., Shevde K. MASP-2 activation is involved in ischemia-related necrotic myocardial injury in humans. Int. J. Cardiol. 2011, [Epub ahead of print].
112. Zhang M., Takahashi K., Alicot E.M., Vorup-Jensen T., Kessler B., Thiel S., Jensenius J.C., Ezekowitz R.A., Moore F.D., Carroll M.C. Activation of the lectin pathway by natural IgM in a model of ischemia/reperfusion injury. J. Immunol. 2006, 177:4727-4734.
113. Zhao H., Montalto M.C., Pfeiffer K.J., Hao L., Stahl G.L. Murine model of gastrointestinal ischemia associated with complement-dependent injury. J. Appl. Physiol. 2002, 93:338-345.
114. Zheng X., Feng B., Chen G., Zhang X., Li M., Sun H., Liu W., Vladau C., Liu R., Jevnikar A.M., Garcia B., Zhong R., Min W.P. Preventing renal ischemia-reperfusion injury using small interfering RNA by targeting complement 3 gene. Am. J. Transplant. 2006, 6:2099-2108.
115. Zheng X., Zhang X., Feng B., Sun H., Suzuki M., Ichim T., Kubo N., Wong A., Min L.R., Budohn M.E., Garcia B., Jevnikar A.M., Min W.P. Gene silencing of complement C5a receptor using siRNA for preventing ischemia/reperfusion injury. Am. J. Pathol. 2008, 173:973-980.
116. Zhou W., Farrar C.A., Abe K., Pratt J.R., Marsh J.E., Wang Y., Stahl G.L., Sacks S.H. Predominant role for C5b-9 in renal ischemia/reperfusion injury. J. Clin. Invest. 2000, 105:1363-1371.
117. Zou C., La Bonte L.R., Pavlov V.I., Stahl G.L. Murine hyperglycemic vasculopathy and cardiomyopathy: whole-genome gene expression analysis predicts cellular targets and regulatory networks influenced by mannose binding lectin. Front. Immunol. 2012, 3. pii: 00015.