Role of complement in the pathomechanism of atherosclerotic vascular diseases

Molecular Immunology

Volumn 46, Issue 14, 2009, Pages 2784-2793

  Széplaki, Gábor ^a,b   Varga, Lilian ^a,b   Füst, George ^a,b   Prohászka, Zoltán ^a,b  

^a SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Atherosclerosis; C5a; C5b 9; Complement; Stroke; Therapy

Indexed keywords

CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C1S INHIBITOR; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT COMPONENT C3C; COMPLEMENT COMPONENT C3D RECEPTOR; COMPLEMENT COMPONENT C4B; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5B; COMPLEMENT COMPONENT C6; COMPLEMENT INHIBITOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; ECULIZUMAB; IMMUNOGLOBULIN; K 76COONA; NAFAMSTAT; NAFAMSTAT MESILATE; PEXELUZIMAB; UNCLASSIFIED DRUG;

ANTIGEN ANTIBODY COMPLEX; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BRAIN INFARCTION; CARDIOVASCULAR RISK; CAROTID ENDARTERECTOMY; CEREBROVASCULAR ACCIDENT; CHLAMYDOPHILA PNEUMONIAE; CLINICAL TRIAL; COMPLEMENT ACTIVATION; COMPLEMENT DEFICIENCY; COMPLEMENT SYSTEM; CORONARY ARTERY BYPASS GRAFT; DRUG EFFICACY; DRUG MECHANISM; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HELICOBACTER PYLORI; HUMAN; HUMORAL IMMUNITY; IMMUNOPATHOGENESIS; INFLAMMATION; NONHUMAN; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW;

ANIMALS; ATHEROSCLEROSIS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; CORONARY RESTENOSIS; DISEASE MODELS, ANIMAL; ENDARTERECTOMY, CAROTID; HUMANS; REPERFUSION INJURY;

EID: 68049127797     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.04.028     Document Type: Review

References (146)

1. Ajjan R., Grant P.J., Futers T.S., Brown J.M., Cymbalista C.M., Boothby M., and Carter A.M. Complement C3 and C-reactive protein levels in patients with stable coronary artery disease. Thromb. Haemost. 94 (2005) 1048-1053
2. Akita N., Nakase H., Kaido T., Kanemoto Y., and Sakaki T. Protective effect of C1 esterase inhibitor on reperfusion injury in the rat middle cerebral artery occlusion model. Neurosurgery 52 (2003) 395-400
3. Ames R.S., Li Y., Sarau H.M., Nuthulaganti P., Foley J.J., Ellis C., Zeng Z., Su K., Jurewicz A.J., Hertzberg R.P., Bergsma D.J., and Kumar C. Molecular cloning and characterization of the human anaphylatoxin C3a receptor. J. Biol. Chem. 271 (1996) 20231-20234
4. Amsterdam E.A., Stahl G.L., Pan H.L., Rendig S.V., Fletcher M.P., and Longhurst J.C. Limitation of reperfusion injury by a monoclonal antibody to C5a during myocardial infarction in pigs. Am. J. Physiol. 268 (1995) H448-H457
5. Arumugam T.V., Shiels I.A., Woodruff T.M., Granger D.N., and Taylor S.M. The role of the complement system in ischemia-reperfusion injury. Shock 21 (2004) 401-409
6. Arumugam T.V., Tang S.C., Lathia J.D., Cheng A., Mughal M.R., Chigurupati S., Magnus T., Chan S.L., Jo D.G., Ouyang X., Fairlie D.P., Granger D.N., Vortmeyer A., Basta M., and Mattson M.P. Intravenous immunoglobulin (IVIG) protects the brain against experimental stroke by preventing complement-mediated neuronal cell death. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 14104-14109
7. Arumugam T.V., Woodruff T.M., Lathia J.D., Selvaraj P.K., Mattson M.P., and Taylor S.M. Neuroprotection in stroke by complement inhibition and immunoglobulin therapy. Neuroscience 158 (2009) 1074-1089
8. Atkinson C., Zhu H., Qiao F., Varela J.C., Yu J., Song H., Kindy M.S., and Tomlinson S. Complement-dependent P-selectin expression and injury following ischemic stroke. J. Immunol. 177 (2006) 7266-7274
9. Barreiro O., de la Fuente H., Mittelbrunn M., and Sanchez-Madrid F. Functional insights on the polarized redistribution of leukocyte integrins and their ligands during leukocyte migration and immune interactions. Immunol. Rev. 218 (2007) 147-164
10. Bergamaschini L., Gobbo G., Gatti S., Caccamo L., Prato P., Maggioni M., Braidotti P., Di Stefano R., and Fassati L.R. Endothelial targeting with C1-inhibitor reduces complement activation in vitro and during ex vivo reperfusion of pig liver. Clin. Exp. Immunol. 126 (2001) 412-420
11. Bhatia V.K., Yun S., Leung V., Grimsditch D.C., Benson G.M., Botto M.B., Boyle J.J., and Haskard D.O. Complement C1q reduces early atherosclerosis in low-density lipoprotein receptor-deficient mice. Am. J. Pathol. 170 (2007) 416-426
12. Bond R., Rerkasem K., and Rothwell P.M. Systematic review of the risks of carotid endarterectomy in relation to the clinical indication for and timing of surgery. Stroke 34 (2003) 2290-2301
13. Brunetti N.D., Correale M., Pellegrino P.L., Cuculo A., and Biase M.D. Acute phase proteins in patients with acute coronary syndrome: correlations with diagnosis, clinical features, and angiographic findings. Eur. J. Intern. Med. 18 (2007) 109-117
14. Buono C., Come C.E., Witztum J.L., Maguire G.F., Connelly P.W., Carroll M., and Lichtman A.H. Influence of C3 deficiency on atherosclerosis. Circulation 105 (2002) 3025-3031
15. Cantin B., Gagnon F., Moorjani S., Despres J.P., Lamarche B., Lupien P.J., and Dagenais G.R. Is lipoprotein(a) an independent risk factor for ischemic heart disease in men? The Quebec Cardiovascular Study. J. Am. Coll. Cardiol. 31 (1998) 519-525
16. Carroll M.C. The complement system in regulation of adaptive immunity. Nat. Immunol. 5 (2004) 981-986
17. Chen N.J., Mirtsos C., Suh D., Lu Y.C., Lin W.J., McKerlie C., Lee T., Baribault H., Tian H., and Yeh W.C. C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 446 (2007) 203-207
18. Christensen H., and Boysen G. C-reactive protein and white blood cell count increases in the first 24 hours after acute stroke. Cerebrovasc. Dis. 18 (2004) 214-219
19. Cornacoff J.B., Hebert L.A., Smead W.L., VanAman M.E., Birmingham D.J., and Waxman F.J. Primate erythrocyte-immune complex-clearing mechanism. J. Clin. Invest. 71 (1983) 236-247
20. D'Ambrosio A.L., Pinsky D.J., and Connolly E.S. The role of the complement cascade in ischemia/reperfusion injury: implications for neuroprotection. Mol. Med. 7 (2001) 367-382
21. Danton G.H., and Dietrich W.D. Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 62 (2003) 127-136
22. Dawber T.R., and Kannel W.B. The Framingham study. An epidemiological approach to coronary heart disease. Circulation 34 (1966) 553-555
23. de Groot H., and Rauen U. Ischemia-reperfusion injury: processes in pathogenetic networks: a review. Transplant. Proc. 39 (2007) 481-484
24. De Simoni M.G., Storini C., Barba M., Catapano L., Arabia A.M., Rossi E., and Bergamaschini L. Neuroprotection by complement (C1) inhibitor in mouse transient brain ischemia. J. Cereb. Blood Flow Metab. 23 (2003) 232-239
25. de Zwaan C., Kleine A.H., Diris J.H., Glatz J.F., Wellens H.J., Strengers P.F., Tissing M., Hack C.E., van Dieijen-Visser M.P., and Hermens W.T. Continuous 48-h C1-inhibitor treatment, following reperfusion therapy, in patients with acute myocardial infarction. Eur. Heart J. 23 (2002) 1670-1677
26. Dmytrijuk A., Robie-Suh K., Cohen M.H., Rieves D., Weiss K., and Pazdur R. FDA report: eculizumab (Soliris) for the treatment of patients with paroxysmal nocturnal hemoglobinuria. Oncologist 13 (2008) 993-1000
27. Dong J., Pratt J.R., Smith R.A., Dodd I., and Sacks S.H. Strategies for targeting complement inhibitors in ischaemia/reperfusion injury. Mol. Immunol. 36 (1999) 957-963
28. Ducruet A.F., Hassid B.G., Mack W.J., Sosunov S.A., Otten M.L., Fusco D.J., Hickman Z.L., Kim G.H., Komotar R.J., Mocco J., and Connolly E.S. C3a receptor modulation of granulocyte infiltration after murine focal cerebral ischemia is reperfusion dependent. J. Cereb. Blood Flow Metab. 28 (2008) 1048-1058
29. Ember J.A., and Hugli T.E. Complement factors and their receptors. Immunopharmacology 38 (1997) 3-15
30. Engstrom G., Hedblad B., Janzon L., and Lindgarde F. Complement C3 and C4 in plasma and incidence of myocardial infarction and stroke: a population-based cohort study. Eur. J. Cardiovasc. Prev. Rehabil. 14 (2007) 392-397
31. Eror A.T., Stojadinovic A., Starnes B.W., Makrides S.C., Tsokos G.C., and Shea-Donohue T. Antiinflammatory effects of soluble complement receptor type 1 promote rapid recovery of ischemia/reperfusion injury in rat small intestine. Clin. Immunol. 90 (1999) 266-275
32. Ferraresso M., Macor P., Valente M., Della Barbera M., D'Amelio F., Borghi O., Raschi E., Durigutto P., Meroni P., and Tedesco F. Posttransplant ischemia-reperfusion injury in transplanted heart is prevented by a minibody to the fifth component of complement. Transplantation 86 (2008) 1445-1451
33. Fiane A.E., Videm V., Lingaas P.S., Heggelund L., Nielsen E.W., Geiran O.R., Fung M., and Mollnes T.E. Mechanism of complement activation and its role in the inflammatory response after thoracoabdominal aortic aneurysm repair. Circulation 108 (2003) 849-856
34. Figueroa E., Gordon L.E., Feldhoff P.W., and Lassiter H.A. The administration of cobra venom factor reduces post-ischemic cerebral injury in adult and neonatal rats. Neurosci. Lett. 380 (2005) 48-53
35. Fleming S.D., and Tsokos G.C. Complement, natural antibodies, autoantibodies and tissue injury. Autoimmun. Rev. 5 (2006) 89-92
36. Folsom A.R., Nieto F.J., McGovern P.G., Tsai M.Y., Malinow M.R., Eckfeldt J.H., Hess D.L., and Davis C.E. Prospective study of coronary heart disease incidence in relation to fasting total homocysteine, related genetic polymorphisms, and B vitamins: the Atherosclerosis Risk in Communities (ARIC) study. Circulation 98 (1998) 204-210
37. Fosbrink M., Niculescu F., and Rus H. The role of c5b-9 terminal complement complex in activation of the cell cycle and transcription. Immunol. Res. 31 (2005) 37-46
38. Frericks H., Kievit J., van Baalen J.M., and van Bockel J.H. Carotid recurrent stenosis and risk of ipsilateral stroke: a systematic review of the literature. Stroke 29 (1998) 244-250
39. Geertinger P., and Sorensen H. Complement and arteriosclerosis. Atherosclerosis 18 (1973) 65-71
40. Girn H.R., Ahilathirunayagam S., Mavor A.I., and Homer-Vanniasinkam S. Reperfusion syndrome: cellular mechanisms of microvascular dysfunction and potential therapeutic strategies. Vasc. Endovascular Surg. 41 (2007) 277-293
41. Graham I.M., Daly L.E., Refsum H.M., Robinson K., Brattstrom L.E., Ueland P.M., Palma-Reis R.J., Boers G.H., Sheahan R.G., Israelsson B., Uiterwaal C.S., Meleady R., McMaster D., Verhoef P., Witteman J., Rubba P., Bellet H., Wautrecht J.C., de Valk H.W., Sales Luis A.C., Parrot-Rouland F.M., Tan K.S., Higgins I., Garcon D., Andria G., et al. Plasma homocysteine as a risk factor for vascular disease. The European Concerted Action Project. JAMA 277 (1997) 1775-1781
42. Groeneveld A.B., Raijmakers P.G., Rauwerda J.A., and Hack C.E. The inflammatory response to vascular surgery-associated ischaemia and reperfusion in man: effect on postoperative pulmonary function. Eur. J. Vasc. Endovasc. Surg. 14 (1997) 351-359
43. Grundy S.M., Cleeman J.I., Merz C.N., Brewer Jr. H.B., Clark L.T., Hunninghake D.B., Pasternak R.C., Smith Jr. S.C., and Stone N.J. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation 110 (2004) 227-239
44. Hansson G.K., and Libby P. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6 (2006) 508-519
45. He J.Q., Wiesmann C., and van Lookeren Campagne M. A role of macrophage complement receptor CRIg in immune clearance and inflammation. Mol. Immunol. 45 (2008) 4041-4047
46. Hill J., Lindsay T.F., Ortiz F., Yeh C.G., Hechtman H.B., and Moore Jr. F.D. Soluble complement receptor type 1 ameliorates the local and remote organ injury after intestinal ischemia-reperfusion in the rat. J. Immunol. 149 (1992) 1723-1728
47. Hill J.H., and Ward P.A. The phlogistic role of C3 leukotactic fragments in myocardial infarcts of rats. J. Exp. Med. 133 (1971) 885-900
48. Hoffmeister H.M., Ehlers R., Buttcher E., Kazmaier S., Szabo S., Beyer M.E., Steinmetz A., and Seipel L. Comparison of C-reactive protein and terminal complement complex in patients with unstable angina pectoris versus stable angina pectoris. Am. J. Cardiol. 89 (2002) 909-912
49. Hollander W., Colombo M.A., Kirkpatrick B., and Paddock J. Soluble proteins in the human atherosclerotic plaque. With spectral reference to immunoglobulins, C3-complement component, alpha 1-antitrypsin and alpha 2-macroglobulin. Atherosclerosis 34 (1979) 391-405
50. Horstick G., Berg O., Heimann A., Gotze O., Loos M., Hafner G., Bierbach B., Petersen S., Bhakdi S., Darius H., Horstick M., Meyer J., and Kempski O. Application of C1-esterase inhibitor during reperfusion of ischemic myocardium: dose-related beneficial versus detrimental effects. Circulation 104 (2001) 3125-3131
51. Huang J., Kim L.J., Mealey R., Marsh Jr. H.C., Zhang Y., Tenner A.J., Connolly Jr. E.S., and Pinsky D.J. Neuronal protection in stroke by an sLex-glycosylated complement inhibitory protein. Science 285 (1999) 595-599
52. Jaeschke H., Farhood A., Bautista A.P., Spolarics Z., and Spitzer J.J. Complement activates Kupffer cells and neutrophils during reperfusion after hepatic ischemia. Am. J. Physiol. 264 (1993) G801-G809
53. Jun S.W., Kim T.H., Lee H.M., Lee S.H., Kim W.J., Park S.J., Kim Y.S., and Lee S.H. Overexpression of the anaphylatoxin receptors, complement anaphylatoxin 3a receptor and complement anaphylatoxin 5a receptor, in the nasal mucosa of patients with mild and severe persistent allergic rhinitis. J. Allergy Clin. Immunol. 122 (2008) 119-125
54. Kirschfink M. Targeting complement in therapy. Immunol. Rev. 180 (2001) 177-189
55. Kornowski R., Hong M.K., Tio F.O., Bramwell O., Wu H., and Leon M.B. In-stent restenosis: contributions of inflammatory responses and arterial injury to neointimal hyperplasia. J. Am. Coll. Cardiol. 31 (1998) 224-230
56. Kostner K.M. Activation of the complement system: a crucial link between inflammation and atherosclerosis?. Eur. J. Clin. Invest. 34 (2004) 800-802
57. Kostner K.M., Fahti R.B., Case C., Hobson P., Tate J., and Marwick T.H. Inflammation, complement activation and endothelial function in stable and unstable coronary artery disease. Clin. Chim. Acta 365 (2006) 129-134
58. Kuehn M.H., Kim C.Y., Ostojic J., Bellin M., Alward W.L., Stone E.M., Sakaguchi D.S., Grozdanic S.D., and Kwon Y.H. Retinal synthesis and deposition of complement components induced by ocular hypertension. Exp. Eye Res. 83 (2006) 620-628
59. La Bonte L.R., Davis-Gorman G., Stahl G.L., and McDonagh P.F. Complement inhibition reduces injury in the type 2 diabetic heart following ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 294 (2008) H1282-H1290
60. Lew S.M., Gross C.E., Bednar M.M., Russell S.J., Fuller S.P., Ellenberger C.L., and Howard D. Complement depletion does not reduce brain injury in a rabbit model of thromboembolic stroke. Brain Res. Bull. 48 (1999) 325-331
61. Libby P. The vascular biology of atherosclerosis. In: Braunwald E., Zipes D.P., and Libby P. (Eds). Heart Disease: A Textbook of Cardiovascular Medicine vol. 1 (2001), W.B. Saunders Company, Philadelphia 995-1010
62. Libby P. Inflammation in atherosclerosis. Nature 420 (2002) 868-874
63. Libby P. Vascular biology of atherosclerosis: overview and state of the art. Am. J. Cardiol. 91 (2003) 3A-6A
64. Libby P., and Ridker P.M. Inflammation and atherosclerosis: role of C-reactive protein in risk assessment. Am. J. Med. 116 Suppl. 6A (2004) 9S-16S
65. Lin Z.H., Fukuda N., Jin X.Q., Yao E.H., Ueno T., Endo M., Saito S., Matsumoto K., and Mugishima H. Complement 3 is involved in the synthetic phenotype and exaggerated growth of vascular smooth muscle cells from spontaneously hypertensive rats. Hypertension 44 (2004) 42-47
66. Manukyan L., Boyajyan A., Arakelyan A., Ayvazyan V., Arakelova E., Sim R., and Grigoryan G. Immunochemical composition of cryoglobulins generated in stroke. J. Clin. Immunol. 29 (2009) 274-281
67. Mizuno M., Blanchin S., Gasque P., Nishikawa K., and Matsuo S. High levels of complement C3a receptor in the glomeruli in lupus nephritis. Am. J. Kidney Dis. 49 (2007) 598-606
68. Mocco J., Wilson D.A., Komotar R.J., Sughrue M.E., Coates K., Sacco R.L., Elkind M.S., and Connolly Jr. E.S. Alterations in plasma complement levels after human ischemic stroke. Neurosurgery 59 (2006) 28-33 (discussion 28-33)
69. Mold C. Role of complement in host defence against bacteria. Microbes. Infect. 1 (1999) 633-638
70. Muscari A., Bastagli L., Poggiopollini G., Tomassetti V., Massarelli G., Cappelletti O., Plate L., Boni P., and Puddu P. Different associations of C-reactive protein, fibrinogen and C3 with traditional risk factors in middle-aged men. Int. J. Cardiol. 83 (2002) 63-71
71. Muscari A., Bozzoli C., Gerratana C., Zaca F., Rovinetti C., Zauli D., La Placa M., and Puddu P. Association of serum IgA and C4 with severe atherosclerosis. Atherosclerosis 74 (1988) 179-186
72. Muscari A., Bozzoli C., Massarelli G., Puddu G.M., Palareti G., Legnani C., D'Atena T., Mazzuca A., Miniero R., Toscano V., et al. Complement components and fibrinogen: correlations and association with previous myocardial infarction. Cardiology 86 (1995) 232-237
73. Muscari A., Bozzoli C., Puddu G.M., Sangiorgi Z., Dormi A., Rovinetti C., Descovich G.C., and Puddu P. Association of serum C3 levels with the risk of myocardial infarction. Am. J. Med. 98 (1995) 357-364
74. Muscari A., Bozzoli C., Puddu G.M., Rovinetti C., Fiorentini G.P., Roversi R.A., and Puddu P. Correlations between serum lipids and complement components in adults without demonstrated atherosclerotic disease. Atherosclerosis 81 (1990) 111-118
75. Muscari A., Martignani C., Bastagli L., Poggiopollini G., Tomassetti V., Baldini L., Cappelletti O., Boni P., Ravaglia G., and Puddu P. A comparison of acute phase proteins and traditional risk factors as markers of combined plaque and intima-media thickness and plaque density in carotid and femoral arteries. Eur. J. Vasc. Endovasc. Surg. 26 (2003) 81-87
76. Muscari A., Massarelli G., Bastagli L., Poggiopollini G., Tomassetti V., Drago G., Martignani C., Pacilli P., Boni P., and Puddu P. Relationship of serum C3 to fasting insulin, risk factors and previous ischaemic events in middle-aged men. Eur. Heart J. 21 (2000) 1081-1090
77. Muscari A., Massarelli G., Bastagli L., Poggiopollini G., Tomassetti V., Volta U., Puddu G.M., and Puddu P. Relationship between serum C3 levels and traditional risk factors for myocardial infarction. Acta Cardiol. 53 (1998) 345-354
78. Muscari A., Mele M.C., Bastagli L., Poggiopollini G., Tomassetti V., Drago G., Legnani C., Barini A., Cappelletti O., Boni P., and Puddu P. Conditional risk factors in men with previous myocardial infarction: relevance of C3 and homocysteine. Acta Cardiol. 56 (2001) 303-311
79. Niculescu F., and Rus H. Complement activation and atherosclerosis. Mol. Immunol. 36 (1999) 949-955
80. Niculescu F., and Rus H. Mechanisms of signal transduction activated by sublytic assembly of terminal complement complexes on nucleated cells. Immunol. Res. 24 (2001) 191-199
81. Nishino H., Czurko A., Fukuda A., Hashitani T., Hida H., Karadi Z., and Lenard L. Pathophysiological process after transient ischemia of the middle cerebral artery in the rat. Brain Res. Bull. 35 (1994) 51-56
82. Okinaga S., Slattery D., Humbles A., Zsengeller Z., Morteau O., Kinrade M.B., Brodbeck R.M., Krause J.E., Choe H.R., Gerard N.P., and Gerard C. C5L2, a nonsignaling C5A binding protein. Biochemistry 42 (2003) 9406-9415
83. Oksjoki R., Jarva H., Kovanen P.T., Laine P., Meri S., and Pentikainen M.O. Association between complement factor H and proteoglycans in early human coronary atherosclerotic lesions: implications for local regulation of complement activation. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 630-636
84. Oksjoki R., Kovanen P.T., and Pentikainen M.O. Role of complement activation in atherosclerosis. Curr. Opin. Lipidol. 14 (2003) 477-482
85. Oksjoki R., Kovanen P.T., Mayranpaa M.I., Laine P., Blom A.M., Meri S., and Pentikainen M.O. Complement regulation in human atherosclerotic coronary lesions. Immunohistochemical evidence that C4b-binding protein negatively regulates the classical complement pathway, and that C5b-9 is formed via the alternative complement pathway. Atherosclerosis 192 (2007) 40-48
86. Oksjoki R., Kovanen P.T., Meri S., and Pentikainen M.O. Function and regulation of the complement system in cardiovascular diseases. Front. Biosci. 12 (2007) 4696-4708
87. Palikhe A., Sinisalo J., Seppanen M., Haario H., Meri S., Valtonen V., Nieminen M.S., and Lokki M.L. Serum complement C3/C4 ratio, a novel marker for recurrent cardiovascular events. Am. J. Cardiol. 99 (2007) 890-895
88. Park P., Haas M., Cunningham P.N., Alexander J.J., Bao L., Guthridge J.M., Kraus D.M., Holers V.M., and Quigg R.J. Inhibiting the complement system does not reduce injury in renal ischemia reperfusion. J. Am. Soc. Nephrol. 12 (2001) 1383-1390
89. Patel S., Thelander E.M., Hernandez M., Montenegro J., Hassing H., Burton C., Mundt S., Hermanowski-Vosatka A., Wright S.D., Chao Y.S., and Detmers P.A. ApoE(-/-) mice develop atherosclerosis in the absence of complement component C5. Biochem. Biophys. Res. Commun. 286 (2001) 164-170
90. Pedersen E.D., Froyland E., Kvissel A.K., Pharo A.M., Skalhegg B.S., Rootwelt T., and Mollnes T.E. Expression of complement regulators and receptors on human NT2-N neurons-effect of hypoxia and reoxygenation. Mol. Immunol. 44 (2007) 2459-2468
91. Pedersen E.D., Waje-Andreassen U., Vedeler C.A., Aamodt G., and Mollnes T.E. Systemic complement activation following human acute ischaemic stroke. Clin. Exp. Immunol. 137 (2004) 117-122
92. Pepys M.B., and Hirschfield G.M. C-reactive protein: a critical update. J. Clin. Invest. 111 (2003) 1805-1812
93. Persson L., Boren J., Robertson A.K., Wallenius V., Hansson G.K., and Pekna M. Lack of complement factor C3, but not factor B, increases hyperlipidemia and atherosclerosis in apolipoprotein E-/- low-density lipoprotein receptor-/- mice. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 1062-1067
94. Prohászka Z., and Füst G. Immunological aspects of heat-shock proteins-the optimum stress of life. Mol. Immunol. 41 (2004) 29-44
95. Ridker P.M., Hennekens C.H., Buring J.E., and Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N. Engl. J. Med. 342 (2000) 836-843
96. Riedemann N.C., Guo R.F., Neff T.A., Laudes I.J., Keller K.A., Sarma V.J., Markiewski M.M., Mastellos D., Strey C.W., Pierson C.L., Lambris J.D., Zetoune F.S., and Ward P.A. Increased C5a receptor expression in sepsis. J. Clin. Invest. 110 (2002) 101-108
97. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340 (1999) 115-126
98. Rugonfalvi-Kiss S., Dósa E., Madsen H.O., Endrész V., Prohászka Z., Laki J., Karádi I., Gönczöl E., Selmeci L., Romics L., Füst G., Entz L., and Garred P. High rate of early restenosis after carotid eversion endarterectomy in homozygous carriers of the normal mannose-binding lectin genotype. Stroke 36 (2005) 944-948
99. Saito E., Fujioka T., Kanno H., Hata E., Ueno T., Matsumoto T., Takahashi Y., Tochihara T., and Yasugi T. Complement receptors in atherosclerotic lesions. Artery 19 (1992) 47-62
100. Scarabin P.Y., Aillaud M.F., Amouyel P., Evans A., Luc G., Ferrieres J., Arveiler D., and Juhan-Vague I. Associations of fibrinogen, factor VII and PAI-1 with baseline findings among 10,500 male participants in a prospective study of myocardial infarction-the PRIME Study. Prospective Epidemiological Study of Myocardial Infarction. Thromb. Haemost. 80 (1998) 749-756
101. Schaefer E.J., Lamon-Fava S., Jenner J.L., McNamara J.R., Ordovas J.M., Davis C.E., Abolafia J.M., Lippel K., and Levy R.I. Lipoprotein(a) levels and risk of coronary heart disease in men. The lipid Research Clinics Coronary Primary Prevention Trial. JAMA 271 (1994) 999-1003
102. Schmiedt W., Kinscherf R., Deigner H.P., Kamencic H., Nauen O., Kilo J., Oelert H., Metz J., and Bhakdi S. Complement C6 deficiency protects against diet-induced atherosclerosis in rabbits. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 1790-1795
103. Schwertz H., Carter J.M., Russ M., Schubert S., Schlitt A., Buerke U., Schmidt M., Hillen H., Werdan K., and Buerke M. Serine protease inhibitor nafamostat given before reperfusion reduces inflammatory myocardial injury by complement and neutrophil inhibition. J. Cardiovasc. Pharmacol. 52 (2008) 151-160
104. Scola A.M., Johswich K.O., Morgan B.P., Klos A., and Monk P.N. The human complement fragment receptor, C5L2, is a recycling decoy receptor. Mol. Immunol. 46 (2009) 1149-1162
105. Seifert P.S., and Kazatchkine M.D. The complement system in atherosclerosis. Atherosclerosis 73 (1988) 91-104
106. Seifert P.S., Roth I., Schmiedt W., Oelert H., Okada N., Okada H., and Bhakdi S. CD59 (homologous restriction factor 20), a plasma membrane protein that protects against complement C5b-9 attack, in human atherosclerotic lesions. Atherosclerosis 96 (1992) 135-145
107. Shagdarsuren E., Bidzhekov K., Djalali-Talab Y., Liehn E.A., Hristov M., Matthijsen R.A., Buurman W.A., Zernecke A., and Weber C. C1-esterase inhibitor protects against neointima formation after arterial injury in atherosclerosis-prone mice. Circulation 117 (2008) 70-78
108. Speidl W.S., Exner M., Amighi J., Kastl S.P., Zorn G., Maurer G., Wagner O., Huber K., Minar E., Wojta J., and Schillinger M. Complement component C5a predicts future cardiovascular events in patients with advanced atherosclerosis. Eur. Heart J. 26 (2005) 2294-2299
109. Stapp J.M., Sjoelund V., Lassiter H.A., Feldhoff R.C., and Feldhoff P.W. Recombinant rat IL-1beta and IL-6 synergistically enhance C3 mRNA levels and complement component C3 secretion by H-35 rat hepatoma cells. Cytokine 30 (2005) 78-85
110. Stein J.H., Osgood R.W., Barnes J.L., Reineck H.J., Pinckard R.N., and McManus L.M. The role of complement in the pathogenesis of postischemic acute renal failure. Miner. Electrolyte Metab. 11 (1985) 256-261
111. Stimler N.P., Hugli T.E., and Bloor C.M. Pulmonary injury induced by C3a and C5a anaphylatoxins. Am. J. Pathol. 100 (1980) 327-348
112. Szabó A., Brazda E., Dósa E., Apor A., Szabolcs Z., and Entz L. Long-term restenosis rate of eversion endarterectomy on the internal carotid artery. Eur. J. Vasc. Endovasc. Surg. 27 (2004) 537-539
113. Szabó A., Laki J., Madsen H.O., Dósa E., Prohászka Z., Rugonfalvi-Kiss S., Kokai M., Acsádi G., Karádi I., Entz L., Selmeci L., Romics L., Füst G., Garred P., and Cervenak L. Early rise in serum VEGF and PDGF levels predisposes patients with a normal MBL2 genotype to restenosis after eversion endarterectomy. Stroke 38 (2007) 2247-2253
114. Széplaki G., Hirschberg K., Gombos T., Varga L., Prohászka Z., Dósa E., Acsády G., Karádi I., Garred P., Entz L., and Füst G. Early complement activation follows eversion carotid endarterectomy and correlates with the time of clamping of the carotid artery. Mol. Immunol. 45 (2008) 3289-3294
115. Széplaki G., Szegedi R., Hirschberg K., Gombos T., Varga L., Karadi I., Entz L., Szeplaki Z., Garred P., Prohaszka Z., and Fust G. Strong complement activation after acute ischemic stroke is associated with unfavorable outcomes. Atherosclerosis 204 (2009) 315-320
116. Széplaki G., Prohászka Z., Duba J., Rugonfalvi-Kiss S., Karádi I., Kókai M., Kramer J., Füst G., Kleiber M., Romics L., and Varga L. Association of high serum concentration of the third component of complement (C3) with pre-existing severe coronary artery disease and new vascular events in women. Atherosclerosis 177 (2004) 383-389
117. Széplaki G., Varga L., Laki J., Dósa E., Madsen H.O., Prohászka Z., Szabó A., Acsády G., Selmeci L., Garred P., Füst G., and Entz L. Elevated complement C3 is associated with early restenosis after eversion carotid endarterectomy. Thromb. Haemost. 96 (2006) 529-534
118. Széplaki G., Varga L., Laki J., Dósa E., Rugonfalvi-Kiss S., Madsen H.O., Prohászka Z., Kocsis A., Gál P., Szabó A., Acsády G., Karádi I., Selmeci L., Garred P., Füst G., and Entz L. Low c1-inhibitor levels predict early restenosis after eversion carotid endarterectomy. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 2756-2762
119. Takabayashi T., Vannier E., Clark B.D., Margolis N.H., Dinarello C.A., Burke J.F., and Gelfand J.A. A new biologic role for C3a and C3a desArg: regulation of TNF-alpha and IL-1 beta synthesis. J. Immunol. 156 (1996) 3455-3460
120. Testa L., Van Gaal W.J., Bhindi R., Biondi-Zoccai G.G., Abbate A., Agostoni P., Porto I., Andreotti F., Crea F., and Banning A.P. Pexelizumab in ischemic heart disease: a systematic review and meta-analysis on 15,196 patients. J. Thorac. Cardiovasc. Surg. 136 (2008) 884-893
121. Thorbjornsdottir P., Kolka R., Gunnarsson E., Bambir S.H., Thorgeirsson G., Kotwal G.J., and Arason G.J. Vaccinia virus complement control protein diminishes formation of atherosclerotic lesions: complement is centrally involved in atherosclerotic disease. Ann. N.Y. Acad. Sci. 1056 (2005) 1-15
122. Tofler G.H., Brezinski D., Schafer A.I., Czeisler C.A., Rutherford J.D., Willich S.N., Gleason R.E., Williams G.H., and Muller J.E. Concurrent morning increase in platelet aggregability and the risk of myocardial infarction and sudden cardiac death. N. Engl. J. Med. 316 (1987) 1514-1518
123. Torzewski M., Klouche M., Hock J., Messner M., Dorweiler B., Torzewski J., Gabbert H.E., and Bhakdi S. Immunohistochemical demonstration of enzymatically modified human LDL and its colocalization with the terminal complement complex in the early atherosclerotic lesion. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 369-378
124. Torzewski M., Torzewski J., Bowyer D.E., Waltenberger J., Fitzsimmons C., Hombach V., and Gabbert H.E. Immunohistochemical colocalization of the terminal complex of human complement and smooth muscle cell alpha-actin in early atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 17 (1997) 2448-2452
125. Trisal V., Paulson T., Hans S.S., and Mittal V. Carotid artery restenosis: an ongoing disease process. Am. Surg. 68 (2002) 275-279 (discussion 279-280)
126. Vakeva A.P., Agah A., Rollins S.A., Matis L.A., Li L., and 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 97 (1998) 2259-2267
127. Van Beek J., Bernaudin M., Petit E., Gasque P., Nouvelot A., MacKenzie E.T., and Fontaine M. Expression of receptors for complement anaphylatoxins C3a and C5a following permanent focal cerebral ischemia in the mouse. Exp. Neurol. 161 (2000) 373-382
128. Vasthare U.S., Barone F.C., Sarau H.M., Rosenwasser R.H., DiMartino M., Young W.F., and Tuma R.F. Complement depletion improves neurological function in cerebral ischemia. Brain Res. Bull. 45 (1998) 413-419
129. Vlaicu R., Niculescu F., Rus H.G., and Cristea A. Immunohistochemical localization of the terminal C5b-9 complement complex in human aortic fibrous plaque. Atherosclerosis 57 (1985) 163-177
130. Vlaicu R., Rus H.G., Niculescu F., and Cristea A. Quantitative determinations of immunoglobulins and complement components in human aortic atherosclerotic wall. Med. Interne 23 (1985) 29-35
131. Wada K., Montalto M.C., and Stahl G.L. Inhibition of complement C5 reduces local and remote organ injury after intestinal ischemia/reperfusion in the rat. Gastroenterology 120 (2001) 126-133
132. Walport M.J. Complement. First of two parts. N. Engl. J. Med. 344 (2001) 1058-1066
133. Walport M.J. Complement. Second of two parts. N. Engl. J. Med. 344 (2001) 1140-1144
134. Ward P.A. Functions of C5a receptors. J. Mol. Med. (2009)
135. Weisman H.F., Bartow T., Leppo M.K., Marsh Jr. H.C., Carson G.R., Concino M.F., Boyle M.P., Roux K.H., Weisfeldt M.L., and Fearon D.T. Soluble human complement receptor type 1: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 249 (1990) 146-151
136. Wick G., Knoflach M., and Xu Q. Autoimmune and inflammatory mechanisms in atherosclerosis. Annu. Rev. Immunol. 22 (2004) 361-403
137. Wick G., Schett G., Amberger A., Kleindienst R., and Xu Q. Is atherosclerosis an immunologically mediated disease?. Immunol. Today 16 (1995) 27-33
138. Wiesmann C., Katschke K.J., Yin J., Helmy K.Y., Steffek M., Fairbrother W.J., McCallum S.A., Embuscado L., DeForge L., Hass P.E., and van Lookeren Campagne M. Structure of C3b in complex with CRIg gives insights into regulation of complement activation. Nature 444 (2006) 217-220
139. Wu G., Hu W., Shahsafaei A., Song W., Dobarro M., Sukhova G.K., Bronson R.R., Shi G.P., Rother R.P., Halperin J.A., and Qin X. Complement regulator CD59 protects against atherosclerosis by restricting the formation of complement membrane attack complex. Circ. Res. 104 (2009) 550-558
140. Yun S., Leung V.W., Botto M., Boyle J.J., and Haskard D.O. Brief report: accelerated atherosclerosis in low-density lipoprotein receptor-deficient mice lacking the membrane-bound complement regulator CD59. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1714-1716
141. Zhang H., Qin G., Liang G., Li J., Barrington R.A., and Liu D.X. C5aR-mediated myocardial ischemia/reperfusion injury. Biochem. Biophys. Res. Commun. 357 (2007) 446-452
142. Zhang M., and Carroll M.C. Natural antibody mediated innate autoimmune response. Mol. Immunol. 44 (2007) 103-110
143. Zheng X., Zhang X., Sun H., Feng B., Li M., Chen G., Vladau C., Chen D., Suzuki M., Min L., Liu W., Zhong R., Garcia B., Jevnikar A., and Min W.P. Protection of renal ischemia injury using combination gene silencing of complement 3 and caspase 3 genes. Transplantation 82 (2006) 1781-1786
144. Zhou W., Farrar C.A., Abe K., Pratt J.R., Marsh J.E., Wang Y., Stahl G.L., and Sacks S.H. Predominant role for C5b-9 in renal ischemia/reperfusion injury. J. Clin. Invest. 105 (2000) 1363-1371
145. Zhu J., Nieto F.J., Horne B.D., Anderson J.L., Muhlestein J.B., and Epstein S.E. Prospective study of pathogen burden and risk of myocardial infarction or death. Circulation 103 (2001) 45-51
146. Zimmerman J.L., Dellinger R.P., Straube R.C., and Levin J.L. Phase I trial of the recombinant soluble complement receptor 1 in acute lung injury and acute respiratory distress syndrome. Crit. Care Med. 28 (2000) 3149-3154