The role of the complement system in metabolic organs and metabolic diseases

Seminars in Immunology

Volumn 25, Issue 1, 2013, Pages 47-53

  Phieler, Julia ^a   Garcia Martin, Ruben ^a   Lambris, John D ^b   Chavakis, Triantafyllos ^a,c  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

Author keywords

Adipose tissue; Complement; Diabetes; Insulin resistance; Liver; Pancreas; Steatosis

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5A; INSULIN;

ADAPTIVE IMMUNITY; ADIPOSE TISSUE; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; DISEASES; FATTY LIVER; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; INSULIN RESISTANCE; LIVER; METABOLIC DISORDER; METABOLISM; NONHUMAN; PANCREAS; PANCREAS ISLET; PHENOTYPE; REVIEW; STRESS; UPREGULATION;

ADIPOSE TISSUE; COMPLEMENT; DIABETES; INSULIN RESISTANCE; LIVER; PANCREAS; STEATOSIS;

ADIPOSE TISSUE; ANIMALS; COMPLEMENT SYSTEM PROTEINS; DIABETES MELLITUS; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INSULIN RESISTANCE; LIVER; LIVER REGENERATION; METABOLIC DISEASES; PANCREATITIS;

EID: 84879885868     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2013.04.003     Document Type: Review

References (122)

1. Petrasek J., Bala S., Csak T., Lippai D., Kodys K., Menashy V., et al. IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. Journal of Clinical Investigation 2012, 122:3476-3489.
2. Zhan Y.T., An W. Roles of liver innate immune cells in nonalcoholic fatty liver disease. World Journal of Gastroenterology 2010, 16:4652-4660.
3. Donath M.Y., Shoelson S.E. Type 2 diabetes as an inflammatory disease. Nature Reviews Immunology 2011, 11:98-107.
4. Donath M.Y., Boni-Schnetzler M., Ellingsgaard H., Ehses J.A. Islet inflammation impairs the pancreatic beta-cell in type 2 diabetes. Physiology (Bethesda) 2009, 24:325-331.
5. Chawla A., Nguyen K.D., Goh Y.P. Macrophage-mediated inflammation in metabolic disease. Nature Reviews Immunology 2011, 11:738-749.
6. Hotamisligil G.S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
7. Chatzigeorgiou A., Karalis K.P., Bornstein S.R., Chavakis T. Lymphocytes in obesity-related adipose tissue inflammation. Diabetologia 2012, 55:2583-2592.
8. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. Journal of Clinical Investigation 2003, 112:1796-1808.
9. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. Journal of Clinical Investigation 2003, 112:1821-1830.
10. Shi H., Kokoeva M.V., Inouye K., Tzameli I., Yin H., Flier J.S. TLR4 links innate immunity and fatty acid-induced insulin resistance. Journal of Clinical Investigation 2006, 116:3015-3025.
11. Pal D., Dasgupta S., Kundu R., Maitra S., Das G., Mukhopadhyay S., et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nature Medicine 2012, 18:1279-1285.
12. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nature Immunology 2010, 11:785-797.
13. Markiewski M.M., Lambris J.D. The role of complement in inflammatory diseases from behind the scenes into the spotlight. American Journal of Pathology 2007, 171:715-727.
14. Zipfel P.F., Skerka C. Complement regulators and inhibitory proteins. Nature Reviews Immunology 2009, 9:729-740.
15. Wagner E., Frank M.M. Therapeutic potential of complement modulation. Nature Reviews Drug Discovery 2010, 9:43-56.
16. Reis E.S., Chen H., Sfyroera G., Monk P.N., Kohl J., Ricklin D., et al. C5a receptor-dependent cell activation by physiological concentrations of desarginated C5a: insights from a novel label-free cellular assay. Journal of Immunology 2012, 189:4797-4805.
17. Gaboriaud C., Thielens N.M., Gregory L.A., Rossi V., Fontecilla-Camps J.C., Arlaud G.J. Structure and activation of the C1 complex of complement: unraveling the puzzle. Trends in Immunology 2004, 25:368-373.
18. Wallis R., Mitchell D.A., Schmid R., Schwaeble W.J., Keeble A.H. Paths reunited: initiation of the classical and lectin pathways of complement activation. Immunobiology 2010, 215:1-11.
19. 2O)Bb). Molecular Immunology 2008, 45:2370-2379.
20. Pangburn M.K., Schreiber R.D., Muller-Eberhard H.J. Formation of the initial C3 convertase of the alternative complement pathway. Acquisition of C3b-like activities by spontaneous hydrolysis of the putative thioester in native C3. Journal of Experimental Medicine 1981, 154:856-867.
21. Kim D.D., Song W.C. Membrane complement regulatory proteins. Clinical Immunology 2006, 118:127-136.
22. Vogt W., Damerau B., Luhmann B., Hesse D., Haller Y. Complement activation in human lymph: modulation by the contact activation system and by leukocytes. International Archives of Allergy and Applied Immunology 1986, 79:423-433.
23. Wiggins R.C., Giclas P.C., Henson P.M. Chemotactic activity generated from the fifth component of complement by plasma kallikrein of the rabbit. Journal of Experimental Medicine 1981, 153:1391-1404.
24. Huber-Lang M., Sarma J.V., Zetoune F.S., Rittirsch D., Neff T.A., McGuire S.R., et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nature Medicine 2006, 12:682-687.
25. Ahren B., Havel P.J., Pacini G., Cianflone K. Acylation stimulating protein stimulates insulin secretion. International Journal of Obesity and Related Metabolic Disorders 2003, 27:1037-1043.
26. Martinez A., Pio R., Lopez J., Cuttitta F. Expression of the adrenomedullin binding protein, complement factor H, in the pancreas and its physiological impact on insulin secretion. Journal of Endocrinology 2001, 170:503-511.
27. Chick W.L., Like A.A. Studies in the diabetic mutant mouse 3. Physiological factors associated with alterations in beta cell proliferation. Diabetologia 1970, 6:243-251.
28. Maedler K., Spinas G.A., Lehmann R., Sergeev P., Weber M., Fontana A., et al. Glucose induces beta-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes 2001, 50:1683-1690.
29. Maedler K., Sergeev P., Ris F., Oberholzer J., Joller-Jemelka H.I., Spinas G.A., et al. Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. Journal of Clinical Investigation 2002, 110:851-860.
30. Homo-Delarche F., Calderari S., Irminger J.C., Gangnerau M.N., Coulaud J., Rickenbach K., et al. Islet inflammation and fibrosis in a spontaneous model of type 2 diabetes, the GK rat. Diabetes 2006, 55:1625-1633.
31. Hull R.L., Westermark G.T., Westermark P., Kahn S.E. Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes. Journal of Clinical Endocrinology and Metabolism 2004, 89:3629-3643.
32. Qi D., Cai K., Wang O., Li Z., Chen J., Deng B., et al. Fatty acids induce amylin expression and secretion by pancreatic beta-cells. American Journal of Physiology - Endocrinology and Metabolism 2010, 298:E99-E107.
33. Klegeris A., McGeer P.L. Complement activation by islet amyloid polypeptide (IAPP) and alpha-synuclein 112. Biochemical and Biophysical Research Communications 2007, 357:1096-1099.
34. Sjolander J., Westermark G.T., Renstrom E., Blom A.M. Islet amyloid polypeptide triggers limited complement activation and binds complement inhibitor C4b-binding protein, which enhances fibril formation. Journal of Biological Chemistry 2011, 287:10824-10833.
35. Eisenbarth G.S. Type I diabetes mellitus A chronic autoimmune disease. New England Journal of Medicine 1986, 314:1360-1368.
36. Shizuru J.A., Taylor-Edwards C., Banks B.A., Gregory A.K., Fathman C.G. Immunotherapy of the nonobese diabetic mouse: treatment with an antibody to T-helper lymphocytes. Science 1988, 240:659-662.
37. Martin A.P., Rankin S., Pitchford S., Charo I.F., Furtado G.C., Lira S.A. Increased expression of CCL2 in insulin-producing cells of transgenic mice promotes mobilization of myeloid cells from the bone marrow, marked insulitis, and diabetes. Diabetes 2008, 57:3025-3033.
38. Kendall P.L., Case J.B., Sullivan A.M., Holderness J.S., Wells K.S., Liu E., et al. Tolerant anti-insulin B cells are effective APCs. Journal of Immunology 2013, 190:2519-2526.
39. Heninger A.K., Monti P., Wilhelm C., Schwaiger P., Kuehn D., Ziegler A.G., et al. Activation of islet autoreactive naive T cells in infants is influenced by homeostatic mechanisms and antigen presenting capacity. Diabetes 2013; Jan 24. [Epub ahead of print].
40. Baxter A.G., Cooke A. Complement lytic activity has no role in the pathogenesis of autoimmune diabetes in NOD mice. Diabetes 1993, 42:1574-1578.
41. Conroy S.J., Abdel-Wahab Y.H., Caraher E.M., Byrne P.M., Murphy E., Nolan J., et al. Evidence for complement-dependent and -independent inhibition of insulin secretion from clonal beta-cells incubated in the presence of sera of newly diagnosed IDDM patients. Journal of Endocrinology 2000, 164:139-147.
42. 2+ levels after incubation in the presence of newly diagnosed Type-1 diabetic patient sera Possible role in serum-induced inhibition of insulin secretion. Journal of Endocrinology 2002, 173:53-62.
43. Caraher E.M., Conroy S.J., Newsholme P. Evidence for enhanced rates of complement activation in serum from patients with newly diagnosed insulin-dependent diabetes mellitus exposed to rat islet cells and complement-dependent induction of islet cell apoptosis. Journal of Endocrinology 1999, 162:143-153.
44. Radillo O., Nocera A., Leprini A., Barocci S., Mollnes T.E., Pocecco M., et al. Complement-fixing islet cell antibodies in type-1 diabetes can trigger the assembly of the terminal complement complex on human islet cells and are potentially cytotoxic. Clinical Immunology and Immunopathology 1996, 79:217-223.
45. Hess K., Alzahrani S.H., Mathai M., Schroeder V., Carter A.M., Howell G., et al. A novel mechanism for hypofibrinolysis in diabetes: the role of complement C3. Diabetologia 2012, 55:1103-1113.
46. Bouwman L.H., Eerligh P., Terpstra O.T., Daha M.R., de Knijff P., Ballieux B.E., et al. Elevated levels of mannose-binding lectin at clinical manifestation of type 1 diabetes in juveniles. Diabetes 2005, 54:3002-3006.
47. Hansen T.K., Thiel S., Knudsen S.T., Gravholt C.H., Christiansen J.S., Mogensen C.E., et al. Elevated levels of mannan-binding lectin in patients with type 1 diabetes. Journal of Clinical Endocrinology and Metabolism 2003, 88:4857-4861.
48. Ostergaard J.A., Bjerre M., Dagnaes-Hansen F., Hansen T.K., Thiel S., Flyvbjerg A. Diabetes-induced changes in mannan-binding lectin levels and complement activation in a mouse model of type 1 diabetes. Scandinavian Journal of Immunology 2013, 77:187-194.
49. Hansen T.K. Mannose-binding lectin (MBL) and vascular complications in diabetes. Hormone and Metabolic Research 2005, 37(Suppl 1):95-98.
50. Pavlov V.I., La Bonte L.R., Baldwin W.M., Markiewski M.M., Lambris J.D., Stahl G.L. Absence of mannose-binding lectin prevents hyperglycemic cardiovascular complications. American Journal of Pathology 2012, 180:104-112.
51. Ostergaard J., Thiel S., Gadjeva M., Hansen T.K., Rasch R., Flyvbjerg A. Mannose-binding lectin deficiency attenuates renal changes in a streptozotocin-induced model of type 1 diabetes in mice. Diabetologia 2007, 50:1541-1549.
52. Planas R., Carrillo J., Sanchez A., de Villa M.C., Nunez F., Verdaguer J., et al. Gene expression profiles for the human pancreas and purified islets in type 1 diabetes: new findings at clinical onset and in long-standing diabetes. Clinical and Experimental Immunology 2010, 159:23-44.
53. Lin M., Yin N., Murphy B., Medof M.E., Segerer S., Heeger P.S., et al. Immune cell-derived c3 is required for autoimmune diabetes induced by multiple low doses of streptozotocin. Diabetes 2010, 59:2247-2252.
54. Fu W., Wojtkiewicz G., Weissleder R., Benoist C., Mathis D. Early window of diabetes determinism in NOD mice, dependent on the complement receptor CRIg, identified by noninvasive imaging. Nature Immunology 2012, 13:361-368.
55. He J.Q., Wiesmann C., van Lookeren Campagne M. A role of macrophage complement receptor CRIg in immune clearance and inflammation. Molecular Immunology 2008, 45:4041-4047.
56. Cook K.S., Groves D.L., Min H.Y., Spiegelman B.M. A developmentally regulated mRNA from 3T3 adipocytes encodes a novel serine protease homologue. Proceedings of the National Academy of Sciences of the United States of America 1985, 82:6480-6484.
57. Choy L.N., Rosen B.S., Spiegelman B.M. Adipsin and an endogenous pathway of complement from adipose cells. Journal of Biological Chemistry 1992, 267:12736-12741.
58. Wilkison W.O., Min H.Y., Claffey K.P., Satterberg B.L., Spiegelman B.M. Control of the adipsin gene in adipocyte differentiation. Identification of distinct nuclear factors binding to single- and double-stranded DNA. Journal of Biological Chemistry 1990, 265:477-482.
59. Choy L.N., Spiegelman B.M. Regulation of alternative pathway activation and C3a production by adipose cells. Obesity Research 1996, 4:521-532.
60. Peake P.W., O'Grady S., Pussell B.A., Charlesworth J.A. Detection and quantification of the control proteins of the alternative pathway of complement in 3T3-L1 adipocytes. European Journal of Clinical Investigation 1997, 27:922-927.
61. Baldo A., Sniderman A.D., St-Luce S., Avramoglu R.K., Maslowska M., Hoang B., et al. The adipsin-acylation stimulating protein system and regulation of intracellular triglyceride synthesis. Journal of Clinical Investigation 1993, 92:1543-1547.
62. Cianflone K.M., Sniderman A.D., Walsh M.J., Vu H.T., Gagnon J., Rodriguez M.A. Purification and characterization of acylation stimulating protein. Journal of Biological Chemistry 1989, 264:426-430.
63. Cianflone K., Lu H., Smith J., Yu W., Wang H. Adiponectin, acylation stimulating protein and complement C3 are altered in obesity in very young children. Clinical Endocrinology 2005, 62:567-572.
64. Scantlebury T., Maslowska M., Cianflone K. Chylomicron-specific enhancement of acylation stimulating protein and precursor protein C3 production in differentiated human adipocytes. Journal of Biological Chemistry 1998, 273:20903-20909.
65. Halkes C.J., van Dijk H., de Jaegere P.P., Plokker H.W., van Der Helm Y., Erkelens D.W., et al. Postprandial increase of complement component 3 in normolipidemic patients with coronary artery disease: effects of expanded-dose simvastatin. Arteriosclerosis, Thrombosis, and Vascular Biology 2001, 21:1526-1530.
66. Maslowska M., Scantlebury T., Germinario R., Cianflone K. Acute in vitro production of acylation stimulating protein in differentiated human adipocytes. Journal of Lipid Research 1997, 38:1-11.
67. Paglialunga S., Fisette A., Yan Y., Deshaies Y., Brouillette J.F., Pekna M., et al. Acylation-stimulating protein deficiency and altered adipose tissue in alternative complement pathway knockout mice. American Journal of Physiology - Endocrinology and Metabolism 2008, 294:E521-E529.
68. Ylitalo K., Pajukanta P., Meri S., Cantor R.M., Mero-Matikainen N., Vakkilainen J., et al. Serum C3 but not plasma acylation-stimulating protein is elevated in Finnish patients with familial combined hyperlipidemia. Arteriosclerosis, Thrombosis, and Vascular Biology 2001, 21:838-843.
69. Faraj M., Sniderman A.D., Cianflone K. ASP enhances in situ lipoprotein lipase activity by increasing fatty acid trapping in adipocytes. Journal of Lipid Research 2004, 45:657-666.
70. Yasruel Z., Cianflone K., Sniderman A.D., Rosenbloom M., Walsh M., Rodriguez M.A. Effect of acylation stimulating protein on the triacylglycerol synthetic pathway of human adipose tissue. Lipids 1991, 26:495-499.
71. Van Harmelen V., Reynisdottir S., Cianflone K., Degerman E., Hoffstedt J., Nilsell K., et al. Mechanisms involved in the regulation of free fatty acid release from isolated human fat cells by acylation-stimulating protein and insulin. Journal of Biological Chemistry 1999, 274:18243-18251.
72. Murray I., Sniderman A.D., Havel P.J., Cianflone K. Acylation stimulating protein (ASP) deficiency alters postprandial and adipose tissue metabolism in male mice. Journal of Biological Chemistry 1999, 274:36219-36225.
73. Xia Z., Stanhope K.L., Digitale E., Simion O.M., Chen L., Havel P., et al. Acylation-stimulating protein (ASP)/complement C3adesArg deficiency results in increased energy expenditure in mice. Journal of Biological Chemistry 2004, 279:4051-4057.
74. Wetsel R.A., Kildsgaard J., Zsigmond E., Liao W., Chan L. Genetic deficiency of acylation stimulating protein (ASP(C3ades-Arg)) does not cause hyperapobetalipoproteinemia in mice. Journal of Biological Chemistry 1999, 274:19429-19433.
75. -/- mice increases insulin resistance via adipocyte inflammatory mechanisms. PLoS ONE 2012, 7:e46883.
76. Johswich K., Martin M., Thalmann J., Rheinheimer C., Monk P.N., Klos A. Ligand specificity of the anaphylatoxin C5L2 receptor and its regulation on myeloid and epithelial cell lines. Journal of Biological Chemistry 2006, 281:39088-39095.
77. Scola A.M., Johswich K.O., Morgan B.P., Klos A., Monk P.N. The human complement fragment receptor, C5L2, is a recycling decoy receptor. Molecular Immunology 2009, 46:1149-1162.
78. Kalant D., Cain S.A., Maslowska M., Sniderman A.D., Cianflone K., Monk P.N. The chemoattractant receptor-like protein C5L2 binds the C3a des-Arg77/acylation-stimulating protein. Journal of Biological Chemistry 2003, 278:11123-11129.
79. Kalant D., MacLaren R., Cui W., Samanta R., Monk P.N., Laporte S.A., et al. C5L2 is a functional receptor for acylation-stimulating protein. Journal of Biological Chemistry 2005, 280:23936-23944.
80. Cain S.A., Monk P.N. The orphan receptor C5L2 has high affinity binding sites for complement fragments C5a and C5a des-Arg(74). Journal of Biological Chemistry 2002, 277:7165-7169.
81. Ward P.A. Functions of C5a receptors. Journal of Molecular Medicine (Berlin) 2009, 87:375-378.
82. Paglialunga S., Schrauwen P., Roy C., Moonen-Kornips E., Lu H., Hesselink M.K., et al. Reduced adipose tissue triglyceride synthesis and increased muscle fatty acid oxidation in C5L2 knockout mice. Journal of Endocrinology 2007, 194:293-304.
83. Fisette A., Munkonda M.N., Oikonomopoulou K., Paglialunga S., Lambris J.D., Cianflone K. C5L2 receptor disruption enhances the development of diet-induced insulin resistance in mice. Immunobiology 2013, 218:127-133.
84. Lim J., Iyer A., Suen J.Y., Seow V., Reid R.C., Brown L., et al. C5aR and C3aR antagonists each inhibit diet-induced obesity, metabolic dysfunction, and adipocyte and macrophage signaling. FASEB Journal 2013, 27:822-831.
85. Langer H.F., Chung K.J., Orlova V.V., Choi E.Y., Kaul S., Kruhlak M.J., et al. Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis. Blood 2010, 116:4395-4403.
86. Mamane Y., Chung Chan C., Lavallee G., Morin N., Xu L.J., Huang J., et al. The C3a anaphylatoxin receptor is a key mediator of insulin resistance and functions by modulating adipose tissue macrophage infiltration and activation. Diabetes 2009, 58:2006-2017.
87. Schadt E.E., Lamb J., Yang X., Zhu J., Edwards S., Guhathakurta D., et al. An integrative genomics approach to infer causal associations between gene expression and disease. Nature Genetics 2005, 37:710-717.
88. Ohinata K., Yoshikawa M. Food intake regulation by central complement system. Advances in Experimental Medicine and Biology 2008, 632:35-46.
89. Alper C.A., Johnson A.M., Birtch A.G., Moore F.D. Human C'3: evidence for the liver as the primary site of synthesis. Science 1969, 163:286-288.
90. Gasque P. Complement: a unique innate immune sensor for danger signals. Molecular Immunology 2004, 41:1089-1098.
91. Qin X., Gao B. The complement system in liver diseases. Cellular & Molecular Immunology 2006, 3:333-340.
92. Mack C., Jungermann K., Gotze O., Schieferdecker H.L. Anaphylatoxin C5a actions in rat liver: synergistic enhancement by C5a of lipopolysaccharide-dependent alpha(2)-macroglobulin gene expression in hepatocytes via IL-6 release from Kupffer cells. Journal of Immunology 2001, 167:3972-3979.
93. Schieferdecker H.L., Schlaf G., Koleva M., Gotze O., Jungermann K. Induction of functional anaphylatoxin C5a receptors on hepatocytes by in vivo treatment of rats with IL-6. Journal of Immunology 2000, 164:5453-5458.
94. Postic C., Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. Journal of Clinical Investigation 2008, 118:829-838.
95. Byun J.S., Jeong W.I. Involvement of hepatic innate immunity in alcoholic liver disease. Immune Network 2010, 10:181-187.
96. Matteoni C.A., Younossi Z.M., Gramlich T., Boparai N., Liu Y.C., McCullough A.J. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 1999, 116:1413-1419.
97. Kleiner D.E., Brunt E.M. Nonalcoholic fatty liver disease: pathologic patterns and biopsy evaluation in clinical research. Seminars in Liver Disease 2012, 32:3-13.
98. Wang H.J., Gao B., Zakhari S., Nagy L.E. Inflammation in alcoholic liver disease. Annual Review of Nutrition 2012, 32:343-368.
99. Jarvelainen H.A., Vakeva A., Lindros K.O., Meri S. Activation of complement components and reduced regulator expression in alcohol-induced liver injury in the rat. Clinical Immunology 2002, 105:57-63.
100. Bykov I.L., Vakeva A., Jarvelainen H.A., Meri S., Lindros K.O. Protective function of complement against alcohol-induced rat liver damage. International Immunopharmacology 2004, 4:1445-1454.
101. Bykov I., Jauhiainen M., Olkkonen V.M., Saarikoski S.T., Ehnholm C., Junnikkala S., et al. Hepatic gene expression and lipid parameters in complement C3(-/-) mice that do not develop ethanol-induced steatosis. Journal of Hepatology 2007, 46:907-914.
102. Bykov I., Junnikkala S., Pekna M., Lindros K.O., Meri S. Complement C3 contributes to ethanol-induced liver steatosis in mice. Annals of Medicine 2006, 38:280-286.
103. Pritchard M.T., McMullen M.R., Stavitsky A.B., Cohen J.I., Lin F., Medof M.E., et al. Differential contributions of C3, C5, and decay-accelerating factor to ethanol-induced fatty liver in mice. Gastroenterology 2007, 132:1117-1126.
104. Cohen J.I., Roychowdhury S., McMullen M.R., Stavitsky A.B., Nagy L.E. Complement and alcoholic liver disease: role of C1q in the pathogenesis of ethanol-induced liver injury in mice. Gastroenterology 2010, 139:664-674. 674.e1.
105. Roychowdhury S., McMullen M.R., Pritchard M.T., Hise A.G., van Rooijen N., Medof M.E., et al. An early complement-dependent and TLR-4-independent phase in the pathogenesis of ethanol-induced liver injury in mice. Hepatology 2009, 49:1326-1334.
106. Rensen S.S., Slaats Y., Driessen A., Peutz-Kootstra C.J., Nijhuis J., Steffensen R., et al. Activation of the complement system in human nonalcoholic fatty liver disease. Hepatology 2009, 50:1809-1817.
107. van Greevenbroek M.M., Jacobs M., van der Kallen C.J., Vermeulen V.M., Jansen E.H., Schalkwijk C.G., et al. The cross-sectional association between insulin resistance and circulating complement C3 is partly explained by plasma alanine aminotransferase, independent of central obesity and general inflammation (the CODAM study). European Journal of Clinical Investigation 2011, 41:372-379.
108. Yesilova Z., Ozata M., Oktenli C., Bagci S., Ozcan A., Sanisoglu S.Y., et al. Increased acylation stimulating protein concentrations in nonalcoholic fatty liver disease are associated with insulin resistance. American Journal of Gastroenterology 2005, 100:842-849.
109. Sreekumar R., Rosado B., Rasmussen D., Charlton M. Hepatic gene expression in histologically progressive nonalcoholic steatohepatitis. Hepatology 2003, 38:244-251.
110. Baumann M., Witzke O., Canbay A., Patschan S., Treichel U., Gerken G., et al. Serum C3 complement concentrations correlate with liver function in patients with liver cirrhosis. Hepato-Gastroenterology 2004, 51:1451-1453.
111. Gregoire F.M., Zhang Q., Smith S.J., Tong C., Ross D., Lopez H., et al. Diet-induced obesity and hepatic gene expression alterations in C57BL/6J and ICAM-1-deficient mice. American Journal of Physiology - Endocrinology and Metabolism 2002, 282:E703-E713.
112. He S., Atkinson C., Evans Z., Ellett J.D., Southwood M., Elvington A., et al. A role for complement in the enhanced susceptibility of steatotic livers to ischemia and reperfusion injury. Journal of Immunology 2009, 183:4764-4772.
113. Michalopoulos G.K., DeFrances M.C. Liver regeneration. Science 1997, 276:60-66.
114. He S., Atkinson C., Qiao F., Cianflone K., Chen X., Tomlinson S. A complement-dependent balance between hepatic ischemia/reperfusion injury and liver regeneration in mice. Journal of Clinical Investigation 2009, 119:2304-2316.
115. Strey C.W., Markiewski M., Mastellos D., Tudoran R., Spruce L.A., Greenbaum L.E., et al. The proinflammatory mediators C3a and C5a are essential for liver regeneration. Journal of Experimental Medicine 2003, 198:913-923.
116. Markiewski M.M., DeAngelis R.A., Strey C.W., Foukas P.G., Gerard C., Gerard N., et al. The regulation of liver cell survival by complement. Journal of Immunology 2009, 182:5412-5418.
117. Clark A., Weymann A., Hartman E., Turmelle Y., Carroll M., Thurman J.M., et al. Evidence for non-traditional activation of complement factor C3 during murine liver regeneration. Molecular Immunology 2008, 45:3125-3132.
118. Daveau M., Benard M., Scotte M., Schouft M.T., Hiron M., Francois A., et al. Expression of a functional C5a receptor in regenerating hepatocytes and its involvement in a proliferative signaling pathway in rat. Journal of Immunology 2004, 173:3418-3424.
119. DeAngelis R.A., Markiewski M.M., Kourtzelis I., Rafail S., Syriga M., Sandor A., et al. A complement-IL-4 regulatory circuit controls liver regeneration. Journal of Immunology 2012, 188:641-648.
120. Abu-Amara M., Yang S.Y., Tapuria N., Fuller B., Davidson B., Seifalian A. Liver ischemia/reperfusion injury: processes in inflammatory networks-a review. Liver Transplantation 2010, 16:1016-1032.
121. Hillebrandt S., Wasmuth H.E., Weiskirchen R., Hellerbrand C., Keppeler H., Werth A., et al. Complement factor 5 is a quantitative trait gene that modifies liver fibrogenesis in mice and humans. Nature Genetics 2005, 37:835-843.
122. Halangk J., Sarrazin C., Neumann K., Puhl G., Mueller T., Teuber G., et al. Evaluation of complement factor 5 variants as genetic risk factors for the development of advanced fibrosis in chronic hepatitis C infection. Journal of Hepatology 2008, 49:339-345.