nach oben

Immunologic Research

Erschienen in:

11.01.2016 | Review

The role of complement system in adipose tissue-related inflammation

verfasst von: Sonia I. Vlaicu, Alexandru Tatomir, Dallas Boodhoo, Stefan Vesa, Petru A. Mircea, Horea Rus

Erschienen in: Immunologic Research | Ausgabe 3/2016

Einloggen, um Zugang zu erhalten

Abstract

As the common factor linking adipose tissue to the metabolic context of obesity, insulin resistance and atherosclerosis are associated with a low-grade chronic inflammatory status, to which the complement system is an important contributor. Adipose tissue synthesizes complement proteins and is a target of complement activation. C3a-desArg/acylation-stimulating protein stimulates lipogenesis and affects lipid metabolism. The C3a receptor and C5aR are involved in the development of adipocytes’ insulin resistance through macrophage infiltration and the activation of adipose tissue. The terminal complement pathway has been found to be instrumental in promoting hyperglycemia-associated tissue damage, which is characteristic of the major vascular complications of diabetes mellitus and diabetic ketoacidosis. As a mediator of the effects of the terminal complement complex C5b-9, RGC-32 has an impact on energy expenditure as well as lipid and glucose metabolic homeostasis. All of this evidence, taken together, indicates an important role for complement activation in metabolic diseases.

Niculescu F, Niculescu T, Rus H. C5b-9 terminal complement complex assembly on apoptotic cells in human arterial wall with atherosclerosis. Exp Mol Pathol. 2004;76:17–23.PubMedCrossRef

Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010;11:785–97.PubMedPubMedCentralCrossRef

Vlaicu SI, Tatomir A, Rus V, Mekala AP, Mircea PA, et al. The role of complement activation in atherogenesis: the first 40 years. Immunol Res. 2015;. doi:10.1007/s12026-015-8669-6.

Dunkelberger JR, Song WC. Complement and its role in innate and adaptive immune responses. Cell Res. 2010;20:34–50.PubMedCrossRef

Cole DS, Morgan BP. Beyond lysis: how complement influences cell fate. Clin Sci (Lond). 2003;104:455–66.CrossRef

Niculescu F, Rus H. The role of complement activation in atherosclerosis. Immunol Res. 2004;30:73–80.PubMedCrossRef

Vlaicu SI, Tegla CA, Cudrici CD, Danoff J, Madani H, et al. Role of C5b-9 complement complex and response gene to complement-32 (RGC-32) in cancer. Immunol Res. 2013;56:109–21.PubMedCrossRef

Hu VW, Esser AF, Podack ER, Wisnieski BJ. The membrane attack mechanism of complement: photolabeling reveals insertion of terminal proteins into target membrane. J Immunol. 1981;127:380–6.PubMed

Laine RO, Esser AF. Detection of refolding conformers of complement protein C9 during insertion into membranes. Nature. 1989;341:63–5.PubMedCrossRef

10.

Podack ER, Tschopp J. Polymerization of the ninth component of complement (C9): formation of poly(C9) with a tubular ultrastructure resembling the membrane attack complex of complement. Proc Natl Acad Sci USA. 1982;79:574–8.PubMedPubMedCentralCrossRef

11.

Tschopp J, Podack ER, Muller-Eberhard HJ. The membrane attack complex of complement: C5b-8 complex as accelerator of C9 polymerization. J Immunol. 1985;134:495–9.PubMed

12.

Whitlow MB, Ramm LE, Mayer MM. Penetration of C8 and C9 in the C5b-9 complex across the erythrocyte membrane into the cytoplasmic space. J Biol Chem. 1985;260:998–1005.PubMed

13.

Tegla CA, Cudrici C, Patel S, Trippe R 3rd, Rus V, et al. Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol Res. 2011;51:45–60.PubMedPubMedCentralCrossRef

14.

Alexopoulos N, Katritsis D, Raggi P. Visceral adipose tissue as a source of inflammation and promoter of atherosclerosis. Atherosclerosis. 2014;233:104–12.PubMedCrossRef

15.

Richardson VR, Smith KA, Carter AM. Adipose tissue inflammation: feeding the development of type 2 diabetes mellitus. Immunobiology. 2013;218:1497–504.PubMedCrossRef

16.

Cianflone K, Maslowska M. Differentiation-induced production of ASP in human adipocytes. Eur J Clin Invest. 1995;25:817–25.PubMedCrossRef

17.

Phieler J, Garcia-Martin R, Lambris JD, Chavakis T. The role of the complement system in metabolic organs and metabolic diseases. Semin Immunol. 2013;25:47–53.PubMedPubMedCentralCrossRef

18.

Sissons JG, West RJ, Fallows J, Williams DG, Boucher BJ, et al. The complement abnormalities of lipodystrophy. N Engl J Med. 1976;294:461–5.PubMedCrossRef

19.

McLean RH, Hoefnagel D. Partial lipodystrophy and familial C3 deficiency. Hum Hered. 1980;30:149–54.PubMedCrossRef

20.

White RT, Damm D, Hancock N, Rosen BS, Lowell BB, et al. Human adipsin is identical to complement factor D and is expressed at high levels in adipose tissue. J Biol Chem. 1992;267:9210–3.PubMed

21.

Choy LN, Rosen BS, Spiegelman BM. Adipsin and an endogenous pathway of complement from adipose cells. J Biol Chem. 1992;267:12736–41.PubMed

22.

Peake PW, O’Grady S, Pussell BA, Charlesworth JA. Detection and quantification of the control proteins of the alternative pathway of complement in 3T3-L1 adipocytes. Eur J Clin Invest. 1997;27:922–7.PubMedCrossRef

23.

Mathieson PW, Wurzner R, Oliveria DB, Lachmann PJ, Peters DK. Complement-mediated adipocyte lysis by nephritic factor sera. J Exp Med. 1993;177:1827–31.PubMedCrossRef

24.

Barbu A, Hamad OA, Lind L, Ekdahl KN, Nilsson B. The role of complement factor C3 in lipid metabolism. Mol Immunol. 2015;67:101–7.PubMedCrossRef

25.

Gauvreau D, Roy C, Tom FQ, Lu H, Miegueu P, et al. A new effector of lipid metabolism: complement factor properdin. Mol Immunol. 2012;51:73–81.PubMedCrossRef

26.

Hertle E, van Greevenbroek MM, Stehouwer CD. Complement C3: an emerging risk factor in cardiometabolic disease. Diabetologia. 2012;55:881–4.PubMedPubMedCentralCrossRef

27.

MacLaren RE, Cui W, Lu H, Simard S, Cianflone K. Association of adipocyte genes with ASP expression: a microarray analysis of subcutaneous and omental adipose tissue in morbidly obese subjects. BMC Med Genomics. 2010;3:3.PubMedPubMedCentralCrossRef

28.

Moreno-Navarrete JM, Martinez-Barricarte R, Catalan V, Sabater M, Gomez-Ambrosi J, et al. Complement factor H is expressed in adipose tissue in association with insulin resistance. Diabetes. 2010;59:200–9.PubMedPubMedCentralCrossRef

29.

Gabrielsson BG, Johansson JM, Lonn M, Jernas M, Olbers T, et al. High expression of complement components in omental adipose tissue in obese men. Obes Res. 2003;11:699–708.PubMedCrossRef

30.

Gupta A, Rezvani R, Lapointe M, Poursharifi P, Marceau P, et al. Downregulation of complement C3 and C3aR expression in subcutaneous adipose tissue in obese women. PLoS ONE. 2014;9:e95478.PubMedPubMedCentralCrossRef

31.

Hillian AD, McMullen MR, Sebastian BM, Roychowdhury S, Kashyap SR, et al. Mice lacking C1q are protected from high fat diet-induced hepatic insulin resistance and impaired glucose homeostasis. J Biol Chem. 2013;288:22565–75.PubMedPubMedCentralCrossRef

32.

Diawara MR, Hue C, Wilder SP, Venteclef N, Aron-Wisnewsky J, et al. Adaptive expression of microRNA-125a in adipose tissue in response to obesity in mice and men. PLoS ONE. 2014;9:e91375.PubMedPubMedCentralCrossRef

33.

van Greevenbroek MM, Ghosh S, van der Kallen CJ, Brouwers MC, Schalkwijk CG, et al. Up-regulation of the complement system in subcutaneous adipocytes from nonobese, hypertriglyceridemic subjects is associated with adipocyte insulin resistance. J Clin Endocrinol Metab. 2012;97:4742–52.PubMedPubMedCentralCrossRef

34.

Cero C, Vostrikov VV, Verardi R, Severini C, Gopinath T, et al. The TLQP-21 peptide activates the G-protein-coupled receptor C3aR1 via a folding-upon-binding mechanism. Structure. 2014;22:1744–53.PubMedPubMedCentralCrossRef

35.

Lim J, Iyer A, Suen JY, Seow V, Reid RC, et al. C5aR and C3aR antagonists each inhibit diet-induced obesity, metabolic dysfunction, and adipocyte and macrophage signaling. Faseb J. 2013;27:822–31.PubMedCrossRef

36.

Mamane Y, Chung Chan C, Lavallee G, Morin N, Xu LJ, 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;58:2006–17.PubMedPubMedCentralCrossRef

37.

Schaffler A, Scholmerich J. Innate immunity and adipose tissue biology. Trends Immunol. 2010;31:228–35.PubMedCrossRef

38.

Blogowski W, Budkowska M, Salata D, Serwin K, Dolegowska B, et al. Clinical analysis of selected complement-derived molecules in human adipose tissue. J Transl Med. 2013;11:11.PubMedPubMedCentralCrossRef

39.

Phieler J, Chung KJ, Chatzigeorgiou A, Klotzsche-von Ameln A, Garcia-Martin R, et al. The complement anaphylatoxin C5a receptor contributes to obese adipose tissue inflammation and insulin resistance. J Immunol. 2013;191:4367–74.PubMedCrossRef

40.

Zhang J, Wright W, Bernlohr DA, Cushman SW, Chen X. Alterations of the classic pathway of complement in adipose tissue of obesity and insulin resistance. Am J Physiol Endocrinol Metab. 2007;292:E1433–40.PubMedCrossRef

41.

Fraser DA, Laust AK, Nelson EL, Tenner AJ. C1q differentially modulates phagocytosis and cytokine responses during ingestion of apoptotic cells by human monocytes, macrophages, and dendritic cells. J Immunol. 2009;183:6175–85.PubMedPubMedCentralCrossRef

42.

Alkhouri N, Gornicka A, Berk MP, Thapaliya S, Dixon LJ, et al. Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J Biol Chem. 2010;285:3428–38.PubMedPubMedCentralCrossRef

43.

Cianflone K, Zakarian R, Couillard C, Delplanque B, Despres JP, et al. Fasting acylation-stimulating protein is predictive of postprandial triglyceride clearance. J Lipid Res. 2004;45:124–31.PubMedCrossRef

44.

MacLaren R, Cui W, Cianflone K. Adipokines and the immune system: an adipocentric view. Adv Exp Med Biol. 2008;632:1–21.PubMedCrossRef

45.

Maslowska M, Sniderman AD, Germinario R, Cianflone K. ASP stimulates glucose transport in cultured human adipocytes. Int J Obes Relat Metab Disord. 1997;21:261–6.PubMedCrossRef

46.

Murray I, Sniderman AD, Cianflone K. Enhanced triglyceride clearance with intraperitoneal human acylation stimulating protein in C57BL/6 mice. Am J Physiol. 1999;277:E474–80.PubMed

47.

Murray I, Sniderman AD, Cianflone K. Mice lacking acylation stimulating protein (ASP) have delayed postprandial triglyceride clearance. J Lipid Res. 1999;40:1671–6.PubMed

48.

Badea TC, Niculescu FI, Soane L, Shin ML, Rus H. Molecular cloning and characterization of RGC-32, a novel gene induced by complement activation in oligodendrocytes. J Biol Chem. 1998;273:26977–81.PubMedCrossRef

49.

Badea T, Niculescu F, Soane L, Fosbrink M, Sorana H, et al. RGC-32 increases p34CDC2 kinase activity and entry of aortic smooth muscle cells into S-phase. J Biol Chem. 2002;277:502–8.PubMedCrossRef

50.

Tegla CA, Cudrici CD, Nguyen V, Danoff J, Kruszewski AM, et al. RGC-32 is a novel regulator of the T-lymphocyte cell cycle. Exp Mol Pathol. 2015;98:328–37.PubMedCrossRef

51.

Vlaicu SI, Cudrici C, Ito T, Fosbrink M, Tegla CA, et al. Role of response gene to complement 32 in diseases. Arch Immunol Ther Exp (Warsz). 2008;56:115–22.CrossRef

52.

Wang JN, Shi N, Xie WB, Guo X, Chen SY. Response gene to complement 32 promotes vascular lesion formation through stimulation of smooth muscle cell proliferation and migration. Arterioscler Thromb Vasc Biol. 2011;31:e19–26.PubMedPubMedCentralCrossRef

53.

Fosbrink M, Cudrici C, Tegla CA, Soloviova K, Ito T, et al. Response gene to complement 32 is required for C5b-9 induced cell cycle activation in endothelial cells. Exp Mol Pathol. 2009;86:87–94.PubMedPubMedCentralCrossRef

54.

Cui XB, Guo X, Chen SY. Response gene to complement 32 deficiency causes impaired placental angiogenesis in mice. Cardiovasc Res. 2013;99:632–9.PubMedPubMedCentralCrossRef

55.

Guo S, Philbrick MJ, An X, Xu M, Wu J. Response gene to complement 32 (RGC-32) in endothelial cells is induced by glucose and helpful to maintain glucose homeostasis. Int J Clin Exp Med. 2014;7:2541–9.PubMedPubMedCentral

56.

Cui XB, Luan JN, Ye J, Chen SY. RGC32 deficiency protects against high-fat diet-induced obesity and insulin resistance in mice. J Endocrinol. 2015;224:127–37.PubMedPubMedCentralCrossRef

57.

Ghosh P, Sahoo R, Vaidya A, Chorev M, Halperin JA. Role of complement and complement regulatory proteins in the complications of diabetes. Endocr Rev. 2015;36:272–88.PubMedCrossRef

58.

Guan LZ, Tong Q, Xu J. Elevated serum levels of mannose-binding lectin and diabetic nephropathy in type 2 diabetes. PLoS ONE. 2015;10:e0119699.PubMedPubMedCentralCrossRef

59.

Geng P, Ding Y, Qiu L, Lu Y. Serum mannose-binding lectin is a strong biomarker of diabetic retinopathy in chinese patients with diabetes. Diabetes Care. 2015;38:868–75.PubMedCrossRef

60.

Hovind P, Hansen TK, Tarnow L, Thiel S, Steffensen R, et al. Mannose-binding lectin as a predictor of microalbuminuria in type 1 diabetes: an inception cohort study. Diabetes. 2005;54:1523–7.PubMedCrossRef

61.

Jenny L, Ajjan R, King R, Thiel S, Schroeder V. Plasma levels of mannan-binding lectin-associated serine proteases MASP-1 and MASP-2 are elevated in type 1 diabetes and correlate with glycaemic control. Clin Exp Immunol. 2015;180:227–32.PubMedCrossRef

62.

Vlaicu R, Niculescu F, Rus HG, Cristea A. Immunohistochemical localization of the terminal C5b-9 complement complex in human aortic fibrous plaque. Atherosclerosis. 1985;57:163–77.PubMedCrossRef

63.

Niculescu F, Hugo F, Rus HG, Vlaicu R, Bhakdi S. Quantitative evaluation of the terminal C5b-9 complement complex by ELISA in human atherosclerotic arteries. Clin Exp Immunol. 1987;69:477–83.PubMedPubMedCentral

64.

Niculescu F, Rus HG, Vlaicu R. Activation of the human terminal complement pathway in atherosclerosis. Clin Immunol Immunopathol. 1987;45:147–55.PubMedCrossRef

65.

Rus HG, Niculescu F, Constantinescu E, Cristea A, Vlaicu R. Immunoelectron-microscopic localization of the terminal C5b-9 complement complex in human atherosclerotic fibrous plaque. Atherosclerosis. 1986;61:35–42.PubMedCrossRef

66.

Rus HG, Niculescu F, Porutiu D, Ghiurca V, Vlaicu R. Cells carrying C5b-9 complement complexes in human atherosclerotic wall. Immunol Lett. 1989;20:305–10.PubMedCrossRef

67.

Niculescu F, Badea T, Rus H. Sublytic C5b-9 induces proliferation of human aortic smooth muscle cells: role of mitogen activated protein kinase and phosphatidylinositol 3-kinase. Atherosclerosis. 1999;142:47–56.PubMedCrossRef

68.

Fosbrink M, Niculescu F, Rus V, Shin ML, Rus H. C5b-9-induced endothelial cell proliferation and migration are dependent on Akt inactivation of forkhead transcription factor FOXO1. J Biol Chem. 2006;281:19009–18.PubMedCrossRef

69.

Vasil KE, Magro CM. Cutaneous vascular deposition of C5b-9 and its role as a diagnostic adjunct in the setting of diabetes mellitus and porphyria cutanea tarda. J Am Acad Dermatol. 2007;56:96–104.PubMedCrossRef

70.

Falk RJ, Sisson SP, Dalmasso AP, Kim Y, Michael AF, et al. Ultrastructural localization of the membrane attack complex of complement in human renal tissues. Am J Kidney Dis. 1987;9:121–8.PubMedCrossRef

71.

Gerl VB, Bohl J, Pitz S, Stoffelns B, Pfeiffer N, et al. Extensive deposits of complement C3d and C5b-9 in the choriocapillaris of eyes of patients with diabetic retinopathy. Invest Ophthalmol Vis Sci. 2002;43:1104–8.PubMed

72.

Rosoklija GB, Dwork AJ, Younger DS, Karlikaya G, Latov N, et al. Local activation of the complement system in endoneurial microvessels of diabetic neuropathy. Acta Neuropathol. 2000;99:55–62.PubMedCrossRef

73.

Mellbin LG, Bjerre M, Thiel S, Hansen TK. Complement activation and prognosis in patients with type 2 diabetes and myocardial infarction: a report from the DIGAMI 2 trial. Diabetes Care. 2012;35:911–7.PubMedPubMedCentralCrossRef

74.

Qin X, Goldfine A, Krumrei N, Grubissich L, Acosta J, et al. Glycation inactivation of the complement regulatory protein CD59: a possible role in the pathogenesis of the vascular complications of human diabetes. Diabetes. 2004;53:2653–61.PubMedCrossRef

75.

Acosta J, Hettinga J, Fluckiger R, Krumrei N, Goldfine A, et al. Molecular basis for a link between complement and the vascular complications of diabetes. Proc Natl Acad Sci USA. 2000;97:5450–5.PubMedPubMedCentralCrossRef

76.

Ghosh P, Vaidya A, Sahoo R, Goldfine A, Herring N, et al. Glycation of the complement regulatory protein CD59 is a novel biomarker for glucose handling in humans. J Clin Endocrinol Metab. 2014;99:E999–1006.PubMedPubMedCentralCrossRef

77.

Krus U, King BC, Nagaraj V, Gandasi NR, Sjolander J, et al. The complement inhibitor CD59 regulates insulin secretion by modulating exocytotic events. Cell Metab. 2014;19:883–90.PubMedCrossRef

78.

Hoffman WH, Cudrici CD, Zafranskaia E, Rus H. Complement activation in diabetic ketoacidosis brains. Exp Mol Pathol. 2006;80:283–8.PubMedCrossRef

79.

Jerath RS, Burek CL, Hoffman WH, Passmore GG. Complement activation in diabetic ketoacidosis and its treatment. Clin Immunol. 2005;116:11–7.PubMedCrossRef

80.

Niculescu F, Soane L, Badea T, Shin M, Rus H. Tyrosine phosphorylation and activation of Janus kinase 1 and STAT3 by sublytic C5b-9 complement complex in aortic endothelial cells. Immunopharmacology. 1999;42:187–93.PubMedCrossRef

81.

Benzaquen LR, Nicholson-Weller A, Halperin JA. Terminal complement proteins C5b-9 release basic fibroblast growth factor and platelet-derived growth factor from endothelial cells. J Exp Med. 1994;179:985–92.PubMedCrossRef

82.

Halperin JA, Taratuska A, Nicholson-Weller A. Terminal complement complex C5b-9 stimulates mitogenesis in 3T3 cells. J Clin Invest. 1993;91:1974–8.PubMedPubMedCentralCrossRef

83.

Saleh J, Al-Wardy N, Farhan H, Al-Khanbashi M, Cianflone K. Acylation stimulating protein: a female lipogenic factor? Obes Rev. 2011;12:440–8.PubMedCrossRef

84.

Yasruel Z, Cianflone K, Sniderman AD, Rosenbloom M, Walsh M, et al. Effect of acylation stimulating protein on the triacylglycerol synthetic pathway of human adipose tissue. Lipids. 1991;26:495–9.PubMedCrossRef

85.

Cianflone K, Maslowska M, Sniderman AD. Acylation stimulating protein (ASP), an adipocyte autocrine: new directions. Semin Cell Dev Biol. 1999;10:31–41.PubMedCrossRef

86.

Murray I, Havel PJ, Sniderman AD, Cianflone K. Reduced body weight, adipose tissue, and leptin levels despite increased energy intake in female mice lacking acylation-stimulating protein. Endocrinology. 2000;141:1041–9.PubMed

87.

Murray I, Sniderman AD, Havel PJ, Cianflone K. Acylation stimulating protein (ASP) deficiency alters postprandial and adipose tissue metabolism in male mice. J Biol Chem. 1999;274:36219–25.PubMedCrossRef

88.

Xia Z, Stanhope KL, Digitale E, Simion OM, Chen L, et al. Acylation-stimulating protein (ASP)/complement C3adesArg deficiency results in increased energy expenditure in mice. J Biol Chem. 2004;279:4051–7.PubMedCrossRef

89.

Schadt EE, Lamb J, Yang X, Zhu J, Edwards S, et al. An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet. 2005;37:710–7.PubMedPubMedCentralCrossRef

90.

Munkonda MN, Lapointe M, Miegueu P, Roy C, Gauvreau D, et al. Recombinant acylation stimulating protein administration to C3-/- mice increases insulin resistance via adipocyte inflammatory mechanisms. PLoS ONE. 2012;7:e46883.PubMedPubMedCentralCrossRef

91.

Fisette A, Lapointe M, Cianflone K. Obesity-inducing diet promotes acylation stimulating protein resistance. Biochem Biophys Res Commun. 2013;437:403–7.PubMedCrossRef

92.

Paglialunga S, Schrauwen P, Roy C, Moonen-Kornips E, Lu H, et al. Reduced adipose tissue triglyceride synthesis and increased muscle fatty acid oxidation in C5L2 knockout mice. J Endocrinol. 2007;194:293–304.PubMedCrossRef

93.

Cerf ME. Beta cell dysfunction and insulin resistance. Front Endocrinol (Lausanne). 2013;4:37.

94.

Lo JC, Ljubicic S, Leibiger B, Kern M, Leibiger IB, et al. Adipsin is an adipokine that improves beta cell function in diabetes. Cell. 2014;158:41–53.PubMedPubMedCentralCrossRef

95.

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. Clin Endocrinol (Oxf). 2005;62:567–72.CrossRef

96.

Engström G, Hedblad B, Eriksson K-F, Janzon L, Lindgärde F. Complement C3 is a risk factor for the development of diabetes: a population-based cohort study. Diabetes. 2005;54:570–5.PubMedCrossRef

97.

Engstrom G, Hedblad B, Janzon L, Lindgarde F. Weight gain in relation to plasma levels of complement factor 3: results from a population-based cohort study. Diabetologia. 2005;48:2525–31.PubMedCrossRef

98.

Nilsson B, Hamad OA, Ahlstrom H, Kullberg J, Johansson L, et al. C3 and C4 are strongly related to adipose tissue variables and cardiovascular risk factors. Eur J Clin Invest. 2014;44:587–96.PubMedCrossRef

99.

Onat A, Uyarel H, Hergenc G, Karabulut A, Albayrak S, et al. Determinants and definition of abdominal obesity as related to risk of diabetes, metabolic syndrome and coronary disease in Turkish men: a prospective cohort study. Atherosclerosis. 2007;191:182–90.PubMedCrossRef

100.

Qin X, Lu Y, Yang X, Peng Q, Wang J, et al. Determination of reference intervals for serum complement C3 and C4 levels in Chinese Han ethnic males. Clin Lab. 2014;60:775–81.PubMed

101.

Warnberg J, Nova E, Moreno LA, Romeo J, Mesana MI, et al. Inflammatory proteins are related to total and abdominal adiposity in a healthy adolescent population: the AVENA Study. Am J Clin Nutr. 2006;84:505–12.PubMed

102.

Hernandez-Mijares A, Jarabo-Bueno MM, Lopez-Ruiz A, Sola-Izquierdo E, Morillas-Arino C, et al. Levels of C3 in patients with severe, morbid and extreme obesity: its relationship to insulin resistance and different cardiovascular risk factors. Int J Obes (Lond). 2007;31:927–32.CrossRef

103.

Oberbach A, Bluher M, Wirth H, Till H, Kovacs P, et al. Combined proteomic and metabolomic profiling of serum reveals association of the complement system with obesity and identifies novel markers of body fat mass changes. J Proteome Res. 2011;10:4769–88.PubMedCrossRef

104.

Sleddering MA, Markvoort AJ, Dharuri HK, Jeyakar S, Snel M, et al. Proteomic analysis in type 2 diabetes patients before and after a very low calorie diet reveals potential disease state and intervention specific biomarkers. PLoS ONE. 2014;9:e112835.PubMedPubMedCentralCrossRef

105.

Nestvold TK, Nielsen EW, Ludviksen JK, Fure H, Landsem A, et al. Lifestyle changes followed by bariatric surgery lower inflammatory markers and the cardiovascular risk factors C3 and C4. Metab Syndr Relat Disord. 2015;13:29–35.PubMedCrossRef

106.

Wlazlo N, van Greevenbroek MM, Ferreira I, Jansen EJ, Feskens EJ, et al. Low-grade inflammation and insulin resistance independently explain substantial parts of the association between body fat and serum C3: the CODAM study. Metabolism. 2012;61:1787–96.PubMedCrossRef

107.

Phillips CM, Kesse-Guyot E, Ahluwalia N, McManus R, Hercberg S, et al. Dietary fat, abdominal obesity and smoking modulate the relationship between plasma complement component 3 concentrations and metabolic syndrome risk. Atherosclerosis. 2012;220:513–9.PubMedCrossRef

108.

Wlazlo N, van Greevenbroek MM, Ferreira I, Feskens EJ, van der Kallen CJ, et al. Complement factor 3 is associated with insulin resistance and with incident type 2 diabetes over a 7-year follow-up period: the CODAM Study. Diabetes Care. 2014;37:1900–9.PubMedCrossRef

109.

De Pergola G, Tartagni M, Bartolomeo N, Bruno I, Masiello M, et al. Possible direct influence of complement 3 in decreasing insulin sensitivity in a cohort of overweight and obese subjects. Endocr Metab Immune Disord Drug Targets. 2013;13:301–5.PubMedCrossRef

110.

Muscari A, Antonelli S, Bianchi G, Cavrini G, Dapporto S, et al. Serum C3 is a stronger inflammatory marker of insulin resistance than C-reactive protein, leukocyte count, and erythrocyte sedimentation rate: comparison study in an elderly population. Diabetes Care. 2007;30:2362–8.PubMedCrossRef

111.

Muscari A, Bozzoli C, Puddu GM, Sangiorgi Z, Dormi A, et al. Association of serum C3 levels with the risk of myocardial infarction. Am J Med. 1995;98:357–64.PubMedCrossRef

112.

Vidigal Fde C, Ribeiro AQ, Babio N, Salas-Salvado J, Bressan J. Prevalence of metabolic syndrome and pre-metabolic syndrome in health professionals: LATINMETS Brazil study. Diabetol Metab Syndr. 2015;7:6.PubMedCrossRef

113.

Onat A, Can G, Rezvani R, Cianflone K. Complement C3 and cleavage products in cardiometabolic risk. Clin Chim Acta. 2011;412:1171–9.PubMedCrossRef

114.

Van Harmelen V, Reynisdottir S, Cianflone K, Degerman E, Hoffstedt J, et al. Mechanisms involved in the regulation of free fatty acid release from isolated human fat cells by acylation-stimulating protein and insulin. J Biol Chem. 1999;274:18243–51.PubMedCrossRef

115.

Ahren B, Havel PJ, Pacini G, Cianflone K. Acylation stimulating protein stimulates insulin secretion. Int J Obes Relat Metab Disord. 2003;27:1037–43.PubMedCrossRef

116.

Saleh J, Wahab RA, Farhan H, Al-Amri I, Cianflone K. Plasma levels of acylation-stimulating protein are strongly predicted by waist/hip ratio and correlate with decreased LDL size in men. ISRN Obes. 2013;2013:342802.PubMedPubMedCentral

117.

Yang Y, Lu HL, Zhang J, Yu HY, Wang HW, et al. Relationships among acylation stimulating protein, adiponectin and complement C3 in lean vs obese type 2 diabetes. Int J Obes (Lond). 2006;30:439–46.CrossRef

118.

Cianflone K, Zhang XJ, Genest J Jr, Sniderman A. Plasma acylation-stimulating protein in coronary artery disease. Arterioscler Thromb Vasc Biol. 1997;17:1239–44.PubMed

119.

Weyer C, Pratley RE. Fasting and postprandial plasma concentrations of acylation-stimulation protein (ASP) in lean and obese Pima Indians compared to Caucasians. Obes Res. 1999;7:444–52.PubMedCrossRef

120.

Wamba PC, Mi J, Zhao XY, Zhang MX, Wen Y, et al. Acylation stimulating protein but not complement C3 associates with metabolic syndrome components in Chinese children and adolescents. Eur J Endocrinol. 2008;159:781–90.PubMedCrossRef

121.

Fujita T, Hemmi S, Kajiwara M, Yabuki M, Fuke Y, et al. Complement-mediated chronic inflammation is associated with diabetic microvascular complication. Diabetes Metab Res Rev. 2013;29:220–6.PubMedCrossRef

122.

Somani R, Richardson VR, Standeven KF, Grant PJ, Carter AM. Elevated properdin and enhanced complement activation in first-degree relatives of South Asian subjects with type 2 diabetes. Diabetes Care. 2012;35:894–9.PubMedPubMedCentralCrossRef

123.

Uza G, Cristea A, Cucuianu MP. Increased level of the complement C3 protein in endogenous hypertriglyceridemia. J Clin Lab Immunol. 1982;8:101–5.PubMed

124.

Vaisar T, Pennathur S, Green PS, Gharib SA, Hoofnagle AN, et al. Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J Clin Invest. 2007;117:746–56.PubMedPubMedCentralCrossRef

Titel: The role of complement system in adipose tissue-related inflammation
verfasst von: Sonia I. Vlaicu
Alexandru Tatomir
Dallas Boodhoo
Stefan Vesa
Petru A. Mircea
Horea Rus
Publikationsdatum: 11.01.2016
Verlag: Springer US
Erschienen in: Immunologic Research / Ausgabe 3/2016
Print ISSN: 0257-277X
Elektronische ISSN: 1559-0755
DOI: https://doi.org/10.1007/s12026-015-8783-5

Neu im Fachgebiet HNO

Erhebliches Risiko für Kehlkopfkrebs bei mäßiger Dysplasie

29.05.2024 Larynxkarzinom Nachrichten

Fast ein Viertel der Personen mit mäßig dysplastischen Stimmlippenläsionen entwickelt einen Kehlkopftumor. Solche Personen benötigen daher eine besonders enge ärztliche Überwachung.

Hörschwäche erhöht Demenzrisiko unabhängig von Beta-Amyloid

29.05.2024 Hörstörungen Nachrichten

Hört jemand im Alter schlecht, nimmt das Hirn- und Hippocampusvolumen besonders schnell ab, was auch mit einem beschleunigten kognitiven Abbau einhergeht. Und diese Prozesse scheinen sich unabhängig von der Amyloidablagerung zu ereignen.

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

17.05.2024 Klinik aktuell Nachrichten

Sie sei „ethisch geboten“, meint Gesundheitsminister Karl Lauterbach: mehr Transparenz über die Qualität von Klinikbehandlungen. Um sie abzubilden, lässt er gegen den Widerstand vieler Länder einen virtuellen Klinik-Atlas freischalten.

Betalaktam-Allergie: praxisnahes Vorgehen beim Delabeling

16.05.2024 Pädiatrische Allergologie Nachrichten

Die große Mehrheit der vermeintlichen Penicillinallergien sind keine. Da das „Etikett“ Betalaktam-Allergie oft schon in der Kindheit erworben wird, kann ein frühzeitiges Delabeling lebenslange Vorteile bringen. Ein Team von Pädiaterinnen und Pädiatern aus Kanada stellt vor, wie sie dabei vorgehen.

Update HNO

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.

Newsletter bestellen

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

The role of complement system in adipose tissue-related inflammation

Abstract

Neu im Fachgebiet HNO

Erhebliches Risiko für Kehlkopfkrebs bei mäßiger Dysplasie

Hörschwäche erhöht Demenzrisiko unabhängig von Beta-Amyloid

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

Betalaktam-Allergie: praxisnahes Vorgehen beim Delabeling

Update HNO

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2016

The balance of the immune system between HLA-G and NK cells in unexplained recurrent spontaneous abortion and polymorphisms analysis

Targeting polo-like kinase 1 suppresses essential functions of alloreactive T cells

The immunosuppressive domain of the transmembrane envelope protein gp41 of HIV-1 binds to human monocytes and B cells

Th9 and Th22 immune response in young patients with type 1 diabetes

Production of porcine TNFα by ADAM17-mediated cleavage negatively regulates porcine reproductive and respiratory syndrome virus infection

Autoimmunity and dysmetabolism of human acquired immunodeficiency syndrome

Neu im Fachgebiet HNO

Erhebliches Risiko für Kehlkopfkrebs bei mäßiger Dysplasie

Hörschwäche erhöht Demenzrisiko unabhängig von Beta-Amyloid

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

Betalaktam-Allergie: praxisnahes Vorgehen beim Delabeling

Update HNO