C5L2 receptor disruption enhances the development of diet-induced insulin resistance in mice

Immunobiology

Volumn 218, Issue 1, 2013, Pages 127-133

  Fisette, Alexandre ^a   Munkonda, Mercedes N ^a   Oikonomopoulou, Katerina ^b   Paglialunga, Sabina ^c   Lambris, John D ^b   Cianflone, Katherine ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Adipokine; Complement; Diabetes; Inflammation; Obesity

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; ADIPOCYTOKINE RECEPTOR; C5L2 RECEPTOR; INSULIN; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; LIPID; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET; EX VIVO STUDY; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; IN VIVO STUDY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIVER; MACROPHAGE; METABOLISM; MOUSE; NONHUMAN; OBESITY; OXIDATION; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

ADIPOSE TISSUE; ANIMALS; BODY FAT DISTRIBUTION; CELLS, CULTURED; CYTOKINES; DIET; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; OBESITY; RECEPTORS, CHEMOKINE; TRIGLYCERIDES;

EID: 84870293902     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.04.001     Document Type: Article

References (36)

1. Ahren B., Havel P.J., Pacini G., Cianflone K. Acylation stimulating protein stimulates insulin secretion. Int. J. Obes. 2003, 27:1037-1043.
2. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
3. Chen N.J., Mirtsos C., Suh D., Lu Y.C., Lin W.J., McKerlie C., Lee T., Baribault H., Tian H., Yeh W.C. C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 2007, 446:203-207.
4. Cianflone K. Acylation stimulating protein and triacylglycerol synthesis: potential drug targets?. Curr. Pharm. Des. 2003, 9:1397-1410.
5. Cianflone K., Xia Z.N., Chen L.Y. Critical review of acylation-stimulating protein physiology in humans and rodents. Biochim. Biophys. Acta 2003, 1609:127-143.
6. Cui W., Lapointe M., Gauvreau D., Kalant D., Cianflone K. Recombinant C3adesArg/acylation stimulating protein (ASP) is highly bioactive: a critical evaluation of C5L2 binding and 3T3-L1 adipocyte activation. Mol. Immunol. 2009, 46:3207-3217.
7. Cui W., Paglialunga S., Kalant D., Lu H., Roy C., Laplante M., Deshaies Y., Cianflone K. Acylation-stimulating protein/C5L2-neutralizing antibodies alter triglyceride metabolism in vitro and in vivo. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1482-E1491.
8. Faraj M., Sniderman A.D., Cianflone K. ASP enhances in situ lipoprotein lipase activity by increasing fatty acid trapping in adipocytes. J. Lipid Res. 2004, 45:657-666.
9. Fisette A., Cianflone K. The ASP and C5L2 pathway: another bridge between inflammation and metabolic homeostasis. Clin. Lipidol. 2010, 5:367-377.
10. Franckhauser S., Elias I., Sopasakis V.R., Ferre T., Nagaev I., Andersson C.X., Agudo J., Ruberte J., Bosch F., Smith U. Overexpression of Il6 leads to hyperinsulinaemia, liver inflammation and reduced body weight in mice. Diabetologia 2008, 51:1306-1316.
11. Goldberg I.J., Eckel R.H., Abumrad N.A. Regulation of fatty acid uptake into tissues: lipoprotein lipase- and CD36-mediated pathways. J. Lipid Res. 2009, 50:S86-S90.
12. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
13. Johswich K., Klos A. C5L2-an anti-inflammatory molecule or a receptor for acylation stimulating protein (C3a-desArg)?. Adv. Exp. Med. Biol. 2007, 598:159-180.
14. Kahn B.B., Flier J.S. Obesity and insulin resistance. J. Clin. Invest. 2000, 106:473-481.
15. 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-Arg(77)/acylation-stimulating protein. J. Biol. Chem. 2003, 278:11123-11129.
16. Kalant D., MacLaren R., Cui W., Samanta R., Monk P.N., Laporte S.A., Cianflone K. C5L2 is a functional receptor for acylation-stimulating protein. J. Biol. Chem. 2005, 280:23936-23944.
17. Kim J.K., Fillmore J.J., Chen Y., Yu C.L., Moore I.K., Pypaert M., Lutz E.P., Kako Y., Velez-Carrasco W., Goldberg I.J., Breslow J.L., Shulman G.I. Tissue-specific overexpression of lipoprotein lipase causes tissue-specific insulin resistance. Proc. Natl. Acad. Sci. U.S.A. 2001, 7522-7527.
18. Kotani K., Peroni O.D., Minokoshi Y., Boss O., Kahn B.B. GLUT4 glucose transporter deficiency increases hepatic lipid production and peripheral lipid utilization. J. Clin. Invest. 2004, 114:1666-1675.
19. Langer H.F., Chung K.J., Orlova V.V., Choi E.Y., Kaul S., Kruhlak M.J., Alatsatianos M., DeAngelis R.A., Roche P.A., Magotti P., Li X.R., Economopoulou M., Rafail S., Lambris J.D., Chavakis T. Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis. Blood 2010, 116:4395-4403.
20. Ma L.J., Mao S.L., Taylor K.L., Kanjanabuch T., Guan Y.F., Zhang Y.H., Brown N.J., Swift L.L., McGuinness O.P., Wasserman D.H., Vaughan D.E., Fogo A.B. Prevention of obesity and insulin resistance in mice lacking plasminogen activator inhibitor 1. Diabetes 2004, 53:336-346.
21. Marcus F., Hosey M.M. Purification and properties of liver fructose 1,6-bisphosphatase from C57Bl-Ksj normal and diabetic mice. J. Biol. Chem. 1980, 255:2481-2486.
22. Maslowska M., Sniderman A.D., Germinario R., Cianflone K. ASP stimulates glucose transport in cultured human adipocytes. Int. J. Obes. 1997, 21:261-266.
23. Murray I., Sniderman A.D., Cianflone K. Enhanced triglyceride clearance with intraperitoneal human acylation stimulating protein in C57BL/6 mice. Am. J. Physiol. Endocrinol. Metab. 1999, 277:E474-E480.
24. Murray I., Sniderman A.D., Cianflone K. Mice lacking acylation stimulating protein (ASP) have delayed postprandial triglyceride clearance. J. Lipid Res. 1999, 40:1671-1676.
25. Onat A., Can G., Rezvani R., Cianflone K. Complement C3 and cleavage products in cardiometabolic risk. Clin. Chim. Acta 2011, 412:1171-1179.
26. Paglialunga S., Fisette A., Munkonda M., Gao Y., Richard D., Cianflone K. The effects of acylation stimulating protein supplementation vs antibody neutralization on energy expenditure in wild type mice. BMC Physiol. 2010, 10.
27. Paglialunga S., Schrauwen P., Roy C., Moonen-Kornips E., Lu H., Hesselink M.K.C., Deshaies Y., Richard D., Cianflone K. Reduced adipose tissue triglyceride synthesis and increased muscle fatty acid oxidation in C5L2 knockout mice. J. Endocrinol. 2007, 194:293-304.
28. Roy C., Paglialunga S., Fisette A., Schrauwen P., Moonen-Kornips E., St Onge J., Hesselink M.K., Richard D., Joanisse D.R., Cianflone K. Shift in metabolic fuel in acylation-stimulating protein-deficient mice following a high-fat diet. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E1051-E1059.
29. 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. Mol. Immunol. 2009, 46:1149-1162.
30. Smith S.J., Cases S., Jensen D.R., Chen H.C., Sande E., Tow B., Sanan D.A., Raber J., Eckel R.H., Farese R.V. Obesity resistance and multiple mechanisms of triglyceride synthesis in mice lacking Dgat. Nat. Genet. 2000, 25:87-90.
31. Tao Y.H., Cianflone K., Sniderman A.D., Colby-Germinario S.P., Germinario R.J. Acylation-stimulating protein (ASP) regulates glucose transport in the rat L6 muscle cell line. Biochim. Biophys. Acta 1997, 1344:221-229.
32. Van Hermelen V., Reynisdottir S., Cianflone K., Degerman E., Hoffstedt J., Nilsell K., Sniderman A., Arner P. 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, 274:18243-18251.
33. Wernstedt I., Olsson B., Jernas M., Paglialunga S., Carlsson L.M.S., Smith U., Cianflone K., Wallenius K., Wallenius V. Increased levels of acylation-stimulating protein in interleukin-6-deficient (IL-6(-/-)) mice. Endocrinology 2006, 147:2690-2695.
34. Xia Z., Sniderman A.D., Cianflone K. Acylation-stimulating protein (ASP) deficiency induces obesity resistance and increased energy expenditure in ob/ob mice. J. Biol. Chem. 2002, 277:45874-45879.
35. Xia Z.N., Stanhope K.L., Digitale E., Simion O.M., Chen L.Y., Havel P., Cianflone K. Acylation-stimulating protein (ASP)/complement C3adesArg deficiency results in increased energy expenditure in mice. J. Biol. Chem. 2004, 279:4051-4057.
36. 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.