Selective activation of PPARγ in skeletal muscle induces endogenous production of adiponectin and protects mice from diet-induced insulin resistance

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 1, 2010, Pages

  Amin, Rajesh H ^a   Mathews, Suresh T ^a   Camp, Heidi S ^b   Ding, Liyun ^b   Leff, Todd ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PFIZER INC   (United States)

Author keywords

Adiponectin; Diabetes; Peroxisome proliferator activated receptor ; Skeletal muscle; Transgenic mice

Indexed keywords

ADIPONECTIN; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ADIPONECTIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE ACTIVATION; GLUCOSE HOMEOSTASIS; INSULIN RESISTANCE; LIPID DIET; MALE; MOUSE; MUSCLE CELL; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; ANIMAL; AUTOCRINE EFFECT; C57BL MOUSE; CYTOLOGY; FAT INTAKE; GENE EXPRESSION; GENETICS; GLUCOSE BLOOD LEVEL; HEART MUSCLE CELL; HOMEOSTASIS; METABOLISM; PHENOTYPE; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; SKELETAL MUSCLE SATELLITE CELL; TRANSGENIC MOUSE;

ADIPONECTIN; ANIMALS; AUTOCRINE COMMUNICATION; BLOOD GLUCOSE; CELLS, CULTURED; DIETARY FATS; GENE EXPRESSION; HOMEOSTASIS; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUTAGENESIS, SITE-DIRECTED; MYOCYTES, CARDIAC; PHENOTYPE; PPAR GAMMA; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 73649126161     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00446.2009     Document Type: Article

References (38)

1. Arany Z, Sellers WR, Livingston DM, Eckner R. E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators. Cell 77: 799-800, 1994.
2. Blau HM, Webster C. Isolation and characterization of human muscle cells. Proc Natl Acad Sci USA 78: 5623-5627, 1981.
3. Braissant O, Foufelle F, Scotto C, Dauca M, Wahli W. Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat. Endocrinology 137: 354-366, 1996.
4. Brooke MH, Kaiser KK. Three "myosin adenosine triphosphatase" systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18: 670-672, 1970.
5. Burant CF, Sreenan S, Hirano K, Tai TA, Lohmiller J, Lukens J, Davidson NO, Ross S, Graves RA. Troglitazone action is independent of adipose tissue. J Clin Invest 100: 2900-2908, 1997.
6. Camp HS, Tafuri SR. Regulation of peroxisome proliferator- activated receptor gamma activity by mitogen-activated protein kinase. J Biol Chem 272: 10811-10816, 1997.
7. Camp HS, Tafuri SR, Leff T. c-Jun N-terminal kinase phosphorylates peroxisome proliferator-activated receptor-gamma1 and negatively regulates its transcriptional activity. Endocrinology 140: 392-397, 1999.
8. Chao L, Marcus-Samuels B, Mason MM, Moitra J, Vinson C, Arioglu E, Gavrilova O, Reitman ML. Adipose tissue is required for the antidiabetic, but not for the hypolipidemic, effect of thiazolidinediones. J Clin Invest 106: 1221-1228, 2000.
9. Ciaraldi TP, Gilmore A, Olefsky JM, Goldberg M, Heidenreich KA. In vitro studies on the action of CS-045, a new antidiabetic agent. Metab Clin Exp 39: 1056-1062, 1990.
10. Civitarese AE, Ukropcova B, Carling S, Hulver M, DeFronzo RA, Mandarino L, Ravussin E, Smith SR. Role of adiponectin in human skeletal muscle bioenergetics. Cell Metab 4: 75-87, 2006.
11. Delaigle AM, Jonas JC, Bauche IB, Cornu O, Brichard SM. Induction of adiponectin in skeletal muscle by inflammatory cytokines: in vivo and in vitro studies. Endocrinology 145: 5589-5597, 2004.
12. Delaigle AM, Senou M, Guiot Y, Many MC, Brichard SM. Induction of adiponectin in skeletal muscle of type 2 diabetic mice: In vivo and in vitro studies. Diabetologia 49: 1311-1323, 2006.
13. Ding G, Qin Q, He N, Francis-David SC, Hou J, Liu J, Ricks E, Yang Q. Adiponectin and its receptors are expressed in adult ventricular cardiomyocytes and upregulated by activation of peroxisome proliferator- activated receptor gamma. J Mol Cell Cardiol 43: 73-84, 2007.
14. Dubowitz V, Brooke MH. Muscle Biopsy: A Modern Approach. Philadelphia, PA: Saunders, 1973.
15. Eckner R, Ewen ME, Newsome D, Gerdes M, DeCaprio JA, Lawrence JB, Livingston DM. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev 8: 869-884, 1994.
16. Fu Y, Luo N, Klein RL, Garvey WT. Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J Lipid Res 46: 1369-1379, 2005.
17. Gross B, Staels B. PPAR agonists: multimodal drugs for the treatment of type-2 diabetes. Best Pract Res Clin Endocrinol Metab 21: 687-710, 2007.
18. He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, Evans RM. Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 100: 15712-15717, 2003.
19. Hevener AL, He W, Barak Y, Le J, Bandyopadhyay G, Olson P, Wilkes J, Evans RM, Olefsky J. Muscle-specific Pparg deletion causes insulin resistance. Nat Med 9: 1491-1497, 2003.
20. Hu E, Kim JB, Sarraf P, Spiegelman BM. Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARgamma. Science 274: 2100-2103, 1996.
21. Ingelsson E, Arnlov J, Zethelius B, Vasan RS, Flyvbjerg A, Frystyk J, Berne C, Hanni A, Lind L, Sundstrom J. Associations of serum adiponectin with skeletal muscle morphology and insulin sensitivity. J Clin Endocrinol Metab 94: 953-957, 2009.
22. Krause MP, Liu Y, Vu V, Chan L, Xu A, Riddell MC, Sweeney G, Hawke TJ. Adiponectin is expressed by skeletal muscle fibers and influences muscle phenotype and function. Am J Physiol Cell Physiol 295: C203-C212, 2008.
23. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 270: 12953-12956, 1995.
24. Liao Y, Takashima S, Maeda N, Ouchi N, Komamura K, Shimomura I, Hori M, Matsuzawa Y, Funahashi T, Kitakaze M. Exacerbation of heart failure in adiponectin-deficient mice due to impaired regulation of AMPK and glucose metabolism. Cardiovasc Res 67: 705-713, 2005.
25. Liu Y, Chewchuk S, Lavigne C, Brule S, Pilon G, Houde V, Xu A, Marette A, Sweeney G. Functional significance of skeletal muscle adiponectin production, changes in animal models of obesity and diabetes and regulation by rosiglitazone treatment. Am J Physiol Endocrinol Metab 297: E657-E664, 2009.
26. Loviscach M, Rehman N, Carter L, Mudaliar S, Mohadeen P, Ciaraldi TP, Veerkamp JH, Henry RR. Distribution of peroxisome proliferator-activated receptors (PPARs) in human skeletal muscle and adipose tissue: relation to insulin action. Diabetologia 43: 304-311, 2000.
27. Machann J, Haring H, Schick F, Stumvoll M. Intramyocellular lipids and insulin resistance. Diabet Obes Metab 6: 239-248, 2004.
28. Niederbichler AD, Hoesel LM, Westfall MV, Gao H, Ipaktchi KR, Sun L, Zetoune FS, Su GL, Arbabi S, Sarma JV, Wang SC, Hemmila MR, Ward PA. An essential role for complement C5a in the pathogenesis of septic cardiac dysfunction. J Exp Med 203: 53-61, 2006.
29. Norris AW, Chen L, Fisher SJ, Szanto I, Ristow M, Jozsi AC, Hirshman MF, Rosen ED, Goodyear LJ, Gonzalez FJ, Spiegelman BM, Kahn CR. Muscle-specific PPARgamma-deficient mice develop increased adiposity and insulin resistance but respond to thiazolidinediones. J Clin Invest 112: 608-618, 2003.
30. Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schon MR, Bluher M, Punkt K. Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29: 895-900, 2006.
31. Oh DK, Ciaraldi T, Henry RR. Adiponectin in health and disease. Diabet Obes Metab 9: 282-289, 2007.
32. Olefsky JM, Saltiel AR. PPAR gamma and the treatment of insulin resistance. Trends Endocrinol Metab 11: 362-368, 2000.
33. Piñeiro R, Iglesias MJ, Gallego R, Raghay K, Eiras S, Rubio J, Diéguez C, Gualillo O, González-Juanatey JR, Lago F. Adiponectin is synthesized and secreted by human and murine cardiomyocytes. FEBS Lett 579: 5163-5169, 2005.
34. Shibata R, Sato K, Pimentel DR, Takemura Y, Kihara S, Ohashi K, Funahashi T, Ouchi N, Walsh K. Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat Med 11: 1096-1103, 2005.
35. Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77: 289-312, 2008.
36. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8: 1288-1295, 2002.
37. Yoon MJ, Lee GY, Chung JJ, Ahn YH, Hong SH, Kim JB. Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes 55: 2562-2570, 2006.
38. Yu JG, Javorschi S, Hevener AL, Kruszynska YT, Norman RA, Sinha M, Olefsky JM. The effect of thiazolidinediones on plasma adiponectin levels in normal, obese, and type 2 diabetic subjects. Diabetes 51: 2968-2974, 2002.