Adiponectin is not required for exercise training-induced improvements in glucose and insulin tolerance in mice

Physiological Reports

Volumn 2, Issue 9, 2014, Pages

  Ritchie, Ian R W ^a   Wright, David C ^a   Dyck, David J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Adiponectin; Adiponectin knockout mice; Exercise training; Glucose and insulin tolerance; Insulin response; Skeletal muscle

Indexed keywords

ADIPONECTIN; CD36 ANTIGEN; GLUCOSE; GLUCOSE TRANSPORTER 4; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; EXERCISE; GASTROCNEMIUS MUSCLE; GENOTYPE; GLUCOSE TOLERANCE; INSULIN RESPONSE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TREADMILL EXERCISE; WESTERN BLOTTING;

EID: 84962904955     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12146     Document Type: Article

References (53)

1. Arita, Y., S. Kihara, N. Ouchi, M. Takahashi, K. Maeda, J. Miyagawa, et al. 1999. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun. 257:79–83.
2. Berg, A. H., T. P. Combs, X. Du, M. Brownlee, and P. E. Scherer. 2001. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat. Med. 7:947–953.
3. Bruce, C. R., M. J. Anderson, A. L. Carey, D. G. Newman, A. Bonen, A. D. Kriketos, et al. 2003. Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J. Clin. Endocrinol. Metab. 88:5444–5451.
4. Bruce, C. R., V. A. Mertz, G. J. Heigenhauser, and D. J. Dyck. 2005. The stimulatory effect of globular adiponectin on insulin-stimulated glucose uptake and fatty acid oxidation is impaired in skeletal muscle from obese subjects. Diabetes 54:3154–3160.
5. Cartee, G. D., and J. O. Holloszy. 1990. Exercise increases susceptibility of muscle glucose transport to activation by various stimuli. Am. J. Physiol. 258:E390–E393.
6. Cartee, G. D., D. A. Young, M. D. Sleeper, J. Zierath, H. Wallberg-Henriksson, and J. O. Holloszy. 1989. Prolonged increase in insulin-stimulated glucose transport in muscle after exercise. Am. J. Physiol. 256:E494–E499.
7. Chibalin, A. V., M. Yu, J. W. Ryder, X. M. Song, D. Galuska, A. Krook, et al. 2000. Exercise-induced changes in expression and activity of proteins involved in insulin signal transduction in skeletal muscle: differential effects on insulin-receptor substrates 1 and 2. Proc. Natl Acad. Sci. USA 97:38–43.
8. Colombo, C., M. Haluzik, J. J. Cutson, K. R. Dietz, B. Marcus-Samuels, C. Vinson, et al. 2003. Opposite effects of background genotype on muscle and liver insulin sensitivity of lipoatrophic mice. Role of triglyceride clearance. J. Biol. Chem. 278:3992–3999.
9. Combs, T. P., A. H. Berg, S. Obici, P. E. Scherer, and L. Rossetti. 2001. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J. Clin. Invest. 108:1875–1881.
10. Farias, J. M., R. M. Maggi, C. B. Tromm, L. A. Silva, T. F. Luciano, S. O. Marques, et al. 2012. Exercise training performed simultaneously to a high-fat diet reduces the degree of insulin resistance and improves adipoR1-2/APPL1 protein levels in mice. Lipids Health Dis. 11:134.
11. Frosig, C., A. J. Rose, J. T. Treebak, B. Kiens, E. A. Richter, and J. F. Wojtaszewski. 2007. Effects of endurance exercise training on insulin signaling in human skeletal muscle: interactions at the level of phosphatidylinositol 3-kinase, Akt, and AS160. Diabetes 56:2093–2102.
12. Fruebis, J., T. S. Tsao, S. Javorschi, D. Ebbets-Reed, M. R. Erickson, F. T. Yen, et al. 2001. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl Acad. Sci. USA 98:2005–2010.
13. Gao, J., E. A. Gulve, and J. O. Holloszy. 1994. Contraction-induced increase in muscle insulin sensitivity: requirement for a serum factor. Am. J. Physiol. 266:E186–E192.
14. Haluzik, M., C. Colombo, O. Gavrilova, S. Chua, N. Wolf, M. Chen, et al. 2004. Genetic background (C57BL/6J versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice. Endocrinology 145:3258–3264.
15. Holmes, B. F., D. P. Sparling, A. L. Olson, W. W. Winder, and G. L. Dohm. 2005. Regulation of muscle GLUT4 enhancer factor and myocyte enhancer factor 2 by AMP-activated protein kinase. Am. J. Physiol. Endocrinol. Metab. 289: E1071–E1076.
16. Host, H. H., P. A. Hansen, L. A. Nolte, M. M. Chen, and J. O. Holloszy. 1998. Rapid reversal of adaptive increases in muscle GLUT-4 and glucose transport capacity after training cessation. J. Appl. Physiol. 84:798–802.
17. Hotta, K., T. Funahashi, N. L. Bodkin, H. K. Ortmeyer, Y. Arita, B. C. Hansen, et al. 2001. Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes 50:1126–1133.
18. Iwabu, M., T. Yamauchi, M. Okada-Iwabu, K. Sato, T. Nakagawa, M. Funata, et al. 2010. Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature 464:1313–1319.
19. Jessen, N., R. Pold, E. S. Buhl, L. S. Jensen, O. Schmitz, and S. Lund. 2003. Effects of AICAR and exercise on insulin-stimulated glucose uptake, signaling, and GLUT-4 content in rat muscles. J. Appl. Physiol. 94:1373–1379.
20. Kandasamy, A. D., M. M. Sung, J. J. Boisvenue, A. J. Barr, and J. R. Dyck. 2012. Adiponectin gene therapy ameliorates high-fat, high-sucrose diet-induced metabolic perturbations in mice. Nutr. Diabetes 2:e45.
21. Kriketos, A. D., S. K. Gan, A. M. Poynten, S. M. Furler, D. J. Chisholm, and L. V. Campbell. 2004. Exercise increases adiponectin levels and insulin sensitivity in humans. Diabetes Care 27:629–630.
22. Kubota, N., Y. Terauchi, T. Kubota, H. Kumagai, S. Itoh, H. Satoh, et al. 2006. Pioglitazone ameliorates insulin resistance and diabetes by both adiponectin-dependent and -independent pathways. J. Biol. Chem. 281:8748–8755.
23. Kump, D. S., and F. W. Booth. 2005. Alterations in insulin receptor signalling in the rat epitrochlearis muscle upon cessation of voluntary exercise. J. Physiol. 562:829–838.
24. Li, L., R. Pan, R. Li, B. Niemann, A. C. Aurich, Y. Chen, et al. 2011. Mitochondrial biogenesis and peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) deacetylation by physical activity: intact adipocytokine signaling is required. Diabetes 60:157–167.
25. Liu, L., Y. Zhang, N. Chen, X. Shi, B. Tsang, and Y. H. Yu. 2007. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J. Clin. Invest. 117:1679–1689.
26. Ma, K., A. Cabrero, P. K. Saha, H. Kojima, L. Li, B. H. Chang, et al. 2002. Increased beta -oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J. Biol. Chem. 277:34658–34661.
27. Maeda, N., I. Shimomura, K. Kishida, H. Nishizawa, M. Matsuda, H. Nagaretani, et al. 2002. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8:731–737.
28. Mao, X., C. K. Kikani, R. A. Riojas, P. Langlais, L. Wang, F. J. Ramos, et al. 2006. APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat. Cell Biol. 8:516–523.
29. McGee, S. L., B. J. van Denderen, K. F. Howlett, J. Mollica, J. D. Schertzer, B. E. Kemp, et al. 2008. AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 57:860–867.
30. McKinsey, T. A., C. L. Zhang, and E. N. Olson. 2000. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc. Natl Acad. Sci. USA 97:14400–14405.
31. Michael, L. F., Z. Wu, R. B. Cheatham, P. Puigserver, G. Adelmant, J. J. Lehman, et al. 2001. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl Acad. Sci. USA 98:3820–3825.
32. Nawrocki, A. R., M. W. Rajala, E. Tomas, U. B. Pajvani, A. K. Saha, M. E. Trumbauer, et al. 2006. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J. Biol. Chem. 281:2654–2660.
33. Ojuka, E. O., T. E. Jones, L. A. Nolte, M. Chen, B. R. Wamhoff, M. Sturek, et al. 2002. Regulation of GLUT4 biogenesis in muscle: evidence for involvement of AMPK and Ca(2+). Am. J. Physiol. Endocrinol. Metab. 282: E1008–E1013.
34. Peterson, J. M., Z. Wei, and G. W. Wong. 2010. C1q/ TNF-related protein-3 (CTRP3), a novel adipokine that regulates hepatic glucose output. J. Biol. Chem. 285:39691–39701.
35. Peterson, J. M., S. Aja, Z. Wei, and G. W. Wong. 2012. CTRP1 protein enhances fatty acid oxidation via AMP-activated protein kinase (AMPK) activation and acetyl-CoA carboxylase (ACC) inhibition. J. Biol. Chem. 287:1576–1587.
36. Richter, E. A., and M. Hargreaves. 2013. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol. Rev. 93:993–1017.
37. Ritchie, I. R., T. L. Macdonald, D. C. Wright, and D. J. Dyck. 2014. Adiponectin is sufficient, but not required, for exercise-induced increases in the expression of skeletal muscle mitochondrial enzymes. J. Physiol. 592, 2653–2665.
38. Rose, A. J., and M. Hargreaves. 2003. Exercise increases Ca2+-calmodulin-dependent protein kinase II activity in human skeletal muscle. J. Physiol. 553:303–309.
39. Schenk, S., and J. F. Horowitz. 2007. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J. Clin. Invest. 117:1690–1698.
40. Smith, J. A., M. Collins, L. A. Grobler, C. J. Magee, and E. O. Ojuka. 2007. Exercise and CaMK activation both increase the binding of MEF2A to the Glut4 promoter in skeletal muscle in vivo. Am. J. Physiol. Endocrinol. Metab. 292:E413–E420.
41. Sriwijitkamol, A., D. K. Coletta, E. Wajcberg, G. B. Balbontin, S. M. Reyna, J. Barrientes, et al. 2007. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes 56:836–848.
42. Vu, V., Y. Liu, S. Sen, A. Xu, and G. Sweeney. 2013. Delivery of adiponectin gene to skeletal muscle using ultrasound targeted microbubbles improves insulin sensitivity and whole body glucose homeostasis. Am. J. Physiol. Endocrinol. Metab. 304:E168–E175.
43. Wallberg-Henriksson, H., S. H. Constable, D. A. Young, and J. O. Holloszy. 1988. Glucose transport into rat skeletal muscle: interaction between exercise and insulin. J. Appl. Physiol. 65:909–913.
44. Wang, C., X. Mao, L. Wang, M. Liu, M. D. Wetzel, K. L. Guan, et al. 2007. Adiponectin sensitizes insulin signaling by reducing p70 S6 kinase-mediated serine phosphorylation of IRS-1. J. Biol. Chem. 282:7991–7996.
45. Winder, W. W., B. F. Holmes, D. S. Rubink, E. B. Jensen, M. Chen, and J. O. Holloszy. 2000. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 88:2219–2226.
46. Wojtaszewski, J. F., B. F. Hansen, Gade, B. Kiens, J. F. Markuns, L. J. Goodyear, et al. 2000. Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. Diabetes 49:325–331.
47. Wong, G. W., S. A. Krawczyk, C. Kitidis-Mitrokostas, T. Revett, R. Gimeno, and H. F. Lodish. 2008. Molecular, biochemical and functional characterizations of C1q/TNF family members: adipose-tissue-selective expression patterns, regulation by PPAR-gamma agonist, cysteine-mediated oligomerizations, combinatorial associations and metabolic functions. Biochem. J. 416:161–177.
48. Wright, D. C., P. C. Geiger, D. H. Han, T. E. Jones, and J. O. Holloszy. 2007. Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J. Biol. Chem. 282:18793–18799.
49. Yamauchi, T., J. Kamon, H. Waki, Y. Terauchi, N. Kubota, K. Hara, et al. 2001. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7:941–946.
50. Yamauchi, T., J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, et al. 2002. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8:1288–1295.
51. Yamauchi, T., Y. Nio, T. Maki, M. Kobayashi, T. Takazawa, M. Iwabu, et al. 2007. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13:332–339.
52. Yano, W., N. Kubota, S. Itoh, T. Kubota, M. Awazawa, M. Moroi, et al. 2008. Molecular mechanism of moderate insulin resistance in adiponectin-knockout mice. Endocr. J. 55:515–522.
53. Zheng, Q., Y. Yuan, W. Yi, W. B. Lau, Y. Wang, X. Wang, et al. 2011. C1q/TNF-related proteins, a family of novel adipokines, induce vascular relaxation through the adiponectin receptor-1/AMPK/eNOS/nitric oxide signaling pathway. Arterioscler. Thromb. Vasc. Biol. 31:2616–2623.