Insulin Receptor Substrates Irs1 and Irs2 Coordinate Skeletal Muscle Growth and Metabolism via the Akt and AMPK Pathways

REFERENCES

• Abbud, W., et al. 2000. Stimulation of AMP-activated protein kinase (AMPK) is associated with enhancement of Glut1-mediated glucose transport. Arch. Biochem. Biophys. 380:347–352.
   PubMedGoogle Scholar
• Araki, E., et al. 1994. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372:186–190.
   PubMed Web of Science ®Google Scholar
• Barnes, B. R., et al. 2005. 5′-AMP-activated protein kinase regulates skeletal muscle glycogen content and ergogenics. FASEB J. 19:773–779.
   PubMed Web of Science ®Google Scholar
• Barnes, K., et al. 2002. Activation of GLUT1 by metabolic and osmotic stress: potential involvement of AMP-activated protein kinase (AMPK). J. Cell Sci. 115:2433–2442.
   PubMedGoogle Scholar
• Bassel-Duby, R., and E. N. Olson. 2006. Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 75:19–37.
   PubMed Web of Science ®Google Scholar
• Bastie, C. C., et al. 2005. FoxO1 stimulates fatty acid uptake and oxidation in muscle cells through CD36-dependent and -independent mechanisms. J. Biol. Chem. 280:14222–14229.
   PubMed Web of Science ®Google Scholar
• Bentzinger, C. F., et al. 2008. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab. 8:411–424.
   PubMed Web of Science ®Google Scholar
• Bruning, J. C., et al. 1998. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell 2:559–569.
   PubMed Web of Science ®Google Scholar
• Cheng, Z., et al. 2009. Foxo1 integrates insulin signaling with mitochondrial function in the liver. Nat. Med. 15:1307–1311.
   PubMed Web of Science ®Google Scholar
• Cho, H., et al. 2001. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292:1728–1731.
   PubMed Web of Science ®Google Scholar
• Copps, K. D., et al. 2010. Irs1 serine 307 promotes insulin sensitivity in mice. Cell Metab. 11:84–92.
   PubMed Web of Science ®Google Scholar
• Cross, D. A. E., et al. 1997. Insulin activates protein kinase B, inhibits glycogen synthase kinase-3 and activates glycogen synthase by rapamycin-insensitive pathways in skeletal muscle and adipose tissue. Growth Regul. 406:211–215.
   Google Scholar
• Dong, X. C., et al. 2008. Inactivation of hepatic Foxo1 by insulin signaling is required for adaptive nutrient homeostasis and endocrine growth regulation. Cell Metab. 8:65–76.
   PubMed Web of Science ®Google Scholar
• Frayn, K. N. 2003. The glucose-fatty acid cycle: a physiological perspective. Biochem. Soc. Trans. 31 (Pt. 6):1115–1119.
   PubMed Web of Science ®Google Scholar
• Fujii, N., N. Jessen, and L. J. Goodyear. 2006. AMP-activated protein kinase and the regulation of glucose transport. Am. J. Physiol. Endocrinol. Metab. 291:E867–E877.
   PubMedGoogle Scholar
• Furuyama, T., K. Kitayama, H. Yamashita, and N. Mori. 2003. Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem. J. 375:365–371.
   PubMed Web of Science ®Google Scholar
• Garofalo, R. S., et al. 2003. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J. Clin. Invest. 112:197–208.
   PubMed Web of Science ®Google Scholar
• Gazdag, A. C., C. L. Dumke, C. R. Kahn, and G. D. Cartee. 1999. Calorie restriction increases insulin-stimulated glucose transport in skeletal muscle from IRS-1 knockout mice. Diabetes 48:1930–1936.
   PubMedGoogle Scholar
• Glass, D. J. 2003. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat. Cell Biol. 5:87–90.
   PubMed Web of Science ®Google Scholar
• Goldberg, A. L. 2007. Functions of the proteasome: from protein degradation and immune surveillance to cancer therapy. Biochem. Soc. Trans. 35:12–17.
   PubMed Web of Science ®Google Scholar
• Greer, E. L., M. R. Banko, and A. Brunet. 2009. AMP-activated protein kinase and FoxO transcription factors in dietary restriction-induced longevity. Ann. N. Y. Acad. Sci. 1170:688–692.
   PubMed Web of Science ®Google Scholar
• Guo, S., et al. 2009. The Irs1 branch of the insulin signaling cascade plays a dominant role in hepatic nutrient homeostasis. Mol. Cell. Biol. 29:5070–5083.
   PubMed Web of Science ®Google Scholar
• Gwinn, D. M., et al. 2008. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30:214–226.
   PubMed Web of Science ®Google Scholar
• Higaki, Y., et al. 1999. Insulin receptor substrate-2 is not necessary for insulin- and exercise-stimulated glucose transport in skeletal muscle. J. Biol. Chem. 274:20791–20795.
   PubMed Web of Science ®Google Scholar
• Howlett, K. F., et al. 2002. Insulin signaling after exercise in insulin receptor substrate-2-deficient mice. Diabetes 51:479–483.
   PubMedGoogle Scholar
• Huang, J., and B. D. Manning. 2008. The TSC1-TSC2 complex: a molecular switchboard controlling cell growth. Biochem. J. 412:179–190.
   PubMed Web of Science ®Google Scholar
• Kahn, B. B., T. Alquier, D. Carling, and D. G. Hardie. 2005. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1:15–25.
   PubMed Web of Science ®Google Scholar
• Kamei, Y., et al. 2004. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J. Biol. Chem. 39:41114–41123.
   Google Scholar
• Karlsson, H. K., and J. R. Zierath. 2007. Insulin signaling and glucose transport in insulin resistant human skeletal muscle. Cell Biochem. Biophys. 48:103–113.
   PubMed Web of Science ®Google Scholar
• Kelley, D. E. 2005. Skeletal muscle fat oxidation: timing and flexibility are everything. J. Clin. Invest. 7:1699–1702.
   Google Scholar
• Kubota, N., et al. 2008. Dynamic functional relay between insulin receptor substrate 1 and 2 in hepatic insulin signaling during fasting and feeding. Cell Metab. 8:49–64.
   PubMed Web of Science ®Google Scholar
• Kumar, A., et al. 2008. Muscle-specific deletion of rictor impairs insulin-stimulated glucose transport and enhances basal glycogen synthase activity. Mol. Cell. Biol. 28:61–70.
   PubMed Web of Science ®Google Scholar
• Laplante, M., and D. M. Sabatini. 2009. mTOR signaling at a glance. J. Cell Sci. 122:3589–3594.
   PubMed Web of Science ®Google Scholar
• Latres, E., et al. 2005. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J. Biol. Chem. 280:2737–2744.
   PubMed Web of Science ®Google Scholar
• Laustsen, P. G., et al. 2007. Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol. Cell. Biol. 27:1649–1664.
   PubMed Web of Science ®Google Scholar
• Lecker, S. H., A. L. Goldberg, and W. E. Mitch. 2006. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J. Am. Soc. Nephrol. 17:1807–1819.
   PubMed Web of Science ®Google Scholar
• Leroith, D., and D. Accili. 2008. Mechanisms of disease: using genetically altered mice to study concepts of type 2 diabetes. Nat. Clin. Pract. Endocrinol. Metab. 4:164–172.
   PubMedGoogle Scholar
• Lin, X., et al. 2004. Dysregulation of insulin receptor substrate 2 in beta cells and brain causes obesity and diabetes. J. Clin. Invest. 114:908–916.
   PubMed Web of Science ®Google Scholar
• Long, Y. C., and J. R. Zierath. 2006. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest. 116:1776–1783.
   PubMed Web of Science ®Google Scholar
• Mammucari, C., et al. 2007. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6:458–471.
   PubMed Web of Science ®Google Scholar
• Mammucari, C., S. Schiaffino, and M. Sandri. 2008. Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 4:524–526.
   PubMed Web of Science ®Google Scholar
• Masiero, E., et al. 2009. Autophagy is required to maintain muscle mass. Cell Metab. 10:507–515.
   PubMed Web of Science ®Google Scholar
• McCurdy, C. E., and G. D. Cartee. 2005. Akt2 is essential for the full effect of calorie restriction on insulin-stimulated glucose uptake in skeletal muscle. Diabetes 54:1349–1356.
   PubMedGoogle Scholar
• Miyamoto, L., et al. 2007. Effect of acute activation of 5′-AMP-activated protein kinase on glycogen regulation in isolated rat skeletal muscle. J. Appl. Physiol. 102:1007–1013.
   PubMedGoogle Scholar
• Morino, K., K. F. Petersen, and G. I. Shulman. 2006. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55 (Suppl. 2):S9–S15.
   PubMed Web of Science ®Google Scholar
• Obsil, T., and V. Obsilova. 2008. Structure/function relationships underlying regulation of FOXO transcription factors. Oncogene 27:2263–2275.
   PubMed Web of Science ®Google Scholar
• Owen, O. E., S. C. Kalhan, and R. W. Hanson. 2002. The key role of anaplerosis and cataplerosis for citric acid cycle function. J. Biol. Chem. 277:30409–30412.
   PubMed Web of Science ®Google Scholar
• Petersen, K. F., et al. 2007. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. U. S. A. 104:12587–12594.
   PubMed Web of Science ®Google Scholar
• Riehle, C., et al. 2008. Insulin receptor substrates (IRS) signaling are essential regulators of mitochondrial function and cardiomyocyte survival. Circulation 118:S444. (Abstract.)
   Google Scholar
• Ruderman, N. B. 1975. Muscle amino acid metabolism and gluconeogenesis. Annu. Rev. Med. 26:245–258.
   PubMed Web of Science ®Google Scholar
• Sacheck, J. M., A. Ohtsuka, S. C. McLary, and A. L. Goldberg. 2004. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am. J. Physiol. Endocrinol. Metab. 287:E591–E601.
   PubMed Web of Science ®Google Scholar
• Sandri, M., et al. 2004. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399–412.
   PubMed Web of Science ®Google Scholar
• Savage, D. B., K. F. Petersen, and G. I. Shulman. 2007. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol. Rev. 87:507–520.
   PubMed Web of Science ®Google Scholar
• Spargo, E., O. E. Pratt, and P. M. Daniel. 1979. Metabolic functions of skeletal muscles of man, mammals, birds and fishes: a review. J. R. Soc. Med. 12:921–925.
   Google Scholar
• Taguchi, A., and M. F. White. 2008. Insulin-like signaling, nutrient homeostasis, and life span. Annu. Rev. Physiol. 70:191–212.
   PubMed Web of Science ®Google Scholar
• Takata, M., et al. 1999. Requirement for Akt (protein kinase B) in insulin-induced activation of glycogen synthase and phosphorylation of 4E-BP1 (PHAS-1). J. Biol. Chem. 274:20611–20618.
   PubMedGoogle Scholar
• Tamemoto, H., et al. 1994. Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature 372:182–186.
   PubMed Web of Science ®Google Scholar
• Winder, W. W. 2001. Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle. J. Appl. Physiol. 91:1017–1028.
   PubMed Web of Science ®Google Scholar
• Winder, W. W., et al. 1997. Phosphorylation of rat muscle acetyl-CoA carboxylase by AMP-activated protein kinase and protein kinase A. J. Appl. Physiol. 82:219–225.
   PubMedGoogle Scholar
• Zhao, J., et al. 2007. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6:472–483.
   PubMed Web of Science ®Google Scholar
• Zhao, J., J. J. Brault, A. Schild, and A. L. Goldberg. 2008. Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 3:378–380.
   Google Scholar
• Zisman, A., et al. 2000. Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med. 6:924–928.
   PubMed Web of Science ®Google Scholar