Essential Role of Insulin and Insulin-Like Growth Factor 1 Receptor Signaling in Cardiac Development and Function

REFERENCES

• Accili, D., J. Drago, E. J. Lee, M. D. Johnson, M. H. Cool, P. Salvatore, L. D. Asico, P. A. Jose, S. I. Taylor, and H. Westphal. 1996. Early neonatal death in mice homozygous for a null allele of the insulin receptor gene. Nat. Genet. 12:106–109.
   PubMed Web of Science ®Google Scholar
• Aihara, Y., M. Kurabayashi, Y. Saito, Y. Ohyama, T. Tanaka, S. Takeda, K. Tomaru, K. Sekiguchi, M. Arai, T. Nakamura, and R. Nagai. 2000. Cardiac ankyrin repeat protein is a novel marker of cardiac hypertrophy: role of M-CAT element within the promoter. Hypertension 36:48–53.
   PubMed Web of Science ®Google Scholar
• Bang, M. L., R. E. Mudry, A. S. McElhinny, K. Trombitas, A. J. Geach, R. Yamasaki, H. Sorimachi, H. Granzier, C. C. Gregorio, and S. Labeit. 2001. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J. Cell Biol. 153:413–427.
   PubMed Web of Science ®Google Scholar
• Belke, D. D., S. Betuing, M. J. Tuttle, C. Graveleau, M. E. Young, M. Pham, D. Zhang, R. C. Cooksey, D. A. McClain, S. E. Litwin, H. Taegtmeyer, D. Severson, C. R. Kahn, and E. D. Abel. 2002. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J. Clin. Investig. 109:629–639.
   PubMed Web of Science ®Google Scholar
• Blakesley, V. A., A. Scrimgeour, D. Esposito, and D. Le Roith. 1996. Signaling via the insulin-like growth factor-I receptor: does it differ from insulin receptor signaling? Cytokine Growth Factor Rev. 7:153–159.
   PubMedGoogle Scholar
• Bluher, M., L. Wilson-Fritch, J. Leszyk, P. G. Laustsen, S. Corvera, and C. R. Kahn. 2004. Role of insulin action and cell size on protein expression patterns in adipocytes. J. Biol. Chem. 279:31902–31909.
   PubMedGoogle Scholar
• Brown, G. C. 1992. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J. 284:1–13.
   PubMed Web of Science ®Google Scholar
• Brüning, J. C., M. D. Michael, J. N. Winnay, T. Hayashi, D. Horsch, D. Accili, L. J. Goodyear, and C. R. Kahn. 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
• Condorelli, G., A. Drusco, G. Stassi, A. Bellacosa, R. Roncarati, G. Iaccarino, M. A. Russo, Y. Gu, N. Dalton, C. Chung, M. V. Latronico, C. Napoli, J. Sadoshima, C. M. Croce, and J. Ross, Jr. 2002. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc. Natl. Acad. Sci. USA 99:12333–12338.
   PubMed Web of Science ®Google Scholar
• Costa, J., M. Borges, C. David, and C. A. Vaz. 2006. Efficacy of lipid lowering drug treatment for diabetic and non-diabetic patients: meta-analysis of randomised controlled trials. BMJ 332:1115–1124.
   PubMed Web of Science ®Google Scholar
• Crackower, M., G. Oudit, I. Kozieradzki, R. Sarao, H. Sun, T. Sasaki, E. Hirsch, A. Suzuki, T. Shioi, J. Irie-Sasaki, R. Sah, H. Cheng, V. Rybin, G. Lembo, L. Fratta, A. Oliveira-dos-Santos, J. Benovic, C. R. Kahn, S. Izumo, S. Steinberg, M. Wymann, P. Backx, and J. Penninger. 2002. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 110:737–749.
   PubMed Web of Science ®Google Scholar
• Dahlquist, K. D., N. Salomonis, K. Vranizan, S. C. Lawlor, and B. R. Conklin. 2002. GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat. Genet. 31:19–20.
   PubMed Web of Science ®Google Scholar
• DeFronzo, R. A. 1997. Pathogenesis of type 2 diabetes: metabolic and molecular implications for identifying diabetes genes. Diabetes Rev. 5:177–269.
   Google Scholar
• Di Cola, G., M. H. Cool, and D. Accili. 1997. Hypoglycemic effect of insulin-like growth factor-1 in mice lacking insulin receptors. J. Clin. Investig. 99:2538–2544.
   PubMedGoogle Scholar
• Fang, Z. Y., J. B. Prins, and T. H. Marwick. 2004. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocrine Rev. 25:543–567.
   PubMed Web of Science ®Google Scholar
• Fernandez, A. M., J. Dupont, R. P. Farrar, S. Lee, B. Stannard, and D. Le Roith. 2002. Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J. Clin. Investig. 109:347–355.
   PubMed Web of Science ®Google Scholar
• Fernandez, A. M., J. K. Kim, S. Yakar, J. Dupont, C. Hernandez-Sanchez, A. L. Castle, J. Filmore, G. I. Shulman, and D. Le Roith. 2001. Functional inactivation of the IGF-I and insulin receptors in skeletal muscle causes type 2 diabetes. Genes Dev. 15:1926–1934.
   PubMedGoogle Scholar
• Giles, T. D. 2003. The patient with diabetes mellitus and heart failure: at-risk issues. Am. J. Med. 115(Suppl. 8A):107S–110S.
   PubMedGoogle Scholar
• Holzenberger, M., P. Leneuve, G. Hamard, B. Ducos, L. Perin, M. Binoux, and Y. Le Bouc. 2000. A targeted partial invalidation of the insulin-like growth factor I receptor gene in mice causes a postnatal growth deficit. Endocrinology 141:2557–2566.
   PubMedGoogle Scholar
• Jeyaseelan, R., C. Poizat, R. K. Baker, S. Abdishoo, L. B. Isterabadi, G. E. Lyons, and L. Kedes. 1997. A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardiomyocytes. J. Biol. Chem. 272:22800–22808.
   PubMed Web of Science ®Google Scholar
• Joshi, R. L., B. Lamothe, N. Cordonnier, K. Mesbah, E. Monthioux, J. Jami, and C. Bucchini. 1996. Targeted disruption of the insulin receptor gene in the mouse results in neonatal lethality. EMBO J. 15:1542–1547.
   PubMed Web of Science ®Google Scholar
• Kim, J. K., M. D. Michael, S. F. Previs, O. D. Peroni, F. Mauvais-Jarvis, S. Neschen, B. B. Kahn, C. R. Kahn, and G. I. Shulman. 2000. Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J. Clin. Investig. 105:1791–1797.
   PubMedGoogle Scholar
• Krenz, M., and J. Robbins. 2004. Impact of beta-myosin heavy chain expression on cardiac function during stress. J. Am. Coll. Cardiol. 44:2390–2397.
   PubMedGoogle Scholar
• Laakso, M. 2001. Cardiovascular disease in type 2 diabetes: challenge for treatment and prevention. J. Intern. Med. 249:225–235.
   PubMed Web of Science ®Google Scholar
• Laustsen, P. G., W. S. Lane, V. Bennett, and G. E. Lienhard. 2001. Association of protein kinase C(lambda) with adducin in 3T3-L1 adipocytes. Biochim. Biophys. Acta 1539:163–172.
   PubMedGoogle Scholar
• Liao, R., M. Jain, L. Cui, J. D'Agostino, F. Aiello, I. Luptak, S. Ngoy, R. M. Mortensen, and R. Tian. 2002. Cardiac-specific overexpression of GLUT1 prevents the development of heart failure attributable to pressure overload in mice. Circulation 106:2125–2131.
   PubMed Web of Science ®Google Scholar
• Lillioja, S., D. M. Mott, M. Spraul, R. Ferraro, J. E. Foley, E. Ravussin, W. C. Knowler, P. H. Bennett, and C. Bogardus. 1993. Insulin resistance and insulin secretory dysfunction as precursors of non-insulin-dependent diabetes mellitus: prospective studies of Pima Indians. N. Engl. J. Med. 329:1988–1992.
   PubMed Web of Science ®Google Scholar
• Liu, J. P., J. Baker, J. A. Perkins, E. J. Robertson, and A. Efstratiadis. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor I (lgf-1) and type 1 IGF receptor (lgf1r). Cell 75:59–72.
   PubMed Web of Science ®Google Scholar
• Louvi, A., D. Accili, and A. Efstratiadis. 1997. Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev. Biol. 189:33–48.
   PubMed Web of Science ®Google Scholar
• Lowell, B. B., and G. I. Shulman. 2005. Mitochondrial dysfunction and type 2 diabetes. Science 307:384–387.
   PubMed Web of Science ®Google Scholar
• Martin, B. C., J. Warram, A. S. Krolewski, R. N. Bergman, J. S. Soeldner, and C. R. Kahn. 1992. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet 340:925–929.
   PubMed Web of Science ®Google Scholar
• McMullen, J. R., T. Shioi, W. Y. Huang, L. Zhang, O. Tarnavski, E. Bisping, M. Schinke, S. Kong, M. C. Sherwood, J. Brown, L. Riggi, P. M. Kang, and S. Izumo. 2004. The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway. J. Biol. Chem. 279:4782–4793.
   PubMed Web of Science ®Google Scholar
• Mootha, V. K., C. M. Lindgren, K. F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstrale, E. Laurila, N. Houstis, M. J. Daly, N. Patterson, J. P. Mesirov, T. R. Golub, P. Tamayo, B. Spiegelman, E. S. Lander, J. N. Hirschhorn, D. Altshuler, and L. C. Groop. 2003. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34:267–273.
   PubMed Web of Science ®Google Scholar
• Mora, A., A. M. Davies, L. Bertrand, I. Sharif, G. R. Budas, S. Jovanovic, V. Mouton, C. R. Kahn, J. M. Lucocq, G. A. Gray, A. Jovanovic, and D. R. Alessi. 2003. Deficiency of PDK1 in cardiac muscle results in heart failure and increased sensitivity to hypoxia. EMBO J. 22:4666–4676.
   PubMed Web of Science ®Google Scholar
• Nadal-Ginard, B., and V. Mahdavi. 1989. Molecular basis of cardiac performance. Plasticity of the myocardium generated through protein isoform switches. J. Clin. Investig. 84:1693–1700.
   PubMed Web of Science ®Google Scholar
• Nathan, D. M., P. A. Cleary, J. Y. Backlund, S. M. Genuth, J. M. Lachin, T. J. Orchard, P. Raskin, and B. Zinman. 2005. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N. Engl. J. Med. 353:2643–2653.
   PubMed Web of Science ®Google Scholar
• Patti, M. E., A. J. Butte, S. Crunkhorn, K. Cusi, R. Berria, S. Kashyap, Y. Miyazaki, I. Kohane, M. Costello, R. Saccone, E. J. Landaker, A. B. Goldfine, E. Mun, R. DeFronzo, J. Finlayson, C. R. Kahn, and L. J. Mandarino. 2003. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. USA 100:8466–8471.
   PubMed Web of Science ®Google Scholar
• Petersen, K. F., S. Dufour, D. Befroy, R. Garcia, and G. I. Shulman. 2004. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350:664–671.
   PubMed Web of Science ®Google Scholar
• Petersen, K. F., S. Dufour, and G. I. Shulman. 2005. Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med. 2:e233.
   PubMed Web of Science ®Google Scholar
• Poornima, I. G., P. Parikh, and R. P. Shannon. 2006. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ. Res. 98:596–605.
   PubMed Web of Science ®Google Scholar
• Pyle, W. G., and R. J. Solaro. 2004. At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ. Res. 94:296–305.
   PubMed Web of Science ®Google Scholar
• Ren, J., W. K. Samson, and J. R. Sowers. 1999. Insulin-like growth factor I as a cardiac hormone: physiological and pathophysiological implications in heart disease. J. Mol. Cell. Cardiol. 31:2049–2061.
   PubMed Web of Science ®Google Scholar
• Saetrum Opgaard, O., and P. H. Wang. 2005. IGF-I is a matter of heart. Growth Horm. IGF Res. 15:89–94.
   PubMedGoogle Scholar
• Saltiel, A. R., and C. R. Kahn. 2001. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799–806.
   PubMed Web of Science ®Google Scholar
• Scheinowitz, M., G. Kessler-Icekson, S. Freimann, R. Zimmermann, W. Schaper, E. Golomb, N. Savion, and M. Eldar. 2003. Short- and long-term swimming exercise training increases myocardial insulin-like growth factor-I gene expression. Growth Horm. IGF Res. 13:19–25.
   PubMed Web of Science ®Google Scholar
• Shefi-Friedman, L., E. Wertheimer, S. Shen, A. Bak, D. Accili, and S. R. Sampson. 2001. Increased IGFR activity and glucose transport in cultured skeletal muscle from insulin receptor null mice. Am. J. Physiol. Endocrinol. Metab. 281:E16–E24.
   PubMedGoogle Scholar
• Shioi, T., P. M. Kang, P. S. Douglas, J. Hampe, C. M. Yballe, J. Lawitts, L. C. Cantley, and S. Izumo. 2000. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J. 19:2537–2548.
   PubMed Web of Science ®Google Scholar
• Shioi, T., J. R. McMullen, P. M. Kang, P. S. Douglas, T. Obata, T. F. Franke, L. C. Cantley, and S. Izumo. 2002. Akt/protein kinase B promotes organ growth in transgenic mice. Mol. Cell. Biol. 22:2799–2809.
   PubMed Web of Science ®Google Scholar
• Shiojima, I., M. Yefremashvili, Z. Luo, Y. Kureishi, A. Takahashi, J. Tao, A. Rosenzweig, C. R. Kahn, E. D. Abel, and K. Walsh. 2002. Akt signaling mediates postnatal heart growth in response to insulin and nutritional status. J. Biol. Chem. 277:37670–37677.
   PubMedGoogle Scholar
• Tardiff, J. C., T. E. Hewett, S. M. Factor, K. L. Vikstrom, J. Robbins, and L. A. Leinwand. 2000. Expression of the beta (slow)-isoform of MHC in the adult mouse heart causes dominant-negative functional effects. Am. J. Physiol. Heart Circ. Physiol. 278:H412–H419.
   PubMedGoogle Scholar
• Uwaifo, G. I., and R. E. Ratner. 2003. The roles of insulin resistance, hyperinsulinemia, and thiazolidinediones in cardiovascular disease. Am. J. Med. 115(Suppl. 8A):12S–19S.
   PubMedGoogle Scholar
• von Lewinski, D., K. Voss, S. Hulsmann, H. Kogler, and B. Pieske. 2003. Insulin-like growth factor-1 exerts Ca2+-dependent positive inotropic effects in failing human myocardium. Circ. Res. 92:169–176.
   PubMed Web of Science ®Google Scholar
• Wang, X., and B. Seed. 2003. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 31:e154.
   PubMed Web of Science ®Google Scholar
• Yechoor, V. K., M. E. Patti, K. Ueki, P. G. Laustsen, R. Saccone, R. Rauniyar, and C. R. Kahn. 2004. Distinct pathways of insulin-regulated versus diabetes-regulated gene expression: an in vivo analysis in MIRKO mice. Proc. Natl. Acad. Sci. USA 101:16525–16530.
   PubMed Web of Science ®Google Scholar
• Zisman, A., O. D. Peroni, D. Abel, M. D. Michael, F. Mauvais-Jarvis, B. B. Lowell, J. F. P. Wojtaszewski, M. F. Hirshman, A. Virkamaki, L. J. Goodyear, C. R. Kahn, and B. B. Kahn. 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
• Zolk, O., M. Frohme, A. Maurer, F. W. Kluxen, B. Hentsch, D. Zubakov, J. D. Hoheisel, I. H. Zucker, S. Pepe, and T. Eschenhagen. 2002. Cardiac ankyrin repeat protein, a negative regulator of cardiac gene expression, is augmented in human heart failure. Biochem. Biophys. Res. Commun. 293:1377–1382.
   PubMedGoogle Scholar
• Zou, Y., S. Evans, J. Chen, H. C. Kuo, R. P. Harvey, and K. R. Chien. 1997. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 124:793–804.
   PubMedGoogle Scholar