Increased basal level of Akt-dependent insulin signaling may be responsible for the development of insulin resistance

American Journal of Physiology - Endocrinology and Metabolism

Volumn 297, Issue 4, 2009, Pages

  Liu, Hui Yu ^a   Hong, Tao ^a,c   Wen, Ge Bo ^c   Han, Jianmin ^a   Zuo, Degen ^a   Liu, Zhenqi ^d   Cao, Wenhong ^a,b  

^a HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

^b DUKE UNIVERSITY HEALTH SYSTEM   (United States)

^c UNIVERSITY OF SOUTH CHINA   (China)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Protein kinase B

Indexed keywords

MITOCHONDRIAL DNA; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; HYPERINSULINEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPID STORAGE; LIVER; MITOCHONDRIAL GENE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; DIETARY FATS; DNA, MITOCHONDRIAL; GLUTATHIONE; IMMUNOBLOTTING; INSULIN; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE, SKELETAL; ONCOGENE PROTEIN V-AKT; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 70349619811     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00374.2009     Document Type: Article

References (53)

1. Abdul-Ghani MA, DeFronzo RA. Mitochondrial dysfunction, insulin resistance, type 2 diabetes mellitus. Curr Diab Rep 8: 173-178, 2008.
2. Accili D. Lilly lecture 2003: the struggle for mastery in insulin action: from triumvirate to republic. Diabetes 53: 1633-1642, 2004.
3. Al-Regaiey KA, Masternak MM, Bonkowski M, Sun L, Bartke A. Long-lived growth hormone receptor knockout mice: interaction of reduced insulin-like growth factor i/insulin signaling and caloric restriction. Endocrinology 146: 851-860, 2005. (Pubitemid 40129843)
4. Anson RM, Guo Z, de Cabo R, Iyun T, Rios M, Hagepanos A, Ingram DK, Lane MA, Mattson MP. Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci USA 100: 6216-6220, 2003. (Pubitemid 36576956)
5. Barja G. Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Res 10: 215-224, 2007. (Pubitemid 46944989)
6. Bluher M, Michael MD, Peroni OD, Ueki K, Carter N, Kahn BB, Kahn CR. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell 3: 25-38, 2002. (Pubitemid 34778393)
7. Cao W, Collins QF, Becker TC, Robidoux J, Lupo J, Xiong Y, Daniel K, Floering L, Collins S. p38 mitogen-activated protein kinase plays a stimulatory role in hepatic gluconeogenesis. J Biol Chem 280: 42731-42737, 2005. (Pubitemid 43049233)
8. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, Ravussin E. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4: e76, 2007. (Pubitemid 46495316)
9. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450: 736-740, 2007. (Pubitemid 350207689)
10. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23: 599-622, 2002.
11. Galgani JE, Uauy RD, Aguirre CA, Diaz EO. Effect of the dietary fat quality on insulin sensitivity. Br J Nutr 100: 471-479, 2008.
12. Garcia-Roves P, Huss JM, Han DH, Hancock CR, Iglesias-Gutierrez E, Chen M, Holloszy JO. Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci USA 104: 10709-10713, 2007. (Pubitemid 47185729)
13. Gregor MF, Hotamisligil GS. Thematic review series: adipocyte Biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48: 1905-1914, 2007.
14. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC, Holloszy JO. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci USA 105: 7815-7820, 2008. (Pubitemid 351872721)
15. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421: 182-187, 2003. (Pubitemid 36090987)
16. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440: 944-948, 2006.
17. Hsieh EA, Chai CM, Hellerstein MK. Effects of caloric restriction on cell proliferation in several tissues in mice: role of intermittent feeding. Am J Physiol Endocrinol Metab 288: E965-E972, 2005.
18. Kaneto H, Matsuoka TA, Katakami N, Kawamori D, Miyatsuka T, Yoshiuchi K, Yasuda T, Sakamoto K, Yamasaki Y, Matsuhisa M. Oxidative stress and the JNK pathway are involved in the development of type 1 and type 2 diabetes. Curr Mol Med 7: 674-686, 2007. (Pubitemid 350201667)
19. Katic M, Kennedy AR, Leykin I, Norris A, McGettrick A, Gesta S, Russell SJ, Bluher M, Maratos-Flier E, Kahn CR. Mitochondrial gene expression and increased oxidative metabolism: role in increased lifespan of fat-specific insulin receptor knock-out mice. Aging Cell 6: 827-839, 2007. (Pubitemid 350131051)
20. Kim JY, van de Wall E, Laplante M, Azzara A, Trujillo ME, Hofmann SM, Schraw T, Durand JL, Li H, Li G, Jelicks LA, Mehler MF, Hui DY, Deshaies Y, Shulman GI, Schwartz GJ, Scherer PE. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Invest 117: 2621-2637, 2007. (Pubitemid 47494363)
21. Kraegen EW, Cooney GJ. Free fatty acids and skeletal muscle insulin resistance. Curr Opin Lipidol 19: 235-241, 2008. (Pubitemid 351653560)
22. Kumashiro N, Tamura Y, Uchida T, Ogihara T, Fujitani Y, Hirose T, Mochizuki H, Kawamori R, Watada H. Impact of oxidative stress and peroxisome proliferator-activated receptor gamma coactivator-1alpha in hepatic insulin resistance. Diabetes 57: 2083-2091, 2008.
23. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18: 231-236, 1998. (Pubitemid 28117260)
24. Lee S, Muniyappa R, Yan X, Chen H, Yue LQ, Hong EG, Kim JK, Quon MJ. Comparison between surrogate indexes of insulin sensitivity and resistance and hyperinsulinemic euglycemic clamp estimates in mice. Am J Physiol Endocrinol Metab 294: E261-E270, 2008. (Pubitemid 351231452)
25. Lerner E, Shug AL, Elson C, Shrago E. Reversible inhibition of adenine nucleotide translocation by long chain fatty acyl coenzyme A esters in liver mitochondria of diabetic and hibernating animals. J Biol Chem 247: 1513-1519, 1972.
26. Li X, Monks B, Ge Q, Birnbaum MJ. Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature 447: 1012-1016, 2007. (Pubitemid 46975750)
27. Liu HY, Yehuda-Shnaidman E, Hong T, Han J, Pi J, Liu Z, Cao W. Prolonged exposure to insulin suppresses mitochondrial production in primary hepatocytes. J Biol Chem 284: 1487-1495, 2009.
28. Loschen G, Flohe L, Chance B. Respiratory chain linked H(2)O(2) production in pigeon heart mitochondria. FEBS Lett 18: 261-264, 1971.
29. Manning BD. Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J Cell Biol 167: 399-403, 2004.
30. Martin B, Mattson MP, Maudsley S. Caloric restriction and intermittent fasting: two potential diets for successful brain aging. Ageing Res Rev 5: 332-353, 2006. (Pubitemid 44374430)
31. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 57: 1071-1077, 2008. (Pubitemid 351978066)
32. Mattson MP, Wan R. Beneficial effects of intermittent fasting and caloric restriction on the cardiovascular and cerebrovascular systems. J Nutr Biochem 16: 129-137, 2005. (Pubitemid 40312164)
33. Monetti M, Levin MC, Watt MJ, Sajan MP, Marmor S, Hubbard BK, Stevens RD, Bain JR, Newgard CB, Farese RV Sr, Hevener AL, and Farese RV Jr. Dissociation of hepatic steatosis and insulin resistance in mice overexpressing DGAT in the liver. Cell Metab 6: 69-78, 2007. (Pubitemid 46995777)
34. Nishino N, Tamori Y, Kasuga M. Insulin efficiently stores triglycerides in adipocytes by inhibiting lipolysis and repressing PGC-1alpha induction. Kobe J Med Sci 53: 99-106, 2007. (Pubitemid 47360765)
35. Pande SV, Blanchaer MC. Reversible inhibition of mitochondrial adenosine diphosphate phosphorylation by long chain acyl coenzyme A esters. J Biol Chem 246: 402-411, 1971.
36. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142, 2003. (Pubitemid 36583097)
37. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, Ebersberger I, Nakashima T, Sarao R, Neely G, Esterbauer H, Kozlov A, Kahn CR, Kroemer G, Rustin P, Burcelin R, Penninger JM. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131: 476-491, 2007. (Pubitemid 350017761)
38. Ristow M. Neurodegenerative disorders associated with diabetes mellitus. J Mol Med 82: 510-529, 2004. (Pubitemid 39149861)
39. Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 117: 1690-1698, 2007. (Pubitemid 46871353)
40. Shrago E, Shu A, Elson C. Regulation of Cell Metabolism by Mitochondrial Transport Systems. Gluconeogenesis: Its Regulation in Mammalian Species, edited by Hanson RW. New York: Wiley, 1976, p. 221-238.
41. Shug AL, Shrago E, Bittar N, Folts JD, Koke JR. Acyl-CoA inhibition of adenine nucleotide translocation in ischemic myocardium. Am J Physiol 228: 689-692, 1975.
42. Southgate RJ, Bruce CR, Carey AL, Steinberg GR, Walder K, Monks R, Watt MJ, Hawley JA, Birnbaum MJ, Febbraio MA. PGC-1alpha gene expression is down-regulated by Akt- mediated phosphorylation and nuclear exclusion of FoxO1 in insulin-stimulated skeletal muscle. FASEB J 19: 2072-2074, 2005. (Pubitemid 41759769)
43. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37: 1163-1167, 1988. (Pubitemid 19035045)
44. Surwit RS, Wang S, Petro AE, Sanchis D, Raimbault S, Ricquier D, Collins S. Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci USA 95: 4061-4065, 1998. (Pubitemid 28173254)
45. Thierbach R, Schulz TJ, Isken F, Voigt A, Mietzner B, Drewes G, von Kleist-Retzow JC, Wiesner RJ, Magnuson MA, Puccio H, Pfeiffer AF, Steinberg P, Ristow M. Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice. Hum Mol Genet 14: 3857-3864, 2005. (Pubitemid 43020087)
46. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205, 2004. (Pubitemid 39243474)
47. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39: 359-407, 2005.
48. Wang MY, Grayburn P, Chen S, Ravazzola M, Orci L, Unger RH. Adipogenic capacity and the susceptibility to type 2 diabetes and metabolic syndrome. Proc Natl Acad Sci USA 105: 6139-6144, 2008. (Pubitemid 351758412)
49. Wojtczak L, Zaluska H. The inhibition of translocation of adenine nucleotides through mitochondrial membranes by oleate. Biochem Biophys Res Commun 28: 76-81, 1967.
50. Wullaert A, van Loo G, Heyninck K, Beyaert R. Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: effects on liver homeostasis and beyond. Endocr Rev 28: 365-386, 2007. (Pubitemid 46984825)
51. Xiong Y, Collins QF, Lupo J, Liu HY, Jie A, Liu D, Cao W. p38 mitogen-activated protein kinase plays an inhibitory role in hepatic lipogenesis. J Biol Chem 282: 4975-4982, 2006.
52. Yang Z, Cheng W, Hong L, Chen W, Wang Y, Lin S, Han J, Zhou H, Gu J. Adenine nucleotide (ADP/ATP) translocase 3 participates in the tumor necrosis factor induced apoptosis of MCF-7 cells. Mol Biol Cell 18: 4681-4689, 2007. (Pubitemid 350060192)
53. Ye J. Role of insulin in the pathogenesis of free fatty acid-induced insulin resistance in skeletal muscle. Endocr Metab Immune Disord Drug Targets 7: 65-74, 2007. (Pubitemid 46380417)