Fatty liver as a consequence and cause of insulin resistance: Lessons from type 2 diabetic liver

Endocrine Journal

Volumn 59, Issue 9, 2012, Pages 745-763

  Takamura, Toshinari ^a   Misu, Hirofumi ^a   Ota, Tsuguhito ^a   Kaneko, Shuichi ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

Fatty liver; Hepatokine; Mitochondria; Reactive oxygen species; Selenoprotein P

Indexed keywords

ALPHA TOCOPHEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PIOGLITAZONE; SELENOPROTEIN P; TRIACYLGLYCEROL;

BODY MASS; CAUSAL ATTRIBUTION; DIABETIC PATIENT; DISEASE ASSOCIATION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HEPATITIS; HUMAN; INSULIN RESISTANCE; LIPID STORAGE; LIVER BIOPSY; MITOCHONDRIAL RESPIRATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; ONSET AGE; OVERNUTRITION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN TARGETING; REVIEW; SYSTEMIC DISEASE; UPREGULATION;

ANIMALS; DIABETES MELLITUS, TYPE 2; FATTY LIVER; HUMANS; INSULIN RESISTANCE; LIVER; MITOCHONDRIA, LIVER; OBESITY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS;

EID: 84867913712     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.EJ12-0228     Document Type: Review

References (69)

1. Yamada T, Katagiri H (2007) Avenues of communication between the brain and tissues/organs involved in energy homeostasis. Endocr J 54: 497-505.
2. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, et al. (2000) Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 6: 87-97.
3. Lauro D, Kido Y, Castle AL, Zarnowski MJ, Hayashi H, Ebina Y, et al. (1998) Impaired glucose tolerance in mice with a targeted impairment of insulin action in muscle and adipose tissue. Nat Genet 20: 294-298.
4. Farese RV, Jr., Zechner R, Newgard CB, Walther TC (2012) The Problem of Establishing Relationships between Hepatic Steatosis and Hepatic Insulin Resistance. Cell Metab 15: 570-573.
5. Ota T, Takamura T, Hirai N, Kobayashi K (2002) Preobesity in world health organization classification involves the metabolic syndrome in Japanese. Diabetes Care 25: 1252-1253.
6. Sakurai M, Ota T, Miura K, Nakagawa H, Kaneko S, Takamura T (2012). BMI, waist circumference and metabolic syndrome: Lessons from Japanese perspectives. In The Handbook of Anthropometry: Physical Measures of Human Form in Health and Disease, Preedy VR, ed. (New York, Springer Science+Business Media), pp. 1973-1988.
7. Perseghin G (2009) Viewpoints on the way to a con-sensus session: where does insulin resistance start? The liver. Diabetes Care 32 Suppl 2: S164-167.
8. Sakurai M, Takamura T, Ota T, Ando H, Akahori H, Kaji K, et al. (2007) Liver steatosis, but not fibrosis, is associated with insulin resistance in nonalcoholic fatty liver disease. J Gastroenterol 42: 312-317.
9. Fabbrini E, Magkos F, Mohammed BS, Pietka T, Abumrad NA, Patterson BW, et al. (2009) Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci U S A 106: 15430-15435.
10. Kita Y, Mizukoshi E, Takamura T, Sakurai M, Takata Y, Arai K, et al. (2007) Impact of diabetes mellitus on prognosis of patients infected with hepatitis C virus. Metabolism 56: 1682-1688.
11. Komura T, Mizukoshi E, Kita Y, Sakurai M, Takata Y, Arai K, et al. (2007) Impact of diabetes on recurrence of hepatocellular carcinoma after surgical treatment in patients with viral hepatitis. Am J Gastroenterol 102: 1939-1946.
12. Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, et al. (2007) Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 13: 332-339.
13. Shimizu A, Takamura T, Matsuzawa N, Nakamura S, Nabemoto S, Takeshita Y, et al. (2007) Regulation of adiponectin receptor expression in human liver and a hepatocyte cell line. Metabolism 56: 1478-1485.
14. Yasui K, Hashimoto E, Komorizono Y, Koike K, Arii S, Imai Y, et al. (2011) Characteristics of patients with nonalcoholic steatohepatitis who develop hepatocellular carcinoma. Clin Gastroenterol Hepatol 9: 428-433: quiz e50.
15. Ota T, Takamura T, Kurita S, Matsuzawa N, Kita Y, Uno M, et al. (2007) Insulin resistance accelerates a dietary rat model of nonalcoholic steatohepatitis. Gastroenterology 132: 282-293.
16. Kurita S, Takamura T, Ota T, Matsuzawa-Nagata N, Kita Y, Uno M, et al. (2008) Olmesartan ameliorates a dietary rat model of non-alcoholic steatohepatitis through its pleiotropic effects. Eur J Pharmacol 588: 316-324.
17. Uno M, Kurita S, Misu H, Ando H, Ota T, Matsuzawa-Nagata N, et al. (2008) Tranilast, an antifibrogenic agent, ameliorates a dietary rat model of nonalcoholic steatohepatitis. Hepatology 48: 109-118.
18. Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, et al. (2010) Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med 362: 1675-1685.
19. Aithal GP, Thomas JA, Kaye PV, Lawson A, Ryder SD, Spendlove I, et al. (2008) Randomized, placebo-controlled trial of pioglitazone in nondiabetic subjects with nonalcoholic steatohepatitis. Gastroenterology 135: 1176-1184.
20. Belfort R, Harrison SA, Brown K, Darland C, Finch J, Hardies J, et al. (2006) A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N Engl J Med 355: 2297-2307.
21. Hamaguchi E, Takamura T, Sakurai M, Mizukoshi E, Zen Y, Takeshita Y, et al. (2010) Histological course of nonalcoholic fatty liver disease in Japanese patients: tight glycemic control, rather than weight reduction, ameliorates liver fibrosis. Diabetes Care 33: 284-286.
22. Takamura T, Sakurai M, Nakamura M, Shimizu A, Ota T, Misu H, et al. (2007) Factors associated with improvement of fasting plasma glucose level by mealtime dosing of a rapid-acting insulin analog in type 2 diabetes. Diabetes Res Clin Pract 75: 278-284.
23. Ludwig J, Viggiano TR, McGill DB, Oh BJ (1980) Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease. Mayo Clin Proc 55: 434-438.
24. Itoh S, Tsukada Y, Motomura Y, Ichinoe A (1979) Five patients with nonalcoholic diabetic cirrhosis. Acta Hepatogastroenterol (Stuttg) 26: 90-97.
25. Takamura T, Sakurai M, Ota T, Ando H, Honda M, Kaneko S (2004) Genes for systemic vascular complications are differentially expressed in the livers of type 2 diabetic patients. Diabetologia 47: 638-647.
26. Kawaguchi T, Sumida Y, Umemura A, Matsuo K, Takahashi M, Takamura T, et al. (2012) Genetic Polymorphisms of the Human PNPLA3 Gene Are Strongly Associated with Severity of Non-Alcoholic Fatty Liver Disease in Japanese. PLoS One 7: e38322.
27. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, et al. (2008) Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 57: 1071-1077.
28. Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, Sai Y, et al. (2012) CCR5 Plays a Critical Role in Obesity-Induced Adipose Tissue Inflammation and Insulin Resistance by Regulating Both Macrophage Recruitment and M1/M2 Status. Diabetes 61: 1680-1690.
29. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Jr., Ory DS, et al. (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 100: 3077-3082.
30. Yamaguchi K, Yang L, McCall S, Huang J, Yu XX, Pandey SK, et al. (2007) Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology 45: 1366-1374.
31. Buettner R, Ottinger I, Scholmerich J, Bollheimer LC (2004) Preserved direct hepatic insulin action in rats with diet-induced hepatic steatosis. Am J Physiol Endocrinol Metab 286: E828-833.
32. Monetti M, Levin MC, Watt MJ, Sajan MP, Marmor S, Hubbard BK, et al. (2007) Dissociation of hepatic steatosis and insulin resistance in mice overexpressing DGAT in the liver. Cell Metab 6: 69-78.
33. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, Ando H, et al. (2007) Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46: 1392-1403.
34. Ide T, Shimano H, Yahagi N, Matsuzaka T, Nakakuki M, Yamamoto T, et al. (2004) SREBPs suppress IRS-2-mediated insulin signalling in the liver. Nat Cell Biol 6: 351-357.
35. Nakamura S, Takamura T, Matsuzawa-Nagata N, Takayama H, Misu H, Noda H, et al. (2009) Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J Biol Chem 284: 14809-14818.
36. Takamura T, Misu H, Yamashita T, Kaneko S (2008) SAGE application in the study of diabetes. Curr Pharm Biotechnol 9: 392-399.
37. Misu H, Takamura T, Matsuzawa N, Shimizu A, Ota T, Sakurai M, et al. (2007) Genes involved in oxidative phosphorylation are coordinately upregulated with fasting hyperglycaemia in livers of patients with type 2 diabetes. Diabetologia 50: 268-277.
38. Yamashita T, Hashimoto S, Kaneko S, Nagai S, Toyoda N, Suzuki T, et al. (2000) Comprehensive gene expression profile of a normal human liver. Biochem Biophys Res Commun 269: 110-116.
39. Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387.
40. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671.
41. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
42. Dahlman I, Forsgren M, Sjogren A, Nordstrom EA, Kaaman M, Naslund E, et al. (2006) Downregulation of electron transport chain genes in visceral adipose tissue in type 2 diabetes independent of obesity and possibly involving tumor necrosis factor-alpha. Diabetes 55: 1792-1799.
43. Takamura T, Honda M, Sakai Y, Ando H, Shimizu A, Ota T, et al. (2007) Gene expression profiles in peripheral blood mononuclear cells reflect the pathophysiology of type 2 diabetes. Biochem Biophys Res Commun 361: 379-384.
44. Bonawitz ND, Chatenay-Lapointe M, Pan Y, Shadel GS (2007) Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab 5: 265-277.
45. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820.
46. Gaines G, Rossi C, Attardi G (1987) Markedly different ATP requirements for rRNA synthesis and mtDNA light strand transcription versus mRNA synthesis in isolated human mitochondria. J Biol Chem 262: 1907-1915.
47. Takamura T, Misu H, Matsuzawa-Nagata N, Sakurai M, Ota T, Shimizu A, et al. (2008) Obesity upregulates genes involved in oxidative phosphorylation in livers of diabetic patients. Obesity (Silver Spring) 16: 2601-2609.
48. Freyer C, Larsson NG (2007) Is energy deficiency good in moderation? Cell 131: 448-450.
49. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, et al. (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 U S A 100: 8466-8471.
50. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, et al. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790.
51. Guigas B, Detaille D, Chauvin C, Batandier C, De Oliveira F, Fontaine E, et al. (2004) Metformin inhibits mitochondrial permeability transition and cell death: a pharmacological in vitro study. Biochem J 382: 877-884.
52. Owen MR, Doran E, Halestrap AP (2000) Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 348 Pt 3: 607-614.
53. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, et al. (2007) Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131: 476-491.
54. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, et al. (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118: 789-800.
55. Sunny NE, Parks EJ, Browning JD, Burgess SC (2011) Excessive hepatic mitochondrial TCA cycle and gluconeogenesis in humans with nonalcoholic fatty liver disease. Cell Metab 14: 804-810.
56. Brown MS, Goldstein JL (2008) Selective versus total insulin resistance: a pathogenic paradox. Cell Metab 7: 95-96.
57. Ootsuji H, Honda M, Kaneko S, Usui S, Okajima M, Okada H, et al. (2010) Altered hepatic gene expression profiles associated with myocardial ischemia. Circ Cardiovasc Genet 3: 68-77.
58. Takeshita Y, Takamura T, Hamaguchi E, Shimizu A, Ota T, Sakurai M, et al. (2006) Tumor necrosis factor-alphainduced production of plasminogen activator inhibitor 1 and its regulation by pioglitazone and cerivastatin in a nonmalignant human hepatocyte cell line. Metabolism 55: 1464-1472.
59. Takeshita Y, Takamura T, Ando H, Hamaguchi E, Takazakura A, Matsuzawa-Nagata N, et al. (2008) Cross talk of tumor necrosis factor-alpha and the reninangiotensin system in tumor necrosis factor-alpha-induced plasminogen activator inhibitor-1 production from hepatocytes. Eur J Pharmacol 579: 426-432.
60. Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K (1996) cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most abundant Gene transcript 1). Biochem Biophys Res Commun 221: 286-289.
61. Ando H, Takamura T, Matsuzawa-Nagata N, Shima KR, Nakamura S, Kumazaki M, et al. (2009) The hepatic circadian clock is preserved in a lipid-induced mouse model of non-alcoholic steatohepatitis. Biochem Biophys Res Commun 380: 684-688.
62. Misu H, Takamura T, Takayama H, Hayashi H, Matsuzawa-Nagata N, Kurita S, et al. (2010) A liver-derived secretory protein, selenoprotein P, causes insulin resistance. Cell Metab 12: 483-495.
63. Yang SJ, Hwang SY, Choi HY, Yoo HJ, Seo JA, Kim SG, et al. (2011) Serum selenoprotein P levels in patients with type 2 diabetes and prediabetes: implications for insulin resistance, inflammation, and atherosclerosis. J Clin Endocrinol Metab 96: E1325-1329.
64. Burk RF, Hill KE (2005) Selenoprotein P: an extracellular protein with unique physical characteristics and a role in selenium homeostasis. Annu Rev Nutr 25: 215-235.
65. Misu H, Ishikura K, Kurita S, Takeshita Y, Ota T, Saito Y, et al. (2012) Inverse correlation between serum levels of selenoprotein P and adiponectin in patients with type 2 diabetes. PLoS One 7: e34952.
66. Stranges S, Marshall JR, Natarajan R, Donahue RP, Trevisan M, Combs GF, et al. (2007) Effects of longterm selenium supplementation on the incidence of type 2 diabetes: a randomized trial. Ann Intern Med 147: 217-223.
67. Iwakami S, Misu H, Takeda T, Sugimori M, Matsugo S, Kaneko S, et al. (2011) Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes. PLoS One 6: e27401.
68. Loh K, Deng H, Fukushima A, Cai X, Boivin B, Galic S, et al. (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10: 260-272.
69. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, Kiehntopf M, et al. (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106: 8665-8670.