Visceral obesity modulates the impact of apolipoprotein C3 gene variants on liver fat content

International Journal of Obesity

Volumn 36, Issue 6, 2012, Pages 774-782

  Peter, A ^a   Kantartzis, K ^a   MacHicao, F ^a   MacHann, J ^a   Wagner, S ^a   Templin, S ^a   Konigsrainer I ^a   Konigsrainer A ^a   Schick, F ^a   Fritsche, A ^a   Haring H U ^a   Stefan, N ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Apo C; hypertriglyceridemia; insulin resistance; non alcoholic fatty liver disease; visceral fat

Indexed keywords

APOLIPOPROTEIN C3; GLUCOSE; MESSENGER RNA; TRIACYLGLYCEROL;

ABDOMINAL OBESITY; ADULT; AGED; ALLELE; ARTICLE; CORRELATION ANALYSIS; FATTY LIVER; FEMALE; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE; GERMANY; HETEROZYGOTE; HUMAN; INSULIN SENSITIVITY; INTERVENTION STUDY; INTRAABDOMINAL FAT; LIFESTYLE MODIFICATION; LIVER BIOPSY; MAJOR CLINICAL STUDY; MALE; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SINGLE NUCLEOTIDE POLYMORPHISM; WAIST CIRCUMFERENCE;

APOLIPOPROTEIN C-III; FATTY LIVER; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENOTYPE; GLUCOSE TOLERANCE TEST; HUMANS; INSULIN RESISTANCE; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; OBESITY, ABDOMINAL; POLYMORPHISM, SINGLE NUCLEOTIDE; PREVALENCE; TRIGLYCERIDES;

EID: 84862193848     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2011.154     Document Type: Article

References (51)

1. Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010; 51: 679-689.
2. Tilg H, Hotamisligil GS. Nonalcoholic fatty liver disease: cytokine-adipokine interplay and regulation of insulin resistance. Gastroenterology 2006; 131: 934-945. (Pubitemid 44307061)
3. Roden M. Mechanisms of Disease: hepatic steatosis in type 2 diabetesFpathogenesis and clinical relevance. Nat Clin Pract Endocrinol Metab 2006; 2: 335-348. (Pubitemid 43885913)
4. Stefan N, Kantartzis K, Haring HU. Causes and metabolic consequences of fatty liver. Endocr Rev 2008; 29: 939-960.
5. Stepanova M, Rafiq N, Younossi ZM. Components of metabolic syndrome are independent predictors of mortality in patients with chronic liver disease: a population-based study. Gut 2010; 59: 1410-1415.
6. Targher G, Bertolini L, Poli F, Rodella S, Scala L, Tessari R et al. Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes 2005; 54: 3541-3546. (Pubitemid 43334347)
7. Kotronen A, Yki-Jarvinen H. Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol 2008; 28: 27-38.
8. Fabbrini E, Magkos F, Mohammed BS, Pietka T, Abumrad NA, Patterson BWet al. Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci USA 2009; 106: 15430-15435.
9. Stefan N, Kantartzis K, Machann J, Schick F, Thamer C, Rittig K et al. Identification and characterization of metabolically benign obesity in humans. Arch Intern Med 2008; 168: 1609-1616.
10. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002; 346: 1221-1231.
11. Fassio E, Alvarez E, Dominguez N, Landeira G, Longo C. Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology 2004; 40: 820-826. (Pubitemid 39288114)
12. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 2005; 129: 113-121. (Pubitemid 41002048)
13. Stefan N, Schick F, Haring HU. Sex hormone-binding globulin and risk of type 2 diabetes. N Engl J Med 2009; 361: 2675-2676.
14. Weikert C, Stefan N, Schulze MB, Pischon T, Berger K, Joost HG et al. Plasma fetuin-a levels and the risk of myocardial infarction and ischemic stroke. Circulation 2008; 118: 2555-2562.
15. Kantartzis K, Machann J, Schick F, Fritsche A, Haring HU, Stefan N. The impact of liver fat vs visceral fat in determining categories of prediabetes. Diabetologia 2010; 53: 882-889.
16. Harrison SA, Day CP. Benefits of lifestyle modification in NAFLD. Gut 2007; 56: 1760-1769.
17. Kantartzis K, Thamer C, Peter A, Machann J, Schick F, Schraml C et al. High cardiorespiratory fitness is an independent predictor of the reduction in liver fat during a lifestyle intervention in nonalcoholic fatty liver disease. Gut 2009; 58: 1281-1288.
18. Tilg H, Moschen A. Update on nonalcoholic fatty liver disease: genes involved in nonalcoholic fatty liver disease and associated inflammation. Curr Opin Clin Nutr Metab Care 2010; 13: 391-396.
19. Dongiovanni P, Valenti L, Rametta R, Daly AK, Nobili V, Mozzi E et al. Genetic variants regulating insulin receptor signalling are associated with the severity of liver damage in patients with non-alcoholic fatty liver disease. Gut 2010; 59: 267-273.
20. Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet 2008; 40: 1461-1465.
21. Kantartzis K, Peter A, Machicao F, Machann J, Wagner S, Konigsrainer I et al. Dissociation between fatty liver and insulin resistance in humans carrying a variant of the patatin-like phospholipase 3 gene. Diabetes 2009; 58: 2616-2623.
22. Kotronen A, Johansson LE, Johansson LM, Roos C,Westerbacka J, Hamsten A et al. A common variant in PNPLA3, which encodes adiponutrin, is associated with liver fat content in humans. Diabetologia 2009; 52: 1056-1060.
23. Aalto-Setala K, Fisher EA, Chen X, Chajek-Shaul T, Hayek T, Zechner R et al. Mechanism of hypertriglyceridemia in human apolipoprotein (apo) CIII transgenic mice. Diminished very low density lipoprotein fractional catabolic rate associated with increased apo CIII and reduced apo E on the particles. J Clin Invest 1992; 90: 1889-1900.
24. de Silva HV, Lauer SJ, Wang J, Simonet WS, Weisgraber KH, Mahley RWet al. Overexpression of human apolipoprotein C-III in transgenic mice results in an accumulation of apolipoprotein B48 remnants that is corrected by excess apolipoprotein E. J Biol Chem 1994; 269: 2324-2335. (Pubitemid 24035450)
25. Zheng C, Khoo C, Ikewaki K, Sacks FM. Rapid turnover of apolipoprotein C-III-containing triglyceride-rich lipoproteins contributing to the formation of LDL subfractions. J Lipid Res 2007; 48: 1190-1203. (Pubitemid 46708686)
26. Olivieri O, Bassi A, Stranieri C, Trabetti E, Martinelli N, Pizzolo F et al. Apolipoprotein C-III, metabolic syndrome, and risk of coronary artery disease. J Lipid Res 2003; 44: 2374-2381. (Pubitemid 38082496)
27. Li WW, Dammerman MM, Smith JD, Metzger S, Breslow JL, Leff T. Common genetic variation in the promoter of the human apo CIII gene abolishes regulation by insulin and may contribute to hypertriglyceridemia. J Clin Invest 1995; 96: 2601-2605.
28. Olivieri O, Stranieri C, Bassi A, Zaia B, Girelli D, Pizzolo F et al. ApoC-III gene polymorphisms and risk of coronary artery disease. J Lipid Res 2002; 43: 1450-1457.
29. Tilly P, Sass C, Vincent-Viry M, Aguillon D, Siest G, Visvikis S. Biological and genetic determinants of serum apoC-III concentration: reference limits from the Stanislas Cohort. J Lipid Res 2003; 44: 430-436. (Pubitemid 37287787)
30. Ferns GA, Stocks J, Ritchie C, Galton DJ. Genetic polymorphisms of apolipoprotein C-III and insulin in survivors of myocardial infarction. Lancet 1985; 2: 300-303. (Pubitemid 15045131)
31. Petersen KF, Dufour S, Hariri A, Nelson-Williams C, Foo JN, Zhang XM et al. Apolipoprotein C3 gene variants in nonalcoholic fatty liver disease. N Engl J Med 2010; 362: 1082-1089.
32. Kozlitina J, Boerwinkle E, Cohen JC, Hobbs HH. Dissociation between APOC3 variants, hepatic triglyceride content and insulin resistance. Hepatology 2011; 53: 467-474.
33. Diehl AM. Genetic susceptibility to hepatic steatosis. N Engl J Med 2010; 362: 1142-1143.
34. Ruiz-Narvaez EA, Sacks FM, Campos H. Abdominal obesity and hyperglycemia mask the effect of a common APOC3 haplotype on the risk of myocardial infarction. Am J Clin Nutr 2008; 87: 1932-1938. (Pubitemid 351872661)
35. Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F. Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 2009; 51: 433-445.
36. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 1999; 22: 1462-1470. (Pubitemid 29418240)
37. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412-419. (Pubitemid 15018832)
38. Stefan N, Machicao F, Staiger H, Machann J, Schick F, Tschritter O et al. Polymorphisms in the gene encoding adiponectin receptor 1 are associated with insulin resistance and high liver fat. Diabetologia 2005; 48: 2282-2291. (Pubitemid 41618919)
39. Stefan N, Fritsche A, Weikert C, Boeing H, Joost HG, Haring HU et al. Plasma fetuin-A levels and the risk of type 2 diabetes. Diabetes 2008; 57: 2762-2767.
40. Stefan N, Hennige AM, Staiger H, Machann J, Schick F, Krober SM et al. Alpha2-Heremans-Schmid glycoprotein/fetuin-A is associated with insulin resistance and fat accumulation in the liver in humans. Diabetes Care 2006; 29: 853-857. (Pubitemid 44115306)
41. Jong MC, Hofker MH, Havekes LM. Role of ApoCs in lipoprotein metabolism: functional differences between ApoC1, ApoC2, and ApoC3. Arterioscler Thromb Vasc Biol 1999; 19: 472-484. (Pubitemid 29135144)
42. Ito Y, Azrolan N, O'Connell A, Walsh A, Breslow JL. Hypertriglyceridemia as a result of human apo CIII gene expression in transgenic mice. Science 1990; 249: 790-793.
43. Maeda N, Li H, Lee D, Oliver P, Quarfordt SH, Osada J. Targeted disruption of the apolipoprotein C-III gene in mice results in hypotriglyceridemia and protection from postprandial hypertriglyceridemia. J Biol Chem 1994; 269: 23610-23616. (Pubitemid 24293564)
44. von Eckardstein A, Holz H, Sandkamp M, Weng W, Funke H, Assmann G. Apolipoprotein C-III(Lys58-Glu). Identification of an apolipoprotein C-III variant in a family with hyperalphalipoproteinemia. J Clin Invest 1991; 87: 1724-1731.
45. Pollin TI, Damcott CM, Shen H, Ott SH, Shelton J, Horenstein RB et al. A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science 2008; 322: 1702-1705.
46. Kawakami A, Aikawa M, Libby P, Alcaide P, Luscinskas FW, Sacks FM. Apolipoprotein CIII in apolipoprotein B lipoproteins enhances the adhesion of human monocytic cells to endothelial cells. Circulation 2006; 113: 691-700.
47. Kawakami A, Aikawa M, Nitta N, Yoshida M, Libby P, Sacks FM. Apolipoprotein CIII-induced THP-1 cell adhesion to endothelial cells involves pertussis toxin-sensitive G protein-and protein kinase C alpha-mediated nuclear factor-kappaB activation. Arterioscler Thromb Vasc Biol 2007; 27: 219-225. (Pubitemid 46360402)
48. Altomonte J, Cong L, Harbaran S, Richter A, Xu J, Meseck M et al. Foxo1 mediates insulin action on apoC-III and triglyceride metabolism. J Clin Invest 2004; 114: 1493-1503. (Pubitemid 40385579)
49. van Hoek M, van Herpt TW, Dehghan A, Hofman A, Lieverse AG, van Duijn CM,Witteman JC, Sijbrands EJ. Association of an APOC3 promoter variant with type 2 diabetes risk and need for insulin treatment in lean persons. Diabetologia 2011; 54: 1360-1367.
50. Kantartzis K, Machicao F, Machann J, Schick F, Fritsche A, Haring HU et al. The DGAT2 gene is a candidate for the dissociation between fatty liver and insulin resistance in humans. Clin Sci (Lond) 2009; 116: 531-537.
51. Amaro A, Fabbrini E, Kars M, Yue P, Schechtman K, Schonfeld G et al. Dissociation between intrahepatic triglyceride content and insulin resistance in familial hypobetalipoproteinemia. Gastroenterology 2010; 139: 149-153.