Coordinated Defects in Hepatic Long Chain Fatty Acid Metabolism and Triglyceride Accumulation Contribute to Insulin Resistance in Non-Human Primates

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Kamath, Subhash ^a   Chavez, Alberto O ^a   Gastaldelli, Amalia ^a,b   Casiraghi, Francesca ^a   Halff, Glenn A ^a   Abrahamian, Gregory A ^a   Davalli, Alberto M ^a,c   Bastarrachea, Raul A ^d   Comuzzie, Anthony G ^d   Guardado Mendoza, Rodolfo ^a   Jimenez Ceja, Lilia M ^a   Mattern, Vicki ^d   Paez, Ana Maria ^a   Ricotti, Andrea ^b   Tejero, Mary E ^d   Higgins, Paul B ^d   Rodriguez Sanchez, Iram Pablo ^d   Tripathy, Devjit ^a   DeFronzo, Ralph A ^a   Dick Jr , Edward J ^d   Cline, Gary W ^e   Folli, Franco ^a,c   more..

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A; BIOLOGICAL MARKER; INSULIN; LONG CHAIN FATTY ACID; SHORT CHAIN FATTY ACID; TRIACYLGLYCEROL; UNSATURATED FATTY ACID; FATTY ACID; GLUCOSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; BODY MASS; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FATTY ACID METABOLISM; FATTY LIVER; FEMALE; HISTOPATHOLOGY; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID COMPOSITION; LIPID LIVER LEVEL; LIPID STORAGE; LIVER BIOPSY; MALE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; UPREGULATION; ANIMAL; GLUCOSE CLAMP TECHNIQUE; LIVER; METABOLISM; PATHOLOGY; STATISTICAL MODEL;

PAPIO; PRIMATES;

ACYL COENZYME A; ADIPOSITY; ANIMALS; FATTY ACIDS; FATTY ACIDS, UNSATURATED; FATTY LIVER; FEMALE; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; HUMANS; INSULIN RESISTANCE; LINEAR MODELS; LIVER; MALE; PAPIO; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRIGLYCERIDES;

EID: 84859366701     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027617     Document Type: Article

References (57)

1. Lazo M, Clark JM, (2008) The epidemiology of nonalcoholic fatty liver disease: a global perspective. Semin Liver Dis 28: 339-350.
2. Angulo P, (2007) Obesity and nonalcoholic fatty liver disease. Nutr Rev 65: S57-63.
3. Moore JB, (2010) Non-alcoholic fatty liver disease: the hepatic consequence of obesity and the metabolic syndrome. Proc Nutr Soc 69: 211-220.
4. Targher G, Day CP, Bonora E, (2010) Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 363: 1341-1350.
5. Bozzetto L, Prinster A, Mancini M, Giacco R, De Natale C, et al.(2011) Liver fat in obesity: role of type 2 diabetes mellitus and adipose tissue distribution. Eur J Clin Invest 41: 39-44.
6. Perseghin G, (2011) Lipids in the wrong place: visceral fat and nonalcoholic steatohepatitis. Diabetes Care 34 (Suppl 2): S367-370.
7. Bugianesi E, Gastaldelli A, Vanni E, Gambino R, Cassader M, et al.(2005) Insulin resistance in non-diabetic patients with non-alcoholic fatty liver disease: sites and mechanisms. Diabetologia 48: 634-642.
8. Kashyap SR, Diab DL, Baker AR, Yerian L, Bajaj H, et al.(2009) Triglyceride levels and not adipokine concentrations are closely related to severity of nonalcoholic fatty liver disease in an obesity surgery cohort. Obesity (Silver Spring) 17: 1696-1701.
9. Fabbrini E, Sullivan S, Klein S, (2010) Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51: 679-689.
10. Gastaldelli A, Cusi K, Pettiti M, Hardies J, Miyazaki Y, et al.(2007) Relationship between hepatic/visceral fat and hepatic insulin resistance in nondiabetic and type 2 diabetic subjects. Gastroenterology 133: 496-506.
11. Roden M, (2006) Mechanisms of Disease: hepatic steatosis in type 2 diabetes-pathogenesis and clinical relevance. Nat Clin Pract Endocrinol Metab 2: 335-348.
12. Nobili V, Marcellini M, Devito R, Ciampalini P, Piemonte F, et al.(2006) NAFLD in children: a prospective clinical-pathological study and effect of lifestyle advice. Hepatology 44: 458-465.
13. Deivanayagam S, Mohammed BS, Vitola BE, Naguib GH, Keshen TH, et al.(2008) Nonalcoholic fatty liver disease is associated with hepatic and skeletal muscle insulin resistance in overweight adolescents. Am J Clin Nutr 88: 257-262.
14. Rector RS, Thyfault JP, Uptergrove GM, Morris EM, Naples SP, et al.(2010) Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model. J Hepatol 52: 727-736.
15. Erion DM, Ignatova ID, Yonemitsu S, Nagai Y, Chatterjee P, et al.(2009) Prevention of hepatic steatosis and hepatic insulin resistance by knockdown of cAMP response element-binding protein. Cell Metab 10: 499-506.
16. Fabbrini E, Conte C, Magkos F, (2009) Methods for assessing intrahepatic fat content and steatosis. Curr Opin Clin Nutr Metab Care 12: 474-481.
17. Chavez AO, Lopez-Alvarenga JC, Tejero ME, Triplitt C, Bastarrachea RA, et al.(2008) Physiological and molecular determinants of insulin action in the baboon. Diabetes 57: 899-908.
18. Chavez AO, Gastaldelli A, Guardado-Mendoza R, Lopez-Alvarenga JC, Leland MM, et al.(2009) Predictive models of insulin resistance derived from simple morphometric and biochemical indices related to obesity and the metabolic syndrome in baboons. Cardiovasc Diabetol 8: 22.
19. Guardado-Mendoza R, Davalli AM, Chavez AO, Hubbard GB, Dick EJ, et al.(2009) Pancreatic islet amyloidosis, beta-cell apoptosis, and alpha-cell proliferation are determinants of islet remodeling in type-2 diabetic baboons. Proc Natl Acad Sci U S A 106: 13992-13997.
20. Zhang X, Zhang R, Raab S, Zheng W, Wang J, et al. Rhesus macaques develop metabolic syndrome with reversible vascular dysfunction responsive to pioglitazone. Circulation 124: 77-86.
21. Seth D, Leo MA, McGuinness PH, Lieber CS, Brennan Y, et al.(2003) Gene expression profiling of alcoholic liver disease in the baboon (Papio hamadryas) and human liver. Am J Pathol 163: 2303-2317.
22. Wene JD, Barnwell GM, Mitchell DS, (1982) Flavor preferences, food intake, and weight gain in baboons (Papio sp.). Physiol Behav 28: 569-573.
23. Groop LC, Bonadonna RC, DelPrato S, Ratheiser K, Zyck K, et al.(1989) Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Evidence for multiple sites of insulin resistance. J Clin Invest 84: 205-213.
24. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, et al.(2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. Journal of Clinical Endocrinology and Metabolism 85: 2402-2410.
25. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al.(1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419.
26. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, et al.(2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313-1321.
27. Neschen S, Morino K, Hammond LE, Zhang D, Liu ZX, et al.(2005) Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab 2: 55-65.
28. Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, et al.(2003) Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37: 917-923.
29. Kotronen A, Yki-Jarvinen H, (2008) Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol 28: 27-38.
30. Reaven GM, (1988) Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 37: 1595-1607.
31. Velloso LA, Folli F, Sun XJ, White MF, Saad MJ, et al.(1996) Cross-talk between the insulin and angiotensin signaling systems. Proc Natl Acad Sci U S A 93: 12490-12495.
32. Cobbold JF, Anstee QM, Goldin RD, Williams HR, Matthews HC, et al.(2009) Phenotyping murine models of non-alcoholic fatty liver disease through metabolic profiling of intact liver tissue. Clin Sci (Lond) 116: 403-413.
33. van Werven JR, Schreuder TC, Nederveen AJ, Lavini C, Jansen PL, et al.(2010) Hepatic unsaturated fatty acids in patients with non-alcoholic fatty liver disease assessed by 3.0T MR spectroscopy. Eur J Radiol 75: e102-107.
34. Hwang JH, Stein DT, Barzilai N, Cui MH, Tonelli J, et al.(2007) Increased intrahepatic triglyceride is associated with peripheral insulin resistance: in vivo MR imaging and spectroscopy studies. Am J Physiol Endocrinol Metab 293: E1663-1669.
35. Perseghin G, Scifo P, De Cobelli F, Pagliato E, Battezzati A, et al.(1999) Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48: 1600-1606.
36. Hodson L, Skeaff CM, Fielding BA, (2008) Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res 47: 348-380.
37. Peter A, Cegan A, Wagner S, Lehmann R, Stefan N, et al.(2009) Hepatic lipid composition and stearoyl-coenzyme A desaturase 1 mRNA expression can be estimated from plasma VLDL fatty acid ratios. Clin Chem 55: 2113-2120.
38. Elinav E, Ali M, Bruck R, Brazowski E, Phillips A, et al.(2009) Competitive inhibition of leptin signaling results in amelioration of liver fibrosis through modulation of stellate cell function. Hepatology 49: 278-286.
39. Friedman SL, (2004) Mechanisms of disease: Mechanisms of hepatic fibrosis and therapeutic implications. Nat Clin Pract Gastroenterol Hepatol 1: 98-105.
40. Bataller R, Brenner DA, (2005) Liver fibrosis. J Clin Invest 115: 209-218.
41. Svegliati-Baroni G, Ridolfi F, Di Sario A, Casini A, Marucci L, et al.(1999) Insulin and insulin-like growth factor-1 stimulate proliferation and type I collagen accumulation by human hepatic stellate cells: differential effects on signal transduction pathways. Hepatology 29: 1743-1751.
42. Konner AC, Bruning JC, (2011) Toll-like receptors: linking inflammation to metabolism. Trends Endocrinol Metab 22: 16-23.
43. Kotronen A, Seppanen-Laakso T, Westerbacka J, Kiviluoto T, Arola J, et al.(2010) Comparison of lipid and fatty acid composition of the liver, subcutaneous and intra-abdominal adipose tissue, and serum. Obesity (Silver Spring) 18: 937-944.
44. Pettinelli P, Videla LA, (2011) Up-Regulation of PPAR-{gamma} mRNA Expression in the Liver of Obese Patients: an Additional Reinforcing Lipogenic Mechanism to SREBP-1c Induction. J Clin Endocrinol Metab.
45. Riserus U, Basu S, Jovinge S, Fredrikson GN, Arnlov J, et al.(2002) Supplementation with conjugated linoleic acid causes isomer-dependent oxidative stress and elevated C-reactive protein: a potential link to fatty acid-induced insulin resistance. Circulation 106: 1925-1929.
46. Pischon T, Hankinson SE, Hotamisligil GS, Rifai N, Willett WC, et al.(2003) Habitual dietary intake of n-3 and n-6 fatty acids in relation to inflammatory markers among US men and women. Circulation 108: 155-160.
47. Bueno AA, Oyama LM, de Oliveira C, Pisani LP, Ribeiro EB, et al.(2008) Effects of different fatty acids and dietary lipids on adiponectin gene expression in 3T3-L1 cells and C57BL/6J mice adipose tissue. Pflugers Arch 455: 701-709.
48. Wendel AA, Purushotham A, Liu LF, Belury MA, (2008) Conjugated linoleic acid fails to worsen insulin resistance but induces hepatic steatosis in the presence of leptin in ob/ob mice. J Lipid Res 49: 98-106.
49. Bose T, Alvarenga JC, Tejero ME, Voruganti VS, Proffitt JM, et al.(2009) Association of monocyte chemoattractant protein-1 with adipocyte number, insulin resistance and liver function markers. J Med Primatol 38: 418-424.
50. Alkhouri N, Dixon LJ, Feldstein AE, (2009) Lipotoxicity in nonalcoholic fatty liver disease: not all lipids are created equal. Expert Rev Gastroenterol Hepatol 3: 445-451.
51. Li ZZ, Berk M, McIntyre TM, Feldstein AE, (2009) Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: role of stearoyl-CoA desaturase. J Biol Chem 284: 5637-5644.
52. Peter A, Cegan A, Wagner S, Elcnerova M, Konigsrainer A, et al.(2011) Relationships between hepatic stearoyl-CoA desaturase-1 activity and mRNA expression with liver fat content in humans. Am J Physiol Endocrinol Metab 300: E321-326.
53. Araya J, Rodrigo R, Videla LA, Thielemann L, Orellana M, et al.(2004) Increase in long-chain polyunsaturated fatty acid n- 6/n- 3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin Sci (Lond) 106: 635-643.
54. Li LO, Ellis JM, Paich HA, Wang S, Gong N, et al.(2009) Liver-specific loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and beta-oxidation and alters phospholipid fatty acid composition. J Biol Chem 284: 27816-27826.
55. Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, et al.(2004) Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 279: 32345-32353.
56. Samuel VT, Liu ZX, Wang A, Beddow SA, Geisler JG, et al.(2007) Inhibition of protein kinase Cepsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J Clin Invest 117: 739-745.
57. Arturi F, Succurro E, Procopio C, Pedace E, Mannino GC, et al. Nonalcoholic Fatty liver disease is associated with low circulating levels of insulin-like growth factor-I. J Clin Endocrinol Metab 96: E1640-1644.