Methionine restriction prevents the progression of hepatic steatosis in leptin-deficient obese mice

Metabolism: Clinical and Experimental

Volumn 62, Issue 11, 2013, Pages 1651-1661

  Malloy, Virginia L ^a   Perrone, Carmen E ^a   Mattocks, Dwight A L ^a   Ables, Gene P ^a   Caliendo, Nicholas S ^a   Orentreich, David S ^a   Orentreich, Norman ^a  

^a Orentreich Foundation for the Advancement of Science Inc   (United States)

Author keywords

Adiponectin; Fatty acid oxidation; Fatty liver; Inflammation; Triglyceride

Indexed keywords

3 HYDROXYBUTYRIC ACID; CHEMOKINE RECEPTOR CCR2; FATTY ACID; INSULIN; MESSENGER RNA; METHIONINE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY FAT; CONTROLLED STUDY; DIET RESTRICTION; FATTY ACID BLOOD LEVEL; FATTY ACID OXIDATION; FATTY LIVER; FOOD INTAKE; GENE EXPRESSION; HISTOPATHOLOGY; INSULIN BLOOD LEVEL; LEPTIN DEFICIENCY; MALE; MOUSE; NONHUMAN; OBESITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT REDUCTION;

ACAC; ACADVL; ACETYL-COA CARBOXYLASE; ACYL-COENZYME A DEHYDROGENASE, VERY LONG CHAIN; ADIPONECTIN; ALANINE AMINOTRANSFERASE; ALT; APOB; APOLIPOPROTEIN B; ASPARTATE AMINOTRANSFERASE; AST; C-C CHEMOKINE RECEPTOR-2; CARBOHYDRATE REGULATORY BINDING PROTEIN; CARNITINE PALMITOYLTRANSFERASE-1A; CCR2; CD 36; CF; CHREBP; CONTROL-FED; CPT1A; DGAT; DIACYLGLYCEROL O-ACYLTRANSFERASE; EGF-LIKE MODULE-CONTAINING MUCIN-LIKE HORMONE RECEPTOR-LIKE 1; EMR1; FAO; FASN; FATTY ACID OXIDATION; FATTY ACID SYNTHASE; FATTY LIVER; FFA; FREE FATTY ACIDS; GLUTATHIONE; GPAM; GSH; HADHA AND HADHB; HDL; HEPATIC CD36 ANTIGEN; HFD; HIGH-DENSITY LIPOPROTEIN; HIGH-FAT DIET; HIGH-MOLECULAR-WEIGHT; HMW; HOMA; HOMEOSTASIS MODEL ASSESSMENT; HYDROXYACYL-COENZYME A DEHYDROGENASE/3-KETOACYL-COENZYME A THIOLASE/ENOYL-COENZYME A HYDRATASE (TRIFUNCTIONAL PROTEIN), ALPHA AND BETA SUBUNITS, RESPECTIVELY; IL6; INFLAMMATION; INSULIN RESISTANCE; INTEGRIN ALPHA X; INTERLEUKIN-6; IR; ITGAX; LDL; LIVER X-RECEPTOR; LOW-DENSITY LIPOPROTEIN; LXR; METHIONINE RESTRICTION; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; MITOCHONDRIAL GLYCEROL-3-PHOSPHATE ACYLTRANSFERASE; MR; MTTP; NAFLD; NASH; NON-ALCOHOLIC FATTY LIVER DISEASE; NON-ALCOHOLIC STEATOHEPATITIS; OB/OB; OBESE MOUSE; PATATIN-LIKE PHOSPHOLIPASE DOMAIN CONTAINING 2; PATATIN-LIKE PHOSPHOLIPASE DOMAIN CONTAINING 3; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR Α; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR Γ; PKLR; PNPLA2; PNPLA3; PPARΑ; PPARΓ; PYRUVATE KINASE-LIVER AND RED BLOOD CELL; REACTIVE OXYGEN SPECIES; ROS; SCD1; SREBF1; STEAROYL-COENZYME A DESATURASE-1; STEROL REGULATORY ELEMENT BINDING TRANSCRIPTION FACTOR 1; TG; TNF-Α; TRIGLYCERIDE; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-Α; VERY-LOW-DENSITY LIPOPROTEIN; VLDL;

3-HYDROXYBUTYRIC ACID; ANIMALS; BIOLOGICAL MARKERS; BLOOD GLUCOSE; DIET; DISEASE PROGRESSION; FATTY ACIDS; FATTY LIVER; GENE EXPRESSION REGULATION; HOMEOSTASIS; INFLAMMATION; INSULIN; LEPTIN; LIPID METABOLISM; LIPOPROTEINS, VLDL; LIVER; MALE; METHIONINE; MICE; MICE, OBESE; OBESITY; OXIDATION-REDUCTION; SEVERITY OF ILLNESS INDEX; TRIGLYCERIDES;

EID: 84886380579     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.06.012     Document Type: Article

References (57)

1. M. Lazo, S.F. Solga, and A. Horska Effect of a 12-month intensive lifestyle intervention on hepatic steatosis in adults with type 2 diabetes Diabetes Care 33 2010 2156 2163
2. J.C. Cohen, J.D. Horton, and H.H. Hobbs Human fatty liver disease: old questions and new insights Science 332 2011 1519 1523
3. J.B. Schwimmer, R. Deutsch, and T. Kahen Prevalence of fatty liver in children and adolescents Pediatrics 118 2006 1388 1393 (Pubitemid 46393782)
4. A. Koteish, and A.M. Diehl Animal models of steatosis Semin Liver Dis 21 2001 89 104 (Pubitemid 32240489)
5. B.N. Reid, G.P. Ables, and O.A. Otlivanchik Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis J Biol Chem 283 2008 13087 13099
6. F.P.W. Radner, I.E. Streith, and G. Schoiswohl Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identification-58 (CGI-58) J Biol Chem 285 2010 7300 7311
7. A.E. Obstfeld, E. Sugaru, and M. Thearle C-C chemokine receptor 2 (CCR2) regulates the hepatic recruitment of myeloid cells that promote obesity-induced hepatic steatosis Diabetes 59 2010 916 925
8. S.S. Choi, and A.M. Diehl Hepatic triglyceride synthesis and nonalcoholic fatty liver disease Curr Opin Lipidol 19 2008 295 300 (Pubitemid 351653569)
9. R.A. Miller, G. Buehner, and Y. Chang Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance Aging Cell 4 2005 119 125 (Pubitemid 41602745)
10. V.L. Malloy, R.A. Krajcik, and S.J. Bailey Methionine restriction decreases visceral fat mass and preserves insulin action in aging male Fischer 344 rats independent of energy restriction Aging Cell 5 2006 305 314 (Pubitemid 44103246)
11. N. Orentreich, J.R. Matias, and A. DeFelice Low methionine ingestion by rats extends life span J Nutr 123 1993 269 274 (Pubitemid 23063011)
12. B.E. Hasek, L.K. Stewart, and T.M. Henagan Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states Am J Physiol Regul Integr Comp Physiol 299 2010 R728 R739
13. E.P. Plaisance, T.M. Henagan, and H. Echlin Role of beta-adrenergic receptors in the hyperphagic and hypermetabolic responses to dietary methionine restriction Am J Physiol Regul Integr Comp Physiol 299 2010 R740 R750
14. C.E. Perrone, D.A.L. Mattocks, and M. Jarvis-Morar Methionine restriction effects on mitochondrial biogenesis and aerobic capacity in white adipose tissue, liver, and skeletal muscle of F344 rats Metab Clin Exp 59 2010 1000 1011
15. A.K. Elshorbagy, M. Valdivia-Garcia, and D.A.L. Mattocks Cysteine supplementation reverses methionine restriction effects on rat adiposity: significance of stearoyl-coenzyme A desaturase J Lipid Res 52 2011 104 112
16. Q.M. Anstee, and R.D. Goldin Mouse models in non-alcoholic fatty liver disease and steatohepatitis research Int J Exp Pathol 87 2006 1 16
17. C.Z. Larter, and M.M. Yeh Animal models of NASH: getting both pathology and metabolic context right J Gastroenterol Hepatol 23 2008 1635 1648
18. J. Folch, M. Lees, and G.H.S. Stanley A simple method for the isolation and purification of total lipids from animal tissues J Biol Chem 226 1957 497 509
19. Z. Li, S. Yang, and H. Lin Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease Hepatology 37 2003 343 350 (Pubitemid 36152533)
20. R.C. Noland, T.L. Woodlief, and B.R. Whitfield Peroxisomal-mitochondrial oxidation in a rodent model of obesity-associated insulin resistance Am J Physiol Endocrinol Metab 293 2007 E986 E1001
21. D.R. Matthews, J.P. Hosker, and A.S. Rudenski Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man Diabetologia 28 1985 412 419 (Pubitemid 15018832)
22. C. Dubuquoy, C. Robichon, and F. Lasnier Distinct regulation of adiponutrin/PNPLA3 gene expression by the transcription factors ChREBP and SREBP1c in mouse and human hepatocytes J Hepatol 55 2011 145 153
23. G.P. Ables, C.E. Perrone, and D. Orentreich Methionine-restricted C57BL/6 J mice are resistant to diet-induced obesity and insulin resistance but have low bone density PLoS One 7 2012 e51357
24. L. Ma, L.N. Robinson, and H.C. Towle ChREBP*Mlx is the principal mediator of glucose-induced gene expression in the liver J Biol Chem 281 2006 28721 28730 (Pubitemid 44507014)
25. P. Angulo Nonalcoholic fatty liver disease N Engl J Med 346 2002 1221 1231
26. A.E. Feldstein, N.W. Werneburg, and A. Canbay Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway Hepatology 40 2004 185 194 (Pubitemid 38868937)
27. T. Hajri, H. Tao, and J. Wattacheril Regulation of adiponectin production by insulin: interactions with tumor necrosis factor- and interleukin-6 Am J Physiol Endocrinol Metab 300 2010 E350 E360
28. N. Maeda, M. Takahashi, and T. Funahashi PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein Diabetes 50 2001 2094 2099 (Pubitemid 33643677)
29. A. Wieckowska, B.G. Papouchado, and Z. Li Increased hepatic and circulating interleukin-6 levels in human nonalcoholic steatohepatitis Am J Gastroenterol 103 2008 1372 1379 (Pubitemid 351813900)
30. Y. Arita, S. Kihara, and N. Ouchi Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity Biochem Biophys Res Commun 257 1999 79 83 (Pubitemid 29299050)
31. J.Y. Kim, E. van de Wall, and M. Laplante Obesity-associated improvements in metabolic profile through expansion of adipose tissue J Clin Invest 117 2007 2621 2637 (Pubitemid 47494363)
32. O. Braissant, F. Foufelle, and C. Scotto Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat Endocrinology 137 1996 354 366 (Pubitemid 26005011)
33. A. Okuno, H. Tamemoto, and K. Tobe Troglitazone increases the number of small adipocytes without the change of white adipose tissue mass in obese Zucker rats J Clin Invest 101 1998 1354 1361 (Pubitemid 28145252)
34. C. Postic, and J. Girard Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice J Clin Invest 118 2008 829 838 (Pubitemid 351364588)
35. A. Xu, Y. Wang, and H. Keshaw The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice J Clin Invest 112 2003 91 100 (Pubitemid 38056380)
36. Y. Liu, R. Retnakaran, and A. Hanley Total and high molecular weight but not trimeric or hexameric forms of adiponectin correlate with markers of the metabolic syndrome and liver injury in Thai subjects J Clin Endocrinol Metab 92 2007 4313 4318 (Pubitemid 350074750)
37. J.W. Perfield, L.C. Ortinau, and R.T. Pickering Altered hepatic lipid metabolism contributes to nonalcoholic fatty liver disease in leptin-deficient Ob/Ob mice J Obes 2013 in press:dx.doi.org/10.1155/2013/296537
38. J.M. Ntambi, M. Miyazaki, and J.P. Stoehr Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity Proc Natl Acad Sci USA 99 2002 11482 11486 (Pubitemid 34920951)
39. C.L.E. Yen, S.J. Stone, and S. Koliwad Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis J Lipid Res 49 2008 2283 2301
40. L. Abu-Elheiga, M.M. Matzuk, and K.A. Abo-Hashema Continuous fatty acid oxidation and reduced fat storage in mice lacking acetyl-CoA carboxylase 2 Science 291 2001 2613 2616 (Pubitemid 32249687)
41. T. Aoyama, J.M. Peters, and N. Iritani Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor alpha (PPARalpha) J Biol Chem 273 1998 5678 5684 (Pubitemid 28124039)
42. E.P. Plaisance, F.L. Greenway, and A. Boudreau Dietary methionine restriction increases fat oxidation in obese adults with metabolic syndrome J Clin Endocrinol Metabol 96 2011 E836 E840
43. D. Greco, A. Kotronen, and J. Westerbacka Gene expression in human NAFLD Am J Physiol Gastrointest Liver Physiol 294 2008 G1281 G1287
44. B.K. Smith, S.S. Jain, and S. Rimbaud FAT/CD36 is located on the outer mitochondrial membrane, upstream of long-chain acyl-CoA synthetase, and regulates palmitate oxidation Biochem J 437 2011 125 134
45. M. Charlton, R. Sreekumar, and D. Rasmussen Apolipoprotein synthesis in nonalcoholic steatohepatitis Hepatology 35 2002 898 904 (Pubitemid 34258385)
46. M. Raabe, M.M. Véniant, and M.A. Sullivan Analysis of the role of microsomal triglyceride transfer protein in the liver of tissue-specific knockout mice J Clin Invest 103 1999 1287 1298 (Pubitemid 29218299)
47. J. Westerbacka, M. Kolak, and T. Kiviluoto Genes involved in fatty acid partitioning and binding, lipolysis, monocyte/macrophage recruitment, and inflammation are overexpressed in the human fatty liver of insulin-resistant subjects Diabetes 56 2007 2759 2765 (Pubitemid 350044919)
48. A.M. Diehl Lessons from animal models of NASH Hepatol Res 33 2005 138 144 (Pubitemid 41799792)
49. I. García-Ruiz, C. Rodríguez-Juan, and T. Díaz-Sanjuán Effects of rosiglitazone on the liver histology and mitochondrial function in ob/ob mice Hepatology 46 2007 414 423 (Pubitemid 47344776)
50. C.W. Wu, E.S.H. Chu, and C.N.Y. Lam PPARgamma is essential for protection against nonalcoholic steatohepatitis Gene Ther 17 2010 790 798
51. C.P. Day, and O.F. James Steatohepatitis: a tale of two "hits"? Gastroenterology 114 1998 842 845
52. P. Caro, J. Gómez, and M. López-Torres Forty percent and eighty percent methionine restriction decrease mitochondrial ROS generation and oxidative stress in rat liver Biogerontology 9 2008 183 196
53. H.J. Park, D.A. DiNatale, and M.Y. Chung Green tea extract attenuates hepatic steatosis by decreasing adipose lipogenesis and enhancing hepatic antioxidant defenses in ob/ob mice J Nutr Biochem 22 2011 393 400
54. R.N. Hardwick, C.D. Fisher, and M.J. Canet Diversity in antioxidant response enzymes in progressive stages of human nonalcoholic fatty liver disease Drug Metab Dispos 38 2010 2293 2301
55. J.P. Richie Jr., Y. Leutzinger, and S. Parthasarathy Methionine restriction increases blood glutathione and longevity in F344 rats FASEB J 8 1994 1302 1307
56. J.A. Haque, R.S. McMahan, and J.S. Campbell Attenuated progression of diet-induced steatohepatitis in glutathione-deficient mice Lab Invest 90 2010 1704 1717
57. E.L. Kendig, Y. Chen, and M. Krishan Lipid metabolism and body composition in Gclm(-/-) mice Toxicol Appl Pharmacol 257 2011 338 348