Genomic and metabolic responses to methionine-restricted and methionine-restricted, cysteine-supplemented diets in fischer 344 rat inguinal adipose tissue, liver and quadriceps muscle

Journal of Nutrigenetics and Nutrigenomics

Volumn 5, Issue 3, 2012, Pages 132-157

  Perrone, Carmen E ^a   Mattocks, Dwight A L ^a   Plummer, Jason D ^a   Chittur, Sridar V ^b   Mohney, Rob ^c   Vignola, Katie ^c   Orentreich, David S ^a   Orentreich, Norman ^a  

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

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c METABOLON INC   (United States)

Author keywords

Cysteine supplementation; Gene expression; Inguinal adipose tissue; Liver; Mass spectrometry; Metabolism; Methionine restriction; Microarrays; Muscle; qPCR

Indexed keywords

13 HYDROXYOCTADECADIENOIC ACID; 3 HYDROXYBUTYRIC ACID; 5 METHYLTETRAHYDROFOLIC ACID; 9 HYDROXYOCTADECADIENOIC ACID; CYSTATHIONINE BETA SYNTHASE; CYSTEINE; FATTY ACID; FIBROBLAST GROWTH FACTOR 21; HOMOCYSTEINE; LONG CHAIN FATTY ACID; METHIONINE; METHIONINE SULFOXIDE; PYRIDOXINE; SULFUR AMINO ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ABDOMINAL FAT; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CAV1 GENE; CDH17 GENE; CONTROLLED STUDY; CXCL16 GENE; DIET RESTRICTION; DIET SUPPLEMENTATION; ELOVL6 GENE; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FGF21 GENE; FISCHER 344 RAT; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOMICS; GLUCONEOGENESIS; GLYCOGENOLYSIS; GLYCOLYSIS; INFLAMMATION; INSULIN SENSITIVITY; KETOGENESIS; LIFESPAN; LIPID METABOLISM; LIPOGENESIS; LIPOLYSIS; LIVER; LPIN1 GENE; MALE; MASS SPECTROMETRY; METABOLISM; METHIONINE RESTRICTION; MICROARRAY ANALYSIS; MMP12 GENE; MYBL1 GENE; NONHUMAN; OBESITY; OXIDATION; PC GENE; PCK1 GENE; PDK1 GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUADRICEPS FEMORIS MUSCLE; QUANTITATIVE ANALYSIS; RAT; WESTERN BLOTTING;

ADIPOSE TISSUE; ANIMALS; CARBOHYDRATES; CYSTATHIONINE BETA-SYNTHASE; CYSTEINE; DIET; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUCONEOGENESIS; INFLAMMATION; KETONES; LIPID METABOLISM; LIVER; MALE; MASS SPECTROMETRY; METHIONINE; NUTRIGENOMICS; QUADRICEPS MUSCLE; RATS; RATS, INBRED F344; TETRAHYDROFOLATES; TISSUE DISTRIBUTION;

EID: 85027927963     PISSN: 16616499     EISSN: 16616758     Source Type: Journal    
DOI: 10.1159/000339347     Document Type: Article

References (63)

1. Orentreich N, Matias JR, DeFelice A, Zimmerman JA: Low methionine ingestion by rats extends life span. J Nutrition 1993; 123: 269-274.
2. Zimmerman JA, Malloy V, Krajcik R, Orentreich N: Nutritional control of aging. Expt Gerontol 2003; 38: 47-52.
3. Malloy V, Krajcik R, Bailey S, Hristopoulos G, Plummer J, Orentreich N: Methionine restriction decreases visceral fat mass and preserves insulin action in aging male Fischer 344 rats independent of energy restriction. Aging Cell 2006; 5: 305-314.
4. Perrone CE, Mattocks DAL, Hristopoulos G, Plummer JD, Krajcik RA, Orentreich N: Methionine restriction effects on 11 -HSD1 activity and lipogenic/lipolytic balance in F344 rat adipose tissue. J Lipid Res 2008; 49: 12-23.
5. Hasek BE, Stewart LK, Henagan TM, Boudreau A, Lenard NR, Black C, Shin J, Huypens P, Malloy VL, Plaisance EP, Krajcik RA, Orentreich N, Gettys TW: Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am J Physiol Regul Integr Comp Physiol 2010; 299:R728-R739.
6. Perrone CE, Mattocks DAL, Jarvis-Morar M, Plummer JD, Orentreich N: Methionine restriction effects on mitochondrial biogenesis and aerobic capacity in white adipose tissue, liver and skeletal muscle of F344 rats. Metab Clin Expt 2010; 59: 1000-1011.
7. Elshorbagy A, Valdivia-Garcia M, Refsum H, Smith AD, Mattocks DAL, Perrone CE: Sulfur amino acids in methionine- restricted rats: hyperhomocysteinemia. Nutrition 2010; 26: 1201-1204.
8. Elshorbagy A, Nurk E, Gjesdal CG, Tell GS, Ueland PM, Nygård O, Tverdal A, Vollset SE, Smith AD, Refsum H: Homocysteine, cysteine, and body composition in the Hordaland Homocysteine Study: does cysteine link amino acid and lipid metabolism? Am J Clin Nutr 2008; 88: 738-746.
9. Elshorbagy A, Valdivia-Garcia M, Mattocks DAL, Plummer JD, Smith AD, Drevon CA, Refsum H, Perrone CE: Cysteine supplementation reverses methionine restriction effects on rat adiposity: significance of stearoyl-coenzyme Adesaturase. J Lipid Res 2011; 52: 104-112.
10. Sampath H, Ntambi JM: The role of stearoyl-CoA desaturase in obesity, insulin resistance and inflammation. Ann NY Acad Sci 2011; 1243: 47-53.
11. Wang J, Wu G, Zhou H, Wang F: Emerging technologies for amino acid nutrition research in the post-genome era. Amino Acids 2009; 37: 177-186.
12. Kussmann M, Raymond F, Affolter M: Omics-driven biomarker discovery in nutrition and health. J Biotech 2006; 124: 758-787.
13. Zhang X, Yap Y, Wei D, Chen G, Chen F: Novel omics technologies in nutrition research. Biotech Adv 2008; 26: 169-176.
14. de Graaf AA, Freidig AP, De Roos B, Jamshidi N, Heinemann M, Rullmann JAC, Hall KD, Adiels M, van Ommen B: Nutritional systems biology modeling: from molecular mechanisms to physiology. PLoS Comput Biol 2009; 5:e1000554.
15. Richie JP, Leutzinger Y, Parthasarathy S, Malloy V, Orentreich N, Zimmerman JA: Methionine restriction increases blood glutathione and longevity in F344 rats. FASEB J 1994; 8: 1302-1307.
16. Evans AM, DeHaven CD, Barret T, Mitchell M, Milgram E: Integrated, non-targeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small molecule complement of biological systems. Anal Chem 2009; 81: 6656-6667.
17. Reitman ZJ, Jin G, Karoly ED, Spasojevic I, Yang J, Kinzler KW, He Y, Bigner DD, Vogelstein B, Yan H: Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc Natl Acad Sci USA 2011; 108: 3270-3275.
18. Ohta T, Matsutomi N, Tsutsui N, Sakairi T, Mitchell M, Milburn MV, Ryals JA, Beebe KD, Guo L: Untargeted metabolomic profiling as an evaluative tool of fenofibrate-induced toxicology in Fischer 344 male rats. Toxicol Pathol 2009; 37: 521-535.
19. DeHaven CD, Evans AM, Dai H, Lawton KA: Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Cheminform 2010; 2: 9.
20. Coskun T, Bina HA, Schneider MA, Dunbar JD, Hu CC, Chen Y, Moller DE, Kharitonenkov A: Fibroblast growth factor 21 corrects obesity in mice. Endocrinology 2008; 149: 6018-6027.
21. Xu J, Lloyd DJ, Hale C, Stanislau S, Chen M, Sivits G, Vonderfecht S, Hecht R, Li YS, Lindberg RA, Chen JL, Jung DY, Zhang Z, Ko HJ, Kim JK, Véniant MM: Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure and improves insulin sensitivity in diet-induced obese mice. Diabetes 2009; 58: 250-259.
22. Plaisance EP, Greenway FL, Boudreau A, Hill KL, Johnson WD, Krajcik RA, Perrone CE, Orentreich N, Cefalu WT, Gettys TW: Dietary methionine restriction increases fat oxidation in obese adults with metabolic syndrome. J Clin Endocrinol Metab 2011; 96:E836-E840.
23. Avila MA, García-Trevijano ER, Lu SC, Corrales FJ, Mato JM: Methylthioadenosine. Int J Biochem Cell Biol 2004; 36: 2125-2130.
24. Wang L, Gill R, Pedersen TL, Higgings LJ, Neuman JW, Rutledge JC: Triglyceride-rich lipoprotein lipolysis releases neutral and FFAs that induce cell inflammation. J Lipid Res 2009; 50: 204-213.
25. Adams AC, Astapova I, Fisher FM, Badman MK, Kurgansky KE, Flier JS, Hollenberg AN, Maratos-Flier E: Thyroid hormone regulates hepatic expression of fibroblast growth factor 21 in a PPARalpha-dependent manner. J Biol Chem 2010; 285: 14078-14082.
26. Yu J, Yu B, Jiang H, Chen D: Conjugated linoleic acid induces hepatic expression of fibroblast growth factor 21 through PPAR . Br J Nutr 2011; 18: 1-5.
27. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT, Hansen BC, Shanafelt AB, Etgen GJ: The metabolic state of diabetic monkeys is regulated by fibroblast growth factor 21. Endocrinology 2007; 148: 774-781.
28. Chau MDL, Gao J, Yang Q, Wu Z, Gromada J: Fibroblast growth factor 21 regulates energy metabolism by activating the AMPK-SIRT1-PGC1 pathway. Proc Natl Acad Sci USA 2010; 107: 12553-12558.
29. Fisher FM, Estall JL, Adams AC, Antonellis PJ, Bina HA, Flier JS, Kharitonenkov A, Spiegelman BM, Maratos-Flier E: Integrated regulation of hepatic metabolism by fibroblast growth factor 21 (FGF21) in vivo. Endocrinology 2011; 152: 2996-3004.
30. Poudyal H, Panchal SK, Diwan V, Brown L: Omega-3 fatty acids and metabolic syndrome: effects and emerging mechanisms of action. Prog Lipid Res 2011; 50: 372-387.
31. Han GS, Carman GM: Characterization of the human lipin1-encoded phosphatidate phosphatase isoforms. J Biol Chem 2010; 285: 14628-14638.
32. Koh YK, Lee MY, Kim JW, Kim M, Moos JS, Lee YJ, Ahn YH, Kim KS: Lipin1 is a key factor for the maturation and maintenance of adipocytes in the regulatory network with CCAAT/enhancer-binding protein alpha and peroxisomeproliferator activated receptor gamma 2. J Biol Chem 2008; 283: 34896-34906.
33. Hanson RW, Reshef L: Glyceroneogenesis revisited. Biochimie 2003; 85: 1199-1205.
34. Beale EG, Hammer RE, Antoine B, Forest C: Glyceroneogenesis comes of age. FASEB J 2002; 16: 1695-1696.
35. Nye C, Kim J, Kalhan SC, Hanson RW: Reassessing triglyceride synthesis in adipose tissue. Trends Endocrinol Metab 2008; 19: 356-361.
36. Sudgen MC, Holness MJ: Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 2003; 284:E855-E862.
37. Ferrante AW Jr: Obesity-induced inflammation: a metabolic dialogue in the language of inflammation. J Intern Med 2007; 262: 408-414.
38. Zeyda M, Gollinger K, Kriehuber E, Kiefer FW, Neuhofer A, Stulnig TM: Newly identified adipose tissue macrophage populations in obesity with distinct chemokine and chemokine receptor expression. Int J Obesity 2010; 34: 1684-1694.
39. Lee HS, Park JH, Kang JH, Kawada T, Yu R, Han IS: Chemokine and chemokine receptor gene expression in the mesenteric adipose tissue of KKAy mice. Cytokine 2009; 46: 160-165.
40. Weissberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K, Charo I, Leibel RL, Ferrante AW Jr: CCR2 modulates inflammatory and metabolic effects of high fat diet. J Clin Invest 2006; 116: 115-124.
41. Kopecky J, Rossmeisl M, Flachs P, Kuda O, Brauner P, Jilkova Z, Stankova B, Tvrzicka E, Bryhn M: n -PUFA: bioavailability and modulation of adipose tissue function. Proc Nutr Soc 2009; 68: 361-369.
42. Flasch P, Rossmeisl M, Bryhn M, Kopecky J: Cellular and molecular effects of n3-polyunsaturated fatty acids on adipose tissue biology and metabolism. Clin Sci (Lond) 2009; 116: 1-16.
43. Delarue J, LeFoll C, Corporeau C, Lucas D: N3 long-chain polyunsaturated fatty acids: a nutritional tool to prevent insulin resistance associated with type-2 diabetes and obesity? Reprod Nutr Dev 2004; 44: 289-299.
44. Elshorbagy A, Church C, Valdivia-Garcia M, Smith AD, Refsum H, Cox R: Dietary cysteine level affects metabolic rate and glycaemic control in adult mice. J Nutr Biochem 2012; 23: 332-340.
45. de Villiers WJ, Cai L, Webb NR, de Beer MC, van der Westhuyzen DR, de Beer FC: CD36 does not play a direct role in HDL or LDL metabolism. J Lipid Res 2001; 42: 1231-1238.
46. Smith BK, Jain SS, Rimbaud S, Dam A, Quadrilatero J, Ventura-Clapier V, Bonen A, Holloway GP: FAT/CD36 is located on the outer mitochondrial membrane, upstream of long-chain acyl-CoA synthase and regulates palmitate oxidation. Biochem J 2011; 437: 125-134.
47. Chen SJ, Rader DJ, Tazeelar J, Kawashiri M, Gao G, Wilson JM: Prolonged correction of hyperlipidemia in mice with familial hypercholesterolemia using an adeno-associated viral vector expressing very-low density lipoprotein receptor. Mol Ther 2000; 2: 256-261.
48. Iynedjian PB: Molecular physiology of mammalian glucokinase. Cell Mol Life Sci 2009; 66: 27-42.
49. Filling C, Keller B, Hirschberg D, Marschall H-U, Jörnvall H, Bennet MJ, Oppermann U: Role of short-chain hydroxyacyl CoA dehydrogenases in SCHAD deficiency. Biochem Biophys Res Commun 2008; 368: 6-11.
50. Yang X, Deignan JL, Qi H, Zhu J, Qian S, Zhong J, Torosyan G, Majid S, Falkard B, Kleinhanz RR, Karlsson J, Castellani LW, Mumick S, Wang K, Xie T, Coon M, Zhang C, Estrada-Smith D, Farber CR, Wang SS, van Nas A, Ghalzarpour A, Zhang B, MacNeil DJ, Lamb JR, Dipple KM, Reitman ML, Mehrabian M, Lum PY, Schadt EE, Lusis AJ, Drake TA: Validation of candidate causal genes for obesity that affect shared metabolic pathways and networks. Nat Gen 2009; 41: 415-423.
51. Bigorgne AE, Bouchet-Delboss L, Naveau S, Dagher I, Prévot S, Durand-Gasselin I, Couderc J, Valet P, Emilie D, Perlemuter G: Obesity-induced lymphocyte hyperresponsiveness to chemokines: a new mechanism of fatty liver inflammation in obese mice. Gastroenterology 2008; 134: 1459-1469.
52. Lu LX, Lee NP, Chan VW, Xue W, Zender L, Zhang C, Mao M, Dai H, Wang XL, Xu MZ, Lee TK, Ng IO, Chen Y, Kung H, Lowe SW, Poon RTP, Wang JH, Luk JM: Targeting cadherin-17 inactivates Wnt signaling and inhibits tumor growth in liver carcinoma. Hepatology 2009; 50: 1453-1463.
53. Wang XQ, Luk JM, Garcia-Barcelo M, Miao X, Leung PP, Ho DW, Cheung ST, Lam BY, Cheung CK, Wong AS, Lau SS, So MT, Yu WC, Cai Q, Liu KS, Hui CK, Lan GK, Poon RT, Wong J, Fan ST: Liver intestine-cadherin (CDH17) haplotype is associated with increased risk of hepatocellular carcinoma. Clin Cancer Res 2006; 12: 5248-5252.
54. de Meijer VE, Sverdlov DY, Le HD, Popov Y, Puder M: Tissue-specific differences in inflammatory infiltrate and matrix metalloproteinase expression in adipose tissue and liver of mice with diet-induced obesity. Hepatol Res 2012; 42: 601-610.
55. Tang B, Mustafa A, Gupta S, Melnyk S, James SJ, Kruger WD: Methionine-deficient diet induces post-transcriptional down-regulation of cystathionine -synthase. Nutrition 2010; 26: 1170-1175.
56. Remacha AF, Souto JC, Piñana JL, Sardà MP, Queraltó AM, Martí-Fabregas J, García-Moll X, Férnandez C, Rodríguez A, Cuesta J: Vitamin B12 deficiency, hyperhomocysteinemia and thrombosis: a case and control study. Int J Hematol 2011; 93: 458-464.
57. Cook S, Hess OM: Homocysteine and B vitamins. Handb Exp Pharmacol 2005; 170: 325-338.
58. Hollowell JG Jr, Coryell ME, Hall WK, Findley JK, Thevaos TG: Homocystinuria as affected by pyridoxine, folic acid and vitamin B12. Proc Soc Exp Biol Med 1968; 129: 327-333.
59. Gurdöl F: Does methionine restriction cause hyperhomocysteinemia? Nutrition 2010; 26: 1205-1206.
60. Abdul-Ghani MA, DeFronzo RA: Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotech 2010; 2010: 476279.
61. Wang Y, Barbacioru C, Hyland F, Xiao W, Hunkapiller KL, Blake J, Chan F, Gonzalez C, Zhang L, Samaha RR: Large scale real-time PCR validation on gene expression measurements on two commercial long-oligonucleotide microarrays. BMC Genomics 2006; 7: 59.
62. Morey JS, Ryan JC, Van Dolan FM: Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 2006; 8: 175-193.
63. Kalhan SC, Uppal SO, Moorman JL, Bennett C, Gruca LL, Parimi PS, Dasarathy S, Serre D, Hanson RW: Metabolic and genomic response to dietary isocaloric protein restriction in the rat. J Biol Chem 2011; 286: 5266-5277.