Dietary methionine restriction in mice elicits an adaptive cardiovascular response to hyperhomocysteinemia

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Ables, Gene P ^a   Ouattara, Amadou ^a   Hampton, Thomas G ^b   Cooke, Diana ^a   Perodin, Frantz ^a   Augie, Ines ^a   Orentreich, David S ^a  

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

^b Mouse Specifics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; APOLIPOPROTEIN E; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 21; METHIONINE;

ADAPTATION; AGE; ANIMAL; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; DEFICIENCY; DIET; DISEASE PREDISPOSITION; DRUG EFFECTS; HYPERHOMOCYSTEINEMIA; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ADIPONECTIN; ADRENERGIC BETA-AGONISTS; AGE FACTORS; ANIMALS; APOLIPOPROTEINS E; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; DIET; DISEASE SUSCEPTIBILITY; FIBROBLAST GROWTH FACTORS; HYPERHOMOCYSTEINEMIA; MALE; METHIONINE; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 84924326097     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08886     Document Type: Article

References (62)

1. Miller, R. A. et al. 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, 119-125 (2005
2. Orentreich, N., Matias, J. R., DeFelice, A. & Zimmerman, J. A. Low methionine ingestion by rats extends life span. J. Nutr. 123, 269-274 (1993
3. Richie, J. P. Jr. et al. Methionine restriction increases blood glutathione and longevity in F344 rats. FASEB J. 8, 1302-1307 (1994
4. Cabreiro, F. et al. Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell 153, 228-239 (2013
5. Lee, B. C. et al. Methionine restriction extends lifespan of Drosophila melanogaster under conditions of low amino-acid status. Nat. Commun. 5, 3592 (2014
6. Sun, L., Sadighi Akha, A. A., Miller, R. A. & Harper, J. M. Life-span extension in mice by preweaning food restriction and by methionine restriction in middle age. J. Gerontol. A Biol. Sci. Med. Sci. 64, 711-722 (2009
7. Ables, G. P., Perrone, C. E., Orentreich, D.&Orentreich, N. Methionine-restricted C57BL/6J mice are resistant to diet-induced obesity and insulin resistance but have low bone density. PLoS. One 7, e51357 (2012
8. Elshorbagy, A. K. et al. Sulfur amino acids in methionine-restricted rats: Hyperhomocysteinemia. Nutrition 26, 1201-1204 (2010
9. Clarke, R. et al. Hyperhomocysteinemia: An independent risk factor for vascular disease. N. Engl. J. Med. 324, 1149-1155 (1991
10. Stipanuk, M. H. Sulfur amino acid metabolism: Pathways for production and removal of homocysteine and cysteine. Annu. Rev. Nutr. 24, 539-577 (2004
11. Austin, R. C., Lentz, S. R. & Werstuck, G. H. Role of hyperhomocysteinemia in endothelial dysfunction and atherothrombotic disease. Cell Death. Differ. 11 Suppl 1, S56-S64 (2004
12. McCully, K. S. Vascular pathology of homocysteinemia: Implications for the pathogenesis of arteriosclerosis. Am. J. Pathol. 56, 111-128 (1969
13. Moghadasian, M. H., McManus, B. M. & Frohlich, J. J. Homocyst(e)ine and coronary artery disease. Clinical evidence and genetic andmetabolic background. Arch. Intern. Med. 157, 2299-2308 (1997
14. Lentz, S. R. Homocysteine and vascular dysfunction. Life Sci. 61, 1205-1215 (1997
15. Austin, R. C., Lentz, S. R. & Werstuck, G. H. Role of hyperhomocysteinemia in endothelial dysfunction and atherothrombotic disease. Cell Death. Differ. 11 Suppl 1, S56-S64 (2004
16. Ma, S. et al. Hyperhomocysteinemia induces cardiac injury by up-regulation of p53-dependent Noxa and Bax expression through the p53 DNA methylation in ApoE(-/-) mice. Acta Biochim. Biophys. Sin. (Shanghai) 45, 391-400 (2013
17. Armitage, J. M. et al. Effects of homocysteine-lowering with folic acid plus vitamin B12 vs placebo on mortality and major morbidity in myocardial infarction survivors: A randomized trial. JAMA 303, 2486-2494 (2010
18. Baszczuk, A. & Kopczynski, Z. Hyperhomocysteinemia in patients with cardiovascular disease. Postepy Hig. Med. Dosw. (Online.) 68, 579-589 (2014
19. Marcus, J., Sarnak, M. J. &Menon, V. Homocysteine lowering and cardiovascular disease risk: Lost in translation. Can. J. Cardiol. 23, 707-710 (2007
20. Marti-Carvajal, A. J., Sola, I., Lathyris, D., Karakitsiou, D. E. & Simancas-Racines, D. Homocysteine-lowering interventions for preventing cardiovascular events. Cochrane. Database. Syst. Rev. 1, CD006612 (2013
21. Chu, V. et al. Method for non-invasively recording electrocardiograms in conscious mice. BMC. Physiol 1, 6 (2001
22. Xing, S. et al. Genetic influence on electrocardiogram time intervals and heart rate in aging mice. Am. J. Physiol Heart Circ. Physiol 296, H1907-H1913 (2009
23. Hofmann, M. A. et al. Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J. Clin. Invest 107, 675-683 (2001
24. Troen, A. M., Lutgens, E., Smith, D. E., Rosenberg, I. H. & Selhub, J. The atherogenic effect of excess methionine intake. Proc. Natl. Acad. Sci. U. S. A 100, 15089-15094 (2003
25. Zhou, J. et al. Dietary supplementation with methionine and homocysteine promotes early atherosclerosis but not plaque rupture in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 21, 1470-1476 (2001
26. Elshorbagy, A. K. et al. Cysteine supplementation reverses methionine restriction effects on rat adiposity: Significance of stearoyl-coenzyme A desaturase. J. Lipid Res. 52, 104-112 (2011
27. Lees, E. K. et al.Methionine restriction restores a younger metabolic phenotype in adult mice with alterations in fibroblast growth factor 21. Aging Cell 5, 817-27 (2014
28. Stone, K. P., Wanders, D., Orgeron, M., Cortez, C. C. & Gettys, T. W. Mechanisms of increased in vivo insulin sensitivity by dietary methionine restriction in mice. Diabetes 11, 3721-33 (2014
29. Liu, S. Q. et al. Endocrine protection of ischemic myocardiumby FGF21 from the liver and adipose tissue. Sci. Rep. 3, 2767 (2013
30. Shibata, R., Murohara, T. & Ouchi, N. Protective role of adiponectin in cardiovascular disease. Curr. Med. Chem. 19, 5459-5466 (2012
31. Drewes, Y. M. et al. Homocysteine levels and treatment effect in the PROspective Study of Pravastatin in the Elderly at Risk. J. Am. Geriatr. Soc. 62, 213-221 (2014
32. Perrone, C. E. et al. Genomic and metabolic responses to methionine-restricted and methionine-restricted, cysteine-supplemented diets in Fischer 344 rat inguinal adipose tissue, liver and quadriceps muscle. J. Nutrigenet. Nutrigenomics. 5, 132-157 (2012
33. Basu, P. et al. Chronic hyperhomocysteinemia causes vascular remodelling by instigating vein phenotype in artery. Arch. Physiol Biochem. 117, 270-282 (2011
34. Wang, X. et al. Homocysteine induces cardiomyocyte dysfunction and apoptosis through p38 MAPK-mediated increase in oxidant stress. J. Mol. Cell Cardiol. 52, 753-760 (2012
35. Guo, H. Y. et al. Hyperhomocysteinemia independently causes and promotes atherosclerosis in LDL receptor-deficient mice. J. Geriatr. Cardiol. 11, 74-78 (2014
36. Chen, Z. et al. Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. Hum. Mol. Genet. 10, 433-443 (2001
37. Watanabe, M. et al.Mice deficient in cystathionine beta-synthase: Animal models for mild and severe homocyst(e)inemia. Proc. Natl. Acad. Sci. U. S. A 92, 1585-1589 (1995
38. Zhou, J. et al. Hyperhomocysteinemia induced by methionine supplementation does not independently cause atherosclerosis in C57BL/6J mice. FASEB J. 22, 2569-2578 (2008
39. Ebbing, M. et al. Combined analyses and extended follow-up of two randomized controlled homocysteine-lowering B-vitamin trials. J. Intern. Med. 268, 367-382 (2010
40. Armitage, J. M. et al. Effects of homocysteine-lowering with folic acid plus vitamin B12 vs placebo on mortality and major morbidity in myocardial infarction survivors: A randomized trial. JAMA 303, 2486-2494 (2010
41. Boyle, A. J. et al. Cardiomyopathy of aging in the mammalian heart is characterized by myocardial hypertrophy, fibrosis and a predisposition towards cardiomyocyte apoptosis and autophagy. Exp. Gerontol. 46, 549-559 (2011
42. Rosenberger, D. et al. Homocysteine enriched diet leads to prolonged QT interval and reduced left ventricular performance in telemetric monitored mice. Nutr. Metab Cardiovasc. Dis. 21, 492-498 (2011
43. Zivkovic, V. et al. The effects of homocysteine-related compounds on cardiac contractility, coronary flow, and oxidative stress markers in isolated rat heart. Mol. Cell Biochem. 370, 59-67 (2012
44. Bell, R. M., Mocanu, M. M. & Yellon, D. M. Retrograde heart perfusion: The Langendorff technique of isolated heart perfusion. J. Mol. Cell Cardiol. 50, 940-950 (2011
45. Pazos-Moura, C. et al. Cardiac dysfunction caused by myocardium-specific expression of a mutant thyroid hormone receptor. Circ. Res. 86, 700-706 (2000
46. Hampton, T. G., Amende, I., Travers, K. E. & Morgan, J. P. Intracellular calcium dynamics in mouse model of myocardial stunning. Am. J. Physiol 274, H1821-H1827 (1998
47. Song, Y., Cho, M., Cho, C. & Rosenfeld, M. E. Methionine-induced hyperhomocysteinemia modulates lipoprotein profile and oxidative stress but not progression of atherosclerosis in aged apolipoprotein E knockout mice. J. Med. Food 12, 137-144 (2009
48. Ma, S. et al. Hyperhomocysteinemia induces cardiac injury by up-regulation of p53-dependent Noxa and Bax expression through the p53 DNA methylation in ApoE(-/-) mice. Acta Biochim. Biophys. Sin. (Shanghai) 45, 391-400 (2013
49. Zhou, J. et al. Effects of vitamin supplementation and hyperhomocysteinemia on atherosclerosis in apoE-deficient mice. Atherosclerosis 168, 255-262 (2003
50. Malloy, V. L. et al. Methionine restriction prevents the progression of hepatic steatosis in leptin-deficient obese mice. Metabolism 62, 1651-1661 (2013
51. Kharitonenkov, A. et al. FGF-21 as a novel metabolic regulator. J. Clin. Invest 115, 1627-1635 (2005
52. Lin, X. L. et al. FGF21 Increases Cholesterol Efflux by Upregulating ABCA1 Through the ERK1/2-PPARgamma-LXRalpha Pathway in THP1 Macrophage-Derived Foam Cells. DNA Cell Biol. 8, 514-21 (2014
53. Planavila, A. et al. Fibroblast growth factor 21 protects against cardiac hypertrophy in mice. Nat. Commun. 4, 2019 (2013
54. Maeda, N. et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8, 731-737 (2002
55. Shibata, R. et al. Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat. Med. 11, 1096-1103 (2005
56. Fang, X. et al. An APPL1-AMPK signaling axis mediates beneficial metabolic effects of adiponectin in the heart. Am. J. Physiol Endocrinol. Metab 299, E721-E729 (2010
57. Elshorbagy, A. K. et al. Cysteine supplementation reverses methionine restriction effects on rat adiposity: Significance of stearoyl-coenzyme A desaturase. J. Lipid Res. 52, 104-112 (2011
58. Subramanian, A. et al.Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A 102, 15545-15550 (2005
59. Mootha, V. K. et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267-273 (2003
60. Kanehisa, M.&Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30 (2000
61. Li, H. H. et al. The ubiquitin ligase MuRF1 protects against cardiac ischemia/reperfusion injury by its proteasome-dependent degradation of phospho-c-Jun. Am. J. Pathol. 178, 1043-1058 (2011
62. Hampton, T. G., Kranias, E. G. & Morgan, J. P. Simultaneous measurement of intracellular calcium and ventricular function in the phospholamban-deficient mouse heart. Biochem. Biophys. Res. Commun. 226, 836-841 (1996