Long-term supplementation with a cystine-based antioxidant delays loss of muscle mass in aging

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 68, Issue 7, 2013, Pages 749-759

  Sinha Hikim, Indrani ^a,b   Sinha Hikim, Amiya P ^a   Parveen, Meher ^a   Shen, Ruoqing ^a   Goswami, Rudrani ^a   Tran, Peter ^a   Crum, Albert ^c   Norris, Keith C ^a,b  

^a CHARLES R DREW UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Proimmune   (United States)

Author keywords

Antioxidant; Mice; Muscle cell apoptosis; Oxidative stress; Sarcopenia.

Indexed keywords

AMPK ALPHA1 SUBUNIT, MOUSE; ANTIOXIDANT; CYSTINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; STRESS ACTIVATED PROTEIN KINASE;

AGING; ANIMAL; APOPTOSIS; ARTICLE; C57BL MOUSE; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; MALE; METABOLISM; MOUSE; MUSCLE CELL APOPTOSIS; OXIDATIVE STRESS; SARCOPENIA; SARCOPENIA.; SKELETAL MUSCLE; TREATMENT OUTCOME;

ANTIOXIDANT; MICE; MUSCLE CELL APOPTOSIS; OXIDATIVE STRESS; SARCOPENIA.;

AGING; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CYSTINE; DISEASE MODELS, ANIMAL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; OXIDATIVE STRESS; SARCOPENIA; TREATMENT OUTCOME;

EID: 84883048598     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/gls334     Document Type: Article

References (44)

1. Census briefs: the older population. Werner, CA: United States Census Bureau, US Department of Commerce. 2010.
2. Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr. 2002;76:473-481. (Pubitemid 34804075)
3. Marzetti E, Leeuwenburgh C. Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp Gerontol. 2006;41:1234-1238. (Pubitemid 44848392)
4. Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755-763. (Pubitemid 28183275)
5. Glass D, Roubenoff R. Recent advances in the biology and therapy of muscle wasting. Ann N Y Acad Sci. 2010;1211:25-36.
6. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science. 2003;302:1575-1577. (Pubitemid 37475703)
7. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005;433:760-764. (Pubitemid 40292986)
8. Braga M, Sinha Hikim AP, Datta S, et al. Involvement of oxidative stress and caspase 2-mediated intrinsic pathway signaling in age-related increase in muscle cell apoptosis in mice. Apoptosis. 2008;13:822-832.
9. Kovacheva EL, Hikim AP, Shen R, Sinha I, Sinha-Hikim I. Testosterone supplementation reverses sarcopenia in aging through regulation of myostatin, c-Jun NH2-terminal kinase, Notch, and Akt signaling pathways. Endocrinology. 2010;151:628-638.
10. Marzetti E, Calvani R, Bernabei R, Leeuwenburgh C. Apoptosis in skeletal myocytes: a potential target for interventions against sarcopenia and physical frailty - a mini-review. Gerontology. 2012;58:99-106.
11. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120:483-495. (Pubitemid 40269763)
12. Martin C, Dubouchaud H, Mosoni L, et al. Abnormalities of mitochondrial function can partly explain the metabolic disorders encountered in sarcopenic gastrocnemius. Aging cell. 2007;1:1-13.
13. Bonetto A, Penna F, Muscaritoli M, et al. Are antioxidants useful for treating skeletal muscle atrophy? Free Radic Biol Med. 2009;47:906-916.
14. Jackson JR, Ryan MJ, Hao Y, Alway SE. Mediation of endogenous antioxidant enzymes and apoptotic signaling by resveratrol following muscle disuse in the gastrocnemius muscles of young and old rats. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1572-R1581.
15. Ryan MJ, Jackson JR, Hao Y, Leonard SS, Alway SE. Inhibition of xanthine oxidase reduces oxidative stress and improves skeletal muscle function in response to electrically stimulated isometric contractions in aged mice. Free Radic Biol Med. 2011;51:38-52.
16. Doria E, Buonocore D, Focarelli A, Marzatico F. Relationship between human aging muscle and oxidative system pathway. Oxid Med Cell Longev. 2012;2012:830257.
17. Sinha-Hikim I, Shen R, Kovacheva E, Crum A, Vaziri ND, Norris KC. Inhibition of apoptotic signalling in spermine-treated vascular smooth muscle cells by a novel glutathione precursor. Cell Biol Int. 2010;34:503-511.
18. Sinha-Hikim I, Shen R, Paul Lee WN, Crum A, Vaziri ND, Norris KC. Effects of a novel cystine-based glutathione precursor on oxidative stress in vascular smooth muscle cells. Am J Physiol, Cell Physiol. 2010;299:C638-C642.
19. Sinha-Hikim I, Sinha-Hikim AP, Shen R, et al. A novel cystine based antioxidant attenuates oxidative stress and hepatic steatosis in dietinduced obese mice. Exp Mol Pathol. 2011;91:419-428.
20. Crum A. Nutritional or therapeutic compositions to increase bodily glutathione levels. US RE39734E. 2007.
21. Sinha-Hikim I, Braga M, Shen R, Sinha Hikim AP. Involvement of c-Jun NH2-terminal kinase and nitric oxide-mediated mitochondriadependent intrinsic pathway signaling in cardiotoxin-induced muscle cell death: role of testosterone. Apoptosis. 2007;12:1965-1978. (Pubitemid 47498228)
22. Dupont-Versteegden EE, Strotman BA, Gurley CM, et al. Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1730-R1740. (Pubitemid 44904141)
23. McKiernan SH, Bua E, McGorray J, Aiken J. Early-onset calorie restriction conserves fiber number in aging rat skeletal muscle. FASEB J. 2004;18:580-581.
24. Hao Y, Jackson JR, Wang Y, Edens N, Pereira SL, Alway SE. ?-Hydroxy-?-methylbutyrate reduces myonuclear apoptosis during recovery from hind limb suspension-induced muscle fiber atrophy in aged rats. Am J Physiol Regul Integr Comp Physiol. 2011;301:R701-R715.
25. Meng SJ, Yu LJ. Oxidative stress, molecular inflammation and sarcopenia. Int J Mol Sci. 2010;11:1509-1526.
26. Tanno M, Kuno A, Yano T, et al. Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem. 2010;285: 8375-8382.
27. Kim MY, Lim JH, Youn HH, et al. Resveratrol prevents renal lipotoxicity and inhibits mesengial cell glucotoxicity in a manner dependent on the AMPK-SIRT1-PGC1? axis in db/db mice. Dibetlogia. 2013;56:204-217.
28. Reznick RM, Zong H, Li J, et al. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab. 2007;5:151-156. (Pubitemid 46172924)
29. Anderson RM, Weindruch R. Metabolic reprogramming, caloric restriction and aging. Trends Endocrinol Metab. 2010;21:134-141.
30. Centeno-Baez C, Dallaire P, Marette A. Resveratrol inhibition of inducible nitric oxide synthase in skeletal muscle involves AMPK but not SIRT1. Am J Physiol Endocrinol Metab. 2011;301: E922-E930.
31. Postic C, Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest. 2008;118:829-838. (Pubitemid 351364588)
32. Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 2009;9:407-416.
33. Shadrach JL, Wagers AJ. Stem cells for skeletal muscle repair. Philos Trans R Soc Lond, B, Biol Sci. 2011;366:2297-2306.
34. Alway SE, Siu PM. Nuclear apoptosis contributes to sarcopenia. Exerc Sport Sci Rev. 2008;36:51-57. (Pubitemid 351440765)
35. Pallafacchina G, Blaauw B, Schiaffino S. Role of satellite cells in muscle growth and maintenance of muscle mass. Nutr Metab Cardiovasc Dis. 2012; Epub ahead of print.
36. Izumiya Y, Hopkins T, Morris C, et al. Fast/Glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab. 2008;7:159-172. (Pubitemid 351168553)
37. Bassel-Duby R, Olson EN. Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem. 2006;75:19-37. (Pubitemid 44118024)
38. Robey RB, Hay N. Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene. 2006;25:4683-4696. (Pubitemid 44187618)
39. Lieberthal W, Zhang L, Patel VA, Levine JS. AMPK protects proximal tubular cells from stress-induced apoptosis by an ATP-independent mechanism: potential role of Akt activation. Am J Physiol Renal Physiol. 2011;301:F1177-F1192.
40. Chopra I, Li HF, Wang H, Webster KA. Phosphorylation of the insulin receptor by AMP-activated protein kinase (AMPK) promotes ligandindependent activation of the insulin signalling pathway in rodent muscle. Diabetologia. 2012;55:783-794.
41. Jackson JR, Ryan MJ, Alway SE. Long-term supplementation with resveratrol alleviates oxidative stress but does not attenuate sarcopenia in aged mice. J Gerontol A Biol Sci Med Sci. 2011;66:751-764.
42. Momken I, Stevens L, Bergouignan A, et al. Resveratrol prevents the wasting disorders of mechanical unloading by acting as a physical exercise mimetic in the rat. FASEB J. 2011;25:3646-3660.
43. Pinheiro CH, Vitzel KF, Curi R. Effect of N-acetylcysteine on markers of skeletal muscle injury after fatiguing contractile activity. Scand J Med Sci Sports. 2012;22:24-33.
44. Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol. 2012;3:1-18.