Cumulative 3-nitrotyrosine in specific muscle proteins is associated with muscle loss during aging

Experimental Gerontology

Volumn 47, Issue 2, 2012, Pages 129-135

  Murakami, Hitoshi ^a,b,d   Guillet, Christelle ^a,b   Tardif, Nicolas ^a,b   Salles, Jerome ^a,b   Migné, Carole ^a,b   Boirie, Yves ^a,b,c   Walrand, Stephane ^a,b,e  

^a CRNH AUVERGNE   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^d AJINOMOTO CO INC   (Japan)

^e NONE   (France)

Author keywords

3 nitrotyrosine; Carbonylation; High calorie diet; Sarcopenia; Skeletal muscle

Indexed keywords

3 NITROTYROSINE; ARACHIS OIL; CASEIN; CELLULOSE; LARD; MINERAL; MUSCLE PROTEIN; RAPESEED OIL; STARCH; SUCROSE; VITAMIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; FOOD COMPOSITION; MALE; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MUSCLE MASS; NITRATION; NONHUMAN; NUTRITIONAL STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; QUADRICEPS FEMORIS MUSCLE; RAT; SKELETAL MUSCLE; STRESS;

RATTUS;

EID: 84856220482     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2011.11.007     Document Type: Article

References (49)

1. Arnal M.A., Mosoni L., Dardevet D., Ribeyre M.C., Bayle G., Prugnaud J., Patureau Mirand P. Pulse protein feeding pattern restores stimulation of muscle protein synthesis during the feeding period in old rats. J. Nutr. 2002, 132:1002-1008.
2. Balagopal P., Rooyackers O.E., Adey D.B., Ades P.A., Nair K.S. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am. J. Physiol. 1997, 273:E790-E800.
3. Bar-Shai M., Reznick A.Z. Reactive nitrogen species induce nuclear factor-kappaB-mediated protein degradation in skeletal muscle cells. Free Radic. Biol. Med. 2006, 40:2112-2125.
4. Barreiro E., Coronell C., Lavina B., Ramirez-Sarmiento A., Orozco-Levi M., Gea J. Aging, sex differences, and oxidative stress in human respiratory and limb muscles. Free Radic. Biol. Med. 2006, 41:797-809.
5. Beal M.F. Oxidatively modified proteins in aging and disease. Free Radic. Biol. Med. 2002, 32:797-803.
6. Boirie Y., Short K.R., Ahlman B., Charlton M., Nair K.S. Tissue-specific regulation of mitochondrial and cytoplasmic protein synthesis rates by insulin. Diabetes 2001, 50:2652-2658.
7. Bolster D.R., Jefferson L.S., Kimball S.R. Regulation of protein synthesis associated with skeletal muscle hypertrophy by insulin-, amino acid- and exercise-induced signalling. Proc. Nutr. Soc. 2004, 63:351-356.
8. Bourgoin F., Bachelard H., Badeau M., Melancon S., Pitre M., Lariviere R., Nadeau A. Endothelial and vascular dysfunctions and insulin resistance in rats fed a high-fat, high-sucrose diet. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H1044-H1055.
9. Cakatay U., Aydin S., Yanar K., Uzun H. Gender-dependent variations in systemic biomarkers of oxidative protein, DNA, and lipid damage in aged rats. Aging Male 2010, 13:51-58.
10. Cakatay U., Telci A., Kayali R., Tekeli F., Akcay T., Sivas A. Relation of aging with oxidative protein damage parameters in the rat skeletal muscle. Clin. Biochem. 2003, 36:51-55.
11. Chander P.N., Gealekman O., Brodsky S.V., Elitok S., Tojo A., Crabtree M., Gross S.S., Goligorsky M.S. Nephropathy in Zucker diabetic fat rat is associated with oxidative and nitrosative stress: prevention by chronic therapy with a peroxynitrite scavenger ebselen. J. Am. Soc. Nephrol. 2004, 15:2391-2403.
12. Chanseaume E., Malpuech-Brugere C., Patrac V., Bielicki G., Rousset P., Couturier K., Salles J., Renou J.P., Boirie Y., Morio B. Diets high in sugar, fat, and energy induce muscle type-specific adaptations in mitochondrial functions in rats. J. Nutr. 2006, 136:2194-2200.
13. Clavel S., Coldefy A.S., Kurkdjian E., Salles J., Margaritis I., Derijard B. Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat Tibialis Anterior muscle. Mech. Ageing Dev. 2006, 127:794-801.
14. Combaret L., Dardevet D., Bechet D., Taillandier D., Mosoni L., Attaix D. Skeletal muscle proteolysis in aging. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12:37-41.
15. Combaret L., Dardevet D., Rieu I., Pouch M.N., Bechet D., Taillandier D., Grizard J., Attaix D. A leucine-supplemented diet restores the defective postprandial inhibition of proteasome-dependent proteolysis in aged rat skeletal muscle. J. Physiol. 2005, 569:489-499.
16. Cortez M.Y., Torgan C.E., Brozinick J.T., Ivy J.L. Insulin resistance of obese Zucker rats exercise trained at two different intensities. Am. J. Physiol. 1991, 261:E613-E619.
17. Cruz-Jentoft A.J., Landi F., Topinkova E., Michel J.P. Understanding sarcopenia as a geriatric syndrome. Curr. Opin. Clin. Nutr. Metab. Care 2010, 13:1-7.
18. Curry-McCoy T.V., Osna N.A., Donohue T.M. Modulation of lysozyme function and degradation after nitration with peroxynitrite. Biochim. Biophys. Acta 2009, 1790:778-786.
19. Dardevet D., Sornet C., Bayle G., Prugnaud J., Pouyet C., Grizard J. Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucine-supplemented meal. J. Nutr. 2002, 132:95-100.
20. Feng J., Xie H., Meany D.L., Thompson L.V., Arriaga E.A., Griffin T.J. Quantitative proteomic profiling of muscle type-dependent and age-dependent protein carbonylation in rat skeletal muscle mitochondria. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:1137-1152.
21. Fugere N.A., Ferrington D.A., Thompson L.V. Protein nitration with aging in the rat semimembranosus and soleus muscles. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61:806-812.
22. Fujimoto H., Kobayashi H., Ohno M. Age-induced reduction in mitochondrial manganese superoxide dismutase activity and tolerance of macrophages against apoptosis induced by oxidized low density lipoprotein. Circ. J. 2010, 74:353-360.
23. Fulle S., Protasi F., Di Tano G., Pietrangelo T., Beltramin A., Boncompagni S., Vecchiet L., Fano G. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp. Gerontol. 2004, 39:17-24.
24. Gomez-Perez Y., Amengual-Cladera E., Catala-Niell A., Thomas-Moya E., Gianotti M., Proenza A.M., Llado I. Gender dimorphism in high-fat-diet-induced insulin resistance in skeletal muscle of aged rats. Cell. Physiol. Biochem. 2008, 22:539-548.
25. Gomez-Perez Y., Amengual-Cladera E., Catala-Niell A., Thomas-Moya E., Gianotti M., Proenza A.M., Llado I. Gender dimorphism in high-fat-diet-induced insulin resistance in skeletal muscle of aged rats. Cell. Physiol. Biochem. 2008, 22:539-548.
26. Guillet C., Prod'homme M., Balage M., Gachon P., Giraudet C., Morin L., Grizard J., Boirie Y. Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J. 2004, 18:1586-1587.
27. Guillet C., Zangarelli A., Mishellany A., Rousset P., Sornet C., Dardevet D., Boirie Y. Mitochondrial and sarcoplasmic proteins, but not myosin heavy chain, are sensitive to leucine supplementation in old rat skeletal muscle. Exp. Gerontol. 2004, 39:745-751.
28. Husom A.D., Peters E.A., Kolling E.A., Fugere N.A., Thompson L.V., Ferrington D.A. Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 2004, 421:67-76.
29. Jackson M.J., Pye D., Palomero J. The production of reactive oxygen and nitrogen species by skeletal muscle. J. Appl. Physiol. 2007, 102:1664-1670.
30. Jagoe R.T., Goldberg A.L. What do we really know about the ubiquitin-proteasome pathway in muscle atrophy?. Curr. Opin. Clin. Nutr. Metab. Care 2001, 4:183-190.
31. Kanski J., Alterman M.A., Schoneich C. Proteomic identification of age-dependent protein nitration in rat skeletal muscle. Free Radic. Biol. Med. 2003, 35:1229-1239.
32. Kayali R., Cakatay U., Tekeli F. Male rats exhibit higher oxidative protein damage than females of the same chronological age. Mech. Ageing Dev. 2007, 128:365-369.
33. Kayali R., Cakatay U., Uzun H., Genc H. Gender difference as regards myocardial protein oxidation in aged rats: male rats have increased oxidative protein damage. Biogerontology 2007, 8:653-661.
34. Leeuwenburgh C., Hansen P., Shaish A., Holloszy J.O., Heinecke J.W. Markers of protein oxidation by hydroxyl radical and reactive nitrogen species in tissues of aging rats. Am. J. Physiol. 1998, 274:R453-R461.
35. Lushaj E.B., Johnson J.K., McKenzie D., Aiken J.M. Sarcopenia accelerates at advanced ages in Fisher 344xBrown Norway rats. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:921-927.
36. Meng S.J, Yu L.J. Oxidative stress, molecular inflammation and sarcopenia. Int J Mol Sci. 2010, 11:1509-1526.
37. Mosoni L., Breuille D., Buffiere C., Obled C., Mirand P.P. Age-related changes in glutathione availability and skeletal muscle carbonyl content in healthy rats. Exp. Gerontol. 2004, 39:203-210.
38. Radak Z., Takahashi R., Kumiyama A., Nakamoto H., Ohno H., Ookawara T., Goto S. Effect of aging and late onset dietary restriction on antioxidant enzymes and proteasome activities, and protein carbonylation of rat skeletal muscle and tendon. Exp. Gerontol. 2002, 37:1423-1430.
39. Rasmussen B.B., Phillips S.M. Contractile and nutritional regulation of human muscle growth. Exerc. Sport Sci. Rev. 2003, 31:127-131.
40. Rattan S.I. Synthesis, modifications, and turnover of proteins during aging. Exp. Gerontol. 1996, 31:33-47.
41. Rooyackers O.E., Adey D.B., Ades P.A., Nair K.S. Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:15364-15369.
42. Sevilla L., Guma A., Enrique-Tarancon G., Mora S., Munoz P., Palacin M., Testar X., Zorzano A. Chronic high-fat feeding and middle-aging reduce in an additive fashion Glut4 expression in skeletal muscle and adipose tissue. Biochem. Biophys. Res. Commun. 1997, 235:89-93.
43. Shimokawa I., Higami Y., Tsuchiya T., Otani H., Komatsu T., Chiba T., Yamaza H. Life span extension by reduction of the growth hormone-insulin-like growth factor-1 axis: relation to caloric restriction. FASEB J. 2003, 17:1108-1109.
44. Soskic V., Groebe K., Schrattenholz A. Nonenzymatic posttranslational protein modifications in ageing. Exp. Gerontol. 2008, 43:247-257.
45. Thompson L.V. Age-related muscle dysfunction. Exp. Gerontol. 2009, 44:106-111.
46. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
47. Van Remmen H., Richardson A. Oxidative damage to mitochondria and aging. Exp. Gerontol. 2001, 36:957-968.
48. Wang Y., Wang P.Y., Qin L.Q., Davaasambuu G., Kaneko T., Xu J., Murata S., Katoh R., Sato A. The development of diabetes mellitus in Wistar rats kept on a high-fat/low-carbohydrate diet for long periods. Endocrine 2003, 22:85-92.
49. Zangarelli A., Chanseaume E., Morio B., Brugere C., Mosoni L., Rousset P., Giraudet C., Patrac V., Gachon P., Boirie Y., Walrand S. Synergistic effects of caloric restriction with maintained protein intake on skeletal muscle performance in 21-month-old rats: a mitochondria-mediated pathway. FASEB J. 2006, 20:2439-2450.