Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat Tibialis Anterior muscle

Mechanisms of Ageing and Development

Volumn 127, Issue 10, 2006, Pages 794-801

  Clavel, Stephan ^a   Coldefy, Anne Sophie ^a   Kurkdjian, Emilie ^b   Salles, Jérôme ^c   Margaritis, Irène ^b   Derijard, Benoît ^a  

^a CNRS   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c CRNH AUVERGNE   (France)

Author keywords

Atrogin 1; E3 ligase; MuRF1; Sarcopenia; Ubiquitin proteasome pathway

Indexed keywords

ATROGIN 1; MESSENGER RNA; PROTEASOME; PROTEIN KINASE B; PROTEIN MURF1; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

AGED; AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; FAST MUSCLE; GENE EXPRESSION REGULATION; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE;

AGING; ANIMALS; CARBON; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR I; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN-PROTEIN LIGASES;

EID: 33748526240     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2006.07.005     Document Type: Article

References (49)

1. Alnaqeeb M.A., and Goldspink G. Changes in fibre type, number and diameter in developing and ageing skeletal muscle. J. Anat. 153 (1987) 31-45
2. Attaix D., Mosoni L., Dardevet D., Combaret L., Mirand P.P., and Grizard J. Altered responses in skeletal muscle protein turnover during aging in anabolic and catabolic periods. Int. J. Biochem. Cell. Biol. 37 (2005) 1962-1973
3. Bodine S.C., Latres E., Baumhueter S., Lai V.K., Nunez L., Clarke B.A., Poueymirou W.T., Panaro F.J., Na E., Dharmarajan K., Pan Z.Q., Valenzuela D.M., DeChiara T.M., Stitt T.N., Yancopoulos G.D., and Glass D.J. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294 (2001) 1704-1708
4. Cai D., Frantz J.D., Tawa Jr. N.E., Melendez P.A., Oh B.C., Lidov H.G., Hasselgren P.O., Frontera W.R., Lee J., Glass D.J., and Shoelson S.E. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 119 (2004) 285-298
5. Cai D., Lee K.K., Li M., Tang M.K., and Chan K.M. Ubiquitin expression is up-regulated in human and rat skeletal muscles during aging. Arch. Biochem. Biophys. 425 (2004) 42-50
6. Cao P.R., Kim H.J., and Lecker S.H. Ubiquitin-protein ligases in muscle wasting. Int. J. Biochem. Cell Biol. 37 (2005) 2088-2097
7. Craiu A., Gaczynska M., Akopian T., Gramm C.F., Fenteany G., Goldberg A.L., and Rock K.L. Lactacystin and clasto-lactacystin beta-lactone modify multiple proteasome beta-subunits and inhibit intracellular protein degradation and major histocompatibility complex class I antigen presentation. J. Biol. Chem. 272 (1997) 13437-13445
8. Deruisseau K.C., Kavazis A.N., and Powers S.K. Selective downregulation of ubiquitin conjugation cascade mRNA occurs in the senescent rat soleus muscle. Exp. Gerontol. 40 (2005) 526-531
9. Ferrington D.A., Husom A.D., and Thompson L.V. Altered proteasome structure, function, and oxidation in aged muscle. FASEB J. 19 (2005) 644-646
10. Goossens V., Grooten J., De Vos K., and Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 8115-8119
11. Greenlund L.J., and Nair K.S. Sarcopenia-consequences, mechanisms, and potential therapies. Mech. Ageing Dev. 124 (2003) 287-299
12. Greiwe J.S., Cheng B., Rubin D.C., Yarasheski K.E., and Semenkovich C.F. Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J. 15 (2001) 475-482
13. Hobler S.C., Williams A., Fischer D., Wang J.J., Sun X., Fischer J.E., Monaco J.J., and Hasselgren P.O. Activity and expression of the 20S proteasome are increased in skeletal muscle during sepsis. Am. J. Physiol. 277 (1999) R434-R440
14. Holloszy J.O., Chen M., Cartee G.D., and Young J.C. Skeletal muscle atrophy in old rats: differential changes in the three fiber types. Mech. Ageing Dev. 60 (1991) 199-213
15. Husom A.D., Peters E.A., Kolling E.A., Fugere N.A., Thompson L.V., and Ferrington D.A. Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 421 (2004) 67-76
16. Jagoe R.T., and Goldberg A.L. What do we really know about the ubiquitin-proteasome pathway in muscle atrophy?. Curr. Opin. Clin. Nutr. Metab. Care 4 (2001) 183-190
17. Kimball S.R., O'Malley J.P., Anthony J.C., Crozier S.J., and Jefferson L.S. Assessment of biomarkers of protein anabolism in skeletal muscle during the life span of the rat: sarcopenia despite elevated protein synthesis. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E772-E780
18. Latres E., Amini A.R., Amini A.A., Griffiths J., Martin F.J., Wei Y., Lin H.C., Yancopoulos G.D., and Glass D.J. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J. Biol. Chem. 280 (2005) 2737-2744
19. Lecker S.H., Jagoe R.T., Gilbert A., Gomes M., Baracos V., Bailey J., Price S.R., Mitch W.E., and Goldberg A.L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18 (2004) 39-51
20. Lecker S.H., Solomon V., Mitch W.E., and Goldberg A.L. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J. Nutr. 129 (1999) 227S-237S
21. Lee D.H., and Goldberg A.L. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell. Biol. 8 (1998) 397-403
22. Lexell J. Human aging, muscle mass, and fiber type composition. J. Gerontol. A Biol. Sci. Med. Sci. 50 (1995) 11-16
23. Li X., Moody M.R., Engel D., Walker S., Clubb Jr. F.J., Sivasubramanian N., Mann D.L., and Reid M.B. Cardiac-specific overexpression of tumor necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation 102 (2000) 1690-1696
24. Li Y.P., Chen Y., John J., Moylan J., Jin B., Mann D.L., and Reid M.B. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 19 (2005) 362-370
25. Li Y.P., Chen Y., Li A.S., and Reid M.B. Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes. Am. J. Physiol. Cell. Physiol. 285 (2003) C806-C812
26. Li Y.P., Lecker S.H., Chen Y., Waddell I.D., Goldberg A.L., and Reid M.B. TNF-alpha increases ubiquitin-conjugating activity in skeletal muscle by up-regulating UbcH2/E220k. FASEB J. 17 (2003) 1048-1057
27. Llovera M., Garcia-Martinez C., Agell N., Lopez-Soriano F.J., and Argiles J.M. TNF can directly induce the expression of ubiquitin-dependent proteolytic system in rat soleus muscles. Biochem. Biophys. Res. Commun. 230 (1997) 238-241
28. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
29. Musaro A., McCullagh K., Paul A., Houghton L., Dobrowolny G., Molinaro M., Barton E.R., Sweeney H.L., and Rosenthal N. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27 (2001) 195-200
30. Passmore L.A., and Barford D. Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem. J. 379 (2004) 513-525
31. Pattison J.S., Folk L.C., Madsen R.W., Childs T.E., and Booth F.W. Transcriptional profiling identifies extensive downregulation of extracellular matrix gene expression in sarcopenic rat soleus muscle. Physiol. Genomics 15 (2003) 34-43
32. Phillips T., and Leeuwenburgh C. Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J. 19 (2005) 668-670
33. Pickart C.M., and Eddins M.J. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695 (2004) 55-72
34. Price S.R. Increased transcription of ubiquitin-proteasome system components: molecular responses associated with muscle atrophy. Int. J. Biochem. Cell. Biol. 35 (2003) 617-628
35. Reid M.B. Response of the ubiquitin-proteasome pathway to changes in muscle activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 (2005) R1423-R1431
36. Reid M.B., and Li Y.P. Tumor necrosis factor-alpha and muscle wasting: a cellular perspective. Respir. Res. 2 (2001) 269-272
37. Rock K.L., Gramm C., Rothstein L., Clark K., Stein R., Dick L., Hwang D., and Goldberg A.L. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78 (1994) 761-771
38. Rooyackers O.E., Adey D.B., Ades P.A., and 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. 93 (1996) 15364-15369
39. Sacheck J.M., Ohtsuka A., McLary S.C., and Goldberg A.L. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E591-E601
40. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., and Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117 (2004) 399-412
41. Short K.R., and Nair K.S. The effect of age on protein metabolism. Curr. Opin. Clin. Nutr. Metab. Care 3 (2000) 39-44
42. Stitt T.N., Drujan D., Clarke B.A., Panaro F., Timofeyva Y., Kline W.O., Gonzalez M., Yancopoulos G.D., and Glass D.J. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14 (2004) 395-403
43. Tintignac L.A., Lagirand J., Batonnet S., Sirri V., Leibovitch M.P., and Leibovitch S.A. Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J. Biol. Chem. 280 (2005) 2847-2856
44. Vigouroux S., Farout L., Clavel S., Briand Y., and Briand M. Increased muscle proteasome activities in rats fed a polyunsaturated fatty acid supplemented diet. Int. J. Biochem. Cell. Biol. 35 (2003) 749-755
45. Volpi E., Sheffield-Moore M., Rasmussen B.B., and Wolfe R.R. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA 286 (2001) 1206-1212
46. Welle S., Bhatt K., Shah B., and Thornton C. Insulin-like growth factor-1 and myostatin mRNA expression in muscle: comparison between 62-77 and 21-31 yr old men. Exp. Gerontol. 37 (2002) 833-839
47. Welle S., Brooks A.I., Delehanty J.M., Needler N., and Thornton C.A. Gene expression profile of aging in human muscle. Physiol. Genomics 14 (2003) 149-159
48. Whitman S.A., Wacker M.J., Richmond S.R., and Godard M.P. Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch. 450 (2005) 437-446
49. Zainal T.A., Oberley T.D., Allison D.B., Szweda L.I., and Weindruch R. Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB J. 14 (2000) 1825-1836