Glucocorticoids regulate mRNA levels for subunits of the 19 S regulatory complex of the 26 S proteasome in fast-twitch skeletal muscles

Biochemical Journal

Volumn 378, Issue 1, 2004, Pages 239-246

  Combaret, Lydie ^a   Taillandier, Daniel ^a   Dardevet, Dominique ^a   Béchet, Daniel ^a   Rallière, Cécile ^a   Claustre, Agnès ^a   Grizard, Jean ^a   Attaix, Didier ^a  

^a CEMAGREF   (France)

Author keywords

26 S proteasome; Dexamethasone; Glucocorticoid; Muscle wasting; Skeletal muscle; Ubiquitin proteasome proteolysis

Indexed keywords

DISEASES; HORMONES; MUSCULOSKELETAL SYSTEM; PROTEINS;

INSULIN-DEPENDENT DIABETES; MUSCLE-WASTING CONDITIONS; STARVATION;

RNA;

ADENOSINE TRIPHOSPHATASE; CHYMOTRYPSIN; DEXAMETHASONE; GLUCOCORTICOID; MESSENGER RNA; PROTEASOME; PROTEIN SUBUNIT; REGULATOR PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTEROID THERAPY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; ENZYME ACTIVITY; FAST MUSCLE; HORMONAL REGULATION; IN VIVO STUDY; MALE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; UBIQUITINATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CHYMOTRYPSIN; CULTURE TECHNIQUES; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; DEXAMETHASONE; ENDOPEPTIDASES; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; LEUPEPTINS; MALE; MULTIENZYME COMPLEXES; MUSCLE FIBERS, FAST-TWITCH; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; PEPTIDE HYDROLASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; RATS; RATS, WISTAR; RNA, MESSENGER; UBIQUITINS;

ANIMALIA;

EID: 1542284640     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031660     Document Type: Article

References (51)

1. 2+-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc. Natl. Acad. Sci. U.S.A. 93, 2714-2718
2. Hasselgren, P. O. (1999) Glucocorticoids and muscle catabolism. Curr. Opin. Clin. Nutr. Metab. Care 2, 201-205
3. Marinovic, A. C., Zheng, B., Mitch, W. E. and Price, S. R. (2002) Ubiquitin (UbC) expression in muscle cells is increased by glucocorticoids through a mechanism involving Sp1 and MEK1 J. Biol. Chem. 277, 16673-16681
4. Dardevet, D., Sornet, C., Taillandier, D., Savary, I., Attaix, D. and Grizard, J. (1995) Sensitivity and protein turnover response to glucocorticoids are different in skeletal muscle from adult and old rats. Lack of regulation of the ubiquitin-proteasome proteolytic pathway in aging. J. Clin. Invest. 96, 2113-2119
5. Mitch, W. E. and Goldberg, A. L. (1996) Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335, 1897-1905
6. Rallière, C., Tauveron, I., Taillandier, D., Guy, L., Boiteux, J. P., Giraud, B., Attaix, D. and Thiéblot, P. (1997) Glucocorticoids do not regulate the expression of proteolytic genes in skeletal muscle from Cushing's syndrome patients. J. Clin. Endocrinol. Metab. 82, 3161-3164
7. Attaix, D., Combaret, L., Kee, A. J. and Taillandier, D. (2003) Mechanisms of ubiquitination and proteasome-dependent proteolysis in skeletal muscle. In Molecular Nutrition (Zempleni, J. and Daniel, H., eds.), pp. 219-235, CABI Publishing, Wallingford
8. Jagoe, R. T. and Goldberg, A. L. (2001) What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr. Opin. Clin. Nutr. Metab. Care 4, 183-190
9. Hasselgren, P. O. and Fischer, J. E. (2001) Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann. Surg. 233, 9-17
10. Lecker, S. H., Solomon, V., Mitch, W. E. and Goldberg, A. L. (1999) Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J. Nutr. 129, 227S-237S
11. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
12. Glickman, M. H. and Ciechanover, A. (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373-428
13. Du, J., Mitch, W. E., Wang, X. N. and Price, S. R. (2000) Glucocorticoids induce proteasome C3 subunit expression in L6 muscle cells by opposing the suppression of its transcription by NF-κB. J. Biol. Chem. 275, 19661-19666
14. Chrysis, D. and Underwood, L. E. (1999) Regulation of components of the ubiquitin system by insulin-like growth factor I and growth hormone in skeletal muscle of rats made catabolic with dexamethasone. Endocrinology 140, 5635-5641
15. Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K. M., Nunez, L., Clarke, B. A., Poueymirou, W. T., Panaro, F. J., Na, E. Q., Dharmarajan, K. et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708
16. Wing, S. S. and Goldberg, A. L. (1993) Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am. J. Physiol. 264, E668-E676
17. Price, S. R., England, B. K., Bailey, J. L., Van Vreede, K. and Mitch, W. E. (1994) Acidosis and glucocorticoids concomitantly increase ubiquitin and proteasome subunit mRNAs in rat muscle. Am. J. Physiol. 266, C955-C960
18. May, R. C., Bailey, J. L., Mitch, W. E., Masud, T. and England, B. K. (1996) Glucocorticoids and acidosis stimulate protein and amino acid catabolism in vivo. Kidney Int. 49, 679-683
19. Fang, C. H., Tiao, G., James, H., Ogle, C., Fischer, J. E. and Hasselgren, P. O. (1995) Burn injury stimulates multiple proteolytic pathways in skeletal muscle, including the ubiquitin-energy dependent pathway. J. Am. Coll. Surg. 180, 161-170
20. Wray, C. J., Mammen, J. M. V. and Hasselgren, P.-O. (2003) Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int. J. Biochem. Cell Biol. 35, 698-705
21. Tiao, G., Fagan, J., Roegner, V., Lieberman, M., Wang, J. J., Fischer, J. E. and Hasselgren, P. O. (1996) Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J. Clin. Invest. 97, 339-348
22. Dardevet, D., Sornet, C., Attaix, D., Baracos, V. E. and Grizard, J. (1994) Insulin-like growth factor-1 and insulin resistance in skeletal muscles of adult and old rats. Endocrinology 134, 1475-1484
23. Tilignac, T., Temparis, S., Combaret, L, Taillandier, D., Pouch, M.-N., Cervek, M., Cardenas, D. M., Le Bricon, T., Debiton, E., Samuels, S. E. et al. (2002) Chemotherapy inhibits skeletal muscle ubiquitin-proteasome-dependent proteolysis. Cancer Res. 62, 2771-2777
24. Tischler, M. E., Desautels, M. and Goldberg, A. L. (1982) Does leucine, leucyl-tRNA, or some metabolite of leucine regulate protein synthesis and degradation in skeletal and cardiac muscle? J. Biol. Chem. 257, 1613-1621
25. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159
26. Deval, C., Mordier, S., Obled, C., Béchet, D., Combaret, L., Attaix, O. and Ferrara, M. (2001) Identification of cathepsin L as a differentially expressed message associated with skeletal muscle wasting. Biochem. J. 360, 143-150
27. Snedecor, G. W. and Cochran, W. G. (1967) Analysis of covariance. Statistical Methods, 6th edn, pp. 419-446, The Iowa State University Press, Ames
28. Dardevet, D., Sornet, C., Savary, I., Debras, E., Patureau-Mirand, P. and Grizard, J. (1998) Glucocorticoid effects on insulin- and IGF-I-regulated muscle protein metabolism during aging. J. Endocrinol. 156, 83-89
29. Ordway, G. A., Neufer, P. D., Chin, E. R. and DeMartino, G. N. (2000) Chronic contractile activity upregulates the proteasome system in rabbit skeletal muscle. J. Appl. Physiol. 88, 1134-1141
30. Combaret, L., Tilignac, T., Claustre, A., Voisin, L., Taillandier, D., Obled, C., Tanaka, K. and Attaix, D. (2002) Torbafylline (HWA 448) inhibits enhanced skeletal muscle ubiquitin-proteasome-dependent proteolysis in cancer and septic rats. Biochem. J. 361, 185-192
31. Hobler, S. C., Tiao, G., Fischer, J. E., Monaco, J. and Hasselgren, P. O. (1998) Sepsis-induced increase in muscle proteolysis is blocked by specific proteasome inhibitors. Am. J. Physiol. 274, R30-R37
32. Fang, C. H., Wang, J. J., Hobler, S., Li, B. G., Fischer, J. E. and Hasselgren, P. O. (1998) Proteasome blockers inhibit protein breakdown in skeletal muscle after burn injury in rats. Clin. Sci. 95, 225-233
33. Price, S. R., Bailey, J. L., Wang, X. N., Jurkovitz, C., England, B. K., Ding, X. Y., Phillips, L. S. and Mitch, W. E. (1996) Muscle wasting in insulinopenic rats results from activation of the ATP-dependent, ubiquitin-proteasome proteolytic pathway by a mechanism including gene transcription. J. Clin. Invest. 98, 1703-1708
34. Bailey, J. L., Wang, X. N., England, B. K., Price, S. R., Ding, X. Y. and Mitch, W. E. (1996) The acidosis of chronic renal failure activates muscle proteolysis in rats by augmenting transcription of genes encoding proteins of the ATP-dependent ubiquitin-proteasome pathway. J. Clin. Invest. 97, 1447-1453
35. Tawa, Jr, N. E., Odessey, R. and Goldberg, A. L. (1997) Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 100, 197-203
36. Lecker, S. H., Solomon, V., Price, S. R., Kwon, Y. T., Mitch, W. E. and Goldberg, A. L. (1999) Ubiquitin conjugation by the N-end rule pathway and mRNAs for its components increase in muscles of diabetic rats. J. Clin. Invest. 104, 1411-1420
37. Saad, M. J., Folli, F., Kahn, J. A. and Kahn, C. R. (1993) Modulation of insulin receptor, insulin receptor substrate-1, and phosphatidylinositol 3-kinase in liver and muscle of dexamethasone-treated rats. J. Clin. Invest. 92, 2065-2072
38. Giorgino, F. and Smith, R. J. (1995) Dexamethasone enhances insulin-like growth factor-I effects on skeletal muscle cell proliferation. Role of specific intracellular signaling pathways. J. Clin. Invest. 96, 1473-1483
39. Giorgino, F., Almahfouz, A., Goodyear, L. J. and Smith, R. J. (1993) Glucocorticoid regulation of insulin receptor and substrate IRS-1 tyrosine phosphorylation in rat skeletal muscle in vivo. J. Clin. Invest. 91, 2020-2030
40. Dardevet, D., Sornet, C., Vary, T. and Grizard, J. (1996) Phosphatidylinositol 3-kinase and p70 s6 kinase participate in the regulation of protein turnover in skeletal muscle by insulin and insulin-like growth factor I. Endocrinology 137, 4087-4094
41. Löw, P., Bussell, K., Dawson, S. P., Billett, M. A., Mayer, R. J. and Reynolds, S. E. (1997) Expression of a 26 S proteasome ATPase subunit, MS73, in muscles that undergo developmentally programmed cell death, and its control by ecdysteroid hormones in the insect Manduca sexta. FEBS Lett. 400, 345-349
42. Lam, Y. A., Lawson, T. G., Velayutham, M., Zweier, J. L. and Pickart, C. M. (2002) A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature (London) 416, 763-767
43. Voges, D., Zwickl, P. and Baumeister, W. (1999) The 26 S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015-1068
44. Kohler, A., Cascio, P., Leggett, D. S., Woo, K. M., Goldberg, A. L. and Finley, O. (2001) The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Mol. Cell 7, 1143-1152
45. Navon, A. and Goldberg, A. L. (2001) Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol. Cell 8, 1339-1349
46. Deveraux, Q., Ustrell, V., Pickart, C. and Rechsteiner, M. (1994) A 26 S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269, 7059-7061
47. Attaix, D., Taillandier, D., Combaret, L., Rallière, C., Larbaud, D., Aurousseau, E. and Tanaka, K. (1997) Expression of subunits of the 19 S complex and of the PA28 activator in rat skeletal muscle. Mol. Biol. Rep. 24, 95-98
48. Whitehouse, A. S. and Tisdale, M. J. (2001) Downregulation of ubiquitin-dependent proteolysis by eicosapentaenoic acid in acute starvation. Biochem. Biophys. Res. Commun. 285, 598-602
49. Whitehouse, A. S., Smith, H. J., Drake, J. L. and Tisdale, M. J. (2001) Mechanism of attenuation of skeletal muscle protein catabolism in cancer cachexia by eicosapentaenoic acid. Cancer Res. 61, 3604-3609
50. Taillandier, D., Aurousseau, E., Combaret, L., Guezennec, C.-Y. and Attaix, D. (2003) Regulation of proteolysis during reloading of the unweighted soleus muscle. Int. J. Biochem. Cell Biol. 35, 665-675
51. Dawson, S. P, Arnold, J. E., Mayer, N. J., Reynolds, S. E., Billett, M. A., Gordon, C., Colleaux, L., Kloetzel, P. M., Tanaka, K. and Mayer, R. J. (1995) Developmental changes of the 26 S proteasome in abdominal intersegmental muscles of Manduca sexta during programmed cell death. J. Biol. Chem. 270, 1850-1858