Ubiquitin-conjugating enzyme E214k/HR6B is dispensable for increased protein catabolism in muscle of fasted mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 283, Issue 3 46-3, 2002, Pages

  Adegoke, Olasunkanmi A J ^a   Bédard, Nathalie ^b   Roest, Henk P ^a   Wing, Simon S ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

Author keywords

Muscle incubation; Muscle wasting; Proteasome; Starvation; Ubiquitin conjugation

Indexed keywords

UBIQUITIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVITY; ENZYME SUBSTRATE; MICHAELIS CONSTANT; MOUSE; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; SOLEUS MUSCLE; STARVATION;

EID: 0036711190     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00097.2002     Document Type: Article

References (60)

1. Adegoke OA, McBurney MI, Samuels SE, and Baracos VE. Luminal amino acids acutely decrease intestinal mucosal protein synthesis and protease mRNA in piglets. J Nutr 129: 1871-1878, 1999.
2. Auclair D, Garrel DR, Chaouki Zerouala A, and Ferland LH. Activation of the ubiquitin pathway in rat skeletal muscle by catabolic doses of glucocorticoids. Am J Physiol Cell Physiol 272: C1007-C1016, 1997.
3. Ausabel FM, Brent R, Kingston DD, Moore DD, Seidman JG, Smith JA, and Struhl K. Current Protocols in Molecular Biology. New York: Wiley, 1993.
4. Bachmair A, Finley D, and Varshavsky A. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234: 179-186, 1986.
5. Bailey JL, Price SR, England BK, Jurkovitz C, Wang X, Ding X, and Mitch WE. Signals regulating accelerated muscle protein catabolism in uremia. Miner Electrolyte Metab 23: 198-200, 1997.
6. Bailey JL, Wang X, and Price SR. The balance between glucocorticoids and insulin regulates muscle proteolysis via the ubiquitin-proteasome pathway. Miner Electrolyte Metab 25: 220-223, 1999.
7. Baracos VE. Regulation of skeletal muscle-protein turnover in cancer-associated cachexia. Nutrition 16: 1015-1018, 2000.
8. Baracos V, DeVivo C, Hoyle D, and Goldberg A. Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am J Physiol Endocrinol Metab 268: E996-E1006, 1995.
9. Baracos VE and Goldberg AL. Maintenance of normal length improves protein balance and energy status in isolated rat skeletal muscles. Am J Physiol Cell Physiol 251: C588-C596, 1986.
10. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, and Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
11. Chrysis D and Underwood L. 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, 1999.
12. Ciechanover A, Orian A, and Schwartz AL. The ubiquitin-mediated proteolytic pathway: Mode of action and clinical implications. J Cell Biochem Suppl 34: 40-51, 2000.
13. Cieslar J, Huang MT, and Dobson GP. Tissue spaces in rat heart, liver, and skeletal muscle in vivo. Am J Physiol Regul Integr Comp Physiol 275: R1530-R1536, 1998.
14. Combaret L, Ralliere C, Taillandier D, Tanaka K, and Attaix D. Manipulation of the ubiquitin-proteasome pathway in cachexia: Pentoxifylline suppresses the activation of 20S and 26S proteasomes in muscles from tumor-bearing rats. Mol Biol Rep 26: 95-101, 1999.
15. Fang CH, Li BG, Sun X, and Hasselgren PO. Insulin-like growth factor I reduces ubiquitin and ubiquitin-conjugating enzyme gene expression but does not inhibit muscle proteolysis in septic rats. Endocrinology 141: 2743-2751, 2000.
16. Fang CH, Sun X, Li BG, Fischer DR, Pritts TA, Penner G, and Hasselgren PO. Burn injuries in rats upregulate the gene expression of the ubiquitin-conjugating enzyme E2(14k) in skeletal muscle. J Burn Care Rehabil 21: 528-534, 2000.
17. Finley D, Ciechanover A, and Varshavsky A. Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85. Cell 37: 43-55, 1984.
18. Fischer D, Sun X, Gang G, Pritts T, and Hasselgren PO. The gene expression of ubiquitin ligase E3alpha is upregulated in skeletal muscle during sepsis in rats - Potential role of glucocorticoids. Biochem Biophys Res Commun 267: 504-508, 2000.
19. Furuno K, Goodman MN, and Goldberg AL. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265: 8550-8557, 1990.
20. Gomes MD, Lecker SH, Jagoe RT, Navon A, and Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001.
21. Goodman MN, McElaney MA, and Ruderman NB. Adaptation to prolonged starvation in the rat: curtailment of skeletal muscle proteolysis. Am J Physiol Endocrinol Metab 241: E321-E327, 1981.
22. Haas AL and Siepmann TJ. Pathways of ubiquitin conjugation. FASEB J 11: 1257-1268, 1997.
23. Hallauer PL and Hastings KE. Coregulation of fast contractile protein transgene and glycolytic enzyme expression in mouse skeletal muscle. Am J Physiol Cell Physiol 282: C113-C124, 2002.
24. Hobler SC, Tiao G, Fischer JE, Monaco J, and Hasselgren PO. Sepsis-induced increase in muscle proteolysis is blocked by specific proteasome inhibitors. Am J Physiol Regul Integr Comp Physiol 274: R30-R37, 1998.
25. 14k mRNA in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 276: R468-R473, 1999.
26. Jagoe RT and Goldberg AL. What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 4: 183-190, 2001.
27. Koken MH, Reynolds P, Jaspers-Dekker I, Prakash L, Prakash S, Bootsma D, and Hoeijmakers JH. Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc Natl Acad Sci USA 88: 8865-8869, 1991.
28. Kwon YT, Xia Z, Davydov IV, Lecker SH, and Varshavsky A. Construction and analysis of mouse strains lacking the ubiquitin ligase UBR1 (E3alpha) of the N-end rule pathway. Mol Cell Biol 21: 8007-8021, 2001.
29. Lecker SH, Solomon V, Price SR, Kwon YT, Mitch WE, and Goldberg AL. 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, 1999.
30. Lorite MJ, Smith HJ, Arnold JA, Morris A, Thompson MG, and Tisdale MJ. Activation of ATP-ubiquitin-dependent proteolysis in skeletal muscle in vivo and murine myoblasts in vitro by a proteolysis-inducing factor (PIF). Br J Cancer 85: 297-302, 2001.
31. Lorite MJ, Thompson MG, Drake JL, Carling G, and Tisdale MJ. Mechanism of muscle protein degradation induced by a cancer cachectic factor. Br J Cancer 78: 850-856, 1998.
32. Lowell BB, Ruderman NB, and Goodman MN. Evidence that lysosomes are not involved in the degradation of myofibrillar proteins in rat skeletal muscle. Biochem J 234: 237-240, 1986.
33. Mansoor O, Beaufrere B, Boirie Y, Ralliere C, Taillandier D, Aurousseau E, Schoeffler P, Arnal M, and Attaix D. Increased mRNA levels for components of the lysosomal, Ca2+-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc Natl Acad Sci USA 93: 2714-2718, 1996.
34. McGrath JP, Jentsch S, and Varshavsky A. UBA 1: An essential yeast gene encoding ubiquitin-activating enzyme. EMBO J 10: 227-236, 1991.
35. Mitch WE, Bailey JL, Wang X, Jurkovitz C, Newby D, and Price SR. Evaluation of signals activating ubiquitin-proteasome proteolysis in a model of muscle wasting. Am J Physiol Cell Physiol 276: C1132-C1138, 1999.
36. Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533, 2001.
37. Pickart CM and Rose IA. Functional heterogeneity of ubiquitin carrier proteins. J Biol Chem 260: 1573-1581, 1985.
38. Price SR, Bailey JL, Wang X, Jurkovitz C, England BK, Ding X, Phillips LS, and Mitch WE. 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, 1996.
39. Rajapurohitam V, Bédard N, and Wing SS. Control of ubiquitination of proteins in rat tissues by ubiquitin-conjugating enzymes and isopeptidases. Am J Physiol Endocrinol Metab 282: E739-E745, 2002.
40. Rajapurohitam V, Morales CR, El-Alfy M, Lefrancois S, Bédard N, and Wing SS. Activation of a UBC4-dependent pathway of ubiquitin conjugation during postnatal development of the rat testis. Dev Biol 212: 217-28, 1999.
41. Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MHM, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JTM, Baarends WM, Bootsma D, Grootegoed JA, and Hoeijmakers JHJ. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 86: 799-810, 1996.
42. Samuels SE, Taillandier D, Aurousseau E, Cherel Y, Le Maho Y, Arnal M, and Attaix D. Gastrointestinal tract protein synthesis and mRNA levels for proteolytic systems in adult fasted rats. Am J Physiol Endocrinol Metab 271: E232-E238, 1996.
43. Smith HJ, Lorite MJ, and Tisdale MJ. Effect of a cancer cachectic factor on protein synthesis/degradation in murine C2C12 myoblasts: Modulation by eicosapentaenoic acid. Cancer Res 59: 5507-5513, 1999.
44. Solomon V, Baracos V, Sarraf P, and Goldberg AL. Rates of ubiquitin conjugation increase when muscles atrophy, largely through activation of the N-end rule pathway. Proc Natl Acad Sci USA 95: 12602-12607, 1998.
45. Solomon V, Lecker SH, and Goldberg AL. The N-end rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle. J Biol Chem 273: 25216-25222, 1998.
46. Strelkov AB, Fields AL, and Baracos VE. Effects of systemic inhibition of prostaglandin production on protein metabolism in tumor-bearing rats. Am J Physiol Cell Physiol 257: C261-C269, 1989.
47. Taillandier D, Aurousseau E, Meynial-Denis D, Bechet D, Ferrara M, Cottin P, Ducastaing A, Bigard X, Guezennec CY, Schmid HP, and Attaix D. Coordinate activation of lysosomal, Ca2+-activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. Biochem J 316: 65-72, 1996.
48. Tawa NE Jr, Odessey R, and Goldberg AL. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J Clin Invest 100: 197-203, 1997.
49. Temparis S, Asensi M, Taillandier D, Aurousseau E, Larbaud D, Obled A, Bechet D, Ferrara M, Estrela JM, and Attaix D. Increased ATP-ubiquitin-dependent proteolysis in skeletal muscles of tumor-bearing rats. Cancer Res 54: 5568-5573, 1994.
50. Varshavsky A. The N-end rule: Functions, mysteries, uses. Proc Natl Acad Sci USA 93: 12142-12149, 1996.
51. Voisin L, Breuille D, Combaret L, Pouyet C, Taillandier D, Aurousseau E, Obled C, and Attaix D. Muscle wasting in a rat model of long-lasting sepsis results from the activation of lysosomal, Ca2+-activated, and ubiquitin-proteasome proteolytic pathways. J Clin Invest 97: 1-8, 1996.
52. Waalkes US. A fluorometric method for the estimation of tyrosine in plasma and tissues. J Lab Clin Med 50: 733-736, 1957.
53. Whitehouse AS, Smith HJ, Drake JL, and Tisdale MJ. Mechanism of attenuation of skeletal muscle protein catabolism in cancer cachexia by eicosapentaenoic acid. Cancer Res 61: 3604-3609, 2001.
54. Whitehouse AS and Tisdale MJ. Downregulation of ubiquitin-dependent proteolysis by eicosapentaenoic acid in acute starvation. Biochem Biophys Res Commun 285: 598-602, 2001.
55. Wilkinson KD. Roles of ubiquitinylation in proteolysis and cellular regulation. Annu Rev Nutr 15: 161-189, 1995.
56. Wing SS and Banville D. 14-kDa ubiquitin-conjugating enzyme: structure of the rat gene and regulation upon fasting and by insulin. Am J Physiol Endocrinol Metab 267: E39-E48, 1994.
57. Wing SS and Bédard N. Insulin-like growth factor I stimulates degradation of an mRNA transcript encoding the 14 kDa ubiquitin-conjugating enzyme. Biochem J 319: 455-461, 1996.
58. Wing SS, Dumas F, and Banville D. A rabbit reticulocyte ubiquitin carrier protein that supports ubiquitin-dependent proteolysis (E214k) is homologous to the yeast DNA repair gene RAD6. J Biol Chem 267: 6495-6501, 1992.
59. Wing SS and Goldberg AL. Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am J Physiol Endocrinol Metab 264: E668-E676, 1993.
60. Wing SS, Haas AL, and Goldberg AL. Increase in ubiquitin-protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation. Biochem J 307: 639-645, 1995.