Muscle wasting in insulinopenic rats results from activation of the ATP- dependent, ubiquitin-proteasome proteolytic pathway by a mechanism including gene transcription

Journal of Clinical Investigation

Volumn 98, Issue 8, 1996, Pages 1703-1708

  Price, S Russ ^a,b   Bailey, James L ^a   Wang, Xiaonan ^a   Jurkovitz, Claudine ^a   England, Brian K ^a   Ding, Xiaoyu ^a   Phillips, Lawrence S ^a   Mitch, William E ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

diabetes; gene expression; insulin; protein degradation; skeletal muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALPAIN; MUSCLE PROTEIN; PROTEASOME; STREPTOZOCIN; UBIQUITIN;

ADIPOSE TISSUE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HYPOINSULINEMIA; LIVER WEIGHT; LYSOSOME; MUSCLE ATROPHY; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT;

EID: 0029861468     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118968     Document Type: Article

References (38)

1. Nair, K.S., G.C. Ford, and D. Halliday. 1987. Effect of intravenous insulin treatment on in vivo whole body leucine kinetics and oxygen consumption in insulin-deprived Type I diabetic patients. Metab. Clin. Exp. 36:491-495.
2. Nair, K.S., G.C. Ford, K. Ekberg, E. Fernqvist-Forbes, and J. Wahren. 1995. Protein dynamics in whole body and in splanchnic and leg tissues in type I diabetic patients. J. Clin. Invest. 95:2926-2937.
3. Nakhooda, A.F., C.-N. Wei, and E.B. Marliss. 1980. Muscle protein catabolism in diabetes: 3-methylhistidine excretion in the spontaneously diabetic "BB" rat. Metab. Clin. Exp. 29:1272-1277.
4. Marchesini, G., G. Forlani, M. Zoli, and E. Pisi. 1982. Muscle protein breakdown in uncontrolled diabetes as assessed by urinary 3-methylhistidine excretion. Diabetologia. 23:456-458.
5. Smith, O.L.K., C.Y. Wong, and R.A. Gelfand. 1989. Skeletal muscle proteolysis in rats with acute streptozotocin-induced diabetes. Diabetes. 38:1117-1122.
6. Gulve, E.A., and J.F. Dice. 1989. Regulation of protein synthesis and degradation in L8 myotubes: effects of serum, insulin, and insulin-like growth factors. Biochem. J. 260:377-387.
7. 3H1 myocytes. Am. J. Physiol. 260:C227-C282.
8. Gelfand, R.A., and E.J. Barrett. 1987. Effect of physiologic hyperinsulinemia on skeletal muscle protein synthesis and breakdown in man. J. Clin. Invest. 80:1-6.
9. Louard, R.J., D.A. Fryburg, R.A. Gelfand, and E.J. Barrett. 1992. Insulin sensitivity of protein and glucose metabolism in human forearm skeletal muscle. J. Clin. Invest. 90:2348-2354.
10. May, R.C., R.A. Kelly, and W.E. Mitch. 1987. Mechanisms for defects in muscle protein metabolism in rats with chronic uremia. The influence of metabolic acidosis. J. Clin. Invest. 79:1099-1103.
11. May, R.C., R.A. Kelly, and W.E. Mitch. 1986. Metabolic acidosis stimulates protein degradation in rat muscle by a glucocorticoid-dependent mechanism. J. Clin. Invest. 77:614-621.
12. Furuno, K., M.N. Goodman, and A.L. Goldberg. 1990. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J. Biol. Chem. 265:8550-8557.
13. Mitch, W.E., R. Medina, S. Greiber, R.C. May, B.K. England, S.R. Price, J.L. Bailey, and A.L. Goldberg. 1994. Metabolic acidosis stimulates muscle protein degradation by activating the ATP-dependent pathway involving ubiquitin and proteasomes. J. Clin. Invest. 93:2127-2133.
14. Bailey, J.L., X. Wang, B.K. England, S.R. Price, X. Ding, and W.E. Mitch. 1996. The acidosis of chronic renal failure activates muscle proteolysis in rats by augmenting transcription of genes encoding the ATP-dependent, ubiquitin-proteasome pathway. J. Clin. Invest. 97:1447-1453.
15. Tiao, G., J.M. Fagan, N. Samuels, J.H. James, K. Hudson, M. Lieberman, J.E. Fischer, and P.-O. Hasselgren. 1994. Sepsis stimulates nonlysosomal. energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J. Clin. Invest. 94:2255-2264.
16. Wing, S.S., and A.L. Goldberg. 1993. Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am. J. Physiol. 264:E668-E676.
17. 2-adrenergic agonist (Clenbuterol). Role of the ATP-ubiquitin-dependent proteolytic pathway. J. Clin. Invest. 95:2367-2372.
18. Baracos, V.E., C. DeVivo, D.H.R. Hoyle, and A.L. Goldberg. 1995. Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am. J. Physiol. 268:E996-E1006.
19. Medina, R., S.S. Wing, and A.L. Goldberg. 1995. Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem. J. 307:631-637.
20. Goldberg, A.L. 1995. Functions of the proteasome: the lysis at the end of the tunnel. Science (Wash. DC). 268:522-523.
21. Hilt, W., and D.H. Wolf. 1996. Proteasomes: destruction as a programme. Trends Biochem. Sci. 21:96-102.
22. Ciechanover, A. 1995. The ubiquitin-proteasome proteolytic pathway. Cell. 79:13-21.
23. Dubiel, W., K. Ferrel, G. Pratt, and M. Rechsteiner. 1992. Subunit 4 of the 26S protease is a member of a novel eukaryotic ATPase family. J. Biol. Chem. 267:22699-22702.
24. Hanada, K., M. Tamai, T. Adachi, K. Oguma, K. Kashiwagi, S. Ohmura, E. Kominami, T. Towatari, and N. Katunuma. 1983. Characterization of the three new analogs of E-64 and their therapeutic application. In Proteinase Inhibitors: Medical and Biological Aspects. N. Katunuma, editor. Springer-Verlag, Tokyo. 25-36.
25. Gronostajski, R.M., A.B. Pardee, and A.L. Goldberg. 1985. The ATP dependence of the degradation of short- and long-lived proteins in growing fibroblasts. J. Biol. Chem. 260:3344-3349.
26. Jensen, T.J., M.A. Loo, S. Pind, D.B. Williams, A.L. Goldberg, and J.R. Riordan. 1995. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell. 83:129-135.
27. Read, M.A., A.S. Neish, F.W. Luscinskas, V.J. Palombella, T. Maniatis, and T. Collins. 1995. The proteasome pathway is required for cytokine-induced endothelial-leukocyte adhesion molecule expression. Immunity. 2:493-506.
28. Palombella, V.J., O.J. Rando, A.L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-kappaB precursor and the activation of NF-kappaB. Cell. 78:773-785.
29. Price, S.R., B.K. England, J.L. Bailey, K. Van Vreede, and W.E. Mitch. 1994. Acidosis and glucocorticoids concomitantly increase ubiquitin and proteasome subunit mRNA levels in rat muscles. Am. J. Physiol. 267:C955-C960.
30. Feinberg, A.P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
31. Clark, A.S., and W.E. Mitch. 1983. Comparison of protein synthesis and degradation in incubated and perfused muscle. Biochem. J. 212:649-653.
32. Goodman, M.N. 1987. Myofibrillar protein breakdown in skeletal muscle is diminished in rats with chronic streptozotocin-induced diabetes. Diabetes. 36:100-105.
33. Kettelhut, I.C., M.T. Pepato, R.H. Migliorini, R. Medina, and A.L. Goldberg. 1994. Regulation of different proteolytic pathways in skeletal muscle in fasting and diabetes mellitus. Braz. J. Med. Biol. Res. 27:981-993.
34. Temparis, S., M. Asensi, D Taillandier, E. Aurousseau, D. Larband, A. Obled, D. Béchet, M. Ferrara, J.M. Estrela, and D. Attaix. 1994. Increased ATP-ubiquitin-dependent proteolysis in skeletal muscles of tumor-bearing rats. Cancer Res. 54:5568-5573.
35. Fang, C.-H., H.J. James, C. Ogle, J.E. Fischer, and P.-O. Hasselgren. 1995. Burn injury stimulates multiple proteolytic pathways in skeletal muscle, including the ubiquitin-energy-dependent pathway. J. Am. Coll. Surg. 180:161-170.
36. Nesher, R., I.E. Karl, K.E. Kaiser, and D.M. Kipnis. 1980. Epitrochlearis muscle. I. Mechanical performance, energetics, and fiber composition. Am. J. Physiol. 239:E454-E460.
37. Ariano, M.A., R.B. Armstrong, and V.R. Edgerton. 1973. Hindlimb muscle fiber populations of five mammals. J. Histochem. Cytochem. 21:51-55.
38. Medina, R., S.S. Wing, and A.L. Goldberg. 1995. Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem. J. 307:631-637.