Muscle protein breakdown and the critical role of the ubiquitin- proteasome pathway in normal and disease states

Journal of Nutrition

Volumn 129, Issue 1 SUPPL., 1999, Pages

  Lecker, Stewart H ^a   Solomon, Vered ^a   Mitch, William E ^b   Goldberg, Alfred L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCLE PROTEIN; PROTEASOME; UBIQUITIN;

CACHEXIA; CLINICAL TRIAL; CONFERENCE PAPER; HUMAN; LYSOSOME; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE METABOLISM; NONHUMAN; PROTEIN DEGRADATION; PROTEIN METABOLISM; SIGNAL TRANSDUCTION; WASTING SYNDROME;

EID: 0032947267     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/129.1.227s     Document Type: Conference Paper

References (105)

1. Akopian, T. N., Kisselev, A. F. & Goldberg, A. L. (1997) Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum. J. Biol. Chem. 272: 1791-1798.
2. Alkalay, I., Yaron, A., Hatzubai, A., Orian, A., Ciechanover, A. & Ben-Neriah, Y. (1995) Stimulation-dependent IkBα phosphorylation marks the NF-kB inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U S A 92: 10599-10560.
3. Bachmair, A., Finley, D. & Varshavsky, A. (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science 234: 179-186.
4. Bailey, J. L., Wang, X., England, B. K., Price, S. R., Ding, X. & 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.
5. Baracos, V. E., DeVivo, C., Hoyle, D. H. & Goldberg, A. L. (1995) Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am. J. Physiol. 268: E996-E1006.
6. Bogyo, M., McMaster, J. S., Gaczynska, M., Tortorella, D., Goldberg, A. L. & Ploegh, H. (1997) Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HsIV by a new class of inhibitors. Proc. Natl. Acad. Sci. U S A 94: 6629-6634.
7. Breuille, D., Farge, M. C., Rose, F., Amal, M., Attaix, D. & Obled, C. (1993) Pentoxifylline decreases body weight loss and muscle protein wasting characteristics of sepsis. Am. J. Physiol. 265: E660-E666.
8. Busch, H. (1984) Ubiquitination of proteins. Methods in Enzymology 106: 238-262.
9. Caiozzo, V. J., Baker, M. J., Herrick, R. E., Tao, M. & Baldwin, K.M. (1994) Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. J. Appl. Physiol. 76: 1764-1773.
10. Caiozzo, V. J., Haddad, F., Baker, M. J., Herrick, R. E., Prietto, N. & Baldwin, K. M. (1996) Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J. Appl. Physiol. 81: 123-132.
11. Cariuk, P., Lorite, M. J., Todorov, P. T., Field, W. N., Wigmore, S. J. & Tisdale, M. J. (1997) Induction of cachexia in mice by a product isolated from the urine of cachectic cancer patients. Br. J. Cancer 76: 606-613.
12. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K. & Varshavsky, A. (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243: 1576-1583.
13. Chiang, H. L., Terlecky, S. R., Plant, C. P. & Dice, J. F. (1989) A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246: 382-385.
14. Chu-Ping, M., Vu, J. H., Proske, R. J., Slaughter, C. A. & Demartino, G. N. (1994) Identification, purification, and characterization of a high molecular weight, ATP-dependent activator (PA700) of the 203 proteasome. J. Biol. Chem. 269: 3539-3547.
15. Ciechanover, A., Hod, Y. & Hershko, A. (1978) A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem. Biophys. Res. Commun. 81: 1100-1105.
16. Clark, A. S., Kelly, R. A. & Mitch, W. E. (1984) Systemic response to thermal injury in rats. Accelerated protein degradation and altered glucose utilization in muscle. J. Clin. Invest. 74: 888-897.
17. Clark, A. S. & Mitch, W. E. (1983) Muscle protein turnover and glucose uptake in acutely uremic rats. Effects of insulin and the duration of renal insufficiency. J. Clin. Invest. 72: 836-845.
18. Clowes, G. H., Jr., O'Donnell, T. F., Blackburn, G. L. & Maki, T. N. (1976) Energy metabolism and proteolysis in traumatized and septic man. Surg. Clin. North Am. 56: 1169-1184.
19. Costelli, P., Carbo, N., Tessitore, L., Bagby, G. J., Lopez-Soriano, F. J., Argiles, J. M. & Baccino, F. M. (1993) Tumor necrosis factor-α mediates changes in tissue protein turnover in a rat cancer cachexia model. J. Clin. Invest. 92: 2783-2789.
20. Coux, O., Tanaka, K. & Goldberg, A. L. (1996) Structure and functions of the 20S and 26S proteasomes. Ann. Rev. Biochem. 65: 801-847.
21. Dice, J. F. (1990) Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem. Sci. 15: 305-309.
22. Dick, L. R., Cruikshank, A. A., Grenier, L., Melandri, F. D., Nunes, S. L. & Stein, R. L. (1996) Mechanistic studies On the inactivation of the proteasome by lactacystin - a central role for clasto-lactacystin beta-lactone. J. Biol. Chem. 271: 7273-7276.
23. Fang, C. H., Tiao, G., James, H., Ogle, C., Fischer, J. E. & Hasselgren, P. O. (1995) Bum injury stimulates multiple proteolytic pathways in skeletal muscle, including the ubiquitin-energy-dependent pathway. J. Am. Coll. Surg. 180: 161-170.
24. Fenteany, G., Standaert, R. F., Lane, W. S., Choi, S., Corey, E. J. & Schreiber, S. L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268: 726-731.
25. Finley, D., Ciechanover, A. & Varshavsky, A. (1984) Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85. Cell 37:43-55.
26. Flakoll, P. J., Wentzel, L. S. & Hyman, S. A. (1995) Protein and glucose metabolism during isolated closed-head injury. Am. J. Physiol. 269: E636-E641.
27. Fulks, R. M., Li, J. B. & Goldberg, A. L. (1975) Effects of insulin, glucose, and amino acids on protein turnover in rat diaphragm. J. Biol. Chem. 250: 290-298.
28. Furuno, K. & Goldberg, A. L. (1986) The activation of protein degradation in muscle by Ca2+ or muscle injury does not involve a lysosomal mechanism. Biochem. J. 237: 859-864.
29. Gaczynska, M., Rock, K. L., Spies, T. & Goldberg, A. L. (1994) Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for Imp2 and Imp7. Proc. Natl. Acad. Sci. U S A 91: 9213-9217.
30. Glickman, M., Rubin, D., Fried, V. & Finley, D. (1998) The regulatory particle of the S. cerevisiae proteasome. Mol. Cell. Biol. [in press].
31. Glotzer, M., Murray, A. W. & Kirschner, M. W. (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138.
32. Goldberg, A. L. (1969) Protein turnover in skeletal muscle. II. Effects of denervation and cortisone on protein catabolism in skeletal muscle. J. Biol. Chem. 244: 3223-3229.
33. Goldberg, A. L., Gaczynska, M., Grant, E., Michalek, M. & Rock, K. L. (1995a) The functions of the proteasome in antigen presentation. In: Protein Kinesis: The Dynamics of Protein Trafficking and Stability. Cold Spring Harbor Laboratory Press, New York, NY. pp. 479-490.
34. Goldberg, A. L. & Goodman, H. M. (1969) Relationship between cortisone and muscle work in determining muscle size. J. Physiol. 200: 667-675.
35. Goldberg, A. L. & St. John, A. C. (1976) Intracellular protein degradation in mammalian and bacterial cells: Part 2. Ann. Rev. Biochem. 45: 747-803.
36. Goldberg, A. L., Stein, R. & Adams, J. (1995b) New Insights Into Proteasome Function - From Archaebacteria to Drug Development. Chem. Biol. 2: 503-508.
37. Goll, D. E., Thompson, V. F., Taylor, R. G. & Christiansen, J. A. (1992) Role of the calpain system in muscle growth. Biochimie 74: 225-237.
38. Goodman, M. N. (1994) Interleukin-6 induces skeletal muscle protein breakdown in rats. Proc. Soc. Exp. Biol. Med. 205: 182-185.
39. Goodman, M. N. (1991) Tumor necrosis factor induces skeletal muscle protein breakdown in rats. Am. J. Physiol. 260: E727-E730.
40. Groll, M., Ditzel, L., Lowe, J., Stock, D., Bochtler, M., Bartunik, H. D. & Huber, R. (1997) Structure of 20S proteasome from yeast at 2.4-angstrom resolution. Nature 386: 463-471.
41. Gronostajski, R. M., Goldberg, A. L. & Pardee, A. B. (1984) The role of increased proteolysis in the atrophy and arrest of proliferation in serum-deprived fibroblasts. J. Cell. Physiol. 121: 189-198.
42. Haas, A. L. & Bright, P. M. (1988) The resolution and characterization of putative ubiquitin carrier protein isozymes from rabbit reticulocytes. J. Biol. Chem. 263: 13258-13267.
43. Haas, A. L. & Rose, I. A. (1982) The mechanism of ubiquitin activating enzyme. A kinetic and equilibrium analysis. J. Biol. Chem. 257: 10329-10337.
44. Hadari, T., Warms, J. V., Rose, I. A. & Hershko, A. (1992) A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains. Role in protein degradation. J. Biol. Chem. 267: 719-727.
45. Handley, P. M., Mueckler, M., Siegel, N. R., Ciechanover, A. & Schwartz, A. L. (1991) Molecular cloning, sequence, and tissue distribution of the human ubiquitin-activating enzyme E1. Proc. Natl. Acad. Sci. U S A 88: 258-262.
46. Hershko, A., Ciechanover, A., Heller, H., Haas, A. L. & Rose, I. A. (1980) Proposed role of ATP in protein breakdown: conjugation of protein with multiple chains of the polypeptide of ATP-dependent proteolysis. Proc. Natl. Acad. Sci. U S A 77: 1783-1786.
47. Hershko, A., Ciechanover, A. & Rose, I. A. (1981) Identification of the active amino acid residue of the polypeptide of ATP-dependent protein breakdown. J. Biol. Chem. 256: 1525-1528.
48. Hoyt, M. A. (1997) Eliminating all obstacles: regulated proteolysis in the eukaryotic cell cycle. Cell 91: 149-151.
49. Huszar, G. (1972) Developmental changes of the primary structure and histidine methylation in rabbit skeletal muscle myosin. Nat. New Biol. 240: 260-264.
50. Isozaki, Y., Mitch, W. E., England, B. K. & Price, S. R. (1996) Protein Degradation and increased mRNAs encoding proteins of the ubiquitin-proteasome proteolytic pathway in BC(3)H1 myocytes require an interaction between glucocorticoids and acidification. Proc. Natl. Acad. Sci. U S A 93: 1967-1971.
51. Jensen, T. J., Loo, M. A., Pind, S., Williams, D. B., Goldberg, A. L. & Riordan, J. R. (1995) Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83: 129-135.
52. Jentsch, S. (1992) The ubiquitin-conjugation system. Ann. Rev. Genet. 26: 179-207.
53. Kam, Y. A., Xu, W., Demartino, G. N. & Cohen, R. E. (1997) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385: 737-740.
54. King, R. W., Jackson, P. K. & Kirschner, M. W. (1994) Mitosis in transition. Cell 79: 563-571.
55. Kisselev, A. F., Akopian, T. N. & Goldberg, A. L. (1998) Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes. J. Biol. Chem. 273: 1982-1989.
56. Lardeux, B. R. & Mortimore, G. E. (1987) Amino acid and hormonal control of macromolecular turnover in perfused rat liver. Evidence for selective autophagy. J. Biol. Chem. 262: 14514-14519.
57. Larsen, C. N. & Finley, D. (1997) Protein translocation channels in the proteasome and other proteases. Cell 91: 431-434.
58. Lawson, D. H., Richmond, A., Nixon, D. W. & Rudman, D. (1982) Metabolic approaches to cancer cachexia. Ann. Rev. Nutr. 2: 277-301.
59. Lowe, J., Stock, D., Jap, B., Zwickl, P., Baumeister, W. & Huber, R. (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 268: 533-539.
60. Lowell, B. B., Ruderman, N. B. & Goodman, M. N. (1986) Evidence that lysosomes are not involved in the degradation of myofibrillar proteins in rat skeletal muscle. Biochem. J. 234: 237-240.
61. Mansoor, O., Beaufrere, B., Boirie, Y., Ralliere, C., Taillandier, D., Aurousseau, E., Schoeffler, P., Amal, M. & Attaix, D. (1996) 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. U S A 93: 2714-2718.
62. May, R. C., Kelly, R. A. & Mitch, W. E. (1987) Mechanisms for defects in muscle protein metabolism in rats with chronic uremia. Influence of metabolic acidosis. J. Clin. Invest. 79: 1099-1103.
63. May, R. C., Kelly, R. A. & Mitch, W. E. (1986) Metabolic acidosis stimulates protein degradation in rat muscle by a glucocorticoid-dependent mechanism. J. Clin. Invest. 77: 614-621.
64. May, R. C., Piepenbrock, N., Kelly, R. A. & Mitch, W. E. (1991) Leucine-induced amino acid antagonism in rats: muscle valine metabolism and growth impairment. J. Nutr. 121: 293-301.
65. Medina, R., Wing, S. S. & Goldberg, A. L. (1995) Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem. J. 307: 631-637.
66. Medina, R., Wing, S. S., Haas, A. & Goldberg, A. L. (1991) Activation of the ubiquitin-ATP-dependent proteolytic system in skeletal muscle during fasting and denervation atrophy. Biomed. Biochim. Acta 50: 347-356.
67. Mellgren, R. L. (1987) Calcium-dependent proteases: an enzyme system active at cellular membranes? FASEB J. 1: 110-115.
68. Michalek, M. T., Grant, E. P., Gramm, C., Goldberg, A. L. & Rock, K. L. (1993) A role for the ubiquitin-dependent proteolytic pathway in MHC class l-restricted antigen presentation. Nature 363: 552-554.
69. Mitch, W. E. & Goldberg, A. L. (1996) Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335: 1897-1905.
70. Mitch, W. E., Medina, R., Grieber, S., May, R. C., England, B. K., Price, S. R., Bailey, J. L. & Goldberg, A. L. (1994) Metabolic acidosis stimulates muscle protein degradation by activating the adenosine triphosphate-dependent pathway involving ubiquitin and proteasomes. J. Clin. Invest. 93: 2127-2133.
71. Murachi, T., Tanaka, K., Hatanaka, M. & Murakami, T. (1980) Intracellular Ca2+-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin). Adv. Enzyme Regul. 19: 407-424.
72. Papa, F. R. & Hochstrasser, M. (1993) The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366: 313-319.
73. Pickart, C. M. (1997) Targeting of substrates to the 26S proteasome. FASEB J. 11: 1055-1066.
74. Pickart, C. M. & Rose, I. A. (1985) Functional heterogeneity of ubiquitin carrier proteins. J. Biol. Chem. 260: 1573-1581.
75. Price, S. R., Bailey, J. L., Wang, X. N., Jurkovitz, C., England, B. K., Ding, X. Y., Phillips, L. S. & 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.
76. Price, S. R., England, B. K., Bailey, J. L., Van Vreede, K. & Mitch, W. E. (1994) Acidosis and glucocorticoids concomitantly increase ubiquitin and proteasome subunit mRNAs in rat muscle. Am. J. Physiol. 267: C955-C960.
77. Reaich, D., Grewal, M., Price, S., Bailey, J., England, B. & Mitch, W. (1994) Catabolism in acute renal failure (ARF): Evidence for stimulation of the ubiquitin-proteasome system and activation of branched-chain aketoacid dehydrogenase (BCKAD). J. Am. Soc. Nephrol. 4: 953.
78. Rechsteiner, M., Huffman, L. & Dubiel, W. (1993) The multicatalytic and 26-S proteases. J. Biol. Chem. 268: 6065-6068.
79. Rock, K. L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. & Goldberg, A.L. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class 1 molecules. Cell 78: 761-771.
80. Salvesen, G. S. & Dixit, V. M. (1997) Caspases: intracellular signaling by proteolysis. Cell 91: 443-446.
81. Scheffner, M., Huibregtse, J. M., Vierstra, R. D. & Howley, P. M. (1993) The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75: 495-505.
82. Scherer, D. C., Brockman, J. A., Chen, Z. J., Maniatis, T. & Ballard, D. W. (1995) Signal-induced degradation of IkBα requires site-specific ubiquitination. Proc. Natl. Acad. Sci. U S A 92: 11259-11263.
83. Schoenheimer, R. (1942) Dynamic State of Body Constituents. Harvard University Press, Cambridge, MA.
84. Seemuller, E., Lupas, A., Stock, D., Lowe, J., Huber, R. & Baumeister, W. (1995) Proteasome from thermoplasma acidophilum - a threonine protease. Science 268: 579-582.
85. Stancovski, I., Gonen, H., Orian, A., Schwartz, A. L. & Ciechanover, A. (1995) Degradation of the proto-oncogene product c-Fos by the ubiquitin proteolytic system in vivo and in vitro: identification and characterization of the conjugating enzymes. Mol. Cell. Biol. 15: 7106-7116.
86. Tawa, N. E. & Goldberg, A. L. (1994) Protein and amino acid metabolism in muscle. In: Myology: Basic and Clinical. 2nd ed. (Engle A. G. & Franzini-Armstrong, C. eds.), Field and Wood, New York, NY. pp. 683-707.
87. Tawa, N. E., Jr. & Goldberg, A. L. (1992) Suppression of muscle protein turnover and amino acid degradation by dietary protein deficiency. Am. J. Physiol. 263: E317-E325.
88. Tawa, N. E., Odessey, R. & Goldberg, A. L. (1997) Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 100: 197-203.
89. Tawa, N. E., Odessey, R. & Goldberg, A. L. (1997) Peptide aldehyde inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscle. J. Clin. Invest. 100: 1-7.
90. Temparis, S., Asensi, M., Taillandier, D., Aurousseau, E., Larbaud, D., Obled, A., Bechet, D., Ferrara, M., Estrela, J. M. & Attaix, D. (1994) Increased ATP-ubiquitin-dependent proteolysis in skeletal muscles of tumor-bearing rats. Cancer Res. 54: 5568-5573.
91. Thomason, D. B. & Booth, F. W. (1990) Atrophy of the soleus muscle by hindlimb unweighting. J. Appl. Physiol. 68: 1-12.
92. Thomason, D. B., Herrick, R. E., Surdyka, D. & Baldwin, K. M. (1987) Time course of soleus muscle myosin expression during hindlimb suspension and recovery. J. Appl. Physiol. 63: 130-137.
93. Tiao, G., Fagan, J. M., Samuels, N., James, J. H., Hudson, K., Lieberman, M., Fischer, J. E. & Hasselgren, P. O. (1994) Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J. Clin. Invest. 94: 2255-2264.
94. Todorov, P., Cariuk, P., McDevitt, T., Coles, B., Fearon, K. & Tisdale, M. (1996) Characterization of a cancer cachectic factor. Nature 379: 739-742.
95. Treier, M., Staszewski, L. M. & Bohmann, D. (1994) Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78: 787-798.
96. Varshavsky, A. (1992) The N-end rule. Cell 69: 725-735.
97. Vinitsky, A., Cardozo, C., Sepp-Lorenzino, L., Michaud, C. & Orlowski, M. (1994) Inhibition of the proteolytic activity of the multicatalytic proteinase complex (proteasome) by substrate-related peptidyl aldehydes. J. Biol. Chem. 269: 29860-29866.
98. Ward, C. L., Omura, S. & Kopito, R. R. (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83:121-127.
99. Waxman, L. (1981) Calcium-activated proteases in mammalian tissues. Methods Enzymol. 80: 664-680.
100. Wilkinson, K. D., Tashayev, V. L., O'Connor, L. B., Larsen, C. N., Kasperek, E. & Pickart, C. M. (1995) Metabolism of the polyubiquitin degradation signal -structure, mechanism, and role of isopeptidase T. Biochemistry 34: 14535-14546.
101. Wing, S. S. & Goldberg, A. L. (1993) Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am. J. Physiol. 264: E668-E676.
102. Wing, S. S., Haas, A. L. & Goldberg, A. L. (1995) 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.
103. Young, V. (1986) Some metabolic and nutritional considerations of dietary protein restriction. In: Contemporary Issues in Nephrology: The Progressive Nature of Renal Disease (Mitch, W., ed.), Churchill Livingstone, New York, NY. pp. 263-283.
104. Young, V. H. & Munro, H. N. (1978) N-t-methylhistidine (3-methylhistidine) and muscle protein turnover: an overview. Fed. Proc. 37: 2291-2300.
105. Zamir, O., Hasselgren, P. O., O'Brien, W., Thompson, R. C. & Fischer, J.E. (1992) Muscle protein breakdown during endotoxemia in rats and after treatment with interteukin-1 receptor antagonist (IL-1ra). Ann. Surg. 216: 381-385; discussion 386-387.