Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T04:59:12.591Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of ubiquitin–proteasome-dependent proteolysis in the remodelling of skeletal muscle

Published online by Cambridge University Press:  05 March 2007

Daniel Taillandier ,
Lydie Combaret ,
Marie-Noëlle Pouch ,
Susan E. Samuels ,
Daniel Béchet  and
Didier Attaix
Daniel Taillandier
Affiliation:
Human Nutrition Research Centre of Clermont-Ferrand and National Institute of Agricultural Research, Nutrition and Protein Metabolism Unit, 63122 Ceyrat, France
Lydie Combaret
Affiliation:
Human Nutrition Research Centre of Clermont-Ferrand and National Institute of Agricultural Research, Nutrition and Protein Metabolism Unit, 63122 Ceyrat, France
Marie-Noëlle Pouch
Affiliation:
Human Nutrition Research Centre of Clermont-Ferrand and National Institute of Agricultural Research, Nutrition and Protein Metabolism Unit, 63122 Ceyrat, France
Susan E. Samuels
Affiliation:
Human Nutrition Research Centre of Clermont-Ferrand and National Institute of Agricultural Research, Nutrition and Protein Metabolism Unit, 63122 Ceyrat, France
Daniel Béchet
Affiliation:
Human Nutrition Research Centre of Clermont-Ferrand and National Institute of Agricultural Research, Nutrition and Protein Metabolism Unit, 63122 Ceyrat, France
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

In skeletal muscle, as in any mammalian tissue, protein levels are dictated by relative rates of protein synthesis and breakdown. Recent studies have shown that the ubiquitin–proteasome-dependent proteolytic pathway is mainly responsible for the breakdown of myofibrillar proteins. In this pathway proteins that are to be degraded are first tagged with a polyubiquitin degradation signal. Ubiquitination is performed by the ubiquitin-activating enzyme, ubiquitin-conjugating enzymes and ubiquitin–protein ligases, which are responsible for the recognition of specific substrates. Polyubiquitinated protein substrates are then specifically recognised and degraded by the 26S proteasome. The present review focuses on: (1) the mechanisms of ubiquitination–deubiquitination that make the system highly selective; (2) the mechanisms of proteolysis in skeletal muscle. In particular, the role of the system in the remodelling of skeletal muscle during exercise and disuse and in recovery or regeneration that prevails during post-atrophic conditions is reviewed.

Keywords

Muscle activity and disuseExerciseMuscle wastingUbiquitin–proteasome-dependent proteolysis
Type
Symposium 5: Muscle hypertrophy: the signals of insulin, amino acids and exercise
Information
Proceedings of the Nutrition Society , Volume 63 , Issue 2 , May 2004 , pp. 357 - 361
Copyright
Copyright © The Nutrition Society 2004

References

Attaix, D, Combaret, L, Kee, AJ & Taillandier, D (2003) Mechanisms of ubiquitination and proteasome-dependent proteolysis in skeletal muscle. In Molecular Nutrition, pp. 219–235 [Zempleni, J, Daniel, H, editors]. Wallingford, Oxon.: CABI Publishing.Google Scholar
Attaix, D & Taillandier, D (1998) The critical role of the ubiquitin-proteasome pathway in muscle wasting in comparison to lysosomal and Ca2+-dependent systems. In Intracellular Protein Degradation, pp. 235–266 [Bittar, EE, Rivett, AJ, editors]. Greenwich, CT JAI Press Inc.Google Scholar
Bodine, SC, Latres, E, Baumhueter, S, Lai, VK, Nunez, L, Clarke, BA et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704–1708.Google Scholar
Bossola, M, Muscaritoli, M, Costelli, P, Grieco, G, Bonelli, G, Pacelli, F, Fanelli, FR, Doglietto, GB & Baccino, FM (2003) Increased muscle proteasome activity correlates with disease severity in gastric cancer patients. Annals of Surgery 237, 384–389.CrossRefGoogle ScholarPubMed
Combaret, L, Béchet, D, Claustre, A, Taillandier, D, Richard, I & Attaix, D (2003) Down-regulation of genes in the lysosomal and ubiquitin-proteasome proteolytic pathways in calpain-3-deficient muscle. International Journal of Biochemistry and Cell Biology 35, 676–684.Google Scholar
Deval, C, Mordier, S, Obled, C, Béchet, D, Combaret, L, Attaix, D & Ferrara, M (2001) Identification of cathepsin L as a differentially-expressed message associated with skeletal muscle wasting. Biochemical Journal 360, 143–150.Google Scholar
Du, J, Wang, X, Miereles, C, Bailey, JL, Debigare, R, Sheng, B, Price, SR & Mitch, SR (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. Journal of Clinical Investigation 113, 115–123.Google Scholar
Duguez, S, Bihan, MC, Gouttefangeas, D, Feasson, L & Freyssenet, D (2003) Myogenic and nonmyogenic cells differentially express proteinases, Hsc/Hsp70, and BAG-1 during skeletal muscle regeneration. American Journal of Physiology 285, E206–E215.Google Scholar
Feasson, L, Stockholm, D, Freyssenet, D, Richard, I, Duguez, S, Beckmann, JS & Denis, C (2002) Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. Journal of Physiology (London) 543, 297–306.Google Scholar
Glickman, MH & Ciechanover, A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiological Reviews 82, 373–428.Google Scholar
Gomes, MD, Lecker, SH, Jagoe, RT, Navon, A & Goldberg, AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proceedings of the National Academy of Sciences USA 98, 14440–14445.CrossRefGoogle ScholarPubMed
Hasselgren, PO, Wray, C & Mammen, J (2002) Molecular regulation of muscle cachexia: it may be more than the proteasome. Biochemical and Biophysical Research Communications 290, 1–10.Google Scholar
Ikemoto, M, Nikawa, T, Takeda, S, Watanabe, C, Katano, T, Baldwin, KM, Izumi, R, Nonaka, I, Towatari, T, Teshima, S, Rokutan, K & Kishi, K (2001) Space shuttle flight (STS-90) enhances degradation of rat myosin heavy chain in association with activation of ubiquitin-proteasome pathway. FASEB Journal 15, 1279–1281.Google Scholar
Jagoe, RT & Goldberg, AL (2001) What do we really know about the ubiquitin-proteasome pathway in muscle atrophy. Current Opinion in Clinical Nutrition and Metabolic Care 4, 183–190.Google Scholar
Jagoe, RT, Lecker, SH, Gomes, M & Goldberg, AL (2002) Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB Journal 16, 1697–1712.Google Scholar
Kee, AJ, Taylor, AJ, Carlsson, AR, Sevette, A, Smith, RC & Thompson, MW (2002) IGF-I has no effect on postexercise suppression of the ubiquitin-proteasome system in rat skeletal muscle. Journal of Applied Physiology 92, 2277–2284.Google Scholar
Mansoor, O, Beaufrère, B, Boirie, Y, Rallière, C, Taillandier, D, Aurousseau, E, Schoeffler, P, Arnal, M & Attaix, D (1996) Increased mRNA levels for components of the lysosomal, Ca 2+ -activated and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proceedings of the National Academy of Sciences USA 93, 2714–2718.Google Scholar
Ordway, GA, Neufer, PD, Chin, ER & DeMartino, GN (2000) Chronic contractile activity upregulates the proteasome system in rabbit skeletal muscle. Journal of Applied Physiology 88, 1134–1141.Google Scholar
Samuels, SE & Baracos, VE (1995) Tissue protein turnover is altered during catch-up growth following E. coli infection in weanling rats. Journal of Nutrition 125, 520–530.Google Scholar
Solomon, V & Goldberg, AL (1996) Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. Journal of Biological Chemistry 271, 26690–26697.Google Scholar
Stupka, N, Tarnopolsky, MA, Yardley, NJ & Phillips, SM (2001) Cellular adaptation to repeated eccentric exercise-induced muscle damage. Journal of Applied Physiology 91, 1669–1678.CrossRefGoogle ScholarPubMed
Taillandier, D, Aurousseau, E, Combaret, L, Guezennec, CY & Attaix, D (2003) Regulation of proteolysis during reloading of the unweighted soleus muscle. International Journal of Biochemistry and Cell Biology 35, 665–675.CrossRefGoogle ScholarPubMed
Taillandier, D, Aurousseau, E Meynial-Denis, D, Béchet, D, Ferrara, M, Cottin, P, Ducastaing, A, Bigard, X, Guezennec, CY, Schmid, HP & Attaix, D (1996) Coordinate activation of lysosomal, Ca 2+ -activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. Biochemical Journal 316, 65–72.Google Scholar
Thompson, HS & Scordilis, SP (1994) Ubiquitin changes in human biceps muscle following exercise-induced damage. Biochemical and Biophysical Research Communications 204, 1193–1198.Google Scholar
Tilignac, T, Temparis, S, Combaret, L, Taillandier, D, Pouch, MN, Cervek, M, Cardenas, DM Le Bricon, T, Debiton, E, Samuels, SE, Madelmont, JC & Attaix, D (2002a) Chemotherapy inhibits skeletal muscle ubiquitin-proteasome-dependent proteolysis. Cancer Research 62, 2771–2777.Google Scholar
Tilignac, T, Temparis, S, Combaret, L, Taillandier, D, Pouch, MN, Cervek, M, Cardenas, DM Le Bricon, T, Debiton, E, Samuels, SE, Madelmont, JC & Attaix, D (2002b) Chemotherapy inhibits skeletal muscle ubiquitin-proteasome-dependent proteolysis: Erratum. Cancer Research 62, 7133.Google Scholar
Willoughby, DS, Priest, JW & Jennings, RA (2000) Myosin heavy chain isoform and ubiquitin protease mRNA expression after passive leg cycling in persons with spinal cord injury. Archives of Physical Medicine and Rehabilitation 81, 157–163.Google Scholar