Muscle hypertrophy is associated with increases in proteasome activity that is independent of MuRF1 and MAFbx expression

Frontiers in Physiology

Volumn 5 FEB, Issue , 2014, Pages

  Baehr, Leslie M ^a   Tunzi, Matthew ^b   Bodine, Sue C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Forkhead transcription factors; Functional overload; Protein degradation; Puromycin; Ubiquitin proteasome system

Indexed keywords

ATROGIN 1; MESSENGER RNA; MUSCLE RING FINGER 1 PROTEIN; PROTEASOME; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; UBIQUITIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION REGULATION; GENE LOSS; MAFBX GENE; MALE; MOUSE; MURF1 GENE; MUSCLE GROWTH; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; PLANTARIS MUSCLE; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; WILD TYPE;

EID: 84895488953     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00069     Document Type: Article

References (46)

1. Adams, V., Mangner, N., Gasch, A., Krohne, C., Gielen, S., Hirner, S., et al. (2008). Induction of MuRF1 is essential for TNF-alpha-induced loss of muscle function in mice. J. Mol. Biol. 384, 48-59. doi: 10.1016/j.jmb.2008.08.087.
2. Auclair, D., Garrel, D. R., Chaouki Zerouala, A., and Ferland, L. H. (1997). Activation of the ubiquitin pathway in rat skeletal muscle by catabolic doses of glucocorticoids. Am. J. Physiol. 272, C1007-C1016.
3. Baar, K., Nader, G., and Bodine, S. (2006). Resistance exercise, muscle loading/unloading and the control of muscle mass. Essays Biochem. 42, 61-74. doi: 10.1042/bse0420061.
4. Baehr, L. M., Furlow, J. D., and Bodine, S. C. (2011). Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids. J. Physiol. 589, 4759-4776. doi: 10.1113/jphysiol.2011.212845.
5. Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K.-M., Nunez, L., Clarke, B. A., et al. (2001a). Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708. doi: 10.1126/science.1065874.
6. Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., et al. (2001b). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014-1019. doi: 10.1038/ncb1101-1014.
7. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K., et al. (1989). A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583. doi: 10.1126/science.2538923.
8. Cohen, S., Brault, J. J., Gygi, S. P., Glass, D. J., Valenzuela, D. M., Gartner, C., et al. (2009). During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J. Cell Biol. 185, 1083-1095. doi: 10.1083/jcb.200901052.
9. Du, J., Wang, X., Miereles, C., Bailey, J. L., Debigare, R., Zheng, B., et al. (2004). Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J. Clin. Invest. 113, 115-123. doi: 10.1172/JCI18330.
10. Fu, H. Y., Minamino, T., Tsukamoto, O., Sawada, T., Asai, M., Kato, H., et al. (2008). Overexpression of endoplasmic reticulum-resident chaperone attenuates cardiomyocyte death induced by proteasome inhibition. Cardiovasc. Res. 79, 600-610. doi: 10.1093/cvr/cvn128.
11. Gomes, A. V., Waddell, D. S., Siu, R., Stein, M., Dewey, S., Furlow, J. D., et al. (2012). Upregulation of proteasome activity in muscle RING finger 1-null mice following denervation. FASEB J. 26, 2986-2999. doi: 10.1096/fj.12-204495.
12. Gomes, M. D., Lecker, S. H., Jagoe, R. T., Navon, A., and Goldberg, A. L. (2001). Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc. Natl. Acad. Sci. U.S.A. 98, 14440-14445. doi: 10.1073/pnas.251541198.
13. Goodman, C. A., Frey, J. W., Mabrey, D. M., Jacobs, B. L., Lincoln, H. C., You, J. S., et al. (2011a). The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J. Physiol. 589, 5485-5501. doi: 10.1113/jphysiol.2011.218255.
14. Goodman, C. A., Mabrey, D. M., Frey, J. W., Miu, M. H., Schmidt, E. K., Pierre, P., et al. (2011b). Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J. 25, 1028-1039. doi: 10.1096/fj.10-168799.
15. Hobler, S. C., Williams, A., Fischer, D., Wang, J. J., Sun, X., Fischer, J. E., et al. (1999). Activity and expression of the 20S proteasome are increased in skeletal muscle during sepsis. Am. J. Physiol. 277, R434-R440.
16. Huey, K. A., Mccall, G. E., Zhong, H., and Roy, R. R. (2007). Modulation of HSP25 and TNF-α during the early stages of functional overload of a rat slow and fast muscle. J. Appl. Physiol. 102, 2307-2314. doi: 10.1152/japplphysiol.00021.2007.
17. Hwee, D. T., Baehr, L. M., Philp, A., Baar, K., and Bodine, S. C. (2013). Maintenance of muscle mass and load-induced growth in Muscle RING Finger 1 null mice with age. Aging Cell. 1, 92-101. doi: 10.1111/acel.12150.
18. Ishido, M., Kami, K., and Masuhara, M. (2004). Localization of MyoD, myogenin and cell cycle regulatory factors in hypertrophying rat skeletal muscles. Acta Physiol. Scand. 180, 281-289. doi: 10.1046/j.0001-6772.2003.01238.x.
19. Jogo, M., Shiraishi, S., and Tamura, T. A. (2009). Identification of MAFbx as a myogenin-engaged F-box protein in SCF ubiquitin ligase. FEBS Lett. 583, 2715-2719. doi: 10.1016/j.febslet.2009.07.033.
20. Koyama, S., Hata, S., Witt, C. C., Ono, Y., Lerche, S., Ojima, K., et al. (2008). Muscle RING-finger protein-1 (MuRF1) as a connector of muscle energy metabolism and protein synthesis. J. Mol. Biol. 376, 1224-1236. doi: 10.1016/j.jmb.2007.11.049.
21. Kubica, N., Crispino, J. L., Gallagher, J. W., Kimball, S. R., and Jefferson, L. S. (2008). Activation of the mammalian target of rapamycin complex 1 is both necessary and sufficient to stimulate eukaryotic initiation factor 2B[var epsilon] mRNA translation and protein synthesis. Int. J. Biochem. Cell Biol. 40, 2522-2533. doi: 10.1016/j.biocel.2008.04.010.
22. Labeit, S., Kohl, C. H., Witt, C. C., Labeit, D., Jung, J., and Granzier, H. (2010). Modulation of muscle atrophy, fatigue and MLC phosphorylation by MuRF1 as indicated by hindlimb suspension studies on MuRF1-KO mice. J. Biomed. Biotechnol. 2010:693741. doi: 10.1155/2010/693741.
23. Lagirand-Cantaloube, J., Offner, N., Csibi, A., Leibovitch, M. P., Batonnet-Pichon, S., Tintignac, L. A., et al. (2008). The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J. 27, 1266-1276. doi: 10.1038/emboj.2008.52.
24. Lang, S. M., Kazi, A. A., Hong-Brown, L., and Lang, C. H. (2012). Delayed recovery of skeletal muscle mass following hindlimb immobilization in mTOR heterozygous mice. PLoS ONE 7:e38910. doi: 10.1371/journal.pone.0038910.
25. Li, Y.-P., Chen, Y., John, J., Moylan, J., Jin, B., Mann, D. L., et al. (2005). TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 19, 362-370. doi: 10.1096/fj.04-2364com.
26. Lokireddy, S., McFarlane, C., Ge, X., Zhang, H., Sze, S. K., Sharma, M., et al. (2011a). Myostatin induces degradation of sarcomeric proteins through a Smad3 signaling mechanism during skeletal muscle wasting. Mol. Endocrinol. 25, 1936-1949. doi: 10.1210/me.2011-1124.
27. Lokireddy, S., Mouly, V., Butler-Browne, G., Gluckman, P. D., Sharma, M., Kambadur, R., et al. (2011b). Myostatin promotes the wasting of human myoblast cultures through promoting ubiquitin-proteasome pathway-mediated loss of sarcomeric proteins. Am. J. Physiol.Cell Physiol. 301, C1316-C1324. doi: 10.1152/ajpcell.00114.2011.
28. Louis, E., Raue, U., Yang, Y., Jemiolo, B., and Trappe, S. (2007). Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 103, 1744-1751. doi: 10.1152/japplphysiol.00679.2007.
29. Marino, J. S., Tausch, B. J., Dearth, C. L., Manacci, M. V., Mcloughlin, T. J., Rakyta, S. J., et al. (2008). β2-Integrins contribute to skeletal muscle hypertrophy in mice. Am. J. Physiol. Cell Physiol. 295, C1026-C1036. doi: 10.1152/ajpcell.212.2008.
30. Minetti, G. C., Feige, J. N., Rosenstiel, A., Bombard, F., Meier, V., Werner, A., et al. (2011). Galphai2 signaling promotes skeletal muscle hypertrophy, myoblast differentiation, and muscle regeneration. Sci. Signal. 4, ra80. doi: 10.1126/scisignal.2002038.
31. 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. doi: 10.1056/NEJM199612193352507.
32. Miyazaki, M., McCarthy, J. J., Fedele, M. J., and Esser, K. A. (2011). Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling. J. Physiol. 589, 1831-1846. doi: 10.1113/jphysiol.2011.205658.
33. Murton, A. J., Constantin, D., and Greenhaff, P. L. (2008). The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim. Biophys. Acta 1782, 730-743. doi: 10.1016/j.bbadis.2008.10.011.
34. Phillips, S. M., Tipton, K. D., Aarsland, A., Wolf, S. E., and Wolfe, R. R. (1997). Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am. J. Physiol. 273, E99-E107.
35. Rayavarapu, S., Coley, W., and Nagaraju, K. (2012). Endoplasmic reticulum stress in skeletal muscle homeostasis and disease. Curr. Rheumatol. Rep. 14, 238-243. doi: 10.1007/s11926-012-0247-5.
36. Rock, K. L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., et al. (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771. doi: 10.1016/S0092-8674(94)90462-6.
37. Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., et al. (2001). Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3, 1009-1013. doi: 10.1038/ncb1101-1009.
38. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., et al. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412. doi: 10.1016/S0092-8674(04)00400-3.
39. Sartori, R., Schirwis, E., Blaauw, B., Bortolanza, S., Zhao, J., Enzo, E., et al. (2013). BMP signaling controls muscle mass. Nat. Genet. 11, 1309-1318. doi: 10.1038/ng.2772.
40. Schmidt, E. K., Clavarino, G., Ceppi, M., and Pierre, P. (2009). SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods 6, 275-277. doi: 10.1038/nmeth.1314.
41. Tintignac, L. A., Lagirand, J., Batonnet, S., Sirri, V., Leibovitch, M. P., and Leibovitch, S. A. (2005). Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J. Biol. Chem. 280, 2847-2856. doi: 10.1074/jbc.M411346200.
42. Tisdale, M. J. (2005). The ubiquitin-proteasome pathway as a therapeutic target for muscle wasting. J. Support. Oncol. 3, 209-217.
43. Vary, T. C., Frost, R. A., and Lang, C. H. (2008). Acute alcohol intoxication increases atrogin-1 and MuRF1 mRNA without increasing proteolysis in skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1777-R1789. doi: 10.1152/ajpregu.00056.2008.
44. Waddell, D. S., Baehr, L. M., Van Den Brandt, J., Johnsen, S. A., Reichardt, H. M., Furlow, J. D., et al. (2008). The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am. J. Physiol. Endocrinol. Metab. 295, E785-E797. doi: 10.1152/ajpendo.00646.2007.
45. Yang, Y., Jemiolo, B., and Trappe, S. (2006). Proteolytic mRNA expression in response to acute resistance exercise in human single skeletal muscle fibers. J. Appl. Physiol. 101, 1442-1450. doi: 10.1152/japplphysiol.00438.2006.
46. Zanchi, N. E., De Siqueira Filho, M. A., Lira, F. S., Rosa, J. C., Yamashita, A. S., De Oliveira Carvalho, C. R., et al. (2009). Chronic resistance training decreases MuRF-1 and Atrogin-1 gene expression but does not modify Akt, GSK-3beta and p70S6K levels in rats. Eur. J. Appl. Physiol. 106, 415-423. doi: 10.1007/s00421-009-1033-6.