Proteasome dysfunction induces muscle growth defects and protein aggregation

Journal of Cell Science

Volumn 127, Issue 24, 2014, Pages 5204-5217

  Kitajima, Yasuo ^a,b   Tashiro, Yoshitaka ^c   Suzuki, Naoki ^a,c,f   Warita, Hitoshi ^a   Kato, Masaaki ^a   Tateyama, Maki ^a   Ando, Risa ^a   Izumi, Rumiko ^a   Yamazaki, Maya ^d   Abe, Manabu ^d   Sakimura, Kenji ^d   Ito, Hidefumi ^e   Urushitani, Makoto ^c   Nagatomi, Ryoichi ^b   Takahashi, Ryosuke ^c   Aoki, Masashi ^a  

^a TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

^e WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^f Harvard University   (United States)

Author keywords

Autophagy; Muscle atrophy; Proteasome; Skeletal muscle

Indexed keywords

PROTEASOME; UBIQUITIN; DNA BINDING PROTEIN; DYSTROPHIN; PROTEASOME INHIBITOR; PROTEIN AGGREGATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; GENE; GENE DELETION; KYPHOSIS; MOUSE; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MUSCLE INJURY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN DEGRADATION; RPT3 GENE; SARCOMERE; SKELETAL MUSCLE; UPREGULATION; ANIMAL; BIOMECHANICS; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSCRIPTION; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA; MUS;

ANIMALS; AUTOPHAGY; BIOMECHANICAL PHENOMENA; DNA-BINDING PROTEINS; DYSTROPHIN; IMMUNOHISTOCHEMISTRY; MICE, KNOCKOUT; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN AGGREGATES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UBIQUITIN;

EID: 84918551446     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.150961     Document Type: Article

References (53)

1. Augusto, V., Padovani, C. R. and Campos, G. E. R. (2004). Skeletal muscle fiber types in C57BL6J mice. Braz. J. Morphol. Sci. 21, 89-94.
2. Bedford, L., Hay, D., Devoy, A., Paine, S., Powe, D. G., Seth, R., Gray, T., Topham, I., Fone, K., Rezvani, N. et al. (2008). Depletion of 26S proteasomes in mouse brain neurons causes neurodegeneration and Lewy-like inclusions resembling human pale bodies. J. Neurosci. 28, 8189-8198.
3. Bonaldo, P. and Sandri, M. (2013). Cellular and molecular mechanisms of muscle atrophy. Dis. Model. Mech. 6, 25-39.
4. Bonuccelli, G., Sotgia, F., Schubert, W., Park, D. S., Frank, P. G., Woodman, S. E., Insabato, L., Cammer, M., Minetti, C. and Lisanti, M. P. (2003). Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and membrane localization of dystrophin and dystrophin-associated proteins. Am. J. Pathol. 163, 1663-1675.
5. Bose, J. K., Huang, C. C. and Shen, C. K. (2011). Regulation of autophagy by neuropathological protein TDP-43. J. Biol. Chem. 286, 44441-44448.
6. Bothe, G. W., Haspel, J. A., Smith, C. L., Wiener, H. H. and Burden, S. J. (2000). Selective expression of Cre recombinase in skeletal muscle fibers. Genesis 26, 165-166.
7. Braun, T. and Gautel, M. (2011). Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat. Rev. Mol. Cell Biol. 12, 349-361.
8. Cai, D., Frantz, J. D., Tawa, N. E., Jr, Melendez, P. A., Oh, B. C., Lidov, H. G., Hasselgren, P. O., Frontera, W. R., Lee, J., Glass, D. J. et al. (2004). IKKbeta/ NF-kappaB activation causes severe muscle wasting in mice. Cell 119, 285- 298.
9. Carmignac, V., Quéré, R. and Durbeej, M. (2011). Proteasome inhibition improves the muscle of laminin a2 chain-deficient mice. Hum. Mol. Genet. 20, 541-552.
10. Demontis, F. and Perrimon, N. (2010). FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143, 813-825.
11. Ding, W. X., Ni, H. M., Gao, W., Yoshimori, T., Stolz, D. B., Ron, D. and Yin, X. M. (2007). Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 171, 513-524.
12. Ferrer, I., Carmona, M., Blanco, R., Moreno, D., Torrejón-Escribano, B. and Olivé, M. (2005). Involvement of clusterin and the aggresome in abnormal protein deposits in myofibrillar myopathies and inclusion body myositis. Brain Pathol. 15, 101-108.
13. Fiesel, F. C. and Kahle, P. J. (2011). TDP-43 and FUS/TLS: cellular functions and implications for neurodegeneration. FEBS J. 278, 3550-3568.
14. Fratta, P., Engel, W. K., McFerrin, J., Davies, K. J., Lin, S. W. and Askanas, V. (2005). Proteasome inhibition and aggresome formation in sporadic inclusionbody myositis and in amyloid-beta precursor protein-overexpressing cultured human muscle fibers. Am. J. Pathol. 167, 517-526.
15. Glass, D. J. (2010). Signaling pathways perturbing muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 13, 225-229.
16. Grumati, P., Coletto, L., Sabatelli, P., Cescon, M., Angelin, A., Bertaggia, E., Blaauw, B., Urciuolo, A., Tiepolo, T., Merlini, L. et al. (2010). Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat. Med. 16, 1313-1320.
17. Haas, K. F., Woodruff, E., 3rd and Broadie, K. (2007). Proteasome function is required to maintain muscle cellular architecture. Biol. Cell 99, 615-626.
18. Jagoe, R. T. and Goldberg, A. L. (2001). What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr. Opin. Clin. Nutr. Metab. Care 4, 183-190.
19. Kaneko, T., Hamazaki, J., Iemura, S., Sasaki, K., Furuyama, K., Natsume, T., Tanaka, K. and Murata, S. (2009). Assembly pathway of the Mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137, 914-925.
20. Kessler, B. M., Tortorella, D., Altun, M., Kisselev, A. F., Fiebiger, E., Hekking, B. G., Ploegh, H. L. and Overkleeft, H. S. (2001). Extended peptide-based inhibitors efficiently target the proteasome and reveal overlapping specificities of the catalytic beta-subunits. Chem. Biol. 8, 913-929.
21. Komatsu, M., Waguri, S., Koike, M., Sou, Y. S., Ueno, T., Hara, T., Mizushima, N., Iwata, J., Ezaki, J., Murata, S. et al. (2007). Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149-1163.
22. Kuma, A. and Mizushima, N. (2010). Physiological role of autophagy as an intracellular recycling system: with an emphasis on nutrient metabolism. Semin. Cell Dev. Biol. 21, 683-690.
23. Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S. R., Mitch, W. E. and Goldberg, A. L. (2004). Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39-51.
24. Lee, D. H. and Goldberg, A. L. (1998). Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403.
25. Lee, J. Y., Hopkinson, N. S. and Kemp, P. R. (2011). Myostatin induces autophagy in skeletal muscle in vitro. Biochem. Biophys. Res. Commun. 415, 632-636.
26. Li, H., Chen, Q., Liu, F., Zhang, X., Li, W., Liu, S., Zhao, Y., Gong, Y. and Yan, C. (2013). Unfolded protein response and activated degradative pathways regulation in GNE myopathy. PLoS ONE 8, e58116.
27. Lyons, G. E., Ontell, M., Cox, R., Sassoon, D. and Buckingham, M. (1990). The expression of myosin genes in developing skeletal muscle in the mouse embryo. J. Cell Biol. 111, 1465-1476.
28. Marx, F. P., Soehn, A. S., Berg, D., Melle, C., Schiesling, C., Lang, M., Kautzmann, S., Strauss, K. M., Franck, T., Engelender, S. et al. (2007). The proteasomal subunit S6 ATPase is a novel synphilin-1 interacting protein- implications for Parkinson's disease. FASEB J. 21, 1759-1767.
29. Masiero, E., Agatea, L., Mammucari, C., Blaauw, B., Loro, E., Komatsu, M., Metzger, D., Reggiani, C., Schiaffino, S. and Sandri, M. (2009). Autophagy is required to maintain muscle mass. Cell Metab. 10, 507-515.
30. McPherron, A. C., Lawler, A. M. and Lee, S. J. (1999). Regulation of anterior/ posterior patterning of the axial skeleton by growth/differentiation factor 11. Nat. Genet. 22, 260-264.
31. Miniou, P., Tiziano, D., Frugier, T., Roblot, N., Le Meur, M. and Melki, J. (1999). Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Res. 27, e27-e30.
32. Mizushima, N., Yoshimori, T. and Levine, B. (2010). Methods in mammalian autophagy research. Cell 140, 313-326.
33. Mourkioti, F., Slonimsky, E., Huth, M., Berno, V. and Rosenthal, N. (2008). Analysis of CRE-mediated recombination driven by myosin light chain 1/3 regulatory elements in embryonic and adult skeletal muscle: a tool to study fiber specification. Genesis 46, 424-430.
34. Nishino, I., Fu, J., Tanji, K., Yamada, T., Shimojo, S., Koori, T., Mora, M., Riggs, J. E., Oh, S. J., Koga, Y. et al. (2000). Primary LAMP-2 deficiency causes Xlinked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 406, 906-910.
35. Nogalska, A., Terracciano, C., D'Agostino, C., King Engel, W. and Askanas, V. (2009). p62/SQSTM1 is overexpressed and prominently accumulated in inclusions of sporadic inclusion-body myositis muscle fibers, and can help differentiating it from polymyositis and dermatomyositis. Acta Neuropathol. 118, 407-413.
36. Raben, N., Hill, V., Shea, L., Takikita, S., Baum, R., Mizushima, N., Ralston, E. and Plotz, P. (2008). Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease. Hum. Mol. Genet. 17, 3897-3908.
37. Ramachandran, N., Munteanu, I., Wang, P., Ruggieri, A., Rilstone, J. J., Israelian, N., Naranian, T., Paroutis, P., Guo, R., Ren, Z. P. et al. (2013). VMA21 deficiency prevents vacuolar ATPase assembly and causes autophagic vacuolar myopathy. Acta Neuropathol. 125, 439-457.
38. Sakao, Y., Kawai, T., Takeuchi, O., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Takeda, K. and Akira, S. (2000). Mouse proteasomal ATPases Psmc3 and Psmc4: genomic organization and gene targeting. Genomics 67, 1-7.
39. Salajegheh, M., Pinkus, J. L., Taylor, J. P., Amato, A. A., Nazareno, R., Baloh, R. H. and Greenberg, S. A. (2009). Sarcoplasmic redistribution of nuclear TDP- 43 in inclusion body myositis. Muscle Nerve 40, 19-31.
40. Salminen, A. and Kaarniranta, K. (2009). Regulation of the aging process by autophagy. Trends Mol. Med. 15, 217-224.
41. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H. and Goldberg, A. L. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412.
42. Stitt, T. N., Drujan, D., Clarke, B. A., Panaro, F., Timofeyva, Y., Kline, W. O., Gonzalez, M., Yancopoulos, G. D. and Glass, D. J. (2004). The IGF-1/PI3K/ Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14, 395-403.
43. Suzuki, N., Motohashi, N., Uezumi, A., Fukada, S., Yoshimura, T., Itoyama, Y., Aoki, M., Miyagoe-Suzuki, Y. and Takeda, S. (2007). NO production results in suspension-induced muscle atrophy through dislocation of neuronal NOS. J. Clin. Invest. 117, 2468-2476.
44. Tashiro, Y., Urushitani, M., Inoue, H., Koike, M., Uchiyama, Y., Komatsu, M., Tanaka, K., Yamazaki, M., Abe, M., Misawa, H. et al. (2012). Motor neuronspecific disruption of proteasomes, but not autophagy, replicates amyotrophic lateral sclerosis. J. Biol. Chem. 287, 42984-42994.
45. Todde, V., Veenhuis, M. and van der Klei, I. J. (2009). Autophagy: principles and significance in health and disease. Biochim. Biophys. Acta 1792, 3-13.
46. Tresse, E., Salomons, F. A., Vesa, J., Bott, L. C., Kimonis, V., Yao, T. P., Dantuma, N. P. and Taylor, J. P. (2010). VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy 6, 217-227.
47. van Eersel, J., Ke, Y. D., Gladbach, A., Bi, M., Götz, J., Kril, J. J. and Ittner, L. M. (2011). Cytoplasmic accumulation and aggregation of TDP-43 upon proteasome inhibition in cultured neurons. PLoS ONE 6, e22850.
48. Vellas, B., Pahor, M., Manini, T., Rooks, D., Guralnik, J. M., Morley, J., Studenski, S., Evans, W., Asbrand, C., Fariello, R. et al. (2013). Designing pharmaceutical trials for sarcopenia in frail older adults: EU/US Task Force recommendations. J. Nutr. Health Aging 17, 612-618.
49. Watts, G. D., Wymer, J., Kovach, M. J., Mehta, S. G., Mumm, S., Darvish, D., Pestronk, A., Whyte, M. P. and Kimonis, V. E. (2004). Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36, 377-381.
50. Weihl, C. C. and Pestronk, A. (2010). Sporadic inclusion body myositis: possible pathogenesis inferred from biomarkers. Curr. Opin. Neurol. 23, 482- 488.
51. Winder, S. J., Lipscomb, L., Angela Parkin, C. and Juusola, M. (2011). The proteasomal inhibitor MG132 prevents muscular dystrophy in zebrafish. PLoS Curr. 3, RRN1286.
52. Yamashita, S., Kimura, E., Tawara, N., Sakaguchi, H., Nakama, T., Maeda, Y., Hirano, T., Uchino, M. and Ando, Y. (2013). Optineurin is potentially associated with TDP-43 and involved in the pathogenesis of inclusion body myositis. Neuropathol. Appl. Neurobiol. 39, 406-416.
53. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H. and Goldberg, A. L. (2007). FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6, 472-483.