Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process

Molecular and Cellular Biology

Volumn 29, Issue 4, 2009, Pages 1095-1106

  Tonoki, Ayako ^a   Kuranaga, Erina ^a,b   Tomioka, Takeyasu ^a   Hamazaki, Jun ^a   Murata, Shigeo ^a   Tanaka, Keiji ^c   Miura, Masayuki ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

19S REGULATORY PARTICLE; 20S PROTEASOME; 26S PROTEASOME; CELL PROTEIN; POLYGLUTAMINE; PROTEASOME; UNCLASSIFIED DRUG;

AGING; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE; GENE IDENTIFICATION; GENE OVEREXPRESSION; LIFESPAN; LOSS OF FUNCTION MUTATION; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; RPN11 GENE; UBIQUITINATION;

AGING; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; LONGEVITY; NERVE DEGENERATION; PEPTIDES; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; SUPPRESSION, GENETIC; UBIQUITINATION;

EID: 59449095881     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01227-08     Document Type: Article

References (43)

1. Bence, N. F., R. M. Sampat, and R. R. Kopito. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-1555.
2. Bonini, N. M. 2002. Chaperoning brain degeneration. Proc. Natl. Acad. Sci. USA 99(Suppl. 4):16407-16411.
3. Chondrogianni, N., and E. S. Gonos. 2005. Proteasome dysfunction in mammalian aging: steps and factors involved. Exp. Gerontol. 40:931-938.
4. Cummings, C. J., E. Reinstein, Y. Sun, B. Antalffy, Y. Jiang, A. Ciechanover, H. T. Orr, A. L. Beaudet, and H. Y. Zoghbi. 1999. Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron 24:879-892.
5. Fernandez-Funez, P., M. L. Nino-Rosales, B. de Gouyon, W. C. She, J. M. Luchak, P. Martinez, E. Turiegano, J. Benito, M. Capovilla, P. J. Skinner, A. McCall, I. Canal, H. T. Orr, H. Y. Zoghbi, and J. Botas. 2000. Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408:101-106.
6. Forster, A., and C. P. Hill. 2003. Proteasome degradation: enter the substrate. Trends Cell Biol. 13:550-553.
7. Fu, H., N. Reis, Y. Lee, M. H. Glickman, and R. D. Vierstra. 2001. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J. 20:7096-7107.
8. Gaczynska, M., P. A. Osmulski, and W. F. Ward. 2001. Caretaker or undertaker? The role of the proteasome in aging. Mech. Ageing Dev. 122:235-254.
9. Gray, D. A., M. Tsirigotis, and J. Woulfe. 2003. Ubiquitin, proteasomes, and the aging brain. Sci. Aging Knowledge Environ. 2003:RE6.
10. Gunawardena, S., L. S. Her, R. G. Brusch, R. A. Laymon, I. R. Niesman, B. Gordesky-Gold, L. Sintasath, N. M. Bonini, and L. S. Goldstein. 2003. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40:25-40.
11. Hamazaki, J., S. Iemura, T. Natsume, H. Yashiroda, K. Tanaka, and S. Murata. 2006. A novel proteasome interacting protein recruits the deubiq-uitinating enzyme UCH37 to 26S proteasomes. EMBO J. 25:4524-4536.
12. Hara, T., K. Nakamura, M. Matsui, A. Yamamoto, Y. Nakahara, R. Suzuki-Migishima, M. Yokoyama, K. Mishima, I. Saito, H. Okano, and N. Mizushima. 2006. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441:885-889.
13. Hsu, A. L., C. T. Murphy, and C. Kenyon. 2003. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300:1142-1145.
14. Imai, J., M. Maruya, H. Yashiroda, I. Yahara, and K. Tanaka. 2003. The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome. EMBO J. 22:3557-3567.
15. Isono, E., N. Saito, N. Kamata, Y. Saeki, and A. Toh-E. 2005. Functional analysis of Rpn6p, a lid component of the 26 S proteasome, using temperature-sensitive rpn6 mutants of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 280:6537-6547.
16. Jackson, G. R., I. Salecker, X. Dong, X. Yao, N. Arnheim, P. W. Faber, M. E. MacDonald, and S. L. Zipursky. 1998. Polyglutamine-expanded human hunting tin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21:633-642.
17. Jana, N. R., E. A. Zemskov, and N. Wang Gh. 2001. Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum. Mol. Genet. 10:1049-1059.
18. Kanuka, H., E. Kuranaga, T. Hiratou, T. Igaki, B. Nelson, H. Okano, and M. Miura. 2003. Cytosol-endoplasmic reticulum interplay by Sec61alpha translocon in polyglutamine-mediated neurotoxicity in Drosophila. Proc. Natl. Acad. Sci. USA 100:11723-11728.
19. Keller, J. N., J. Gee, and Q. Ding. 2002. The proteasome in brain aging. Ageing Res. Rev. 1:279-293.
20. Kennerdell, J. R., and R. W. Carthew. 2000. Heritable gene silencing in Drosophila using double-stranded RNA. Nat. Biotechnol. 18:896-898.
21. Komatsu, M., S. Waguri, T. Chiba, S. Murata, J. Iwata, I. Tanida, T. Ueno, M. Koike, Y. Uchiyama, E. Kominami, and K. Tanaka. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884.
22. Kuranaga, E., H. Kanuka, A. Tonoki, K. Takemoto, T. Tomioka, M. Kobayashi, S. Hayashi, and M. Miura. 2006. Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 126: 583-596.
23. Lashuel, H. A., D. Hartley, B. M. Petre, T. Walz, and P. T. Lansbury, Jr. 2002. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418:291.
24. Leggett, D. S., J. Hanna, A. Borodovsky, B. Crosas, M. Schmidt, R. T. Baker, T. Walz, H. Ploegh, and D. Finley. 2002. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10:495-507.
25. Liu, C. W., X. Li, D. Thompson, K. Wooding, T. L. Chang, Z. Tang, H. Yu, P. J. Thomas, and G. N. DeMartino. 2006. ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol. Cell 24:39-50.
26. Mattson, M. P., and T. Magnus. 2006. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 7:278-294.
27. Mayeux, R. 2003. Epidemiology of neurodegeneration. Annu. Rev. Neurosci. 26:81-104.
28. McGuire, S. E., P. T. Le, A. J. Osborn, K. Matsumoto, and R. L. Davis. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
29. Mizushima, N., B. Levine, A. M. Cuervo, and D. J. Klionsky. 2008. Autophagy fights disease through cellular self-digestion. Nature 451:1069-1075.
30. Morimoto, R. I. 2008. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22:1427-1438.
31. Morley, J. F., H. R. Brignull, J. J. Weyers, and R. I. Morimoto. 2002. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99:10417-10422.
32. Taylor, J. P., J. Hardy, and K. H. Fischbeck. 2002. Toxic proteins in neurodegenerative disease. Science 296:1991-1995.
33. Toba, G., T. Ohsako, N. Miyata, T. Ohtsuka, K. H. Seong, and T. Aigaki. 1999. The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 151: 725-737.
34. Tower, J., G. H. Karpen, N. Craig, and A. C. Spradling. 1993. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics 133:347-359.
35. Verma, R., L. Aravind, R. Oania, W. H. McDonald, J. R. Yates III, E. V. Koonin, and R. J. Deshaies. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298: 611-615.
36. Vernace, V. A., L. Arnaud, T. Schmidt-Glenewinkel, and M. E. Figueiredo-Pereira. 2007. Aging perturbs 26S proteasome assembly in Drosophila melanogaster. FASEB J. 21:2672-2682.
37. Voges, D., P. Zwickl, and W. Baumeister. 1999. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68:1015-1068.
38. Walker, G. A., and G. J. Lithgow. 2003. Lifespan extension in C. elegans by a molecular chaperone dependent upon insulin-like signals. Aging Cell 2:131-139.
39. Warrick, J. M., H. L. Paulson, G. L. Gray-Board, Q. T. Bui, K. H. Fischbeck, R. N. Pittman, and N. M. Bonini. 1998. Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell 93:939-949.
40. Yamazaki, D., J. Horiuchi, Y. Nakagami, S. Nagano, T. Tamura, and M. Saitoe. 2007. The Drosophila DCO mutation suppresses age-related memory impairment without affecting lifespan. Nat. Neurosci. 10:478-484.
41. Yao, T., and R. E. Cohen. 2002. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419:403-407.
42. Yokoyama, K., K. Fukumoto, T. Murakami, S. Harada, R. Hosono, R. Wadhwa, Y. Mitsui, and S. Ohkuma. 2002. Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett. 516:53-57.
43. Yun, C., A. Stanhill, Y. Yang, Y. Zhang, C. M. Haynes, C. F. Xu, T. A. Neubert, A. Mor, M. R. Philips, and D. Ron. 2008. Proteasomal adaptation to environmental stress links resistance to proteotoxicity with longevity in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105:7094-7099.