Regulation of the 26S proteasome complex during oxidative stress

Science Signaling

Volumn 3, Issue 151, 2010, Pages

  Wang, Xiaorong ^a,b   Yen, James ^a,c   Kaiser, Peter ^a   Huang, Lan ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Zymo Research Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

26S PROTEASOME; CELL PROTEIN; HYDROGEN PEROXIDE; PROTEASOME; PROTEIN ECM29; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE; ECM29 PROTEIN, S CEREVISIAE; OXIDIZING AGENT; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR; YAP1 PROTEIN, S CEREVISIAE;

ANIMAL CELL; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SENSITIVITY ANALYSIS; UBIQUITINATION; CELL STRAIN HEK293; DOSE RESPONSE; DRUG EFFECT; GENETICS; METABOLISM; MUTATION; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; WESTERN BLOTTING;

MAMMALIA;

BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, DRUG; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; MASS SPECTROMETRY; MUTATION; OXIDANTS; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 78649980437     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2001232     Document Type: Article

References (41)

1. A. L. Goldberg, Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899 (2003).
2. D. Voges, P. Zwickl, W. Baumeister, The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015-1068 (1999).
3. C. M. Pickart, R. E. Cohen, Proteasomes and their kin: Proteases in the machine age. Nat. Rev. Mol. Cell Biol. 5, 177-187 (2004).
4. M. Groll, L. Ditzel, J. Lowe, D. Stock, M. Bochtler, H. D. Bartunik, R. Huber, Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386, 463-471 (1997).
5. M. H. Glickman, D. M. Rubin, O. Coux, I. Wefes, G. Pfeifer, Z. Cjeka, W. Baumeister, V. A. Fried, D. Finley, A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615-623 (1998).
6. M. Schmidt, J. Hanna, S. Elsasser, D. Finley, Proteasome-associated proteins: Regulation of a proteolytic machine. Biol. Chem. 386, 725-737 (2005).
7. R. Verma, R. Oania, J. Graumann, R. J. Deshaies, Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118, 99-110 (2004).
8. S. Elsasser, D. Finley, Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 7, 742-749 (2005).
9. R. Verma, L. Aravind, R. Oania, W. H. McDonald, J. R. Yates III, E. V. Koonin, R. J. Deshaies, Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615 (2002).
10. W. Dubiel, G. Pratt, K. Ferrell, M. Rechsteiner, Purification of an 11 S regulator of the multicatalytic protease. J. Biol. Chem. 267, 22369-22377 (1992).
11. C. P. Ma, C. A. Slaughter, G. N. DeMartino, Identification, purification, and characterization of a protein activator (PA28) of the 20 S proteasome (macropain). J. Biol. Chem. 267, 10515-10523 (1992).
12. X. Gao, J. Li, G. Pratt, S. Wilk, M. Rechsteiner, Purification procedures determine the proteasome activation properties of REGg (PA28g). Arch. Biochem. Biophys. 425, 158-164 (2004).
13. V. Ustrell, L. Hoffman, G. Pratt, M. Rechsteiner, PA200, a nuclear proteasome activator involved in DNA repair. EMBO J. 21, 3516-3525 (2002).
14. F. Zhang, Y. Hu, P. Huang, C. A. Toleman, A. J. Paterson, J. E. Kudlow, Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J. Biol. Chem. 282, 22460-22471 (2007).
15. X. Wang, C. Guerrero, P. Kaiser, L. Huang, Proteomics of proteasome complexes and ubiquitinated proteins. Expert Rev. Proteomics 4, 649-665 (2007).
16. A. V. Gomes, C. Zong, R. D. Edmondson, X. Li, E. Stefani, J. Zhang, R. C. Jones, S. Thyparambil, G. W. Wang, X. Qiao, F. Bardag-Gorce, P. Ping, Mapping the murine cardiac 26S proteasome complexes. Circ. Res. 99, 362-371 (2006).
17. T. Jung, T. Grune, The proteasome and its role in the degradation of oxidized proteins. IUBMB Life 60, 743-752 (2008).
18. K. J. Davies, Degradation of oxidized proteins by the 20S proteasome. Biochimie 83, 301-310 (2001).
19. N. Breusing, T. Grune, Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol. Chem. 389, 203-209 (2008).
20. B. Friguet, Oxidized protein degradation and repair in ageing and oxidative stress. FEBS Lett. 580, 2910-2916 (2006).
21. T. Reinheckel, N. Sitte, O. Ullrich, U. Kuckelkorn, K. J. Davies, T. Grune, Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J. 335 (Pt 3), 637-642 (1998).
22. T. Reinheckel, T. Grune, K. J. Davies, The measurement of protein degradation in response to oxidative stress. Methods Mol. Biol. 99, 49-60 (2000).
23. F. Shang, A. Taylor, Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem. J. 307, 297-303 (1995).
24. F. Shang, X. Gong, A. Taylor, Activity of ubiquitin-dependent pathway in response to oxidative stress. Ubiquitin-activating enzyme is transiently up-regulated. J. Biol. Chem. 272, 23086-23093 (1997).
25. X. Wang, C. F. Chen, P. R. Baker, P. L. Chen, P. Kaiser, L. Huang, Mass spectrometric characterization of the affinity-purified human 26S proteasome complex. Biochemistry 46, 3553-3565 (2007).
26. X. Wang, L. Huang, Identifying dynamic interactors of protein complexes by quantitative mass spectrometry. Mol. Cell. Proteomics 7, 46-57 (2008).
27. 2 stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 273, 22480-22489 (1998).
28. C. Tagwerker, K. Flick, M. Cui, C. Guerrero, Y. Dou, B. Auer, P. Baldi, L. Huang, P. Kaiser, A tandem affinity tag for two-step purification under fully denaturing conditions: Application in ubiquitin profiling and protein complex identification combined with in vivo cross-linking. Mol. Cell. Proteomics 5, 737-748 (2006).
29. D. S. Leggett, J. Hanna, A. Borodovsky, B. Crosas, M. Schmidt, R. T. Baker, T. Walz, H. Ploegh, D. Finley, Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10, 495-507 (2002).
30. M. F. Kleijnen, J. Roelofs, S. Park, N. A. Hathaway, M. Glickman, R. W. King, D. Finley, Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat. Struct. Mol. Biol. 14, 1180-1188 (2007).
31. A. Lehmann, A. Niewienda, K. Jechow, K. Janek, C. Enenkel, Ecm29 fulfils quality control functions in proteasome assembly. Mol. Cell 38, 879-888 (2010).
32. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J. 19, 5157-5166 (2000).
33. R. Shringarpure, T. Grune, J. Mehlhase, K. J. Davies, Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J. Biol. Chem. 278, 311-318 (2003).
34. T. Grune, T. Reinheckel, K. J. Davies, Degradation of oxidized proteins in mammalian cells. FASEB J. 11, 526-534 (1997).
35. Y. Inai, M. Nishikimi, Increased degradation of oxidized proteins in yeast defective in 26 S proteasome assembly. Arch. Biochem. Biophys. 404, 279-284 (2002).
36. J. Kurepa, J. A. Smalle, Structure, function and regulation of plant proteasomes. Biochimie 90, 324-335 (2008).
37. V. A. Vernace, L. Arnaud, T. Schmidt-Glenewinkel, M. E. Figueiredo-Pereira, Aging perturbs 26S proteasome assembly in Drosophila melanogaster. FASEB J. 21, 2672-2682 (2007).
38. M. Bajorek, D. Finley, M. H. Glickman, Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr. Biol. 13, 1140-1144 (2003).
39. S. Elsasser, M. Schmidt, D. Finley, Characterization of the proteasome using native gel electrophoresis. Methods Enzymol. 398, 353-363 (2005).
40. L. Fang, X. Wang, K. Yamoah, P. L. Chen, Z. Q. Pan, L. Huang, Characterization of the human COP9 signalosome complex using affinity purification and mass spectrometry. J. Proteome Res. 7, 4914-4925 (2008).
41. Acknowledgments: We thank the members of the Huang and Kaiser laboratories for their help during this study, especially Y. Yang, C. Yu, P. Pan, and K. Flick. We are grateful to S. Elsasser and D. Finley at Harvard Medical School for their help with the proteasome proteolytic activity assay. We thank R. Aphasizhev for his help with the Fujifilm LAS400. Funding: This work was supported by NIH grants (GM-74830, GM-74830AS1, and UCLA U19 seed grant/UCLA-43510 to L.H. and GM-66164 and GM66164AS1 to P.K.). Author contributions: X.W. participated in experimental design, performed the experiments, analyzed the data, generated all of the figures and tables (except for Fig. 4), and contributed to the writing of Materials and Methods; J.Y. performed the experiments for Fig. 4; P.K. and L.H. designed the experiments, analyzed the results, and wrote the manuscript. Competing interests: The authors declare that they have no competing interests.