The immunoproteasome, the 20S proteasome and the PA28αβ proteasome regulator are oxidative-stress-adaptive proteolytic complexes

Biochemical Journal

Volumn 432, Issue 3, 2010, Pages 585-594

  Pickering, Andrew M ^a,b   Koop, Alison L ^a,b   Teoh, Cheryl Y ^a,b   Ermak, Gennady ^a,b   Grune, Tilman ^c   Davies, Kelvin J A ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Aging; Free radical; Hormesis; Protein degradation; Protein oxidation; Ubiquitin proteasome system

Indexed keywords

AGING; HORMESIS; PROTEIN DEGRADATION; PROTEIN OXIDATION; UBIQUITIN-PROTEASOME SYSTEM;

CELL CULTURE; CELL PROLIFERATION; DEGRADATION; FREE RADICALS; OXIDATION; PLANTS (BOTANY); RNA;

PROTEINS;

20S PROTEASOME; HYDROGEN PEROXIDE; IMMUNOPROTEASOME; PA28ALPHA BETA PROTEASOME; PROTEASOME; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; DNA REPLICATION; DRUG RESISTANCE; EMBRYO CELL; ENZYME ACTIVATION; FIBROBLAST; GENE SILENCING; HORMESIS; MOUSE; MOUSE EMBRYO; MUTANT; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS;

ADAPTATION, PHYSIOLOGICAL; AGING; ANIMALS; CELL LINE; CELL PROLIFERATION; DNA REPLICATION; ENZYME INDUCTION; HUMANS; HYDROGEN PEROXIDE; MICE; OSMOLAR CONCENTRATION; OXIDANTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CARBONYLATION; PROTEINS; RNA, SMALL INTERFERING;

MURINAE;

EID: 78649848069     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100878     Document Type: Article

References (51)

1. Davies, K. J. (1986) Intracellular proteolytic systems may function as secondary antioxidant defenses: an hypothesis. J. Free Radical Biol. Med. 2, 155-173
2. Davies, K. J. and Goldberg, A. L. (1987) Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells. J. Biol. Chem. 262, 8227-8234
3. Pacifici, R. E., Kono, Y. and Davies, K. J. (1993) Hydrophobicity as the signal for selective degradation of hydroxyl radical-modified hemoglobin by the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 268, 15405-15411
4. Grune, T., Reinheckel, T. and Davies, K. J. (1996) Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J. Biol. Chem. 271, 15504-15509
5. Ullrich, O., Reinheckel, T., Sitte, N., Hass, R., Grune, T. and Davies, K. J. (1999) Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc. Natl. Acad. Sci. U.S.A. 96, 6223-6228
6. Davies, K. J. (2001) Degradation of oxidized proteins by the 20S proteasome. Biochimie 83, 301-310 (Pubitemid 32293650)
7. Bota, D. A. and Davies, K. J. (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 4, 674-680
8. Bota, D. A., Ngo, J. K. and Davies, K. J. (2005) Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radical Biol. Med. 38, 665-677
9. Bulteau, A. L., Lundberg, K. C., Ikeda-Saito, M., Isaya, G. and Szweda, L. I. (2005) Reversible redox-dependent modulation of mitochondrial aconitase and proteolytic activity during in vivo cardiac ischemia/reperfusion. Proc. Natl. Acad. Sci. U.S.A. 102, 5987-5991
10. Bulteau, A. L., Szweda, L. I. and Friguet, B. (2006) Mitochondrial protein oxidation and degradation in response to oxidative stress and aging. Exp. Gerontol. 41, 653-657
11. Chondrogianni, N., Stratford, F. L., Trougakos, I. P., Friguet, B., Rivett, A. J. and Gonos, E. S. (2003) Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation. J. Biol. Chem. 278, 28026-28037
12. Fucci, L., Oliver, C. N., Coon, M. J. and Stadtman, E. R. (1983) Inactivation of key metabolic enzymes by mixed-function oxidation reactions: possible implication in protein turnover and ageing. Proc. Natl. Acad. Sci. U.S.A. 80, 1521-1525
13. Keller, J. N., Schmitt, F. A., Scheff, S. W., Ding, Q., Chen, Q., Butterfield, D. A. and Markesbery, W. R. (2005) Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 64, 1152-1156
14. Shang, F. and Taylor, A. (1995) 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
15. Shringarpure, R., Grune, T., Mehlhase, J. and Davies, K. J. (2003) Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J. Biol. Chem. 278, 311-318
16. Whittier, J. E., Xiong, Y., Rechsteiner, M. C. and Squier, T. C. (2004) Hsp90 enhances degradation of oxidized calmodulin by the 20 S proteasome. J. Biol. Chem. 279, 46135-46142
17. Ahn, K., Erlander, M., Leturcq, D., Peterson, P. A., Fruh, K. and Yang, Y. (1996) In vivo characterization of the proteasome regulator PA28. J. Biol. Chem. 271, 18237-18242
18. Coux, O., Tanaka, K. and Goldberg, A. L. (1996) Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65, 801-847
19. Ciechanover, A. (1994) The ubiquitin - proteasome proteolytic pathway. Cell 79, 13-21
20. Tanaka, K. and Kasahara, M. (1998) The MHC class I ligand-generating system: roles of immunoproteasomes and the interferon-γ-inducible proteasome activator PA28. Immunol. Rev. 163, 161-176
21. Fruh, K. and Yang, Y. (1999) Antigen presentation by MHC class I and its regulation by interferon γ. Curr. Opin. Immunol. 11, 76-81
22. Fehling, H. J., Swat, W., Laplace, C., Kuhn, R., Rajewsky, K., Muller, U. and von Boehmer, H. (1994) MHC class I expression in mice lacking the proteasome subunit LMP-7. Science 265, 1234-1237
23. Davies, K. J. (1999) The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress. IUBMB Life 48, 41-47
24. Davies, K. J. (2000) Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50, 279-289
25. Wiese, A. G., Pacifici, R. E. and Davies, K. J. (1995) Transient adaptation of oxidative stress in mammalian cells. Arch. Biochem. Biophys. 318, 231-240
26. Ermak, G., Harris, C. D. and Davies, K. J. (2002) The DSCR1 (Adapt78) isoform 1 protein calcipressin 1 inhibits calcineurin and protects against acute calcium-mediated stress damage, including transient oxidative stress. FASEB J. 16, 814-824
27. Sitte, N., Huber, M., Grune, T., Ladhoff, A., Doecke, W. D., Von Zglinicki, T. and Davies, K. J. (2000) Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J. 14, 1490-1498
28. Sitte, N., Merker, K., Von Zglinicki, T., Davies, K. J. and Grune, T. (2000) Protein oxidation and degradation during cellular senescence of human BJ fibroblasts Part II: aging of nondividing cells. FASEB J. 14, 2503-2510
29. Ferrington, D. A., Husom, A. D. and Thompson, L. V. (2005) Altered proteasome structure, function, and oxidation in aged muscle. FASEB J. 19, 644-646
30. Ferrington, D. A., Hussong, S. A., Roehrich, H., Kapphahn, R. J., Kavanaugh, S. M., Heuss, N. D. and Gregerson, D. S. (2008) Immunoproteasome responds to injury in the retina and brain. J. Neurochem. 106, 158-169
31. Husom, A. D., Peters, E. A., Kolling, E. A., Fugere, N. A., Thompson, L. V. and Ferrington, D. A. (2004) Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 421, 67-76
32. 2-induced transferrin receptor-dependent apoptosis in endothelial cells: role of ubiquitin - proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 100, 10653-10658
33. Thomas, S., Kotamraju, S., Zielonka, J., Harder, D. R. and Kalyanaraman, B. (2007) Hydrogen peroxide induces nitric oxide and proteosome activity in endothelial cells: a bell-shaped signaling response. Free Radical Biol. Med. 42, 1049-1061
34. Kotamraju, S., Matalon, S., Matsunaga, T., Shang, T., Hickman-Davis, J. M. and Kalyanaraman, B. (2006) Upregulation of immunoproteasomes by nitric oxide: potential antioxidative mechanism in endothelial cells. Free Radical Biol. Med. 40, 1034-1044
35. Yamano, T., Murata, S., Shimbara, N., Tanaka, N., Chiba, T., Tanaka, K., Yui, K. and Udono, H. (2002) Two distinct pathways mediated by PA28 and hsp90 in major histocompatibility complex class I antigen processing. J. Exp. Med. 196, 185-196
36. Tanaka, K., Yashiroda, H. and Tanahashi, N. (2006) Preparation of Proteasomes. Cell Biology: a Laboratory Handbook (Celis, J. E., ed.), pp. 91-97, Elsevier, Amsterdam
37. Tanahashi, N., Murakami, Y., Minami, Y., Shimbara, N., Hendil, K. B. and Tanaka, K. (2000) Hybrid proteasomes: induction by interferon-γ and contribution to ATP-dependent proteolysis. J. Biol. Chem. 275, 14336-14345
38. Jentoft, N. and Dearborn, D. G. (1979) Labeling of proteins by reductive methylation using sodium cyanoborohydride. J. Biol. Chem. 254, 4359-4365
39. Muratani, M. and Tansey, W. P. (2003) How the ubiquitin - proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4, 192-201
40. Collins, G. A. and Tansey, W. P. (2006) The proteasome: a utility tool for transcription? Curr. Opin. Genet. Dev. 16, 197-202
41. Lipford, J. R. and Deshaies, R. J. (2003) Diverse roles for ubiquitin-dependent proteolysis in transcriptional activation. Nat. Cell Biol. 5, 845-850
42. Swaffield, J. C., Bromberg, J. F. and Johnston, S. A. (1992) Alterations in a yeast protein resembling HIV Tat-binding protein relieve requirement for an acidic activation domain in GAL4. Nature 357, 698-700
43. Dennis, A. P., Lonard, D. M., Nawaz, Z. and O'Malley, B. W. (2005) Inhibition of the 26S proteasome blocks progesterone receptor-dependent transcription through failed recruitment of RNA polymerase II. J. Steroid Biochem. Mol. Biol. 94, 337-346
44. Lipford, J. R., Smith, G. T., Chi, Y. and Deshaies, R. J. (2005) A putative stimulatory role for activator turnover in gene expression. Nature 438, 113-116 (Pubitemid 41599830)
45. Teoh, C. Y. and Davies, K. J. (2004) Potential roles of protein oxidation and the immunoproteasome in MHC class I antigen presentation: the 'PrOxI' hypothesis. Arch. Biochem. Biophys. 423, 88-96
46. Grune, T., Reinheckel, T., North, J. A., Li, R., Bescos, P. B., Shringarpure, R. and Davies, K. J. (2002) Ezrin turnover and cell shape changes catalyzed by proteasome in oxidatively stressed cells. FASEB J. 16, 1602-1610
47. Reinheckel, T., Sitte, N., Ullrich, O., Kuckelkorn, U., Davies, K. J. and Grune, T. (1998) Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem J. 335, 637-642
48. Medicherla, B. and Goldberg, A. L. (2008) Heat shock and oxygen radicals stimulate ubiquitin-dependent degradation mainly of newly synthesized proteins. J. Cell Biol. 182, 663-673
49. Reinheckel, T., Grune, T. and Davies, K. J. (2000) The measurement of protein degradation in response to oxidative stress. Methods Mol. Biol. 99, 49-60
50. Pacifici, R. E. and Davies, K. J. (1990) Protein degradation as an index of oxidative stress. Methods Enzymol. 186, 485-502 (Pubitemid 20279991)
51. Fagan, J. M., Waxman, L. and Goldberg, A. L. (1986) Red blood cells contain a pathway for the degradation of oxidant-damaged hemoglobin that does not require ATP or ubiquitin. J. Biol. Chem. 261, 5705-5713