Reversible 26S proteasome disassembly upon mitochondrial stress

Cell Reports

Volumn 7, Issue 5, 2014, Pages 1371-1380

  Livnat Levanon, Nurit ^a   Kevei, Éva ^b   Kleifeld, Oded ^a,c   Krutauz, Daria ^a   Segref, Alexandra ^b   Rinaldi, Teresa ^d   Erpapazoglou, Zoi ^e   Cohen, Mickael ^e   Reis, Noa ^a   Hoppe, Thorsten ^b   Glickman, MichaelH ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b UNIVERSITY OF COLOGNE   (Germany)

^c MONASH UNIVERSITY   (Australia)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CYSTEINE; PROTEASOME; REACTIVE OXYGEN METABOLITE; UBIQUITIN; 26S PROTEASOME; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL AGING; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DISASSEMBLY; PROTEIN FUNCTION; PROTEIN METABOLISM; BINDING AFFINITY; BINDING SITE; BIOACCUMULATION; CELL ASSAY; CELL FUNCTION; CELL LEVEL; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME METABOLISM; ENZYME REGULATION; MITOCHONDRION; MOLECULAR DYNAMICS; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RESIDUE ANALYSIS; UBIQUITINATION;

EUKARYOTA;

EID: 84902330507     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.030     Document Type: Article

References (57)

1. Altmann K., Westermann B. Role of essential genes in mitochondrial morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell 2005, 16:5410-5417.
2. Ambrosio G., Zweier J.L., Duilio C., Kuppusamy P., Santoro G., Elia P.P., Tritto I., Cirillo P., Condorelli M., Chiariello M., et al. Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J.Biol. Chem. 1993, 268:18532-18541.
3. Bader N., Grune T. Protein oxidation and proteolysis. Biol. Chem. 2006, 387:1351-1355.
4. Bajorek M., Finley D., Glickman M.H. Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr. Biol. 2003, 13:1140-1144.
5. Bardag-Gorce F., Oliva J., Lin A., Li J., French B.A., French S.W. Proteasome inhibitor up regulates liver antioxidative enzymes in rat model of alcoholic liver disease. Exp. Mol. Pathol. 2011, 90:123-130.
6. Beck F., Unverdorben P., Bohn S., Schweitzer A., Pfeifer G., Sakata E., Nickell S., Plitzko J.M., Villa E., Baumeister W., Förster F. Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. USA 2012, 109:14870-14875.
7. Cecarini V., Bonfili L., Cuccioloni M., Mozzicafreddo M., Rossi G., Buizza L., Uberti D., Angeletti M., Eleuteri A.M. Crosstalk between the ubiquitin-proteasome system and autophagy in a human cellular model of Alzheimer's disease. Biochim. Biophys. Acta 2012, 1822:1741-1751.
8. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J.Biol. Chem. 2003, 278:36027-36031.
9. Cohen M.M., Leboucher G.P., Livnat-Levanon N., Glickman M.H., Weissman A.M. Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol. Biol. Cell 2008, 19:2457-2464.
10. Cohen M.M., Amiott E.A., Day A.R., Leboucher G.P., Pryce E.N., Glickman M.H., McCaffery J.M., Shaw J.M., Weissman A.M. Sequential requirements for the GTPase domain of the mitofusin Fzo1 and the ubiquitin ligase SCFMdm30 in mitochondrial outer membrane fusion. J.Cell Sci. 2011, 124:1403-1410.
11. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
12. Davies K.J. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001, 83:301-310.
13. de Moura M.B., dos Santos L.S., Van Houten B. Mitochondrial dysfunction in neurodegenerative diseases and cancer. Environ. Mol. Mutagen. 2010, 51:391-405.
14. Demasi M., Silva G.M., Netto L.E. 20S proteasome from Saccharomyces cerevisiae is responsive to redox modifications and is S-glutathionylated. J.Biol. Chem. 2003, 278:679-685.
15. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
16. Friguet B., Bulteau A.L., Petropoulos I. Mitochondrial protein quality control: implications in ageing. Biotechnol. J. 2008, 3:757-764.
17. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
18. Glickman M.H., Rubin D.M., Coux O., Wefes I., Pfeifer G., Cjeka Z., Baumeister W., Fried V.A., Finley D. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 1998, 94:615-623.
19. Glickman M.H., Rubin D.M., Fried V.A., Finley D. The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell. Biol. 1998, 18:3149-3162.
20. Green D.R., Galluzzi L., Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011, 333:1109-1112.
21. Grune T., Merker K., Sandig G., Davies K.J. Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem. Biophys. Res. Commun. 2003, 305:709-718.
22. Hayes J.D., Flanagan J.U., Jowsey I.R. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 2005, 45:51-88.
23. Heo J.M., Livnat-Levanon N., Taylor E.B., Jones K.T., Dephoure N., Ring J., Xie J., Brodsky J.L., Madeo F., Gygi S.P., et al. A stress-responsive system for mitochondrial protein degradation. Mol. Cell 2010, 40:465-480.
24. Kosower N.S., Kosower E.M. Diamide: an oxidant probe for thiols. Methods Enzymol. 1995, 251:123-133.
25. Kruegel U., Robison B., Dange T., Kahlert G., Delaney J.R., Kotireddy S., Tsuchiya M., Tsuchiyama S., Murakami C.J., Schleit J., et al. Elevated proteasome capacity extends replicative lifespan in Saccharomyces cerevisiae. PLoS Genet. 2011, 7:e1002253.
26. Layfield R., Alban A., Mayer R.J., Lowe J. The ubiquitin protein catabolic disorders. Neuropathol. Appl. Neurobiol. 2001, 27:171-179.
27. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
28. Livnat-Levanon N., Glickman M.H. Ubiquitin-proteasome system and mitochondria - reciprocity. Biochim. Biophys. Acta 2011, 1809:80-87.
29. Manalo D.J., Lin Z., Liu A.Y. Redox-dependent regulation of the conformation and function of human heat shock factor 1. Biochemistry 2002, 41:2580-2588.
30. Matiuhin Y., Kirkpatrick D.S., Ziv I., Kim W., Dakshinamurthy A., Kleifeld O., Gygi S.P., Reis N., Glickman M.H. Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome. Mol. Cell 2008, 32:415-425.
31. Merz S., Westermann B. Genome-wide deletion mutant analysis reveals genes required for respiratory growth, mitochondrial genome maintenance and mitochondrial protein synthesis in Saccharomyces cerevisiae. Genome Biol. 2009, 10:R95.
32. Mukhopadhyay D., Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315:201-205.
33. Okamoto K., Shaw J.M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 2005, 39:503-536.
34. Orlowski M., Wilk S. Ubiquitin-independent proteolytic functions of the proteasome. Arch. Biochem. Biophys. 2003, 415:1-5.
35. Page M.M., Robb E.L., Salway K.D., Stuart J.A. Mitochondrial redox metabolism: aging, longevity and dietary effects. Mech. Ageing Dev. 2010, 131:242-252.
36. Rambold A.S., Kostelecky B., Lippincott-Schwartz J. Together we are stronger: fusion protects mitochondria from autophagosomal degradation. Autophagy 2011, 7:1568-1569.
37. Reinheckel T., Sitte N., Ullrich O., Kuckelkorn U., Davies K.J., Grune T. Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J. 1998, 335:637-642.
38. Rinaldi T., Ricordy R., Bolotin-Fukuhara M., Frontali L. Mitochondrial effects of the pleiotropic proteasomal mutation mpr1/rpn11: uncoupling from cell cycle defects in extragenic revertants. Gene 2002, 286:43-51.
39. Ross C.A., Pickart C.M. The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol. 2004, 14:703-711.
40. Rubin D.M., Glickman M.H., Larsen C.N., Dhruvakumar S., Finley D. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 1998, 17:4909-4919.
41. Scandalios J.G. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz. J. Med. Biol. Res. 2005, 38:995-1014.
42. Sedensky M.M., Morgan P.G. Mitochondrial respiration and reactive oxygen species in mitochondrial aging mutants. Exp. Gerontol. 2006, 41:237-245.
43. Segref A., Torres S., Hoppe T. A screenable invivo assay to study proteostasis networks in Caenorhabditis elegans. Genetics 2011, 187:1235-1240.
44. Segref A., Kevei É., Pokrzywa W., Schmeisser K., Mansfeld J., Livnat-Levanon N., Ensenauer R., Glickman M.H., Ristow M., Hoppe T. Pathogenesis of human mitochondrial diseases is modulated by reduced activity of the ubiquitin/proteasome system. Cell Metab. 2014, 19:642-652.
45. Sheridan C., Martin S.J. Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion 2010, 10:640-648.
46. Shringarpure R., Grune T., Davies K.J. Protein oxidation and 20S proteasome-dependent proteolysis in mammalian cells. Cell. Mol. Life Sci. 2001, 58:1442-1450.
47. Shringarpure R., Grune T., Mehlhase J., Davies K.J. Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J.Biol. Chem. 2003, 278:311-318.
48. Silva G.M., Netto L.E., Simoes V., Santos L.F., Gozzo F.C., Demasi M.A., Oliveira C.L., Bicev R.N., Klitzke C.F., Sogayar M.C., Demasi M. Redox control of 20S proteasome gating. Antioxid. Redox Signal. 2012, 16:1183-1194.
49. Sitte N., Merker K., Grune T. Proteasome-dependent degradation of oxidized proteins in MRC-5 fibroblasts. FEBS Lett. 1998, 440:399-402.
50. Taylor E.B., Rutter J. Mitochondrial quality control by the ubiquitin-proteasome system. Biochem. Soc. Trans. 2011, 39:1509-1513.
51. Tonoki A., Kuranaga E., Tomioka T., Hamazaki J., Murata S., Tanaka K., Miura M. Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol. Cell. Biol. 2009, 29:1095-1106.
52. Tsvetkov P., Myers N., Moscovitz O., Sharon M., Prilusky J., Shaul Y. Thermo-resistant intrinsically disordered proteins are efficient 20S proteasome substrates. Mol. Biosyst. 2012, 8:368-373.
53. Turrens J.F. Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 1997, 17:3-8.
54. Vendelbo M.H., Nair K.S. Mitochondrial longevity pathways. Biochim. Biophys. Acta 2011, 1813:634-644.
55. Wang X., Yen J., Kaiser P., Huang L. Regulation of the 26S proteasome complex during oxidative stress. Sci. Signal. 2010, 3:ra88.
56. Yao T.P. The role of ubiquitin in autophagy-dependent protein aggregate processing. Genes Cancer 2010, 1:779-786.
57. Ziv I., Matiuhin Y., Kirkpatrick D.S., Erpapazoglou Z., Leon S., Pantazopoulou M., Kim W., Gygi S.P., Haguenauer-Tsapis R., Reis N., et al. A perturbed ubiquitin landscape distinguishes between ubiquitin in trafficking and in proteolysis. Mol. Cell Proteomics 2011, 10. M111.009753.