E6-AP association promotes SOD1 aggresomes degradation and suppresses toxicity

Neurobiology of Aging

Volumn 34, Issue 4, 2013, Pages 1310.e11-1310.e23

  Mishra, Amit ^a   Maheshwari, Megha ^b   Chhangani, Deepak ^a   Fujimori Tonou, Noriko ^c   Endo, Fumito ^c,d   Joshi, Ajay Prakash ^a   Jana, Nihar Ranjan ^b   Yamanaka, Koji ^c,e,f,g  

^a INDIAN INSTITUTE OF TECHNOLOGY JODHPUR   (India)

^b NATIONAL BRAIN RESEARCH CENTRE   (India)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f SAITAMA UNIVERSITY   (Japan)

^g KYOTO UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Cytotoxicity; E6 AP; SOD1

Indexed keywords

CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; E6 AP UBIQUITIN PROTEIN LIGASE; HEAT SHOCK PROTEIN 70; UNCLASSIFIED DRUG;

AGGRESOME; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL INCLUSION; CELL PROTECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; GENE MUTATION; IMMUNOPRECIPITATION; MOUSE; NERVE DEGENERATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UBIQUITINATION;

EID: 84872308389     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.08.016     Document Type: Article

References (46)

1. Ballinger C.A., Connell P., Wu Y., Hu Z., Thompson L.J., Yin L.Y., Patterson C. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 1999, 19:4535-4545.
2. Baneyx F., Mujacic M. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol. 2004, 22:1399-1408.
3. Boillee S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
4. Bruijn L.I., Becher M.W., Lee M.K., Anderson K.L., Jenkins N.A., Copeland N.G., Sisodia S.S., Rothstein J.D., Borchelt D.R., Price D.L., Cleveland D.W. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1997, 18:327-338.
5. Bruijn L.I., Houseweart M.K., Kato S., Anderson K.L., Anderson S.D., Ohama E., Reaume A.G., Scott R.W., Cleveland D.W. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 1998, 281:1851-1854.
6. Chhangani D., Joshi A.P., Mishra A. E3 ubiquitin ligases in protein quality control mechanism. Mol. Neurobiol. 2012, 45:571-585.
7. Chiti F., Dobson C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 2006, 75:333-366.
8. Dai Q., Zhang C., Wu Y., McDonough H., Whaley R.A., Godfrey V., Li H.H., Madamanchi N., Xu W., Neckers L., Cyr D., Patterson C. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 2003, 22:5446-5458.
9. Dickey C.A., Patterson C., Dickson D., Petrucelli L. Brain CHIP: removing the culprits in neurodegenerative disease. Trends Mol. Med. 2007, 13:32-38.
10. Dikshit P., Jana N.R. The co-chaperone CHIP is induced in various stresses and confers protection to cells. Biochem. Biophys. Res. Commun. 2007, 357:761-765.
11. Ganesan S., Rohde G., Eckermann K., Sroka K., Schaefer M.K., Dohm C.P., Kermer P., Haase G., Wouters F., Bahr M., Weishaupt J.H. Mutant SOD1 detoxification mechanisms in intact single cells. Cell Death Differ. 2008, 15:312-321.
12. Glessner J.T., Wang K., Cai G., Korvatska O., Kim C.E., Wood S., Zhang H., Estes A., Brune C.W., Bradfield J.P., Imielinski M., Frackelton E.C., Reichert J., Crawford E.L., Munson J., Sleiman P.M., Chiavacci R., Annaiah K., Thomas K., Hou C., Glaberson W., Flory J., Otieno F., Garris M., Soorya L., Klei L., Piven J., Meyer K.J., Anagnostou E., Sakurai T., Game R.M., Rudd D.S., Zurawiecki D., McDougle C.J., Davis L.K., Miller J., Posey D.J., Michaels S., Kolevzon A., Silverman J.M., Bernier R., Levy S.E., Schultz R.T., Dawson G., Owley T., McMahon W.M., Wassink T.H., Sweeney J.A., Nurnberger J.I., Coon H., Sutcliffe J.S., Minshew N.J., Grant S.F., Bucan M., Cook E.H., Buxbaum J.D., Devlin B., Schellenberg G.D., Hakonarson H. Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 2009, 459:569-573.
13. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
14. Harbord M. Levodopa responsive Parkinsonism in adults with Angelman Syndrome. J. Clin. Neurosci. 2001, 8:421-422.
15. Huibregtse J.M., Scheffner M., Howley P.M. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell. Biol. 1993, 13:775-784.
16. Imai Y., Soda M., Hatakeyama S., Akagi T., Hashikawa T., Nakayama K.I., Takahashi R. CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol. Cell 2002, 10:55-67.
17. Imai Y., Soda M., Takahashi R. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem. 2000, 275:35661-35664.
18. Jana N.R., Zemskov E.A., Wang G., Nukina N. 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. 2001, 10:1049-1059.
19. Matentzoglu K., Scheffner M. Ubiquitin ligase E6-AP and its role in human disease. Biochem. Soc. Trans. 2008, 36(Pt. 5):797-801.
20. Matsumoto G., Stojanovic A., Holmberg C.I., Kim S., Morimoto R.I. Structural properties and neuronal toxicity of amyotrophic lateral sclerosis-associated Cu/Zn superoxide dismutase 1 aggregates. J. Cell Biol. 2005, 171:75-85.
21. Meacham G.C., Patterson C., Zhang W., Younger J.M., Cyr D.M. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell Biol. 2001, 3:100-105.
22. Min J.N., Whaley R.A., Sharpless N.E., Lockyer P., Portbury A.L., Patterson C. CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Mol. Cell. Biol. 2008, 28:4018-4025.
23. Mishra A., Dikshit P., Purkayastha S., Sharma J., Nukina N., Jana N.R. E6-AP promotes misfolded polyglutamine proteins for proteasomal degradation and suppresses polyglutamine protein aggregation and toxicity. J. Biol. Chem. 2008, 283:7648-7656.
24. Mishra A., Godavarthi S.K., Jana N.R. UBE3A/E6-AP regulates cell proliferation by promoting proteasomal degradation of p27. Neurobiol. Dis. 2009, 36:26-34.
25. Mishra A., Godavarthi S.K., Maheshwari M., Goswami A., Jana N.R. The ubiquitin ligase E6-AP is induced and recruited to aggresomes in response to proteasome inhibition and may be involved in the ubiquitination of Hsp70-bound misfolded proteins. J. Biol. Chem. 2009, 284:10537-10545.
26. Mishra A., Jana N.R. Regulation of turnover of tumor suppressor p53 and cell growth by E6-AP, a ubiquitin protein ligase mutated in Angelman mental retardation syndrome. Cell. Mol. Life Sci. 2008, 65:656-666.
27. Miyazaki K., Fujita T., Ozaki T., Kato C., Kurose Y., Sakamoto M., Kato S., Goto T., Itoyama Y., Aoki M., Nakagawara A. NEDL1, a novel ubiquitin-protein isopeptide ligase for dishevelled-1, targets mutant superoxide dismutase-1. J. Biol. Chem. 2004, 279:11327-11335.
28. Mosser D.D., Caron A.W., Bourget L., Denis-Larose C., Massie B. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 1997, 17:5317-5327.
29. Mulherkar S.A., Sharma J., Jana N.R. The ubiquitin ligase E6-AP promotes degradation of alpha-synuclein. J. Neurochem. 2009, 110:1955-1964.
30. Murata S., Minami Y., Minami M., Chiba T., Tanaka K. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2001, 2:1133-1138.
31. Niwa J., Ishigaki S., Hishikawa N., Yamamoto M., Doyu M., Murata S., Tanaka K., Taniguchi N., Sobue G. Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J. Biol. Chem. 2002, 277:36793-36798.
32. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
33. Qian S.B., McDonough H., Boellmann F., Cyr D.M., Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 2006, 440:551-555.
34. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., Rahmani Z., Krizus A., Mckenna-Yasek D., Cayabyab A., Gaston S.M., Berger R., Tanzi R.E., Halperin J.J., Herzfeldt B., Bergh R.V.D., Hung W., Bird T., Deng G., Mulder D.W., Smyth C., Laing N.G., Soriano E., Pericak-Vance M.A., Haines J., Rouleau G.A., Gusella J.S., Horvitz H.R., Brown R.H. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis [Erratum in 1993;364:362]. Nature 1993, 362:59-62.
35. Rosenbaum J.C., Fredrickson E.K., Oeser M.L., Garrett-Engele C.M., Locke M.N., Richardson L.A., Nelson Z.W., Hetrick E.D., Milac T.I., Gottschling D.E., Gardner R.G. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol. Cell 2011, 41:93-106.
36. Scheffner M., Nuber U., Huibregtse J.M. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 1995, 373:81-83.
37. Stegmuller J., Bonni A. Destroy to create: E3 ubiquitin ligases in neurogenesis. F1000 Biol. Rep. 2010, 2. pii, 38.
38. Tovchigrechko A., Vakser I.A. GRAMM-X public web server for protein-protein docking. Nucleic Acids Res. 2006, 34:W310-W314.
39. Urushitani M., Kurisu J., Tateno M., Hatakeyama S., Nakayama K., Kato S., Takahashi R. CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. J. Neurochem. 2004, 90:231-244.
40. Wang X.S., Simmons Z., Liu W., Boyer P.J., Connor J.R. Differential expression of genes in amyotrophic lateral sclerosis revealed by profiling the post mortem cortex. Amyotroph. Lateral Scler. 2006, 7:201-210.
41. Yamanaka K., Chun S.J., Boillee S., Fujimori-Tonou N., Yamashita H., Gutmann D.H., Takahashi R., Misawa H., Cleveland D.W. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci. 2008, 11:251-253.
42. Yamashita H., Kawamata J., Okawa K., Kanki R., Nakamizo T., Hatayama T., Yamanaka K., Takahashi R., Shimohama S. Heat-shock protein 105 interacts with and suppresses aggregation of mutant Cu/Zn superoxide dismutase: clues to a possible strategy for treating ALS. J. Neurochem. 2007, 102:1497-1505.
43. Ying Z., Wang H., Fan H., Zhu X., Zhou J., Fei E., Wang G. Gp78, an ER associated E3, promotes SOD1 and ataxin-3 degradation. Hum. Mol. Genet. 2009, 18:4268-4281.
44. Yonashiro R., Sugiura A., Miyachi M., Fukuda T., Matsushita N., Inatome R., Ogata Y., Suzuki T., Dohmae N., Yanagi S. Mitochondrial ubiquitin ligase MITOL ubiquitinates mutant SOD1 and attenuates mutant SOD1-induced reactive oxygen species generation. Mol. Biol. Cell 2009, 20:4524-4530.
45. Yost H.J., Lindquist S. RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 1986, 45:185-193.
46. Young J.C., Agashe V.R., Siegers K., Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell. Biol. 2004, 5:781-791.