Proteasomes Activate Aggresome Disassembly and Clearance by Producing Unanchored Ubiquitin Chains

Molecular Cell

Volumn 51, Issue 6, 2013, Pages 819-828

  Hao, Rui ^a   Nanduri, Priyaanka ^a   Rao, Yanhua ^a   Panichelli, R Scott ^a   Ito, Akihiro ^b,c   Yoshida, Minoru ^b,c   Yao, Tso Pang ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RIKEN   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; HISTONE DEACETYLASE 6; LYSINE; MYOSIN ADENOSINE TRIPHOSPHATASE; POH1 ENZYME; PROTEASOME; UBIQUITINATED PROTEIN; UNANCHORED UBIQUITIN CHAIN; UNCLASSIFIED DRUG;

AGGRESOME; ARTICLE; AUTOPHAGY; CELL STRAIN HEK293; CLEARANCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME DEGRADATION; ENZYME SUBUNIT; HUMAN; HUMAN CELL; MICROINJECTION; MOLECULE; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; UBIQUITINATION;

AUTOPHAGY; HISTONE DEACETYLASES; HUMANS; INCLUSION BODIES; NEURODEGENERATIVE DISEASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEOLYSIS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84884593127     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.08.016     Document Type: Article

References (31)

1. Bennett E.J., Shaler T.A., Woodman B., Ryu K.Y., Zaitseva T.S., Becker C.H., Bates G.P., Schulman H., Kopito R.R. Global changes to the ubiquitin system in Huntington's disease. Nature 2007, 448:704-708.
2. Burnett B.G., Pittman R.N. The polyglutamine neurodegenerative protein ataxin 3 regulates aggresome formation. Proc. Natl. Acad. Sci. USA 2005, 102:4330-4335.
3. Butler K.V., Kalin J., Brochier C., Vistoli G., Langley B., Kozikowski A.P. Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J.Am. Chem. Soc. 2010, 132:10842-10846.
4. Cooper E.M., Cutcliffe C., Kristiansen T.Z., Pandey A., Pickart C.M., Cohen R.E. K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J. 2009, 28:621-631.
5. Gallery M., Blank J.L., Lin Y., Gutierrez J.A., Pulido J.C., Rappoli D., Badola S., Rolfe M., Macbeth K.J. The JAMM motif of humandeubiquitinase Poh1 is essential for cell viability. Mol. Cancer Ther. 2007, 6:262-268.
6. Gao Y.S., Hubbert C.C., Lu J., Lee Y.S., Lee J.Y., Yao T.P. Histone deacetylase 6 regulates growth factor-induced actin remodeling and endocytosis. Mol. Cell. Biol. 2007, 27:8637-8647.
7. Holmberg C.I., Staniszewski K.E., Mensah K.N., Matouschek A., Morimoto R.I. Inefficient degradation of truncated polyglutamine proteins by the proteasome. EMBO J. 2004, 23:4307-4318.
8. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., Yoshida M., Wang X.F., Yao T.P. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417:455-458.
9. Iwata A., Riley B.E., Johnston J.A., Kopito R.R. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J.Biol. Chem. 2005, 280:40282-40292.
10. Johnston J.A., Ward C.L., Kopito R.R. Aggresomes: a cellular response to misfolded proteins. J.Cell Biol. 1998, 143:1883-1898.
11. Kawaguchi Y., Kovacs J.J., McLaurin A., Vance J.M., Ito A., Yao T.P. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003, 115:727-738.
12. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000, 10:524-530.
13. Lee J.Y., Koga H., Kawaguchi Y., Tang W., Wong E., Gao Y.S., Pandey U.B., Kaushik S., Tresse E., Lu J., et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 2010, 29:969-980.
14. McNaught K.S., Olanow C.W., Halliwell B., Isacson O., Jenner P. Failure of the ubiquitin-proteasome system in Parkinson's disease. Nat. Rev. Neurosci. 2001, 2:589-594.
15. McNaught K.S., Shashidharan P., Perl D.P., Jenner P., Olanow C.W. Aggresome-related biogenesis of Lewy bodies. Eur. J. Neurosci. 2002, 16:2136-2148.
16. Ouyang H., Ali Y.O., Ravichandran M., Dong A., Qiu W., MacKenzie F., Dhe-Paganon S., Arrowsmith C.H., Zhai R.G. Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J.Biol. Chem. 2012, 287:2317-2327.
17. Pai M.T., Tzeng S.R., Kovacs J.J., Keaton M.A., Li S.S., Yao T.P., Zhou P. Solution structure of the Ubp-M BUZ domain, a highly specific protein module that recognizes the C-terminal tail of free ubiquitin. J.Mol. Biol. 2007, 370:290-302.
18. Pandey U.B., Nie Z., Batlevi Y., McCray B.A., Ritson G.P., Nedelsky N.B., Schwartz S.L., DiProspero N.A., Knight M.A., Schuldiner O., et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447:859-863.
19. Reyes-Turcu F.E., Horton J.R., Mullally J.E., Heroux A., Cheng X., Wilkinson K.D. The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 2006, 124:1197-1208.
20. Snyder H., Mensah K., Theisler C., Lee J., Matouschek A., Wolozin B. Aggregated and monomeric alpha-synuclein bind to the S6' proteasomal protein and inhibit proteasomal function. J.Biol. Chem. 2003, 278:11753-11759.
21. Tran P.B., Miller R.J. Aggregates in neurodegenerative disease: crowds and power?. Trends Neurosci. 1999, 22:194-197.
22. Venkatraman P., Wetzel R., Tanaka M., Nukina N., Goldberg A.L. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol. Cell 2004, 14:95-104.
23. Verma R., Aravind L., Oania R., McDonald W.H., Yates J.R., Koonin E.V., Deshaies R.J. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002, 298:611-615.
24. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
25. Webb J.L., Ravikumar B., Atkins J., Skepper J.N., Rubinsztein D.C. Alpha-Synuclein is degraded by both autophagy and the proteasome. J.Biol. Chem. 2003, 278:25009-25013.
26. Wigley W.C., Fabunmi R.P., Lee M.G., Marino C.R., Muallem S., DeMartino G.N., Thomas P.J. Dynamic association of proteasomal machinery with the centrosome. J.Cell Biol. 1999, 145:481-490.
27. Xia Z.P., Sun L., Chen X., Pineda G., Jiang X., Adhikari A., Zeng W., Chen Z.J. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 2009, 461:114-119.
28. Yao T.P. The role of ubiquitin in autophagy-dependent protein aggregate processing. Genes Cancer 2010, 1:779-786.
29. Yao T., Cohen R.E. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 2002, 419:403-407.
30. Zeng W., Sun L., Jiang X., Chen X., Hou F., Adhikari A., Xu M., Chen Z.J. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141:315-330.
31. Zhang X., Yuan Z., Zhang Y., Yong S., Salas-Burgos A., Koomen J., Olashaw N., Parsons J.T., Yang X.J., Dent S.R., et al. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol. Cell 2007, 27:197-213.