Histone deacetylase 6 regulates cytotoxic α-synuclein accumulation through induction of the heat shock response

Neurobiology of Aging

Volumn 35, Issue 10, 2014, Pages 2316-2328

  Du, Yunlan ^a   Wang, Fei ^a   Zou, Jing ^a   Le, Weidong ^b   Dong, Qing ^a   Wang, Zhiying ^a   Shen, Fei ^a   Yu, Ling ^a   Li, Yansheng ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Heat shock; Histone deacetylase 6; Parkinson's disease; Ubiquitin proteasome system; synuclein

Indexed keywords

ALPHA SYNUCLEIN; CHAPERONE; DOPAMINE; HEAT SHOCK PROTEIN 90; HEAT SHOCK TRANSCRIPTION FACTOR 1; HISTONE DEACETYLASE 6; OLIGOMER; PROTEASOME; UBIQUITINATED PROTEIN; DNA BINDING PROTEIN; HDAC6 PROTEIN, MOUSE; HISTONE DEACETYLASE; HSF1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HEAT SHOCK RESPONSE; MALE; MOUSE; NERVE DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OPEN FIELD TEST; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; PHYSIOLOGY; PROTEINOSIS; TOXICITY; UBIQUITINATION;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; HISTONE DEACETYLASES; HSP90 HEAT-SHOCK PROTEINS; MALE; MICE, INBRED C57BL; MOLECULAR CHAPERONES; MOLECULAR TARGETED THERAPY; PARKINSON DISEASE; PROTEIN AGGREGATION, PATHOLOGICAL; TRANSCRIPTION FACTORS; UBIQUITINATION;

EID: 84903817087     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.04.029     Document Type: Article

References (57)

1. Bobrowska A., Paganetti P., Matthias P., Bates G.P. HDAC6 knock-out increases tubulin acetylation but does not modify disease progression in the R6/2 mouse model of Huntington's disease. PLoS One 2011, 6:e20696.
2. Boyault C., Gilquin B., Zhang Y., Rybin V., Garman E., Meyer-Klaucke W., Matthias P., Muller C.W., Khochbin S. HDAC6-p97/VCP controlled polyubiquitin chain turnover. EMBO J. 2006, 25:3357-3366.
3. Boyault C., Sadoul K., Pabion M., Khochbin S. HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene 2007, 26:5468-5476.
4. Boyault C., Zhang Y., Fritah S., Caron C., Gilquin B., Kwon S.H., Garrido C., Yao T.P., Vourc'h C., Matthias P., Khochbin S. HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev. 2007, 21:2172-2181.
5. Bruinsma I.B., Bruggink K.A., Kinast K., Versleijen A.A., Segers-Nolten I.M., Subramaniam V., Kuiperij H.B., Boelens W., de Waal R.M., Verbeek M.M. Inhibition of alpha-synuclein aggregation by small heat shock proteins. Proteins 2011, 79:2956-2967.
6. Chen S., Owens G.C., Makarenkova H., Edelman D.B. HDAC6 regulates mitochondrial transport in hippocampal neurons. PLoS One 2010, 5:e10848.
7. Chen W.Q., Zhao X.L., Wang D.L., Li S.T., Hou Y., Hong Y., Cheng Y.Y. Effects of epigallocatechin-3-gallate on behavioral impairments induced by psychological stress in rats. Exp. Biol. Med. (Maywood) 2010, 235:577-583.
8. Cook C., Gendron T.F., Scheffel K., Carlomagno Y., Dunmore J., DeTure M., Petrucelli L. Loss of HDAC6, a novel CHIP substrate, alleviates abnormal tau accumulation. Hum. Mol. Genet. 2012, 21:2936-2945.
9. Danzer K.M., Ruf W.P., Putcha P., Joyner D., Hashimoto T., Glabe C., Hyman B.T., McLean P.J. Heat-shock protein 70 modulates toxic extracellular alpha-synuclein oligomers and rescues trans-synaptic toxicity. FASEB J. 2011, 25:326-336.
10. Diogenes M.J., Dias R.B., Rombo D.M., Vicente Miranda H., Maiolino F., Guerreiro P., Nasstrom T., Franquelim H.G., Oliveira L.M., Castanho M.A., Lannfelt L., Bergstrom J., Ingelsson M., Quintas A., Sebastiao A.M., Lopes L.V., Outeiro T.F. Extracellular alpha-synuclein oligomers modulate synaptic transmission and impair LTP via NMDA-receptor activation. J.Neurosci. 2012, 32:11750-11762.
11. Donmez G., Arun A., Chung C.Y., McLean P.J., Lindquist S., Guarente L. SIRT1 protects against alpha-synuclein aggregation by activating molecular chaperones. J.Neurosci. 2012, 32:124-132.
12. Du G., Liu X., Chen X., Song M., Yan Y., Jiao R., Wang C.C. Drosophila histone deacetylase 6 protects dopaminergic neurons against {alpha}-synuclein toxicity by promoting inclusion formation. Mol. Biol. Cell 2010, 21:2128-2137.
13. Du Y., Li X., Yang D., Zhang X., Chen S., Huang K., Le W. Multiple molecular pathways are involved in the neuroprotection of GDNF against proteasome inhibitor induced dopamine neuron degeneration invivo. Exp. Biol. Med. (Maywood) 2008, 233:881-890.
14. Du Y., Yang D., Li L., Luo G., Li T., Fan X., Wang Q., Zhang X., Wang Y., Le W. An insight into the mechanistic role of p53-mediated autophagy induction in response to proteasomal inhibition-induced neurotoxicity. Autophagy 2009, 5:663-675.
15. Emmanouilidou E., Stefanis L., Vekrellis K. Cell-produced alpha-synuclein oligomers are targeted to, and impair, the 26S proteasome. Neurobiol. Aging 2010, 31:953-968.
16. Engelender S. Ubiquitination of alpha-synuclein and autophagy in Parkinson's disease. Autophagy 2008, 4:372-374.
17. Fiesel F.C., Schurr C., Weber S.S., Kahle P.J. TDP-43 knockdown impairs neurite outgrowth dependent on its target histone deacetylase 6. Mol. Neurodegener. 2011, 6:64.
18. Fukada M., Hanai A., Nakayama A., Suzuki T., Miyata N., Rodriguiz R.M., Wetsel W.C., Yao T.P., Kawaguchi Y. Loss of deacetylation activity of HDAC6 affects emotional behavior in mice. PLoS One 2012, 7:e30924.
19. Hinault M.P., Farina-Henriquez-Cuendet A., Goloubinoff P. Molecular chaperones and associated cellular clearance mechanisms against toxic protein conformers in Parkinson's disease. Neurodegener. Dis. 2011, 8:397-412.
20. Hoshino T., Murao N., Namba T., Takehara M., Adachi H., Katsuno M., Sobue G., Matsushima T., Suzuki T., Mizushima T. Suppression of Alzheimer's disease-related phenotypes by expression of heat shock protein 70 in mice. J.Neurosci. 2011, 31:5225-5234.
21. 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.
22. 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.
23. Ju J.S., Miller S.E., Hanson P.I., Weihl C.C. Impaired protein aggregate handling and clearance underlie the pathogenesis of p97/VCP-associated disease. J.Biol. Chem. 2008, 283:30289-30299.
24. Junn E., Ronchetti R.D., Quezado M.M., Kim S.Y., Mouradian M.M. Tissue transglutaminase-induced aggregation of alpha-synuclein: implications for Lewy body formation in Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U.S.A 2003, 100:2047-2052.
25. Kalia L.V., Kalia S.K., McLean P.J., Lozano A.M., Lang A.E. alpha-Synuclein oligomers and clinical implications for Parkinson disease. Ann. Neurol. 2013, 73:155-169.
26. Kang R., Zeh H.J., Lotze M.T., Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011, 18:571-580.
27. 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.
28. Kilpatrick K., Novoa J.A., Hancock T., Guerriero C.J., Wipf P., Brodsky J.L., Segatori L. Chemical induction of Hsp70 reduces α-synuclein aggregation in neuroglioma cells. ACS Chem. Biol. 2013, 8:1460-1468.
29. Kimura H., Yukitake H., Tajima Y., Suzuki H., Chikatsu T., Morimoto S., Funabashi Y., Omae H., Ito T., Yoneda Y., Takizawa M. ITZ-1, a client-selective Hsp90 inhibitor, efficiently induces heat shock factor 1 activation. Chem. Biol. 2010, 17:18-27.
30. Kovacs J.J., Murphy P.J., Gaillard S., Zhao X., Wu J.T., Nicchitta C.V., Yoshida M., Toft D.O., Pratt W.B., Yao T.P. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 2005, 18:601-607.
31. Lee J.T., Wheeler T.C., Li L., Chin L.S. Ubiquitination of alpha-synuclein by Siah-1 promotes alpha-synuclein aggregation and apoptotic cell death. Hum. Mol. Genet. 2008, 17:906-917.
32. Lee J.Y., Koga H., Kawaguchi Y., Tang W., Wong E., Gao Y.S., Pandey U.B., Kaushik S., Tresse E., Lu J., Taylor J.P., Cuervo A.M., Yao T.P. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 2010, 29:969-980.
33. Lee J.Y., Nagano Y., Taylor J.P., Lim K.L., Yao T.P. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J.Cell Biol. 2010, 189:671-679.
34. Lee Y.P., Kim D.W., Kang H.W., Hwang J.H., Jeong H.J., Sohn E.J., Kim M.J., Ahn E.H., Shin M.J., Kim D.S., Kang T.C., Kwon O.S., Cho S.W., Park J., Eum W.S., Choi S.Y. PEP-1-heat shock protein 27 protects from neuronal damage in cells and in a Parkinson's disease mouse model. FEBS J. 2012, 279:1929-1942.
35. Li X.M., Ma H.B., Ma Z.Q., Li L.F., Xu C.L., Qu R., Ma S.P. Ameliorative and neuroprotective effect in MPTP model of Parkinson's disease by Zhen-Wu-Tang (ZWT), a traditional Chinese medicine. J.Ethnopharmacol. 2010, 130:19-27.
36. Miki Y., Mori F., Tanji K., Kakita A., Takahashi H., Wakabayashi K. Accumulation of histone deacetylase 6, an aggresome-related protein, is specific to Lewy bodies and glial cytoplasmic inclusions. Neuropathology 2011, 31:561-568.
37. Mollenhauer B., Locascio J.J., Schulz-Schaeffer W., Sixel-Doring F., Trenkwalder C., Schlossmacher M.G. alpha-Synuclein and tau concentrations in cerebrospinal fluid of patients presenting with parkinsonism: a cohort study. Lancet Neurol. 2011, 10:230-240.
38. Muchowski P.J., Wacker J.L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 2005, 6:11-22.
39. Neef D.W., Jaeger A.M., Thiele D.J. Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases. Nat. Rev. Drug Discov. 2011, 10:930-944.
40. Nishida Y., Arakawa S., Fujitani K., Yamaguchi H., Mizuta T., Kanaseki T., Komatsu M., Otsu K., Tsujimoto Y., Shimizu S. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009, 461:654-658.
41. Oosterhof N., Dekens D.W., Lawerman T.F., van Dijk M. Yet another role for SIRT1: reduction of alpha-synuclein aggregation in stressed neurons. J.Neurosci. 2012, 32:6413-6414.
42. 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.
43. Ozansoy M., Basak A.N. The central theme of Parkinson's disease: alpha-synuclein. Mol. Neurobiol. 2013, 47:460-465.
44. 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., Padmanabhan R., Hild M., Berry D.L., Garza D., Hubbert C.C., Yao T.P., Baehrecke E.H., Taylor J.P. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447:859-863.
45. Parmigiani R.B., Xu W.S., Venta-Perez G., Erdjument-Bromage H., Yaneva M., Tempst P., Marks P.A. HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proc. Natl. Acad. Sci. U.S.A 2008, 105:9633-9638.
46. Pemberton S., Madiona K., Pieri L., Kabani M., Bousset L., Melki R. Hsc70 protein interaction with soluble and fibrillar alpha-synuclein. J.Biol. Chem. 2011, 286:34690-34699.
47. Price D.L., Rockenstein E., Ubhi K., Phung V., MacLean-Lewis N., Askay D., Cartier A., Spencer B., Patrick C., Desplats P., Ellisman M.H., Masliah E. Alterations in mGluR5 expression and signaling in Lewy body disease and in transgenic models of alpha-synucleinopathy-implications for excitotoxicity. PLoS One 2010, 5:e14020.
48. Putcha P., Danzer K.M., Kranich L.R., Scott A., Silinski M., Mabbett S., Hicks C.D., Veal J.M., Steed P.M., Hyman B.T., McLean P.J. Brain-permeable small-molecule inhibitors of Hsp90 prevent alpha-synuclein oligomer formation and rescue alpha-synuclein-induced toxicity. J.Pharmacol. Exp. Ther. 2010, 332:849-857.
49. Rubinsztein D.C., Codogno P., Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat. Rev. Drug Discov. 2012, 11:709-730.
50. Su M., Shi J.J., Yang Y.P., Li J., Zhang Y.L., Chen J., Hu L.F., Liu C.F. HDAC6 regulates aggresome-autophagy degradation pathway of alpha-synuclein in response to MPP+-induced stress. J.Neurochem. 2011, 117:112-120.
51. Tapia M., Wandosell F., Garrido J.J. Impaired function of HDAC6 slows down axonal growth and interferes with axon initial segment development. PLoS One 2010, 5:e12908.
52. Tofaris G.K., Kim H.T., Hourez R., Jung J.W., Kim K.P., Goldberg A.L. Ubiquitin ligase Nedd4 promotes alpha-synuclein degradation by the endosomal-lysosomal pathway. Proc. Natl. Acad. Sci. U.S.A 2011, 108:17004-17009.
53. Tsika E., Moysidou M., Guo J., Cushman M., Gannon P., Sandaltzopoulos R., Giasson B.I., Krainc D., Ischiropoulos H., Mazzulli J.R. Distinct region-specific alpha-synuclein oligomers in A53T transgenic mice: implications for neurodegeneration. J.Neurosci. 2010, 30:3409-3418.
54. Wang X.H., Lu G., Hu X., Tsang K.S., Kwong W.H., Wu F.X., Meng H.W., Jiang S., Liu S.W., Ng H.K., Poon W.S. Quantitative assessment of gait and neurochemical correlation in a classical murine model of Parkinson's disease. BMC Neurosci. 2012, 13:142.
55. Waxman E.A., Covy J.P., Bukh I., Li X., Dawson T.M., Giasson B.I. Leucine-rich repeat kinase 2 expression leads to aggresome formation that is not associated with alpha-synuclein inclusions. J.Neuropathol. Exp. Neurol. 2009, 68:785-796.
56. Zhang Y., Ahn Y.H., Benjamin I.J., Honda T., Hicks R.J., Calabrese V., Cole P.A., Dinkova-Kostova A.T. HSF1-dependent upregulation of Hsp70 by sulfhydryl-reactive inducers of the KEAP1/NRF2/ARE pathway. Chem. Biol. 2011, 18:1355-1361.
57. Zilberman Y., Ballestrem C., Carramusa L., Mazitschek R., Khochbin S., Bershadsky A. Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J.Cell Sci. 2009, 122:3531-3541.