ROCK-phosphorylated vimentin modifies mutant huntingtin aggregation via sequestration of IRBIT

Molecular Neurodegeneration

Volumn 7, Issue 1, 2012, Pages

  Bauer, Peter O ^a,c   Hudec, Roman ^a,d   Goswami, Anand ^a   Kurosawa, Masaru ^a   Matsumoto, Gen ^a   Mikoshiba, Katsuhiko ^a,b   Nukina, Nobuyuki ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NATIONAL CANCER INSTITUTE   (United States)

^d SLOVAK UNIVERSITY OF TECHNOLOGY   (Slovakia)

Author keywords

Aggregation; Huntingtin; IP3R1; IRBIT; Rho kinase; Vimentin

Indexed keywords

HUNTINGTIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR 1; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR 1 INTERACTING PROTEIN RELEASED WITH IP3; POLYGLUTAMINE; PROTEIN; RHO KINASE; UNCLASSIFIED DRUG; VIMENTIN;

ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; HUNTINGTON CHOREA; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ANIMALS; BLOTTING, WESTERN; CELL LINE; HUMANS; HUNTINGTON DISEASE; IMMUNOPRECIPITATION; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; PHOSPHORYLATION; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; TRANSFECTION; VIMENTIN;

EID: 84865318493     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-7-43     Document Type: Article

References (53)

1. Huntington's disease genetics. Myers RH, NeuroRx 2004 1 255 262 10.1602/neurorx.1.2.255 15717026
2. Trinucleotide repeat disorders. Orr HT, Zoghbi HY, Annu Rev Neurosci 2007 30 575 621 10.1146/annurev.neuro.29.051605.113042 17417937
3. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntingtons Disease Collaborative Research Group, Cell 1993 72 971 983 10.1016/0092-8674(93)90585-E 8458085
4. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N, Science 1997 277 1990 1993 10.1126/science.277.5334. 1990 9302293
5. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Saudou F, Finkbeiner S, Devys D, Greenberg ME, Cell 1998 95 55 66 10.1016/S0092-8674(00)81782-1 9778247
6. Huntingtin and the molecular pathogenesis of Huntington's disease, Fourth in molecular medicine review series. Landles C, Bates GP, EMBO Rep 2004 5 958 963 10.1038/sj.embor.7400250 15459747
7. The pathogenic mechanisms of polyglutamine diseases and current therapeutic strategies. Bauer PO, Nukina N, J Neurochem 2009 110 1737 1765 10.1111/j.1471-4159.2009.06302.x 19650870
8. Mitochondrial dysfunction in Huntingtons disease: the bioenergetics of isolated and in situ mitochondria from transgenic mice. Oliveira JMA, Jekabsons MB, Chen S, Lin A, Rego CA, Goncalves J, Ellerby LM, Nicholls DJ, J Neurochem 2007 101 241 249 10.1111/j.1471-4159.2006.04361.x 17394466
9. Mitochondrial bioenergetics and dynamics in Huntingtons disease: tripartite synapses and selective striatal degeneration. Oliveira JMA, J Bioenerg Biomembr 2010 42 227 234 10.1007/s10863-010-9287-6 20454921
10. Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates. Franke WW, Schmid E, Winter S, Osborn M, Weber K, Exp Cell Res 1979 123 25 46 10.1016/0014-4827(79) 90418-X 114401
11. In vitro differentiation of mouse teratocarcinoma cells monitored by intermediate filament expression. Paulin D, Jakob H, Jacob F, Weber K, Osborn M, Differentiation 1982 22 90 99 10.1111/j.1432-0436.1982.tb01231.x 6182048
12. Localization of vimentin, the nonspecific intermediate filament protein, in embryonal glia and in early differentiating neurons, In vivo and in vitro immunofluorescence study of the rat embryo with vimentin and neurofilament antisera. Bignami A, Raju T, Dahl D, Dev Biol 1982 91 286 295 10.1016/0012-1606(82)90035-5 7047260
13. Intermediate-sized filaments of human endothelial cells. Franke WW, Schmid E, Osborn M, Weber K, J Cell Biol 1979 81 570 580 10.1083/jcb.81.3.570 379021
14. Synemin isoforms during mouse development: multiplicity of partners in vascular and neuronal systems. Izmiryan A, Franco CA, Paulin D, Li Z, Xue Z, Exp Cell Res 2009 315 769 783 10.1016/j.yexcr.2008.12.009 19124017
15. Neurofibrillary tangles in senile dementia of the Alzheimer type share an antigenic determinant with intermediate filaments of the vimentin class. Yen SH, Gaskin F, Fu SM, Am J Pathol 1983 113 373 381 6196977
16. Neuronal expression of vimentin in the Alzheimer's disease brain may be part of a generalized dendritic damage-response mechanism. Levin EC, Acharya NK, Sedeyn JC, Venkataraman V, D'Andrea MR, Wang HY, Nagele RG, Brain Res 2009 1298 194 207 19728994
17. Dynamic association of proteasomal machinery with the centrosome. Wigley WC, Fabunmi RP, Lee MG, Marino CR, Muallem S, DeMartino GN, Thomas PJ, J Cell Biol 1999 145 481 490 10.1083/jcb.145.3.481 10225950
18. Degradation of CFTR by the ubiquitin-proteasome pathway. Ward CL, Omura S, Kopito RR, Cell 1995 83 121 127 10.1016/0092-8674(95)90240-6 7553863
19. Aggresomes: a cellular response to misfolded proteins. Johnston JA, Ward CL, Kopito RR, J Cell Biol 1998 143 1883 1898 10.1083/jcb.143.7.1883 9864362
20. Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Waelter S, Boeddrich A, Lurz R, Scherzinger E, Lueder G, Lehrach H, Wanker EE, Mol Biol Cell 2001 12 1393 1407 11359930
21. Expanded polyglutamine stretches form an 'aggresome'. Shimohata T, Sato A, Burke JR, Strittmatter WJ, Tsuji S, Onodera O, Neurosci Lett 2002 323 215 218 10.1016/S0304-3940(02)00162-3 11959423
22. IRBIT, a novel inositol 1,4,5-trisphosphate (IP3) receptor-binding protein, is released from the IP3 receptor upon IP3 binding to the receptor. Ando H, Mizutani A, Matsu-ura T, Mikoshiba K, J Biol Chem 2003 278 10602 10612 10.1074/jbc.M210119200 12525476
23. IRBIT suppresses IP3 receptor activity by competing with IP3 for the common binding site on the IP3 receptor. Ando H, Mizutani A, Kiefer H, Tsuzurugi D, Michikawa T, Mikoshiba K, Mol Cell 2006 22 795 806 10.1016/j.molcel.2006.05. 017 16793548
24. Protein phosphatase-1 is a novel regulator of the interaction between IRBIT and the inositol 1,4,5-trisphosphate receptor. Devogelaere B, Beullens M, Sammels E, Derua R, Waelkens E, Van Lint J, Parys JB, Missiaen L, Bollen M, De Smedt H, Biochem J 2007 407 303 311 10.1042/BJ20070361 17635105
25. Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Tang TS, Tu H, Chan EY, Maximov A, Wang Z, Wellington CL, Hayden MR, Bezprozvanny I, Neuron 2003 39 227 239 10.1016/S0896-6273(03)00366-0 12873381
26. Inositol 1,4,5-tripshosphate receptor, calcium signaling and Huntington's disease. Bezprozvanny I, Subcell Biochem 2007 45 323 335 10.1007/978-1-4020- 6191-2-11 18193642
27. Genetic ablation and chemical inhibition of IP3R1 reduce mutant huntingtin aggregation. Bauer PO, Hudec R, Ozaki S, Okuno M, Ebisui E, Mikoshiba K, Nukina N, Biochem Biophys Res Commun 2011 416 13 17 10.1016/j.bbrc.2011.10. 096 22056561
28. Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Tang TS, Slow E, Lupu V, Stavrovskaya IG, Sugimori M, Llinás R, Kristal BS, Hayden MR, Bezprozvanny I, Proc Natl Acad Sci USA 2005 102 2602 2607 10.1073/pnas.0409402102 15695335
29. Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. Goto H, Kosako H, Tanabe K, Yanagida M, Sakurai M, Amano M, Kaibuchi K, Inagaki M, J Biol Chem 1998 273 11728 11736 10.1074/jbc.273.19.11728 9565595
30. Localized phosphorylation of vimentin by rho-kinase in neuroblastoma N2a cells. Nakamura Y, Hashimoto R, Amano M, Nagata K, Matsumoto N, Goto H, Fukusho E, Mori H, Kashiwagi Y, Kudo T, Inagaki M, Takeda M, Genes Cells 2000 5 823 837 10.1046/j.1365-2443.2000.00372.x 11029658
31. The small GTP-binding protein Rho binds to and activates a 160kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. Ishizaki T, Maekawa M, Fujisawa K, Okawa K, Iwamatsu A, Fujita A, Watanabe N, Saito Y, Kakizuka A, Morii N, Narumiya S, EMBO J 1996 15 1885 1893 8617235
32. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. Matsui T, Amano M, Yamamoto T, Chihara K, Nakafuku M, Ito M, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K, EMBO J 1996 15 2208 2216 8641286
33. Rocks: multifunctional kinases in cell behavior. Riento K, Ridley AJ, Nat Rev Mol Cell Biol 2003 4 446 456 10.1038/nrm1128 12778124
34. A rapid cellular FRET assay of polyglutamine aggregation identifies a novel inhibitor. Pollitt SK, Pallos J, Shao J, Desai UA, Ma AA, Thompson LM, Marsh JL, Diamond MI, Neuron 2003 40 685 694 10.1016/S0896-6273(03)00697-4 14622574
35. ROCK and PRK-2 mediate the inhibitory effect of Y-27632 on polyglutamine aggregation. Shao J, Welch WJ, Diamond MI, FEBS Lett 2008 582 1637 1642 10.1016/j.febslet.2008.04.009 18423405
36. Phosphorylation of profilin by ROCK1 regulates polyglutamine aggregation. Shao J, Welch WJ, Diprospero NA, Diamond MI, Mol Cell Biol 2008 28 5196 5208 10.1128/MCB.00079-08 18573880
37. Inhibition of Rho kinases enhances the degradation of mutant huntingtin. Bauer PO, Wong HK, Oyama F, Goswami A, Okuno M, Kino Y, Miyazaki H, Nukina N, J Biol Chem 2009 284 13153 13164 10.1074/jbc.M809229200 19278999
38. Enhanced degradation of mutant huntingtin by rho kinase inhibition is mediated through activation of proteasome and macroautophagy. Bauer PO, Nukina N, Autophagy 2009 5 747 748 10.4161/auto.5.5.8704 19411823
39. Dopaminergic signaling and striatal neurodegeneration in Huntingtons Disease. Tang TS, Chen X, Liu J, Bezprozvanny I, J Neurosci 2007 27 7899 7910 10.1523/JNEUROSCI.1396-07.2007 17652581
40. Dopamine D2 receptor stimulation potentiates polyQ-Huntingtin-induced mouse striatal neuron dysfunctions via Rho/ROCK-II activation. Deyts C, Galan-Rodriguez B, Martin E, Bouveyron N, Roze E, Charvin D, Caboche J, Bétuing S, PLoS One 2009 4 8287 10.1371/journal.pone.0008287 20016831
41. Y-27632 improves rotarod performance and reduces huntingtin levels in R6/2 mice. Li M, Huang Y, Ma AA, Lin E, Diamond MI, Neurobiol Dis 2009 3 413 420
42. Novel functions of vimentin in cell adhesion, migration, and signaling. Ivaska J, Pallari HM, Nevo J, Eriksson JE, Exp Cell Res 2007 313 2050 2062 10.1016/j.yexcr.2007.03.040 17512929
43. Cross-talk among intracellular signaling pathways mediates the diphenyl ditelluride actions on the hippocampal cytoskeleton of young rats. Heimfarth L, Loureiro SO, Reis KP, de Lima BO, Zamboni F, Gandolfi T, Narvaes R, da Rocha JB, Pessoa-Pureur R, Chem Res Toxicol 2011 24 1754 1764 10.1021/tx200307u 21879721
44. Potentiation of nerve growth factor-induced neurite outgrowth by the ROCK inhibitor Y-27632: a possible role of IP3 receptors. Minase T, Ishima T, Itoh K, Hashimoto K, Eur J Pharmacol 2010 648 67 73 10.1016/j.ejphar.2010.09.007 20854802
45. Ndel1 promotes axon regeneration via intermediate filaments. Toth C, Shim SY, Wang J, Jiang Y, Neumayer G, Belzil C, Liu WQ, Martinez J, Zochodne D, Nguyen MD, PLoS One 2008 3 2014 10.1371/journal.pone.0002014 18431495
46. 2+ channel: from discovery to new signaling concepts. Mikoshiba K, J Neurochem 2007 102 1426 1446 10.1111/j.1471-4159.2007. 04825.x 17697045
47. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Taylor JP, Tanaka F, Robitschek J, Sandoval CM, Taye A, Markovic-Plese S, Fischbeck KH, Hum Mol Genet 2003 12 749 757 10.1093/hmg/ddg074 12651870
48. Monoclonal antibodies distinctively recognizing the subtypes of inositol 1,4,5-trisphosphate receptor: application to the studies on inflammatory cells. Sugiyama T, Furuya A, Monkawa T, Yamamoto-Hino M, Satoh S, Ohmori K, Miyawaki A, Hanai N, Mikoshiba K, Hasegawa M, FEBS Lett 1994 354 149 154 10.1016/0014-5793(94)01099-4 7957915
49. A cerebellar Purkinje cell marker P400 protein is an inositol 1,4,5-trisphosphate (InsP3) receptor protein. Purification and characterization of InsP3 receptor complex. Maeda N, Niinobe M, Mikoshiba K, EMBO J 1990 9 61 67 2153079
50. Caspase activation during apoptotic cell death induced by expanded polyglutamine in N2a cells. Wang GH, Mitsui K, Kotliarova S, Yamashita A, Nagao Y, Tokuhiro S, Iwatsubo T, Kanazawa I, Nukina N, Neuroreport 1999 10 2435 2438 10.1097/00001756-199908200-00001 10574348
51. Pro-apoptotic protein kinase C delta is associated with intranuclear inclusions in a transgenic model of Huntington's disease. Zemskov EA, Jana NR, Kurosawa M, Miyazaki H, Sakamoto N, Nekooki M, Nukina N, J Neurochem 2003 87 395 406 10.1046/j.1471-4159.2003.02002.x 14511117
52. rAAV-mediated shRNA ameliorated neuropathology in Huntington disease model mouse. Machida Y, Okada T, Kurosawa M, Oyama F, Ozawa K, Nukina N, Biochem Biophys Res Commun 2006 343 190 197 10.1016/j.bbrc.2006.02.141 16530728
53. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Matsumoto G, Wada K, Okuno M, Kurosawa M, Nukina N, Mol Cell 2011 44 279 289 10.1016/j.molcel.2011.07.039 22017874