Role of TPPP/p25 on α-synuclein-mediated oligodendroglial degeneration and the protective effect of SIRT2 inhibition in a cellular model of multiple system atrophy

Neurochemistry International

Volumn 57, Issue 8, 2010, Pages 857-866

  Hasegawa, Takafumi ^a   Baba, Toru ^a   Kobayashi, Michiko ^a   Konno, Masatoshi ^a   Sugeno, Naoto ^a   Kikuchi, Akio ^a   Itoyama, Yasuto ^a,b   Takeda, Atsushi ^a  

^a TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

Author keywords

Synuclein; Glial cytoplasmic inclusion; Multiple system atrophy; Oligodendroglia; Sirtuin 2; Tubulin polymerization promoting protein

Indexed keywords

ALPHA SYNUCLEIN; OLIGOMER; PROTEIN; PROTEIN P25; SIRTUIN 2; TUBULIN POLYMERIZATION PROMOTING PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL DEGENERATION; CELL INCLUSION; CELL PROTECTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; NEUROPATHOLOGY; OLIGODENDROGLIA; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SHY DRAGER SYNDROME;

ALPHA-SYNUCLEIN; APOPTOSIS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HUMANS; MULTIPLE SYSTEM ATROPHY; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PHOSPHORYLATION; SERINE; SIRTUIN 2;

EID: 78649634791     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2010.09.002     Document Type: Article

References (67)

1. J.P. Anderson, D.E. Walker, J.M. Goldstein, R. de Laat, K. Banducci, R.J. Caccavello, R. Barbour, J. Huang, K. Kling, M. Lee, L. Diep, P.S. Keim, X. Shen, T. Chataway, M.G. Schlossmacher, P. Seubert, D. Schenk, S. Sinha, W.P. Gai, and T.J. Chilcote Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease J. Biol. Chem. 281 2006 29739 29752
2. S. Arawaka, M. Wada, S. Goto, H. Karube, M. Sakamoto, C.H. Ren, S. Koyama, H. Nagasawa, H. Kimura, T. Kawanami, K. Kurita, K. Tajima, M. Daimon, M. Baba, T. Kido, S. Saino, K. Goto, H. Asao, C. Kitanaka, E. Takashita, S. Hongo, T. Nakamura, T. Kayama, Y. Suzuki, K. Kobayashi, T. Katagiri, K. Kurokawa, M. Kurimura, I. Toyoshima, K. Niizato, K. Tsuchiya, T. Iwatsubo, M. Muramatsu, H. Matsumine, and T. Kato The role of G-protein-coupled receptor kinase 5 in pathogenesis of sporadic Parkinson's disease J. Neurosci. 26 2006 9227 9238
3. K. Arima, K. Ueda, N. Sunohara, K. Arakawa, S. Hirai, M. Nakamura, H. Tonozuka-Uehara, and M. Kawai NACP/alpha-synuclein immunoreactivity in fibrillary components of neuronal and oligodendroglial cytoplasmic inclusions in the pontine nuclei in multiple system atrophy Acta Neuropathol. 96 1998 439 444
4. D.J. Burn, and E. Jaros Multiple system atrophy: cellular and molecular pathology Mol. Pathol. 54 2001 419 426
5. L. Chen, and M.B. Feany Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease Nat. Neurosci. 8 2005 657 663
6. E. Croisier, and M.B. Graeber Glial degeneration and reactive gliosis in alpha-synucleinopathies: the emerging concept of primary gliodegeneration Acta Neuropathol. 112 2006 517 530
7. D.W. Dickson, W. Liu, J. Hardy, M. Farrer, N. Mehta, R. Uitti, M. Mark, T. Zimmerman, L. Golbe, J. Sage, A. Sima, C. D'Amato, R. Albin, S. Gilman, and S.H. Yen Widespread alterations of alpha-synuclein in multiple system atrophy Am. J. Pathol. 155 1999 1241 1251 (Pubitemid 29488931)
8. G. Fillon, and P.J. Kahle Alpha-synuclein transgenic mice: relevance to multiple system atrophy Mov. Disord. 20 Suppl. 12 2005 S64 S66
9. H. Fujiwara, M. Hasegawa, N. Dohmae, A. Kawashima, E. Masliah, M.S. Goldberg, J. Shen, K. Takio, and T. Iwatsubo Alpha-Synuclein is phosphorylated in synucleinopathy lesions Nat. Cell. Biol. 4 2002 160 164
10. J.E. Galvin, V.M. Lee, and J.Q. Trojanowski Synucleinopathies: clinical and pathological implications Arch. Neurol. 58 2001 186 190
11. O.S. Gorbatyuk, S. Li, L.F. Sullivan, W. Chen, G. Kondrikova, F.P. Manfredsson, R.J. Mandel, and N. Muzyczka The phosphorylation state of Ser-129 in human alpha-synuclein determines neurodegeneration in a rat model of Parkinson disease Proc. Natl. Acad. Sci. U.S.A. 105 2008 763 768
12. J.G. Graham, and D.R. Oppenheimer Orthostatic hypotension and nicotine sensitivity in a case of multiple system atrophy J. Neurol. Neurosurg. Psychiatry 32 1969 28 34
13. K. Harting, and B. Knoll SIRT2-mediated protein deacetylation: an emerging key regulator in brain physiology and pathology Eur. J. Cell. Biol. 89 2009 262 269
14. T. Hasegawa, M. Matsuzaki-Kobayashi, A. Takeda, N. Sugeno, A. Kikuchi, K. Furukawa, G. Perry, M.A. Smith, and Y. Itoyama Alpha-synuclein facilitates the toxicity of oxidized catechol metabolites: implications for selective neurodegeneration in Parkinson's disease FEBS Lett. 580 2006 2147 2152
15. T. Hasegawa, M. Matsuzaki, A. Takeda, A. Kikuchi, H. Akita, G. Perry, M.A. Smith, and Y. Itoyama Accelerated alpha-synuclein aggregation after differentiation of SH-SY5Y neuroblastoma cells Brain Res. 1013 2004 51 59
16. E. Hlavanda, J. Kovacs, J. Olah, F. Orosz, K.F. Medzihradszky, and J. Ovadi Brain-specific p25 protein binds to tubulin and microtubules and induces aberrant microtubule assemblies at substoichiometric concentrations Biochemistry 41 2002 8657 8664
17. K.A. Jellinger P25alpha immunoreactivity in multiple system atrophy and Parkinson disease Acta Neuropathol. 112 2006 112
18. K.A. Jellinger, and P.L. Lantos Papp-Lantos inclusions and the pathogenesis of multiple system atrophy: an update Acta Neuropathol. 119 2010 657 667
19. P.J. Kahle Alpha-Synucleinopathy models and human neuropathology: similarities and differences Acta Neuropathol. 115 2008 87 95
20. Y. Kawaguchi, J.J. Kovacs, A. McLaurin, J.M. Vance, A. Ito, and T.P. Yao The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress Cell 115 2003 727 738
21. A.G. Kazantsev, and L.M. Thompson Therapeutic application of histone deacetylase inhibitors for central nervous system disorders Nat. Rev. Drug Discov. 7 2008 854 868
22. A. Kikuchi, A. Takeda, N. Okamura, M. Tashiro, T. Hasegawa, S. Furumoto, M. Kobayashi, N. Sugeno, T. Baba, Y. Miki, F. Mori, K. Wakabayashi, Y. Funaki, R. Iwata, S. Takahashi, H. Fukuda, H. Arai, Y. Kudo, K. Yanai, and Y. Itoyama In vivo visualization of {alpha}-synuclein deposition by carbon-11-labelled 2-[2-(2-dimethylaminothiazol-5-yl)ethenyl]-6-[2-(fluoro)ethoxy]benzoxazole positron emission tomography in multiple system atrophy Brain 133 2010 1772 1778
23. G.G. Kovacs, E. Gelpi, A. Lehotzky, R. Hoftberger, A. Erdei, H. Budka, and J. Ovadi The brain-specific protein TPPP/p25 in pathological protein deposits of neurodegenerative diseases Acta Neuropathol. 113 2007 153 161
24. G.G. Kovacs, L. Laszlo, J. Kovacs, P.H. Jensen, E. Lindersson, G. Botond, T. Molnar, A. Perczel, F. Hudecz, G. Mezo, A. Erdei, L. Tirian, A. Lehotzky, E. Gelpi, H. Budka, and J. Ovadi Natively unfolded tubulin polymerization promoting protein TPPP/p25 is a common marker of alpha-synucleinopathies Neurobiol. Dis. 17 2004 155 162
25. C.L. Kragh, L.B. Lund, F. Febbraro, H.D. Hansen, W.P. Gai, O. El-Agnaf, C. Richter-Landsberg, and P.H. Jensen {alpha}-Synuclein aggregation and Ser-129 phosphorylation-dependent cell death in oligodendroglial cells J. Biol. Chem. 284 2009 10211 10222
26. J.T. Lee, J. Xu, J.M. Lee, G. Ku, X. Han, D.I. Yang, S. Chen, and C.Y. Hsu Amyloid-beta peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway J. Cell. Biol. 164 2004 123 131
27. W. Li, B. Zhang, J. Tang, Q. Cao, Y. Wu, C. Wu, J. Guo, E.A. Ling, and F. Liang Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating alpha-tubulin J. Neurosci. 27 2007 2606 2616
28. E. Lindersson, D. Lundvig, C. Petersen, P. Madsen, J.R. Nyengaard, P. Hojrup, T. Moos, D. Otzen, W.P. Gai, P.C. Blumbergs, and P.H. Jensen p25alpha Stimulates alpha-synuclein aggregation and is co-localized with aggregated alpha-synuclein in alpha-synucleinopathies J. Biol. Chem. 280 2005 5703 5715
29. M. Matsuzaki, T. Hasegawa, A. Takeda, A. Kikuchi, K. Furukawa, Y. Kato, and Y. Itoyama Histochemical features of stress-induced aggregates in alpha-synuclein overexpressing cells Brain Res. 1004 2004 83 90
30. D.W. Miller, J.M. Johnson, S.M. Solano, Z.R. Hollingsworth, D.G. Standaert, and A.B. Young Absence of alpha-synuclein mRNA expression in normal and multiple system atrophy oligodendroglia J. Neural. Transm. 112 2005 1613 1624
31. J.C. Milne, and J.M. Denu The Sirtuin family: therapeutic targets to treat diseases of aging Curr. Opin. Chem. Biol. 12 2008 11 17
32. E. Miyake Establishment of a human oligodendroglial cell line Acta Neuropathol. 46 1979 51 55
33. S. Nakamura, Y. Kawamoto, S. Nakano, and I. Akiguchi Expression of the endocytosis regulatory proteins Rab5 and Rabaptin-5 in glial cytoplasmic inclusions from brains with multiple system atrophy Clin. Neuropathol. 19 2000 51 56
34. K. Nakayama, Y. Suzuki, and I. Yazawa Microtubule depolymerization suppresses alpha-synuclein accumulation in a mouse model of multiple system atrophy Am. J. Pathol. 174 2009 1471 1480
35. M. Nishie, F. Mori, M. Yoshimoto, H. Takahashi, and K. Wakabayashi A quantitative investigation of neuronal cytoplasmic and intranuclear inclusions in the pontine and inferior olivary nuclei in multiple system atrophy Neuropathol. Appl. Neurobiol. 30 2004 546 554
36. B.J. North, B.L. Marshall, M.T. Borra, J.M. Denu, and E. Verdin The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase Mol. Cell. 11 2003 437 444
37. M. Okochi, J. Walter, A. Koyama, S. Nakajo, M. Baba, T. Iwatsubo, L. Meijer, P.J. Kahle, and C. Haass Constitutive phosphorylation of the Parkinson's disease associated alpha-synuclein J. Biol. Chem. 275 2000 390 397
38. T.F. Outeiro, E. Kontopoulos, S.M. Altmann, I. Kufareva, K.E. Strathearn, A.M. Amore, C.B. Volk, M.M. Maxwell, J.C. Rochet, P.J. McLean, A.B. Young, R. Abagyan, M.B. Feany, B.T. Hyman, and A.G. Kazantsev Sirtuin 2 inhibitors rescue alpha-synuclein-mediated toxicity in models of Parkinson's disease Science 317 2007 516 519
39. J. Ovadi, and F. Orosz An unstructured protein with destructive potential: TPPP/p25 in neurodegeneration Bioessays 31 2009 676 686
40. K.E. Paleologou, A.W. Schmid, C.C. Rospigliosi, H.Y. Kim, G.R. Lamberto, R.A. Fredenburg, P.T. Lansbury Jr., C.O. Fernandez, D. Eliezer, M. Zweckstetter, and H.A. Lashuel Phosphorylation at Ser-129 but not the phosphomimics S129E/D inhibits the fibrillation of alpha-synuclein J. Biol. Chem. 283 2008 16895 16905
41. J. Pallos, L. Bodai, T. Lukacsovich, J.M. Purcell, J.S. Steffan, L.M. Thompson, and J.L. Marsh Inhibition of specific HDACs and sirtuins suppresses pathogenesis in a Drosophila model of Huntington's disease Hum. Mol. Genet. 17 2008 3767 3775
42. M.I. Papp, and P.L. Lantos Accumulation of tubular structures in oligodendroglial and neuronal cells as the basic alteration in multiple system atrophy J. Neurol. Sci. 107 1992 172 182
43. S. Probst-Cousin, C.H. Rickert, K.W. Schmid, and F. Gullotta Cell death mechanisms in multiple system atrophy J. Neuropathol. Exp. Neurol. 57 1998 814 821
44. C. Richter-Landsberg, M. Gorath, J.Q. Trojanowski, and V.M. Lee alpha-synuclein is developmentally expressed in cultured rat brain oligodendrocytes J. Neurosci. Res. 62 2000 9 14
45. A. Shiratsuchi, S. Sato, A. Oomori, K. Ishiguro, T. Uchida, and K. Imahori cDNA cloning of a novel brain-specific protein p25 Biochim. Biophys. Acta 1251 1995 66 68
46. Y.J. Song, D.M. Lundvig, Y. Huang, W.P. Gai, P.C. Blumbergs, P. Hojrup, D. Otzen, G.M. Halliday, and P.H. Jensen p25alpha relocalizes in oligodendroglia from myelin to cytoplasmic inclusions in multiple system atrophy Am. J. Pathol. 171 2007 1291 1303
47. C.M. Southwood, M. Peppi, S. Dryden, M.A. Tainsky, and A. Gow Microtubule deacetylases, SirT2 and HDAC6, in the nervous system Neurochem. Res. 32 2007 187 195
48. M.G. Spillantini, R.A. Crowther, R. Jakes, N.J. Cairns, P.L. Lantos, and M. Goedert Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies Neurosci. Lett. 251 1998 205 208 (Pubitemid 28381082)
49. N. Stefanova, P. Bucke, S. Duerr, and G.K. Wenning Multiple system atrophy: an update Lancet Neurol. 8 2009 1172 1178
50. N. Stefanova, M. Reindl, W. Poewe, and G.K. Wenning In vitro models of multiple system atrophy Mov. Disord. 20 Suppl. 12 2005 S53 56
51. N. Stefanova, F. Tison, M. Reindl, W. Poewe, and G.K. Wenning Animal models of multiple system atrophy Trends Neurosci. 28 2005 501 506 (Pubitemid 41187800)
52. N. Sugeno, A. Takeda, T. Hasegawa, M. Kobayashi, A. Kikuchi, F. Mori, K. Wakabayashi, and Y. Itoyama Serine 129 phosphorylation of alpha-synuclein induces unfolded protein response-mediated cell death J. Biol. Chem. 283 2008 23179 23188
53. J.Y. Sung, J. Kim, S.R. Paik, J.H. Park, Y.S. Ahn, and K.C. Chung Induction of neuronal cell death by Rab5A-dependent endocytosis of alpha-synuclein J. Biol. Chem. 276 2001 27441 27448
54. M. Takahashi, K. Tomizawa, K. Ishiguro, K. Sato, A. Omori, S. Sato, A. Shiratsuchi, T. Uchida, and K. Imahori A novel brain-specific 25 kDa protein (p25) is phosphorylated by a Ser/Thr-Pro kinase (TPK II) from tau protein kinase fractions FEBS Lett. 289 1991 37 43
55. A. Takeda, T. Hasegawa, M. Matsuzaki-Kobayashi, N. Sugeno, A. Kikuchi, Y. Itoyama, and K. Furukawa Mechanisms of neuronal death in synucleinopathy J. Biomed. Biotechnol. 2006 2006 19365
56. N. Tokesi, A. Lehotzky, I. Horvath, B. Szabo, J. Olah, P. Lau, and J. Ovadi TPPP/p25 promotes tubulin acetylation by inhibiting histone deacetylase 6 J. Biol. Chem. 285 2010 17896 17906
57. J. Tong, H. Wong, M. Guttman, L.C. Ang, L.S. Forno, M. Shimadzu, A.H. Rajput, M.D. Muenter, S.J. Kish, O. Hornykiewicz, and Y. Furukawa Brain alpha-synuclein accumulation in multiple system atrophy, Parkinson's disease and progressive supranuclear palsy: a comparative investigation Brain 133 2009 172 188
58. P.H. Tu, J.E. Galvin, M. Baba, B. Giasson, T. Tomita, S. Leight, S. Nakajo, T. Iwatsubo, J.Q. Trojanowski, and V.M. Lee Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein Ann. Neurol. 44 1998 415 422
59. Y. Uezono, E. Nakamura, Y. Ueda, I. Shibuya, Y. Ueta, H. Yokoo, T. Yanagita, Y. Toyohira, H. Kobayashi, N. Yanagihara, and A. Wada Production of cAMP by adrenomedullin in human oligodendroglial cell line KG1C: comparison with calcitonin gene-related peptide and amylin Brain Res. Mol. Brain Res. 97 2001 59 69
60. V.N. Uversky, and A.L. Fink Amino acid determinants of alpha-synuclein aggregation: putting together pieces of the puzzle FEBS Lett. 522 2002 9 13
61. O. Vincze, N. Tokesi, J. Olah, E. Hlavanda, A. Zotter, I. Horvath, A. Lehotzky, L. Tirian, K.F. Medzihradszky, J. Kovacs, F. Orosz, and J. Ovadi Tubulin polymerization promoting proteins (TPPPs): members of a new family with distinct structures and functions Biochemistry 45 2006 13818 13826
62. K. Wakabayashi, S. Hayashi, A. Kakita, M. Yamada, Y. Toyoshima, M. Yoshimoto, and H. Takahashi Accumulation of alpha-synuclein/NACP is a cytopathological feature common to Lewy body disease and multiple system atrophy Acta Neuropathol. 96 1998 445 452
63. K. Wakabayashi, and H. Takahashi Cellular pathology in multiple system atrophy Neuropathology 26 2006 338 345
64. G.K. Wenning, and N. Stefanova Recent developments in multiple system atrophy J. Neurol. 256 2009 1791 1808
65. G.K. Wenning, N. Stefanova, K.A. Jellinger, W. Poewe, and M.G. Schlossmacher Multiple system atrophy: a primary oligodendrogliopathy Ann. Neurol. 64 2008 239 246
66. I. Yazawa, B.I. Giasson, R. Sasaki, B. Zhang, S. Joyce, K. Uryu, J.Q. Trojanowski, and V.M. Lee Mouse model of multiple system atrophy alpha-synuclein expression in oligodendrocytes causes glial and neuronal degeneration Neuron 45 2005 847 859
67. M. Yoshida Multiple system atrophy: alpha-synuclein and neuronal degeneration Neuropathology 27 2007 484 493