Tau - An inhibitor of deacetylase HDAC6 function

Journal of Neurochemistry

Volumn 109, Issue 6, 2009, Pages 1756-1766

  Perez, Mar ^a,b   Santa Maria, Ismael ^b,g   De Barreda, Elena Gomez ^b   Zhu, Xiongwei ^c   Cuadros, Raquel ^b   Cabrero, Jose Roman ^a,d   Sanchez Madrid, Francisco ^a,d   Dawson, Hana N ^e   Vitek, Michael P ^e   Perry, George ^c,f   Smith, Mark A ^c   Avila, Jesus ^a,b,g  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CSIC   (Spain)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f University of San Antonio   (United States)

^g CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Alzheimer's disease; Histone deacetylase; Tau; Tubulin acetylation

Indexed keywords

ALPHA TUBULIN; HISTONE DEACETYLASE 6; TAU PROTEIN;

ACETYLATION; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

ACETYLATION; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; BORONIC ACIDS; BRAIN; CELLS, CULTURED; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HUMANS; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; POSTMORTEM CHANGES; TAU PROTEINS; TRANSFECTION; TUBULIN;

MUS;

EID: 65949122957     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06102.x     Document Type: Article

References (53)

1. Avila J. (1990) Microtubule dynamics. FASEB J. 4, 3284 3290. (Pubitemid 120012575)
2. Avila J., Lucas J. J., Perez M. Hernandez F. (2004) Role of tau protein in both physiological and pathological conditions. Physiol. Rev. 84, 361 384. (Pubitemid 38365487)
3. Cabrero J. R., Serrador J. M., Barreiro O. et al. (2006) Lymphocyte chemotaxis is regulated by histone deacetylase 6, independently of its deacetylase activity. Mol. Biol. Cell 17, 3435 3445. (Pubitemid 44156438)
4. Caceres A. Kosik K. S. (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461 463. (Pubitemid 20065232)
5. Caron C., Boyault C. Khochbin S. (2005) Regulatory cross-talk between lysine acetylation and ubiquitination: role in the control of protein stability. BioEssays 27, 408 415. (Pubitemid 40592597)
6. Creppe C., Malinouskaya L., Volvert M. L. et al. (2009) Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136, 551 564.
7. Dawson H. N., Ferreira A., Eyster M. V., Ghoshal N., Binder L. I. Vitek M. P. (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J. Cell Sci. 114, 1179 1187. (Pubitemid 32288531)
8. Deglon N., Tseng J. L., Bensadoun J. C., Zurn A. D., Arsenijevic Y., Pereira de Almeida L., Zufferey R., Trono D. Aebischer P. (2000) Self-inactivating lentiviral vectors with enhanced transgene expression as potential gene transfer system in Parkinson's disease. Hum. Gene Ther. 11, 179 190. (Pubitemid 30044050)
9. Ding H., Dolan P. J. Johnson G. V. (2008) Histone deacetylase 6 interacts with the microtubule-associated protein tau. J. Neurochem. 106, 2119 2130.
10. Drubin D. G. Kirschner M. W. (1986) Tau protein function in living cells. J. Cell Biol. 103, 2739 2746. (Pubitemid 17008019)
11. Estiu G., Greenberg E., Harrison C. B., Kwiatkowski N. P., Mazitschek R., Bradner J. E. Wiest O. (2008) Structural origin of selectivity in class II-selective histone deacetylase inhibitors. J. Med. Chem. 51, 2898 2906.
12. Fantin V. R. Richon V. M. (2007) Mechanisms of resistance to histone deacetylase inhibitors and their therapeutic implications. Clin. Cancer Res. 13, 7237 7242.
13. Fleming J., Spinoulas A., Zheng M., Cunningham S. C., Ginn S. L., McQuilty R. C., Rowe P. B. Alexander I. E. (2005) Partial correction of sensitivity to oxidant stress in Friedreich ataxia patient fibroblasts by frataxin-encoding adeno-associated virus and lentivirus vectors. Hum. Gene Ther. 16, 947 956. (Pubitemid 41153864)
14. Garcia-Escudero V., Gargini R. Izquierdo M. (2008) Glioma regression in vitro and in vivo by a suicide combined treatment. Mol. Cancer Res. 6, 407 417.
15. Greenberg S. G. Davies P. (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl Acad. Sci. USA 87, 5827 5831. (Pubitemid 20240381)
16. Gregoretti I. V., Lee Y. M. Goodson H. V. (2004) Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338, 17 31. (Pubitemid 38429783)
17. Gu W. Roeder R. G. (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595 606. (Pubitemid 27357952)
18. Haggarty S. J., Koeller K. M., Wong J. C., Grozinger C. M. Schreiber S. L. (2003) Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl Acad. Sci. USA 100, 4389 4394. (Pubitemid 36457739)
19. Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., Sato-Yoshitake R., Takei Y., Noda T. Hirokawa N. (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369, 488 491. (Pubitemid 24210568)
20. Hempen B. Brion J. P. (1996) Reduction of acetylated alpha-tubulin immunoreactivity in neurofibrillary tangle-bearing neurons in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 55, 964 972. (Pubitemid 126449410)
21. Hernandez F., Perez M., Lucas J. J. Avila J. (2002) Sulfo- glycosaminoglycan content affects PHF-tau solubility and allows the identification of different types of PHFs. Brain Res. 935, 65 72. (Pubitemid 34327846)
22. Hernandez F., Perez M., Lucas J. J., Mata A. M., Bhat R. Avila J. (2004) Glycogen synthase kinase-3 plays a crucial role in tau exon 10 splicing and intranuclear distribution of SC35. Implications for Alzheimer's disease. J. Biol. Chem. 279, 3801 3806. (Pubitemid 38140625)
23. Hook S. S., Orian A., Cowley S. M. Eisenman R. N. (2002) Histone deacetylase 6 binds polyubiquitin through its zinc finger (PAZ domain) and copurifies with deubiquitinating enzymes. Proc. Natl Acad. Sci. USA 99, 13425 13430. (Pubitemid 35215397)
24. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., Yoshida M., Wang X. F. Yao T. P. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417, 455 458. (Pubitemid 34563539)
25. Ito A., Kawaguchi Y., Lai C. H., Kovacs J. J., Higashimoto Y., Appella E. Yao T. P. (2002) MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J. 21, 6236 6245. (Pubitemid 35415340)
26. Iwata A., Riley B. E., Johnston J. A. Kopito R. R. (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 280, 40282 40292. (Pubitemid 41779165)
27. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y. Yoshimori T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720 5728.
28. Kanai Y., Chen J. Hirokawa N. (1992) Microtubule bundling by tau proteins in vivo: analysis of functional domains. EMBO J. 11, 3953 3961.
29. Kawaguchi Y., Kovacs J. J., McLaurin A., Vance J. M., Ito A. Yao T. P. (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115, 727 738. (Pubitemid 38030301)
30. Kazantsev A. G. Thompson L. M. (2008) Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat. Rev. Drug Discov. 7, 854 868.
31. Kopke E., Tung Y. C., Shaikh S., Alonso A. C., Iqbal K. Grundke-Iqbal I. (1993) Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J. Biol. Chem. 268, 24374 24384. (Pubitemid 23335430)
32. LeDizet M. Piperno G. (1987) Identification of an acetylation site of Chlamydomonas alpha-tubulin. Proc. Natl Acad. Sci. USA 84, 5720 5724.
33. Maruta H., Greer K. Rosenbaum J. L. (1986) The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J. Cell Biol. 103, 571 579. (Pubitemid 16055052)
34. Matsuyama A., Shimazu T., Sumida Y. et al. (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820 6831. (Pubitemid 36014554)
35. North B. J., Marshall B. L., Borra M. T., Denu J. M. Verdin E. (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 11, 437 444. (Pubitemid 36293837)
36. Nuydens R., Van Den Kieboom G., Nolten C., Verhulst C., Van Osta P., Spittaels K., Van den Haute C., De Feyter E., Geerts H. Van Leuven F. (2002) Coexpression of GSK-3beta corrects phenotypic aberrations of dorsal root ganglion cells, cultured from adult transgenic mice overexpressing human protein tau. Neurobiol. Dis. 9, 38 48. (Pubitemid 34174563)
37. Pandey U. B., Nie Z., Batlevi Y. et al. (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447, 859 863. (Pubitemid 46920134)
38. Perez M., Valpuesta J. M., Medina M., Montejo de Garcini E. Avila J. (1996) Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction. J. Neurochem. 67, 1183 1190. (Pubitemid 26277931)
39. Piperno G., LeDizet M. Chang X. J. (1987) Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol. 104, 289 302.
40. Reed N. A., Cai D., Blasius T. L., Jih G. T., Meyhofer E., Gaertig J. Verhey K. J. (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16, 2166 2172.
41. Rubinsztein D. C. (2007) Autophagy induction rescues toxicity mediated by proteasome inhibition. Neuron 54, 854 856. (Pubitemid 46907509)
42. Santa-Maria I., Hernandez F., Del Rio J., Moreno F. J. Avila J. (2007) Tramiprosate, a drug of potential interest for the treatment of Alzheimer's disease, promotes an abnormal aggregation of tau. Mol. Neurodegener. 2, 17. (Pubitemid 350046026)
43. Schulze E., Asai D. J., Bulinski J. C. Kirschner M. (1987) Posttranslational modification and microtubule stability. J. Cell Biol. 105, 2167 2177. (Pubitemid 18019067)
44. Southwood C. M., Peppi M., Dryden S., Tainsky M. A. Gow A. (2007) Microtubule deacetylases, SirT2 and HDAC6, in the nervous system. Neurochem. Res. 32, 187 195. (Pubitemid 46238864)
45. Spillantini M. G. Goedert M. (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci. 21, 428 433. (Pubitemid 28449072)
46. Takemura R., Okabe S., Umeyama T., Kanai Y., Cowan N. J. Hirokawa N. (1992) Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J. Cell Sci. 103, 953 964. (Pubitemid 23042239)
47. Tran A. D., Marmo T. P., Salam A. A. et al. (2007) HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions. J. Cell Sci. 120, 1469 1479. (Pubitemid 46780039)
48. Tseng B. P., Green K. N., Chan J. L., Blurton-Jones M. LaFerla F. M. (2008) Abeta inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol. Aging 29, 1607 1618.
49. Yang X. J. Seto E. (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206 218.
50. Zhang Y., Li N., Caron C., Matthias G., Hess D., Khochbin S. Matthias P. (2003) HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 22, 1168 1179. (Pubitemid 36313600)
51. Zhang Y., Kwon S., Yamaguchi T. et al. (2008) Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol. Cell. Biol. 28, 1688 1701.
52. Zhu X., Rottkamp C. A., Boux H., Takeda A., Perry G. Smith M. A. (2000) Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J. Neuropathol. Exp. Neurol. 59, 880 888.
53. Zhu X., Su B., Wang Y., Mondragon-Rodriguez S., Cash A., Avila J., Perry G. Smith M. A. (2007) Increased tubulin acetylation in Alzheimer disease. J. Neurochem. 102, 75.