Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation

Journal of Neuroscience

Volumn 27, Issue 13, 2007, Pages 3571-3583

  Dompierre, Jim P ^a,b   Godin, Juliette D ^a,b   Charrin, Bénédicte C ^a,b   Cordelières, Fabrice P ^a,b,c   King, Stephen J ^d   Humbert, Sandrine ^a,b   Saudou, Frédéric ^a,b  

^a INSTITUT D'OPTIQUE GRADUATE SCHOOL   (France)

^b CNRS   (France)

^c Plate forme Imagerie Cellulaire et Tissulaire   (France)

^d UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

BDNF; Huntington's disease; Microtubules; Neuroprotection; Polyglutamine; Transport

Indexed keywords

ALPHA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; DYNEIN ADENOSINE TRIPHOSPHATASE; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; KINESIN; LYSINE; PACLITAXEL; TRICHOSTATIN A; TUBACIN; TUBULIN; UNCLASSIFIED DRUG; VORINOSTAT;

ACETYLATION; ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEACETYLATION; DRUG EFFECT; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; HUNTINGTON CHOREA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; PROTEIN TRANSPORT;

ACETYLATION; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL LINE; CELLS, CULTURED; CEREBRAL CORTEX; HISTONE DEACETYLASES; HUNTINGTON DISEASE; HYDROXAMIC ACIDS; MICE; MICROSCOPY, VIDEO; MICROTUBULES; MOLECULAR MOTOR PROTEINS; NEUROPROTECTIVE AGENTS; TRANSPORT VESICLES; TUBULIN; VISUAL CORTEX;

EID: 34047175919     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0037-07.2007     Document Type: Article

References (61)

1. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856-860.
2. Baquet ZC, Gorski JA, Jones KR (2004) Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J Neurosci 24:4250-4258.
3. Bingham JB, King SJ, Schroer TA (1998) Purification of dynactin and dynein from brain tissue. Methods Enzymol 298:171-184.
4. Butler R, Bates GP (2006) Histone deacetylase inhibitors as therapeutics for polyglutamine disorders. Nat Rev Neurosci 7:784-796.
5. Butowt R, von Bartheld CS (2007) Conventional kinesin-I motors participate in the anterograde axonal transport of neurotrophins in the visual system. J Neurosci Res, in press.
6. Ciechanover A, Brundin P (2003) The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40:427-446.
7. Drummond DC, Noble CO, Kirpotin DB, Guo Z, Scott GK, Benz CC (2005) Clinical development of histone deacetylase inhibitors as anticancer agents. Annu Rev Pharmacol Toxicol 45:495-528.
8. Evans L, Mitchison T, Kirschner M (1985) Influence of the centrosome on the structure o0f nucleated microtubules. J Cell Biol 100:1185-1191.
9. Gaertig J, Cruz MA, Bowen J, Gu L, Pennock DG, Gorovsky MA (1995) Acetylation of lysine 40 in alpha-tubulin is not essential in Tetrahymena thermophila. J Cell Biol 129:1301-1310.
10. Gauthier LR, Charrin BC, Borrell-Pages M, Dompierre JP, Rangone H, Cordelieres FP, De Mey J, MacDonald ME, Lessmann V, Humbert S, Saudou F (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118:127-138.
11. Goldstein LS, Laymon RA, McIntosh JR (1986) A microtubule-associated protein in Drosophila melanogaster: identification, characterization, and isolation of coding sequences. J Cell Biol 102:2076-2087.
12. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, Gordesky-Gold B, Sintasath L, Bonini NM, Goldstein LS (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40:25-40.
13. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL (2003) Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci USA 100:4389-4394.
14. Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20:5887-5897.
15. Haubensak W, Narz F, Heumann R, Lessmann V (1998) BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. J Cell Sci 111:1483-1493.
16. Hempen B, Brion JP (1996) Reduction of acetylated alpha-tubulin immunoreactivity in neurofibrillary tangle-bearing neurons in Alzheimer's disease. J Neuropathol Exp Neurol 55:964-972.
17. Hu E, Dul E, Sung CM, Chen Z, Kirkpatrick R, Zhang GF, Johanson K, Liu R, Lago A, Hofmann G, Macarron R, de los Frailes M, Perez P, Krawiec J, Winkler J, Jaye M (2003) Identification of novel isoform-selective inhibitors within class I histone deacetylases. J Pharmacol Exp Ther 307:720-728.
18. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417:455-458.
19. Humbert S, Bryson EA, Cordelieres FP, Connors NC, Datta SR, Finkbeiner S, Greenberg ME, Saudou F (2002) The IGF-1/Akt pathway is neuroprotective in Huntington's disease and involves Huntingtin phosphorylation by Akt. Dev Cell 2:831-837.
20. Ingold AL, Cohn SA, Scholey JM (1988) Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J Cell Biol 107:2657-2667.
21. Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280:40282-40292.
22. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414:643-648.
23. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115:727-738.
24. Kohara K, Kitamura A, Morishima M, Tsumoto T (2001) Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291:2419-2423.
25. Kozminski KG, Diener DR, Rosenbaum JL (1993) High level expression of nonacetylatable alpha-tubulin in Chlamydomonas reinhardtii. Cell Motil Cytoskeleton 25:158-170.
26. Krebs A, Goldie KN, Hoenger A (2004) Complex formation with kinesin motor domains affects the structure of microtubules. J Mol Biol 335:139-153.
27. Lee WC, Yoshihara M, Littleton JT (2004) Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc Natl Acad Sci USA 101:3224 -3229.
28. Glued form distinct plus-end complexes. FEBS Lett 580:1327-1332.
29. MacDonald ME, Gines S, Gusella JF, Wheeler VC (2003) Huntington's Disease. Neuromolecular Med 4:7-20.
30. Mallik R, Petrov D, Lex SA, King SJ, Gross SP (2005) Building complexity: an in vitro study of cytoplasmic dynein with in vivo implications. Curr Biol 15:2075-2085.
31. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA (1992) Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 103:857-862.
32. Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, Horinouchi S, Yoshida M (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21:6820-6831.
33. McGuire JR, Rong J, Li SH, Li XJ (2006) Interaction of Huntingtin-associated protein-1 with kinesin light chain: implications in intracellular trafficking in neurons. J Biol Chem 281:3552-3559.
34. Mizuno N, Toba S, Edamatsu M, Watai-Nishii J, Hirokawa N, Toyoshima YY, Kikkawa M (2004) Dynein and kinesin share an overlapping microtubule-binding site. EMBO J 23:2459-2467.
35. Nogales E, Wolf SG, Downing KH (1998) Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391:199-203.
36. North BJ, Marshall BL, Borra MT, Denu JM, Verdin E (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 11:437-444.
37. Pigino G, Morfini G, Pelsman A, Mattson MP, Brady ST, Busciglio J (2003) Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J Neurosci 23:4499-4508.
38. Piperno G, Fuller MT (1985) Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J Cell Biol 101:2085-2094.
39. Qin ZH, Wang Y, Kegel KB, Kazantsev A, Apostol BL, Thompson LM, Yoder J, Aronin N, DiFiglia M (2003) Autophagy regulates the processing of amino terminal huntingtin fragments. Hum Mol Genet 12:3231-3244.
40. Ravikumar B, Duden R, Rubinsztein DC (2002) Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 11:1107-1117.
41. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O'Kane CJ, Brown SD, Rubinsztein DC (2005) Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 37:771-776.
42. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16:2166-2172.
43. Saragoni L, Hernandez P, Maccioni RB (2000) Differential association of tau with subsets of microtubules containing posttranslationally-modified tubulin variants in neuroblastoma cells. Neurochem Res 25:59-70.
44. Saudou F, Finkbeiner S, Devys D, Greenberg ME (1998) Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95:55-66.
45. Seigneurin-Berny D, Verdel A, Curtet S, Lemercier C, Garin J, Rousseaux S, Khochbin S (2001) Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol Cell Biol 21:8035-8044.
46. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567-1572.
47. Skiniotis G, Cochran JC, Muller J, Mandelkow E, Gilbert SP, Hoenger A (2004) Modulation of kinesin binding by the C-termini of tubulin. EMBO J 23:989-999.
48. Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, Grosveld F, van Cappellen G, Akhmanova A, Galjart N (2003) Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci 23:2655-2664.
49. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307:1282-1288.
50. Szebenyi G, Morfini GA, Babcock A, Gould M, Selkoe K, Stenoien DL, Young M, Faber PW, MacDonald ME, McPhaul MJ, Brady ST (2003) Neuropathogenic forms of huntingtin and androgen receptor inhibit fast axonal transport. Neuron 40:41-52.
51. Taddei A, Roche D, Bickmore WA, Almouzni G (2005) The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy? EMBO Rep 6:520-524.
52. Toomre D, Keller P, White J, Olivo JC, Simons K (1999) Dual-color visualization of trans-Golgi network to plasma membrane traffic along microtubules in living cells. J Cell Sci 112:21-33.
53. Trettel F, Rigamonti D, Hilditch-Maguire P, Wheeler VC, Sharp AH, Persichetti F, Cattaneo E, MacDonald ME (2000) Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum Mol Genet 9:2799-2809.
54. Trushina E, Dyer RB, Badger II JD, Ure D, Eide L, Tran DD, Vrieze BT, Legendre-Guillemin V, McPherson PS, Mandavilli BS, Van Houten B, Zeitlin S, McNiven M, Aebersold R, Hayden M, Parisi JE, Seeberg E, Dragatsis I, Doyle K, Bender A, et al. (2004) Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol Cell Biol 24:8195-8209.
55. Vaughan KT, Tynan SH, Faulkner NE, Echeverri CJ, Vallee RB (1999) Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J Cell Sci 112:1437-1447.
56. Wada Y, Hamasaki T, Satir P (2000) Evidence for a novel affinity mechanism of motor-assisted transport along microtubules. Mol Biol Cell 11:161-169.
57. Webb JL, Ravikumar B, Rubinsztein DC (2004) Microtubule disruption inhibits autophagosome-lysosome fusion: implications for studying the roles of aggresomes in polyglutamine diseases. Int J Biochem Cell Biol 36:2541-2550.
58. Westermann S, Weber K (2003) Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 4:938-947.
59. Xia Z, Dudek H, Miranti CK, Greenberg ME (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16:5425-5436.
60. Yano H, Chao MV (2004) Mechanisms of neurotrophin receptor vesicular transport. J Neurobiol 58:244-257.
61. 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.