Hdac6 knock-out increases tubulin acetylation but does not modify disease progression in the R6/2 mouse model of Huntington's disease

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Bobrowska, Anna ^a   Paganetti, Paolo ^b,d   Matthias, Patrick ^c   Bates, Gillian P ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b NOVARTIS PHARMA AG   (Switzerland)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^d AC IMMUNE SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE DEACETYLASE 6; HUNTINGTIN; TUBULIN; HDAC6 PROTEIN, MOUSE; HISTONE DEACETYLASE; HUNTINGTON PROTEIN, MOUSE; NERVE PROTEIN; NUCLEAR PROTEIN;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; DISEASE MODEL; DRUG TARGETING; ENZYME INHIBITION; EXON; FEMALE; GENE LOSS; GENE MUTATION; HDAC6 GENE; HUNTINGTON CHOREA; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN TRANSPORT; ADULT; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; GENETICS; HISTOLOGY; HUMAN; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; TRANSGENE; TRANSGENIC MOUSE;

ANIMALIA; MUS;

ACETYLATION; ADULT; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HISTONE DEACETYLASES; HUMANS; HUNTINGTON DISEASE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; TRANSGENES; TUBULIN;

EID: 79958064073     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020696     Document Type: Article

References (62)

1. Bates G, Harper PS, Jones L, (2002) Huntington's disease Oxford Oxford University Press pp. xvi 558.
2. Novak MJ, Tabrizi SJ, (2010) Huntington's disease. BMJ 340: c3109.
3. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
4. Tabrizi SJ, Langbehn DR, Leavitt BR, Roos RAC, Durr A, et al. (2009) Biological and clinical manifestations of Huntington's disease in the longitudinal TRACK-HD study: cross-sectional analysis of baseline data. The Lancet Neurology 8: 791-801.
5. Tabrizi SJ, Scahill RI, Durr A, Roos RAC, Leavitt BR, et al. (2011) Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. The Lancet Neurology 10: 31-42.
6. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993.
7. Zuccato C, Valenza M, Cattaneo E, (2010) Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol Rev 90: 905-981.
8. Butler R, Bates GP, (2006) Histone deacetylase inhibitors as therapeutics for polyglutamine disorders. Nat Rev Neurosci 7: 784-796.
9. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB, (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370: 737-749.
10. Finkel T, Deng CX, Mostoslavsky R, (2009) Recent progress in the biology and physiology of sirtuins. Nature 460: 587-591.
11. Bates EA, Victor M, Jones AK, Shi Y, Hart AC, (2006) Differential contributions of Caenorhabditis elegans histone deacetylases to Huntingtin polyglutamine toxicity. Journal of Neuroscience 26: 2830-2838.
12. Hockly E, Richon VM, Woodman B, Smith DL, Zhou X, et al. (2003) Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington's disease. Proc Natl Acad Sci U S A 100: 2041-2046.
13. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413: 739-743.
14. Pallos J, Bodai L, Lukacsovich T, Purcell JM, Steffan JS, et al. (2008) Inhibition of specific HDACs and sirtuins suppresses pathogenesis in a Drosophila model of Huntington's disease. Hum Mol Genet 17: 3767-3775.
15. Khan N, Jeffers M, Kumar S, Hackett C, Boldog F, et al. (2008) Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 409: 581-589.
16. Grozinger CM, Hassig CA, Schreiber SL, (1999) Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc Natl Acad Sci U S A 96: 4868-4873.
17. Seigneurin-Berny D, Verdel A, Curtet S, Lemercier C, Garin J, et al. (2001) Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol Cell Biol 21: 8035-8044.
18. Zhang Y, Li N, Caron C, Matthias G, Hess D, et al. (2003) HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 22: 1168-1179.
19. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, et al. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417: 455-458.
20. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, et al. (2005) HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 18: 601-607.
21. Zhang X, Yuan Z, Zhang Y, Yong S, Salas-Burgos A, et al. (2007) HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol Cell 27: 197-213.
22. Kopito RR, (2000) Aggresomes, inclusion bodies and protein aggregation. Trends in Cell Biology 10: 524-530.
23. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, et al. (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115: 727-738.
24. Kwon S, Zhang Y, Matthias P, (2007) The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev 21: 3381-3394.
25. 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.
26. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, et al. (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447: 859-863.
27. Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E, et al. (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 29: 969-980.
28. Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, et al. (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27: 3571-3583.
29. Mahlknecht U, Schnittger S, Landgraf F, Schoch C, Ottmann OG, et al. (2001) Assignment of the human histone deacetylase 6 gene (HDAC6) to X chromosome p11.23 by in situ hybridization. Cytogenet Cell Genet 93: 135-136.
30. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, et al. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87: 493-506.
31. Moffitt H, McPhail GD, Woodman B, Hobbs C, Bates GP, (2009) Formation of polyglutamine inclusions in a wide range of non-CNS tissues in the HdhQ150 knock-in mouse model of Huntington's disease. PLoS One 4: e8025.
32. Landles C, Sathasivam K, Weiss A, Woodman B, Moffitt H, et al. (2010) Proteolysis of Mutant Huntingtin Produces an Exon 1 Fragment That Accumulates as an Aggregated Protein in Neuronal Nuclei in Huntington Disease. Journal of Biological Chemistry 285: 8808-8823.
33. Woodman B, Butler R, Landles C, Lupton MK, Tse J, et al. (2007) The Hdh(Q150/Q150) knock-in mouse model of HD and the R6/2 exon 1 model develop comparable and widespread molecular phenotypes. Brain Res Bull 72: 83-97.
34. Sathasivam K, Lane A, Legleiter J, Warley A, Woodman B, et al. (2010) Identical oligomeric and fibrillar structures captured from the brains of R6/2 and knock-in mouse models of Huntington's disease. Hum Mol Genet 19: 65-78.
35. Kuhn A, Goldstein DR, Hodges A, Strand AD, Sengstag T, et al. (2007) Mutant huntingtin's effects on striatal gene expression in mice recapitulate changes observed in human Huntington's disease brain and do not differ with mutant huntingtin length or wild-type huntingtin dosage. Human Molecular Genetics 16: 1845-1861.
36. Zhang Y, Kwon S, Yamaguchi T, Cubizolles F, Rousseaux S, et al. (2008) Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol Cell Biol 28: 1688-1701.
37. Luthi-Carter R, Hanson SA, Strand AD, Bergstrom DA, Chun W, et al. (2002) Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain. Human Molecular Genetics 11: 1911-1926.
38. Gao YS, Hubbert CC, Lu J, Lee YS, Lee JY, et al. (2007) Histone deacetylase 6 regulates growth factor-induced actin remodeling and endocytosis. Mol Cell Biol 27: 8637-8647.
39. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, et al. (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16: 2166-2172.
40. Gauthier LR, Charrin BC, Borrell-Pages M, Dompierre JP, Rangone H, et al. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118: 127-138.
41. Zuccato C, Cattaneo E, (2009) Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 5: 311-322.
42. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, et al. (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389: 856-860.
43. Crook ZR, Housman D, (2011) Huntington's Disease: Can Mice Lead the Way to Treatment? Neuron 69: 423-435.
44. Martin EJ, Kim M, Velier J, Sapp E, Lee HS, et al. (1999) Analysis of Huntingtin-associated protein 1 in mouse brain and immortalized striatal neurons. J Comp Neurol 403: 421-430.
45. Apostol BL, Simmons DA, Zuccato C, Illes K, Pallos J, et al. (2008) CEP-1347 reduces mutant huntingtin-associated neurotoxicity and restores BDNF levels in R6/2 mice. Mol Cell Neurosci 39: 8-20.
46. Cepeda C, Cummings DM, Hickey MA, Kleiman-Weiner M, Chen JY, et al. (2010) Rescuing the Corticostriatal Synaptic Disconnection in the R6/2 Mouse Model of Huntington's Disease: Exercise, Adenosine Receptors and Ampakines. PLoS Curr 2.
47. Seo H, Kim W, Isacson O, (2008) Compensatory changes in the ubiquitin-proteasome system, brain-derived neurotrophic factor and mitochondrial complex II/III in YAC72 and R6/2 transgenic mice partially model Huntington's disease patients. Hum Mol Genet 17: 3144-3153.
48. Cho S-R, Benraiss A, Chmielnicki E, Samdani A, Economides A, et al. (2007) Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease. The Journal of Clinical Investigation 117: 2889-2902.
49. Canals JM, Pineda JR, Torres-Peraza JF, Bosch M, Martin-Ibanez R, et al. (2004) Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J Neurosci 24: 7727-7739.
50. Gharami K, Xie Y, An JJ, Tonegawa S, Xu B, (2008) Brain-derived neurotrophic factor over-expression in the forebrain ameliorates Huntington's disease phenotypes in mice. J Neurochem 105: 369-379.
51. Du G, Liu X, Chen X, Song M, Yan Y, et al. (2010) Drosophila histone deacetylase 6 protects dopaminergic neurons against {alpha}-synuclein toxicity by promoting inclusion formation. Mol Biol Cell 21: 2128-2137.
52. Pandey UB, Batlevi Y, Baehrecke EH, Taylor JP, (2007) HDAC6 at the intersection of autophagy, the ubiquitin-proteasome system and neurodegeneration. Autophagy 3: 643-645.
53. Ding H, Dolan PJ, Johnson GV, (2008) Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem 106: 2119-2130.
54. Benn CL, Butler R, Mariner L, Nixon J, Moffitt H, et al. (2009) Genetic knock-down of HDAC7 does not ameliorate disease pathogenesis in the R6/2 mouse model of Huntington's disease. PLoS One 4: e5747.
55. Hockly E, Woodman B, Mahal A, Lewis CM, Bates G, (2003) Standardization and statistical approaches to therapeutic trials in the R6/2 mouse. Brain Res Bull 61: 469-479.
56. Hockly E, Tse J, Barker AL, Moolman DL, Beunard JL, et al. (2006) Evaluation of the benzothiazole aggregation inhibitors riluzole and PGL-135 as therapeutics for Huntington's disease. Neurobiol Dis 21: 228-236.
57. Sathasivam K, Woodman B, Mahal A, Bertaux F, Wanker EE, et al. (2001) Centrosome disorganization in fibroblast cultures derived from R6/2 Huntington's disease (HD) transgenic mice and HD patients. Hum Mol Genet 10: 2425-2435.
58. Ko J, Ou S, Patterson PH, (2001) New anti-huntingtin monoclonal antibodies: implications for huntingtin conformation and its binding proteins. Brain Research Bulletin 56: 319-329.
59. Weiss A, Roscic A, Paganetti P, (2009) Inducible mutant huntingtin expression in HN10 cells reproduces Huntington's disease-like neuronal dysfunction. Mol Neurodegener 4: 11.
60. Weiss A, Abramowski D, Bibel M, Bodner R, Chopra V, et al. (2009) Single-step detection of mutant huntingtin in animal and human tissues: a bioassay for Huntington's disease. Anal Biochem 395: 8-15.
61. Szapacs ME, Mathews TA, Tessarollo L, Ernest Lyons W, Mamounas LA, et al. (2004) Exploring the relationship between serotonin and brain-derived neurotrophic factor: analysis of BDNF protein and extraneuronal 5-HT in mice with reduced serotonin transporter or BDNF expression. Journal of Neuroscience Methods 140: 81-92.
62. Benn CL, Fox H, Bates GP, (2008) Optimisation of region-specific reference gene selection and relative gene expression analysis methods for pre-clinical trials of Huntington's disease. Mol Neurodegener 3: 17.