Genome-wide histone acetylation is altered in a transgenic mouse model of Huntington's disease

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  McFarland, Karen N ^a,c   Das, Sudeshna ^a   Sun, Ting Ting ^a   Leyfer, Dmitri ^a,d   Xia, Eva ^a   Sangrey, Gavin R ^a   Kuhn, Alexandre ^b   Luthi Carter, Ruth ^b   Clark, Timothy W ^a   Sadri Vakili, Ghazaleh ^a   Cha, Jang Ho J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b EPFL   (Switzerland)

^c UNIVERSITY OF FLORIDA   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; HISTONE H3; PHENYLBUTYRATE; SPB 11; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFECT; FEMALE; GENE EXPRESSION; GENE INTERACTION; GENE LOCUS; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUNTINGTON CHOREA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION;

ACETYLATION; ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENETIC LOCI; GENOME; GENOME-WIDE ASSOCIATION STUDY; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUNTINGTON DISEASE; MALE; MICE; MICE, TRANSGENIC;

ANIMALIA; MUS; MUS MUSCULUS; RODENTIA;

EID: 84864409298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041423     Document Type: Article

References (56)

1. 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.
2. Bates G, Harper PS, Jones L,(2002) Huntington's Disease.
3. Cha JH,(2007) Transcriptional signatures in Huntington's disease. Prog Neurobiol 83: 228-248.
4. Stack EC, Del Signore SJ, Luthi-Carter R, Soh BY, Goldstein DR, et al.(2007) Modulation of nucleosome dynamics in Huntington's disease. Hum Mol Genet 16: 1164-1175.
5. Ryu H, Lee J, Hagerty SW, Soh BY, McAlpin SE, et al.(2006) ESET/SETDB1 gene expression and histone H3 (K9) trimethylation in Huntington's disease. Proc Natl Acad Sci U S A 103: 19176-19181.
6. Sadri-Vakili G, Bouzou B, Benn CL, Kim MO, Chawla P, et al.(2007) Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models. Hum Mol Genet 16: 1293-1306.
7. Kim MO, Chawla P, Overland RP, Xia E, Sadri-Vakili G, et al.(2008) Altered histone monoubiquitylation mediated by mutant huntingtin induces transcriptional dysregulation. J Neurosci 28: 3947-3957.
8. Igarashi S, Morita H, Bennett KM, Tanaka Y, Engelender S, et al.(2003) Inducible PC12 cell model of Huntington's disease shows toxicity and decreased histone acetylation. Neuroreport 14: 565-568.
9. Sadri-Vakili G, Cha JH,(2006) Mechanisms of disease: Histone modifications in Huntington's disease. Nat Clin Pract Neurol 2: 330-338.
10. Kouzarides T,(2007) Chromatin modifications and their function. Cell 128: 693-705.
11. Li B, Carey M, Workman JL,(2007) The role of chromatin during transcription. Cell 128: 707-719.
12. VG A, Faulkner R, Mirsky AE,(1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci U S A 51: 786-794.
13. Marushige K,(1976) Activation of chromatin by acetylation of histone side chains. Proc Natl Acad Sci U S A 73: 3937-3941.
14. Kazantsev AG,(2009) New therapeutic strategies for treatment of neurodegenerative diseases. Curr Pharm Des 15: 3917-3918.
15. Gottesfeld JM, Pandolfo M,(2009) Development of histone deacetylase inhibitors as therapeutics for neurological disease. Future Neurol 4: 775-784.
16. 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.
17. 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. Hum Mol Genet 16: 1845-1861.
18. Huang DW, Sherman BT, Lempicki RA,(2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
19. Koch CM, Andrews RM, Flicek P, Dillon SC, Karaoz U, et al.(2007) The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res 17: 691-707.
20. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, et al.(2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318.
21. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, et al.(2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903.
22. Roh TY, Cuddapah S, Cui K, Zhao K,(2006) The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci U S A 103: 15782-15787.
23. Roh TY, Cuddapah S, Zhao K,(2005) Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19: 542-552.
24. Benn CL, Sun T, Sadri-Vakili G, McFarland KN, DiRocco DP, et al.(2008) Huntingtin modulates transcription, occupies gene promoters in vivo, and binds directly to DNA in a polyglutamine-dependent manner. J Neurosci 28: 10720-10733.
25. Riggs MG, Whittaker RG, Neumann JR, Ingram VM,(1977) n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature 268: 462-464.
26. Vidali G, Boffa LC, Bradbury EM, Allfrey VG,(1978) Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci U S A 75: 2239-2243.
27. Vidali G, Boffa LC, Mann RS, Allfrey VG,(1978) Reversible effects of Na-butyrate on histone acetylation. Biochem Biophys Res Commun 82: 223-227.
28. Boffa LC, Vidali G, Mann RS, Allfrey VG,(1978) Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J Biol Chem 253: 3364-3366.
29. Ferrante RJ, Kubilus JK, Lee J, Ryu H, Beesen A, et al.(2003) Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J Neurosci 23: 9418-9427.
30. 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.
31. 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.
32. 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.
33. Gardian G, Browne SE, Choi DK, Klivenyi P, Gregorio J, et al.(2005) Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington's disease. J Biol Chem 280: 556-563.
34. Zadori D, Geisz A, Vamos E, Vecsei L, Klivenyi P,(2009) Valproate ameliorates the survival and the motor performance in a transgenic mouse model of Huntington's disease. Pharmacol Biochem Behav 94: 148-153.
35. Monti B, Gatta V, Piretti F, Raffaelli SS, Virgili M, et al.(2010) Valproic acid is neuroprotective in the rotenone rat model of Parkinson's disease: involvement of alpha-synuclein. Neurotox Res 17: 130-141.
36. Minamiyama M, Katsuno M, Adachi H, Waza M, Sang C, et al.(2004) Sodium butyrate ameliorates phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Hum Mol Genet 13: 1183-1192.
37. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, et al.(2010) Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35: 870-880.
38. Ricobaraza A, Cuadrado-Tejedor M, Perez-Mediavilla A, Frechilla D, Del Rio J, et al.(2009) Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 34: 1721-1732.
39. Ying M, Xu R, Wu X, Zhu H, Zhuang Y, et al.(2006) Sodium butyrate ameliorates histone hypoacetylation and neurodegenerative phenotypes in a mouse model for DRPLA. J Biol Chem 281: 12580-12586.
40. Ryu H, Smith K, Camelo SI, Carreras I, Lee J, et al.(2005) Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J Neurochem 93: 1087-1098.
41. Petri S, Kiaei M, Kipiani K, Chen J, Calingasan NY, et al.(2006) Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 22: 40-49.
42. Rai M, Soragni E, Jenssen K, Burnett R, Herman D, et al.(2008) HDAC inhibitors correct frataxin deficiency in a Friedreich ataxia mouse model. PLoS One 3: e1958.
43. Jenuwein T, Allis CD,(2001) Translating the histone code. Science 293: 1074-1080.
44. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, et al.(2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138: 1122-1136.
45. Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, et al.(2009) ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell 33: 248-256.
46. Saksouk N, Avvakumov N, Champagne KS, Hung T, Doyon Y, et al.(2009) HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol Cell 33: 257-265.
47. Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, et al.(2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131: 58-69.
48. Ou JN, Torrisani J, Unterberger A, Provencal N, Shikimi K, et al.(2007) Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochem Pharmacol 73: 1297-1307.
49. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, et al.(2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12: 829-838.
50. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, et al.(2002) HDAC6 is a microtubule-associated deacetylase. Nature 417: 455-458.
51. 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.
52. Jeong H, Then F, Melia TJJ, Mazzulli JR, Cui L, et al.(2009) Acetylation targets mutant huntingtin to autophagosomes for degradation. Cell 137: 60-72.
53. Braveman MW, Chen-Plotkin AS, Yohrling GJ, Cha JH,(2004) Chromatin immunoprecipitation technique for study of transcriptional dysregulation in intact mouse brain. Methods Mol Biol 277: 261-276.
54. Chen-Plotkin AS, Sadri-Vakili G, Yohrling GJ, Braveman MW, Benn CL, et al.(2006) Decreased association of the transcription factor Sp1 with genes downregulated in Huntington's disease. Neurobiol Dis 22: 233-241.
55. Tusher VG, Tibshirani R, Chu G,(2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
56. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics Methods and Protocols: Methods in Molecular Biology. Krawetz S, Misener S, editors. Totowa, NJ: Humana Press. pp. 365-386.