Genome-wide increase in histone H2A ubiquitylation in a mouse model of huntington’s disease

Journal of Huntington's Disease

Volumn 2, Issue 3, 2013, Pages 263-277

  McFarland, Karen N ^a,d   Das, Sudeshna ^a   Sun, Ting Ting ^a   Leyfer, Dmitri ^a,e   Kim, Mee Ohk ^a   Xia, Eva ^a   Sangrey, Gavin R ^a   Kuhn, Alexandre ^b   Luthi Carter, Ruth ^b,c   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 LEICESTER   (United Kingdom)

^d UNIVERSITY OF FLORIDA   (United States)

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

Author keywords

Histone ubiquitylation; Huntington s disease; R6 2 mouse; Transcriptional regulation

Indexed keywords

CHROMATIN CONJUGATE PROTEIN A24; HISTONE; TRANSCRIPTOME; UBIQUITIN;

ANIMAL; ARTICLE; BRAIN; CHROMATIN IMMUNOPRECIPITATION; DISEASE MODEL; DNA MICROARRAY; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; HISTONE UBIQUITINATION; HUNTINGTON CHOREA; METABOLISM; MOUSE; R6/2 MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTIONAL REGULATION; UBIQUITINATION;

HISTONE UBIQUITYLATION; HUNTINGTON'S DISEASE; R6/2 MOUSE; TRANSCRIPTIONAL REGULATION;

ANIMALS; BRAIN; CHROMATIN IMMUNOPRECIPITATION; DISEASE MODELS, ANIMAL; GENE SILENCING; HISTONES; HUNTINGTON DISEASE; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; UBIQUITINATION; UBIQUITINS;

EID: 84907220759     PISSN: 18796397     EISSN: 18796400     Source Type: Journal    
DOI: 10.3233/JHD-130066     Document Type: Article

References (35)

1. Cha JH. Transcriptional signatures in Huntington’s disease. Prog Neurobiol. 2007;83:228-48.
2. Goldknopf IL, Busch H. Isopeptide linkage between nonhistone and histone 2A polypeptides of chromosomal conjugate-protein A24. Proc Natl Acad Sci USA. 1977;74:864-8.
3. Goldknopf IL, Taylor CW, Baum RM, Yeoman LC, Olson MO, Prestayko AW, Busch H. Isolation and characterization of protein A24, a "histone-like" non-histone chromosomal protein. J Biol Chem. 1975;250:7182-7.
4. Nickel BE, Davie JR. Structure of polyubiquitinated histone H2A. Biochemistry. 1989;28:964-8.
5. Weake VM, Workman JL. Histone ubiquitination: Triggering gene activity. Mol Cell. 2008;29:653-63.
6. Cao R, Tsukada Y, Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell. 2005;20:845-54.
7. Wei J, Zhai L, Xu J, Wang H. Role of Bmi1 in H2A ubiquitylation and Hox gene silencing. J Biol Chem. 2006; 281:22537-44.
8. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature. 2004;431:873-8.
9. Zhou W, Zhu P, Wang J, Pascual G, Ohgi KA, Lozach J, Glass CK, Rosenfeld MG. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol Cell. 2008;29:69-80.
10. An JY, Kim EA, Jiang Y, Zakrzewska A, Kim DE, Lee MJ, Mook-Jung I, Zhang Y, Kwon YT. UBR2 mediates transcriptional silencing during spermatogenesis via histone ubiquitination. Proc Natl Acad Sci USA. 2010;107:1912-7.
11. Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JH, Grootegoed JA. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol. 1999;207:322-33.
12. de Napoles M, Mermoud JE, Wakao R, Tang YA, Endoh M, Appanah R, Nesterova TB, Silva J, Otte AP, Vidal M, Koseki H, Brockdorff N. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell. 2004;7:663-76.
13. Fang J, Chen T, Chadwick B, Li E, ZhangY. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem. 2004;279:52812-5.
14. Smith KP, Byron M, Clemson CM, Lawrence JB. Ubiquitinated proteins including uH2A on the human and mouse inactiveXchromosome: Enrichment in gene rich bands. Chromosoma. 2004;113:324-35.
15. Jason LJ, Finn RM, Lindsey G, Ausio J. Histone H2A ubiquitination does not preclude histone H1 binding, but it facilitates its association with the nucleosome. J Biol Chem. 2005;280:4975-82.
16. Zhu P, Zhou W, Wang J, Puc J, Ohgi KA, Erdjument-Bromage H, Tempst P, Glass CK, Rosenfeld MG. A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol Cell. 2007;27:609-21.
17. Sadri-Vakili G, Bouzou B, Benn CL, Kim MO, Chawla P, Overland RP, Glajch KE, Xia E, Qiu Z, Hersch SM, ClarkTW, Yohrling GJ, Cha JH. Histones associated with downregulated genes are hypo-acetylated in Huntington’s disease models. Hum Mol Genet. 2007;16:1293-306.
18. Kim MO, Chawla P, Overland RP, Xia E, Sadri-Vakili G, Cha JH. Altered histone monoubiquitylation mediated by mutant huntingtin induces transcriptional dysregulation. J Neurosci. 2008;28:3947-57.
19. Bett JS, Benn CL, Ryu KY, Kopito RR, Bates GP. The polyubiquitin Ubc gene modulates histone H2A monoubiquitylation in the R6/2 mouse model of Huntington’s disease. J Cell Mol Med. 2009;13:2645-57.
20. Kuhn A, Goldstein DR, Hodges A, Strand AD, Sengstag T, Kooperberg C, Becanovic K, Pouladi MA, Sathasivam K, Cha JH, Hannan AJ, Hayden MR, Leavitt BR, Dunnett SB, Ferrante RJ, Albin R, Shelbourne P, Delorenzi M, Augood SJ, Faull RL, Olson JM, Bates GP, Jones L, Luthi-Carter R. 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 wildtype huntingtin dosage. Hum Mol Genet. 2007;16:1845-61.
21. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 1996;87:493-506.
22. Braveman MW, Chen-Plotkin AS, Yohrling GJ, Cha JH. Chromatin immunoprecipitation technique for study of transcriptional dysregulation in intact mouse brain. Methods Mol Biol. 2004;277:261-76.
23. Chen-Plotkin AS, Sadri-Vakili G, Yohrling GJ, Braveman MW, Benn CL, Glajch KE, DiRocco DP, Farrell LA, Krainc D, Gines S, MacDonald ME, Cha JH. Decreased association of the transcription factor Sp1 with genes downregulated in Huntington’s disease. Neurobiol Dis. 2006;22: 233-41.
24. McFarland KN, Das S, Sun TT, Leyfer D, Xia E, Sangrey GR, Kuhn A, Luthi-Carter R, Clark TW, Sadri-Vakili G, Cha JH. Genome-Wide Histone Acetylation Is Altered in a Transgenic Mouse Model of Huntington’s Disease. PLoS One. 2012;7:e41423.
25. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
26. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37: 1-3.
27. Kallin EM, Cao R, Jothi R, Xia K, Cui K, Zhao K, Zhang Y. Genome-wide uH2A localization analysis highlights Bmi1- dependent deposition of the mark at repressed genes. PLoS Genet. 2009;5:e1000506.
28. Zhou W, Wang X, Rosenfeld MG. HistoneH2Aubiquitination in transcriptional regulation and DNA damage repair. Int J Biochem Cell Biol. 2009;41:12-5.
29. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403:41-5.
30. Ogawa H, Ishiguro K, Gaubatz S, Livingston DM, Nakatani Y. A complex with chromatin modifiers that occupies E2F and Myc-responsive genes in G0 cells. Science. 2002;296: 1132-6.
31. Joo HY, Zhai L, Yang C, Nie S, Erdjument-Bromage H, Tempst P, Chang C, Wang H. Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature. 2007;449:1068-72.
32. Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapic-Otrin V, Levine AS. The DDB1-CUL4ADDB2 ubiq uitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A atUV-damagedDNAsites. Proc Natl Acad Sci USA. 2006;103:2588-93.
33. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell. 2007;131:887-900.
34. Bergink S, Salomons FA, Hoogstraten D, Groothuis TA, de Waard H, Wu J, Yuan L, Citterio E, Houtsmuller AB, Neefjes J, Hoeijmakers JH, VermeulenW, Dantuma NP. DNAdamage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 2006;20:1343-52.
35. Illuzzi J, Yerkes S, Parekh-Olmedo H, Kmiec EB. DNA breakage and induction of DNA damage response proteins precede the appearance of visible mutant huntingtin aggregates. J Neurosci Res. 2009;87:733-47.