Wiz binds active promoters and CTCF-binding sites and is required for normal behaviour in the mouse

eLife

Volumn 5, Issue JULY, 2016, Pages

  Isbel, Luke ^a   Prokopuk, Lexie ^a,c   Wu, Haoyu ^b   Daxinger, Lucia ^a,b   Oey, Harald ^a,d   Spurling, Alex ^a   Lawther, Adam J ^a   Hale, Matthew W ^a   Whitelaw, Emma ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CTCF; CTCF PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN; PROTEIN BINDING; WIZ PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; MALE; MASS SPECTROMETRY; NONHUMAN; POLYMERASE CHAIN REACTION; PROBABILITY; RNA EXTRACTION; SEQUENCE ANALYSIS; TELEMETRY; VALIDATION PROCESS; WESTERN BLOTTING; ANIMAL; ANIMAL BEHAVIOR; CEREBELLUM; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; PROMOTER REGION;

ANIMALS; BEHAVIOR, ANIMAL; BINDING SITES; CCCTC-BINDING FACTOR; CEREBELLUM; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA;

EID: 84983036023     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15082     Document Type: Article

References (59)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11: R106. doi: 10.1186/gb-2010-11-10-r106
2. Anders S, Pyl PT, Huber W. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169. doi: 10.1093/bioinformatics/btu638
3. Balemans MC, Huibers MM, Eikelenboom NW, Kuipers AJ, van Summeren RC, Pijpers MM, Tachibana M, Shinkai Y, van Bokhoven H, Van der Zee CE. 2010. Reduced exploration, increased anxiety, and altered social behavior: Autistic-like features of euchromatin histone methyltransferase 1 heterozygous knockout mice. Behavioural Brain Research 208: 47-55. doi: 10.1016/j.bbr.2009.11.008
4. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837. doi: 10.1016/j.cell.2007.05.009
5. Bell AC, West AG, Felsenfeld G. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98: 387-396. doi: 10.1016/S0092-8674(00)81967-4
6. Bian C, Chen Q, Yu X. 2015. The zinc finger proteins ZNF644 and WIZ regulate the G9a/GLP complex for gene repression. eLife 4: e05606. doi: 10.7554/eLife.05606
7. Blewitt ME, Vickaryous NK, Hemley SJ, Ashe A, Bruxner TJ, Preis JI, Arkell R, Whitelaw E. 2005. An N-ethyl-N-nitrosourea screen for genes involved in variegation in the mouse. PNAS 102: 7629-7634. doi: 10.1073/pnas.0409375102
8. Boyle AL, Ward DC. 1992. Isolation and initial characterization of a large repeat sequence element specific to mouse chromosome 8. Genomics 12: 517-525. doi: 10.1016/0888-7543(92)90443-V
9. Chaturvedi C-P, Hosey AM, Palii C, Perez-Iratxeta C, Nakatani Y, Ranish JA, Dilworth FJ, Brand M. 2009. Dual role for the methyltransferase G9a in the maintenance of -globin gene transcription in adult erythroid cells. PNAS 106: 18303-18308. doi: 10.1073/pnas.0906769106
10. Cléard F, Spierer P. 2001. Position-effect variegation in Drosophila: The modifier Su(var)3-7 is a modular DNA-binding protein. EMBO Reports 2: 1095-1100. doi: 10.1093/embo-reports/kve243
11. Daxinger L, Harten SK, Oey H, Epp T, Isbel L, Huang E, Whitelaw N, Apedaile A, Sorolla A, Yong J, Bharti V, Sutton J, Ashe A, Pang Z, Wallace N, Gerhardt DJ, Blewitt ME, Jeddeloh JA, Whitelaw E. 2013. An ENU mutagenesis screen identifies novel and known genes involved in epigenetic processes in the mouse. Genome Biology 14: R96. doi: 10.1186/gb-2013-14-9-r96
12. Duhl DMJ, Vrieling H, Miller KA, Wolff GL, Barsh GS. 1994. Neomorphic agouti mutations in obese yellow mice. Nature Genetics 8: 59-65. doi: 10.1038/ng0994-59
13. Fodor BD, Shukeir N, Reuter G, Jenuwein T. 2010. Mammalian Su(var) genes in chromatin control. Annual Review of Cell and Developmental Biology 26: 471-501. doi: 10.1146/annurev.cellbio.042308.113225
14. Guo Y, Xu Q, Canzio D, Shou J, Li J, Gorkin DU, Jung I, Wu H, Zhai Y, Tang Y, Lu Y, Wu Y, Jia Z, Li W, Zhang MQ, Ren B, Krainer AR, Maniatis T, Wu Q. 2015. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162: 900-910. doi: 10.1016/j.cell.2015.07.038
15. Harten SK, Oey H, Bourke LM, Bharti V, Isbel L, Daxinger L, Faou P, Robertson N, Matthews JM, Whitelaw E. 2015. The recently identified modifier of murine metastable epialleles, Rearranged L-Myc Fusion, is involved in maintaining epigenetic marks at CpG island shores and enhancers. BMC Biology 13: 21. doi: 10.1186/s12915-015-0128-2
16. Henikoff S. 1990. Position-effect variegation after 60 years. Trends in Genetics 6: 422-426. doi: 10.1016/0168-9525(90)90304-O
17. Hirayama T, Tarusawa E, Yoshimura Y, Galjart N, Yagi T. 2012. CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Reports 2: 345-357. doi: 10.1016/j.celrep.2012.06.014
18. Isbel L, Srivastava R, Oey H, Spurling A, Daxinger L, Puthalakath H, Whitelaw E. 2015. Trim33 binds and silences a class of young endogenous retroviruses in the mouse testis; a novel component of the arms race between retrotransposons and the host genome. PLoS Genetics 11: e1005693. doi: 10.1371/journal.pgen.1005693
19. Jenuwein T, Laible G, Dorn R, Reuter G. 1998. SET domain proteins modulate chromatin domains in eu- and heterochromatin. Cellular and Molecular Life Sciences 54: 80-93. doi: 10.1007/s000180050127
20. Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, Roskin KM, Schwartz M, Sugnet CW, Thomas DJ, Weber RJ, Haussler D, Kent WJ, University of California Santa Cruz. 2003. The UCSC genome browser database. Nucleic Acids Research 31: 51-54. doi: 10.1093/nar/gkg129
21. Kawaguchi M, Toyama T, Kaneko R, Hirayama T, Kawamura Y, Yagi T. 2008. Relationship between DNA methylation states and transcription of individual isoforms encoded by the protocadherin-alpha gene cluster. Journal of Biological Chemistry 283: 12064-12075. doi: 10.1074/jbc.M709648200
22. Kleefstra T, Brunner HG, Amiel J, Oudakker AR, Nillesen WM, Magee A, Geneviève D, Cormier-Daire V, van Esch H, Fryns JP, Hamel BC, Sistermans EA, de Vries BB, van Bokhoven H. 2006. Loss-of-function mutations in euchromatin histone methyl transferase 1 (EHMT1) cause the 9q34 subtelomeric deletion syndrome. The American Journal of Human Genetics 79: 370-377. doi: 10.1086/505693
23. Kohmura N, Senzaki K, Hamada S, Kai N, Yasuda R, Watanabe M, Ishii H, Yasuda M, Mishina M, Yagi T. 1998. Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20: 1137-1151. doi: 10.1016/S0896-6273(00)80495-X
24. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with bowtie 2. Nature Methods 9: 357-359. doi: 10.1038/nmeth.1923
25. Lee DY, Northrop JP, Kuo MH, Stallcup MR. 2006. Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors. Journal of Biological Chemistry 281: 8476-8485. doi: 10.1074/jbc.M511093200
26. Lipkin SM, Näär AM, Kalla KA, Sack RA, Rosenfeld MG. 1993. Identification of a novel zinc finger protein binding a conserved element critical for Pit-1-dependent growth hormone gene expression. Genes & Development 7: 1674-1687. doi: 10.1101/gad.7.9.1674
27. Ma XS, Chao SB, Huang XJ, Lin F, Qin L, Wang XG, Meng TG, Zhu CC, Schatten H, Liu HL, Sun QY. 2015. The dynamics and regulatory mechanism of pronuclear H3k9me2 asymmetry in mouse zygotes. Scientific Reports 5: 17924. doi: 10.1038/srep17924
28. Machanick P, Bailey TL. 2011. MEME-ChIP: Motif analysis of large DNA datasets. Bioinformatics 27: 1696-1697. doi: 10.1093/bioinformatics/btr189
29. Matsumoto K, Ishii N, Yoshida S, Shiosaka S, Wanaka A, Tohyama M. 1998. Molecular cloning and distinct developmental expression pattern of spliced forms of a novel zinc finger gene wiz in the mouse cerebellum. Molecular Brain Research 61: 179-189. doi: 10.1016/S0169-328X(98)00216-2
30. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. 1999. Epigenetic inheritance at the agouti locus in the mouse. Nature Genetics 23: 314-318. doi: 10.1038/15490
31. Mulligan P, Westbrook TF, Ottinger M, Pavlova N, Chang B, Macia E, Shi YJ, Barretina J, Liu J, Howley PM, Elledge SJ, Shi Y. 2008. CDYL bridges REST and histone methyltransferases for gene repression and suppression of cellular transformation. Molecular Cell 32: 718-726. doi: 10.1016/j.molcel.2008.10.025
32. Oh ST, Kim KB, Chae YC, Kang JY, Hahn Y, Seo SB. 2014. H3K9 histone methyltransferase G9a-mediated transcriptional activation of p21. FEBS Letters 588: 685-691. doi: 10.1016/j.febslet.2014.01.039
33. Ong CT, Corces VG. 2014. CTCF: An architectural protein bridging genome topology and function. Nature Reviews Genetics 15: 234-246. doi: 10.1038/nrg3663
34. Petersen CC. 2007. The functional organization of the barrel cortex. Neuron 56: 339-355. doi: 10.1016/j.neuron.2007.09.017
35. Pugacheva EM, Rivero-Hinojosa S, Espinoza CA, Méndez-Catalá CF, Kang S, Suzuki T, Kosaka-Suzuki N, Robinson S, Nagarajan V, Ye Z, Boukaba A, Rasko JE, Strunnikov AV, Loukinov D, Ren B, Lobanenkov VV. 2015. Comparative analyses of CTCF and BORIS occupancies uncover two distinct classes of CTCF binding genomic regions. Genome Biology 16: 161. doi: 10.1186/s13059-015-0736-8
36. Purcell DJ, Jeong KW, Bittencourt D, Gerke DS, Stallcup MR. 2011. A distinct mechanism for coactivator versus corepressor function by histone methyltransferase G9a in transcriptional regulation. Journal of Biological Chemistry 286: 41963-41971. doi: 10.1074/jbc.M111.298463
37. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KVK, Whitelaw E. 2003. Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission. PNAS 100: 2538-2543. doi: 10.1073/pnas.0436776100
38. Rathert P, Dhayalan A, Murakami M, Zhang X, Tamas R, Jurkowska R, Komatsu Y, Shinkai Y, Cheng X, Jeltsch A. 2008. Protein lysine methyltransferase G9a acts on non-histone targets. Nature Chemical Biology 4: 344-346. doi: 10.1038/nchembio.88
39. Schuh R, Aicher W, Gaul U, Côte S, Preiss A, Maier D, Seifert E, Nauber U, Schröder C, Kemler R, Jäckle H. 1986. A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Krüppel, a Drosophila segmentation gene. Cell 47: 1025-1032. doi: 10.1016/0092-8674(86)90817-2
40. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, Ren B. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120. doi: 10.1038/nature11243
41. Simon JM, Parker JS, Liu F, Rothbart SB, Ait-Si-Ali S, Strahl BD, Jin J, Davis IJ, Mosley AL, Pattenden SG. 2015. A role for widely interspaced zinc finger (WIZ) in retention of the G9a methyltransferase on chromatin. Journal of Biological Chemistry 290: 26088-26102. doi: 10.1074/jbc.M115.654459
42. Tachibana M, Sugimoto K, Fukushima T, Shinkai Y. 2001. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. Journal of Biological Chemistry 276: 25309-25317. doi: 10.1074/jbc.M101914200
43. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y. 2002. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes & Development 16: 1779-1791. doi: 10.1101/gad.989402
44. Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, Iwanari H, Sakihama T, Kodama T, Hamakubo T, Shinkai Y. 2005. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes & Development 19: 815-826. doi: 10.1101/gad.1284005
45. Toyoda S, Kawaguchi M, Kobayashi T, Tarusawa E, Toyama T, Okano M, Oda M, Nakauchi H, Yoshimura Y, Sanbo M, Hirabayashi M, Hirayama T, Hirabayashi T, Yagi T. 2014. Developmental epigenetic modification regulates stochastic expression of clustered protocadherin genes, generating single neuron diversity. Neuron 82: 94-108. doi: 10.1016/j.neuron.2014.02.005
46. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111. doi: 10.1093/bioinformatics/btp120
47. Ueda J, Tachibana M, Ikura T, Shinkai Y. 2006. Zinc finger protein Wiz links G9a/GLP histone methyltransferases to the co-repressor molecule CtBP. Journal of Biological Chemistry 281: 20120-20128. doi: 10.1074/jbc.M603087200
48. Walf AA, Frye CA. 2007. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature Protocols 2: 322-328. doi: 10.1038/nprot.2007.44
49. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. 2009. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nature Genetics 41: 246-250. doi: 10.1038/ng.297
50. Wen B, Wu H, Loh YH, Briem E, Daley GQ, Feinberg AP. 2012. Euchromatin islands in large heterochromatin domains are enriched for CTCF binding and differentially DNA-methylated regions. BMC Genomics 13: 566. doi: 10.1186/1471-2164-13-566
51. Willemsen MH, Vulto-van Silfhout AT, Nillesen WM, Wissink-Lindhout WM, van Bokhoven H, Philip N, Berry-Kravis EM, Kini U, van Ravenswaaij-Arts CM, Delle Chiaie B, Innes AM, Houge G, Kosonen T, Cremer K, Fannemel M, Stray-Pedersen A, Reardon W, Ignatius J, Lachlan K, Mircher C, et al. 2012. Update on Kleefstra syndrome. Molecular Syndromology 2: 202-212. doi: 10.1159/000335648
52. Wu Q, Zhang T, Cheng JF, Kim Y, Grimwood J, Schmutz J, Dickson M, Noonan JP, Zhang MQ, Myers RM, Maniatis T. 2001. Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome Research 11: 389-404. doi: 10.1101/gr.167301
53. Wu Q, Maniatis T. 1999. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97: 779-790. doi: 10.1016/S0092-8674(00)80789-8
54. Xiao T, Wallace J, Felsenfeld G. 2011. Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Molecular and Cellular Biology 31: 2174-2183. doi: 10.1128/MCB.05093-11
55. Ye T, Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I, Tora L. 2011. seqMINER: An integrated ChIP-seq data interpretation platform. Nucleic Acids Research 39: e35. doi: 10.1093/nar/gkq1287
56. Yokota S, Hirayama T, Hirano K, Kaneko R, Toyoda S, Kawamura Y, Hirabayashi M, Hirabayashi T, Yagi T. 2011. Identification of the cluster control region for the protocadherin-beta genes located beyond the protocadherin-gamma cluster. Journal of Biological Chemistry 286: 31885-31895. doi: 10.1074/jbc.M111.245605
57. Yuan X, Feng W, Imhof A, Grummt I, Zhou Y. 2007. Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Molecular Cell 27: 585-595. doi: 10.1016/j.molcel.2007.06.021
58. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G. 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Molecular Cell 13: 291-298. doi: 10.1016/S1097-2765(04)00029-2
59. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biology 9: R137. doi: 10.1186/gb-2008-9-9-r137