Genomic and proteomic analyses of prdm5 reveal interactions with insulator binding proteins in embryonic stem cells

Molecular and Cellular Biology

Volumn 33, Issue 22, 2013, Pages 4504-4516

  Galli, Giorgio Giacomo ^a,d,e   Carrara, Matteo ^b   Francavilla, Chiara ^c   de Lichtenberg, Kristian Honnens ^a   Olsen, Jesper Velgaard ^c   Calogero, Raffaele Adolfo ^b   Lund, Anders Henrik ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COHESIN; HISTONE METHYLTRANSFERASE; PRDM5 PROTEIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SEQUENCE; GENE TARGETING; GENOME ANALYSIS; GENOMICS; INSULATOR ELEMENT; KARYOTYPING; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEOMICS; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; MICE; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEOMICS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS, TFIII;

EID: 84887006823     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00545-13     Document Type: Article

References (60)

1. Fog CK, Galli GG, Lund AH. 2012. PRDM proteins: important players in differentiation and disease. Bioessays 34:50-60.
2. Huang S. 2002. Histone methyltransferases, diet nutrients and tumour suppressors. Nat. Rev. Cancer 2:469-476.
3. Hayashi K, Yoshida K, Matsui Y. 2005. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374-378.
4. Eom GH, Kim K, Kim SM, Kee HJ, Kim JY, Jin HM, Kim JR, Kim JH, Choe N, Kim KB, Lee J, Kook H, Kim N, Seo SB. 2009. Histone methyltransferase PRDM8 regulates mouse testis steroidogenesis. Biochem. Biophys. Res. Commun. 388:131-136.
5. Kim KC, Geng L, Huang S. 2003. Inactivation of a histone methyltransferase by mutations in human cancers. Cancer Res. 63:7619-7623.
6. Huang S, Shao G, Liu L. 1998. The PR domain of the Rb-binding zinc finger protein RIZ1 is a protein binding interface and is related to the SET domain functioning in chromatin-mediated gene expression. J. Biol. Chem. 273:15933-15939.
7. Fumasoni I, Meani N, Rambaldi D, Scafetta G, Alcalay M, Ciccarelli FD. 2007. Family expansion and gene rearrangements contributed to the functional specialization of PRDM genes in vertebrates. BMC Evol. Biol. 7:187.
8. Kinameri E, Inoue T, Aruga J, Imayoshi I, Kageyama R, Shimogori T, Moore AW. 2008. Prdm proto-oncogene transcription factor family expression and interaction with the Notch-Hes pathway in mouse neurogenesis. PLoS One 3:e3859.
9. Chia NY, Chan YS, Feng B, Lu X, Orlov YL, Moreau D, Kumar P, Yang L, Jiang J, Lau MS, Huss M, Soh BS, Kraus P, Li P, Lufkin T, Lim B, Clarke ND, Bard F, Ng HH. 2010. A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature 468:316- 320.
10. Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J. 2011. Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18:120-127.
11. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM. 2008. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454:961-967.
12. Chuikov S, Levi BP, Smith ML, Morrison SJ. 2010. Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat. Cell Biol. 12:999-1006.
13. Zhang Y, Stehling-Sun S, Lezon-Geyda K, Juneja SC, Coillard L, Chatterjee G, Wuertzer CA, Camargo F, Perkins AS. 2011. PR-domaincontaining Mds1-Evi1 is critical for long-term hematopoietic stem cell function. Blood 118:3853-3861.
14. Deng Q, Huang S. 2004. PRDM5 is silenced in human cancers and has growth suppressive activities. Oncogene 23:4903-4910.
15. Shu XS, Geng H, Li L, Ying J, Ma C, Wang Y, Poon FF, Wang X, Ying Y, Yeo W, Srivastava G, Tsao SW, Yu J, Sung JJ, Huang S, Chan AT, Tao Q. 2011. The epigenetic modifier PRDM5 functions as a tumor suppressor through modulating WNT/beta-catenin signaling and is frequently silenced in multiple tumors. PLoS One 6:e27346.
16. Watanabe Y, Kim HS, Castoro RJ, Chung W, Estecio MR, Kondo K, Guo Y, Ahmed SS, Toyota M, Itoh F, Suk KT, Cho MY, Shen L, Jelinek J, Issa JP. 2009. Sensitive and specific detection of early gastric cancer with DNA methylation analysis of gastric washes. Gastroenterology 136:2149- 2158.
17. Watanabe Y, Toyota M, Kondo Y, Suzuki H, Imai T, Ohe-Toyota M, Maruyama R, Nojima M, Sasaki Y, Sekido Y, Hiratsuka H, Shinomura Y, Imai K, Itoh F, Tokino T. 2007. PRDM5 identified as a target of epigenetic silencing in colorectal and gastric cancer. Clin. Cancer Res. 13:4786-4794.
18. Meani N, Pezzimenti F, Deflorian G, Mione M, Alcalay M. 2009. The tumor suppressor PRDM5 regulates Wnt signaling at early stages of zebrafish development. PLoS One 4:e4273.
19. Galli GG, de Lichtenberg KH, Carrara M, Hans W, Wuelling M, Mentz B, Multhaupt HA, Fog CK, Jensen KT, Rappsilber J, Vortkamp A, Coulton L, Fuchs H, Gailus-Durner V, Hrabe de Angelis M, Calogero RA, Couchman JR, Lund AH. 2012. Prdm5 regulates collagen gene transcription by association with RNA polymerase II in developing bone. PLoS Genet. 8:e1002711.
20. Burkitt Wright EM, Spencer HL, Daly SB, Manson FD, Zeef LA, Urquhart J, Zoppi N, Bonshek R, Tosounidis I, Mohan M, Madden C, Dodds A, Chandler KE, Banka S, Au L, Clayton-Smith J, Khan N, Biesecker LG, Wilson M, Rohrbach M, Colombi M, Giunta C, Black GC. 2011. Mutations in PRDM5 in brittle cornea syndrome identify a pathway regulating extracellular matrix development and maintenance. Am. J. Hum. Genet. 88:767-777.
21. Duan Z, Person RE, Lee HH, Huang S, Donadieu J, Badolato R, Grimes HL, Papayannopoulou T, Horwitz MS. 2007. Epigenetic regulation of protein-coding and microRNA genes by the Gfi1-interacting tumor suppressor PRDM5. Mol. Cell. Biol. 27:6889-6902.
22. Gondor A, Ohlsson R. 2009. Chromosome crosstalk in three dimensions. Nature 461:212-217.
23. Dillon N. 2006. Gene regulation and large-scale chromatin organization in the nucleus. Chromosome Res. 14:117-126.
24. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B. 2008. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948-951.
25. Phillips JE, Corces VG. 2009. CTCF: master weaver of the genome. Cell 137:1194-1211.
26. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM. 2008. Cohesin mediates transcriptional insulation by CCCTCbinding factor. Nature 451:796-801.
27. Handoko L, Xu H, Li G, Ngan CY, Chew E, Schnapp M, Lee CW, Ye C, Ping JL, Mulawadi F, Wong E, Sheng J, Zhang Y, Poh T, Chan CS, Kunarso G, Shahab A, Bourque G, Cacheux-Rataboul V, Sung WK, Ruan Y, Wei CL. 2011. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet. 43:630-638.
28. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K. 2009. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 19:24-32.
29. Moqtaderi Z, Wang J, Raha D, White RJ, Snyder M, Weng Z, Struhl K. 2010. Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat. Struct. Mol. Biol. 17:635- 640.
30. Moqtaderi Z, Struhl K. 2004. Genome-wide occupancy profile of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Mol. Cell. Biol. 24:4118-4127.
31. Carriere L, Graziani S, Alibert O, Ghavi-Helm Y, Boussouar F, Humbertclaude H, Jounier S, Aude JC, Keime C, Murvai J, Foglio M, Gut M, Gut I, Lathrop M, Soutourina J, Gerard M, Werner M. 2012. Genomic binding of Pol III transcription machinery and relationship with TFIIS transcription factor distribution in mouse embryonic stem cells. Nucleic Acids Res. 40:270-283.
32. Oler AJ, Alla RK, Roberts DN, Wong A, Hollenhorst PC, Chandler KJ, Cassiday PA, Nelson CA, Hagedorn CH, Graves BJ, Cairns BR. 2010. Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat. Struct. Mol. Biol. 17:620-628.
33. Raab JR, Chiu J, Zhu J, Katzman S, Kurukuti S, Wade PA, Haussler D, Kamakaka RT. 2012. Human tRNA genes function as chromatin insulators. EMBO J. 31:330-350.
34. Bryja V, Bonilla S, Arenas E. 2006. Derivation of mouse embryonic stem cells. Nat. Protoc. 1:2082-2087.
35. Lundby A, Olsen JV. 2011. GeLCMS for in-depth protein characterization and advanced analysis of proteomes. Methods Mol. Biol. 753:143- 155.
36. Kelstrup CD, Young C, Lavallee R, Nielsen ML, Olsen JV. 2012. Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole orbitrap mass spectrometer. J. Proteome Res. [Epub ahead of print.]
37. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. 2011. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10:1794-1805.
38. Hubner NC, Mann M. 2011. Extracting gene function from proteinprotein interactions using quantitative BAC interactomics (QUBIC). Methods 53:453-459.
39. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, Hyman A, Mann M. 2010. Quantitative proteomics combined with BAC transgeneomics reveals in vivo protein interactions. J. Cell Biol. 189:739- 754.
40. Kim D, Salzberg SL. 2011. TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol. 12:R72.
41. Roberts A, Pimentel H, Trapnell C, Pachter L. 2011. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 27:2325-2329.
42. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7:562-578.
43. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80.
44. ENCODE Project Consortium. 2011. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9:e1001046.
45. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:430-435.
46. 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 Res. 39:e35.
47. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, Green RD, Zhang MQ, Lobanenkov VV, Ren B. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128: 1231-1245.
48. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28:495-501.
49. Pasini D, Bracken AP, Hansen JB, Capillo M, Helin K. 2007. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27:3769-3779.
50. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C, Shimotohno K, Ishikawa F, Li E, Ueda HR, Nakayama J, Okano M. 2006. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11:805-814.
51. Donze D. 2012. Extra-transcriptional functions of RNA polymerase III complexes: TFIIIC as a potential global chromatin bookmark. Gene 493: 169-175.
52. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M. 2008. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40:1016- 1022.
53. Fraser P, Bickmore W. 2007. Nuclear organization of the genome and the potential for gene regulation. Nature 447:413-417.
54. Xu N, Tsai CL, Lee JT. 2006. Transient homologous chromosome pairing marks the onset of X inactivation. Science 311:1149-1152.
55. Chaumeil J, Le Baccon P, Wutz A, Heard E. 2006. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev. 20:2223-2237.
56. Bell AC, Felsenfeld G. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482-485.
57. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, Woodfine K, Krueger C, Reik W, Peters JM, Murrell A. 2009. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet 5:e1000739.
58. White RJ. 2011. Transcription by RNA polymerase III: more complex than we thought. Nat. Rev. Genet. 12:459-463.
59. Losada A, Hirano T. 2005. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19:1269-1287.
60. Galli GG, Multhaupt HA, Carrara M, de Lichtenberg KH, Christensen IB, Linnemann D, Santoni-Rugiu E, Calogero RA, Lund AH. 22 July 2013. Prdm5 suppresses ApcMin-driven intestinal adenomas and regulates monoacylglycerol lipase expression. Oncogene.