HSA21 Single-minded 2 (SIM2) binding sites co-localize with super-enhancers and pioneer transcription factors in pluripotent mouse ES cells

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Letourneau, Audrey ^a   Cobellis, Gilda ^b   Fort, Alexandre ^c   Santoni, Federico ^a   Garieri, Marco ^a   Falconnet, Emilie ^a   Ribaux, Pascale ^a   Vannier, Anne ^a,d   Guipponi, Michel ^a,d   Carninci, Piero ^c   Borel, Christelle ^a   Antonarakis, Stylianos E ^a,d,e  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c RIKEN   (Japan)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e Institute of Genetics and Genomics of Geneva (iGE3)   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HSA21; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SIM2; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA; SIM2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DNA MODIFICATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE LOCUS; GENE ONTOLOGY; GENE REGULATORY NETWORK; GENE TARGETING; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; ENHANCER REGION; GENETICS; METABOLISM; PROCEDURES; SEQUENCE ANALYSIS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DNA; ENHANCER ELEMENTS, GENETIC; MICE; MOUSE EMBRYONIC STEM CELLS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION FACTORS;

EID: 84957562741     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126475     Document Type: Article

References (63)

1. Antonarakis SE, Lyle R, Dermitzakis ET, Reymond A, Deutsch S. Chromosome 21 and down syndrome: from genomics to pathophysiology. Nat Rev Genet. 2004;5(10):725-38. PMID: 15510164
2. Gardiner K. Transcriptional dysregulation in Down syndrome: predictions for altered protein complex stoichiometries and post-translational modifications, and consequences for learning/behavior genes ELK, CREB, and the estrogen and glucocorticoid receptors. Behav Genet. 2006;36(3):439-53. PMID: 16502135
3. Kewley RJ, Whitelaw ML, Chapman-Smith A. The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int J Biochem Cell Biol. 2004;36(2):189-204. PMID: 14643885
4. Crews ST. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 1998;12(5):607-20. PMID: 9499397
5. Panda S, Hogenesch JB, Kay SA. Circadian rhythms from flies to human. Nature. 2002;417(6886):329-35. PMID: 12015613
6. Thomas JB, Crews ST, Goodman CS. Molecular genetics of the single-minded locus: a gene involved in the development of the Drosophila nervous system. Cell. 1988;52(1):133-41. PMID: 3345559
7. Nambu JR, Franks RG, Hu S, Crews ST. The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell. 1990;63(1):63-75. PMID: 2242162
8. Nambu JR, Lewis JO, Wharton KA Jr, Crews ST. The Drosophila single-minded gene encodes a helixloophelix protein that acts as a master regulator of CNS midline development. Cell. 1991;67(6):1157-67. PMID: 1760843
9. Xiao H, Hrdlicka LA, Nambu JR. Alternate functions of the single-minded and rhomboid genes in development of the Drosophila ventral neuroectoderm. Mech Dev. 1996;58(1-2):65-74. PMID: 8887324
10. Estes P, Mosher J, Crews ST. Drosophila single-minded represses gene transcription by activating the expression of repressive factors. Dev Biol. 2001;232(1):157-75. PMID: 11254355
11. Sonnenfeld M, Ward M, Nystrom G, Mosher J, Stahl S, Crews S. The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development. 1997;124(22):4571-82. PMID: 9409674
12. Ema M, Suzuki M, Morita M, Hirose K, Sogawa K, Matsuda Y, et al. cDNA cloning of a murine homologue of Drosophila single-minded, its mRNA expression in mouse development, and chromosome localization. Biochem Biophys Res Commun. 1996;218(2):588-94. PMID: 8561800
13. Yamaki A, Noda S, Kudoh J, Shindoh N, Maeda H, Minoshima S, et al. The mammalian single-minded (SIM) gene: mouse cDNA structure and diencephalic expression indicate a candidate gene for Down syndrome. Genomics. 1996;35(1):136-43. PMID: 8661114
14. Moffett P, Dayo M, Reece M, McCormick MK, Pelletier J. Characterization of msim, a murine homologue of the Drosophila sim transcription factor. Genomics. 1996;35(1):144-55. PMID: 8661115
15. Dahmane N, Charron G, Lopes C, Yaspo ML, Maunoury C, Decorte L, et al. Down syndrome-critical region contains a gene homologous to Drosophila sim expressed during rat and human central nervous system development. Proc Natl Acad Sci USA. 1995;92(20):9191-5. PMID: 7568099
16. Chrast R, Scott HS, Chen H, Kudoh J, Rossier C, Minoshima S, et al. Cloning of two human homologs of the Drosophila single-minded gene SIM1 on chromosome 6q and SIM2 on 21q within the Down syndrome chromosomal region. Genome Res. 1997;7(6):615-24. PMID: 9199934
17. Fan CM, Kuwana E, Bulfone A, Fletcher CF, Copeland NG, Jenkins NA, et al. "Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down syndrome.". Mol Cell Neurosci. 1996;7(6):519. PMID: 8875433
18. Rachidi M, Lopes C, Charron G, Delezoide AL, Paly E, Bloch B, et al. Spatial and temporal localization during embryonic and fetal human development of the transcription factor SIM2 in brain regions altered in Down syndrome. Int J Dev Neurosci. 2005;23(5):475-84. PMID: 15946822
19. Ema M, Ikegami S, Hosoya T, Mimura J, Ohtani H, Nakao K, et al. Mild impairment of learning and memory in mice overexpressing the mSim2 gene located on chromosome 16: an animal model of Down's syndrome. Hum Mol Genet. 1999;8(8):1409-15. PMID: 10400987
20. Chrast R, Scott HS, Madani R, Huber L, Wolfer DP, Prinz M, et al. Mice trisomic for a bacterial artificial chromosome with the single-minded 2 gene (Sim2) show phenotypes similar to some of those present in the partial trisomy 16 mouse models of Down syndrome. Hum Mol Genet. 2000;9(12):1853-64. PMID: 10915774
21. Meng X, Peng B, Shi J, Zheng Y, Chen H, Zhang J, et al. Effects of overexpression of Sim2 on spatial memory and expression of synapsin I in rat hippocampus. Cell Biol Int. 2006;30(10):841-7. PMID: 16963290
22. Goshu E, Jin H, Fasnacht R, Sepenski M, Michaud JL, Fan CM. Sim2 mutants have developmental defects not overlapping with those of Sim1 mutants. Mol Cell Biol. 2002;22(12):4147-57. PMID: 12024028
23. Shamblott MJ, Bugg EM, Lawler AM, Gearhart JD. Craniofacial abnormalities resulting from targeted disruption of the murine Sim2 gene. Dev Dyn. 2002;224(4):373-80. PMID: 12203729
24. De Cegli R, Romito A, Iacobacci S, Mao L, Lauria M, Fedele AO, et al. A mouse embryonic stem cell bank for inducible overexpression of human chromosome 21 genes. Genome Biol. 2010;11(6):R64. doi: 10.1186/gb-2010-11-6-r64 PMID: 20569505
25. Masui S, Shimosato D, Toyooka Y, Yagi R, Takahashi K, Niwa H. An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit. Nucleic acids research. 2005;33(4):e43. PMID: 15741176
26. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60. doi: 10.1093/bioinformatics/btp324 PMID: 19451168
27. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576-89. doi: 10.1016/j.molcel.2010.05.004 PMID: 20513432
28. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139-40. doi: 10.1093/bioinformatics/btp616 PMID: 19910308
29. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956
30. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research. 2009;37(1):1-13. doi: 10.1093/nar/gkn923 PMID: 19033363
31. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545-50. PMID: 16199517
32. Zhang Y, Wong CH, Birnbaum RY, Li G, Favaro R, Ngan CY, et al. Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations. Nature. 2013;504(7479):306-10. doi: 10.1038/nature12716 PMID: 24213634
33. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell. 2008;133(6):1106-17. doi: 10.1016/j. cell.2008.04.043 PMID: 18555785
34. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature. 2010;467(7314):430-5. doi: 10.1038/nature09380 PMID: 20720539
35. Santoni FA, Hartley O, Luban J. Deciphering the code for retroviral integration target site selection. PLoS Comput Biol. 2010;6(11):e1001008. doi: 10.1371/journal.pcbi.1001008 PMID: 21124862
36. Kwak H-I, Gustafson T, Metz RP, Laffin B, Schedin P, Porter WW. Inhibition of breast cancer growth and invasion by single-minded 2s. Carcinogenesis. 2007;28(2):259-66. PMID: 16840439
37. Aleman MJ, DeYoung MP, Tress M, Keating P, Perry GW, Narayanan R. Inhibition of Single Minded 2 gene expression mediates tumor-selective apoptosis and differentiation in human colon cancer cells. Proc Natl Acad Sci USA. 2005;102(36):12765-70. PMID: 16129820
38. Deyoung MP, Scheurle D, Damania H, Zylberberg C, Narayanan R. Down's syndrome-associated single minded gene as a novel tumor marker. Anticancer Res. 2002;22(6 A):3149-57. PMID: 12530058
39. He Q, Li G, Su Y, Shen J, Liu Q, Ma X, et al. Single minded 2-s (SIM2-s) gene is expressed in human GBM cells and involved in GBM invasion. Cancer Biol Ther. 2010;9(6):430-6. PMID: 20448453
40. Lu B, Asara JM, Sanda MG, Arredouani MS. The role of the transcription factor SIM2 in prostate cancer. PLoS One. 2011;6(12):e28837. doi: 10.1371/journal.pone.0028837 PMID: 22174909
41. Fullwood MJ, Han Y, Wei CL, Ruan X, Ruan Y. Chromatin interaction analysis using paired-end tag sequencing. Curr Protoc Mol Biol. 2010; Chapter 21:Unit 21 15 1-25.
42. Li G, Fullwood MJ, Xu H, Mulawadi FH, Velkov S, Vega V, et al. ChIA-PET tool for comprehensive chromatin interaction analysis with paired-end tag sequencing. Genome Biol. 2010;11(2):R22. doi: 10. 1186/gb-2010-11-2-r22 PMID: 20181287
43. Young RA. Control of the embryonic stem cell state. Cell. 2011;144(6):940-54. doi: 10.1016/j.cell. 2011.01.032 PMID: 21414485
44. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell. 2013;153(2):307-19. doi: 10. 1016/j.cell.2013.03.035 PMID: 23582322
45. Beby F, Lamonerie T. The homeobox gene Otx2 in development and disease. Exp Eye Res. 2013;111:9-16. doi: 10.1016/j.exer.2013.03.007 PMID: 23523800
46. Matsuo I, Kuratani S, Kimura C, Takeda N, Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 1995;9(21):2646-58. PMID: 7590242
47. Chassaing N, Sorrentino S, Davis EE, Martin-Coignard D, Iacovelli A, Paznekas W, et al. OTX2 mutations contribute to the otocephaly-dysgnathia complex. J Med Genet. 2012;49(6):373-9. doi: 10.1136/jmedgenet-2012-100892 PMID: 22577225
48. Schilter KF, Schneider A, Bardakjian T, Soucy JF, Tyler RC, Reis LM, et al. OTX2 microphthalmia syndrome: four novel mutations and delineation of a phenotype. Clin Genet. 2010;79(2):158-68.
49. Hoyer J, Ekici AB, Endele S, Popp B, Zweier C, Wiesener A, et al. Haploinsufficiency of ARID1B, a member of the SWI/SNF-a chromatin-remodeling complex, is a frequent cause of intellectual disability. Am J Hum Genet. 2012;90(3):565-72. doi: 10.1016/j.ajhg.2012.02.007 PMID: 22405089
50. Santen GW, Aten E, Sun Y, Almomani R, Gilissen C, Nielsen M, et al. Mutations in SWI/SNF chromatin remodeling complex gene ARID1B cause Coffin-Siris syndrome. Nat Genet. 2012;44(4):379-80. doi: 10.1038/ng.2217 PMID: 22426309
51. Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y, Hibi-Ko Y, et al. Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat Genet. 2012;44(4):376-8. doi: 10.1038/ng. 2219 PMID: 22426308
52. Janz R, Sudhof TC, Hammer RE, Unni V, Siegelbaum SA, Bolshakov VY. Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron. 1999;24(3):687-700. PMID: 10595519
53. Ma Y, Certel K, Gao Y, Niemitz E, Mosher J, Mukherjee A, et al. Functional interactions between Drosophila bHLH/PAS, Sox, and POU transcription factors regulate CNS midline expression of the slit gene. J Neurosci. 2000;20(12):4596-605. PMID: 10844029
54. Magnani L, Eeckhoute J, Lupien M. Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends Genet. 2011;27(11):465-74. doi: 10.1016/j.tig.2011.07.002 PMID: 21885149
55. Serandour AA, Avner S, Percevault F, Demay F, Bizot M, Lucchetti-Miganeh C, et al. Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res. 2011;21(4):555-65. doi: 10.1101/gr.111534.110 PMID: 21233399
56. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell. 2008;132(6):958-70. doi: 10.1016/j.cell. 2008.01.018 PMID: 18358809
57. Soufi A, Donahue G, Zaret KS. Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome. Cell. 2012;151(5):994-1004. doi: 10.1016/j.cell.2012.09.045 PMID: 23159369
58. Bergsland M, Ramskold D, Zaouter C, Klum S, Sandberg R, Muhr J. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev. 2011;25(23):2453-64. doi: 10.1101/gad. 176008.111 PMID: 22085726
59. Liber D, Domaschenz R, Holmqvist PH, Mazzarella L, Georgiou A, Leleu M, et al. Epigenetic priming of a pre-B cell-specific enhancer through binding of Sox2 and Foxd3 at the ESC stage. Cell Stem Cell. 2010;7(1):114-26. doi: 10.1016/j.stem.2010.05.020 PMID: 20621055
60. Nishiyama A, Xin L, Sharov AA, Thomas M, Mowrer G, Meyers E, et al. Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell. 2009;5(4):420-33. doi: 10.1016/j.stem.2009.07.012 PMID: 19796622
61. Wu JQ, Habegger L, Noisa P, Szekely A, Qiu C, Hutchison S, et al. Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing. Proc Natl Acad Sci USA. 2010;107(11):5254-9. doi: 10.1073/pnas.0914114107 PMID: 20194744
62. Lin M, Pedrosa E, Shah A, Hrabovsky A, Maqbool S, Zheng D, et al. RNA-Seq of human neurons derived from iPS cells reveals candidate long non-coding RNAs involved in neurogenesis and neuropsychiatric disorders. PLoS One. 2011;6(9):e23356. doi: 10.1371/journal.pone.0023356 PMID: 21915259
63. Hubbard KS, Gut IM, Lyman ME, McNutt PM. Longitudinal RNA sequencing of the deep transcriptome during neurogenesis of cortical glutamatergic neurons from murine ESCs. F1000Research. 2013;2:35. doi: 10.12688/f1000research.2-35.v1 PMID: 24358889