Diverse Roles and Interactions of the SWI/SNF Chromatin Remodeling Complex Revealed Using Global Approaches

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A systems understanding of nuclear organization and events is critical for determining how cells divide, differentiate, and respond to stimuli and for identifying the causes of diseases. Chromatin remodeling complexes such as SWI/SNF have been implicated in a wide variety of cellular processes including gene expression, nuclear organization, centromere function, and chromosomal stability, and mutations in SWI/SNF components have been linked to several types of cancer. To better understand the biological processes in which chromatin remodeling proteins participate, we globally mapped binding regions for several components of the SWI/SNF complex throughout the human genome using ChIP-Seq. SWI/SNF components were found to lie near regulatory elements integral to transcription (e.g. 5′ ends, RNA Polymerases II and III, and enhancers) as well as regions critical for chromosome organization (e.g. CTCF, lamins, and DNA replication origins). Interestingly we also find that certain configurations of SWI/SNF subunits are associated with transcripts that have higher levels of expression, whereas other configurations of SWI/SNF factors are associated with transcripts that have lower levels of expression. To further elucidate the association of SWI/SNF subunits with each other as well as with other nuclear proteins, we also analyzed SWI/SNF immunoprecipitated complexes by mass spectrometry. Individual SWI/SNF factors are associated with their own family members, as well as with cellular constituents such as nuclear matrix proteins, key transcription factors, and centromere components, implying a ubiquitous role in gene regulation and nuclear function. We find an overrepresentation of both SWI/SNF-associated regions and proteins in cell cycle and chromosome organization. Taken together the results from our ChIP and immunoprecipitation experiments suggest that SWI/SNF facilitates gene regulation and genome function more broadly and through a greater diversity of interactions than previously appreciated.

Vyšlo v časopise: Diverse Roles and Interactions of the SWI/SNF Chromatin Remodeling Complex Revealed Using Global Approaches. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1002008
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002008

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1. JacksonDAIborraFJMandersEMCookPR 1998 Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei. Mol Biol Cell 9 1523 1536

2. CookPR 1999 The organization of replication and transcription. Science 284 1790 1795

3. CookPR 2010 A model for all genomes: the role of transcription factories. J Mol Biol 395 1 10 doi:10.1016/j.jmb.2009.10.031

4. ClapierCRCairnsBR 2009 The biology of chromatin remodeling complexes. Annu Rev Biochem 78 273 304 doi:10.1146/annurev.biochem.77.062706.153223

5. de la SernaILOhkawaYImbalzanoAN 2006 Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 7 461 473 doi:10.1038/nrg1882

6. WuJILessardJCrabtreeGR 2009 Understanding the words of chromatin regulation. Cell 136 200 206 doi:10.1016/j.cell.2009.01.009

7. PhelanMLSifSNarlikarGJKingstonRE 1999 Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol Cell 3 247 253

8. ChenJArcherTK 2005 Regulating SWI/SNF subunit levels via protein-protein interactions and proteasomal degradation: BAF155 and BAF170 limit expression of BAF57. Mol Cell Biol 25 9016 9027 doi:10.1128/MCB.25.20.9016-9027.2005

9. SohnDHLeeKYLeeCOhJChungH 2007 SRG3 interacts directly with the major components of the SWI/SNF chromatin remodeling complex and protects them from proteasomal degradation. J Biol Chem 282 10614 10624 doi:10.1074/jbc.M610563200

10. PercipallePVisaN 2006 Molecular functions of nuclear actin in transcription. J Cell Biol 172 967 971 doi:10.1083/jcb.200512083

11. CastanoEPhilimonenkoVVKahleMFukalováJKalendováA 2010 Actin complexes in the cell nucleus: new stones in an old field. Histochem Cell Biol 133 607 626 doi:10.1007/s00418-010-0701-2

12. RandoOJZhaoKJanmeyPCrabtreeGR 2002 Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc Natl Acad Sci U.S.A 99 2824 2829 doi:10.1073/pnas.032662899

13. VersteegeISévenetNLangeJRousseau-MerckMFAmbrosP 1998 Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394 203 206 doi:10.1038/28212

14. SévenetNLellouch-TubianaASchofieldDHoang-XuanKGesslerM 1999 Spectrum of hSNF5/INI1 somatic mutations in human cancer and genotype-phenotype correlations. Hum Mol Genet 8 2359 2368

15. WongJNakajimaYWestermannSShangCKangJ 2007 A protein interaction map of the mitotic spindle. Mol Biol Cell 18 3800 3809 doi:10.1091/mbc.E07-06-0536

16. HuangDWShermanBTLempickiRA 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4 44 57 doi:10.1038/nprot.2008.211

17. WiegandKShahSAl-AghaOZhaoYTseK 2010 ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med

18. JonesSWangTShihIMaoTNakayamaK 2010 Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330 228 231 doi:10.1126/science.1196333

19. Van MaeleBBusschotsKVandekerckhoveLChristFDebyserZ 2006 Cellular co-factors of HIV-1 integration. Trends Biochem Sci 31 98 105 doi:10.1016/j.tibs.2005.12.002

20. TurelliPDoucasVCraigEMangeatBKlagesN 2001 Cytoplasmic recruitment of INI1 and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. Mol Cell 7 1245 1254

21. DasSCanoJKalpanaGV 2009 Multimerization and DNA binding properties of INI1/hSNF5 and its functional significance. J Biol Chem 284 19903 19914 doi:10.1074/jbc.M808141200

22. IsakoffMSSansamCGTamayoPSubramanianAEvansJA 2005 Inactivation of the Snf5 tumor suppressor stimulates cell cycle progression and cooperates with p53 loss in oncogenic transformation. Proc Natl Acad Sci U.S.A 102 17745 17750 doi:10.1073/pnas.0509014102

23. LeeYSSohnDHHanDLeeHSeongRH 2007 Chromatin remodeling complex interacts with ADD1/SREBP1c to mediate insulin-dependent regulation of gene expression. Mol Cell Biol 27 438 452 doi:10.1128/MCB.00490-06

24. XiQHeWZhangXHLeHMassaguéJ 2008 Genome-wide impact of the BRG1 SWI/SNF chromatin remodeler on the transforming growth factor beta transcriptional program. J Biol Chem 283 1146 1155 doi:10.1074/jbc.M707479200

25. SimoneC 2006 SWI/SNF: the crossroads where extracellular signaling pathways meet chromatin. J Cell Physiol 207 309 314 doi:10.1002/jcp.20514

26. RozowskyJEuskirchenGAuerbachRKZhangZDGibsonT 2009 PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol 27 66 75 doi:10.1038/nbt.1518

27. BickelPBoleyNBrownJHuangHZhangN 2010 Subsampling methods for genomic inference. Annals of Applied Statistics 4 1660 1697 doi:10.1214/10-AOAS363

28. CuddapahSJothiRSchonesDERohTCuiK 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 doi:10.1101/gr.082800.108

29. HeintzmanNDHonGCHawkinsRDKheradpourPStarkA 2009 Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459 108 112 doi:10.1038/nature07829

30. NiZAbou El HassanMXuZYuTBremnerR 2008 The chromatin-remodeling enzyme BRG1 coordinates CIITA induction through many interdependent distal enhancers. Nat Immunol 9 785 793 doi:10.1038/ni.1619

31. Bazett-JonesDPCôtéJLandelCCPetersonCLWorkmanJL 1999 The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNA-histone contacts within these domains. Mol Cell Biol 19 1470 1478

32. NomaKCamHPMaraiaRJGrewalSIS 2006 A role for TFIIIC transcription factor complex in genome organization. Cell 125 859 872 doi:10.1016/j.cell.2006.04.028

33. RaabJRKamakakaRT 2010 Insulators and promoters: closer than we think. Nat Rev Genet 11 439 446 doi:10.1038/nrg2765

34. OlerAJAllaRKRobertsDNWongAHollenhorstPC 2010 Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat Struct Mol Biol 17 620 628 doi:10.1038/nsmb.1801

35. BarskiAChepelevILikoDCuddapahSFlemingAB 2010 Pol II and its associated epigenetic marks are present at Pol III-transcribed noncoding RNA genes. Nat Struct Mol Biol 17 629 634 doi:10.1038/nsmb.1806

36. UrnovFDWolffeAP 2001 Chromatin remodeling and transcriptional activation: the cast (in order of appearance). Oncogene 20 2991 3006 doi:10.1038/sj.onc.1204323

37. MorinRBainbridgeMFejesAHirstMKrzywinskiM 2008 Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. BioTechniques 45 81 94 doi:10.2144/000112900

38. SaundersACoreLJLisJT 2006 Breaking barriers to transcription elongation. Nat Rev Mol Cell Biol 7 557 567 doi:10.1038/nrm1981

39. FudaNJArdehaliMBLisJT 2009 Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461 186 192 doi:10.1038/nature08449

40. Affymetrix and Cold Spring Harbor Laboratory ENCODE Transcriptome Projects 2009 Post-transcriptional processing generates a diversity of 5'-modified long and short RNAs. Nature 457 1028 32 doi:10.1038/nature07759

41. HanahanDWeinbergRA 2000 The hallmarks of cancer. Cell 100 57 70

42. MalovannayaALiYBulynkoYJungSYWangY 2010 Streamlined analysis schema for high-throughput identification of endogenous protein complexes. Proc Natl Acad Sci U.S.A 107 2431 2436 doi:10.1073/pnas.0912599106

43. XueYCanmanJCLeeCSNieZYangD 2000 The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes. Proc Natl Acad Sci U.S.A 97 13015 13020 doi:10.1073/pnas.240208597

44. BourgoRJSiddiquiHFoxSSolomonDSansamCG 2009 SWI/SNF deficiency results in aberrant chromatin organization, mitotic failure, and diminished proliferative capacity. Mol Biol Cell 20 3192 3199 doi:10.1091/mbc.E08-12-1224

45. UniProt Consortium 2010 The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res 38 D142 148 doi:10.1093/nar/gkp846

46. MisteliT 2007 Beyond the sequence: cellular organization of genome function. Cell 128 787 800 doi:10.1016/j.cell.2007.01.028

47. DechatTPfleghaarKSenguptaKShimiTShumakerDK 2008 Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22 832 853 doi:10.1101/gad.1652708

48. CrispMLiuQRouxKRattnerJBShanahanC 2006 Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172 41 53 doi:10.1083/jcb.200509124

49. HaqueFLloydDJSmallwoodDTDentCLShanahanCM 2006 SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26 3738 3751 doi:10.1128/MCB.26.10.3738-3751.2006

50. ShimiTPfleghaarKKojimaSPackCSoloveiI 2008 The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 22 3409 3421 doi:10.1101/gad.1735208

51. ReyesJCMuchardtCYanivM 1997 Components of the human SWI/SNF complex are enriched in active chromatin and are associated with the nuclear matrix. J Cell Biol 137 263 274

52. MoirRDMontag-LowyMGoldmanRD 1994 Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J Cell Biol 125 1201 1212

53. CohenSMChastainPDRossonGBGrohBSWeissmanBE 2010 BRG1 co-localizes with DNA replication factors and is required for efficient replication fork progression. Nucleic Acids Res 38 6906 6919 doi:10.1093/nar/gkq559

54. SeoSHerrALimJRichardsonGARichardsonH 2005 Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19 1723 1734 doi:10.1101/gad.1319105

55. CadoretJMeischFHassan-ZadehVLuytenIGuilletC 2008 Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci U.S.A 105 15837 15842 doi:10.1073/pnas.0805208105

56. RymeJAspPBöhmSCavellánEFarrantsAO 2009 Variations in the composition of mammalian SWI/SNF chromatin remodelling complexes. J Cell Biochem 108 565 576 doi:10.1002/jcb.22288

57. DinantCLuijsterburgMSHöferTvon BornstaedtGVermeulenW 2009 Assembly of multiprotein complexes that control genome function. J Cell Biol 185 21 26 doi:10.1083/jcb.200811080

58. RinoJCarvalhoTBragaJDesterroJMPLührmannR 2007 A stochastic view of spliceosome assembly and recycling in the nucleus. PLoS Comput Biol 3 2019 2031 doi:10.1371/journal.pcbi.0030201

59. LuijsterburgMSvon BornstaedtGGourdinAMPolitiAZMonéMJ 2010 Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair. J Cell Biol 189 445 463 doi:10.1083/jcb.200909175

60. LiuHKangHLiuRChenXZhaoK 2002 Maximal induction of a subset of interferon target genes requires the chromatin-remodeling activity of the BAF complex. Mol Cell Biol 22 6471 6479

61. BouwmeesterTBauchARuffnerHAngrandPBergaminiG 2004 A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 6 97 105 doi:10.1038/ncb1086

62. HsiaoPFryerCJTrotterKWWangWArcherTK 2003 BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23 6210 6220

63. BelandiaBOrfordRLHurstHCParkerMG 2002 Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J 21 4094 4103

64. WeissmanBKnudsenKE 2009 Hijacking the chromatin remodeling machinery: impact of SWI/SNF perturbations in cancer. Cancer Res 69 8223 8230 doi:10.1158/0008-5472.CAN-09-2166

65. BarlowCALaishramRSAndersonRA 2010 Nuclear phosphoinositides: a signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol 20 25 35 doi:10.1016/j.tcb.2009.09.009

66. RayAMirSNWaniGZhaoQBattuA 2009 Human SNF5/INI1, a component of the human SWI/SNF chromatin remodeling complex, promotes nucleotide excision repair by influencing ATM recruitment and downstream H2AX phosphorylation. Mol Cell Biol 29 6206 6219 doi:10.1128/MCB.00503-09

67. HoLRonanJLWuJStaahlBTChenL 2009 An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci U.S.A 106 5181 5186 doi:10.1073/pnas.0812889106

68. EwingRMChuPElismaFLiHTaylorP 2007 Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol Syst Biol 3 89 doi:10.1038/msb4100134

69. LambertJMitchellLRudnerABaetzKFigeysD 2009 A novel proteomics approach for the discovery of chromatin-associated protein networks. Mol Cell Proteomics 8 870 882 doi:10.1074/mcp.M800447-MCP200

70. GavinABöscheMKrauseRGrandiPMarziochM 2002 Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415 141 147 doi:10.1038/415141a

71. GavinAAloyPGrandiPKrauseRBoescheM 2006 Proteome survey reveals modularity of the yeast cell machinery. Nature 440 631 636 doi:10.1038/nature04532

72. BreitkreutzAChoiHSharomJRBoucherLNeduvaV 2010 A global protein kinase and phosphatase interaction network in yeast. Science 328 1043 1046 doi:10.1126/science.1176495

73. Lallemand-BreitenbachVde ThéH 2010 PML nuclear bodies. Cold Spring Harb Perspect Biol 2 a000661 doi:10.1101/cshperspect.a000661

74. ReyesJCMuchardtCYanivM 1997 Components of the human SWI/SNF complex are enriched in active chromatin and are associated with the nuclear matrix. J Cell Biol 137 263 274

75. MuchardtCReyesJCBourachotBLeguoyEYanivM 1996 The hbrm and BRG-1 proteins, components of the human SNF/SWI complex, are phosphorylated and excluded from the condensed chromosomes during mitosis. EMBO J 15 3394 3402

76. GüttingerSLaurellEKutayU 2009 Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 10 178 191 doi:10.1038/nrm2641

77. NielsenALSanchezCIchinoseHCerviñoMLerougeT 2002 Selective interaction between the chromatin-remodeling factor BRG1 and the heterochromatin-associated protein HP1alpha. EMBO J 21 5797 5806

78. LavigneMEskelandRAzebiSSaint-AndréVJangSM 2009 Interaction of HP1 and Brg1/Brm with the globular domain of histone H3 is required for HP1-mediated repression. PLoS Genet 5 e1000769 doi:10.1371/journal.pgen.1000769

79. WilsonBGWangXShenXMcKennaESLemieuxME 2010 Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18 316 328 doi:10.1016/j.ccr.2010.09.006

80. SchuettengruberBChourroutDVervoortMLeblancBCavalliG 2007 Genome regulation by polycomb and trithorax proteins. Cell 128 735 45 doi:10.1016/j.cell.2007.02.009

81. KwonSHWorkmanJL 2008 The heterochromatin protein 1 (HP1) family: put away a bias toward HP1. Mol Cells 26 217 227

82. YeQCallebautIPezhmanACourvalinJCWormanHJ 1997 Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J Biol Chem 272 14983 14989

83. MétivierRGallaisRTiffocheCLe PéronCJurkowskaRZ 2008 Cyclical DNA methylation of a transcriptionally active promoter. Nature 452 45 50 doi:10.1038/nature06544

84. AuerbachRKEuskirchenGRozowskyJLamarre-VincentNMoqtaderiZ 2009 Mapping accessible chromatin regions using Sono-Seq. Proc Natl Acad Sci U.S.A 106 14926 14931 doi:10.1073/pnas.0905443106

85. BentleyDRBalasubramanianSSwerdlowHPSmithGPMiltonJ 2008 Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456 53 59 doi:10.1038/nature07517

86. EuskirchenGMRozowskyJSWeiCLeeWHZhangZD 2007 Mapping of transcription factor binding regions in mammalian cells by ChIP: comparison of array- and sequencing-based technologies. Genome Res 17 898 909 doi:10.1101/gr.5583007

87. Gene Ontology Consortium 2010 The Gene Ontology in 2010: extensions and refinements. Nucleic Acids Res 38 D331 335 doi:10.1093/nar/gkp1018

88. KanehisaMGotoSFurumichiMTanabeMHirakawaM 2010 KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38 D355 360 doi:10.1093/nar/gkp896

89. KlukasCSchreiberF 2007 Dynamic exploration and editing of KEGG pathway diagrams. Bioinformatics 23 344 350 doi:10.1093/bioinformatics/btl611

90. ENCODE Project Consortium 2004 The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306 636 640 doi:10.1126/science.1105136

91. ZhangZDRozowskyJLamHYKDuJSnyderM 2007 Tilescope: online analysis pipeline for high-density tiling microarray data. Genome Biol 8 R81 doi:10.1186/gb-2007-8-5-r81