The Fun30 Chromatin Remodeler Fft3 Controls Nuclear Organization and Chromatin Structure of Insulators and Subtelomeres in Fission Yeast

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Steglich, Babett ^a   Strålfors, Annelie ^a   Khorosjutina, Olga ^a   Persson, Jenna ^a   Smialowska, Agata ^a,d   Javerzat, Jean Paul ^b,c   Ekwall, Karl ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c Institut de Biochimie et Genetique Cellulaires   (France)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BQT4 PROTEIN; CONDENSIN; FFT3 PROTEIN; FUNGAL PROTEIN; PROLINE; PROTEIN MAN1; RNA POLYMERASE II; TRANSCRIPTION FACTOR III; TRANSCRIPTION FACTOR IIIC; UNCLASSIFIED DRUG; CHROMATIN; FFT3 PROTEIN, S POMBE; MAN1 PROTEIN, S POMBE; MEMBRANE PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; NUCLEOSOME; SCHIZOSACCHAROMYCES POMBE PROTEIN; TRANSFER RNA;

ARTICLE; BINDING SITE; BQT4 GENE; CELL NUCLEUS MEMBRANE; CELLULAR PARAMETERS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME STRUCTURE; CONTROLLED STUDY; FUNGAL GENE; GENOME ANALYSIS; INSULATOR ELEMENT; LONG TERMINAL REPEAT; NONHUMAN; NUCLEAR ORGANIZATION; NUCLEOSOME; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE; SUBTELOMERE; TELOMERE; TRANSCRIPTION REGULATION; UPREGULATION; BIOSYNTHESIS; CELL NUCLEUS; CHROMATIN; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; SCHIZOSACCHAROMYCES;

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; GENE EXPRESSION REGULATION, FUNGAL; INSULATOR ELEMENTS; MEMBRANE PROTEINS; NUCLEAR PROTEINS; NUCLEOSOMES; RNA, TRANSFER; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TELOMERE; TERMINAL REPEAT SEQUENCES; TRANSCRIPTION, GENETIC;

EID: 84926340066     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005101     Document Type: Article

References (59)

1. Bermejo R, Kumar A, Foiani M, (2012) Preserving the genome by regulating chromatin association with the nuclear envelope. Trends in Cell Biology 22: 465–473. doi: 10.1016/j.tcb.2012.05.007 22771046
2. Smith OK, Aladjem MI (2014) Chromatin Structure and Replication Origins: Determinants of Chromosome Replication and Nuclear Organization. Journal of Molecular Biology. E-pub ahead of print.
3. Wendt KS, Grosveld FG, (2014) Transcription in the context of the 3D nucleus. Current Opinion in Genetics & Development 25C: 62–67.
4. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, et al. (2006) Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nature Genetics 38: 1005–1014. 16878134
5. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, et al. (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453: 948–951. doi: 10.1038/nature06947 18463634
6. Ikegami K, Egelhofer TA, Strome S, Lieb JD, (2010) Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2. Genome Biology 11: R120. doi: 10.1186/gb-2010-11-12-r120 21176223
7. Steglich B, Filion GJ, van Steensel B, Ekwall K, (2012) The inner nuclear membrane proteins Man1 and Ima1 link to two different types of chromatin at the nuclear periphery in S. pombe. Nucleus 3: 77–87. 22156748
8. Pinheiro I, Margueron R, Shukeir N, Eisold M, Fritzsch C, et al. (2012) Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150: 948–960. doi: 10.1016/j.cell.2012.06.048 22939622
9. Towbin BD, González-Aguilera C, Sack R, Gaidatzis D, Kalck V, et al. (2012) Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150: 934–947. doi: 10.1016/j.cell.2012.06.051 22939621
10. Zuleger N, Boyle S, Kelly DA, las Heras de JI, Lazou V, et al. (2013) Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biology 14: R14. doi: 10.1186/gb-2013-14-2-r14 23414781
11. Buchanan L, Durand-Dubief M, Roguev A, Sakalar C, Wilhelm B, et al. (2009) The Schizosaccharomyces pombe JmjC-protein, Msc1, prevents H2A.Z localization in centromeric and subtelomeric chromatin domains. PLoS Genet 5: e1000726. doi: 10.1371/journal.pgen.1000726 19911051
12. Zofall M, Fischer T, Zhang K, Zhou M, Cui B, et al. (2009) Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature 461: 419–422. doi: 10.1038/nature08321 19693008
13. Mata J, Lyne R, Burns G, Bähler J, (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nature Genetics 32: 143–147. 12161753
14. Strålfors A, Walfridsson J, Bhuiyan H, Ekwall K, (2011) The FUN30 chromatin remodeler, Fft3, protects centromeric and subtelomeric domains from euchromatin formation. PLoS Genet 7: e1001334. doi: 10.1371/journal.pgen.1001334 21437270
15. Flaus A, Martin DMA, Barton GJ, Owen-Hughes T, (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Research 34: 2887–2905. 16738128
16. Neves-Costa A, Will WR, Vetter AT, Miller JR, Varga-Weisz P, (2009) The SNF2-family member Fun30 promotes gene silencing in heterochromatic loci. PLoS ONE 4: e8111. doi: 10.1371/journal.pone.0008111 19956593
17. Rowbotham SP, Barki L, Neves-Costa A, Santos F, Dean W, et al. (2011) Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Molecular Cell 42: 285–296. doi: 10.1016/j.molcel.2011.02.036 21549307
18. Yu Q, Zhang X, Bi X, (2011) Roles of chromatin remodeling factors in the formation and maintenance of heterochromatin structure. Journal of Biological Chemistry 286: 14659–14669. doi: 10.1074/jbc.M110.183269 21388962
19. Chen X, Cui D, Papusha A, Zhang X, Chu C-D, et al. (2012) The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489: 576–580. doi: 10.1038/nature11355 22960743
20. Costelloe T, Louge R, Tomimatsu N, Mukherjee B, Martini E, et al. (2012) The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489: 581–584. doi: 10.1038/nature11353 22960744
21. Durand-Dubief M, Will WR, Petrini E, Theodorou D, Harris RR, et al. (2012) SWI/SNF-like chromatin remodeling factor Fun30 supports point centromere function in S. cerevisiae. PLoS Genet 8: e1002974. doi: 10.1371/journal.pgen.1002974 23028372
22. Eapen VV, Sugawara N, Tsabar M, Wu W-H, Haber JE, (2012) The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Molecular and Cellular Biology 32: 4727–4740. doi: 10.1128/MCB.00566-12 23007155
23. Chikashige Y, Yamane M, Okamasa K, Tsutsumi C, Kojidani T, et al. (2009) Membrane proteins Bqt3 and -4 anchor telomeres to the nuclear envelope to ensure chromosomal bouquet formation. The Journal of Cell Biology 187: 413–427. doi: 10.1083/jcb.200902122 19948484
24. Woolcock KJ, Stunnenberg R, Gaidatzis D, Hotz H-R, Emmerth S, et al. (2012) RNAi keeps Atf1-bound stress response genes in check at nuclear pores. Genes & Development 26: 683–692.
25. Laurent BC, Treich I, Carlson M, (1993) The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. Genes & Development 7: 583–591.
26. Corona DF, Längst G, Clapier CR, Bonte EJ, Ferrari S, et al. (1999) ISWI is an ATP-dependent nucleosome remodeling factor. Molecular Cell 3: 239–245. 10078206
27. Huang Y, Maraia RJ, (2001) Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucleic Acids Research 29: 2675–2690. 11433012
28. Noma K-II, Cam HP, Maraia RJ, Grewal SIS, (2006) A role for TFIIIC transcription factor complex in genome organization. Cell 125: 859–872. 16751097
29. Moqtaderi Z, Struhl K, (2004) Genome-wide occupancy profile of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Molecular and Cellular Biology 24: 4118–4127. 15121834
30. Moqtaderi Z, Wang J, Raha D, White RJ, Snyder M, et al. (2010) Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat Struct Mol Biol 17: 635–640. doi: 10.1038/nsmb.1794 20418883
31. Huang Y, Hamada M, Maraia RJ, (2000) Isolation and cloning of four subunits of a fission yeast TFIIIC complex that includes an ortholog of the human regulatory protein TFIIICbeta. J Biol Chem 275: 31480–31487. 10906331
32. Dumay-Odelot H, Acker J, Arrebola R, Sentenac A, Marck C, (2002) Multiple roles of the tau131 subunit of yeast transcription factor IIIC (TFIIIC) in TFIIIB assembly. Molecular and Cellular Biology 22: 298–308. 11739742
33. Haeusler RA, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR, (2008) Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes & Development 22: 2204–2214.
34. Iwasaki O, Tanaka A, Tanizawa H, Grewal SIS, Noma K-II, (2010) Centromeric localization of dispersed Pol III genes in fission yeast. Molecular Biology of the Cell 21: 254–265. doi: 10.1091/mbc.E09-09-0790 19910488
35. Van Bortle K, Corces VG (2013) The role of chromatin insulators in nuclear architecture and genome function. Current Opinion in Genetics & Development.
36. Mekhail K, Seebacher J, Gygi SP, Moazed D, (2008) Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456: 667–670. doi: 10.1038/nature07460 18997772
37. Grund SE, Fischer T, Cabal GG, Antúnez O, Pérez-Ortín JE, et al. (2008) The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. The Journal of Cell Biology 182: 897–910. doi: 10.1083/jcb.200803098 18762579
38. Byeon B, Wang W, Barski A, Ranallo RT, Bao K, et al. (2013) The ATP-dependent chromatin remodeling enzyme Fun30 represses transcription by sliding promoter-proximal nucleosomes. Journal of Biological Chemistry 288: 23182–23193. doi: 10.1074/jbc.M113.471979 23779104
39. Nakayama T, Shimojima T, Hirose S, (2012) The PBAP remodeling complex is required for histone H3.3 replacement at chromatin boundaries and for boundary functions. Development 139: 4582–4590. doi: 10.1242/dev.083246 23136390
40. Yajima M, Fairbrother WG, Wessel GM, (2012) ISWI contributes to ArsI insulator function in development of the sea urchin. Development 139: 3613–3622. doi: 10.1242/dev.081828 22949616
41. Carabana J, Watanabe A, Hao B, Krangel MS, (2011) A barrier-type insulator forms a boundary between active and inactive chromatin at the murine TCRβ locus. J Immunol 186: 3556–3562. doi: 10.4049/jimmunol.1003164 21317385
42. Valenzuela L, Kamakaka RT, (2006) Chromatin insulators. Annu Rev Genet 40: 107–138. 16953792
43. Cam HP, Noma K-II, Ebina H, Levin HL, Grewal SIS, (2008) Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451: 431–436. 18094683
44. Strålfors A, Ekwall K, Meyers RA, (2012) Heterochromatin and Euchromatin—Organization, Boundaries, and Gene Regulation. In: Epigenetic Regulation and epigenomics: Advances in Moleular Biology and Medicine. Wilwy-VCH Verlag GmbH & Co. KGaA. pp. 171–189.
45. Jordan IK, Rogozin IB, Glazko GV, Koonin EV, (2003) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19: 68–72. 12547512
46. Kirkland JG, Raab JR, Kamakaka RT (2012) TFIIIC bound DNA elements in nuclear organization and insulation. Biochim Biophys Acta.
47. Neumann FR, Dion V, Gehlen LR, Tsai-Pflugfelder M, Schmid R, et al. (2012) Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes & Development 26: 369–383.
48. Li B, (2012) Telomere components as potential therapeutic targets for treating microbial pathogen infections. Front Oncol 2: 156. doi: 10.3389/fonc.2012.00156 23125966
49. Landeira D, Navarro M, (2007) Nuclear repositioning of the VSG promoter during developmental silencing in Trypanosoma brucei. The Journal of Cell Biology 176: 133–139. 17210949
50. Riethman H, Ambrosini A, Paul S, (2005) Human subtelomere structure and variation. Chromosome Res 13: 505–515. 16132815
51. Ottaviani A, Schluth-Bolard C, Rival-Gervier S, Boussouar A, Rondier D, et al. (2009) Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF. The EMBO Journal 28: 2428–2436. doi: 10.1038/emboj.2009.201 19644448
52. Ottaviani A, Schluth-Bolard C, Gilson E, Magdinier F, (2010) D4Z4 as a prototype of CTCF and lamins-dependent insulator in human cells. Nucleus 1: 30–36. doi: 10.4161/nucl.1.1.10799 21327102
53. Durand-Dubief M, Ekwall K, (2009) Chromatin immunoprecipitation using microarrays. Methods Mol Biol 529: 279–295. doi: 10.1007/978-1-59745-538-1_18 19381973
54. Vogel MJ, Peric-Hupkes D, van Steensel B, (2007) Detection of in vivo protein-DNA interactions using DamID in mammalian cells. Nat Protoc 2: 1467–1478. 17545983
55. Xue Y, Haas SA, Brino L, Gusnanto A, Reimers M, et al. (2004) A DNA microarray for fission yeast: minimal changes in global gene expression after temperature shift. Yeast 21: 25–39. 14745780
56. Meister P, Gehlen LR, Varela E, Kalck V, Gasser SM, (2010) Visualizing yeast chromosomes and nuclear architecture. Meth Enzymol 470: 535–567. doi: 10.1016/S0076-6879(10)70021-5 20946824
57. Lantermann A, Strålfors A, Fagerström-Billai F, Korber P, Ekwall K, (2009) Genome-wide mapping of nucleosome positions in Schizosaccharomyces pombe. Methods 48: 218–225. doi: 10.1016/j.ymeth.2009.02.004 19233281
58. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Meth 9: 357–359.
59. Chen K, Xi Y, Pan X, Li Z, Kaestner K, et al. (2013) DANPOS: dynamic analysis of nucleosome position and occupancy by sequencing. Genome Research 23: 341–351. doi: 10.1101/gr.142067.112 23193179