The ATP-dependent chromatin remodeling enzyme Fun30 represses transcription by sliding promoter-proximal nucleosomes

Journal of Biological Chemistry

Volumn 288, Issue 32, 2013, Pages 23182-23193

  Byeon, Boseon ^a   Wang, Wei ^a   Barski, Artem ^b   Ranallo, Ryan T ^c   Bao, Kan ^a   Schones, Dustin E ^b   Zhao, Keji ^b   Wu, Carl ^c   Wu, Wei Hua ^a,c  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN REMODELING; DNA REPAIR; IN-VITRO; NUCLEOSOME SLIDING; NUCLEOSOMES; REGULATION OF TRANSCRIPTION;

ENZYMES; TRANSCRIPTION;

CHROMOSOMES;

ADENOSINE TRIPHOSPHATE; FUN30 PROTEIN; HISTONE; HISTONE H2B; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ARTICLE; BINDING AFFINITY; CARBOHYDRATE METABOLISM; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENZYME LOCALIZATION; ENZYME PURIFICATION; FUN30 GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TARGETING; HISTONE MODIFICATION; HISTONE UBIQUITINATION; IN VITRO STUDY; MEIOSIS; NONHUMAN; NUCLEOSOME; NUCLEOSOME MAPPING ANALYSIS; NUCLEOSOME SLIDING ACTIVITY; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; STRESS; TRANSCRIPTION REGULATION; UPREGULATION;

CHROMATIN REGULATION; CHROMATIN REMODELING; FUN30; GENE REGULATION; NUCLEOSOME; NUCLEOSOME MAPPING; NUCLEOSOME-FREE REGION; YEAST TRANSCRIPTION;

ADENOSINE TRIPHOSPHATE; CHROMATIN ASSEMBLY AND DISASSEMBLY; HISTONES; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITINATION;

EID: 84881456132     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.471979     Document Type: Article

References (63)

1. Luger, K., MAder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260
2. Banaszynski, L. A., Allis, C. D., and Lewis, P. W. (2010) Histone variants in metazoan development. Dev. Cell 19, 662-674
3. Ray-Gallet, D., and Almouzni, G. (2010) Nucleosome dynamics and histone variants. Essays Biochem. 48, 75-87
4. Talbert, P. B., and Henikoff, S. (2010) Histone variants. Ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11, 264-275
5. Clapier, C. R., and Cairns, B. R. (2009) The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304
6. Jiang, C., and Pugh, B. F. (2009) Nucleosome positioning and gene regulation. Advances through genomics. Nat. Rev. Genet. 10, 161-172
7. Ransom, M., Dennehey, B. K., and Tyler, J. K. (2010) Chaperoning histones during DNA replication and repair. Cell 140, 183-195
8. Seeber, A., Hauer, M., and Gasser, S. M. (2013) Nucleosome remodelers in double-strand break repair. Curr. Opin. Genet. Dev. 23, 174-184
9. Rando, O. J., and Winston, F. (2012) Chromatin and transcription in yeast. Genetics 190, 351-387
10. Jiang, C., and Pugh, B. F. (2009) A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome. Genome Biol. 10, R109
11. Brogaard, K., Xi, L., Wang, J. P., and Widom, J. (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature 486, 496-501
12. Yuan, G. C., Liu, Y. J., Dion, M. F., Slack, M. D., Wu, L. F., Altschuler, S. J., and Rando, O. J. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626-630
13. Schones, D. E., and Zhao, K. (2008) Genome-wide approaches to studying chromatin modifications. Nat. Rev. Genet. 9, 179-191
14. Cairns, B. R. (2009) The logic of chromatin architecture and remodelling at promoters. Nature 461, 193-198
15. Albert, I., Mavrich, T. N., Tomsho, L. P., Qi, J., Zanton, S. J., Schuster, S. C., and Pugh, B. F. (2007) Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572-576
16. Raisner, R. M., Hartley, P. D., Meneghini, M. D., Bao, M. Z., Liu, C. L., Schreiber, S. L., Rando, O. J., and Madhani, H. D. (2005) Histone variant H2A.Z marks the 5ends of both active and inactive genes in euchromatin. Cell 123, 233-248
17. Luk, E., Ranjan, A., Fitzgerald, P. C., Mizuguchi, G., Huang, Y., Wei, D., and Wu, C. (2010) Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143, 725-736
18. Segal, E., and Widom, J. (2009) What controls nucleosome positions? Trends Genet. 25, 335-343
19. Jansen, A., and Verstrepen, K. J. (2011) Nucleosome positioning in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 75, 301-320
20. Sadeh, R., and Allis, C. D. (2011) Genome-wide "re"-modeling of nucleosome positions. Cell 147, 263-266
21. Dürr, H., Flaus, A., Owen-Hughes, T., and Hopfner, K. P. (2006) Snf2 family ATPases and DExx box helicases. Differences and unifying concepts from high-resolution crystal structures. Nucleic Acids Res. 34, 4160-4167
22. Narlikar, G. J. (2010) A proposal for kinetic proof reading by ISWI family chromatin remodeling motors. Curr. Opin. Chem. Biol. 14, 660-665
23. Hota, S. K., and Bartholomew, B. (2011) Diversity of operation in ATP-dependent chromatin remodelers. Biochim. Biophys. Acta 1809, 476-487
24. Tsukiyama, T., Daniel, C., Tamkun, J., and Wu, C. (1995) ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83, 1021-1026
25. Clark, M. W., Zhong, W. W., Keng, T., Storms, R. K., Barton, A., Kaback, D. B., and Bussey, H. (1992) Identification of a Saccharomyces cerevisiae homolog of the SNF2 transcriptional regulator in theDNAsequence of an 8.6 kb region in the LTE1-CYS1 interval on the left arm of chromosome I. Yeast 8, 133-145
26. Barton, A. B., and Kaback, D. B. (1994) Molecular cloning of chromosome I DNA from Saccharomyces cerevisiae. Analysis of the genes in the FUN38-MAK16-SPO7 region. J. Bacteriol. 176, 1872-1880
27. Neves-Costa, A., Will, W. R., Vetter, A. T., Miller, J. R., and Varga-Weisz, P. (2009) The SNF2-family member Fun30 promotes gene silencing in heterochromatic loci. PLoS ONE 4, e8111
28. Rowbotham, S. P., Barki, L., Neves-Costa, A., Santos, F., Dean, W., Hawkes, N., Choudhary, P., Will, W. R., Webster, J., Oxley, D., Green, C. M., Varga-Weisz, P., and Mermoud, J. E. (2011) Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell 42, 285-296
29. StrAlfors, A., Walfridsson, J., Bhuiyan, H., and Ekwall, K. (2011) The FUN30 chromatin remodeler, Fft3, protects centromeric and subtelomeric domains from euchromatin formation. PLoS Genet. 7, e1001334
30. Yu, Q., Zhang, X., and Bi, X. (2011) Roles of chromatin remodeling factors in the formation and maintenance of heterochromatin structure. J. Biol. Chem. 286, 14659-14669
31. Costelloe, T., Louge, R., Tomimatsu, N., Mukherjee, B., Martini, E., Khadaroo, B., Dubois, K., Wiegant, W. W., Thierry, A., Burma, S., van Attikum, H., and Llorente, B. (2012) The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489, 581-584
32. Chen, X., Cui, D., Papusha, A., Zhang, X., Chu, C. D., Tang, J., Chen, K., Pan, X., and Ira, G. (2012) The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489, 576-580
33. Eapen, V. V., Sugawara, N., Tsabar, M., Wu, W. H., and Haber, J. E. (2012) The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol. Cell Biol. 32, 4727-4740
34. Awad, S., Ryan, D., Prochasson, P., Owen-Hughes, T., and Hassan, A. H. (2010) The Snf2 homolog Fun30 acts as a homodimeric ATP-dependent chromatin-remodeling enzyme. J. Biol. Chem. 285, 9477-9484
35. Morrison, A. J., and Shen, X. (2009) Chromatin remodelling beyond transcription. The INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol. 10, 373-384
36. Udugama, M., Sabri, A., and Bartholomew, B. (2011) The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell Biol. 31, 662-673
37. Shen, X., Mizuguchi, G., Hamiche, A., and Wu, C. (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406, 541-544
38. Papamichos-Chronakis, M., Watanabe, S., Rando, O. J., and Peterson, C. L. (2011) Global regulation of H2A.Z localization by the INO80 chromatinremodeling enzyme is essential for genome integrity. Cell 144, 200-213
39. Mizuguchi, G., Shen, X., Landry, J., Wu, W. H., Sen, S., and Wu, C. (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303, 343-348
40. Krogan, N. J., Keogh, M. C., Datta, N., Sawa, C., Ryan, O. W., Ding, H., Haw, R. A., Pootoolal, J., Tong, A., Canadien, V., Richards, D. P., Wu, X., Emili, A., Hughes, T. R., Buratowski, S., and Greenblatt, J. F. (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 12, 1565-1576
41. Wapinski, I., Pfeffer, A., Friedman, N., and Regev, A. (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54-61
42. Fazzio, T. G., Gelbart, M. E., and Tsukiyama, T. (2005) Two distinct mechanisms of chromatin interaction by the Isw2 chromatin remodeling complex in vivo. Mol. Cell Biol. 25, 9165-9174
43. Thoma, F. (1996) Mapping of nucleosome positions. Methods Enzymol. 274, 197-214
44. Weiner, A., Hughes, A., Yassour, M., Rando, O. J., and Friedman, N. (2010) High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res. 20, 90-100
45. Cristianini, N., and Hahn, M. W. (2007) Introduction to Computational Genomics. A case Studies Approach, Chapter 2, pp. 34-35, Cambridge University Press, Cambridge, UK
46. Mizuguchi, G., Wu, W. H., Alami, S., and Luk, E. (2012) Biochemical assay for histone H2A.Z replacement by the yeast SWR1 chromatin remodeling complex. Methods Enzymol. 512, 275-291
47. Hamiche, A., Sandaltzopoulos, R., Gdula, D. A., and Wu, C. (1999) ATPdependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97, 833-842
48. Hartman, J. L., 4th, Garvik, B., and Hartwell, L. (2001) Principles for the buffering of genetic variation. Science 291, 1001-1004
49. Collins, S. R., Miller, K. M., Maas, N. L., Roguev, A., Fillingham, J., Chu, C. S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., Ding, H., Xu, H., Han, J., Ingvarsdottir, K., Cheng, B., Andrews, B., Boone, C., Berger, S. L., Hieter, P., Zhang, Z., Brown, G. W., Ingles, C. J., Emili, A., Allis, C. D., Toczyski, D. P., Weissman, J. S., Greenblatt, J. F., and Krogan, N. J. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446, 806-810
50. Marques, M., Laflamme, L., Gervais, A. L., and Gaudreau, L. (2010) Reconciling the positive and negative roles of histone H2A.Z in gene transcription. Epigenetics 5, 267-272
51. Xu, Z., Wei, W., Gagneur, J., Perocchi, F., Clauder-Münster, S., Camblong, J., Guffanti, E., Stutz, F., Huber, W., and Steinmetz, L. M. (2009) Bidirectional promoters generate pervasive transcription in yeast. Nature 457, 1033-1037
52. Gkikopoulos, T., Schofield, P., Singh, V., Pinskaya, M., Mellor, J., Smolle, M., Workman, J. L., Barton, G. J., and Owen-Hughes, T. (2011) A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333, 1758-1760
53. Yadon, A. N., Van de Mark, D., Basom, R., Delrow, J., Whitehouse, I., and Tsukiyama, T. (2010) Chromatin remodeling around nucleosome-free regions leads to repression of noncoding RNA transcription. Mol. Cell Biol. 30, 5110-5122
54. Chen, K., Wilson, M. A., Hirsch, C., Watson, A., Liang, S., Lu, Y., Li, W., and Dent, S. Y. (2013) Stabilization of the promoter nucleosomes in nucleosome-free regions by the yeast Cyc8-Tup1 corepressor. Genome Res. 23, 312-322
55. Pokholok, D. K., Harbison, C. T., Levine, S., Cole, M., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, P. A., Herbolsheimer, E., Zeitlinger, J., Lewitter, F., Gifford, D. K., and Young, R. A. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517-527
56. Batta, K., Zhang, Z., Yen, K., Goffman, D. B., and Pugh, B. F. (2011) Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev. 25, 2254-2265
57. Cairns, B. R., Kim, Y. J., Sayre, M. H., Laurent, B. C., and Kornberg, R. D. (1994)Amultisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. Proc. Natl. Acad. Sci. U.S.A. 91, 1950-1954
58. Chandrasekharan, M. B., Huang, F., and Sun, Z. W. (2010) Histone H2B ubiquitination and beyond. Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics 5, 460-468
59. Durand-Dubief, M., Will, W. R., Petrini, E., Theodorou, D., Harris, R. R., Crawford, M. R., Paszkiewicz, K., Krueger, F., Correra, R. M., Vetter, A. T., Miller, J. R., Kent, N. A., and Varga-Weisz, P. (2012) SWI/SNF-like chromatin remodeling factor Fun30 supports point centromere function in S. cerevisiae. PLoS Genet. 8, e1002974
60. Hartley, P. D., and Madhani, H. D. (2009) Mechanisms that specify promoter nucleosome location and identity. Cell 137, 445-458
61. Whitehouse, I., Rando, O. J., Delrow, J., and Tsukiyama, T. (2007) Chromatin remodelling at promoters suppresses antisense transcription. Nature 450, 1031-1035
62. Goldmark, J. P., Fazzio, T. G., Estep, P. W., Church, G. M., and Tsukiyama, T. (2000) The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103, 423-433
63. Yen, K., Vinayachandran, V., Batta, K., Koerber, R. T., and Pugh, B. F. (2012) Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149, 1461-1473