The Histone Chaperones FACT and Spt6 Restrict H2A.Z from Intragenic Locations

Molecular Cell

Volumn 58, Issue 6, 2015, Pages 1113-1123

  Jeronimo, Célia ^a   Watanabe, Shinya ^b   Kaplan, Craig D ^c   Peterson, Craig L ^b   Robert, François ^a,d  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; RNA POLYMERASE II; CHROMATIN; HISTONE; HTZ1 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; NUCLEOSOME; POB3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SPT16 PROTEIN, S CEREVISIAE; SPT6 PROTEIN, S CEREVISIAE; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; B CELL LYMPHOMA; CELL CYCLE ARREST; CELL MUTANT; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; DNA METHYLATION; DNA PROTEIN COMPLEX; IMMUNOPRECIPITATION; NUCLEOSOME; PHENOTYPE; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BLOTTING, WESTERN; CHROMATIN; GENE EXPRESSION REGULATION, FUNGAL; HISTONE CHAPERONES; HISTONES; MODELS, GENETIC; MUTATION; NUCLEAR PROTEINS; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 84937640515     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.03.030     Document Type: Article

References (77)

1. Adam M., Robert F., Larochelle M., Gaudreau L. H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol. Cell. Biol. 2001, 21:6270-6279.
2. Ahmed S., Dul B., Qiu X., Walworth N.C. Msc1 acts through histone H2A.Z to promote chromosome stability in Schizosaccharomyces pombe. Genetics 2007, 177:1487-1497.
3. Avvakumov N., Nourani A., Côté J. Histone chaperones: modulators of chromatin marks. Mol. Cell 2011, 41:502-514.
4. Bataille A.R., Jeronimo C., Jacques P.E., Laramée L., Fortin M.E., Forest A., Bergeron M., Hanes S.D., Robert F. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol. Cell 2012, 45:158-170.
5. Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science 2003, 301:1090-1093.
6. Billon P., Côté J. Precise deposition of histone H2A.Z in chromatin for genome expression and maintenance. Biochim. Biophys. Acta 2013, 1819:290-302.
7. Bortvin A., Winston F. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 1996, 272:1473-1476.
8. Brewster N.K., Johnston G.C., Singer R.A. Characterization of the CP complex, an abundant dimer of Cdc68 and Pob3 proteins that regulates yeast transcriptional activation and chromatin repression. J. Biol. Chem. 1998, 273:21972-21979.
9. Burgess R.J., Zhang Z. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 2013, 20:14-22.
10. Chambers A.L., Ormerod G., Durley S.C., Sing T.L., Brown G.W., Kent N.A., Downs J.A. The INO80 chromatin remodeling complex prevents polyploidy and maintains normal chromatin structure at centromeres. Genes Dev. 2012, 26:2590-2603.
11. Cheung V., Chua G., Batada N.N., Landry C.R., Michnick S.W., Hughes T.R., Winston F. Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol. 2008, 6:e277.
12. Chu Y., Sutton A., Sternglanz R., Prelich G. The BUR1 cyclin-dependent protein kinase is required for the normal pattern of histone methylation by SET2. Mol. Cell. Biol. 2006, 26:3029-3038.
13. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
14. Clark-Adams C.D., Norris D., Osley M.A., Fassler J.S., Winston F. Changes in histone gene dosage alter transcription in yeast. Genes Dev. 1988, 2:150-159.
15. Coleman-Derr D., Zilberman D. Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet. 2012, 8:e1002988.
16. Conerly M.L., Teves S.S., Diolaiti D., Ulrich M., Eisenman R.N., Henikoff S. Changes in H2A.Z occupancy and DNA methylation during B-cell lymphomagenesis. Genome Res. 2010, 20:1383-1390.
17. Coulombe C., Poitras C., Nordell-Markovits A., Brunelle M., Lavoie M.A., Robert F., Jacques P.E. VAP: a versatile aggregate profiler for efficient genome-wide data representation and discovery. Nucleic Acids Res. 2014, 42:W485-W493.
18. DeGennaro C.M., Alver B.H., Marguerat S., Stepanova E., Davis C.P., Bähler J., Park P.J., Winston F. Spt6 regulates intragenic and antisense transcription, nucleosome positioning, and histone modifications genome-wide in fission yeast. Mol. Cell. Biol. 2013, 33:4779-4792.
19. Deyter G.M., Biggins S. The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes Dev. 2014, 28:1815-1826.
20. Dryhurst D., Ausió J. Histone H2A.Z deregulation in prostate cancer. Cause or effect?. Cancer Metastasis Rev. 2014, 33:429-439.
21. Fan J.Y., Rangasamy D., Luger K., Tremethick D.J. H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol. Cell 2004, 16:655-661.
22. Garcia H., Miecznikowski J.C., Safina A., Commane M., Ruusulehto A., Kilpinen S., Leach R.W., Attwood K., Li Y., Degan S., et al. Facilitates chromatin transcription complex is an "accelerator" of tumor transformation and potential marker and target of aggressive cancers. Cell Rep. 2013, 4:159-173.
23. Guillemette B., Bataille A.R., Gévry N., Adam M., Blanchette M., Robert F., Gaudreau L. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 2005, 3:e384.
24. Hanai K., Furuhashi H., Yamamoto T., Akasaka K., Hirose S. RSF governs silent chromatin formation via histone H2Av replacement. PLoS Genet. 2008, 4:e1000011.
25. Hardy S., Robert F. Random deposition of histone variants: A cellular mistake or a novel regulatory mechanism?. Epigenetics 2010, 5:368-372.
26. Hardy S., Jacques P.-É., Gévry N., Forest A., Fortin M.-E., Laflamme L., Gaudreau L., Robert F. The euchromatic and heterochromatic landscapes are shaped by antagonizing effects of transcription on H2A.Z deposition. PLoS Genet. 2009, 5:e1000687.
27. Hartzog G.A., Wada T., Handa H., Winston F. Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes Dev. 1998, 12:357-369.
28. Haruki H., Nishikawa J., Laemmli U.K. The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol. Cell 2008, 31:925-932.
29. Heo K., Kim H., Choi S.H., Choi J., Kim K., Gu J., Lieber M.R., Yang A.S., An W. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell 2008, 30:86-97.
30. Ivanovska I., Jacques P.E., Rando O.J., Robert F., Winston F. Control of chromatin structure by spt6: different consequences in coding and regulatory regions. Mol. Cell. Biol. 2011, 31:531-541.
31. Jamai A., Puglisi A., Strubin M. Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol. Cell 2009, 35:377-383.
32. Jeronimo C., Robert F. Kin28 regulates the transient association of Mediator with core promoters. Nat. Struct. Mol. Biol. 2014, 21:449-455.
33. Jiang C., Pugh B.F. A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome. Genome Biol. 2009, 10:R109.
34. Kaplan C.D., Morris J.R., Wu C., Winston F. Spt5 and spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev. 2000, 14:2623-2634.
35. Kaplan C.D., Laprade L., Winston F. Transcription elongation factors repress transcription initiation from cryptic sites. Science 2003, 301:1096-1099.
36. Kobor M.S., Venkatasubrahmanyam S., Meneghini M.D., Gin J.W., Jennings J.L., Link A.J., Madhani H.D., Rine J. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2004, 2:E131.
37. Krogan N.J., Kim M., Ahn S.H., Zhong G., Kobor M.S., Cagney G., Emili A., Shilatifard A., Buratowski S., Greenblatt J.F. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 2002, 22:6979-6992.
38. Krogan N.J., Keogh M.-C., Datta N., Sawa C., Ryan O.W., Ding H., Haw R.A., Pootoolal J., Tong A., Canadien V., et al. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 2003, 12:1565-1576.
39. Krogan N.J., Baetz K., Keogh M.C., Datta N., Sawa C., Kwok T.C., Thompson N.J., Davey M.G., Pootoolal J., Hughes T.R., et al. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc. Natl. Acad. Sci. USA 2004, 101:13513-13518.
40. Lowary P.T., Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 1998, 276:19-42.
41. Luger K., Rechsteiner T.J., Richmond T.J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 1999, 119:1-16.
42. Luger K., Rechsteiner T.J., Richmond T.J. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 1999, 304:3-19.
43. Malik H.S., Henikoff S. Phylogenomics of the nucleosome. Nat. Struct. Biol. 2003, 10:882-891.
44. Malone E.A., Clark C.D., Chiang A., Winston F. Mutations in SPT16/CDC68 suppress cis- and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol. Cell. Biol. 1991, 11:5710-5717.
45. Mao Z., Pan L., Wang W., Sun J., Shan S., Dong Q., Liang X., Dai L., Ding X., Chen S., et al. Anp32e, a higher eukaryotic histone chaperone directs preferential recognition for H2A.Z. Cell Res. 2014, 24:389-399.
46. Mason P.B., Struhl K. The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol. Cell. Biol. 2003, 23:8323-8333.
47. McDonald S.M., Close D., Xin H., Formosa T., Hill C.P. Structure and biological importance of the Spn1-Spt6 interaction, and its regulatory role in nucleosome binding. Mol. Cell 2010, 40:725-735.
48. Mizuguchi G., Shen X., Landry J., Wu W.-H., Sen S., Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 2004, 303:343-348.
49. Monteiro F.L., Baptista T., Amado F., Vitorino R., Jerónimo C., Helguero L.A. Expression and functionality of histone H2A variants in cancer. Oncotarget 2014, 5:3428-3443.
50. Morillo-Huesca M., Maya D., Muñoz-Centeno M.C., Singh R.K., Oreal V., Reddy G.U., Liang D., Géli V., Gunjan A., Chávez S. FACT prevents the accumulation of free histones evicted from transcribed chromatin and a subsequent cell cycle delay in G1. PLoS Genet. 2010, 6:e1000964.
51. Narlikar G.J., Sundaramoorthy R., Owen-Hughes T. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 2013, 154:490-503.
52. Obri A., Ouararhni K., Papin C., Diebold M.L., Padmanabhan K., Marek M., Stoll I., Roy L., Reilly P.T., Mak T.W., et al. ANP32E is a histone chaperone that removes H2A.Z from chromatin. Nature 2014, 505:648-653.
53. Orphanides G., LeRoy G., Chang C.H., Luse D.S., Reinberg D. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 1998, 92:105-116.
54. Papamichos-Chronakis M., Watanabe S., Rando O.J., Peterson C.L. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 2011, 144:200-213.
55. Perales R., Erickson B., Zhang L., Kim H., Valiquett E., Bentley D. Gene promoters dictate histone occupancy within genes. EMBO J. 2013, 32:2645-2656.
56. Prendergast J.A., Murray L.E., Rowley A., Carruthers D.R., Singer R.A., Johnston G.C. Size selection identifies new genes that regulate Saccharomyces cerevisiae cell proliferation. Genetics 1990, 124:81-90.
57. Rangasamy D. Histone variant H2A.Z can serve as a new target for breast cancer therapy. Curr. Med. Chem. 2010, 17:3155-3161.
58. Rangasamy D., Greaves I., Tremethick D.J. RNA interference demonstrates a novel role for H2A.Z in chromosome segregation. Nat. Struct. Mol. Biol. 2004, 11:650-655.
59. Ranjan A., Mizuguchi G., FitzGerald P.C., Wei D., Wang F., Huang Y., Luk E., Woodcock C.L., Wu C. Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement. Cell 2013, 154:1232-1245.
60. Ren B., Robert F., Wyrick J.J., Aparicio O., Jennings E.G., Simon I., Zeitlinger J., Schreiber J., Hannett N., Kanin E., et al. Genome-wide location and function of DNA binding proteins. Science 2000, 290:2306-2309.
61. Rossetto D., Cramet M., Wang A.Y., Steunou A.L., Lacoste N., Schulze J.M., Côté V., Monnet-Saksouk J., Piquet S., Nourani A., et al. Eaf5/7/3 form a functionally independent NuA4 submodule linked to RNA polymerase II-coupled nucleosome recycling. EMBO J. 2014, 33:1397-1415.
62. Santisteban M.S., Hang M., Smith M.M. Histone variant H2A.Z and RNA polymerase II transcription elongation. Mol. Cell. Biol. 2011, 31:1848-1860.
63. Sarcinella E., Zuzarte P.C., Lau P.N., Draker R., Cheung P. Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol. Cell. Biol. 2007, 27:6457-6468.
64. Schwabish M.A., Struhl K. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 2004, 24:10111-10117.
65. Suganuma T., Workman J.L. Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 2011, 80:473-499.
66. Swaminathan J., Baxter E.M., Corces V.G. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev. 2005, 19:65-76.
67. Talbert P.B., Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 2010, 11:264-275.
68. Tessarz P., Kouzarides T. Histone core modifications regulating nucleosome structure and dynamics. Nat. Rev. Mol. Cell Biol. 2014, 15:703-708.
69. Voth W.P., Takahata S., Nishikawa J.L., Metcalfe B.M., Näär A.M., Stillman D.J. A role for FACT in repopulation of nucleosomes at inducible genes. PLoS ONE 2014, 9:e84092.
70. Weber C.M., Henikoff S. Histone variants: dynamic punctuation in transcription. Genes Dev. 2014, 28:672-682.
71. Weber C.M., Ramachandran S., Henikoff S. Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol. Cell 2014, 53:819-830.
72. Winston F., Chaleff D.T., Valent B., Fink G.R. Mutations affecting Ty-mediated expression of the HIS4 gene of Saccharomyces cerevisiae. Genetics 1984, 107:179-197.
73. Yen K., Vinayachandran V., Pugh B.F. SWR-C and INO80 chromatin remodelers recognize nucleosome-free regions near +1 nucleosomes. Cell 2013, 154:1246-1256.
74. Yoh S.M., Cho H., Pickle L., Evans R.M., Jones K.A. The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export. Genes Dev. 2007, 21:160-174.
75. Youdell M.L., Kizer K.O., Kisseleva-Romanova E., Fuchs S.M., Duro E., Strahl B.D., Mellor J. Roles for Ctk1 and Spt6 in regulating the different methylation states of histone H3 lysine 36. Mol. Cell. Biol. 2008, 28:4915-4926.
76. Zilberman D., Coleman-Derr D., Ballinger T., Henikoff S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 2008, 456:125-129.
77. Zlatanova J., Thakar A. H2A.Z: view from the top. Structure 2008, 16:166-179.