A role for Chd1 and Set2 in negatively regulating DNA replication in Saccharomyces cerevisiae

Genetics

Volumn 178, Issue 2, 2008, Pages 649-659

  Biswas, Debabrata ^a,b   Takahata, Shinya ^a   Xin, Hua ^a   Dutta Biswas, Rinku ^a   Yu, Yaxin ^a   Formosa, Tim ^a   Stillman, David J ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; METHYLTRANSFERASE; PROTEIN CHD1; PROTEIN CTF4; PROTEIN MEC1; PROTEIN ORC2; PROTEIN SERINE THREONINE KINASE; PROTEIN SET2; RIBONUCLEOTIDE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA REPLICATION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

CHROMATIN; DNA REPLICATION; DNA-BINDING PROTEINS; GENE DELETION; HYDROXYUREA; METHYLTRANSFERASES; MUTAGENESIS; MUTATION; RIBONUCLEOSIDE DIPHOSPHATE REDUCTASE; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 40849124522     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.084202     Document Type: Article

References (77)

1. ALCASABAS, A. A., A. J. OSBORN, J. BACHANT, F. HU, P. J. WERLER et al., 2001 Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3: 958-965.
2. BAO, Y., and X. SHEN, 2007 Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 17: 126-131.
3. BELOTSERKOVSKAYA, R., S. OH, V. A. BONDARENKO, G. ORPHANIDES, V. M. STUDITSKY et al., 2003 FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
4. BERGER, S. L., 2007 The complex language of chromatin regulation during transcription. Nature 447: 407-412.
5. BETZ, J. L., M. CHANG, T. M. WASHBURN, S. E. PORTER, C. L. MUELLER et al., 2002 Phenotypic analysis of Paf1/RNA polymerase II complex mutations reveals connections to cell cycle regulation, protein synthesis, and lipid and nucleic acid metabolism. Mol. Genet. Genomics 268: 272-285.
6. BHOITE, L. T., and D. J. STILLMAN, 1998 Residues in the Swi5 zinc finger protein that mediate cooperative DNA-binding with the Pho2 homeodomain protein. Mol. Cell. Biol. 18: 6436-6446.
7. BISWAS, D., Y. YU, M. PRALL, T. FORMOSA and D. J. STILLMAN, 2005 The yeast FACT complex has a role in transcriptional initiation. Mol. Cell. Biol. 25: 5812-5822.
8. BISWAS, D., R. DUTTA-BISWAS, D. MITRA, Y. SHIBATA, B. D. STRAHL et al., 2006 Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J. 25: 4479-4489.
9. BISWAS, D., R. DUTTA-BISWAS and D. J. STILLMAN, 2007 Chd1 and yFACT act in opposition in regulating transcription. Mol. Cell. Biol. 27: 6279-6287.
10. BOSTELMAN, L. J., A. M. KELLER, A. M. ALBRECHT, A. ARAT and J. S. THOMPSON, 2007 Methylation of histone H3 lysine-79 by Dot1p plays multiple roles in the response to UV damage in Saccharomyces cerevisiae. DNA Repair 6: 383-395.
11. BREWSTER, N. K., G. C. JOHNSTON and R. A. SINGER, 2001 A bipartite yeast SSRP1 analog comprised of Pob3 and Nhp6 proteins modulates transcription. Mol. Cell. Biol. 21: 3491-3502.
12. BUDD, M. E., A. H. TONG, P. POLACZEK, X. PENG, C. BOONE et al., 2005 A network of multi-tasking proteins at the DNA replication fork preserves genome stability. PLoS Genet. 1: e61.
13. CAIRNS, B. R., 2005 Chromatin remodeling complexes: strength in diversity, precision through specialization. Curr. Opin. Genet. Dev. 15: 185-190.
14. CARROZZA, M. J., B. LI, L. FLORENS, T. SUGANUMA, S. K. SWANSON et al., 2005 Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581-592.
15. CHA, R. S., and N. KLECKNER, 2002 ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602-606.
16. CORDA, Y., V. SCHRAMKE, M. P. LONGHESE, T. SMOKVINA, V. PACIOTTI et al., 1999 Interaction between Set1p and checkpoint protein Mec3p in DNA repair and telomere functions. Nat. Genet. 21: 204-208.
17. DA-SILVA, L. F., and B. P. DUNCKER, 2007 ORC function in late G1: maintaining the license for DNA replication. Cell Cycle 6: 128-130.
18. DANIEL, J. A., M. G. PRAY-GRANT and P. A. GRANT, 2005 Effector proteins for methylated histones: an expanding family. Cell Cycle 4: 919-926.
19. DESANY, B. A., A. A. ALCASABAS, J. B. BACHANT and S. J. ELLEDGE, 1998 Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12: 2956-2970.
20. DRYHURST, D., A. A. THAMBIRAJAH and J. AUSIO, 2004 New twists on H2A.Z: a histone variant with a controversial structural and functional past. Biochem. Cell Biol. 82: 490-497.
21. EKLUND, H., U. UHLIN, M. FARNEGARDH, D. T. LOGAN and P. NORDLUND, 2001 Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 77: 177-268.
22. FLANAGAN, J. F., B. J. BLUS, D. KIM, K. L. CLINES, F. RASTINEJAD et al., 2007 Molecular implications of evolutionary differences in CHD double chromodomains. J. Mol. Biol. 369: 334-342.
23. FOIANI, M., A. PELLICIOLI, M. LOPES, C. LUCCA, M. FERRARI et al., 2000 DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae. Mutat. Res. 451: 187-196.
24. FORMOSA, T., 2003 Changing the DNA landscape: putting a SPN on chromatin. Curr. Top. Microbiol. Immunol. 274: 171-201.
25. FORMOSA, T., P. ERIKSSON, J. WITTMEYER, J. GINN, Y. YU et al., 2001 Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. EMBO J. 20: 3506-3517.
26. FORMOSA, T., S. RUONE, M. D. ADAMS, A. E. OLSEN, P. ERIKSSON et al., 2002 Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162: 1557-1571.
27. GREEN, E. M., A. J. ANTCZAK, A. O. BAILEY, A. A. FRANCO, K. J. WU et al., 2005 Replication- independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15: 2044-2049.
28. GUNJAN, A., J. PAIK and A. VERREAULT, 2005 Regulation of histone synthesis and nucleosome assembly. Biochimie 87: 625-635.
29. HANNA, J. S., E. S. KROLL, V. LUNDBLAD and F. A. SPENCER, 2001 Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol. Cell. Biol. 21: 3144-3158.
30. JOSHI, A. A., and K. STRUHL, 2005 Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20: 971-978.
31. KAI, M., and T. S. WANG, 2003 Checkpoint responses to replication stalling: inducing tolerance and preventing mutagenesis. Mutat. Res. 532: 59-73.
32. KAPLAN, C. D., L. LAPRADE and F. WINSTON, 2003 Transcription elongation factors repress transcription initiation from cryptic sites. Science 301: 1096-1099.
33. KELLEY, D. E., D. G. STOKES and R. P. PERRY, 1999 CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/ helicase-like domain for proper association with chromatin. Chromosoma 108: 10-25.
34. KEOGH, M. C., S. K. KURDISTANI, S. A. MORRIS, S. H. AHN, V. PODOLNY et al., 2005 Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605.
35. KOC, A., L. J. WHEELER, C. K. MATHEWS and G. F. MERRILL, 2004 Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J. Biol. Chem. 279: 223-230.
36. KROGAN, N. J., M. KIM, S. H. AHN, G. ZHONG, M. S. KOBOR et al., 2002 RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22: 6979-6992.
37. KROGAN, N. J., M. KIM, A. TONG, A. GOLSHANI, G. CAGNEY et al., 2003 Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23: 4207-4218.
38. LI, B., L. HOWE, S. ANDERSON, J. R. YATES, 3RD and J. L. WORKMAN, 2003 The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 278: 8897-8903.
39. LIU, C. L., T. KAPLAN, M. KIM, S. BURATOWSKI, S. L. SCHREIBER et al., 2005 Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3: e328.
40. LOPES, M., C. COTTA-RAMUSINO, A. PELLICIOLI, G. LIBERI, P. PLEVANI et al., 2001 The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
41. MALONE, E. A., C. D. CLARK, A. CHIANG and F. WINSTON, 1991 Mutations in SPT68/CDC68 suppress cis- and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 5710-5717.
42. MASON, P. B., and K. STRUHL, 2003 The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol. Cell. Biol. 23: 8323-8333.
43. MITRA, D., E. J. PARNELL, J. W. LANDON, Y. YU and D. J. STILLMAN, 2006 SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment. Mol. Cell. Biol. 26: 4095-4110.
44. MORRISON, A. J., J. HIGHLAND, N. J. KROGAN, A. ARBEL-EDEN, J. F. GREENBLATT et al., 2004 INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119: 767-775.
45. NEDELCHEVA-VELEVA, M. N., D. B. KRASTEV and S. S. STOYNOV, 2006 Coordination of DNA synthesis and replicative unwinding by the S-phase checkpoint pathways. Nucleic Acids Res. 34: 4138-4146.
46. O'DONNELL, A. F., N. K. BREWSTER, J. KURNIAWAN, L. V. MINARD, G. C. JOHNSTON et al., 2004 Domain organization of the yeast histone chaperone FACT: the conserved N-terminal domain of FACT subunit Spt16 mediates recovery from replication stress. Nucleic Acids Res. 32: 5894-5906.
47. OKUHARA, K., K. OHTA, H. SEO, M. SHIODA, T. YAMADA et al., 1999 A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr. Biol. 9: 341-350.
48. ORPHANIDES, G., G. LEROY, C. H. CHANG, D. S. LUSE and D. REINBERG, 1998 FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92: 105-116.
49. ORPHANIDES, G., W. H. WU, W. S. LANE, M. HAMPSEY and D. REINBERG, 1999 The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400: 284-288.
50. PARSONS, A. B., R. L. BROST, H. DING, Z. LI, C. ZHANG et al., 2004 Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 22: 62-69.
51. PASERO, P., K. SHIMADA and B. P. DUNCKER, 2003 Multiple roles of replication forks in S phase checkpoints: sensors, effectors and targets. Cell Cycle 2: 568-572.
52. POKHOLOK, D. K., C. T. HARBISON, S. LEVINE, M. COLE, N. M. HANNETT et al., 2005 Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
53. PROCHASSON, P., L. FLORENS, S. K. SWANSON, M. P. WASHBURN and J. L. WORKMAN, 2005 The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 19: 2534-2539.
54. RAO, B., Y. SHIBATA, B. D. STRAHL and J. D. LIEB, 2005 Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide. Mol. Cell. Biol. 25: 9447-9459.
55. RAY-GALLET, D., J. P. QUIVY, C. SCAMPS, E. M. MARTINI, M. LIPINSKI et al., 2002 HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 9: 1091-1100.
56. RHOADES, A. R., S. RUONE and T. FORMOSA, 2004 Structural features of nucleosomes reorganized by yeast FACT and its HMG box component, Nhp6. Mol. Cell. Biol. 24: 3907-3917.
57. ROWLEY, A., R. A. SINGER and J. C. JOHNSTON, 1991 CDC68, a yeast gene that affects regulation of cell proliferation and transcription, encodes a protein with a highly acidic carboxyl terminus. Mol. Cell. Biol. 11: 5718-5726.
58. SAUNDERS, A., J. WERNER, E. D. ANDRULIS, T. NAKAYAMA, S. HIROSE et al., 2003 Tracking FACTand the RNA polymerase II elongation complex through chromatin in vivo. Science 301: 1094-1096.
59. SCHLESINGER, M. B., and T. FORMOSA, 2000 POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155: 1593-1606.
60. SCHRAMKE, V., H. NEECKE, V. BREVET, Y. CORDA, G. LUCCHINI et al., 2001 The set1Δ mutation unveils a novel signaling pathway relayed by the Rad53-dependent hyperphosphorylation of replication protein A that leads to transcriptional activation of repair genes. Genes Dev. 15: 1845-1858.
61. SHERMAN, F., 1991 Getting started with yeast. Methods Enzymol. 194: 1-21.
62. SIMIC, R., D. L. LINDSTROM, H. G. TRAN, K. L. ROINICK, P. J. COSTA et al., 2003 Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J. 22: 1846-1856.
63. SOLLIER, J., W. LIN, C. SOUSTELLE, K. SUHRE, A. NICOLAS et al., 2004 Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J. 23: 1957-1967.
64. STRAHL, B. D., P. A. GRANT, S. D. BRIGGS, Z. W. SUN, J. R. BONE et al., 2002 Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell. Biol. 22: 1298-1306.
65. TERCERO, J. A., and J. F. DIFFLEY, 2001 Regulation of DNA replication fork progression through damaged DNA by the Mec1/ Rad53 checkpoint. Nature 412: 553-557.
66. TRAN, H. G., D. J. STEGER, V. R. IYER and A. D. JOHNSON, 2000 The chromo domain protein chd1p from budding yeast is an ATP-dependent chromatin-modifying factor. EMBO J. 19: 2323-2331.
67. TSUKIYAMA, T., J. PALMER, C. C. LANDEL, J. SHILOACH and C. WU, 1999 Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 13: 686-697.
68. VAN ATTIKUM, H., and S. M. GASSER, 2005 The histone code at DNA breaks: A guide to repair? Nat. Rev. Mol. Cell. Biol. 6: 757-765.
69. VANDEMARK, A. P., M. BLANKSMA, E. FERRIS, A. HEROUX, C. P. HILL et al., 2006 The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol. Cell 22: 363-374.
70. VANDEMARK, A. P., X. XIN, L. MCCULLOUGH, R. RAWLINS, S. BENTLEY et al., 2008 Structural and functional analysis of the Spt16p Nterminal domain reveals overlapping roles of yFACT subunits. J. Biol. Chem. (in press).
71. WITTMEYER, J., and T. FORMOSA, 1997 The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/ Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17: 4178-4190.
72. WITTMEYER, J., L. JOSS and T. FORMOSA, 1999 Spt16 and Pob3 of Saccharomyces cerevisiae form an essential, abundant heterodimer that is nuclear, chromatin-associated, and copurifies with DNA polymerase alpha. Biochemistry 38: 8961-8971.
73. WOODAGE, T., M. A. BASRAI, A. D. BAXEVANIS, P. HIETER and F. S. COLLINS, 1997 Characterization of the CHD family of proteins. Proc. Natl. Acad. Sci. USA 94: 11472-11477.
74. WYSOCKI, R., A. JAVAHERI, S. ALLARD, F. SHA, J. COTE et al., 2005 Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25: 8430-8443.
75. XIAO, T., H. HALL, K. O. KIZER, Y. SHIBATA, M. C. HALL et al., 2003 Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17: 654-663.
76. ZHAO, X., E. G. MULLER and R. ROTHSTEIN, 1998 A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2: 329-340.
77. ZHOU, Y., and T. S. WANG, 2004 A coordinated temporal interplay of nucleosome reorganization factor, sister chromatin cohesion factor, and DNA polymerase alpha facilitates DNA replication. Mol. Cell. Biol. 24: 9568-9579.