The mitotic Clb cyclins are required to alleviate HIR-mediated repression of the yeast histone genes at the G1/S transition

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 1, 2012, Pages 16-27

  Amin, Amit Dipak ^a   Dimova, Dessislava K ^b   Ferreira, Monica E ^a   Vishnoi, Nidhi ^a   Hancock, Leandria C ^a   Osley, Mary Ann ^c   Prochasson, Philippe ^a  

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

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Asf1; Cell cycle; Clb cyclin; HIR complex; Histone gene; Rtt106

Indexed keywords

CYCLIN B1; CYCLIN B2; CYCLINE; HISTONE; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; HISTONE TRANSCRIPTION REGULATOR 1; HISTONE TRANSCRIPTION REGULATOR 2; HISTONE TRANSCRIPTION REGULATOR 3; PROTEIN; PROTEIN CDC42; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA HISTONE INTERACTION; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME SYNTHESIS; GENE EXPRESSION; GENE LOCUS; GENE REPRESSION; GENETIC TRANSCRIPTION; HISTONE UBIQUITINATION; IN VIVO STUDY; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UBIQUITINATION;

CELL CYCLE PROTEINS; CYCLIN B; CYCLINS; DNA-BINDING PROTEINS; F-BOX PROTEINS; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; MITOSIS; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES;

EID: 81055138247     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.09.003     Document Type: Article

References (85)

1. Wittenberg C., Reed S.I. Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes. Oncogene 2005, 24:2746-2755.
2. Bahler J. Cell-cycle control of gene expression in budding and fission yeast. Annu. Rev. Genet. 2005, 39:69-94.
3. Dynlacht B.D. Regulation of transcription by proteins that control the cell cycle. Nature 1997, 389:149-152.
4. Koch C., Nasmyth K. Cell cycle regulated transcription in yeast. Curr. Opin. Cell Biol. 1994, 6:451-459.
5. Nasmyth K. At the heart of the budding yeast cell cycle. Trends Genet. 1996, 12:405-412.
6. Spellman P.T., Sherlock G., Zhang M.Q., Iyer V.R., Anders K., Eisen M.B., Brown P.O., Botstein D., Futcher B. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 1998, 9:3273-3297.
7. Andrews B., Measday V. The cyclin family of budding yeast: abundant use of a good idea. Trends Genet. 1998, 14:66-72.
8. Amon A., Tyers M., Futcher B., Nasmyth K. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 1993, 74:993-1007.
9. Koch C., Schleiffer A., Ammerer G., Nasmyth K. Switching transcription on and off during the yeast cell cycle: Cln/Cdc28 kinases activate bound transcription factor SBF (Swi4/Swi6) at start, whereas Clb/Cdc28 kinases displace it from the promoter in G2. Genes Dev. 1996, 10:129-141.
10. Althoefer H., Schleiffer A., Wassmann K., Nordheim A., Ammerer G. Mcm1 is required to coordinate G2-specific transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 1995, 15:5917-5928.
11. Maher M., Cong F., Kindelberger D., Nasmyth K., Dalton S. Cell cycle-regulated transcription of the CLB2 gene is dependent on Mcm1 and a ternary complex factor. Mol. Cell. Biol. 1995, 15:3129-3137.
12. Moll T., Tebb G., Surana U., Robitsch H., Nasmyth K. The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5. Cell 1991, 66:743-758.
13. Sanders S.L., Herskowitz I. The BUD4 protein of yeast, required for axial budding, is localized to the mother/BUD neck in a cell cycle-dependent manner. J. Cell Biol. 1996, 134:413-427.
14. Chan H.M., Shikama N., La Thangue N.B. Control of gene expression and the cell cycle. Essays Biochem. 2001, 37:87-96.
15. Dyson N. The regulation of E2F by pRB-family proteins. Genes Dev. 1998, 12:2245-2262.
16. Frolov M.V., Dyson N.J. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci. 2004, 117:2173-2181.
17. Helin K. Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev. 1998, 8:28-35.
18. Zwicker J., Muller R. Cell-cycle regulation of gene expression by transcriptional repression. Trends Genet. 1997, 13:3-6.
19. Adams P.D., Li X., Sellers W.R., Baker K.B., Leng X., Harper J.W., Taya Y., Kaelin W.G. Retinoblastoma protein contains a C-terminal motif that targets it for phosphorylation by cyclin-cdk complexes. Mol. Cell. Biol. 1999, 19:1068-1080.
20. Kato J., Matsushime H., Hiebert S.W., Ewen M.E., Sherr C.J. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 1993, 7:331-342.
21. Costanzo M., Nishikawa J.L., Tang X., Millman J.S., Schub O., Breitkreuz K., Dewar D., Rupes I., Andrews B., Tyers M. CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 2004, 117:899-913.
22. de Bruin R.A., McDonald W.H., Kalashnikova T.I., Yates J., Wittenberg C. Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. Cell 2004, 117:887-898.
23. Gunjan A., Paik J., Verreault A. Regulation of histone synthesis and nucleosome assembly. Biochimie 2005, 87:625-635.
24. Osley M.A. The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 1991, 60:827-861.
25. Freeman K.B., Karns L.R., Lutz K.A., Smith M.M. Histone H3 transcription in Saccharomyces cerevisiae is controlled by multiple cell cycle activation sites and a constitutive negative regulatory element. Mol. Cell. Biol. 1992, 12:5455-5463.
26. Osley M.A., Gould J., Kim S., Kane M.Y., Hereford L. Identification of sequences in a yeast histone promoter involved in periodic transcription. Cell 1986, 45:537-544.
27. Eriksson P.R., Ganguli D., Clark D.J. Spt10 and Swi4 control the timing of histone H2A/H2B gene activation in budding yeast. Mol. Cell. Biol. 2011, 31:557-572.
28. Spector M.S., Raff A., DeSilva H., Lee K., Osley M.A. Hir1p and Hir2p function as transcriptional corepressors to regulate histone gene transcription in the Saccharomyces cerevisiae cell cycle. Mol. Cell. Biol. 1997, 17:545-552.
29. Osley M.A., Lycan D. Trans-acting regulatory mutations that alter transcription of Saccharomyces cerevisiae histone genes. Mol. Cell. Biol. 1987, 7:4204-4210.
30. Xu H., Kim U.J., Schuster T., Grunstein M. Identification of a new set of cell cycle-regulatory genes that regulate S-phase transcription of histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 1992, 12:5249-5259.
31. DeSilva H., Lee K., Osley M.A. Functional dissection of yeast Hir1p, a WD repeat-containing transcriptional corepressor. Genetics 1998, 148:657-667.
32. Sherwood P.W., Tsang S.V., Osley M.A. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 1993, 13:28-38.
33. Green E.M., Antczak A.J., Bailey A.O., Franco A.A., Wu K.J., Yates J.R., Kaufman P.D. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 2005, 15:2044-2049.
34. Prochasson P., Florens L., Swanson S.K., Washburn M.P., Workman J.L. The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 2005, 19:2534-2539.
35. Amin A.D., Vishnoi N., Prochasson P. A global requirement for the HIR complex in the assembly of chromatin. Biochim. Biophys. Acta, Gene Regul. Mech. 2011, 10.1016/j.bbagrm.2011.07.008.
36. Lamour V., Lecluse Y., Desmaze C., Spector M., Bodescot M., Aurias A., Osley M.A., Lipinski M. A human homolog of the S. cerevisiae HIR1 and HIR2 transcriptional repressors cloned from the DiGeorge syndrome critical region. Hum. Mol. Genet. 1995, 4:791-799.
37. L. Moran, Factors involved in temporal and autogenous control of histone synthesis in Saccharomyces cerevisiae, in, vol. Ph.D. Thesis, New York: Cornell University, 1994.
38. Vishnoi N., Flaherty K., Hancock L.C., Ferreira M.E., Amin A.D., Prochasson P. Separation-of-function mutation in HPC2, a member of the HIR complex in S. cerevisiae, results in derepression of the histone genes but does not confer cryptic TATA phenotypes. Biochim. Biophys. Acta, Gene Regul. Mech. 2011, 1809:557-566.
39. Dimova D., Nackerdien Z., Furgeson S., Eguchi S., Osley M.A. A role for transcriptional repressors in targeting the yeast Swi/Snf complex. Mol. Cell 1999, 4:75-83.
40. Fillingham J., Kainth P., Lambert J.P., van Bakel H., Tsui K., Pena-Castillo L., Nislow C., Figeys D., Hughes T.R., Greenblatt J., Andrews B.J. Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression. Mol. Cell 2009, 35:340-351.
41. Ferreira M.E., Flaherty K., Prochasson P. The Saccharomyces cerevisiae histone chaperone Rtt106 mediates the cell cycle recruitment of SWI/SNF and RSC to the HIR-dependent histone genes. PLoS One 2011, 6:e21113.
42. Ng H.H., Robert F., Young R.A., Struhl K. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev. 2002, 16:806-819.
43. Hill J., Donald K.A., Griffiths D.E. DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res. 1991, 19:5791.
44. Hereford L.M., Osley M.A., Ludwig T.R., McLaughlin C.S. Cell-cycle regulation of yeast histone mRNA. Cell 1981, 24:367-375.
45. Moran L., Norris D., Osley M.A. A yeast H2A-H2B promoter can be regulated by changes in histone gene copy number. Genes Dev. 1990, 4:752-763.
46. Cross S.L., Smith M.M. Comparison of the structure and cell cycle expression of mRNAs encoded by two histone H3-H4 loci in Saccharomyces cerevisiae. Mol. Cell. Biol. 1988, 8:945-954.
47. Hereford L., Bromley S., Osley M.A. Periodic transcription of yeast histone genes. Cell 1982, 30:305-310.
48. White J.H., Green S.R., Barker D.G., Dumas L.B., Johnston L.H. The CDC8 transcript is cell cycle regulated in yeast and is expressed coordinately with CDC9 and CDC21 at a point preceding histone transcription. Exp. Cell Res. 1987, 171:223-231.
49. Feldman R.M., Correll C.C., Kaplan K.B., Deshaies R.J. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 1997, 91:221-230.
50. Mathias N., Johnson S.L., Winey M., Adams A.E., Goetsch L., Pringle J.R., Byers B., Goebl M.G. Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identifies a conserved family of proteins. Mol. Cell. Biol. 1996, 16:6634-6643.
51. Schneider B.L., Yang Q.H., Futcher A.B. Linkage of replication to start by the Cdk inhibitor Sic1. Science 1996, 272:560-562.
52. Schwob E., Bohm T., Mendenhall M.D., Nasmyth K. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 1994, 79:233-244.
53. Skowyra D., Craig K.L., Tyers M., Elledge S.J., Harper J.W. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 1997, 91:209-219.
54. DeSalle L.M., Pagano M. Regulation of the G1 to S transition by the ubiquitin pathway. FEBS Lett. 2001, 490:179-189.
55. Breeden L. Cell cycle-regulated promoters in budding yeast. Trends Genet. 1988, 4:249-253.
56. Patton E.E., Willems A.R., Tyers M. Combinatorial control in ubiquitin-dependent proteolysis: don't Skp the F-box hypothesis. Trends Genet. 1998, 14:236-243.
57. Peters J.M. SCF and APC: the Yin and Yang of cell cycle regulated proteolysis. Curr. Opin. Cell Biol. 1998, 10:759-768.
58. Willems A.R., Goh T., Taylor L., Chernushevich I., Shevchenko A., Tyers M. SCF ubiquitin protein ligases and phosphorylation-dependent proteolysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:1533-1550.
59. Epstein C.B., Cross F.R. CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 1992, 6:1695-1706.
60. Kuhne C., Linder P. A new pair of B-type cyclins from Saccharomyces cerevisiae that function early in the cell cycle. EMBO J. 1993, 12:3437-3447.
61. Schwob E., Nasmyth K. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 1993, 7:1160-1175.
62. Amon A., Irniger S., Nasmyth K. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 1994, 77:1037-1050.
63. Han M., Grunstein M. Nucleosome loss activates yeast downstream promoters in vivo. Cell 1988, 55:1137-1145.
64. Kim U.J., Han M., Kayne P., Grunstein M. Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J. 1988, 7:2211-2219.
65. Fitch I., Dahmann C., Surana U., Amon A., Nasmyth K., Goetsch L., Byers B., Futcher B. Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell 1992, 3:805-818.
66. Richardson H., Lew D.J., Henze M., Sugimoto K., Reed S.I. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes Dev. 1992, 6:2021-2034.
67. Bloom J., Cross F.R. Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. Mol. Cell Biol. 2007, 8:149-160.
68. D. Dimova, Antagonizing transcriptional repression of a cell cycle regulated yeast promoter, in, vol. Ph.D. Thesis, New York: Cornell University, 2000.
69. Sutton A., Bucaria J., Osley M.A., Sternglanz R. Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics 2001, 158:587-596.
70. Eriksson P.R., Mendiratta G., McLaughlin N.B., Wolfsberg T.G., Marino-Ramirez L., Pompa T.A., Jainerin M., Landsman D., Shen C.H., Clark D.J. Global regulation by the yeast Spt10 protein is mediated through chromatin structure and the histone upstream activating sequence elements. Mol. Cell. Biol. 2005, 25:9127-9137.
71. Hess D., Winston F. Evidence that Spt10 and Spt21 of Saccharomyces cerevisiae play distinct roles in vivo and functionally interact with MCB-binding factor, SCB-binding factor and Snf1. Genetics 2005, 170:87-94.
72. Hierck B.P., Molin D.G., Boot M.J., Poelmann R.E., Gittenberger-de Groot A.C. A chicken model for DGCR6 as a modifier gene in the DiGeorge critical region. Pediatr. Res. 2004, 56:440-448.
73. Iyer V.R., Horak C.E., Scafe C.S., Botstein D., Snyder M., Brown P.O. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 2001, 409:533-538.
74. Koch C., Moll T., Neuberg M., Ahorn H., Nasmyth K. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 1993, 261:1551-1557.
75. Moll T., Schwob E., Koch C., Moore A., Auer H., Nasmyth K. Transcription factors important for starting the cell cycle in yeast. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1993, 340:351-360.
76. Simon I., Barnett J., Hannett N., Harbison C.T., Rinaldi N.J., Volkert T.L., Wyrick J.J., Zeitlinger J., Gifford D.K., Jaakkola T.S., Young R.A. Serial regulation of transcriptional regulators in the yeast cell cycle. Cell 2001, 106:697-708.
77. Xu F., Zhang K., Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 2005, 121:375-385.
78. Surana U., Robitsch H., Price C., Schuster T., Fitch I., Futcher A.B., Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 1991, 65:145-161.
79. Amon A., Surana U., Muroff I., Nasmyth K. Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature 1992, 355:368-371.
80. Kellogg D.R., Murray A.W. NAP1 acts with Clb1 to perform mitotic functions and to suppress polar bud growth in budding yeast. J. Cell Biol. 1995, 130:675-685.
81. Ubersax J.A., Woodbury E.L., Quang P.N., Paraz M., Blethrow J.D., Shah K., Shokat K.M., Morgan D.O. Targets of the cyclin-dependent kinase Cdk1. Nature 2003, 425:859-864.
82. Cross F.R., Schroeder L., Bean J.M. Phosphorylation of the Sic1 inhibitor of B-type cyclins in Saccharomyces cerevisiae is not essential but contributes to cell cycle robustness. Genetics 2007, 176:1541-1555.
83. Loog M., Morgan D.O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 2005, 434:104-108.
84. Hall C., Nelson D.M., Ye X., Baker K., DeCaprio J.A., Seeholzer S., Lipinski M., Adams P.D. HIRA, the human homologue of yeast Hir1p and Hir2p, is a novel cyclin-cdk2 substrate whose expression blocks S-phase progression. Mol. Cell. Biol. 2001, 21:1854-1865.
85. Lambert J.P., Fillingham J., Siahbazi M., Greenblatt J., Baetz K., Figeys D. Defining the budding yeast chromatin-associated interactome. Mol. Syst. Biol. 2010, 6:448.