The fission yeast homeodomain protein Yox1p binds to MBF and confines MBF-dependent cell-cycle transcription to G1-S via negative feedback

PLoS Genetics

Volumn 5, Issue 8, 2009, Pages

  Aligianni, Sofia ^a,d   Lackner, Daniel H ^a,e   Klier, Steffi ^b   Rustici, Gabriella ^c   Wilhelm, Brian T ^a,f   Marguerat, Samuel ^a   Codlin, Sandra ^a   Brazma, Alvis ^c   De Bruin, Robertus A M ^b   Bähler, Jürg ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^f INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; HOMEODOMAIN PROTEIN; HOMEODOMAIN PROTEIN YOX1P; MLUI CELL CYCLE BOX BINDING FACTOR; UNCLASSIFIED DRUG; DSC1 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN; TRANSCRIPTION FACTOR; YOX1 PROTEIN, S POMBE;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME REPRESSION; GENE DELETION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; MAMMAL; NEGATIVE FEEDBACK; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; YEAST; CELL CYCLE; CYTOLOGY; DOWN REGULATION; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; SCHIZOSACCHAROMYCES;

MAMMALIA; SACCHAROMYCETALES; SCHIZOSACCHAROMYCETACEAE;

CELL CYCLE; CELL CYCLE PROTEINS; DOWN-REGULATION; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, FUNGAL; HOMEODOMAIN PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 70149096483     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000626     Document Type: Article

References (61)

1. Bähler J (2005) Cell-cycle control of gene expression in budding and fission yeast. Annu Rev Genet 39: 69-94.
2. Breeden LL (2003) Periodic transcription: a cycle within a cycle. Curr Biol 13: R31-R38.
3. Wittenberg C, Reed SI (2005) Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes. Oncogene 24: 2746-2755. (Pubitemid 40638086)
4. Nevins JR (2001) The Rb/E2F pathway and cancer. Hum Mol Genet 10: 699-703.
5. Sherr CJ, McCormick F (2002) The RB and p53 pathways in cancer. Cancer Cell 2: 103-112.
6. Trimarchi JM, Lees JA (2002) Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3: 11-20.
7. Lowndes NF, McInerny CJ, Johnson AL, Fantes PA, Johnston LH (1992) Control of DNA synthesis genes in fission yeast by the cell-cycle gene cdc10+. Nature 355: 449-453.
8. Caligiuri M, Beach D (1993) Sct1 functions in partnership with Cdc10 in a transcription complex that activates cell cycle START and inhibits differentiation. Cell 72: 607-619. (Pubitemid 23077748)
9. Whitehall S, Stacey P, Dawson K, Jones N (1999) Cell cycle-regulated transcription in fission yeast: Cdc10-Res protein interactions during the cell cycle and domains required for regulated transcription. Mol Biol Cell 10: 3705-3715. (Pubitemid 29534020)
10. Zhu Y, Takeda T, Whitehall S, Peat N, Jones N (1997) Functional characterization of the fission yeast Start-specific transcription factor Res2. EMBO J 16: 1023-1034. (Pubitemid 27113181)
11. + transcription in fission yeast. Mol Genet Genomics 269: 765-775.
12. Oliva A, Rosebrock A, Ferrezuelo F, Pyne S, Chen H, et al. (2005) The cell cycle-regulated genes of Schizosaccharomyces pombe. PLoS Biol 3: e225. doi:10.1371/journal.pbio.0030225. (Pubitemid 41032191)
13. Peng X, Karuturi RK, Miller LD, Lin K, Jia Y, et al. (2005) Identification of cell cycle-regulated genes in fission yeast. Mol Biol Cell 16: 1026-1042. (Pubitemid 40349543)
14. Rustici G, Mata J, Kivinen K, Lio P, Penkett CJ, et al. (2004) Periodic gene expression program of the fission yeast cell cycle. Nat Genet 36: 809-817. (Pubitemid 39014097)
15. Baum B, Wuarin J, Nurse P (1997) Control of S-phase periodic transcription in the fission yeast mitotic cycle. EMBO J 16: 4676-4688. (Pubitemid 27326605)
16. Nakashima N, Tanaka K, Sturm S, Okayama H (1995) Fission yeast Rep2 is a putative transcriptional activator subunit for the cell cycle 'start' function of Res2-Cdc10. EMBO J 14: 4794-4802.
17. Tahara S, Tanaka K, Yuasa Y, Okayama H (1998) Functional domains of rep2, a transcriptional activator subunit for Res2-Cdc10, controlling the cell cycle "start". Mol Biol Cell 9: 1577-1588.
18. White S, Khaliq F, Sotiriou S, McInerny CJ (2001) The role of DSC1 components cdc10+, rep1+ and rep2+ in MCB gene transcription at the mitotic G1-S boundary in fission yeast. Curr Genet 40: 251-259. (Pubitemid 34036858)
19. AytéJ, Schweitzer C, Zarzov P, Nurse P, DeCaprio JA (2001) Feedback regulation of the MBF transcription factor by cyclin Cig2. Nat Cell Biol 3: 1043-1050. (Pubitemid 33130454)
20. de Bruin RA, Kalashnikova TI, Aslanian A, Wohlschlegel J, Chahwan C, et al. (2008) DNA replication checkpoint promotes G1-S transcription by inactivating the MBF repressor Nrm1. Proc Natl Acad Sci USA 105: 11230-11235.
21. de Bruin RA, Kalashnikova TI, Chahwan C, McDonald WH, Wohlschlegel J, et al. (2006) Constraining G1-specific transcription to late G1 phase: the MBFassociated corepressor Nrm1 acts via negative feedback. Mol Cell 23: 483-496. (Pubitemid 44205489)
22. Watson A, Mata J, Bahler J, Carr A, Humphrey T (2004) Global gene expression responses of fission yeast to ionizing radiation. Mol Biol Cell 15: 851-860. (Pubitemid 38146498)
23. Chu Z, Li J, Eshaghi M, Peng X, Karuturi RK, et al. (2007) Modulation of cell cycle-specific gene expressions at the onset of S phase arrest contributes to the robust DNA replication checkpoint response in fission yeast. Mol Biol Cell 18: 1756-1767. (Pubitemid 46717557)
24. Dutta C, Patel PK, Rosebrock A, Oliva A, Leatherwood J, et al. (2008) The DNA Replication Checkpoint Directly Regulates MBF-Dependent G1/S Transcription. Mol Cell Biol 28: 5977-5985.
25. Kaufmann E (1993) In vitro binding to the leucine tRNA gene identifies a novel yeast homeobox gene. Chromosoma 102: 174-179.
26. Pramila T, Miles S, GuhaThakurta D, Jemiolo D, Breeden LL (2002) Conserved homeodomain proteins interact with MADS box protein Mcm1 to restrict ECBdependent transcription to the M/G1 phase of the cell cycle. Genes Dev 16: 3034-3045. (Pubitemid 35424191)
27. Horak CE, Luscombe NM, Qian J, Bertone P, Piccirrillo S, et al. (2002) Complex transcriptional circuitry at the G1/S transition in Saccharomyces cerevisiae. Genes Dev 16: 3017-3033. (Pubitemid 35424190)
28. Iyer VR, Horak CE, Scafe CS, Botstein D, Snyder M, et al. (2001) Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409: 533-538. (Pubitemid 32144361)
29. Gordon C, Fantes P (1986) The cdc22 gene of Schizosaccharomyces pombe encodes a cell cycle-regulated transcript. EMBO J 5: 2981-2985.
30. Kelly TJ, Martin GS, Forsburg SL, Stephen RJ, Russo A, et al. (1993) The fission yeast cdc18+ gene product couples S phase to START and mitosis. Cell 74: 371-382. (Pubitemid 23221712)
31. Martín-Cuadrado AB, Dueñas E, Sipiczki M, Vázquez de Aldana CR, Del Rey F (2003) The endo-beta-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe. J Cell Sci 116: 1689-1698.
32. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, et al. (2007) A Network of Multiple Regulatory Layers Shapes Gene Expression in Fission Yeast. Mol Cell 26: 145-155. (Pubitemid 46550937)
33. Davey J (1992) Mating pheromones of the fission yeast Schizosaccharomyces pombe: purification and structural characterization of M-factor and isolation and analysis of two genes encoding the pheromone. EMBO J 11: 951-960.
34. Yabana N, Yamamoto M (1996) Schizosaccharomyces pombe map1+ encodes a MADS-box-family protein required for cell-type-specific gene expression. Mol Cell Biol 16: 3420-3428. (Pubitemid 26199861)
35. Marguerat S, Jensen TS, de Lichtenberg U, Wilhelm BT, Jensen LJ, et al. (2006) The more the merrier: comparative analysis of microarray studies on cell cycleregulated genes in fission yeast. Yeast 23: 261-277.
36. Mata J, Lyne R, Burns G, Bähler J (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32: 143-147. (Pubitemid 34977209)
37. Mata J, Bähler J (2006) Global roles of Ste11p, cell type, and pheromone in the control of gene expression during early sexual differentiation in fission yeast. Proc Natl Acad Sci USA. pp 15517-15522. (Pubitemid 44625624)
38. Miyamoto M, Tanaka K, Okayama H (1994) res2+, a new member of the cdc10+/SWI4 family, controls the 'start' of mitotic and meiotic cycles in fission yeast. EMBO J 13: 1873-1880.
39. Nadeem F, Blair D, McInerny C (2006) Pol5p, a novel binding partner to Cdc10p in fission yeast involved in rRNA production. Mol Genet Genomics 276: 391-401. (Pubitemid 44328127)
40. Heichinger C, Penkett CJ, Bähler J, Nurse P (2006) Genome-wide characterization of fission yeast DNA replication origins. EMBO J 25: 5171-5179. (Pubitemid 44658534)
41. McInerny CJ, Partridge JF, Mikesell GE, Creemer DP, Breeden LL (1997) A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription. Genes Dev 11: 1277-1288.
42. MacKay VL, Mai B, Waters L, Breeden LL (2001) Early cell cycle box-mediated transcription of CLN3 and SWI4 contributes to the proper timing of the G(1)-to- S transition in budding yeast. Mol Cell Biol 21: 4140-4148. (Pubitemid 32565296)
43. Mai B, Miles S, Breeden LL (2002) Characterization of the ECB binding complex responsible for the M/G1-specific Transcription of CLN3 and SWI4. Mol Cell Biol 22: 430-441. (Pubitemid 34027489)
44. Simon I, Barnett J, Hannett N, Harbison CT, Rinaldi NJ, et al. (2001) Serial regulation of transcriptional regulators in the yeast cell cycle. Cell 106: 697-708. (Pubitemid 32900661)
45. Bueno A, Russell P (1993) Two fission yeast B-type cyclins, cig2 and Cdc13, have different functions in mitosis. Mol Cell Biol 13: 2286-2297. (Pubitemid 23097707)
46. Kennedy PJ, Vashisht AA, Hoe K-L, Kim D-U, Park H-O, et al. (2008) A genome-wide screen of genes involved in cadmium tolerance in Schizosaccharomyces pombe. Toxicol Sci 106: 124-139.
47. Foster R, Mikesell GE, Breeden L (1993) Multiple SWI6-dependent cis-acting elements control SWI4 transcription through the cell cycle. Mol Cell Biol 13: 3792-3801. (Pubitemid 23157316)
48. McInerny CJ, Kersey PJ, Creanor J, Fantes PA (1995) Positive and negative roles for cdc10 in cell cycle gene expression. Nucleic Acids Res 23: 4761-4768.
49. Takayama Y, Takahashi K (2007) Differential regulation of repeated histone genes during the fission yeast cell cycle. Nucleic Acids Res 35: 3223-3237. (Pubitemid 47073589)
50. Blackwell C, Martin KA, Greenall A, Pidoux A, Allshire RC, et al. (2004) The Schizosaccharomyces pombe HIRA-like protein Hip1 is required for the periodic expression of histone genes and contributes to the function of complex centromeres. Mol Cell Biol 24: 4309-4320. (Pubitemid 41071001)
51. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, et al. (2008) Distinct Modes of Regulation by Chromatin Encoded through Nucleosome Positioning Signals. PLoS Comput Biol 4: e1000216. doi:10.1371/journal. pcbi.1000216.
52. Bosco G, Du W, Orr-Weaver TL (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat Cell Biol 3: 289-295. (Pubitemid 32201324)
53. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie A 3rd, et al. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943-951.
54. Robyr D, Grunstein M (2003) Genomewide histone acetylation microarrays. Methods 31: 83-89.
55. Flick KM, Spielewoy N, Kalashnikova TI, Guaderrama M, Zhu Q, et al. (2003) Grr1-dependent inactivation of Mth1 mediates glucose-induced dissociation of Rgt1 from HXT gene promoters. Mol Biol Cell 14: 3230-3241. (Pubitemid 37013123)
56. Bernstein BE, Humphrey EL, Liu CL, Schreiber SL (2004) The use of chromatin immunoprecipitation assays in genome-wide analyses of histone modifications. Methods Enzymol 376: 349-360. (Pubitemid 38200190)
57. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl 1): S96-104. (Pubitemid 41185642)
58. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121. (Pubitemid 32397092)
59. Boddy MN, Gaillard P-HL, McDonald WH, Shanahan P, Yates JR 3rd, et al. (2001) Mus81-Eme1 Are Essential Components of a Holliday Junction Resolvase. Cell 107: 537-548.
60. Lyne R, Burns G, Mata J, Penkett CJ, Rustici G, et al. (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4: 27. (Pubitemid 39546626)
61. Lim WK, Wang K, Lefebvre C, Califano A (2007) Comparative analysis of microarray normalization procedures: effects on reverse engineering gene networks. Bioinformatics 23: i282-288. (Pubitemid 47244411)