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PMID: 15616197 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Identification of cell cycle-regulated genes in fission yeast.

Molecular biology of the cell ·Vol. 16 ·No. 3 ·2005-03-00 ·Pages 1026-42

Peng X, Karuturi RK, Miller LD, Lin K, Jia Y, Kondu P, Wang L, Wong LS, Liu ET, Balasubramanian MK, Liu J

Abstract

Cell cycle progression is both regulated and accompanied by periodic changes in the expression levels of a large number of genes. To investigate cell cycle-regulated transcriptional programs in the fission yeast Schizosaccharomyces pombe, we developed a whole-genome oligonucleotide-based DNA microarray. Microarray analysis of both wild-type and cdc25 mutant cell cultures was performed to identify transcripts whose levels oscillated during the cell cycle. Using an unsupervised algorithm, we identified 747 genes that met the criteria for cell cycle-regulated expression. Peaks of gene expression were found to be distributed throughout the entire cell cycle. Furthermore, we found that four promoter motifs exhibited strong association with cell cycle phase-specific expression. Examination of the regulation of MCB motif-containing genes through the perturbation of DNA synthesis control/MCB-binding factor (DSC/MBF)-mediated transcription in arrested synchronous cdc10 mutant cell cultures revealed a subset of functional targets of the DSC/MBF transcription factor complex, as well as certain gene promoter requirements. Finally, we compared our data with those for the budding yeast Saccharomyces cerevisiae and found approximately 140 genes that are cell cycle regulated in both yeasts, suggesting that these genes may play an evolutionarily conserved role in regulation of cell cycle-specific processes. Our complete data sets are available at http://giscompute.gis.a-star.edu.sg/~gisljh/CDC.

MeSH Terms
Algorithms Amino Acid Motifs Cell Cycle Cell Cycle Proteins/genetics Cell Nucleus/metabolism Cell Separation Cluster Analysis Computational Biology/methods DNA/metabolism DNA, Complementary/metabolism Flow Cytometry Fungal Proteins/genetics G1 Phase G2 Phase Gene Expression Regulation, Fungal Genome, Fungal Genotype Internet Models, Statistical Normal Distribution Oligonucleotide Array Sequence Analysis Promoter Regions, Genetic RNA, Messenger/metabolism S Phase Saccharomyces cerevisiae/genetics Schizosaccharomyces/genetics,metabolism Species Specificity Temperature Transcription, Genetic ras-GRF1/genetics
Chemicals
Cell Cycle Proteins DNA, Complementary Fungal Proteins RNA, Messenger ras-GRF1 DNA
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Peng Xu
Genome Institute of Singapore, Singapore 138672, Singapore.
Karuturi R Krishna Murthy
Miller Lance D
Lin Kui
Jia Yonghui
Kondu Pinar
Wang Long
Wong Lim-Soon
Liu Edison T
Balasubramanian Mohan K
Liu Jianhua
References (75)
75 references, click to expand
  1. Serial regulation of transcriptional regulators in the yeast cell cycle.
    Cell. 2001 Sep 21;106(6):697-708 PMID: 11572776
  2. Positive and negative roles for cdc10 in cell cycle gene expression.
    Nucleic Acids Res. 1995 Dec 11;23(23):4761-8 PMID: 8532516
  3. Cell cycle, DNA damage and heat shock regulate suc22+ expression in fission yeast.
    Mol Gen Genet. 1996 Sep 13;252(3):284-91 PMID: 8842148
  4. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
    Mol Biol Cell. 1998 Dec;9(12):3273-97 PMID: 9843569
  5. Genetic and physiological analysis of DNA replication in fission yeast.
    Methods Enzymol. 1997;283:440-59 PMID: 9251040
  6. A role for the START gene-specific transcription factor complex in the inactivation of cyclin B and Cut2 destruction.
    Mol Biol Cell. 2000 Oct;11(10):3411-24 PMID: 11029045
  7. Coordination of growth and division during the cell cycle of fission yeast.
    Cold Spring Harb Symp Quant Biol. 1991;56:557-65 PMID: 1668089
  8. The S. pombe sep1 gene encodes a nuclear protein that is required for periodic expression of the cdc15 gene.
    FEBS Lett. 2000 Sep 15;481(2):105-8 PMID: 10996305
  9. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  10. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis.
    Cell. 1995 Aug 11;82(3):435-44 PMID: 7634333
  11. Molecular evidence for the early colonization of land by fungi and plants.
    Science. 2001 Aug 10;293(5532):1129-33 PMID: 11498589
  12. Fission yeast Fizzy-related protein srw1p is a G(1)-specific promoter of mitotic cyclin B degradation.
    EMBO J. 2000 Aug 1;19(15):3968-77 PMID: 10921878
  13. A new role for MCM1 in yeast: cell cycle regulation of SW15 transcription.
    Genes Dev. 1991 Dec;5(12B):2405-19 PMID: 1752436
  14. The wee1 protein kinase is required for radiation-induced mitotic delay.
    Nature. 1992 Mar 26;356(6367):353-5 PMID: 1549179
  15. A fission yeast gene, him1(+)/dfp1(+), encoding a regulatory subunit for Hsk1 kinase, plays essential roles in S-phase initiation as well as in S-phase checkpoint control and recovery from DNA damage.
    Mol Cell Biol. 1999 Aug;19(8):5535-47 PMID: 10409743
  16. A zinc finger protein controls the onset of premeiotic DNA synthesis of fission yeast in a Mei2-independent cascade.
    EMBO J. 1994 Apr 15;13(8):1881-7 PMID: 8168486
  17. Regulation of the G1 phase of the cell cycle by periodic stabilization and degradation of the p25rum1 CDK inhibitor.
    EMBO J. 1998 Jan 15;17(2):482-97 PMID: 9430640
  18. A B-type cyclin negatively regulates conjugation via interacting with cell cycle 'start' genes in fission yeast.
    EMBO J. 1994 Apr 15;13(8):1863-72 PMID: 7909513
  19. Cmk2, a novel serine/threonine kinase in fission yeast.
    FEBS Lett. 2002 Jul 31;524(1-3):79-86 PMID: 12135745
  20. Orp1, a member of the Cdc18/Cdc6 family of S-phase regulators, is homologous to a component of the origin recognition complex.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12475-9 PMID: 8618924
  21. Periodic gene expression program of the fission yeast cell cycle.
    Nat Genet. 2004 Aug;36(8):809-17 PMID: 15195092
  22. The role of DSC1 components cdc10+, rep1+ and rep2+ in MCB gene transcription at the mitotic G1-S boundary in fission yeast.
    Curr Genet. 2001 Dec;40(4):251-9 PMID: 11795845
  23. Fission yeast cdc25 is a cell-cycle regulated protein.
    Biochem Biophys Res Commun. 1990 Feb 28;167(1):301-9 PMID: 2178610
  24. S. pombe gene sds22+ essential for a midmitotic transition encodes a leucine-rich repeat protein that positively modulates protein phosphatase-1.
    Cell. 1991 Jan 11;64(1):149-57 PMID: 1846086
  25. A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast.
    Mol Cell. 2003 Jan;11(1):175-87 PMID: 12535531
  26. Cell cycle regulation of Dfp1, an activator of the Hsk1 protein kinase.
    Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8443-8 PMID: 10411894
  27. cdt1 is an essential target of the Cdc10/Sct1 transcription factor: requirement for DNA replication and inhibition of mitosis.
    EMBO J. 1994 Jan 15;13(2):425-34 PMID: 8313888
  28. The fission yeast cdc18+ gene product couples S phase to START and mitosis.
    Cell. 1993 Jul 30;74(2):371-82 PMID: 7916658
  29. The Number of Chromosomes in SCHIZOSACCHAROMYCES POMBE: Light Microscopy of Stained Preparations.
    Genetics. 1977 Nov;87(3):491-7 PMID: 17248776
  30. The rad21 gene product of Schizosaccharomyces pombe is a nuclear, cell cycle-regulated phosphoprotein.
    J Biol Chem. 1995 Mar 31;270(13):7703-11 PMID: 7706319
  31. Deletion of the sep1(+) forkhead transcription factor homologue is not lethal but causes hyphal growth in Schizosaccharomyces pombe.
    Biochem Biophys Res Commun. 1999 Sep 24;263(2):465-74 PMID: 10491317
  32. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1.
    Nat Cell Biol. 2001 Nov;3(11):966-72 PMID: 11715017
  33. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe.
    Yeast. 1998 Jul;14(10):943-51 PMID: 9717240
  34. Histone gene organization of fission yeast: a common upstream sequence.
    EMBO J. 1985 Dec 16;4(13A):3531-8 PMID: 4092687
  35. Regulation of calcineurin gene expression in Schizosaccharomyces pombe. Dependence on the ste11 transcription factor.
    J Biol Chem. 1995 Oct 20;270(42):24794-9 PMID: 7559598
  36. Mik1 levels accumulate in S phase and may mediate an intrinsic link between S phase and mitosis.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2579-84 PMID: 10716991
  37. Feedback regulation of the MBF transcription factor by cyclin Cig2.
    Nat Cell Biol. 2001 Dec;3(12):1043-50 PMID: 11781565
  38. Plo1(+) regulates gene transcription at the M-G(1) interval during the fission yeast mitotic cell cycle.
    EMBO J. 2002 Nov 1;21(21):5745-55 PMID: 12411492
  39. Analysis of a histone H2A variant from fission yeast: evidence for a role in chromosome stability.
    Mol Gen Genet. 1994 Dec 1;245(5):628-35 PMID: 7808414
  40. Microarrays and cell cycle transcription in yeast.
    Curr Opin Cell Biol. 2000 Dec;12(6):710-5 PMID: 11063936
  41. Mutations that define the optimal half-site for binding yeast GCN4 activator protein and identify an ATF/CREB-like repressor that recognizes similar DNA sites.
    Mol Cell Biol. 1990 Oct;10(10):5077-86 PMID: 2204805
  42. Cloning of a calmodulin kinase I homologue from Schizosaccharomyces pombe.
    J Biol Chem. 2000 Jan 7;275(1):685-90 PMID: 10617667
  43. MCB-mediated regulation of cell cycle-specific cdc22+ transcription in fission yeast.
    Mol Genet Genomics. 2003 Sep;269(6):765-75 PMID: 12898217
  44. sep1+ encodes a transcription-factor homologue of the HNF-3/forkhead DNA-binding-domain family in Schizosaccharomyces pombe.
    Gene. 1997 Nov 20;202(1-2):1-5 PMID: 9427538
  45. Organization, primary structure, and evolution of histone H2A and H2B genes of the fission yeast Schizosaccharomyces pombe.
    Mol Cell Biol. 1985 Nov;5(11):3261-9 PMID: 3018512
  46. Cell cycle-regulated transcription in fission yeast: Cdc10-Res protein interactions during the cell cycle and domains required for regulated transcription.
    Mol Biol Cell. 1999 Nov;10(11):3705-15 PMID: 10564266
  47. Locating regions of differential variability in DNA and protein sequences.
    Genetics. 1999 Sep;153(1):485-95 PMID: 10471728
  48. Geometry of gene expression dynamics.
    Bioinformatics. 2002 Sep;18(9):1176-83 PMID: 12217909
  49. The endo-beta-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe.
    J Cell Sci. 2003 May 1;116(Pt 9):1689-98 PMID: 12665550
  50. The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe.
    J Cell Sci. 1988 Mar;89 ( Pt 3):343-57 PMID: 3198697
  51. Transcriptional regulation and function during the human cell cycle.
    Nat Genet. 2001 Jan;27(1):48-54 PMID: 11137997
  52. Assessment of the sensitivity and specificity of oligonucleotide (50mer) microarrays.
    Nucleic Acids Res. 2000 Nov 15;28(22):4552-7 PMID: 11071945
  53. Improved fourier transform method for unsupervised cell-cycle regulated gene prediction.
    Proc IEEE Comput Syst Bioinform Conf. 2004;:194-203 PMID: 16448013
  54. Universal control mechanism regulating onset of M-phase.
    Nature. 1990 Apr 5;344(6266):503-8 PMID: 2138713
  55. Mutations in the cdc10 start gene of Schizosaccharomyces pombe implicate the region of homology between cdc10 and SWI6 as important for p85cdc10 function.
    Mol Gen Genet. 1992 Sep;234(3):449-56 PMID: 1406591
  56. In situ-synthesized novel microarray optimized for mouse stem cell and early developmental expression profiling.
    Genome Res. 2003 May;13(5):1011-21 PMID: 12727912
  57. Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast.
    Science. 2000 Jun 23;288(5474):2215-9 PMID: 10864871
  58. The genome sequence of Schizosaccharomyces pombe.
    Nature. 2002 Feb 21;415(6874):871-80 PMID: 11859360
  59. mik1(+) G1-S transcription regulates mitotic entry in fission yeast.
    FEBS Lett. 2001 Aug 17;503(2-3):131-4 PMID: 11513869
  60. High dosage expression of a zinc finger protein, Grt1, suppresses a mutant of fission yeast slp1(+), a homolog of CDC20/p55CDC/Fizzy.
    J Cell Sci. 2000 Nov;113 ( Pt 22):3989-99 PMID: 11058086
  61. The effect of cell mass on the cell cycle timing and duration of S-phase in fission yeast.
    J Cell Sci. 1979 Oct;39:215-33 PMID: 528581
  62. Fission yeast Rep2 is a putative transcriptional activator subunit for the cell cycle 'start' function of Res2-Cdc10.
    EMBO J. 1995 Oct 2;14(19):4794-802 PMID: 7588609
  63. Identification of genes periodically expressed in the human cell cycle and their expression in tumors.
    Mol Biol Cell. 2002 Jun;13(6):1977-2000 PMID: 12058064
  64. The fission yeast pfh1(+) gene encodes an essential 5' to 3' DNA helicase required for the completion of S-phase.
    Nucleic Acids Res. 2002 Nov 1;30(21):4728-39 PMID: 12409464
  65. pct1+, which encodes a new DNA-binding partner of p85cdc10, is required for meiosis in the fission yeast Schizosaccharomyces pombe.
    Genes Dev. 1994 Apr 15;8(8):885-98 PMID: 7926774
  66. spo12 is a multicopy suppressor of mcs3 that is periodically expressed in fission yeast mitosis.
    Mol Gen Genet. 2000 Oct;264(3):306-16 PMID: 11085271
  67. Identification and expression of uvi31+, a UV-inducible gene from Schizosaccharomyces pombe.
    Environ Mol Mutagen. 1997;30(1):72-81 PMID: 9258332
  68. Control of DNA synthesis genes in fission yeast by the cell-cycle gene cdc10+.
    Nature. 1992 Jan 30;355(6359):449-53 PMID: 1734281
  69. The fission yeast cdc19+ gene encodes a member of the MCM family of replication proteins.
    J Cell Sci. 1994 Oct;107 ( Pt 10):2779-88 PMID: 7876346
  70. The fission yeast NIMA kinase Fin1p is required for spindle function and nuclear envelope integrity.
    EMBO J. 2002 Apr 2;21(7):1713-22 PMID: 11927555
  71. res2+, a new member of the cdc10+/SWI4 family, controls the 'start' of mitotic and meiotic cycles in fission yeast.
    EMBO J. 1994 Apr 15;13(8):1873-80 PMID: 8168485
  72. A genome-wide transcriptional analysis of the mitotic cell cycle.
    Mol Cell. 1998 Jul;2(1):65-73 PMID: 9702192
  73. cdc25+ functions as an inducer in the mitotic control of fission yeast.
    Cell. 1986 Apr 11;45(1):145-53 PMID: 3955656
  74. The G1/S cyclin Cig2p during meiosis in fission yeast.
    Mol Biol Cell. 2002 Jun;13(6):2080-90 PMID: 12058071
  75. Sct1 functions in partnership with Cdc10 in a transcription complex that activates cell cycle START and inhibits differentiation.
    Cell. 1993 Feb 26;72(4):607-19 PMID: 7916653
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.e04-04-0299
Published
2005-03-00
Epub
2004-00-22
Pages
1026-42
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC551471
Subset
IM
External Links
PubMed source DOI: 10.1091/mbc.e04-04-0299 PMC Full Text View journal details
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