Molecular and General Genetics MGG

, Volume 248, Issue 4, pp 491–498

A fission yeast gene mapping close tosuc1 encodes a protein containing two bromodomains

  • Stephen J. Aves
  • John Hindley
  • Geraldine A. Phear
  • Nicholas Tongue
Original Paper

Abstract

A novel gene,brd1, has been cloned from the fission yeastSchizosaccharomyces pombe. The predictedbrd1 product contains two copies of an imperfect repeat of 96 amino acid residues in its N-terminal half. These each include a region with high homology to the bromodomains found in transcriptional activator proteins from a diversity of eukaryotes. An in vivo deletion of the completebrd1 open reading frame is not lethal but cells exhibit thermosensitivity, with reductions in both cell growth and stationary phase survival at 36°C.brd1 maps adjacent to the genesuc1, but is expressed separately to give a low abundance 2.1 kb mRNA.

Key words

Schizosaccharomyces pombe Bromodomain Transcriptional activation Coactivator Stationary phase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson S (1981) Shotgun DNA sequencing using cloned DNase I-generated fragments. Nucleic Acids Res 9: 3015–3027Google Scholar
  2. Beach D, Nurse P (1981) High frequency transformation of the fission yeastSchizosaccharomyces pombe. Nature 290:140–142Google Scholar
  3. Conaway RC, Conaway JQ (1993) General initiation factors for RNA polymerase II. Annu Rev Biochem 62:161–190Google Scholar
  4. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395Google Scholar
  5. Gansheroff LJ, Dollard C, Tan P, Winston F (1995) TheSaccharomyces cerevisiae SPT7 gene encodes a very acidic protein important for transcription in vivo. Genetics 139:523–536Google Scholar
  6. Georgakopoulos T, Thireos G (1992) Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription. EMBO J 11:4145–4152Google Scholar
  7. Grimm C, Kohli J, Murray J, Maundrell K (1988) Genetic engineering ofSchizosaccharomyces pombe: a system for gene disruption and replacement using theura4 gene as a selectable marker. Mol Gen Genet 215:81–86Google Scholar
  8. Hayles J, Beach D, Durkacz B, Nurse P (1986a) The fission yeast cell cycle control genecdc2: isolation of a sequencesuc1 that suppressescdc2 mutant function. Mol Gen Genet 202:291–293Google Scholar
  9. Hayles J, Aves S, Nurse P (1986b)suc1 is an essential gene involved in both the cell cycle and growth in fission yeast. EMBO J 5:3373–3379Google Scholar
  10. Haynes SR, Mozer BA, Bhatia-Dey N, Dawid IB (1989) TheDrosophila fsh locus, a maternal effect homeotic gene, encodes apparent membrane proteins. Dev Biol 134:246–257Google Scholar
  11. Haynes SR, Dollard C, Winston F, Beck S, Trowsdale J, Dawid IB (1992) The bromodomain: a conserved sequence found in human,Drosophila and yeast proteins. Nucleic Acids Res 20:2603Google Scholar
  12. Hindley J, Phear G, Stein M, Beach D (1987)suc encodes a predicted 13-kilodalton protein that is essential for cell viability and is directly involved in the division cycle ofSchizosaccharomyces pombe. Mol Cell Biol 7:504–511Google Scholar
  13. Hong GF (1982) A systematic DNA sequencing strategy. J Mol Biol 158:539–549Google Scholar
  14. Hultman T, Ståhl S, Hornes E, Uhlén M (1989) Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res 17:4937–4946Google Scholar
  15. Hultman T, Bergh S, Moks T, Uhlén M (1991) Bidirectional solid phase sequencing of in vitro amplified plasmid DNA. BioTechniques 10:84–93Google Scholar
  16. Johnson PF, McKnight SI (1989) Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem 58:799–839Google Scholar
  17. Khavari PA, Peterson CL, Tamkun JW, Mendel DB, Crabtree GR (1993) BRG1 contains a conserved domain of theSWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366:170–174Google Scholar
  18. Kokubo T, Gong D-W, Yamashita S, Horikoshi M, Roeder RG, Nakatani Y (1993)Drosophila 230-kD TFIID subunit, a functional homolog of the human cell cycle gene product, negatively regulates DNA binding of the TATA box-binding subunit of TFIID. Genes Dev 7:1033–1046Google Scholar
  19. Laurent BC, Treitel MA, Carlson M (1991) Functional interdependence of the yeast SNF2, SNF5 and SNF6 proteins in transcriptional activation. Proc Natl Acad Sci USA 88:2687–2691Google Scholar
  20. Laurent BC, Yang X, Carlson M (1992) An essentialSaccharomyces cerevisiae gene homologous toSNF2 encodes a helicase-related protein in a new family. Mol Cell Biol 12:1893–1902Google Scholar
  21. Laurent BC, Treich I, Carlson M (1993) The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for trancriptional activation. Genes Dev 7: 583–591Google Scholar
  22. Leupold U (1950) Die Vererbung von Homothallie und Heterothallie beiSchizosaccharomyces pombe. C R Lab Carlsberg Sér Physiol 24: 381–480Google Scholar
  23. Lewin B (1990) Commitment and activation at pol II promoters: a tail of protein-protein interactions. Cell 61: 1161–1164Google Scholar
  24. Lygerou Z, Conesa C, Lesage P, Swanson RN, Ruet A, Carlson M, Sentenac A, Séraphin B (1994) The yeastBDF1 gene encodes a transcription factor involved in the expression of a broad class of genes including snRNAs. Nucleic Acids Res 22:5332–5340Google Scholar
  25. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  26. Marcus GA, Silverman N, Berger SL, Horiuchi J, Guarente L (1994) Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. EMBO J 13: 4807–4815Google Scholar
  27. Mitchell PJ, Tjian R (1989) transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245:371–378Google Scholar
  28. Moreno S, Klar A, Nurse P (1990) An introduction to molecular genetic analysis of the fission yeastSchizosaccharomyces pombe. Methods Enzymol 194:793–823Google Scholar
  29. Muchardt C, Yaniv M (1993) A human homologue ofSaccharomyces cerevisiae SNF2/SWI2 andDrosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J 12:4279–4290Google Scholar
  30. Neigeborn L, Carlson M (1984) Genes affecting the regulation ofSUC2 gene expression by glucose repression inSaccharomyces cerevisiae. Genetics 108:845–858Google Scholar
  31. Peterson CL, Herskowitz I (1992) Characterisation of the yeastSWI1, SWI2 andSWI3 genes, which encode a global activator of transcription. Cell 68: 573–583Google Scholar
  32. Prabhala G, Rosenberg GH, Käufer NF (1992) Architectural features of pre-mRNA introns in the fission yeastSchizosaccharomyces pombe. Yeast 8: 171–182Google Scholar
  33. Pugh BF, Tjian R (1992) Diverse transcriptional functions of the multisubunit eukaryotic TFIID complex. J Biol Chem 267: 679–682Google Scholar
  34. Rothstein RJ (1983) One-step gene disruption in yeast. Methods Enzymol 101: 202–211Google Scholar
  35. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467Google Scholar
  36. Sanger F, Coulson AR, Barrell BG, Smith AJH, Roe BA (1980) Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol 143:161–178Google Scholar
  37. Sawadogo M, Sentenac A (1990) RNA polymerase B (II) and general transcription factors. Annu Rev Biochem 59: 711–754Google Scholar
  38. Sekiguchi T, Nohiro Y, Nakamura Y, Hisamoto N, Nishimoto T (1991) The humanCCG1 gene, essential for progression of the G1 phase, encodes a 210-kilodalton nuclear DNA-binding protein. Mol Cell Biol 11:3317–3325Google Scholar
  39. Staden R, McLachlan AD (1982) Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res 10:141–156Google Scholar
  40. Stern M, Jensen R, Herskowitz I (1984) FiveSW1 genes are required for expression of theHO gene in yeast. J Mol Biol 178:853–868Google Scholar
  41. Tamkun JW, Deuring R, Scott MP, Kissinger M, Pattatucci AM, Kaufman TC, Kennison JA (1992) brahma:a regulator ofDrosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68:561–572Google Scholar
  42. Tsuchiya E, Uno M, Kiguchi A, Masuoka K, Kanemori Y, Okabe S, Mikayawa T (1992) TheSaccharomyces cerevisiae NPS1 gene, a novelCDC gene which encodes a 160 kDa nuclear protein involved in G2 phase control. EMBO J 11: 4017–4026Google Scholar
  43. Weinzierl ROJ, Dynlacht BD, Tjian R (1993) Largest subunit ofDrosophila transcription factor IID directs assembly of a complex containing TBP and a coactivator. Nature 362:511–517Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Stephen J. Aves
    • 1
  • John Hindley
    • 2
  • Geraldine A. Phear
    • 2
  • Nicholas Tongue
    • 1
  1. 1.Department of Biological SciencesUniversity of Exeter, Washington Singer LaboratoriesExeterUK
  2. 2.Department of BiochemistryUniversity of BristolBristolUK
  3. 3.Department of RadiologyEccles Institute of Human Genetics, University of UtahSalt Lake CityUSA

Personalised recommendations