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. 1999 Jan;151(1):45–55. doi: 10.1093/genetics/151.1.45

The MSN1 and NHP6A genes suppress SWI6 defects in Saccharomyces cerevisiae.

J Sidorova 1, L Breeden 1
PMCID: PMC1460468  PMID: 9872947

Abstract

Ankyrin (ANK) repeats were first found in the Swi6 transcription factor of Saccharomyces cerevisiae and since then were identified in many proteins of eukaryotes and prokaryotes. These repeats are thought to serve as protein association domains. In Swi6, ANK repeats affect DNA binding of both the Swi4/Swi6 and Mbp1/Swi6 complexes. We have previously described generation of random mutations within the ANK repeats of Swi6 that render the protein temperature sensitive in its ability to activate HO transcription. Two of these SWI6 mutants were used in a screen for high copy suppressors of this phenotype. We found that MSN1, which encodes a transcriptional activator, and NHP6A, which encodes an HMG-like protein, are able to suppress defective Swi6 function. Both of these gene products are involved in HO transcription, and Nhp6A may also be involved in CLN1 transcription. Moreover, because overexpression of NHP6A can suppress caffeine sensitivity of one of the SWI6 ANK mutants, swi6-405, other SWI6-dependent genes may also be affected by Nhp6A. We hypothesize that Nhp6A and Msn1 modulate Swi6-dependent gene transcription indirectly, through effects on chromatin structure or other transcription factors, because we have not been able to demonstrate that either Msn1 or Nhp6A interact with the Swi4/Swi6 complex.

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Selected References

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  1. Andrews B. J., Herskowitz I. The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature. 1989 Dec 14;342(6251):830–833. doi: 10.1038/342830a0. [DOI] [PubMed] [Google Scholar]
  2. Andrews B. J., Moore L. A. Interaction of the yeast Swi4 and Swi6 cell cycle regulatory proteins in vitro. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11852–11856. doi: 10.1073/pnas.89.24.11852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Andrews B. J., Moore L. Mutational analysis of a DNA sequence involved in linking gene expression to the cell cycle. Biochem Cell Biol. 1992 Oct-Nov;70(10-11):1073–1080. doi: 10.1139/o92-152. [DOI] [PubMed] [Google Scholar]
  4. Bork P. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins. 1993 Dec;17(4):363–374. doi: 10.1002/prot.340170405. [DOI] [PubMed] [Google Scholar]
  5. Breeden L., Mikesell G. E. Cell cycle-specific expression of the SWI4 transcription factor is required for the cell cycle regulation of HO transcription. Genes Dev. 1991 Jul;5(7):1183–1190. doi: 10.1101/gad.5.7.1183. [DOI] [PubMed] [Google Scholar]
  6. Breeden L., Nasmyth K. Regulation of the yeast HO gene. Cold Spring Harb Symp Quant Biol. 1985;50:643–650. doi: 10.1101/sqb.1985.050.01.078. [DOI] [PubMed] [Google Scholar]
  7. Breeden L. Start-specific transcription in yeast. Curr Top Microbiol Immunol. 1996;208:95–127. doi: 10.1007/978-3-642-79910-5_5. [DOI] [PubMed] [Google Scholar]
  8. Butler A. P., Mardian J. K., Olins D. E. Nonhistone chromosomal protein HMG 1 interactions with DNA. Fluorescence and thermal denaturation studies. J Biol Chem. 1985 Sep 5;260(19):10613–10620. [PubMed] [Google Scholar]
  9. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  10. Costigan C., Kolodrubetz D., Snyder M. NHP6A and NHP6B, which encode HMG1-like proteins, are candidates for downstream components of the yeast SLT2 mitogen-activated protein kinase pathway. Mol Cell Biol. 1994 Apr;14(4):2391–2403. doi: 10.1128/mcb.14.4.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dirick L., Moll T., Auer H., Nasmyth K. A central role for SWI6 in modulating cell cycle Start-specific transcription in yeast. Nature. 1992 Jun 11;357(6378):508–513. doi: 10.1038/357508a0. [DOI] [PubMed] [Google Scholar]
  12. Eide D., Guarente L. Increased dosage of a transcriptional activator gene enhances iron-limited growth of Saccharomyces cerevisiae. J Gen Microbiol. 1992 Feb;138(2):347–354. doi: 10.1099/00221287-138-2-347. [DOI] [PubMed] [Google Scholar]
  13. Espinet C., de la Torre M. A., Aldea M., Herrero E. An efficient method to isolate yeast genes causing overexpression-mediated growth arrest. Yeast. 1995 Jan;11(1):25–32. doi: 10.1002/yea.320110104. [DOI] [PubMed] [Google Scholar]
  14. Estruch F., Carlson M. Increased dosage of the MSN1 gene restores invertase expression in yeast mutants defective in the SNF1 protein kinase. Nucleic Acids Res. 1990 Dec 11;18(23):6959–6964. doi: 10.1093/nar/18.23.6959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ewaskow S. P., Sidorova J. M., Hendle J., Emery J. C., Lycan D. E., Zhang K. Y., Breeden L. L. Mutation and modeling analysis of the Saccharomyces cerevisiae Swi6 ankyrin repeats. Biochemistry. 1998 Mar 31;37(13):4437–4450. doi: 10.1021/bi972652e. [DOI] [PubMed] [Google Scholar]
  16. Ge H., Roeder R. G. The high mobility group protein HMG1 can reversibly inhibit class II gene transcription by interaction with the TATA-binding protein. J Biol Chem. 1994 Jun 24;269(25):17136–17140. [PubMed] [Google Scholar]
  17. Gimeno C. J., Fink G. R. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol. 1994 Mar;14(3):2100–2112. doi: 10.1128/mcb.14.3.2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heichman K. A., Roberts J. M. The yeast CDC16 and CDC27 genes restrict DNA replication to once per cell cycle. Cell. 1996 Apr 5;85(1):39–48. doi: 10.1016/s0092-8674(00)81080-6. [DOI] [PubMed] [Google Scholar]
  19. Henkel T., Zabel U., van Zee K., Müller J. M., Fanning E., Baeuerle P. A. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-kappa B subunit. Cell. 1992 Mar 20;68(6):1121–1133. doi: 10.1016/0092-8674(92)90083-o. [DOI] [PubMed] [Google Scholar]
  20. Igual J. C., Johnson A. L., Johnston L. H. Coordinated regulation of gene expression by the cell cycle transcription factor Swi4 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO J. 1996 Sep 16;15(18):5001–5013. [PMC free article] [PubMed] [Google Scholar]
  21. 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 Sep 17;261(5128):1551–1557. doi: 10.1126/science.8372350. [DOI] [PubMed] [Google Scholar]
  22. Kolodrubetz D., Burgum A. Duplicated NHP6 genes of Saccharomyces cerevisiae encode proteins homologous to bovine high mobility group protein 1. J Biol Chem. 1990 Feb 25;265(6):3234–3239. [PubMed] [Google Scholar]
  23. Lambrechts M. G., Bauer F. F., Marmur J., Pretorius I. S. Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8419–8424. doi: 10.1073/pnas.93.16.8419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Madden K., Sheu Y. J., Baetz K., Andrews B., Snyder M. SBF cell cycle regulator as a target of the yeast PKC-MAP kinase pathway. Science. 1997 Mar 21;275(5307):1781–1784. doi: 10.1126/science.275.5307.1781. [DOI] [PubMed] [Google Scholar]
  25. McIntosh E. M., Atkinson T., Storms R. K., Smith M. Characterization of a short, cis-acting DNA sequence which conveys cell cycle stage-dependent transcription in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jan;11(1):329–337. doi: 10.1128/mcb.11.1.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McIntosh E. M., Ord R. W., Storms R. K. Transcriptional regulation of the cell cycle-dependent thymidylate synthase gene of Saccharomyces cerevisiae. Mol Cell Biol. 1988 Nov;8(11):4616–4624. doi: 10.1128/mcb.8.11.4616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Measday V., Moore L., Ogas J., Tyers M., Andrews B. The PCL2 (ORFD)-PHO85 cyclin-dependent kinase complex: a cell cycle regulator in yeast. Science. 1994 Nov 25;266(5189):1391–1395. doi: 10.1126/science.7973731. [DOI] [PubMed] [Google Scholar]
  28. Nasmyth K., Dirick L. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell. 1991 Sep 6;66(5):995–1013. doi: 10.1016/0092-8674(91)90444-4. [DOI] [PubMed] [Google Scholar]
  29. Ogas J., Andrews B. J., Herskowitz I. Transcriptional activation of CLN1, CLN2, and a putative new G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell. 1991 Sep 6;66(5):1015–1026. doi: 10.1016/0092-8674(91)90445-5. [DOI] [PubMed] [Google Scholar]
  30. Partridge J. F., Mikesell G. E., Breeden L. L. Cell cycle-dependent transcription of CLN1 involves swi4 binding to MCB-like elements. J Biol Chem. 1997 Apr 4;272(14):9071–9077. doi: 10.1074/jbc.272.14.9071. [DOI] [PubMed] [Google Scholar]
  31. Paull T. T., Carey M., Johnson R. C. Yeast HMG proteins NHP6A/B potentiate promoter-specific transcriptional activation in vivo and assembly of preinitiation complexes in vitro. Genes Dev. 1996 Nov 1;10(21):2769–2781. doi: 10.1101/gad.10.21.2769. [DOI] [PubMed] [Google Scholar]
  32. Paull T. T., Johnson R. C. DNA looping by Saccharomyces cerevisiae high mobility group proteins NHP6A/B. Consequences for nucleoprotein complex assembly and chromatin condensation. J Biol Chem. 1995 Apr 14;270(15):8744–8754. doi: 10.1074/jbc.270.15.8744. [DOI] [PubMed] [Google Scholar]
  33. Primig M., Sockanathan S., Auer H., Nasmyth K. Anatomy of a transcription factor important for the start of the cell cycle in Saccharomyces cerevisiae. Nature. 1992 Aug 13;358(6387):593–597. doi: 10.1038/358593a0. [DOI] [PubMed] [Google Scholar]
  34. Ramer S. W., Elledge S. J., Davis R. W. Dominant genetics using a yeast genomic library under the control of a strong inducible promoter. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11589–11593. doi: 10.1073/pnas.89.23.11589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shykind B. M., Kim J., Sharp P. A. Activation of the TFIID-TFIIA complex with HMG-2. Genes Dev. 1995 Jun 1;9(11):1354–1365. doi: 10.1101/gad.9.11.1354. [DOI] [PubMed] [Google Scholar]
  36. Sidorova J. M., Mikesell G. E., Breeden L. L. Cell cycle-regulated phosphorylation of Swi6 controls its nuclear localization. Mol Biol Cell. 1995 Dec;6(12):1641–1658. doi: 10.1091/mbc.6.12.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sidorova J., Breeden L. Analysis of the SWI4/SWI6 protein complex, which directs G1/S-specific transcription in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Feb;13(2):1069–1077. doi: 10.1128/mcb.13.2.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Singh J., Dixon G. H. High mobility group proteins 1 and 2 function as general class II transcription factors. Biochemistry. 1990 Jul 3;29(26):6295–6302. doi: 10.1021/bi00478a026. [DOI] [PubMed] [Google Scholar]
  39. Thompson C. C., Brown T. A., McKnight S. L. Convergence of Ets- and notch-related structural motifs in a heteromeric DNA binding complex. Science. 1991 Aug 16;253(5021):762–768. doi: 10.1126/science.1876833. [DOI] [PubMed] [Google Scholar]

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