1887

Abstract

In haploid cells, the -specific genes are expressed, whereas in the α haploid and /α diploid cell types their transcription is repressed. It is shown in this report that Itc1p, a component of the ATP-dependent Isw2p–Itc1p chromatin remodelling complex, is required for the repression of -specific genes. It has previously been reported that disruption of the gene leads, in α cells, to an aberrant cell morphology resembling the polarized mating projection of cells responding to pheromone. The activation of the pheromone signalling pathway in mutants of both mating types was examined and found to be constitutively active in α but not in cells. Furthermore, unlike the wild-type, α and / cells secrete -factor and express significant levels of other -specific genes. The results indicate that the inappropriate -factor production in a α context, due to the derepression of the -specific genes, produces an autocrine signalling loop that leads to the aberrant morphology displayed by α cells. It is suggested that the Isw2p–Itc1p complex contributes to maintain the repressive chromatin structure described for the operator present in the promoters of -specific genes.

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2003-02-01
2022-01-27
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References

  1. Bardwell L, Cook J. G, Voora D, Baggott D. M, Martinez A. R., Thorner J. 1998; Repression of yeast Ste12 transcription factor by direct binding of unphosphorylated Kss1 MAPK and its regulation by the Ste7 MEK. Genes Dev 12:2887–2898
    [Google Scholar]
  2. Blumer K. J, Reneke J. E., Thorner J. 1988; The STE2 gene product is the ligand-binding component of the alpha-factor receptor of Saccharomyces cerevisiae . J Biol Chem 263:10836–10842
    [Google Scholar]
  3. Caplan S., Kurjan J. 1991; Role of alpha-factor and the MF alpha 1 alpha-factor precursor in mating in yeast. Genetics 127:299–307
    [Google Scholar]
  4. Choi K. Y, Satterberg B, Lyons D. M., Elion E. A. 1994; Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae . Cell 78:499–512
    [Google Scholar]
  5. Christianson T. W, Sikorski R. S, Dante M, Shero J. H., Hieter P. 1992; Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119–122
    [Google Scholar]
  6. Cullen P. J, Schultz J, Horecka J, Stevenson B. J, Jigami Y., Sprague G. F. 2000; Defects in protein glycosylation cause SHO1 -dependent activation of a STE12 signaling pathway in yeast. Genetics 155:1005–1018
    [Google Scholar]
  7. de Groot P. W. J, Ruiz C, Vázquez de Aldana C. R. 14 other authors 2001; A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae . Comp Funct Genomics 2:124–142
    [Google Scholar]
  8. de Nobel H, Ruiz C, Martín H, Morris W, Brul S, Molina M., Klis F. M. 2000; Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2 lacZ expression, glucanase resistance and thermotolerance. Microbiology 146:2121–2132
    [Google Scholar]
  9. Deuring R, Fanti L, Armstrong J. A. 11 other authors 2000; The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell 5:355–365
    [Google Scholar]
  10. Dohlman H. G., Thorner J. W. 2001; Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu Rev Biochem 70:703–754
    [Google Scholar]
  11. Erdman S., Snyder M. 2001; A filamentous growth response mediated by the yeast mating pathway. Genetics 159:919–928
    [Google Scholar]
  12. Escribano M. V, Mazón M. J. 2000; Disruption of six novel ORFs from Saccharomyces cerevisiae chromosome VII and phenotypic analysis of the deletants. Yeast 16:621–630
    [Google Scholar]
  13. Fields S., Herskowitz I. 1987; Regulation by the yeast mating-type locus of STE12 , a gene required for cell-type-specific expression. Mol Cell Biol 7:3818–3821
    [Google Scholar]
  14. Gelbart M. E, Rechsteiner T, Richmond T. J., Tsukiyama T. 2001; Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol Cell Biol 21:2098–2106
    [Google Scholar]
  15. Goldmark J. P, Fazzio T. G, Estep P. W, Church G. M., Tsukiyama T. 2000; The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103:423–433
    [Google Scholar]
  16. Goutte C., Johnson A. D. 1994; Recognition of a DNA operator by a dimer composed of two different homeodomain proteins. EMBO J 13:1434–1442
    [Google Scholar]
  17. Gustin M. C, Albertyn J, Alexander M., Davenport K. 1998; MAP kinase pathways in the yeast Saccharomyces cerevisiae . Microbiol Mol Biol Rev 62:1264–1300
    [Google Scholar]
  18. Hagen D. C, McCaffrey G., Sprague G. F. Jr 1991; Pheromone response elements are necessary and sufficient for basal and pheromone-induced transcription of the FUS1 gene of Saccharomyces cerevisiae . Mol Cell Biol 11:2952–2961
    [Google Scholar]
  19. Herskowitz I. 1995; MAP kinase pathways in yeast: for mating and more. Cell 80:187–197
    [Google Scholar]
  20. Huang L, Zhang W., Roth S. Y. 1997; Amino termini of histones H3 and H4 are required for a1-alpha2 repression in yeast. Mol Cell Biol 17:6555–6562
    [Google Scholar]
  21. Ito H, Fukuda Y, Murata K., Kimura A. 1983; Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168
    [Google Scholar]
  22. Jenness D. D, Burkholder A. C., Hartwell L. H. 1983; Binding of alpha-factor pheromone to yeast a cells: chemical and genetic evidence for an alpha-factor receptor. Cell 35:521–529
    [Google Scholar]
  23. Johnson A. D. 1995; Molecular mechanisms of cell-type determination in budding yeast. Curr Opin Genet Dev 5:552–558
    [Google Scholar]
  24. Keleher C. A, Redd M. J, Schultz J, Carlson M., Johnson A. D. 1992; Ssn6-Tup1 is a general repressor of transcription in yeast. Cell 68:709–719
    [Google Scholar]
  25. Kent N. A, Karabetsou N, Politis P. K., Mellor J. 2001; In vivo chromatin remodeling by yeast ISWI homologs Isw1p and Isw2p. Genes Dev 15:619–626
    [Google Scholar]
  26. Kirkman-Correia C, Stroke I. L., Fields S. 1993; Functional domains of the yeast Ste12 protein, a pheromone-responsive transcriptional activator. Mol Cell Biol 13:3765–3772
    [Google Scholar]
  27. Komachi K, Redd M. J., Johnson A. D. 1994; The WD repeats of Tup1 interact with the homeo domain protein alpha 2. Genes Dev 8:2857–2867
    [Google Scholar]
  28. Leber R, Silles E, Sandoval I. V., Mazón M. J. 2001; Yol082p, a novel CVT protein involved in the selective targeting of aminopeptidase I to the yeast vacuole. J Biol Chem 276:29210–29217
    [Google Scholar]
  29. Leberer E, Dignard D, Harcus D, Thomas D. Y., Whiteway M. 1992; The protein kinase homologue Ste20p is required to link the yeast pheromone response G-protein beta gamma subunits to downstream signalling components. EMBO J 11:4815–4824
    [Google Scholar]
  30. Lee B. N., Elion E. A. 1999; The MAPKKK Ste11 regulates vegetative growth through a kinase cascade of shared signaling components. Proc Natl Acad Sci U S A 96:12679–12684
    [Google Scholar]
  31. Ma D, Cook J. G., Thorner J. 1995; Phosphorylation and localization of Kss1, a MAP kinase of the Saccharomyces cerevisiae pheromone response pathway. Mol Biol Cell 6:889–909
    [Google Scholar]
  32. MacKay V. L, Welch S. K, Insley M. Y, Manney T. R, Holly J, Saari G. C., Parker M. L. 1988; The Saccharomyces cerevisiae BAR1 gene encodes an exported protein with homology to pepsin. Proc Natl Acad Sci U S A 85:55–59
    [Google Scholar]
  33. Madhani H. D, Styles C. A., Fink G. R. 1997; MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91:673–684
    [Google Scholar]
  34. Mak A., Johnson A. D. 1993; The carboxy-terminal tail of the homeo domain protein alpha 2 is required for function with a second homeo domain protein. Genes Dev 7:1862–1870
    [Google Scholar]
  35. Martín H, Arroyo J, Sánchez M, Molina M., Nombela C. 1993; Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37 degrees C. Mol Gen Genet 241:177–184
    [Google Scholar]
  36. Martín H, Mendoza A, Rodríguez-Pachón J. M, Molina M., Nombela C. 1997; Characterization of SKM1 , a Saccharomyces cerevisiae gene encoding a novel Ste20/PAK-like protein kinase. Mol Microbiol 23:431–444
    [Google Scholar]
  37. Martín H, Rodríguez-Pachón J. M, Ruiz C, Nombela C., Molina M. 2000; Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae . J Biol Chem 275:1511–1519
    [Google Scholar]
  38. Miyajima I, Nakafuku M, Nakayama N, Brenner C, Miyajima A, Kaibuchi K, Arai K, Kaziro Y., Matsumoto K. 1987; GPA1 , a haploid-specific essential gene, encodes a yeast homolog of mammalian G protein which may be involved in mating factor signal transduction. Cell 50:1011–1019
    [Google Scholar]
  39. Nijbroek G. L., Michaelis S. 1998; Functional assays for analysis of yeast ste6 mutants. Methods Enzymol 292:193–212
    [Google Scholar]
  40. Printen J. A., Sprague G. F. Jr 1994; Protein-protein interactions in the yeast pheromone response pathway: Ste5p interacts with all members of the MAP kinase cascade. Genetics 138:609–619
    [Google Scholar]
  41. Rodríguez-Pachón J. M, Martín H, North G, Rotger R, Nombela C., Molina M. 2002; A novel connection between the yeast Cdc42 GTPase and the Slt2-mediated cell integrity pathway identified through the effect of secreted Salmonella GTPase modulators. J Biol Chem 277:27094–27102
    [Google Scholar]
  42. Roth A. F, Nelson B, Boone C., Davis N. G. 2000; Asg7p-Ste3p inhibition of pheromone signaling: regulation of the zygotic transition to vegetative growth. Mol Cell Biol 20:8815–8825
    [Google Scholar]
  43. Rothstein R. 1991; Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol 194:281–301
    [Google Scholar]
  44. Russell D. W, Jensen R, Zoller M. J, Burke J, Errede B, Smith M., Herskowitz I. 1986; Structure of the Saccharomyces cerevisiae HO gene and analysis of its upstream regulatory region. Mol Cell Biol 6:4281–4294
    [Google Scholar]
  45. Sabbagh W. Jr, Flatauer L. J, Bardwell A. J., Bardwell L. 2001; Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol Cell 8:683–691
    [Google Scholar]
  46. Shimizu M, Roth S. Y, Szent-Gyorgyi C., Simpson R. T. 1991; Nucleosomes are positioned with base pair precision adjacent to the alpha 2 operator in Saccharomyces cerevisiae . EMBO J 10:3033–3041
    [Google Scholar]
  47. Smith D. L., Johnson A. D. 1992; A molecular mechanism for combinatorial control in yeast: MCM1 protein sets the spacing and orientation of the homeodomains of an alpha 2 dimer. Cell 68:133–142
    [Google Scholar]
  48. Sugiyama M., Nikawa J. 2001; The Saccharomyces cerevisiae Isw2p-Itc1p complex represses INO1 expression and maintains cell morphology. J Bacteriol 183:4985–4993
    [Google Scholar]
  49. Trachtulcova P, Janatova I, Kohlwein S. D., Hasek J. 2000; Saccharomyces cerevisiae gene ISW2 encodes a microtubule-interacting protein required for premeiotic DNA replication. Yeast 16:35–47
    [Google Scholar]
  50. Tsukiyama T, Palmer J, Landel C. C, Shiloach J., Wu C. 1999; Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae . Genes Dev 13:686–697
    [Google Scholar]
  51. Tzamarias D., Struhl K. 1994; Functional dissection of the yeast Cyc8-Tup1 transcriptional co-repressor complex. Nature 369:758–761
    [Google Scholar]
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