The Gal3p-Gal80p-Gal4p transcription switch of yeast: Gal3p destabilizes the Gal80p-Gal4p complex in response to galactose and ATP

Molecular and Cellular Biology

Volumn 19, Issue 11, 1999, Pages 7828-7840

  Sil, Alok Kumar ^a   Alam, Samina ^a   Xin, Ping ^a   Ma, Ly ^a   Morgan, Melissa ^a   Lebo, Colleen M ^a   Woods, Michael P ^a   Hopper, James E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GALACTOSE; TRANSCRIPTION FACTOR;

ARTICLE; MOLECULAR INTERACTION; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0000225069     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.11.7828     Document Type: Article

References (84)

1. Adams, A., D. E. Gottschling, C. A. Kaiser, and T. Stearns. 1997. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
2. Amberg, D. C., D. Botstein, and E. M. Beaslej. 1995. Precise gene disruption in Saccharomyces cerevisiae by double fusion polymerase chain reaction. Yeast 11:1275-1280.
3. Ansari, A. Z., R. J. Reece, and M. Ptashne. 1998. A transcriptional activating region with two contrasting modes of protein interaction. Proc. Natl. Acad. Sci. USA 95:13543-13548.
4. Barberis, A., J. Pearlberg, N. Simkovich, S. Farrell, P. Reinagel, C. Bamdad, G. Sigal, and M. Ptashne. 1995. Contact with a component of the polymerase II holoenzyme suffices for gene activation. Cell 81:359-368.
5. Bartel, P. L., and S. Fields. 1995. Analyzing protein-protein interactions using two-hybrid system. Methods Enzymol. 254:241-263.
6. Bhat, P. J., and J. E. Hopper. 1992. Overproduction of the GAL1 or GAL3 protein causes galactose-independent activation of the GAL4 protein: evidence for a new model of induction for the yeast GAL/MEL regulon. Mol. Cell. Biol. 12:2701-2707.
7. Bhat, P. J., D. Oh, and J. E. Hopper. 1990. Analysis of the GAL3 signal transduction pathway activating GAL4 protein-dependent transcription in Saccharomyces cerevisiae. Genetics 125:281-291.
8. Blank, T. E., M. P. Woods, C. M. Lebo, P. Xin, and J. E. Hopper. 1997. Novel Gal3 proteins showing altered Gal80p binding cause constitutive transcription of Gal4p-activated genes in Saccharomyces cerevisiae. Mol. Cell. Biol, 17:2566-2575.
9. Boeke, J. D., F. LaCroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346.
10. Bram, R. J., and R. D. Kornberg. 1985. Specific protein binding to far upstream activating sequences in polymerase II promoters. Proc. Natl. Acad. Sci. USA 82:43-47.
11. Brent, R., and M. Ptashne. 1985. A eukaryotic transcriptional activator bearing the DNA specificity of a prokaryotic repressor. Cell 43:729-736.
12. Broach, J. R. 1979. Galactose regulation in Saccharomyces cerevisiae. The enzymes encoded by the GAL7, 10, 1 cluster are co-ordinately controlled and separately translated. J. Mol. Biol. 131:41-53.
13. Carey, M., H. Kakidani, J. Leatherwood, F. Mostashari, and M. Ptashne. 1989. An amino-terminal fragment of GAL4 binds DNA as a dimer. J. Mol. Biol. 209:423-432.
14. Cavender, J. F., A. Conn, M. Epler, H. Lacko, and M. J. Tevethia. 1995. Simian virus 40 large T antigen contains two independent activities that cooperate with a ras oncogene to transform rat embryo fibroblasts. J. Virol. 69:923-934.
15. Chen, D. C., B. C. Yang, and T. T. Kuo. 1992. One-step transformation of yeast in stationary phase. Curr. Genet. 21:83-84.
16. Czyz, M., M. M. Nagiec, and R. C. Dickson. 1993. Autoregulation of GAL4 transcription is essential for rapid growth of Kluyveromyces lactis on lactose and galactose. Nucleic Acids Res. 21:4378-4382.
17. Denis, C. L., J. Ferguson, and E. T. Young. 1983. mRNA levels for the fermentative alcohol dehydrogenase of Saccharomyces cerevisiae decrease upon growth on a nonfermentable carbon source. J. Biol. Chem. 258:1165-1171.
18. Ding, W. V., and S. A. Johnston. 1997. The DNA binding and activation domains of Gal4p are sufficient for conveying its regulatory signals. Mol. Cell. Biol. 17:2538-2549.
19. Douglas, H., and G. Pelroy. 1963. A gene controlling inducibility of the galactose pathway enzymes in Saccharomyces. Biochim. Biophys. Acta 68: 155-156.
20. Douglas, H. C., and C. D. Hawthorne. 1972. Uninducible mutants in the gal i locus of Saccharomyces cerevisiae. J. Bacteriol. 109:1139-1143.
21. Erhart, E., and C. P. Hollenberg. 1981. Curing of Saccharomyces cerevisiae 2-μm DNA by transformation. Curr. Genet. 3:83-89.
22. Erhart, E., and C. P. Hollenberg. 1983. The presence of a defective LEU2 gene on 2 mu DNA recombinant plasmids of Saccharomyces cerevisiae is responsible for curing and high copy number. J. Bacteriol. 156:625-635.
23. Fujiki, M., and K. Verner. 1993. Coupling of cytosolic protein synthesis and mitochondrial protein import in yeast. Evidence for cotranslational import in vivo. J. Biol. Chem. 268:1914-1920.
24. Gadhavi, P. L. 1998. Structural dissection of the DNA-binding domain of the yeast transcriptional activator GAL4 reveals an alpha-helical region responsible for dimerization. J. Protein Chem. 17:591-598.
25. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
26. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base-pair restriction sites. Gene 74:527-534.
27. Giniger, E., S. M. Varnum, and M. Ptashne. 1985. Specific DNA binding of GAL4, a positive regulatory protein of yeast. Cell 40:767-774.
28. Guldener, U., S. Heck, T. Fielder, J. Beinhauer, and J. H. Hegemann. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24:2519-2524.
29. Harper, J. W., G. R. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
30. Igarashi, M., T. Segawa, Y. Nogi, Y. Suzuki, and T. Fukasawa. 1987. Autogenous regulation of the Saccharomyces cerevisiae regulatory gene GAL80. Mol. Gen. Genet. 207:273-279.
31. Irani, M., W. E. Taylor, and E. T. Young. 1987. Transcription of the ADH2 gene in Saccharomyces cerevisiae is limited by positive factors that bind competitively to its intact promoter region on multicopy plasmids. Mol. Cell. Biol. 7:1233-1241.
32. Johnston, M., and M. Carlson. 1992. Regulation of carbon and phosphate utilization, vol. II. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
33. Johnston, M., and J. Dover. 1988. Mutational analysis of the GAL4-encoded transcriptional activator protein of Saccharomyces cerevisiae. Genetics 120: 63-74.
34. Johnston, S. A., and J. E. Hopper. 1982. Isolation of the yeast regulatory gene GAL4 and analysis of its dosage effects on the galactose/melibiose regulon. Proc. Natl. Acad. Sci. USA 79:6971-6975.
35. Johnston, S. A., J. M. Salmeron, Jr., and S. S. Dincher. 1987. Interaction of positive and negative regulatory proteins in the galactose regulon of yeast. Cell 50:143-146.
36. Keegan, L., G. Gill, and M. Ptashne. 1986. Separation of DNA binding from the transcription-activating function of a eukaryotic regulatory protein. Science 231:699-704.
37. Koh, S. S., A. Z. Ansari, M. Ptashne, and R. A. Young. 1998. An activator target in the RNA polymerase II holoenzyme. Mol. Cell 1:895-904.
38. Leuther, K. K., and S. A. Johnston. 1992. Nondissociation of GAL4 and GAL80 in vivo after galactose induction. Science 256:1333-1335.
39. Leuther, K. K., J. M. Salmeron, and S. A Johnston. 1993. Genetic evidence that an activation domain of GAL4 does not require acidity and may form a beta sheet. Cell 72:575-585.
40. Lohr, D., P. Venkov, and J. Zlatanova. 1995. Transcriptional regulation in the yeast GAL gene family: a complex genetic network. FASEB J. 9:777-787.
41. Lue, N. F., D. I. Chasman, A. R. Buchman, and R. D. Kornberg. 1987. Interaction of GAL4 and GAL80 gene regulatory proteins in vitro. Mol. Cell. Biol. 7:3446-3451.
42. Ma, J., and M. Ptashne. 1987. The carboxy-terminal 30 amino acids of GAL4 are recognized by GAL80. Cell 50:137-142.
43. Ma, J., and M. Ptashne. 1987. Deletion analysis of GAL4 defines two transcriptional activating segments. Cell 48:847-853.
44. Ma, J., and M. Ptashne. 1987. A new class of yeast transcriptional activators. Cell 51:113-119.
45. Marmorstein, R., M. Carey, M. Ptashne, and S. C. Harrison. 1992. DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356:408-414.
46. Melcher, K., and S. A. Johnston. 1995. GAL4 interacts with TATA-binding protein and coactivators. Mol. Cell. Biol. 15:2839-2848.
47. Meyer, J., A. Walker-Jonah, and C. P. Hollenberg. 1991. Galactokinase encoded by GAL1 is a bifunctional protein required for induction of the GAL genes in Kluyveromyces lactis and is able to suppress the Gal3 phenotype in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:5454-5461.
48. Mylin, L. M., K. J. Hofmann, L. D. Schultz, and J. E. Hopper. 1990. Regulated GAL4 expression cassette providing controllable and high-level output from high-copy galactose promoters in yeast. Methods Enzymol. 185: 297-308.
49. Nogi, Y. 1986. GAL3 gene product is required for maintenance of the induced state of the GAL cluster genes in Saccharomyces cerevisiae. J. Bacteriol. 165:101-106.
50. Nogi, Y., and T. Fukasawa. 1984. Nucleotide sequence of the yeast regulatory gene GAL80. Nucleic Acids Res. 12:9287-9298.
51. Nogi, Y., K. Matsumoto, A. Toh-e, and Y. Oshima. 1977. Interaction of super-repressible and dominant constitutive mutations for the synthesis of galactose pathway enzymes in Saccharomyces cerevisiae. Mol. Gen. Genet. 152:137-144.
52. Pan, T., Y. D. Halvorsen, R. C. Dickson, and J. E. Coleman. 1990. The transcription factor LAC9 from Kluyveromyces lactis-like GAL4 from Saccharomyces cerevisiae forms a Zn(II)2Cys6 binuclear cluster. J. Biol. Chem. 265:21427-21429.
53. Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346-356.
54. Platt, A., and R. J. Reece. 1998. The yeast galactose genetic switch is mediated by the formation of a Ga14p-Ga180p-Ga13p complex. EMBO J. 17:4086-4091.
55. Post-Beittenmiller, M. A., R. W. Hamilton, and J. E. Hopper. 1984. Regulation of basal and induced levels of the MEL1 transcript in Saccharomyces cerevisiae. Mol. Cell. Biol. 4:1238-1245.
56. Reece, R. J., and A. Platt 1997. Signaling activation and repression of RNA polymerase II transcription in yeast. Bioessays 19:1001-1010.
57. Riley, M. I., J. E. Hopper, S. A. Johnston, and R. C. Dickson. 1987. GAL4 of Saccharomyces cerevisiae activates the lactose-galactose regulon of Kluyveromyces lactis and creates a new phenotype: glucose repression of the regulon. Mol. Cell. Biol. 7:780-786.
58. Rose, M. D., F. Winston, and P. Heiter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
59. Rose, M. D., P. Novick, J. H. Thomas, D. Holstein, and G. R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60:237-243.
60. Sadowski, I., C. Costa, and R. Dhanawansa. 1996. Phosphorylation of Ga14p at a single C-terminal residue is necessary for galactose-inducible transcription. Mol. Cell. Biol. 16:4879-4887.
61. Sadowski, I., J. Ma, S. Triezenberg, and M. Ptashne. 1988. GAL4-VP16 is an unusually potent transcriptional activator. Nature 335:563-564.
62. Salmeron, J. M., Jr., and S. A. Johnston. 1986. Analysis of the Kluyveromyces lactis positive regulatory gene LAC9 reveals functional homology to, but sequence divergence from the Saccharomyces cerevisiae GAL4 gene. Nucleic Acids Res. 14:7767-7781.
63. Salmeron, J. M., Jr., S. D. Langdon, and S. A. Johnston. 1989. Interaction between transcriptional activator protein LAC9 and negative regulatory protein GAL80. Mol. Cell. Biol. 9:2950-2956.
64. Salmeron, J. M., Jr., K. K. Leuther, and S. A. Johnston. 1990. GAL4 mutations that separate the transcriptional activation and GAL80-interactive functions of the yeast GAL4 protein. Genetics 125:21-27.
65. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
66. Sil, A. K., et al. Unpublished data.
67. Silver, P. A., L. P. Keegan, and M. Ptashine. 1984. Amino terminus of the yeast GAL4 gene product is sufficient for nuclear localization. Proc. Natl. Acad. Sci. USA 81:5951-5955.
68. Stone, G., and I. Sadowski. 1993. GAL4 is regulated by a glucose-responsive functional domain. EMBO J. 12:1375-1385.
69. Suzuki-Fujimoto, T., M. Fukuma, K. I. Yano, H. Sakurai, A. Vonika, S. A. Johnston, and T. Fukasawa. 1996. Analysis of the galactose signal transduction pathway in Saccharomyces cerevisiae: interaction between Gal3p and Gal180p. Mol. Cell. Biol. 16:2504-2508.
70. Torchia, T. E., R. W. Hamilton, C. L. Cano, and J. E. Hopper. 1984. Disruption of regulatory gene GAL80 in Saccharomyces cerevisiae: effects on carbon-controlled regulation of the galactose/melibiose pathway genes. Mol. Cell. Biol. 4:1521-1527.
71. Torchia, T. E., and J. E. Hopper. 1986. Genetic and molecular analysis of the GAL3 gene in the expression of the galactose/melibiose regulon of Saccharomyces cerevisiae. Genetics 113:229-246.
72. Tornow, J., and G. M. Santangelo. 1990. Efficient expression of the Saccharomyces cerevisiae gtycolytic gene ADH1 is dependent upon a cis-acting regulatory element (UASRPG) found initially in genes encoding ribosomal proteins. Gene 90:79-85.
73. Triezenberg, S. J. Personal communication.
74. Verner, K., and M. Weber. 1989. Protein import into mitochondria in a homologous yeast in vitro system. J. Biol. Chem. 264:3877-3879.
75. Vojtek, A. B., and S. M. Hollenberg. 1995. Ras-Raf interaction: two-hybrid analysis. Methods Enzymol. 255:331-342.
76. Webster, T. D., and R. C. Dickson. 1988. The organization and transcription of the galactose gene cluster of Kluyveromyces lactis. Nucleic Acids Res. 16:8011-8028.
77. Woods, M. P., and J. E. Hopper. Unpublished data.
78. Wu, Y., R. J. Reece, and M. Ptashne. 1996. Quantitation of putative activator-target affinities predicts transcriptional activating potentials. EMBO J. 15:3951-3963.
79. Yano, K., and T. Fukasawa. 1997. Galactose-dependent reversible interaction of Gal3p with Gal80p in the induction pathway of Gal4p-activated genes of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94:1721-1726.
80. Yocum, R. R., and M. Johnston. 1984. Molecular cloning of the GAL80 gene from Saccharomyces cerevisiae and characterization of a gal80 deletion. Gene 32:75-82.
81. Zachariae, W., and K. D. Breunig. 1993. Expression of the transcriptional activator LAC9 (KlGAL4) in Kluyveromyces lactis is controlled by autoregulation. Mol. Cell. Biol. 13:3058-3066.
82. Zenke, F. T., R. Engles, V. Vollenbroich, J. Meyer, C. P. Hollenberg, and K. D. Breunig. 1996. Activation of Ga14p by galactose-dependent interaction of galactokinase and Gal80p. Science 272:1662-1665. (Erratum, 273:417, 1996.)
83. Zenke, F. T., L. Kapp, and K. D. Breunig. 1999. Regulated phosphorylation of the Gal4p inhibitor Gal80p of Kluyveromyces lactis revealed by mutational analysis. Biol. Chem. 380:419-430.
84. Zenke, F. T., W. Zachariae, A. Lunkes, and K. D. Breunig. 1993. Gal80 proteins of Kluyveromyces lactis and Saccharomyces cerevisiae are highly conserved but contribute differently to glucose repression of the galactose regulon. Mol. Cell. Biol. 13:7566-7576.