Regulated phosphorylation of the gal4p inhibitor gal80p of Kluyveromyces lactis revealed by mutational analysis

Biological Chemistry

Volumn 380, Issue 4, 1999, Pages 419-430

  Zenke, Frank T ^a,c   Kapp, Lutz ^a,b   Breunig, Karin D ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Activator; GAL genes; Transcription; Yeast regulation

Indexed keywords

FUNGAL PROTEIN; GALACTOSE;

ARTICLE; CULTURE MEDIUM; GENETIC TRANSCRIPTION; KLUYVEROMYCES; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; YEAST;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA PRIMERS; FUNGAL PROTEINS; KLUYVEROMYCES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPROTEINS; PHOSPHORYLATION; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

EID: 0032947871     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.1999.056     Document Type: Article

References (51)

1. Alani, E., Cao, L., and Kleckner, N. (1987). A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116, 541-545.
2. Ammerer, G. (1983). Expression of genes in yeast using the ADCI promoter. Methods Enzymol. 101, 192-201.
3. Bhat, P.J., and Hopper, J.E. (1991). The mechanism of inducer formation in gal3 mutants of the yeast galactose system is independent of normal galactose metabolism and mitochondrial respiratory function. Genetics 128, 233-239.
4. Bhat, P.J., and Hopper, J.E. (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.
5. Bhat, P.J., Oh, D., and Hopper, J.E. (1990). Analysis of the GAL3 signal transduction pathway activating GAL4 protein-dependent transcription in Saccharomyces cerevisiae. Genetics 125, 281-291.
6. Bianchi, M.M., Falcone, C., Jie, C.X., Wésolowski-Louvel, M., Frontali, L., and Fukuhara, H. (1987). Transformation of the yeast Kluyveromyces lactis by new vectors derived from the 1.6 μm circular plasmid pKD1. Curr Genet. 12, 185-192.
7. Blank, T.E., Woods, M.P., Lebo, C.M., Xin, P., and Hopper, J.E. (1997). Novel Gal3 proteins showing altered Gal80p binding cause constitutive transcription of Gal4p-activated genes in Saccharomyces cerevisiae. Mol. Cell Biol. 17, 2566-2575.
8. Boeke, J.D., LaCroute, F., and Fink, G.F. (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.
9. Boles, E., Göhlmann, H.W.H., and Zimmermann, F.K. (1996). Cloning of a second gene encoding 6-phosphofructo-2-kinase in yeast, and characterization of mutant strains without fructose-2,6-bisphosphate. Mol. Microbiol. 20, 65-76.
10. Breunig, K.D., and Kuger, P. (1987). Functional homology between the yeast regulatory proteins GAL4 and LAC9: LAC9-mediated transcriptional activation in Kluyveromyces lactis involves protein binding to a regulatory sequence homologous to the GAL4 protein-binding site. Mol. Cell Biol. 7, 4400-4406.
11. Chasman, D.I., and Kornberg, R.D. (1990). GAL4 protein: purification, association with GAL80 protein, and conserved domain structure. Mol. Cell Biol. 10, 2916-2923.
12. Czyz, M., Nagiec, M.M., and Dickson, R.C. (1993). Autoregulation of GAL4 transcription is essential for rapid growth of Kluyveromyces lactis on lactose and galactose. Nucleic Acids Res. 21, 4378-4382.
13. Douglas, H.C., and Hawthorne, D.C. (1972). Uninducible mutants in the gal locus of Saccharoymces cerevisiae. J. Bacteriol. 109, 1139-1143.
14. Johnston, M. (1987). A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol. Rev. 51, 458-476.
15. Johnston, M., and Carlson, M. (1992). Regulation of carbon and phosphate utilization. In: The Molecular and Cellular Biology of the Yeast Saccharomyces cerevisiae. Vol. II. E.W. Jones, J.R. Pringle, and J.R. Broach, eds. (Cold Spring Harbor: Cold Spring Harbor Laboratory Press), pp. 193-281.
16. Johnston, S.A., Salmeron, J.M., Jr., and Dincher, S.S. (1987). Interaction of positive and negative regulatory proteins in the galactose regulon of yeast. Cell 50, 143-146.
17. Kunkel, T.A., Roberts, J.D., and Zakour, R.A. (1987). Rapid and efficient site-specific mutagenensis without phenotypic selection. Methods Enzymol. 154, 367-382.
18. Leuther, K.K., and Johnston, S.A. (1992). Nondissociation of GAL4 and GAL80 in vivo after galactose induction. Science 256, 1333-1335.
19. Lohr, D., Venkov, P., and Zlatanova, J. (1995). Transcriptional regulation in the yeast GAL gene family: A complex genetic network. FASEB J. 9, 777-787.
20. Lue, N.F., Chasman, D.I., Buchman, A.R., and Kornberg, R.D. (1987). Interaction of GAL4 and GAL30 gene regulatory proteins in vitro. Mol. Cell Biol. 7, 3446-3451.
21. Ma, J., and Ptashne, M. (1987). The carboxy-terminal 30 amino acids of GAL4 are recognized by GAL80. Cell 50, 137-142.
22. Maniatis, T., Fritsch, E.F., and Sambrook, J. (1982). Molecular Cloning: A Laboratory Manual (Cold Spring Harbor, N.Y., USA: Cold Spring Harbor Laboratory).
23. Meyer, J., Walker-Jonah, A., and Hollenberg, C.P. (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.
24. Nogi, Y., and Fukasawa, T. (1989). Functional domains of a negative regulatory protein, GAL80, of Saccharomyces cerevisiae. Mol. Cell Biol. 9, 3009-3017.
25. Nogi, Y., Matsumoto, K., Toh-e, A., and Oshima, Y. (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.
26. Pan, T., Halvorsen, Y.-D., Dickson, R.C., and Coleman, J.E. (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.
27. Parthun, M.R., and Jaehning, J.A. (1992). A transcriptionally active form of GAL4 is phosphorylated and associated with GAL80. Mol. Cell Biol. 12, 4981-4987.
28. Platt, A., and Reece, R.J. (1998). The yeast galactose genetic switch is mediated by the formation of a Gal4p-Gal80p-Gal3p complex. EMBO J. 17, 4086-4091.
29. Reece, R.J., and Platt, A. (1997). Signalling activation and repression of RNA polymerase II transcription in yeast. BioEssays 19, 1001-1010.
30. Riley, M.I., Hopper, J.E., Johnston, S.A., and Dickson, R.C. (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.
31. Riley, M.I., and Dickson, R.C. (1984). Genetic and biochemical characterization of the galactose gene cluster in Kluyveromyces lactis. J. Bacteriol. 158, 705-712.
32. Rotman, B., and Spiegelman, S. (1953). The conversion of negatives to positives in "slow" adapting populations of yeast. J. Bacteriol. 66, 492-497.
33. Sadowski, I., Cosat, C., and Dhanawansa, R. (1996). Phosphorylation of Gal4p at a single C-terminal residue is necessary for galactose-inducible transcription. Mol. Cell Biol. 16, 4879-4887.
34. Salmeron, J.M., and Johnston, S.A. (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.
35. Salmeron, J.M., Langdon, S.D., and Johnston, S.A. (1989). Interaction between transcriptional activator protein LAC9 and negative regulatory protein GAL80. Mol. Cell Biol. 9, 2950-2956.
36. Schulz, W.A., Ebling, B., Hasse, A., Zenke, F., and Breunig, K. (1993). Highly efficient transactivation by the yeast Kluyveromyces lactis transcription factor LAC9 and its inhibition by the negative regulator GAL80 in mammalian cells. Biol. Chem. Hoppe-Seyler 374, 313-318.
37. Sherman, F., Fink, G.R., and Hicks, J.B. (1986). Laboratory Course Manual for Methods in Yeast Genetics. (Cold Spring Harbor, N.Y., USA: Cold Spring Harbor Laboratory).
38. Smith, D.B., and Johnson, K.S. (1988). Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67, 31-40.
39. Suzuki-Fujimoto, T., Fukuma, M., Yano, K.-I., Sakurai, H., Vonika, A., Johnston, S.A., and Fukasawa, T. (1996). Analysis of the galactose signal transduction pathway in Saccharomyces cerevisiae: Interaction between Gal3p and Gal180p. Mol. Cell Biol. 16, 2504-2508.
40. Walker-Jonah, A. (1988). Studies on the regulation of lactose utilisation in the yeast Kluyveromyces lactis. PhD Thesis, Heinrich-Heine-Universität Düsseldorf.
41. Wray, L.V.J., Witte, M.W., Dickson, R.C., and Riley, M.I. (1987). Characterization of a positive regulatory gene, LAC9, that controls induction of the lactose-galactose regulon of Kluyveromyces lactis: structural and functional relationships to GAL4 of Saccharomyces cerevisiae. Mol. Cell Biol. 7, 1111-1121.
42. Wu, Y., Reece, R.J., and Ptashne, M. (1996). Quantitation of putative activator-target affinities predicts transcriptional activating potentials. EMBO J. 15, 3951-3963.
43. Yano, K.-I., and Fukasawa, T. (1997). Galactose-dependent reversible interaction of Gal3p with Ga180p in the induction pathway of Gal4p-activated genes of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94, 1721-1726.
44. Yocum, R.R., Hanley, S., West, R.W., Jr., and Ptashne, M. (1984). Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol. Cell Biol. 4, 1985-1998.
45. Yun, S.-J., Hiraoka, Y., Nishizawa, M., Takio, K.,Titani, K., Nogi, Y., and Fukasawa, T. (1991). Purification and characterization of the yeast negative regulatory protein GAL80. J. Biol. Chem. 266, 693-697.
46. Zachariae, W. (1994). Regulation des Hefetranskriptionsaktivators Lac9. PhD thesis, Heinrich-Heine-Universität Düsseldorf.
47. Zachariae, W., and Breunig, K. D. (1993). Expression of the transcriptional activator LAC9 (KIGAL4) in Kluyveromyces lactis is controlled by autoregulation. Mol. Cell Biol. 13, 3058-3066.
48. Zachariae, W., Kuger, P., and Breunig, K.D. (1993). Glucose repression of lactose/galactose metabolism in Kluyveromyces lactis is determined by the concentration of the transcriptional activator LAC9 (KIGAL4). Nucl. Acids Res. 21, 69-77.
49. Zenke, F.T. (1995). Regulation des Lac9-Inhibitors Gal80 in Hefe. PhD thesis, Heinrich-Heine-Universität Düsseldorf.
50. Zenke, F., Zachariae, W., Lunkes, A., and Breunig, K.D. (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.
51. Zenke, F.T., Engels, R., Vollenbroich, V., Meyer, J., Hollenberg, C.P., and Breunig, K.D. (1996). Activation of Gal4p by galactose-dependent interaction of galactokinase and Ga180p. Science 272, 1662-1665.