The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae

EMBO Journal

Volumn 17, Issue 5, 1998, Pages 1236-1247

  Lorenz, Michael C ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Ammonium permease; MEP2; Pseudohyphal differentiation; Yeast

Indexed keywords

AMMONIA; AMMONIUM PERMEASE; CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE; NITROGEN; PERMEASE; PHEROMONE; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DIPLOIDY; GENE MUTATION; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; SENSOR; STARVATION; YEAST; YEAST CELL;

CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; CYCLIC AMP; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GTP-BINDING PROTEIN ALPHA SUBUNITS; GTP-BINDING PROTEINS; HETEROTRIMERIC GTP-BINDING PROTEINS; ION TRANSPORT; MEMBRANE TRANSPORT PROTEINS; MUTATION; PROTEIN KINASES; QUATERNARY AMMONIUM COMPOUNDS; RAS PROTEINS; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SUPPRESSION, GENETIC;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0032473497     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.5.1236     Document Type: Article

References (62)

1. Alspaugh,J.A., Perfect,J.R. and Heitman,J. (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev., 11, 3206-3217.
2. Andre,B. (1995) An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast, 11, 1575-1611.
3. Banuett, F. (1991) Identification of genes governing filamentous growth and tumor induction by the plant pathogen Ustilago maydis. Proc. Natl Acad. Sci. USA, 88, 3922-3926.
4. Cardenas, M.E., Lim, E. and Heitman, J. (1995) Mutations that perturb cyclophilin A ligand binding pocket confer cyclosporin A resistance in Saccharomyces cerevisiae. J. Biol. Chem., 270, 20997-21002.
5. Coschigano, P.W. and Magasanik, B. (1991) The URE2 gene product of Saccharomyces cerevisiae plays an important role in the cellular response to the nitrogen source and has homology to gluthathione S-transferases. Mol. Cell Biol., 11, 822-832.
6. Doherty, D. (1970) L-Glutamate dehydrogenase, yeast. Methods Enzymol., 17A, 850-856.
7. Dubois, E. and Grenson, M. (1979) Methylamine/ammonia uptake systems in Saccharomyces cerevisiae: Multiplicity and regulation. Mol. Gen. Genet., 175, 67-76.
8. Field, J., Nikawa, J.-i., Broek, D., MacDonald, B., Rodgers, L., Wilson, I.A., Lerner,R.A. and Wigler,M. (1988) Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol., 8, 2159-2165.
9. Gietz,R.D. and Sugino,A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene, 74, 527-534.
10. Gimeno,C.J. and Fink,G.R. (1994) Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol. Cell. Biol., 14, 2100-2112.
11. Gimeno,C.J., Ljungdahl,P.O., Styles,C.A. and Fink,G.R. (1992) Unipolar cell divisions in the yeast S.cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell, 68, 1077-1090.
12. Gold,S., Duncan,G., Barrett,K. and Kronstad,J. (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev., 8, 2805-2816.
13. Grenson,M. (1983a) Inactivation-reactivation process and repression of permease formation regulate several ammonia-sensitive permeases in the yeast Saccharomyces cerevisiae. Eur. J. Biochem., 133, 135-139.
14. Grenson,M. (1983b) Study of the positive control of the general amino acid permease and other ammonia-sensitive uptake systems by the product of NPRl gene in the yeast Saccharomyces cerevisiae. Eur. J. Biochem., 133, 141-144.
15. Grenson, M (1992) Amino acid transporters in yeast: structure, function and regulation. In de Pont,J. (ed.), Molecular Aspects of Transport Proteins. Elsevier, New York. pp. 219-245.
16. Grenson,M. and Acheroy,B. (1982) Mutations affecting the activity and the regulation of the general amino-acid permease of Saccharomyces cerevisiae. Mol. Gen. Genet., 188, 261-265.
17. Grenson,M. and Dubois,E. (1982) Pleiotropic deficiency in nitrogenuptake systems and derepression of nitrogen-catabolic enzymes in npr-1 mutants of Saccharomyces cerevisiae. Eur. J. Biochem., 121, 643-647.
18. Grenson,M., Mousset,M., Wiame,J.M. and Bechet,J. (1966) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. I. Evidence for a specific arginine-transporting system. Biochim. Biophys. Acta, 127, 325-338.
19. Hartmann,H.A., Kahmann,R. and Bolker,M. (1996) The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J., 15, 1632-1641.
20. Hein,C., Springael, J.-Y., Volland,C., Haguenauer-Tsapis,R. and Andre,B. (1995) NPI1, an essential yeast gene involved in induced degradation of Gapl and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol., 18, 77-87.
21. Huibregste,J.M., Scheffner,M., Beaudenon,S. and Howley,P.M. (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl Acad. Sci. USA, 92, 2563-2567.
22. Isshiki,T., Mochizuki,N., Maeda,T. and Yamamoto,M. (1992) Characterization of a fission yeast gene, gpa2, that encodes a Gα subunit involved in the monitoring of nutrition. Genes Dev., 6, 2455-2462.
23. Kron,S.J., Styles,C.A. and Fink,G.R. (1994) Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol. Biol. Cell. 5, 1003-1022,
24. Kronstad,J.W. (1997) Virulence and cAMP in smuts, blasts and blights. Trends Plant Sci., 2, 193-199.
25. Kübler,E., Mösch,H.-U., Rupp,S. and Lisanti.M.P (1997) Gpa2p. a G protein α-subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism. J. Biol. Chem., 272, 20321-20323.
26. Kwon-Chung,K.J., Edman,J.C. and Wickes,B.L. (1992) Genetic association of mating types and virulence in Cryptococcus neoformans. Infect, Immun., 60, 602-605.
27. Laloux, I., Jacobs,E. and Dubois,E. (1994) Involvement of SRE element of Tyl transposon in TEC 1-dependent transcriptional activation. Nucleic Acids Res., 22, 999-1005.
28. Liang,H. and Gaber,R.F. (1996) A novel signal transduction pathway in Saccharomyces cerevisiae defined by Snf3-regulated expression of HXT6. Mol. Biol. Cell, 7, 1953-1966.
29. Liu,H., Styles,C.A. and Fink,G.R. (1993) Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science, 262, 1741-1744.
30. Lo,H.-J., Kohler,J.R., DiDomenico,B., Loebenberg,D., Cacciapuoti,A. and Fink,G.R. (1997) Nonfilamentous C.albicans mutants are avirulent. Cell, 90, 939-949.
31. Lorenz,M.C. and Heitman,J. (1997) Yeast pseudohyphal growth is regulated by GPA2, a G protein α homolog. EMBO J., 16, 7008-7018.
32. Madhani,H.D. and Fink,G.R. (1997) Combinatorial control required for the specificity of yeast MAPK signaling. Science, 275, 1314-1317.
33. Madi, L., McBride, S.K., Bailey, L.A. and Ebbole, D.J. (1997) rco-3, a gene involved in glucose transport and conidiation in Neurospora crassa. Genetics, 146, 499-506.
34. Maeda,T., Mochizuki,N. and Yamainoto,M. (1990) Adenylyl cyclase is dispensable for vegetative cell growth in the fission yeast Schizosaccharomyces pombe, Proc. Natl Acad. Sci. USA, 87, 7814-7818.
35. Magasanik.B. (1992) Regulation of nitrogen utilization. In Jones,E.W., Pringle,J.Rand Broach,J.R. (eds), The Molecular and Cellular Biology of the Yeast Saccharomyces. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 283-317.
36. Marini,A.-M., Soussi-Boudekou,S., Vissers,S. and Andre,B. (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol. Cell. Biol., 17, 4282-4293.
37. Marini,A.-M., Vissers,S., Urrestarazu,A. and Andre,B. (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J., 13, 3456-3463.
38. Minehart,P.L., and Magasanik,B. (1991) Sequence and expression of GLN3, a positive nitrogen regulatory gene of Saccharomyces cerevisiae encoding a protein with a putative zinc finger DNA-binding domain. Mol. Cell Biol., 11, 6216-6228.
39. Mitchell,A.P., and Magasanik,B. (1983) Purification and characterization of glutamine synthetase from Saccharomyces cerevisiae. J. Biol. Chem., 258, 119-124.
40. Mosch,H.-U., Roberts,R.L. and Fink,G.R. (1996 Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc. Natl Acad. Sci USA, 93, 5352-5356.
41. Nakafuku,M. et al. (1988) Isolation of a second yeast Saccharomyces cerevisiae gene (GPA2) coding for guanine nucleotide-binding regulatory protein: Studies on its structure and possible functions. Proc. Natl Acad. Sci. USA, 85, 1374-1378.
42. Niimi,M., Niimi,K., Tokunaga,J. and Nakayama,H. (1980) Changes in cyclic nucleotide levels and dimorphic transition in Candida albicans. J. Bacteriol., 142, 1010-1014.
43. Ozcan, S., Dover, J., Rosenwald,A.G., Woelfl,S. and Johnston,M. (1996) Two glucose transporters in S.cerevisiae are glucose sensors that generate a signal for induction of gene expression. Proc. Natl Acad. Sci. USA, 93, 12428-12432.
44. Palkova,Z., Janderova,B., Gabriel,J., Zikanova,B., Pospisek,M., and Forstova,J. (1997) Ammonia mediates communication between yeast colonies. Nature, 390, 532-536.
45. Regenfelder,E., Spellig,T., Hartmann,A., Lauenstein,S., Bölker,M. and Kahmann,R. (1996) G proteins in Ustilago maydis: transmission of multiple signals? EMBO J., 16, 1934-1942.
46. Sabie,F.T. and Gadd,G.M. (1992) Effect of nucleosides and nucleotides and the relationship between cellular adenosine 3′:5′-cyclic monophosphate (cyclic AMP) and germ tube formation in Candida albicans, Mycopathologia, 119, 147-156.
47. Schneider,B.L., Seufert,W., Steiner,B., Yang,Q.H, and Futcher,B. (1995) Use of polyrnerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae. Yeast, 11, 1265-1274.
48. Schiestl,R.H., Manivasakam,P., Woods,R.A. and Gietz,R.D. (1993) Introducing DNA into yeast by transformation. Methods, 5, 79-85.
49. Sherman,F. (1991) Getting started with yeast. Methods Enzymol., 194, 3-21.
50. Sikorski,R.S. and Hieter,P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
51. Stanbrough,M., Rowen,D.W., and Magasanik,B. (1995) Role of the GATA factors Gln3p and Nillp of Saccharomyces cerevisiae in the expression of nitrogen-regulated genes. Proc, Natl Acad. Sci. USA, 92, 9450-9454.
52. Stevenson,B.J., Rhodes,N., Errede,B. and Sprague,G.F.,Jr. (1992) Constitutive mutants of the protein kinase STE11 activate the pheromone response pathway in the absence of the G protein. Genes Dev.,6, 1293-1304.
53. 3 with the use of glutamic dehydrogenase. Methods Enzymol., 17, 955.
54. Toda,T. et al. (1985) In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell, 40, 27-36.
55. Tolkacheva,T., McNamara,P., Piekarz,E. and Courchesne,W. (1994) Cloning of a Cryptococcus neoformans gene, GPA1, encoding a Gprotein α-subunit homolog. Infect, Immun., 62, 2849-2856.
56. Vandenbol,M., Jauniaux,J.-C. and Grenson,M (1990) The Saccharomyces cerevisiae NPR1 gene required for the activity of ammonia-sensitive amino acid permeases encodes a protein kinase homologue. Mol. Gen. Genet., 222, 393-399.
57. Vandenbol,M., Jauniaux,J.-C, Vissers,S. and Grenson,M. (1987) Isolation of the NPR1 gene responsible for the reactivation of ammonia-sensitive amino acid permeases in Saccharomyces cerevisiae. Eur. J. Biochem., 164, 607-612.
58. Wach,A., Brachat,A, Pohimann,R. and Philippsen,P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast, 10, 1793-1808.
59. Wickes,B.L., Mayorga.M.E., Edman,U. and Edman,J.C. (1996) Dimorphism and haploid fruiting in Cryptococcus neoformans: Association with the α-mating type. Proc. Natl Acad. Sci. USA, 93, 7327-7331.
60. Wickner, R.B. (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science, 264, 566-569.
61. Xu, S., Falvey, D.A., and Brandriss,M.C. (1995) Roles of URE2 and CLN3 in the proline utilization pathway in Saccharomyces cerevisiae. Mol. Cell Biol., 15, 2321-2330.
62. Yarden,O., Plamann,M., Ebbole,D.I. and Yanofsky,C. (1992) cot-1, a gene required for hyphal elongation in Neurospora crassa, encodes a protein kinase. EMBO J., 11, 2159-2166.