Home LiteratureArticle Details
PMID: 10233147 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae.

Molecular biology of the cell ·Vol. 10 ·No. 5 ·1999-05-00 ·Pages 1325-35

Mösch HU, Kübler E, Krappmann S, Fink GR, Braus GH

Abstract

The two highly conserved RAS genes of the budding yeast Saccharomyces cerevisiae are redundant for viability. Here we show that haploid invasive growth development depends on RAS2 but not RAS1. Ras1p is not sufficiently expressed to induce invasive growth. Ras2p activates invasive growth using either of two downstream signaling pathways, the filamentation MAPK (Cdc42p/Ste20p/MAPK) cascade or the cAMP-dependent protein kinase (Cyr1p/cAMP/PKA) pathway. This signal branch point can be uncoupled in cells expressing Ras2p mutant proteins that carry amino acid substitutions in the adenylyl cyclase interaction domain and therefore activate invasive growth solely dependent on the MAPK cascade. Both Ras2p-controlled signaling pathways stimulate expression of the filamentation response element-driven reporter gene depending on the transcription factors Ste12p and Tec1p, indicating a crosstalk between the MAPK and the cAMP signaling pathways in haploid cells during invasive growth.

MeSH Terms
Adenylyl Cyclases/metabolism Amino Acid Sequence Binding Sites Calcium-Calmodulin-Dependent Protein Kinases/metabolism Cell Cycle Proteins/genetics,metabolism Conserved Sequence Cyclic AMP/metabolism Cyclic AMP-Dependent Protein Kinases/metabolism DNA-Binding Proteins/genetics,metabolism FMN Reductase Fungal Proteins/genetics,metabolism GTP-Binding Proteins/genetics,metabolism Gene Expression Regulation, Fungal Genes, Reporter Genes, Suppressor Haploidy Intracellular Signaling Peptides and Proteins MAP Kinase Kinase Kinases Molecular Sequence Data Mutation NADH, NADPH Oxidoreductases/genetics,metabolism Protein Serine-Threonine Kinases/genetics,metabolism Saccharomyces cerevisiae/genetics,growth & development,metabolism Saccharomyces cerevisiae Proteins Transcription Factors/genetics,metabolism cdc42 GTP-Binding Protein, Saccharomyces cerevisiae ras Proteins/genetics,metabolism
Chemicals
Cell Cycle Proteins DNA-Binding Proteins Fungal Proteins Intracellular Signaling Peptides and Proteins STE12 protein, S cerevisiae Saccharomyces cerevisiae Proteins TEC1 protein, S cerevisiae Transcription Factors Cyclic AMP FMN Reductase NADH, NADPH Oxidoreductases ferric citrate iron reductase Protein Serine-Threonine Kinases Cyclic AMP-Dependent Protein Kinases Calcium-Calmodulin-Dependent Protein Kinases MAP Kinase Kinase Kinases STE20 protein, S cerevisiae GTP-Binding Proteins RAS1 protein, S cerevisiae RAS2 protein, S cerevisiae cdc42 GTP-Binding Protein, Saccharomyces cerevisiae ras Proteins Adenylyl Cyclases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mösch H U
Institute for Microbiology and Genetics, Georg-August-University, D-37077 Göttingen, Germany.
Kübler E
Krappmann S
Fink G R
Braus G H
References (42)
42 references, click to expand
  1. Divergent roles of RAS1 and RAS2 in yeast longevity.
    J Biol Chem. 1994 Jul 15;269(28):18638-45 PMID: 8034612
  2. Requirement of Saccharomyces cerevisiae Ras for completion of mitosis.
    Science. 1995 Nov 17;270(5239):1213-5 PMID: 7502049
  3. Gpa2p, a G-protein alpha-subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism.
    J Biol Chem. 1997 Aug 15;272(33):20321-3 PMID: 9252333
  4. Raf: the holy grail of Ras biology?
    Trends Cell Biol. 1994 Oct;4(10):347-50 PMID: 14731620
  5. ATTS, a new and conserved DNA binding domain.
    Plant Cell. 1991 Aug;3(8):747-8 PMID: 1820817
  6. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5352-6 PMID: 8643578
  7. Combinatorial control required for the specificity of yeast MAPK signaling.
    Science. 1997 Feb 28;275(5304):1314-7 PMID: 9036858
  8. The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae.
    EMBO J. 1998 Aug 10;17(5):1236-47 PMID: 9482721
  9. Elements of the yeast pheromone response pathway required for filamentous growth of diploids.
    Science. 1993 Dec 10;262(5140):1741-4 PMID: 8259520
  10. Two nuclear mutations that block mitochondrial protein import in yeast.
    Proc Natl Acad Sci U S A. 1984 Aug;81(15):4819-23 PMID: 6235522
  11. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  12. Differential activation of yeast adenylyl cyclase by Ras1 and Ras2 depends on the conserved N terminus.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11009-13 PMID: 7479926
  13. An adenylate cyclase from Saccharomyces cerevisiae that is stimulated by RAS proteins with effector mutations.
    Mol Cell Biol. 1988 Jan;8(1):52-61 PMID: 3275878
  14. S. cerevisiae genes IRA1 and IRA2 encode proteins that may be functionally equivalent to mammalian ras GTPase activating protein.
    Cell. 1990 Mar 9;60(5):803-7 PMID: 2178777
  15. Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog.
    EMBO J. 1997 Dec 1;16(23):7008-18 PMID: 9384580
  16. GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p Galpha subunit and functions in a Ras-independent pathway.
    EMBO J. 1998 Apr 1;17(7):1996-2007 PMID: 9524122
  17. Genetic analysis of yeast RAS1 and RAS2 genes.
    Cell. 1984 Jun;37(2):437-45 PMID: 6327067
  18. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase.
    Cell. 1987 Jul 17;50(2):277-87 PMID: 3036373
  19. RAS genes in Saccharomyces cerevisiae: signal transduction in search of a pathway.
    Trends Genet. 1991 Jan;7(1):28-33 PMID: 1848378
  20. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle.
    Cell. 1991 May 31;65(5):875-83 PMID: 2040016
  21. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS.
    Cell. 1992 Mar 20;68(6):1077-90 PMID: 1547504
  22. SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription.
    Mol Cell Biol. 1995 Dec;15(12):6854-63 PMID: 8524252
  23. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth.
    Genes Dev. 1994 Dec 15;8(24):2974-85 PMID: 8001818
  24. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  25. Sequence-specific initiator elements focus initiation of transcription to distinct sites in the yeast TRP4 promoter.
    EMBO J. 1992 Dec;11(12):4583-90 PMID: 1425591
  26. Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast.
    Genetics. 1992 Nov;132(3):665-73 PMID: 1468625
  27. Ras-related proteins in signal transduction and growth control.
    Mol Reprod Dev. 1995 Dec;42(4):500-6 PMID: 8607982
  28. Differential structural requirements for interaction of Ras protein with its distinct downstream effectors.
    J Biol Chem. 1996 Mar 8;271(10):5353-60 PMID: 8621388
  29. MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation.
    Cell. 1997 Nov 28;91(5):673-84 PMID: 9393860
  30. The cellular content of Cdc25p, the Ras exchange factor in Saccharomyces cerevisiae, is regulated by destabilization through a cyclin destruction box.
    J Biol Chem. 1995 Sep 1;270(35):20742-7 PMID: 7657656
  31. The TEA domain: a novel, highly conserved DNA-binding motif.
    Cell. 1991 Jul 12;66(1):11-2 PMID: 2070413
  32. The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 Jan;9(1):161-71 PMID: 9436998
  33. Saccharomyces cerevisiae TEC1 is required for pseudohyphal growth.
    Mol Microbiol. 1996 Mar;19(6):1255-63 PMID: 8730867
  34. In vitro reconstitution of cdc25 regulated S. cerevisiae adenylyl cyclase and its kinetic properties.
    EMBO J. 1990 Mar;9(3):641-51 PMID: 2155776
  35. Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity.
    Mol Cell Biol. 1991 Jul;11(7):3537-44 PMID: 1904541
  36. TEC1, a gene involved in the activation of Ty1 and Ty1-mediated gene expression in Saccharomyces cerevisiae: cloning and molecular analysis.
    Mol Cell Biol. 1990 Jul;10(7):3541-50 PMID: 2192259
  37. Stimulation of membrane ruffling and MAP kinase activation by distinct effectors of RAS.
    Science. 1996 Feb 9;271(5250):810-2 PMID: 8628998
  38. The CDC25 protein of Saccharomyces cerevisiae promotes exchange of guanine nucleotides bound to ras.
    Mol Cell Biol. 1991 May;11(5):2641-6 PMID: 2017169
  39. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae.
    Mol Cell Biol. 1987 Apr;7(4):1371-7 PMID: 3037314
  40. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  41. The three yeast A kinases have specific signaling functions in pseudohyphal growth.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13783-7 PMID: 9811878
  42. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae.
    Genetics. 1997 Mar;145(3):671-84 PMID: 9055077
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1999-05-00
Pages
1325-35
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC25273
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com