Abstract
Cell differentiation requires the ability to detect and respond appropriately to a variety of extracellular signals. Here we investigate a differentiation switch induced by changes in the concentration of a single stimulus. Yeast cells exposed to high doses of mating pheromone undergo cell division arrest. Cells at intermediate doses become elongated and divide in the direction of a pheromone gradient (chemotropic growth). Either of the pheromone-responsive MAP kinases, Fus3 and Kss1, promotes cell elongation, but only Fus3 promotes chemotropic growth. Whereas Kss1 is activated rapidly and with a graded dose-response profile, Fus3 is activated slowly and exhibits a steeper dose-response relationship (ultrasensitivity). Fus3 activity requires the scaffold protein Ste5; when binding to Ste5 is abrogated, Fus3 behaves like Kss1, and the cells no longer respond to a gradient or mate efficiently with distant partners. We propose that scaffold proteins serve to modulate the temporal and dose-response behavior of the MAP kinase.
MeSH Terms
Adaptor Proteins, Signal Transducing/metabolism
Cell Differentiation/drug effects
Enzyme Activation
MAP Kinase Signaling System
Mitogen-Activated Protein Kinases/metabolism
Pheromones/pharmacology
Saccharomyces cerevisiae/cytology,drug effects,enzymology,growth & development
Saccharomyces cerevisiae Proteins/metabolism
Chemicals
Adaptor Proteins, Signal Transducing
Pheromones
STE5 protein, S cerevisiae
Saccharomyces cerevisiae Proteins
FUS3 protein, S cerevisiae
KSS1 protein, S cerevisiae
Mitogen-Activated Protein Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Hao Nan
Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
Nayak Sujata
Behar Marcelo
Shanks Ryan H
Nagiec Michal J
Errede Beverly
Hasty Jeffrey
Elston Timothy C
Dohlman Henrik G
References (31)
31 references, click to expand
-
A GTP-exchange factor required for cell orientation.
Nature. 1998 Jan 8;391(6663):195-8
PMID: 9428768
-
Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway.
Nature. 1997 Nov 6;390(6655):85-8
PMID: 9363895
-
Protein-protein interactions in the yeast pheromone response pathway: Ste5p interacts with all members of the MAP kinase cascade.
Genetics. 1994 Nov;138(3):609-19
PMID: 7851759
-
Amplification and adaptation in regulatory and sensory systems.
Science. 1982 Jul 16;217(4556):220-5
PMID: 7089556
-
Pheromone signaling mechanisms in yeast: a prototypical sex machine.
Science. 2004 Nov 26;306(5701):1508-9
PMID: 15567849
-
The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway.
Science. 2006 Feb 10;311(5762):822-6
PMID: 16424299
-
Graded mode of transcriptional induction in yeast pheromone signalling revealed by single-cell analysis.
Yeast. 2001 Oct;18(14):1331-8
PMID: 11571757
-
Saccharomyces cerevisiae cells execute a default pathway to select a mate in the absence of pheromone gradients.
J Cell Biol. 1995 Nov;131(4):845-61
PMID: 7490289
-
MAPK-mediated bimodal gene expression and adaptive gradient sensing in yeast.
Nature. 2007 Mar 1;446(7131):46-51
PMID: 17310144
-
A conserved protein interaction network involving the yeast MAP kinases Fus3 and Kss1.
J Cell Biol. 2004 Jan 19;164(2):267-77
PMID: 14734536
-
Mitogen-activated protein kinases with distinct requirements for Ste5 scaffolding influence signaling specificity in Saccharomyces cerevisiae.
Mol Cell Biol. 2005 Mar;25(5):1793-803
PMID: 15713635
-
Combinatorial control required for the specificity of yeast MAPK signaling.
Science. 1997 Feb 28;275(5304):1314-7
PMID: 9036858
-
Spatial regulation of Fus3 MAP kinase activity through a reaction-diffusion mechanism in yeast pheromone signalling.
Nat Cell Biol. 2007 Nov;9(11):1319-26
PMID: 17952059
-
Mutational analysis suggests that activation of the yeast pheromone response mitogen-activated protein kinase pathway involves conformational changes in the Ste5 scaffold protein.
Mol Biol Cell. 2000 Nov;11(11):4033-49
PMID: 11071925
-
Distinct roles for two Galpha-Gbeta interfaces in cell polarity control by a yeast heterotrimeric G protein.
Mol Biol Cell. 2008 Jan;19(1):181-97
PMID: 17978098
-
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
-
Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles.
Science. 2000 Feb 4;287(5454):873-80
PMID: 10657304
-
Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 and KSS1.
Genes Dev. 1992 Jul;6(7):1280-92
PMID: 1628831
-
Persistent activation by constitutive Ste7 promotes Kss1-mediated invasive growth but fails to support Fus3-dependent mating in yeast.
Mol Cell Biol. 2004 Oct;24(20):9221-38
PMID: 15456892
-
MAPK specificity in the yeast pheromone response independent of transcriptional activation.
Curr Biol. 2001 Aug 21;11(16):1266-71
PMID: 11525741
-
A filamentous growth response mediated by the yeast mating pathway.
Genetics. 2001 Nov;159(3):919-28
PMID: 11729141
-
Specification of sites for polarized growth in Saccharomyces cerevisiae and the influence of external factors on site selection.
Mol Biol Cell. 1992 Sep;3(9):1025-35
PMID: 1421575
-
Differential input by Ste5 scaffold and Msg5 phosphatase route a MAPK cascade to multiple outcomes.
EMBO J. 2004 Jul 7;23(13):2564-76
PMID: 15192700
-
Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation.
Mol Cell. 2001 Sep;8(3):683-91
PMID: 11583629
-
Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae.
Cell. 1994 Aug 12;78(3):499-512
PMID: 8062390
-
FAR1 is required for oriented polarization of yeast cells in response to mating pheromones.
J Cell Biol. 1995 Nov;131(4):863-73
PMID: 7490290
-
An amplified sensitivity arising from covalent modification in biological systems.
Proc Natl Acad Sci U S A. 1981 Nov;78(11):6840-4
PMID: 6947258
-
Polarization of yeast cells in spatial gradients of alpha mating factor.
Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8332-6
PMID: 8397402
-
Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation.
Cell. 1995 Jan 27;80(2):179-85
PMID: 7834738
-
Elements of the yeast pheromone response pathway required for filamentous growth of diploids.
Science. 1993 Dec 10;262(5140):1741-4
PMID: 8259520
-
The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes.
Science. 1998 May 8;280(5365):895-8
PMID: 9572732