Artículo

Yu, R.C.; Pesce, C.G.; Colman-Lerner, A.; Lok, L.; Pincus, D.; Serra, E.; Holl, M.; Benjamin, K.; Gordon, A.; Brent, R. "Negative feedback that improves information transmission in yeast signalling" (2008) Nature. 456(7223):755-761
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Haploid Saccharomyces cerevisiae yeast cells use a prototypic cell signalling system to transmit information about the extracellular concentration of mating pheromone secreted by potential mating partners. The ability of cells to respond distinguishably to different pheromone concentrations depends on how much information about pheromone concentration the system can transmit. Here we show that the mitogen-activated protein kinase Fus3 mediates fast-acting negative feedback that adjusts the dose response of the downstream system response to match the dose response of receptor-ligand binding. This 'dose-response alignment', defined by a linear relationship between receptor occupancy and downstream response, can improve the fidelity of information transmission by making downstream responses corresponding to different receptor occupancies more distinguishable and reducing amplification of stochastic noise during signal transmission. We also show that one target of the feedback is a previously uncharacterized signal-promoting function of the regulator of G-protein signalling protein Sst2. Our work suggests that negative feedback is a general mechanism used in signalling systems to align dose responses and thereby increase the fidelity of information transmission. ©2008 Macmillan Publishers Limited. All rights reserved.

Registro:

Documento: Artículo
Título:Negative feedback that improves information transmission in yeast signalling
Autor:Yu, R.C.; Pesce, C.G.; Colman-Lerner, A.; Lok, L.; Pincus, D.; Serra, E.; Holl, M.; Benjamin, K.; Gordon, A.; Brent, R.
Filiación:Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, CA 94704, United States
Microscale Life Sciences Center, University of Washington, Seattle, WA 98195, United States
Instituto de Fisiología, Biología Molecular Y Neurociencias, CONICET, Universidad de Buenos Aires, Argentina
Synopsys, Mountain View, CA 94043, United States
Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, United States
Centre de Genètica Mèdica I Molecular, Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain
Biodesign Institute, Arizona State University, Tempe, AZ 85387, United States
Amyris Biotechnologies, Emeryville, CA 94608, United States
Physics Department, Brookhaven National Laboratory, Upton, NY 11973, United States
Palabras clave:g protein signalling protein sst2; membrane protein; mitogen activated protein kinase; mitogen activated protein kinase fus3; sex pheromone; unclassified drug; concentration (composition); dose-response relationship; enzyme activity; feedback mechanism; mating behavior; protein; sex pheromone; signaling; yeast; article; cell communication; cell function; dose response; downstream processing; hormone release; information dissemination; ligand binding; negative feedback; nonhuman; priority journal; receptor binding; Saccharomyces cerevisiae; signal transduction; yeast cell; Saccharomyces cerevisiae
Año:2008
Volumen:456
Número:7223
Página de inicio:755
Página de fin:761
DOI: http://dx.doi.org/10.1038/nature07513
Título revista:Nature
Título revista abreviado:Nature
ISSN:00280836
CODEN:NATUA
CAS:mitogen activated protein kinase, 142243-02-5
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00280836_v456_n7223_p755_Yu

Referencias:

  • Dohlman, H.G., Thorner, J.W., Regulation of G protein-initiated signal transduction in yeast: Paradigms and principles (2001) Annu. Rev. Biochem, 70, pp. 703-754
  • Jackson, C.L., Hartwell, L.H., Courtship in S. cerevisiae: Both cell types choose mating partners by responding to the strongest pheromone signal (1990) Cell, 63, pp. 1039-1051
  • Segall, J.E., Polarization of yeast cells in spatial gradients of alpha mating factor (1993) Proc. Natl Acad. Sci. USA, 90, pp. 8332-8336
  • Schrick, K., Garvik, B., Hartwell, L.H., Mating in Saccharomyces cerevisiae: The role of the pheromone signal transduction pathway in the chemotropic response to pheromone (1997) Genetics, 147, pp. 19-32
  • Colman-Lerner, A., Regulated cell-to-cell variation in a cell-fate decision system (2005) Nature, 437, pp. 699-706
  • Yi, T.M., Kitano, H., Simon, M.I., A quantitative characterization of the yeast heterotrimeric G protein cycle (2003) Proc. Natl Acad. Sci. USA, 100, pp. 10764-10769
  • Cuatrecasas, P., Insulin-receptor interactions in adipose tissue cells: Direct measurement and properties (1971) Proc. Natl Acad. Sci. USA, 68, pp. 1264-1268
  • Kasai, M., Changeux, J.P., In vitro excitation of purified membrane by cholinergic agonists (1971) J. Membr. Biol, 6, pp. 58-80
  • Amir, S.M., Carraway Jr, T.F., Kohn, L.D., Winand, R.J., The binding of thyrotropin to isolated bovine thyroid plasma membranes (1973) J. Biol. Chem, 248, pp. 4092-4100
  • Lin, S.Y., Goodfriend, T.L., Angiotensin receptors (1970) Am. J. Physiol, 218, pp. 1319-1328
  • Knauer, D.J., Wiley, H.S., Cunningham, D.D., Relationship between epidermal growth factor receptor occupancy and mitogenic response. Quantitative analysis using a steady state model system (1984) J. Biol. Chem, 259, pp. 5623-5631
  • Nagashima, T., Quantitative transcriptional control of Erbb receptor signaling undergoes graded to biphasic response for cell differentiation (2007) J. Biol. Chem, 282, pp. 4045-4056
  • Simons Jr, S.S., Oshima, H., Szapary, D., Higher levels of control: Modulation of steroid hormone-regulated gene transcription (1992) Mol. Endocrinol, 6, pp. 995-1002
  • Rousseau, G.G., Baxter, J.D., Glucocorticoid receptors (1979) Monogr. Endocrinol, 12, pp. 49-77
  • Bloom, E., Nuclear binding of glucocorticoid receptors: Relations between cytosol binding, activation and the biological response (1980) J. Steroid Biochem, 12, pp. 175-184
  • Pedraza, J.M., van Oudenaarden, A., Noise propagation in gene networks (2005) Science, 307, pp. 1965-1969
  • Black, H.S., Stabilized feed-back amplifiers (1934) Electr. Eng, 53, pp. 114-120
  • Bhalla, U.S., Ram, P.T., Iyengar, R., MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network (2002) Science, 297, pp. 1018-1023
  • Black, J.W., Leff, P., Operational models of pharmacological agonism (1983) Proc. R. Soc. Lond. B, 220, pp. 141-162
  • Savageau, M.A., Comparison of classical and autogenous systems of regulation in inducible operons (1974) Nature, 252, pp. 546-549
  • Becskei, A., Serrano, L., Engineering stability in gene networks by autoregulation (2000) Nature, 405, pp. 590-593
  • Barkai, N., Leibler, S., Robustness in simple biochemical networks (1997) Nature, 387, pp. 913-917
  • Gordon, A., Single-cell quantification of molecules and rates using open-source microscope-based cytometry (2007) Nature Methods, 4, pp. 175-181
  • Gartner, A., Nasmyth, K., Ammerer, G., Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of Fus3 and Kss1 (1992) Genes Dev, 6, pp. 1280-1292
  • Tedford, K., Kim, S., Sa, D., Stevens, K., Tyers, M., Regulation of the mating pheromone and invasive growth responses in yeast by two map kinase substrates (1997) Curr. Biol, 7, pp. 228-238
  • Miyawaki, A., Tsien, R.Y., Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein (2000) Methods Enzymol, 327, pp. 472-500
  • van Drogen, F., Stucke, V.M., Jorritsma, G., Peter, M., Map kinase dynamics in response to pheromones in budding yeast (2001) Nature Cell Biol, 3, pp. 1051-1059
  • Bhattacharyya, R.P., The ste5 scaffold allosterically modulates signaling output of the yeast mating pathway (2006) Science, 311, pp. 822-826
  • Maleri, S., Persistent activation by constitutive Ste7 promotes Kss1-mediated invasive growth but fails to support Fus3-dependent mating in yeast (2004) Mol. Cell. Biol, 24, pp. 9221-9238
  • Gruhler, A., Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway (2005) Mol. Cell. Proteomics, 4, pp. 310-327
  • Shao, D., Zheng, W., Qiu, W., Ouyang, Q., Tang, C., Dynamic studies of scaffold-dependent mating pathway in yeast (2006) Biophys. J, 91, pp. 3986-4001
  • Bishop, A.C., A chemical switch for inhibitor-sensitive alleles of any protein kinase (2000) Nature, 407, pp. 395-401
  • Ballon, D.R., DEP-domain-mediated regulation of GPCR signaling responses (2006) Cell, 126, pp. 1079-1093
  • Heximer, S.P., Blumer, K.J., RGS proteins: Swiss army knives in seven-transmembrane domain receptor signaling networks (2007) Sci. STKE, , pe2 2007
  • May, L.T., Leach, K., Sexton, P.M., Christopoulos, A., Allosteric modulation of G protein-coupled receptors (2007) Annu. Rev. Pharmacol. Toxicol, 47, pp. 1-51
  • Budas, G.R., Churchill, E.N., Mochly-Rosen, D., Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury (2007) Pharmacol. Res, 55, pp. 523-536
  • Lindsley, C.W., Barnett, S.F., Layton, M.E., Bilodeau, M.T., The PI3K/Akt pathway: Recent progress in the development of ATP-competitive and allosteric Akt kinase inhibitors (2008) Curr. Cancer Drug Targets, 8, pp. 7-18
  • Shannon, C., A mathematical theory of communication (1948) Bell Syst. Tech. J, 27, pp. 379-423
  • Bialek, W., Rieke, F., de Ruyter van Steveninck, R.R., Warland, D., Reading a neural code (1991) Science, 252, pp. 1854-1857
  • Tkacik, G., Callan, C., Bialek, W., Information flow and optimization in transcriptional regulation (2008) Proc. Natl. Acad. Sci. U.S.A, 26, pp. 12265-12270
  • Gregor, T., Tank, D.W., Wieschaus, E.F., Bialek, W., Probing the limits to positional information (2007) Cell, 130, pp. 153-164
  • Ausubel, F.M., (1987) Current Protocols in Molecular Biology, , John Wiley & Sons, Inc
  • Guthrie, C., Fink, G.R., (1991) Methods in Enzymology, Guide to Yeast Genetics and Molecular Biology, , Academic
  • Brun, R., Couet, O., Vandroni, C. & Zanarini, O. PAW Physics Analysis Workstation CERN program library entry q121 (CERN, Geneva, 1989); Jenness, D.D., Burkholder, A.C., Hartwell, L.H., Binding of alpha-factor pheromone to Saccharomyces cerevisiae a cells: Dissociation constant and number of binding sites (1986) Mol. Cell. Biol, 6, pp. 318-320
  • Bajaj, A., Afluorescent α-factor analogue exhibits multiple steps on binding to its g protein coupled receptor in yeast (2004) Biochemistry, 43, pp. 13564-13578
  • Andersson, J., Simpson, D.M., Qi, M., Wang, Y., Elion, E.A., Differential input by Ste5 scaffold and Msg5 phosphatase route a MAPK cascade to multiple outcomes (2004) EMBO J, 23, pp. 2564-2576

Citas:

---------- APA ----------
Yu, R.C., Pesce, C.G., Colman-Lerner, A., Lok, L., Pincus, D., Serra, E., Holl, M.,..., Brent, R. (2008) . Negative feedback that improves information transmission in yeast signalling. Nature, 456(7223), 755-761.
http://dx.doi.org/10.1038/nature07513
---------- CHICAGO ----------
Yu, R.C., Pesce, C.G., Colman-Lerner, A., Lok, L., Pincus, D., Serra, E., et al. "Negative feedback that improves information transmission in yeast signalling" . Nature 456, no. 7223 (2008) : 755-761.
http://dx.doi.org/10.1038/nature07513
---------- MLA ----------
Yu, R.C., Pesce, C.G., Colman-Lerner, A., Lok, L., Pincus, D., Serra, E., et al. "Negative feedback that improves information transmission in yeast signalling" . Nature, vol. 456, no. 7223, 2008, pp. 755-761.
http://dx.doi.org/10.1038/nature07513
---------- VANCOUVER ----------
Yu, R.C., Pesce, C.G., Colman-Lerner, A., Lok, L., Pincus, D., Serra, E., et al. Negative feedback that improves information transmission in yeast signalling. Nature. 2008;456(7223):755-761.
http://dx.doi.org/10.1038/nature07513