IDEAS home Printed from https://ideas.repec.org/a/nat/nature/v456y2008i7223d10.1038_nature07513.html
   My bibliography  Save this article

Negative feedback that improves information transmission in yeast signalling

Author

Listed:
  • Richard C. Yu

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA)

  • C. Gustavo Pesce

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA)

  • Alejandro Colman-Lerner

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • Larry Lok

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • David Pincus

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • Eduard Serra

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • Mark Holl

    (Microscale Life Sciences Center, University of Washington, Seattle, Washington 98195, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • Kirsten Benjamin

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • Andrew Gordon

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA
    Present addresses: Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina (A.C.-L.); Synopsys, Mountain View, California 94043, USA (L.L.); Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California 94158, USA (D.P.); Centre de Genètica Mèdica i Molecular, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona 08907, Spain (E.S.); Biodesign Institute, Arizona State University, Tempe, Arizona 85387, USA (M.H.); Amyris Biotechnologies, Emeryville, California 94608, USA (K.B.); Physics Department, Brookhaven National Laboratory, Upton, New York 11973, USA (A.G.).)

  • Roger Brent

    (Molecular Sciences Institute, 2168 Shattuck Avenue, Berkeley, California 94704, USA)

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.

Suggested Citation

  • Richard C. Yu & C. Gustavo Pesce & Alejandro Colman-Lerner & Larry Lok & David Pincus & Eduard Serra & Mark Holl & Kirsten Benjamin & Andrew Gordon & Roger Brent, 2008. "Negative feedback that improves information transmission in yeast signalling," Nature, Nature, vol. 456(7223), pages 755-761, December.
    • Handle: RePEc:nat:nature:v:456:y:2008:i:7223:d:10.1038_nature07513
    DOI: 10.1038/nature07513
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/nature07513
    File Function: Abstract
    Download Restriction: Access to the full text of the articles in this series is restricted.
    File URL: https://libkey.io/10.1038/nature07513?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    As the access to this document is restricted, you may want to search for a different version of it.

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Gabriele Micali & Gerardo Aquino & David M Richards & Robert G Endres, 2015. "Accurate Encoding and Decoding by Single Cells: Amplitude Versus Frequency Modulation," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-21, June.
    2. Sara Hooshangi & William E Bentley, 2011. "LsrR Quorum Sensing “Switch” Is Revealed by a Bottom-Up Approach," PLOS Computational Biology, Public Library of Science, vol. 7(9), pages 1-11, September.
    3. Michael Chevalier & Ophelia Venturelli & Hana El-Samad, 2015. "The Impact of Different Sources of Fluctuations on Mutual Information in Biochemical Networks," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-21, October.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:nature:v:456:y:2008:i:7223:d:10.1038_nature07513. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    We have no bibliographic references for this item. You can help adding them by using this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.