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Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops

Author

Listed:
  • Tina Freisinger

    (Max-Planck-Institute of Biochemistry, Cellular Dynamics and Cell Patterning)

  • Ben Klünder

    (Arnold Sommerfeld Center for Theoretical Physics, and Centre for Nanoscience)

  • Jared Johnson

    (Baker Laboratory, Cornell University)

  • Nikola Müller

    (Max-Planck-Institute of Biochemistry, Cellular Dynamics and Cell Patterning)

  • Garwin Pichler

    (Max-Planck-Institute of Biochemistry, Cellular Dynamics and Cell Patterning
    Present address: Department of Biology II and Center for Integrated Protein Science Munich (CIPSM), Ludwig Maximilians University Munich, Großhaderner Street 2, 82152 Martinsried, Germany)

  • Gisela Beck

    (Max-Planck-Institute of Biochemistry, Cellular Dynamics and Cell Patterning)

  • Michael Costanzo

    (Terrence Donnelly Centre for Cellular and Biomolecular Research, University of Toronto)

  • Charles Boone

    (Terrence Donnelly Centre for Cellular and Biomolecular Research, University of Toronto)

  • Richard A. Cerione

    (Baker Laboratory, Cornell University)

  • Erwin Frey

    (Arnold Sommerfeld Center for Theoretical Physics, and Centre for Nanoscience)

  • Roland Wedlich-Söldner

    (Max-Planck-Institute of Biochemistry, Cellular Dynamics and Cell Patterning)

Abstract

Establishment of cell polarity—or symmetry breaking—relies on local accumulation of polarity regulators. Although simple positive feedback is sufficient to drive symmetry breaking, it is highly sensitive to stochastic fluctuations typical for living cells. Here, by integrating mathematical modelling with quantitative experimental validations, we show that in the yeast Saccharomyces cerevisiae a combination of actin- and guanine nucleotide dissociation inhibitor-dependent recycling of the central polarity regulator Cdc42 is needed to establish robust cell polarity at a single site during yeast budding. The guanine nucleotide dissociation inhibitor pathway consistently generates a single-polarization site, but requires Cdc42 to cycle rapidly between its active and inactive form, and is therefore sensitive to perturbations of the GTPase cycle. Conversely, actin-mediated recycling of Cdc42 induces robust symmetry breaking but cannot restrict polarization to a single site. Our results demonstrate how cells optimize symmetry breaking through coupling between multiple feedback loops.

Suggested Citation

  • Tina Freisinger & Ben Klünder & Jared Johnson & Nikola Müller & Garwin Pichler & Gisela Beck & Michael Costanzo & Charles Boone & Richard A. Cerione & Erwin Frey & Roland Wedlich-Söldner, 2013. "Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops," Nature Communications, Nature, vol. 4(1), pages 1-11, June.
    • Handle: RePEc:nat:natcom:v:4:y:2013:i:1:d:10.1038_ncomms2795
    DOI: 10.1038/ncomms2795
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    Cited by:

    1. David M. Rutkowski & Vincent Vincenzetti & Dimitrios Vavylonis & Sophie G. Martin, 2024. "Cdc42 mobility and membrane flows regulate fission yeast cell shape and survival," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Fridtjof Brauns & Leila Iñigo de la Cruz & Werner K.-G. Daalman & Ilse Bruin & Jacob Halatek & Liedewij Laan & Erwin Frey, 2023. "Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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