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Mutual inhibition between PTEN and PIP3 generates bistability for polarity in motile cells

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  • Satomi Matsuoka

    (Laboratory for Cell Signaling Dynamics, RIKEN QBiC
    Osaka University
    Laboratory for Cell Signaling Dynamics, RIKEN BDR)

  • Masahiro Ueda

    (Laboratory for Cell Signaling Dynamics, RIKEN QBiC
    Osaka University
    Osaka University
    Laboratory for Cell Signaling Dynamics, RIKEN BDR)

Abstract

Phosphatidylinositol 3,4,5-trisphosphate (PIP3) and PIP3 phosphatase (PTEN) are enriched mutually exclusively on the anterior and posterior membranes of eukaryotic motile cells. However, the mechanism that causes this spatial separation between the two molecules is unknown. Here we develop a method to manipulate PIP3 levels in living cells and used it to show PIP3 suppresses the membrane localization of PTEN. Single-molecule measurements of membrane-association and -dissociation kinetics and of lateral diffusion reveal that PIP3 suppresses the PTEN binding site required for stable PTEN membrane binding. Mutual inhibition between PIP3 and PTEN provides a mechanistic basis for bistability that creates a PIP3-enriched/PTEN-excluded state and a PTEN-enriched/PIP3-excluded state underlying the strict spatial separation between PIP3 and PTEN. The PTEN binding site also mediates the suppression of PTEN membrane localization in chemotactic signaling. These results illustrate that the PIP3-PTEN bistable system underlies a cell’s decision-making for directional movement irrespective of the environment.

Suggested Citation

  • Satomi Matsuoka & Masahiro Ueda, 2018. "Mutual inhibition between PTEN and PIP3 generates bistability for polarity in motile cells," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-06856-0
    DOI: 10.1038/s41467-018-06856-0
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    Cited by:

    1. Hyun Gyu Lee & Kyoung J Lee, 2021. "Neighbor-enhanced diffusivity in dense, cohesive cell populations," PLOS Computational Biology, Public Library of Science, vol. 17(9), pages 1-26, September.
    2. Tatsat Banerjee & Satomi Matsuoka & Debojyoti Biswas & Yuchuan Miao & Dhiman Sankar Pal & Yoichiro Kamimura & Masahiro Ueda & Peter N. Devreotes & Pablo A. Iglesias, 2023. "A dynamic partitioning mechanism polarizes membrane protein distribution," Nature Communications, Nature, vol. 14(1), pages 1-24, December.

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