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A dynamic partitioning mechanism polarizes membrane protein distribution

Author

Listed:
  • Tatsat Banerjee

    (Johns Hopkins University
    Johns Hopkins University)

  • Satomi Matsuoka

    (RIKEN Center for Biosystems Dynamics Research
    Osaka University)

  • Debojyoti Biswas

    (Johns Hopkins University)

  • Yuchuan Miao

    (Johns Hopkins University
    Johns Hopkins University)

  • Dhiman Sankar Pal

    (Johns Hopkins University)

  • Yoichiro Kamimura

    (RIKEN Center for Biosystems Dynamics Research)

  • Masahiro Ueda

    (RIKEN Center for Biosystems Dynamics Research
    Osaka University)

  • Peter N. Devreotes

    (Johns Hopkins University
    Johns Hopkins University)

  • Pablo A. Iglesias

    (Johns Hopkins University
    Johns Hopkins University)

Abstract

The plasma membrane is widely regarded as the hub of the numerous signal transduction activities. Yet, the fundamental biophysical mechanisms that spatiotemporally compartmentalize different classes of membrane proteins remain unclear. Using multimodal live-cell imaging, here we first show that several lipid-anchored membrane proteins are consistently depleted from the membrane regions where the Ras/PI3K/Akt/F-actin network is activated. The dynamic polarization of these proteins does not depend upon the F-actin-based cytoskeletal structures, recurring shuttling between membrane and cytosol, or directed vesicular trafficking. Photoconversion microscopy and single-molecule measurements demonstrate that these lipid-anchored molecules have substantially dissimilar diffusion profiles in different regions of the membrane which enable their selective segregation. When these diffusion coefficients are incorporated into an excitable network-based stochastic reaction-diffusion model, simulations reveal that the altered affinity mediated selective partitioning is sufficient to drive familiar propagating wave patterns. Furthermore, normally uniform integral and lipid-anchored membrane proteins partition successfully when membrane domain-specific peptides are optogenetically recruited to them. We propose “dynamic partitioning” as a new mechanism that can account for large-scale compartmentalization of a wide array of lipid-anchored and integral membrane proteins during various physiological processes where membrane polarizes.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43615-2
    DOI: 10.1038/s41467-023-43615-2
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    References listed on IDEAS

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