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Deterministic early endosomal maturations emerge from a stochastic trigger-and-convert mechanism

Author

Listed:
  • Harrison M. York

    (Monash University)

  • Kunaal Joshi

    (Purdue University)

  • Charles S. Wright

    (Purdue University)

  • Laura Z. Kreplin

    (Monash University)

  • Samuel J. Rodgers

    (Monash University)

  • Ullhas K. Moorthi

    (Monash University)

  • Hetvi Gandhi

    (Monash University)

  • Abhishek Patil

    (Monash University)

  • Christina A. Mitchell

    (Monash University)

  • Srividya Iyer-Biswas

    (Purdue University
    Santa Fe Institute)

  • Senthil Arumugam

    (Monash University
    Monash University
    Monash University
    University of New South Wales)

Abstract

Endosomal maturation is critical for robust and timely cargo transport to specific cellular compartments. The most prominent model of early endosomal maturation involves a phosphoinositide-driven gain or loss of specific proteins on individual endosomes, emphasising an autonomous and stochastic description. However, limitations in fast, volumetric imaging long hindered direct whole cell-level measurements of absolute numbers of maturation events. Here, we use lattice light-sheet imaging and bespoke automated analysis to track individual very early (APPL1-positive) and early (EEA1-positive) endosomes over the entire population, demonstrating that direct inter-endosomal contact drives maturation between these populations. Using fluorescence lifetime, we show that this endosomal interaction is underpinned by asymmetric binding of EEA1 to very early and early endosomes through its N- and C-termini, respectively. In combination with agent-based simulation which supports a ‘trigger-and-convert’ model, our findings indicate that APPL1- to EEA1-positive maturation is driven not by autonomous events but by heterotypic EEA1-mediated interactions, providing a mechanism for temporal and population-level control of maturation.

Suggested Citation

  • Harrison M. York & Kunaal Joshi & Charles S. Wright & Laura Z. Kreplin & Samuel J. Rodgers & Ullhas K. Moorthi & Hetvi Gandhi & Abhishek Patil & Christina A. Mitchell & Srividya Iyer-Biswas & Senthil , 2023. "Deterministic early endosomal maturations emerge from a stochastic trigger-and-convert mechanism," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40428-1
    DOI: 10.1038/s41467-023-40428-1
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    References listed on IDEAS

    as
    1. David H. Murray & Marcus Jahnel & Janelle Lauer & Mario J. Avellaneda & Nicolas Brouilly & Alice Cezanne & Hernán Morales-Navarrete & Enrico D. Perini & Charles Ferguson & Andrei N. Lupas & Yannis Kal, 2016. "An endosomal tether undergoes an entropic collapse to bring vesicles together," Nature, Nature, vol. 537(7618), pages 107-111, September.
    2. Samuel J. Rodgers & Lisa M. Ooms & Viola M. J. Oorschot & Ralf B. Schittenhelm & Elizabeth V. Nguyen & Sabryn A. Hamila & Natalie Rynkiewicz & Rajendra Gurung & Matthew J. Eramo & Absorn Sriratana & C, 2021. "INPP4B promotes PI3Kα-dependent late endosome formation and Wnt/β-catenin signaling in breast cancer," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Laura Picas & Julien Viaud & Kristine Schauer & Stefano Vanni & Karim Hnia & Vincent Fraisier & Aurélien Roux & Patricia Bassereau & Frédérique Gaits-Iacovoni & Bernard Payrastre & Jocelyn Laporte & J, 2014. "BIN1/M-Amphiphysin2 induces clustering of phosphoinositides to recruit its downstream partner dynamin," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
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