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A tripartite organelle platform links growth factor receptor signaling to mitochondrial metabolism

Author

Listed:
  • Deborah Mesa

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Elisa Barbieri

    (European Institute of Oncology IRCCS)

  • Andrea Raimondi

    (IRCCS San Raffaele Hospital Scientific Institute
    Institute for Research in Biomedicine)

  • Stefano Freddi

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Giorgia Miloro

    (European Institute of Oncology IRCCS)

  • Gorana Jendrisek

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Giusi Caldieri

    (European Institute of Oncology IRCCS)

  • Micaela Quarto

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Irene Schiano Lomoriello

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Maria Grazia Malabarba

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Arianna Bresci

    (Politecnico di Milano)

  • Francesco Manetti

    (Politecnico di Milano)

  • Federico Vernuccio

    (Politecnico di Milano)

  • Hind Abdo

    (The AIRC Institute of Molecular Oncology)

  • Giorgio Scita

    (Università degli Studi di Milano
    The AIRC Institute of Molecular Oncology)

  • Letizia Lanzetti

    (University of Torino Medical School
    FPO-IRCCS)

  • Dario Polli

    (Politecnico di Milano
    CNR Institute for Photonics and Nanotechnology (CNR-IFN))

  • Carlo Tacchetti

    (IRCCS San Raffaele Hospital Scientific Institute
    Vita-Salute San Raffaele University)

  • Paolo Pinton

    (University of Ferrara)

  • Massimo Bonora

    (University of Ferrara)

  • Pier Paolo Di Fiore

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

  • Sara Sigismund

    (Università degli Studi di Milano
    European Institute of Oncology IRCCS)

Abstract

One open question in the biology of growth factor receptors is how a quantitative input (i.e., ligand concentration) is decoded by the cell to produce specific response(s). Here, we show that an EGFR endocytic mechanism, non-clathrin endocytosis (NCE), which is activated only at high ligand concentrations and targets receptor to degradation, requires a tripartite organelle platform involving the plasma membrane (PM), endoplasmic reticulum (ER) and mitochondria. At these contact sites, EGFR-dependent, ER-generated Ca2+ oscillations are sensed by mitochondria, leading to increased metabolism and ATP production. Locally released ATP is required for cortical actin remodeling and EGFR-NCE vesicle fission. The same biochemical circuitry is also needed for an effector function of EGFR, i.e., collective motility. The multiorganelle signaling platform herein described mediates direct communication between EGFR signaling and mitochondrial metabolism, and is predicted to have a broad impact on cell physiology as it is activated by another growth factor receptor, HGFR/MET.

Suggested Citation

  • Deborah Mesa & Elisa Barbieri & Andrea Raimondi & Stefano Freddi & Giorgia Miloro & Gorana Jendrisek & Giusi Caldieri & Micaela Quarto & Irene Schiano Lomoriello & Maria Grazia Malabarba & Arianna Bre, 2024. "A tripartite organelle platform links growth factor receptor signaling to mitochondrial metabolism," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49543-z
    DOI: 10.1038/s41467-024-49543-z
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    References listed on IDEAS

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