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MFF-dependent mitochondrial fission regulates presynaptic release and axon branching by limiting axonal mitochondria size

Author

Listed:
  • Tommy L. Lewis

    (Columbia University
    Mortimer B. Zuckerman Mind Brain Behavior Institute
    Oklahoma Medical Research Foundation)

  • Seok-Kyu Kwon

    (Columbia University
    Mortimer B. Zuckerman Mind Brain Behavior Institute
    Brain Science Institute, Korea Institute of Science and Technology)

  • Annie Lee

    (Columbia University
    Mortimer B. Zuckerman Mind Brain Behavior Institute)

  • Reuben Shaw

    (Salk Institute for Biological Studies)

  • Franck Polleux

    (Columbia University
    Mortimer B. Zuckerman Mind Brain Behavior Institute
    Kavli Institute for Brain Science at Columbia University)

Abstract

Neurons display extreme degrees of polarization, including compartment-specific organelle morphology. In cortical, long-range projecting, pyramidal neurons (PNs), dendritic mitochondria are long and tubular whereas axonal mitochondria display uniformly short length. Here we explored the functional significance of maintaining small mitochondria for axonal development in vitro and in vivo. We report that the Drp1 ‘receptor’ Mitochondrial fission factor (MFF) is required for determining the size of mitochondria entering the axon and then for maintenance of their size along the distal portions of the axon without affecting their trafficking properties, presynaptic capture, membrane potential or ability to generate ATP. Strikingly, this increase in presynaptic mitochondrial size upon MFF downregulation augments their capacity for Ca2+ ([Ca2+]m) uptake during neurotransmission, leading to reduced presynaptic [Ca2+]c accumulation, decreased presynaptic release and terminal axon branching. Our results uncover a novel mechanism controlling neurotransmitter release and axon branching through fission-dependent regulation of presynaptic mitochondrial size.

Suggested Citation

  • Tommy L. Lewis & Seok-Kyu Kwon & Annie Lee & Reuben Shaw & Franck Polleux, 2018. "MFF-dependent mitochondrial fission regulates presynaptic release and axon branching by limiting axonal mitochondria size," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-07416-2
    DOI: 10.1038/s41467-018-07416-2
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    Cited by:

    1. Andrea Irazoki & Isabel Gordaliza-Alaguero & Emma Frank & Nikolaos Nikiforos Giakoumakis & Jordi Seco & Manuel Palacín & Anna Gumà & Lykke Sylow & David Sebastián & Antonio Zorzano, 2023. "Disruption of mitochondrial dynamics triggers muscle inflammation through interorganellar contacts and mitochondrial DNA mislocation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Marine Lanfranchi & Sozerko Yandiev & Géraldine Meyer-Dilhet & Salma Ellouze & Martijn Kerkhofs & Raphael Dos Reis & Audrey Garcia & Camille Blondet & Alizée Amar & Anita Kneppers & Hélène Polvèche & , 2024. "The AMPK-related kinase NUAK1 controls cortical axons branching by locally modulating mitochondrial metabolic functions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Koen Kole & Bas J. B. Voesenek & Maria E. Brinia & Naomi Petersen & Maarten H. P. Kole, 2022. "Parvalbumin basket cell myelination accumulates axonal mitochondria to internodes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Daniel M. Virga & Stevie Hamilton & Bertha Osei & Abigail Morgan & Parker Kneis & Emiliano Zamponi & Natalie J. Park & Victoria L. Hewitt & David Zhang & Kevin C. Gonzalez & Fiona M. Russell & D. Grah, 2024. "Activity-dependent compartmentalization of dendritic mitochondria morphology through local regulation of fusion-fission balance in neurons in vivo," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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