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Oligodendroglia metabolically support axons and contribute to neurodegeneration

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  • Youngjin Lee

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Brett M. Morrison

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Yun Li

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Sylvain Lengacher

    (School of Life Sciences, Brain Mind Institute, Ecole Polytechnique Federale de Lausanne (EPFL), Station 19, CH-1015 Lausanne, Switzerland)

  • Mohamed H. Farah

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Paul N. Hoffman

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Yiting Liu

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Akivaga Tsingalia

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Lin Jin

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Ping-Wu Zhang

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA)

  • Luc Pellerin

    (University of Lausanne, 7 Rue du Bugnon, CH-1005 Lausanne, Switzerland)

  • Pierre J. Magistretti

    (School of Life Sciences, Brain Mind Institute, Ecole Polytechnique Federale de Lausanne (EPFL), Station 19, CH-1015 Lausanne, Switzerland)

  • Jeffrey D. Rothstein

    (The Johns Hopkins University, 855 North Wolfe Street, Rangos 248, Baltimore, Maryland 21205, USA
    The Johns Hopkins University, 855 North Wolfe Street, Rangos 270, Baltimore, Maryland 21205, USA
    The Brain Science Institute, The Johns Hopkins University, 855 North Wolfe Street, Rangos 270, Baltimore, Maryland 21205, USA)

Abstract

Oligodendroglia support axon survival and function through mechanisms independent of myelination, and their dysfunction leads to axon degeneration in several diseases. The cause of this degeneration has not been determined, but lack of energy metabolites such as glucose or lactate has been proposed. Lactate is transported exclusively by monocarboxylate transporters, and changes to these transporters alter lactate production and use. Here we show that the most abundant lactate transporter in the central nervous system, monocarboxylate transporter 1 (MCT1, also known as SLC16A1), is highly enriched within oligodendroglia and that disruption of this transporter produces axon damage and neuron loss in animal and cell culture models. In addition, this same transporter is reduced in patients with, and in mouse models of, amyotrophic lateral sclerosis, suggesting a role for oligodendroglial MCT1 in pathogenesis. The role of oligodendroglia in axon function and neuron survival has been elusive; this study defines a new fundamental mechanism by which oligodendroglia support neurons and axons.

Suggested Citation

  • Youngjin Lee & Brett M. Morrison & Yun Li & Sylvain Lengacher & Mohamed H. Farah & Paul N. Hoffman & Yiting Liu & Akivaga Tsingalia & Lin Jin & Ping-Wu Zhang & Luc Pellerin & Pierre J. Magistretti & J, 2012. "Oligodendroglia metabolically support axons and contribute to neurodegeneration," Nature, Nature, vol. 487(7408), pages 443-448, July.
    • Handle: RePEc:nat:nature:v:487:y:2012:i:7408:d:10.1038_nature11314
    DOI: 10.1038/nature11314
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    Cited by:

    1. Ellen McMullen & Helen Hertenstein & Katrin Strassburger & Leon Deharde & Marko Brankatschk & Stefanie Schirmeier, 2023. "Glycolytically impaired Drosophila glial cells fuel neural metabolism via β-oxidation," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    2. Shan Yao & Min-Dong Xu & Ying Wang & Shen-Ting Zhao & Jin Wang & Gui-Fu Chen & Wen-Bing Chen & Jian Liu & Guo-Bin Huang & Wen-Juan Sun & Yan-Yan Zhang & Huan-Li Hou & Lei Li & Xiang-Dong Sun, 2023. "Astrocytic lactate dehydrogenase A regulates neuronal excitability and depressive-like behaviors through lactate homeostasis in mice," Nature Communications, Nature, vol. 14(1), pages 1-18, 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.

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