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Articles, Cellular/Molecular

Regulation of Oligodendrocyte Development and Myelination by Glucose and Lactate

Johanne E. Rinholm, Nicola B. Hamilton, Nicoletta Kessaris, William D. Richardson, Linda H. Bergersen and David Attwell
Journal of Neuroscience 12 January 2011, 31 (2) 538-548; DOI: https://doi.org/10.1523/JNEUROSCI.3516-10.2011
Johanne E. Rinholm
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Nicola B. Hamilton
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Nicoletta Kessaris
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William D. Richardson
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Linda H. Bergersen
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David Attwell
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Abstract

In the gray matter of the brain, astrocytes have been suggested to export lactate (derived from glucose or glycogen) to neurons to power their mitochondria. In the white matter, lactate can support axon function in conditions of energy deprivation, but it is not known whether lactate acts by preserving energy levels in axons or in oligodendrocytes, the myelinating processes of which are damaged rapidly in low energy conditions. Studies of cultured cells suggest that oligodendrocytes are the cell type in the brain that consumes lactate at the highest rate, in part to produce membrane lipids presumably for myelin. Here, we use pH imaging to show that oligodendrocytes in the white matter of the rat cerebellum and corpus callosum take up lactate via monocarboxylate transporters (MCTs), which we identify as MCT1 by confocal immunofluorescence and electron microscopy. Using cultured slices of developing cerebral cortex from mice in which oligodendrocyte lineage cells express GFP (green fluorescent protein) under the control of the Sox10 promoter, we show that a low glucose concentration reduces the number of oligodendrocyte lineage cells and myelination. Myelination is rescued when exogenous l-lactate is supplied. Thus, lactate can support oligodendrocyte development and myelination. In CNS diseases involving energy deprivation at times of myelination or remyelination, such as periventricular leukomalacia leading to cerebral palsy, stroke, and secondary ischemia after spinal cord injury, lactate transporters in oligodendrocytes may play an important role in minimizing the inhibition of myelination that occurs.

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The Journal of Neuroscience: 31 (2)
Journal of Neuroscience
Vol. 31, Issue 2
12 Jan 2011
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Regulation of Oligodendrocyte Development and Myelination by Glucose and Lactate
Johanne E. Rinholm, Nicola B. Hamilton, Nicoletta Kessaris, William D. Richardson, Linda H. Bergersen, David Attwell
Journal of Neuroscience 12 January 2011, 31 (2) 538-548; DOI: 10.1523/JNEUROSCI.3516-10.2011

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Regulation of Oligodendrocyte Development and Myelination by Glucose and Lactate
Johanne E. Rinholm, Nicola B. Hamilton, Nicoletta Kessaris, William D. Richardson, Linda H. Bergersen, David Attwell
Journal of Neuroscience 12 January 2011, 31 (2) 538-548; DOI: 10.1523/JNEUROSCI.3516-10.2011
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  • Roles of lactate in glial energy metabolism
    Heikki Savolainen
    Published on: 13 January 2011
  • Published on: (13 January 2011)
    Page navigation anchor for Roles of lactate in glial energy metabolism
    Roles of lactate in glial energy metabolism
    • Heikki Savolainen, Professor

    This convincing investigation on the role of L-lactate as an energy scource in glia may have important implications. The monocarboxylate transporter is not highly specific for L-lactate: it also transports D-lactate, which cannot be metabolized to pyruvate by the same dehydrogenase, into cells.

    D-lactate accumulates in diabetes and in propylene glycol intoxication (Talasniemi et al. 2008) and it is only metaboli...

    Show More

    This convincing investigation on the role of L-lactate as an energy scource in glia may have important implications. The monocarboxylate transporter is not highly specific for L-lactate: it also transports D-lactate, which cannot be metabolized to pyruvate by the same dehydrogenase, into cells.

    D-lactate accumulates in diabetes and in propylene glycol intoxication (Talasniemi et al. 2008) and it is only metabolized by high Km mitochondrial D- lactate oxidase. Blood D-lactate levels above 3 mM are associated with encephalopathy. Therefore, it is tempting to speculate that D-lactate from excessive methylglyoxal in diabetes could contribute to neural complications of the disease.

    Another element is that the myelination and myelin maturation in man extends well in the late teens (Savolainen and Palo, 1972) which places the young sufferers of diabetes at a special risk.

    References

    Savolainen H, Palo J. Proteins of human glial cell membrane. FEBS Lett 1972; 20: 71-74

    Talasniemi JP, Pennanen S, Savolainen H, et al. Assay of D-lactate in diabetic plasma and urine. Clin Biochem 2008; 41: 1099-1103

    Show Less
    Competing Interests: None declared.

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