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Cited by 40Neuroscience and Neuropharmacology ResearchIon Transport and Channel RegulationIon channel regulation and function

The Na(+)/K(+) pump dominates control of glycolysis in hippocampal dentate granule cells

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Meyer, Dylan J, Díaz-García, Carlos Manlio, Nathwani, Nidhi, Rahman, Mahia, Yellen, Gary·2022·eLife
DOI 10.7554/elife.81645PMC PMC9592084

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Abstract

Cellular ATP that is consumed to perform energetically expensive tasks must be replenished by new ATP through the activation of metabolism. Neuronal stimulation, an energetically demanding process, transiently activates aerobic glycolysis, but the precise mechanism underlying this glycolysis activation has not been determined. We previously showed that neuronal glycolysis is correlated with Ca 2+ influx, but is not activated by feedforward Ca 2+ signaling (Díaz-García et al., 2021a). Since ATP-powered Na + and Ca 2+ pumping activities are increased following stimulation to restore ion gradients and are estimated to consume most neuronal ATP, we aimed to determine if they are coupled to neuronal glycolysis activation. By using two-photon imaging of fluorescent biosensors and dyes in dentate granule cell somas of acute mouse hippocampal slices, we observed that production of cytoplasmic NADH, a byproduct of glycolysis, is strongly coupled to changes in intracellular Na + , while intracellular Ca 2+ could only increase NADH production if both forward Na + /Ca 2+ exchange and Na + /K + pump activity were intact. Additionally, antidromic stimulation-induced intracellular [Na + ] increases were reduced >50% by blocking Ca 2+ entry. These results indicate that neuronal glycolysis activation is predominantly a response to an increase in activity of the Na + /K + pump, which is strongly potentiated by Na + influx through the Na + /Ca 2+ exchanger during extrusion of Ca 2+ following stimulation.

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  • APOE4-induced decline in ATP production and Na+/K+-ATPase α1 expression will collectively reduce the activity of Na+/K+-ATPase critical for maintaining RMP and neuronal excitability especially during energetically demanding processes such as seizures.

    “In addition, APOE4-induced decline in ATP production (Fig. 4C, J) and Na+/K+-ATPase α1 expression (Fig. 3A-E) will collectively reduce the activity of Na+/K+-ATPase critical for maintaining RMP and neuronal excitability (Fig. 3F-J) (Sun et al., 2022; Zhang et al., 2022) especially during energetically demanding processes such as seizures (Meyer et al., 2022) (Fig. 6).”

    From APOE4 reduces hippocampal expression of phosphoglycerate kinase 1 and sodium potassium pump to enhance seizure susceptibility in mice (2026) · cites this paper as Meyer et al., 2022

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Cited by

Sorted by citations

Authors
Meyer, D. J., Díaz-García, C. M., Nathwani, N., Rahman, M., & Yellen, G.
Affiliations
  • Harvard University (US)
  • Department of Neurobiology, Harvard Medical School
Corresponding author
Yellen, Gary
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2022-10-12
Volume
11
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.81645
PMC
PMC9592084
OpenAlex
W4304692485
Cited by
40
References
9
Citations by year
2026: 10 · 2025: 13 · 2024: 10 · 2023: 7
FWCI
3.33
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institute of Neurological Disorders and Stroke (R01 NS102586, F32 NS116105, F32 NS100331)
  • National Institute of General Medical Sciences (R01 GM124038)
  • Harvard Mahoney Neuroscience Institute (Postdoctoral Fellowship)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Keywords
Na+/K+-ATPase, aerobic glycolysis, dentate gyrus granule cells, hippocampus, intracellular sodium, NADH, Na+/Ca2+ exchanger, calcium influx, ATP consumption, neuronal energy metabolism, antidromic stimulation, two-photon imaging
MeSH terms
Adenosine Triphosphate, Animals, Calcium, Coloring Agents, Glycolysis, Hippocampus, NAD, Sodium, Sodium-Calcium Exchanger, Mice

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