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Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division

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  • Joon Ho Kang

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Brain Science Institute, Korea Institute of Science and Technology)

  • Georgios Katsikis

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Zhaoqi Li

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Kiera M. Sapp

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Max A. Stockslager

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Daniel Lim

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Matthew G. Heiden

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Dana-Farber Cancer Institute)

  • Michael B. Yaffe

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Scott R. Manalis

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Teemu P. Miettinen

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Medical Research Council Laboratory for Molecular Cell Biology, University College London)

Abstract

The energetic demands of a cell are believed to increase during mitosis, but the rates of ATP synthesis and consumption during mitosis have not been quantified. Here, we monitor mitochondrial membrane potential of single lymphocytic leukemia cells and demonstrate that mitochondria hyperpolarize from the G2/M transition until the metaphase-anaphase transition. This hyperpolarization was dependent on cyclin-dependent kinase 1 (CDK1) activity. By using an electrical circuit model of mitochondria, we quantify mitochondrial ATP synthesis rates in mitosis from the single-cell time-dynamics of mitochondrial membrane potential. We find that mitochondrial ATP synthesis decreases by approximately 50% during early mitosis and increases back to G2 levels during cytokinesis. Consistently, ATP levels and ATP synthesis are lower in mitosis than in G2 in synchronized cell populations. Overall, our results provide insights into mitotic bioenergetics and suggest that cell division is not a highly energy demanding process.

Suggested Citation

  • Joon Ho Kang & Georgios Katsikis & Zhaoqi Li & Kiera M. Sapp & Max A. Stockslager & Daniel Lim & Matthew G. Heiden & Michael B. Yaffe & Scott R. Manalis & Teemu P. Miettinen, 2020. "Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18769-y
    DOI: 10.1038/s41467-020-18769-y
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