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

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...

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Autores principales: Kang, Joon Ho, Katsikis, Georgios, Li, Zhaoqi, Sapp, Kiera M., Stockslager, Max A., Lim, Daniel, Vander Heiden, Matthew G., Yaffe, Michael B., Manalis, Scott R., Miettinen, Teemu P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536222/
https://www.ncbi.nlm.nih.gov/pubmed/33020492
http://dx.doi.org/10.1038/s41467-020-18769-y
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author Kang, Joon Ho
Katsikis, Georgios
Li, Zhaoqi
Sapp, Kiera M.
Stockslager, Max A.
Lim, Daniel
Vander Heiden, Matthew G.
Yaffe, Michael B.
Manalis, Scott R.
Miettinen, Teemu P.
author_facet Kang, Joon Ho
Katsikis, Georgios
Li, Zhaoqi
Sapp, Kiera M.
Stockslager, Max A.
Lim, Daniel
Vander Heiden, Matthew G.
Yaffe, Michael B.
Manalis, Scott R.
Miettinen, Teemu P.
author_sort Kang, Joon Ho
collection PubMed
description 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.
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spelling pubmed-75362222020-10-19 Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division Kang, Joon Ho Katsikis, Georgios Li, Zhaoqi Sapp, Kiera M. Stockslager, Max A. Lim, Daniel Vander Heiden, Matthew G. Yaffe, Michael B. Manalis, Scott R. Miettinen, Teemu P. Nat Commun Article 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. Nature Publishing Group UK 2020-10-05 /pmc/articles/PMC7536222/ /pubmed/33020492 http://dx.doi.org/10.1038/s41467-020-18769-y Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Kang, Joon Ho
Katsikis, Georgios
Li, Zhaoqi
Sapp, Kiera M.
Stockslager, Max A.
Lim, Daniel
Vander Heiden, Matthew G.
Yaffe, Michael B.
Manalis, Scott R.
Miettinen, Teemu P.
Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division
title Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division
title_full Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division
title_fullStr Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division
title_full_unstemmed Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division
title_short Monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased ATP synthesis during cell division
title_sort monitoring and modeling of lymphocytic leukemia cell bioenergetics reveals decreased atp synthesis during cell division
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536222/
https://www.ncbi.nlm.nih.gov/pubmed/33020492
http://dx.doi.org/10.1038/s41467-020-18769-y
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