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Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells

Cancer growth is predicted to require substantial rates of substrate catabolism and ATP turnover to drive unrestricted biosynthesis and cell growth. While substrate limitation can dramatically alter cell behavior, the effects of substrate limitation on total cellular ATP production rate is poorly un...

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Autores principales: Louie, Maggie C., Ton, Justin, Brady, Maurice L., Le, Diem T., Mar, Jordon N., Lerner, Chad A., Gerencser, Akos A., Mookerjee, Shona A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7667374/
https://www.ncbi.nlm.nih.gov/pubmed/33224868
http://dx.doi.org/10.3389/fonc.2020.01703
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author Louie, Maggie C.
Ton, Justin
Brady, Maurice L.
Le, Diem T.
Mar, Jordon N.
Lerner, Chad A.
Gerencser, Akos A.
Mookerjee, Shona A.
author_facet Louie, Maggie C.
Ton, Justin
Brady, Maurice L.
Le, Diem T.
Mar, Jordon N.
Lerner, Chad A.
Gerencser, Akos A.
Mookerjee, Shona A.
author_sort Louie, Maggie C.
collection PubMed
description Cancer growth is predicted to require substantial rates of substrate catabolism and ATP turnover to drive unrestricted biosynthesis and cell growth. While substrate limitation can dramatically alter cell behavior, the effects of substrate limitation on total cellular ATP production rate is poorly understood. Here, we show that MCF7 breast cancer cells, given different combinations of the common cell culture substrates glucose, glutamine, and pyruvate, display ATP production rates 1.6-fold higher than when cells are limited to each individual substrate. This increase occurred mainly through faster oxidative ATP production, with little to no increase in glycolytic ATP production. In comparison, non-transformed C2C12 myoblast cells show no change in ATP production rate when substrates are limited. In MCF7 cells, glutamine allows unexpected access to oxidative capacity that pyruvate, also a strictly oxidized substrate, does not. Pyruvate, when added with other exogenous substrates, increases substrate-driven oxidative ATP production, by increasing both ATP supply and demand. Overall, we find that MCF7 cells are highly flexible with respect to maintaining total cellular ATP production under different substrate-limited conditions, over an acute (within minutes) timeframe that is unlikely to result from more protracted (hours or more) transcription-driven changes to metabolic enzyme expression. The near-identical ATP production rates maintained by MCF7 and C2C12 cells given single substrates reveal a potential difficulty in using substrate limitation to selectively starve cancer cells of ATP. In contrast, the higher ATP production rate conferred by mixed substrates in MCF7 cells remains a potentially exploitable difference.
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spelling pubmed-76673742020-11-20 Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells Louie, Maggie C. Ton, Justin Brady, Maurice L. Le, Diem T. Mar, Jordon N. Lerner, Chad A. Gerencser, Akos A. Mookerjee, Shona A. Front Oncol Oncology Cancer growth is predicted to require substantial rates of substrate catabolism and ATP turnover to drive unrestricted biosynthesis and cell growth. While substrate limitation can dramatically alter cell behavior, the effects of substrate limitation on total cellular ATP production rate is poorly understood. Here, we show that MCF7 breast cancer cells, given different combinations of the common cell culture substrates glucose, glutamine, and pyruvate, display ATP production rates 1.6-fold higher than when cells are limited to each individual substrate. This increase occurred mainly through faster oxidative ATP production, with little to no increase in glycolytic ATP production. In comparison, non-transformed C2C12 myoblast cells show no change in ATP production rate when substrates are limited. In MCF7 cells, glutamine allows unexpected access to oxidative capacity that pyruvate, also a strictly oxidized substrate, does not. Pyruvate, when added with other exogenous substrates, increases substrate-driven oxidative ATP production, by increasing both ATP supply and demand. Overall, we find that MCF7 cells are highly flexible with respect to maintaining total cellular ATP production under different substrate-limited conditions, over an acute (within minutes) timeframe that is unlikely to result from more protracted (hours or more) transcription-driven changes to metabolic enzyme expression. The near-identical ATP production rates maintained by MCF7 and C2C12 cells given single substrates reveal a potential difficulty in using substrate limitation to selectively starve cancer cells of ATP. In contrast, the higher ATP production rate conferred by mixed substrates in MCF7 cells remains a potentially exploitable difference. Frontiers Media S.A. 2020-11-02 /pmc/articles/PMC7667374/ /pubmed/33224868 http://dx.doi.org/10.3389/fonc.2020.01703 Text en Copyright © 2020 Louie, Ton, Brady, Le, Mar, Lerner, Gerencser and Mookerjee. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Oncology
Louie, Maggie C.
Ton, Justin
Brady, Maurice L.
Le, Diem T.
Mar, Jordon N.
Lerner, Chad A.
Gerencser, Akos A.
Mookerjee, Shona A.
Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells
title Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells
title_full Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells
title_fullStr Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells
title_full_unstemmed Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells
title_short Total Cellular ATP Production Changes With Primary Substrate in MCF7 Breast Cancer Cells
title_sort total cellular atp production changes with primary substrate in mcf7 breast cancer cells
topic Oncology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7667374/
https://www.ncbi.nlm.nih.gov/pubmed/33224868
http://dx.doi.org/10.3389/fonc.2020.01703
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