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Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance

Chemotherapy remains the standard of care for most cancers worldwide, however development of chemoresistance due to the presence of the drug-effluxing ATP binding cassette (ABC) transporters remains a significant problem. The development of safe and effective means to overcome chemoresistance is cri...

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Autores principales: Giddings, Emily L., Champagne, Devin P., Wu, Meng-Han, Laffin, Joshua M., Thornton, Tina M., Valenca-Pereira, Felipe, Culp-Hill, Rachel, Fortner, Karen A., Romero, Natalia, East, James, Cao, Phoebe, Arias-Pulido, Hugo, Sidhu, Karatatiwant S., Silverstrim, Brian, Kam, Yoonseok, Kelley, Shana, Pereira, Mark, Bates, Susan E., Bunn, Janice Y., Fiering, Steven N., Matthews, Dwight E., Robey, Robert W., Stich, Domink, D’Alessandro, Angelo, Rincon, Mercedes
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8121950/
https://www.ncbi.nlm.nih.gov/pubmed/33990571
http://dx.doi.org/10.1038/s41467-021-23071-6
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author Giddings, Emily L.
Champagne, Devin P.
Wu, Meng-Han
Laffin, Joshua M.
Thornton, Tina M.
Valenca-Pereira, Felipe
Culp-Hill, Rachel
Fortner, Karen A.
Romero, Natalia
East, James
Cao, Phoebe
Arias-Pulido, Hugo
Sidhu, Karatatiwant S.
Silverstrim, Brian
Kam, Yoonseok
Kelley, Shana
Pereira, Mark
Bates, Susan E.
Bunn, Janice Y.
Fiering, Steven N.
Matthews, Dwight E.
Robey, Robert W.
Stich, Domink
D’Alessandro, Angelo
Rincon, Mercedes
author_facet Giddings, Emily L.
Champagne, Devin P.
Wu, Meng-Han
Laffin, Joshua M.
Thornton, Tina M.
Valenca-Pereira, Felipe
Culp-Hill, Rachel
Fortner, Karen A.
Romero, Natalia
East, James
Cao, Phoebe
Arias-Pulido, Hugo
Sidhu, Karatatiwant S.
Silverstrim, Brian
Kam, Yoonseok
Kelley, Shana
Pereira, Mark
Bates, Susan E.
Bunn, Janice Y.
Fiering, Steven N.
Matthews, Dwight E.
Robey, Robert W.
Stich, Domink
D’Alessandro, Angelo
Rincon, Mercedes
author_sort Giddings, Emily L.
collection PubMed
description Chemotherapy remains the standard of care for most cancers worldwide, however development of chemoresistance due to the presence of the drug-effluxing ATP binding cassette (ABC) transporters remains a significant problem. The development of safe and effective means to overcome chemoresistance is critical for achieving durable remissions in many cancer patients. We have investigated the energetic demands of ABC transporters in the context of the metabolic adaptations of chemoresistant cancer cells. Here we show that ABC transporters use mitochondrial-derived ATP as a source of energy to efflux drugs out of cancer cells. We further demonstrate that the loss of methylation-controlled J protein (MCJ) (also named DnaJC15), an endogenous negative regulator of mitochondrial respiration, in chemoresistant cancer cells boosts their ability to produce ATP from mitochondria and fuel ABC transporters. We have developed MCJ mimetics that can attenuate mitochondrial respiration and safely overcome chemoresistance in vitro and in vivo. Administration of MCJ mimetics in combination with standard chemotherapeutic drugs could therefore become an alternative strategy for treatment of multiple cancers.
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spelling pubmed-81219502021-05-18 Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance Giddings, Emily L. Champagne, Devin P. Wu, Meng-Han Laffin, Joshua M. Thornton, Tina M. Valenca-Pereira, Felipe Culp-Hill, Rachel Fortner, Karen A. Romero, Natalia East, James Cao, Phoebe Arias-Pulido, Hugo Sidhu, Karatatiwant S. Silverstrim, Brian Kam, Yoonseok Kelley, Shana Pereira, Mark Bates, Susan E. Bunn, Janice Y. Fiering, Steven N. Matthews, Dwight E. Robey, Robert W. Stich, Domink D’Alessandro, Angelo Rincon, Mercedes Nat Commun Article Chemotherapy remains the standard of care for most cancers worldwide, however development of chemoresistance due to the presence of the drug-effluxing ATP binding cassette (ABC) transporters remains a significant problem. The development of safe and effective means to overcome chemoresistance is critical for achieving durable remissions in many cancer patients. We have investigated the energetic demands of ABC transporters in the context of the metabolic adaptations of chemoresistant cancer cells. Here we show that ABC transporters use mitochondrial-derived ATP as a source of energy to efflux drugs out of cancer cells. We further demonstrate that the loss of methylation-controlled J protein (MCJ) (also named DnaJC15), an endogenous negative regulator of mitochondrial respiration, in chemoresistant cancer cells boosts their ability to produce ATP from mitochondria and fuel ABC transporters. We have developed MCJ mimetics that can attenuate mitochondrial respiration and safely overcome chemoresistance in vitro and in vivo. Administration of MCJ mimetics in combination with standard chemotherapeutic drugs could therefore become an alternative strategy for treatment of multiple cancers. Nature Publishing Group UK 2021-05-14 /pmc/articles/PMC8121950/ /pubmed/33990571 http://dx.doi.org/10.1038/s41467-021-23071-6 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Giddings, Emily L.
Champagne, Devin P.
Wu, Meng-Han
Laffin, Joshua M.
Thornton, Tina M.
Valenca-Pereira, Felipe
Culp-Hill, Rachel
Fortner, Karen A.
Romero, Natalia
East, James
Cao, Phoebe
Arias-Pulido, Hugo
Sidhu, Karatatiwant S.
Silverstrim, Brian
Kam, Yoonseok
Kelley, Shana
Pereira, Mark
Bates, Susan E.
Bunn, Janice Y.
Fiering, Steven N.
Matthews, Dwight E.
Robey, Robert W.
Stich, Domink
D’Alessandro, Angelo
Rincon, Mercedes
Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance
title Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance
title_full Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance
title_fullStr Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance
title_full_unstemmed Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance
title_short Mitochondrial ATP fuels ABC transporter-mediated drug efflux in cancer chemoresistance
title_sort mitochondrial atp fuels abc transporter-mediated drug efflux in cancer chemoresistance
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8121950/
https://www.ncbi.nlm.nih.gov/pubmed/33990571
http://dx.doi.org/10.1038/s41467-021-23071-6
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