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Transient heat release during induced mitochondrial proton uncoupling

Non-shivering thermogenesis through mitochondrial proton uncoupling is one of the dominant thermoregulatory mechanisms crucial for normal cellular functions. The metabolic pathway for intracellular temperature rise has widely been considered as steady-state substrate oxidation. Here, we show that a...

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Autores principales: Rajagopal, Manjunath C., Brown, Jeffrey W., Gelda, Dhruv, Valavala, Krishna V., Wang, Huan, Llano, Daniel A., Gillette, Rhanor, Sinha, Sanjiv
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6659641/
https://www.ncbi.nlm.nih.gov/pubmed/31372518
http://dx.doi.org/10.1038/s42003-019-0535-y
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author Rajagopal, Manjunath C.
Brown, Jeffrey W.
Gelda, Dhruv
Valavala, Krishna V.
Wang, Huan
Llano, Daniel A.
Gillette, Rhanor
Sinha, Sanjiv
author_facet Rajagopal, Manjunath C.
Brown, Jeffrey W.
Gelda, Dhruv
Valavala, Krishna V.
Wang, Huan
Llano, Daniel A.
Gillette, Rhanor
Sinha, Sanjiv
author_sort Rajagopal, Manjunath C.
collection PubMed
description Non-shivering thermogenesis through mitochondrial proton uncoupling is one of the dominant thermoregulatory mechanisms crucial for normal cellular functions. The metabolic pathway for intracellular temperature rise has widely been considered as steady-state substrate oxidation. Here, we show that a transient proton motive force (pmf) dissipation is more dominant than steady-state substrate oxidation in stimulated thermogenesis. Using transient intracellular thermometry during stimulated proton uncoupling in neurons of Aplysia californica, we observe temperature spikes of ~7.5 K that decay over two time scales: a rapid decay of ~4.8 K over ~1 s followed by a slower decay over ~17 s. The rapid decay correlates well in time with transient electrical heating from proton transport across the mitochondrial inner membrane. Beyond ~33 s, we do not observe any heating from intracellular sources, including substrate oxidation and pmf dissipation. Our measurements demonstrate the utility of transient thermometry in better understanding the thermochemistry of mitochondrial metabolism.
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spelling pubmed-66596412019-08-01 Transient heat release during induced mitochondrial proton uncoupling Rajagopal, Manjunath C. Brown, Jeffrey W. Gelda, Dhruv Valavala, Krishna V. Wang, Huan Llano, Daniel A. Gillette, Rhanor Sinha, Sanjiv Commun Biol Article Non-shivering thermogenesis through mitochondrial proton uncoupling is one of the dominant thermoregulatory mechanisms crucial for normal cellular functions. The metabolic pathway for intracellular temperature rise has widely been considered as steady-state substrate oxidation. Here, we show that a transient proton motive force (pmf) dissipation is more dominant than steady-state substrate oxidation in stimulated thermogenesis. Using transient intracellular thermometry during stimulated proton uncoupling in neurons of Aplysia californica, we observe temperature spikes of ~7.5 K that decay over two time scales: a rapid decay of ~4.8 K over ~1 s followed by a slower decay over ~17 s. The rapid decay correlates well in time with transient electrical heating from proton transport across the mitochondrial inner membrane. Beyond ~33 s, we do not observe any heating from intracellular sources, including substrate oxidation and pmf dissipation. Our measurements demonstrate the utility of transient thermometry in better understanding the thermochemistry of mitochondrial metabolism. Nature Publishing Group UK 2019-07-26 /pmc/articles/PMC6659641/ /pubmed/31372518 http://dx.doi.org/10.1038/s42003-019-0535-y Text en © The Author(s) 2019 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
Rajagopal, Manjunath C.
Brown, Jeffrey W.
Gelda, Dhruv
Valavala, Krishna V.
Wang, Huan
Llano, Daniel A.
Gillette, Rhanor
Sinha, Sanjiv
Transient heat release during induced mitochondrial proton uncoupling
title Transient heat release during induced mitochondrial proton uncoupling
title_full Transient heat release during induced mitochondrial proton uncoupling
title_fullStr Transient heat release during induced mitochondrial proton uncoupling
title_full_unstemmed Transient heat release during induced mitochondrial proton uncoupling
title_short Transient heat release during induced mitochondrial proton uncoupling
title_sort transient heat release during induced mitochondrial proton uncoupling
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6659641/
https://www.ncbi.nlm.nih.gov/pubmed/31372518
http://dx.doi.org/10.1038/s42003-019-0535-y
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