ATP synthase: a moonlighting enzyme with unprecedented functions

Vigneau, Jean-Nicolas; Fahimi, Peyman; Ebert, Maximilian; Cheng, Youji; Tannahill, Connor; Muir, P. H.; Nguyen‐Dang, T. T.; Matta, Chérif F.

doi:10.1039/d1cc06793a

Cited by 9 publications

(6 citation statements)

References 51 publications

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“…Matta and colleagues have also argued, based on thermodynamic principles ( Matta and Massa, 2015 ), that the true efficiency of ATP synthase must be close to 90%, taking account of heat dissipation by informational transactions (Landauer’s principle, Landauer, 1961 ) which is compensated by the inherent electrostatic potential of the enzyme ( Vigneau et al, 2022 ). This may partly explain why the additional temperature decrease produced by inhibiting ATP synthase in addition to inhibiting respiration is both small, but non-negligible.…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial temperature homeostasis resists external metabolic stresses

Terzioglu,

Veeroja,

Montonen

et al. 2023

eLife

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Based on studies with a fluorescent reporter dye, Mito Thermo Yellow, and the genetically encoded gTEMP ratiometric fluorescent temperature indicator targeted to mitochondria, the temperature of active mitochondria in four mammalian and one insect cell-line was estimated to be up to 15 °C above that of the external environment to which the cells were exposed. High mitochondrial temperature was maintained in the face of a variety of metabolic stresses, including substrate starvation or modification, decreased ATP demand due to inhibition of cytosolic protein synthesis, inhibition of the mitochondrial adenine nucleotide transporter and, if an auxiliary pathway for electron transfer was available via the alternative oxidase, even respiratory poisons acting downstream of complex I. We propose that the high temperature of active mitochondria is an inescapable consequence of the biochemistry of oxidative phosphorylation and is homeostatically maintained as a primary feature of mitochondrial metabolism. Mitochondria are at least 15 °C hotter than their external environment in living cells. In response to diverse metabolic stresses, mitochondrial temperature re-adjusts to this value whenever possible.

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Section: Discussionmentioning

confidence: 99%

Mitochondrial temperature homeostasis resists external metabolic stresses

Terzioglu,

Veeroja,

Montonen

et al. 2023

eLife

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“…Na + to be selected and sorted for excretion by the kidney [216][217][218]. These ideas also place a limit on the thermodynamic efficiency of a molecular machine like ATP synthase/ATPase which acts as a sorting machine, picking protons for transport parallel or antiparallel to a pH gradient, respectively, across mitochondrial inner membranes or bacterial membranes [242][243][244][245][246].…”

Section: Closing Remarksmentioning

confidence: 99%

The sounds of science—a symphony for many instruments and voices: part II

’t Hooft,

Phillips,

Zeilinger

et al. 2024

Phys. Scr.

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Despite its amazing quantitative successes and contributions to revolutionary technologies, physics currently faces many unsolved mysteries ranging from the meaning of quantum mechanics to the nature of the dark energy that will determine the future of the Universe. It is clearly prohibitive for the general reader, and even the best informed physicists, to follow the vast number of technical papers published in the thousands of specialized journals. For this reason, we have asked the leading experts across many of the most important areas of physics to summarise their global assessment of some of the most important issues. In lieu of an extremely long abstract summarising the contents, we invite the reader to look at the section headings and their authors, and then to indulge in a feast of stimulating topics spanning the current frontiers of fundamental physics from ‘The Future of Physics’ by William D Phillips and ‘What characterises topological effects in physics?’ by Gerard ’t Hooft through the contributions of the widest imaginable range of world leaders in their respective areas. This paper is presented as a preface to exciting developments by senior and young scientists in the years that lie ahead, and a complement to the less authoritative popular accounts by journalists.

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“…Matta and colleagues have also argued, based on thermodynamic principles 54 , that the true efficiency of ATP synthase must be close to 90%, taking account of heat dissipation by informational transactions (Landauer's principle 55 ) which is compensated by the inherent electrostatic potential of the enzyme 56 . This may partly explain why the additional temperature decrease produced by inhibiting ATP synthase in addition to inhibiting respiration is both small, but non-negligible.…”

Section: Theoretical Considerationsmentioning

confidence: 99%

Mitochondrial temperature homeostasis resists external metabolic stresses

Terzioglu,

Veeroja,

Montonen

et al. 2023

Preprint

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Based on studies with a fluorescent reporter dye, Mito Thermo Yellow, and the genetically encoded gTEMP ratiometric fluorescent temperature indicator targeted to mitochondria, the temperature of active mitochondria in four mammalian and one insect cell-line was estimated to be up to 15 °C above that of the external environment to which the cells were exposed. High mitochondrial temperature was maintained in the face of a variety of metabolic stresses, including substrate starvation or modification, decreased ATP demand due to inhibition of cytosolic protein synthesis, inhibition of the mitochondrial adenine nucleotide transporter and, if an auxiliary pathway for electron transfer was available via the alternative oxidase, even respiratory poisons acting downstream of complex I. We propose that the high temperature of active mitochondria is an inescapable consequence of the biochemistry of oxidative phosphorylation and is homeostatically maintained as a primary feature of mitochondrial metabolism.IMPACT STATEMENTMitochondria are at least 15 °C hotter than their external environment in living cells. In response to diverse metabolic stresses, mitochondrial temperature re-adjusts to this value whenever possible.

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ATP synthase: a moonlighting enzyme with unprecedented functions

Abstract: ATP synthase’s intrinsic molecular electrostatic potential (MESP) adds constructively to, and hence reinforces, the chemiosmotic voltage. This ATP synthase voltage represents a new free energy term that appears to have...

Cited by 9 publications

References 51 publications

Mitochondrial temperature homeostasis resists external metabolic stresses

Mitochondrial temperature homeostasis resists external metabolic stresses

The sounds of science—a symphony for many instruments and voices: part II

Mitochondrial temperature homeostasis resists external metabolic stresses

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