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Cited by 111Mitochondrial Function and PathologyATP Synthase and ATPases Researchthermodynamics and calorimetric analyses

Top-down control analysis of temperature effect on oxidative phosphorylation

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DUFOUR, Sylvie, ROUSSE, Nicole, CANIONI, Paul, DIOLEZ, Philippe·1996·Biochemical Journal
DOI 10.1042/bj3140743PMC PMC1217120
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Abstract

The effects of temperature on the control of respiration rate, phosphorylation rate, proton leakage rate, the protonmotive force and the effective ATP/O ratio were determined in isolated rat liver mitochondria over a range of respiratory conditions by applying top-down elasticity and control analyses. Simultaneous measurements of membrane potential, oxidation and phosphorylation rates were performed under various ATP turnover rates, ranging from state 4 to state 3. Although the activities of the three subsystems decreased with temperature (over 30-fold between 37 and 4 °C), the effective ATP/O ratio exhibited a maximum at 25 °C, far below the physiological value. Top-down elasticity analysis revealed that maximal membrane potential was maintained over the range of temperature studied, and that the proton leakage rate was considerably reduced at 4 °C. These results definitely rule out a possible uncoupling of mitochondria at low temperature. At 4 °C, the decrease in ATP/O ratio is explained by the relative decrease in phosphorylation processes revealed by the decrease in depolarization after ADP addition [Diolez and Moreau (1985) Biochim. Biophys. Acta 806, 56–63]. The change in depolarization between 37 and 25 °C was too small to explain the decrease in ATP/O ratio. This result is best explained by the changes in the elasticity of proton leakage to membrane potential between 37 and 25 °C, leading to a higher leak rate at 37 °C for the same value of membrane potential. Top-down control analysis showed that despite the important changes in activities of the three subsystems between 37 and 25 °C, the patterns of the control distribution are very similar. However, a different pattern was obtained at 4 °C under all phosphorylating conditions. Surprisingly, control by the proton leakage subsystem was almost unchanged, although both control patterns by substrate oxidation and phosphorylation subsystems were affected at 4 °C. In comparison with results for 25 and 37 °C, at 4 °C there was evidence for increased control by the phosphorylation subsystem over both fluxes of oxidation and phosphorylation as well as on the ATP/O ratio when the system is close to state 3. However, the pattern of control coefficients as a function of mitochondrial activity also showed enhanced control exerted by the substrate oxidation subsystem under all intermediate conditions. These results suggest that passive membrane permeability to protons is not involved in the effect of temperature on the control of oxidative phosphorylation.

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  • At lower temperatures, mammalian mitochondria have a reduced respiratory rate and hyperpolarization of the mitochondrial membrane, potentially due to decreased ATPase activity, resulting in accumulation of reduced flavins and cytochromes.

    “At lower temperatures, mammalian mitochondria have a reduced respiratory rate and hyperpolarization of the mitochondrial membrane, potentially due to decreased ATPase activity [64][65][66][67], which results in the accumulation of reduced flavins and cytochromes (Fig 3A).”

    From Mitochondrial Activity and Cyr1 Are Key Regulators of Ras1 Activation of C. albicans Virulence Pathways (2015) · cites this paper as [65]

    In the Effect of temperature on oxidative phosphorylation section (Figure 3), the paper reports lower respiration rates at 4 °C and a higher membrane potential during state 3 than at 25 °C. It attributes the reduced depolarization to relative inhibition of the phosphorylation subsystem, but does not specifically identify decreased ATPase activity or report accumulation of reduced flavins and cytochromes. State 4 membrane potential was slightly lower, not higher, at 4 °C. (LLM, conf=0.85)

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1 of the 36 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

  1. Ogawa, S., Rottenberg, H., Brown, T. R., Shulman, R. G., Castillo, C. L. and Glynn, P. (1978) Proc. Natl. Acad. Sci. U.S.A. 75, 1796-1800
  2. Brand, M. D. and Brown, G. C. (1994) in Biothermokinetics (Westerhoff, H. V., ed.), pp. 27-35, Intercept Ltd, Andover Received 3 July 1995/4 October 1995 ; accepted 31 October 1995
  3. Brand, M. D., Chien, L.-F. and Rolfe, D. F. S. (1993) Biochem. Soc. Trans. 21, 757-762
  4. Diolez, P., Kesseler, A., Haraux, F., Valerio, M., Brinkmann, K. and Brand, M. D. (1993) Biochem. Soc. Trans. 21, 769-773

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Authors
DUFOUR, S., ROUSSE, N., CANIONI, P., & DIOLEZ, P.
Affiliations
Centre National de la Recherche Scientifique (FR)
ORCID
Venue
Biochemical Journal
Publisher
Portland Press Ltd.
Published
1996-03-15
Volume
314
Issue
3
Pages
743-751
ISSN
  • 0264-6021 (ISSN-L)
  • 1470-8728
DOI
10.1042/bj3140743
PMC
PMC1217120
OpenAlex
W1762890948
Cited by
111
References
36
Citations by year
2026: 3 · 2025: 3 · 2024: 2 · 2023: 6 · 2022: 2 · 2021: 3 · 2020: 4 · 2019: 3 · 2018: 2 · 2017: 5 · 2016: 2 · 2015: 9 · 2014: 4 · 2013: 3 · 2012: 2
FWCI
1.01
Type
journal article
Language
en
Open access
Locations
  • Biochemical Journal (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
  • Physical Sciences › Chemistry › Physical and Theoretical Chemistry › thermodynamics and calorimetric analyses
Keywords
temperature effects, oxidative phosphorylation, elasticity analysis, proton leak, proton motive force, mitochondrial membrane potential, uncoupling, state 3 respiration, state 4 respiration, substrate oxidation, liver mitochondria, control coefficients
MeSH terms
Adenosine Triphosphate, Animals, Elasticity, Intracellular Membranes, Kinetics, Male, Membrane Potentials, Mitochondria, Liver, Oxidative Phosphorylation, Oxygen Consumption, Temperature, Thermodynamics, Rats, Wistar, Rats

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