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Effect of acute cold exposure on cardiac mitochondrial function: role of sirtuins

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Abstract

Cardiac function depends mainly on mitochondrial metabolism. Cold conditions increase the risk of cardiovascular diseases by increasing blood pressure. Adaptive thermogenesis leads to increased mitochondrial biogenesis and function in skeletal muscles and adipocytes. Here, we studied the effect of acute cold exposure on cardiac mitochondrial function and its regulation by sirtuins. Significant increase in mitochondrial DNA copy number as measured by the ratio between mitochondrial-coded COX-II and nuclear-coded cyclophilin A gene expression by qRT-PCR and increase in the expression of PGC-1α, a mitochondriogenic factor and its downstream target NRF-1 were observed on cold exposure. This was associated with an increase in the activity of SIRT-1, which is known to activate PGC-1α. Mitochondrial SIRT-3 was also upregulated. Increase in sirtuin activity was reflected in total protein acetylome, which decreased in cold-exposed cardiac tissue. An increase in mitochondrial MnSOD further indicated enhanced mitochondrial function. Further evidence for this was obtained from ex vivo studies of cardiac tissue treated with norepinephrine, which caused a significant increase in mitochondrial MnSOD and SIRT-3. SIRT-3 appears to mediate the regulation of MnSOD, as treatment with AGK-7, a SIRT-3 inhibitor reversed the norepinephrine-induced upregulation of MnSOD. It, therefore, appears that SIRT-3 activation in response to SIRT-1–PGC-1α activation contributes to the regulation of cardiac mitochondrial activity during acute cold exposure.

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Data availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Abbreviations

BAT:

Brown adipose tissue

NE:

Norepinephrine

SNS:

Sympathetic nervous system

Tfam:

Mitochondrial transcription factor A

UCP-1:

Uncoupling Protein-1

SOD:

Superoxide dismutase

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Funding

Mithra. S. Mohan was supported by the Kerala State Council for Science, Technology and Environment in the form of research fellowship. Saja. K was supported by the University Grants Commission—Basic Scientific Research in the form of start-up grant—and the Department of Science and Technology—Science Engineering Research Board in the form of Young investigator program. Aswani. S. S and Aparna.N. S were supported by Joint CSIR-UGC fellowship under UGC scheme.

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Authors and Affiliations

  1. Department of Biochemistry, University of Kerala, Kariavattom, Thiruvananthapuram, Kerala, 695581, India

    Mithra. S. Mohan, S. S. Aswani, N. S. Aparna & K. Saja

  2. Department of Computational Biology and Bioinformatics, University of Kerala, Kariavattom, Thiruvananthapuram, Kerala, 695581, India

    P. R. Sudhakaran

  3. Department of Biochemistry, Government College, Kariavattom, Thiruvananthapuram, Kerala, 695581, India

    P. T. Boban

Authors
  1. Mithra. S. Mohan
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  2. S. S. Aswani
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  3. N. S. Aparna
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  4. P. T. Boban
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  5. P. R. Sudhakaran
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  6. K. Saja
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Contributions

Mithra. S. Mohan, P. R. Sudhakaran and Saja. K conceptualized the study and planned the experiments and discussed the results. Mithra. S. Mohan wrote the draft of the manuscript. Saja. K, P. R. Sudhakaran and P. T. Boban reviewed and edited the manuscript. Mithra. S. Mohan, Aswani. S. S. and Aparna N. S. carried out the experiments. All authors participated in the design of the study and interpretation and analysis of the data and reviewed the manuscript.

Corresponding author

Correspondence to K. Saja.

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Experiments in this research were reviewed and approved by the animal ethical committee, University of Kerala (IAEC-KU-12b/2014-15).

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Mohan, M.S., Aswani, S.S., Aparna, N.S. et al. Effect of acute cold exposure on cardiac mitochondrial function: role of sirtuins. Mol Cell Biochem 478, 2257–2270 (2023). https://doi.org/10.1007/s11010-022-04656-1

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