SDH Subunit C Regulates Muscle Oxygen Consumption and Fatigability in an Animal Model of Pulmonary Emphysema
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Abstract
Patients with pulmonary emphysema often develop locomotor muscle dysfunction, which is independently associated with disability and higher mortality in that population. Muscle dysfunction entails reduced force generation capacity, which partially depends on fibers’ oxidative potential, yet very little mechanistic research has focused on muscle respiration in pulmonary emphysema. Using a recently established animal model of pulmonary emphysema–driven skeletal muscle dysfunction, we found downregulation of SDHC (succinate dehydrogenase subunit C) in association with lower oxygen consumption and fatigue tolerance in locomotor muscles. Reduced SDH activity has been previously observed in muscles from patients with pulmonary emphysema, and we found that SDHC is required to support respiration in cultured muscle cells. Moreover, in vivo gain of SDH function in emphysema animals’ muscles resulted in better oxygen consumption rate and fatigue tolerance. These changes correlated with a larger number of relatively more oxidative type 2-A and 2X fibers and a reduced amount of 2B fibers. Our data suggest that SDHC is a key regulator of respiration and fatigability in pulmonary emphysema–driven skeletal muscles, which could be impactful in developing strategies aimed at attenuating this comorbidity.
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In a mouse model of emphysema (IL-13 transgenic mice), reduced SDH (CII) activity underlies decreased mitochondrial respiration in the extensor digitorum longus.
“Recently, Balnis and colleagues evidenced a reduced SDH (CII) activity underlying a decreased mitochondrial respiration in the extensor digitorum longis of a mouse model of emphysema (IL-13 transgenic mice) [102].”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [102]
The Results report reduced oxygen consumption in extensor digitorum longus (EDL) muscle from IL13 transgenic mice. The paper also reports reduced SDH activity in tibialis anterior muscle and concludes that SDHC downregulation is at least partially responsible for muscle metabolic dysfunction. It does not establish that reduced SDH activity in EDL specifically underlies the entire decrease in its respiration (page numbers unavailable in our copy). (LLM, conf=0.86)
Experimental — accuracy not yet measuredMitochondrial function can regulate muscle fiber phenotype in vivo, as transfecting the defective CII subunit C into mouse muscles increased both mitochondrial respiration and oxidative myofiber proportion.
“Importantly, transfecting the defective CII subunit C to mice muscles significantly increased both mitochondrial function (respiration) and oxidative myofibers’ proportion, indicating that mitochondrial function could regulate the muscle fiber phenotype in vivo.”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [102]
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Balnis, J., Vincent, C. E., Jones, A., Drake, L. A., Coon, J. J., Lee, C. G., Elias, J. A., Singer, H. A., & Jaitovich, A. (2020) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2019-0439le · Cited by 12 · see citing works
Self-citationRegenerating muscles the type 2 way
Leavy, O. (2013) · Nature reviews. Immunology · doi:10.1038/nri3460 · Cited by 4 · see citing works
Flagged first, then by citations
1 of the 88 references couldn’t be matched to a known paper.
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Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting
Henrot, P., Dupin, I., Schilfarth, P., Esteves, P., Blervaque, L., Zysman, M., Gouzi, F., Hayot, M., Pomiès, P., & Berger, P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076454 · Cited by 85 · see citing works
Roth‐Walter, F., Adcock, I. M., Benito‐Villalvilla, C., Bianchini, R., Bjermer, L. H., Caramori, G., Cari, L., Chung, K. F., Diamant, Z., Eguíluz‐Gracia, I., et al. (2023) · Allergy · doi:10.1111/all.15977 · Cited by 31 · see citing works
The flux of energy in critical illness and the obesity paradox
Jaitovich, A., & Hall, J. B. (2025) · Physiological Reviews · doi:10.1152/physrev.00029.2024 · Cited by 33 · see citing works
Self-citationHuang, T., Liang, Z., Wang, K., Miao, X., & Zheng, L. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1459717 · Cited by 39 · see citing works
Deaccelerated Myogenesis and Autophagy in Genetically Induced Pulmonary Emphysema
Balnis, J., Drake, L. A., Singer, D. V., Vincent, C. E., Korponay, T. C., D’Armiento, J., Lee, C. G., Elias, J. A., Singer, H. A., & Jaitovich, A. (2022) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2021-0351oc · Cited by 27 · see citing works
Self-citationSuccinate dehydrogenase complex subunit C: Role in cellular physiology and disease
Wang, Q., Li, M., Zeng, N., Zhou, Y., & Yan, J. (2023) · Experimental Biology and Medicine · doi:10.1177/15353702221147567 · Cited by 27 · see citing works
Ruff, Z. D. V., Miller, M. J., Moro, T., Reidy, P. T., Ebert, S. M., Volpi, E., Adams, C. M., & Rasmussen, B. B. (2025) · GeroScience · doi:10.1007/s11357-025-01564-2 · Cited by 19 · see citing works
Integrating Mechanisms of Exacerbated Atrophy and Other Adverse Skeletal Muscle Impact in COPD
Taivassalo, T., & Hepple, R. T. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.861617 · Cited by 16 · see citing works
Jaitovich, A. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00292.2022 · Cited by 14 · see citing works
Self-citationBalnis, J., Tufts, A., Jackson, E. L., Drake, L. A., Singer, D. V., Lacomis, D., Lee, C. G., Elias, J. A., Doles, J. D., Maher, L. J., et al. (2024) · Science Advances · doi:10.1126/sciadv.ado8549 · Cited by 11 · see citing works
Self-citationRapamycin improves satellite cells’ autophagy and muscle regeneration during hypercapnia
Balnis, J., Jackson, E. L., Drake, L. A., Singer, D. V., Ramos, R. B., Singer, H. A., & Jaitovich, A. (2024) · JCI Insight · doi:10.1172/jci.insight.182842 · Cited by 10 · see citing works
Self-citationCell-Based Measurement of Mitochondrial Function in Human Airway Smooth Muscle Cells
Bhat, S. M., Yap, J. Q., Ramirez, O. R., Delmotte, P. F., & Sieck, G. C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411506 · Cited by 5 · see citing works
Schumacker, P. T. (2021) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2021-0200ed · Cited by 5 · see citing works
Chronic succinate exposure does not cause liver injury
Balnis, J., Jackson, E. L., Drake, L. A., Vincent, C. E., Lee, H., Singer, H. A., & Jaitovich, A. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00129.2025 · Cited by 4 · see citing works
Self-citationLu, X., Gong, T., Liu, Y., Fu, J., Zhang, Q., Jin, M., & Wang, Y. (2025) · Food Bioscience · doi:10.1016/j.fbio.2025.106638 · Cited by 2 · see citing works
Huang, J.-Q., Wang, P.-X., Zhang, X.-Y., You, Y.-T., Zhan, J., Xu, D.-H., Liu, Y., Zhu, X., & Bao, X. (2026) · Redox Biology · doi:10.1016/j.redox.2026.104308 · Cited by 1 · see citing works
Dysregulated myogenesis and autophagy in genetically induced pulmonary emphysemaPreprint
Balnis, J., Drake, L. A., Singer, D. V., Vincent, C. E., Korponay, T. C., D'Armiento, J. M., Lee, C. G., Elias, J. A., Singer, H. A., & Jaitovich, A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.08.450201
Self-citationGao, Q., Mao, Y., Shu, X., Wang, W., Xia, J., & Wu, W. C. (2026) · Antioxidants · doi:10.3390/antiox15070837
- Authors
- Balnis, J., Drake, L. A., Vincent, C. E., Korponay, T. C., Singer, D. V., Lacomis, D., Lee, C. G., Elias, J. A., Jourd’heuil, D., Singer, H. A., & Jaitovich, A.
- Affiliations
- Albany Medical College (US)
- Institute for Clinical Pharmacodynamics (United States) (US)
- University of Pittsburgh (US)
- Brown University (US)
- Corresponding author
- Jaitovich, Ariel
- ORCID
- Venue
- American Journal of Respiratory Cell and Molecular Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2021-09-01
- Volume
- 65
- Issue
- 3
- Pages
- 259-271
- ISSN
- 1044-1549 (ISSN-L)
- 1535-4989
- PMC
- PMC8485989
- OpenAlex
- W3158049040
- Cited by
- 19
- References
- 88
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 4 · 2022: 3 · 2021: 3
- FWCI
- 0.94
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- American Journal of Respiratory Cell and Molecular Biology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (PO1 HL114501, GM108538)
- National Heart, Lung, and Blood Institute (HL130704, HL114501, K01HL130704, PO1 HL114501, R01HL049426, R01HL142807, HL115813, R01HL115813, P01HL114501)
- National Institute of General Medical Sciences (P41GM108538)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
- Keywords
- emphysema, skeletal muscle oxygen consumption, muscle fatigue, muscle respiration, muscle fiber composition, oxidative capacity
- MeSH terms
- Animals, Disease Models, Animal, Fatigue, Membrane Proteins, Mice, Transgenic, Oxygen Consumption, Pulmonary Emphysema, Muscle, Skeletal, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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