pH-gated succinate secretion regulates muscle remodeling in response to exercise
Open accessAbstract
In response to skeletal muscle contraction during exercise, paracrine factors coordinate tissue remodeling, which underlies this healthy adaptation. Here we describe a pH-sensing metabolite signal that initiates muscle remodeling upon exercise. In mice and humans, exercising skeletal muscle releases the mitochondrial metabolite succinate into the local interstitium and circulation. Selective secretion of succinate is facilitated by its transient protonation, which occurs upon muscle cell acidification. In the protonated monocarboxylic form, succinate is rendered a transport substrate for monocarboxylate transporter 1, which facilitates pH-gated release. Upon secretion, succinate signals via its cognate receptor SUCNR1 in non-myofibrillar cells in muscle tissue to control muscle-remodeling transcriptional programs. This succinate-SUCNR1 signaling is required for paracrine regulation of muscle innervation, muscle matrix remodeling, and muscle strength in response to exercise training. In sum, we define a bioenergetic sensor in muscle that utilizes intracellular pH and succinate to coordinate tissue adaptation to exercise.
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Succinate release from muscle cells occurs in a pH-dependent manner via monocarboxylate transporter 1 and is facilitated by transient protonation of succinate upon muscle cell acidification.
“This release occurs in a pH-dependent manner via monocarboxylate transporter 1 and is facilitated by transient protonation of succinate upon muscle cell acidification (191).”
From Regulation and function of the mammalian tricarboxylic acid cycle (2023) · cites this paper as [191]
Circulating succinate binds its receptor SUCNR1 in nonmyofibrillar cells in muscle tissue to initiate transcriptional programs that support tissue remodeling in response to exercise.
“Circulating succinate binds its receptor SUCNR1 in nonmyofibrillar cells in muscle tissue to initiate transcriptional programs that support tissue remodeling in response to exercise (191).”
From Regulation and function of the mammalian tricarboxylic acid cycle (2023) · cites this paper as [191]
Both mouse and human muscle cells selectively release succinate during physical activity.
“Notably, both mouse and human muscle cells selectively release succinate during physical activity (191).”
From Regulation and function of the mammalian tricarboxylic acid cycle (2023) · cites this paper as [191]
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Edman, S., Flockhart, M., Larsen, F. J., & Apró, W. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101854 · Cited by 23 · see citing works
Amino Acid and Glucose Fermentation Maintain ATP Content in Mouse and Human Malignant Glioma Cells
Lee, D. C., Ta, N. L., Mukherjee, P., Duraj, T., Domin, M. A., Greenwood, B. P., Karmacharya, S., Narain, N. R., Kiebish, M. A., Chinopoulos, C., et al. (2024) · ASN NEURO · doi:10.1080/17590914.2024.2422268 · Cited by 21 · see citing works
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Targeting Mitochondria for Cancer Treatment
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Gas regulation of complex II reversal via electron shunting to fumarate in the mammalian ETC
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- Authors
- Reddy, A., Bozi, L. H. M., Yaghi, O. K., Mills, E. L., Xiao, H., Nicholson, H. E., Paschini, M., Paulo, J. A., Garrity, R., Laznik-Bogoslavski, D., Ferreira, J. C. B., Carl, C. S., Sjøberg, K. A., Wojtaszewski, J. F. P., Jeppesen, J. F., Kiens, B., Gygi, S. P., Richter, E. A., Mathis, D., & Chouchani, E. T.
- Affiliations
- Harvard University (US)
- Boston Children's Hospital (US)
- Dana-Farber Cancer Institute (US)
- Universidade de São Paulo (BR)
- University of Copenhagen (DK)
- Novo Nordisk (Denmark) (DK)
- Corresponding author
- Chouchani, Edward T.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2020-10
- Volume
- 183
- Issue
- 1
- Pages
- 62-75.e17
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7778787
- OpenAlex
- W3086698680
- Cited by
- 279
- References
- 82
- Citations by year
- 2026: 38 · 2025: 58 · 2024: 63 · 2023: 44 · 2022: 41 · 2021: 33 · 2020: 2
- FWCI
- 9.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- skeletal muscle remodeling, intracellular pH, protonation, MCT1, SUCNR1, paracrine signaling, muscle innervation, extracellular matrix remodeling, muscle strength, exercise training, mitochondrial metabolites
- MeSH terms
- Monocarboxylate Transport Protein 1, Animals, Humans, Hydrogen-Ion Concentration, Inflammation, Mitochondria, Muscle Contraction, Succinates, Signal Transduction, Muscle, Skeletal, Succinic Acid, Monocarboxylic Acid Transporters, Symporters, Receptors, G-Protein-Coupled, Mice
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