The DOI matches its Crossref record; 82 of the 82 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Trapnell, C., Roberts, A., Goff, L. A., Pertea, G. M., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.016 · Cited by 12,145
Enrichr: a comprehensive gene set enrichment analysis web server 2016 update
Kuleshov, M. V., Jones, M. R., Rouillard, A. D., Fernandez, N. F., Duan, Q., Wang, Z., Koplev, S., Jenkins, S. L., Jagodnik, K. M., Lachmann, A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw377 · Cited by 10,799
Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool
Chen, E. Y., Tan, C. M., Kou, Y., Duan, Q., Wang, Z., Meirelles, G. V., Clark, N. R., & Ma’ayan, A. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-128 · Cited by 7,814
Glucose clamp technique: a method for quantifying insulin secretion and resistance.
DeFronzo, R. A., Tobin, J. D., & Andres, R. (1979) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1979.237.3.e214 · Cited by 7,425
Full-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137
Elias, J. E., & Gygi, S. P. (2007) · Nature Methods · doi:10.1038/nmeth1019 · Cited by 3,925
Self-citationGOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists
Eden, E., Navon, R., Steinfeld, I., Lipson, D., & Yakhini, Z. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-48 · Cited by 3,356
Mitochondrial TCA cycle metabolites control physiology and disease
Martínez-Reyes, I., & Chandel, N. S. (2020) · Nature Communications · doi:10.1038/s41467-019-13668-3 · Cited by 2,813
(2012) · doi:10.1016/j.jmoldx.2011.08.002 · Cited by 2,567
iDISCO: A Simple, Rapid Method to Immunolabel Large Tissue Samples for Volume Imaging
Renier, N., Wu, Z., Simon, D. J., Yang, J. H., Ariel, P., & Tessier‐Lavigne, M. (2014) · Cell · doi:10.1016/j.cell.2014.10.010 · Cited by 1,856
Cited by
Sorted by citations
Regulation and function of the mammalian tricarboxylic acid cycle
Arnold, P. K., & Finley, L. W. S. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102838 · Cited by 535
Metabolites as signalling molecules
Baker, S. A., & Rutter, J. P. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00572-w · Cited by 398
Elia, I., Rowe, J. H., Johnson, S. E., Joshi, S., Notarangelo, G., Kurmi, K., Weiss, S. A., Freeman, G. J., Sharpe, A. H., & Haigis, M. C. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.06.008 · Cited by 362
Exercise Metabolism and Adaptation in Skeletal Muscle
Smith, J. A. B., Murach, K. A., Dyar, K. A., & Zierath, J. R. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00606-x · Cited by 342
An exercise-inducible metabolite that suppresses feeding and obesity
Li, V. L., He, Y., Contrepois, K., Liu, H., Kim, J. T., Wiggenhorn, A. L., Tanzo, J. T., Tung, A. S.-H., Lyu, X., Zushin, P.-J. H., et al. (2022) · Nature · doi:10.1038/s41586-022-04828-5 · Cited by 331
Fumarate is a terminal electron acceptor in the mammalian electron transport chain
Spinelli, J. B., Rosen, P. C., Sprenger, H.-G., Puszynska, A. M., Mann, J. L., Roessler, J. M., Cangelosi, A. L., Henne, A., Condon, K. J., Zhang, T., et al. (2021) · Science · doi:10.1126/science.abi7495 · Cited by 221
Machado, S. A., Pasquarelli-do-Nascimento, G., da Silva, D. S., Farias, G. R., Santos, I. D. O., Baptista, L. B., & Magalhães, K. G. (2022) · Nutrition & Metabolism · doi:10.1186/s12986-022-00694-0 · Cited by 239
The molecular athlete: exercise physiology from mechanisms to medals
Furrer, R., Hawley, J. A., & Handschin, C. (2023) · Physiological Reviews · doi:10.1152/physrev.00017.2022 · Cited by 253
Succinate metabolism and its regulation of host-microbe interactions
Wei, Y., Ma, X., Zhao, J., Wang, X., & Gao, C. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2190300 · Cited by 204
UCP1 governs liver extracellular succinate and inflammatory pathogenesis
Mills, E. L., Harmon, C., Jedrychowski, M. P., Xiao, H., Garrity, R., Tran, N., Bradshaw, G. A., Fu, A., Szpyt, J., Reddy, A. J., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00389-5 · Cited by 189
Extracellular succinate hyperpolarizes M2 macrophages through SUCNR1/GPR91-mediated Gq signaling
Trauelsen, M., Hiron, T. K., Lin, D., Petersen, J. E., Breton, B., Husted, A. S., Hjorth, S. A., Inoue, A., Frimurer, T. M., Bouvier, M., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109246 · Cited by 189
Plasma Metabolome Profiling of Resistance Exercise and Endurance Exercise in Humans
Morville, T. H., Sahl, R. E., Möritz, T., Helge, J. W., & Clemmensen, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108554 · Cited by 179
Cui, H., Chen, Y., Li, K., Zhan, R., Zhao, M., Xu, Y., Lin, Z., Fu, Y., He, Q., Tang, P. C. Y., et al. (2021) · European Heart Journal · doi:10.1093/eurheartj/ehab605 · Cited by 169
Burtscher, J., Millet, G. P., Place, N., Kayser, B., & Zanou, N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126479 · Cited by 164
Heusch, G., Andreadou, I., Bell, R., Bertero, E., Bøtker, H. E., Davidson, S. M., Downey, J. M., Eaton, P., Ferdinandy, P., Gersh, B. J., et al. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102894 · Cited by 141
Huang, H., Li, G., He, Y., Chen, J., Yan, J., Zhang, Q., Li, L., & Cai, X. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1404441 · Cited by 155
Cardio-onco-metabolism: metabolic remodelling in cardiovascular disease and cancer
Karlstaedt, A., Moslehi, J. J., & de Boer, R. A. (2022) · Nature Reviews Cardiology · doi:10.1038/s41569-022-00698-6 · Cited by 130
Exercise preserves physical fitness during aging through AMPK and mitochondrial dynamics
Campos, J. C., Bozi, L. H. M., Krum, B. N., Bechara, L. R. G., Ferreira, N. D., Arini, G. S., Albuquerque, R. P. E., Traa, A., Ogawa, T., van der Bliek, A. M., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204750120 · Cited by 121
Rethinking succinate: an unexpected hormone-like metabolite in energy homeostasis
Fernández‐Veledo, S., Ceperuelo‐Mallafré, V., & Vendrell, J. J. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.06.003 · Cited by 110
Ischemia-Selective Cardioprotection by Malonate for Ischemia/Reperfusion Injury
Prag, H. A., Aksentijević, D., Dannhorn, A., Giles, A. V., Mulvey, J. F., Sauchanka, O., Du, L., Bates, G. R., Reinhold, J., Kula‐Alwar, D., et al. (2022) · Circulation Research · doi:10.1161/circresaha.121.320717 · Cited by 103
Why succinate? Physiological regulation by a mitochondrial coenzyme Q sentinel
Murphy, M. P., & Chouchani, E. T. (2022) · Nature Chemical Biology · doi:10.1038/s41589-022-01004-8 · Cited by 105
Interactions between insulin and exercise
Richter, E. A., Sylow, L., & Hargreaves, M. (2021) · Biochemical Journal · doi:10.1042/bcj20210185 · Cited by 99
Exercise-Mediated Browning of White Adipose Tissue: Its Significance, Mechanism and Effectiveness
Mu, W.-J., Zhu, J.-Y., Chen, M., & Guo, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111512 · Cited by 99
Cancer-derived extracellular succinate: a driver of cancer metastasis
Kuo, C.-C., Wu, J.-Y., & Wu, K. K. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00878-z · Cited by 107
Organism-wide, cell-type-specific secretome mapping of exercise training in mice
Wei, W., Riley, N. M., Lyu, X., Shen, X., Guo, J., Raun, S. H., Zhao, M., Moya-Garzón, M. D., Basu, H., Tung, A. S.-H., et al. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.04.011 · Cited by 101
Mitochondria as Key Players in the Pathogenesis and Treatment of Rheumatoid Arthritis
Clayton, S. A., MacDonald, L., Kurowska‐Stolarska, M., & Clark, A. R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.673916 · Cited by 100
Molecular insights of exercise therapy in disease prevention and treatment
Walzik, D., Chirino, T. Y. W., Zimmer, P., & Joisten, N. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01841-0 · Cited by 95
The Role of the Skeletal Muscle Secretome in Mediating Endurance and Resistance Training Adaptations
Leuchtmann, A. B., Adak, V., Dilbaz, S., & Handschin, C. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.709807 · Cited by 84
“, 2008) and, in muscle fibers, stimulates monocarboxylate transporter (MCT)1-facilitated, pH-gated release of succinate (Reddy et al., 2020).”
BackgroundOsuna‐Prieto, F. J., Martínez‐Téllez, B., Ortiz-Alvarez, L., Di, X., Jurado‐Fasoli, L., Xu, H., Ceperuelo‐Mallafré, V., Núñez‐Roa, C., Köhler, I., Segura‐Carretero, A., et al. (2021) · Cardiovascular Diabetology · doi:10.1186/s12933-021-01333-3 · Cited by 81
Kaneshige, A., Kaji, T., Zhang, L., Saito, H., Nakamura, A., Kurosawa, T., Ikemoto‐Uezumi, M., Tsujikawa, K., Seno, S., Hori, M., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.11.003 · Cited by 88
Villanueva-Carmona, T., Cedó, L., Madeira, A., Ceperuelo‐Mallafré, V., Rodríguez‐Peña, M., Núñez‐Roa, C., Maymó‐Masip, E., Repollés-de-Dalmau, M., Badia, J., Keiran, N., et al. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.03.004 · Cited by 84
Gudgeon, N. H., Munford, H., Bishop, E. L., Hill, J., Fulton-Ward, T., Bending, D., Roberts, J., Tennant, D. A., & Dimeloe, S. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111193 · Cited by 85
Irisin acts through its integrin receptor in a two-step process involving extracellular Hsp90α
Mu, A., Wales, T. E., Zhou, H., Draga-Coletă, S.-V., Gorgulla, C., Blackmore, K. A., Mittenbühler, M. J., Kim, C. R., Laznik-Bogoslavski, D., Zhang, Q., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.05.008 · Cited by 82
Mittenbühler, M. J., Jedrychowski, M. P., Vranken, J. G. V., Sprenger, H., Wilensky, S. E., Dumesic, P. A., Sun, Y., Tartaglia, A., Laznik-Bogoslavski, D., Mu, A., et al. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2022.12.014 · Cited by 68
Bioinspired Supramolecular Hydrogel from Design to Applications
Gao, F., Yang, X., & Song, W. (2023) · Small Methods · doi:10.1002/smtd.202300753 · Cited by 67
Differences in muscle satellite cell dynamics during muscle hypertrophy and regeneration
Fukada, S., Higashimoto, T., & Kaneshige, A. (2022) · Skeletal Muscle · doi:10.1186/s13395-022-00300-0 · Cited by 71
Carnosine regulation of intracellular pH homeostasis promotes lysosome-dependent tumor immunoevasion
Yan, R., Zhang, P., Shen, S., Zeng, Y., Wang, T., Chen, Z., Ma, W., Feng, J., Suo, C., Zhang, T., et al. (2024) · Nature Immunology · doi:10.1038/s41590-023-01719-3 · Cited by 64
Richter, E. A., Bilan, P. J., & Klip, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00033.2024 · Cited by 64
The role and therapeutic potential of stem cells in skeletal muscle in sarcopenia
Cai, Z., Liu, D., Yang, Y., Xie, W., He, M., Yu, D., Wu, Y., Wang, X., Xiao, W., & Li, Y. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02706-5 · Cited by 58
Glycolytic lactate in diabetic kidney disease
Darshi, M., Kugathasan, L., Maity, S., Sridhar, V. S., Fernandez, R. A., Limonte, C. P., Grajeda, B. I., Saliba, A., Zhang, G., Drel, V. R., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.168825 · Cited by 61
Ergothioneine controls mitochondrial function and exercise performance via direct activation of MPST
Sprenger, H., Mittenbühler, M. J., Sun, Y., Vranken, J. G. V., Schindler, S., Jayaraj, A., Khetarpal, S. A., Smythers, A. L., Vargas‐Castillo, A., Puszynska, A. M., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.01.024 · Cited by 64
Intertwined Relationship of Mitochondrial Metabolism, Gut Microbiome and Exercise Potential
Imdad, S., Lim, W., Kim, J., & Kang, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052679 · Cited by 60
Oncometabolites at the crossroads of genetic, epigenetic and ecological alterations in cancer
Lanzetti, L. (2024) · Cell Death and Differentiation · doi:10.1038/s41418-024-01402-6 · Cited by 57
Complex II Biology in Aging, Health, and Disease
Goetzman, E. S., Gong, Z., Zhang, B. B., & Muzumdar, R. H. (2023) · Antioxidants · doi:10.3390/antiox12071477 · Cited by 54
Preventing mitochondrial reverse electron transport as a strategy for cardioprotection
Prag, H. A., Murphy, M. P., & Krieg, T. (2023) · Basic Research in Cardiology · doi:10.1007/s00395-023-01002-4 · Cited by 58
Depletion of creatine phosphagen energetics with a covalent creatine kinase inhibitor
Darabedian, N., Ji, W., Fan, M., Lin, S., Seo, H., Vinogradova, E. V., Yaron, T. M., Mills, E. L., Xiao, H., Senkane, K., et al. (2023) · Nature Chemical Biology · doi:10.1038/s41589-023-01273-x · Cited by 51
Iverson, T. M., Singh, P. K., & Cecchini, G. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104761 · Cited by 57
Mitochondrial heterogeneity and adaptations to cellular needs
Granath-Panelo, M., & Kajimura, S. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01410-1 · Cited by 50
Metabolic Signatures of Performance in Elite World Tour Professional Male Cyclists
Nemkov, T. G., Cendali, F. I., Stefanoni, D., Martinez, J. L., Hansen, K. C., San-Millán, I., & D’Alessandro, A. (2023) · Sports Medicine · doi:10.1007/s40279-023-01846-9 · Cited by 48
Extracellular Succinate: A Physiological Messenger and a Pathological Trigger
Wu, K. K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241311165 · Cited by 48
Lei, I., Huang, W., Noly, P., Naik, S., Ghali, M., Liu, L., Pagani, F. D., Ela, A. S. A. A. A. E., Pober, J. S., Pitt, B., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.ade3782 · Cited by 44
Oxidative stress and metabolism meet epigenetic modulation in physical exercise
García‐Giménez, J. L., Cánovas‐Cervera, I., & Pallardó, F. V. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.01.008 · Cited by 50
An energetics perspective on geroscience: mitochondrial protonmotive force and aging
Berry, B. J., & Kaeberlein, M. R. (2021) · GeroScience · doi:10.1007/s11357-021-00365-7 · Cited by 44
The Warburg hypothesis and the emergence of the mitochondrial metabolic theory of cancer
Seyfried, T. N., Lee, D. C., Duraj, T., Ta, N. L., Mukherjee, P., Kiebish, M. A., Arismendi-Morillo, G., & Chinopoulos, C. (2025) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-025-10059-w · Cited by 45
Spontaneous hydrolysis and spurious metabolic properties of α-ketoglutarate esters
Parker, S. J., Encarnación-Rosado, J., Hollinshead, K. E. R., Hollinshead, D. M., Ash, L. J., Rossi, J. A. K., Lin, E. Y., Sohn, A. S. W., Philips, M. R., Jones, D. R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25228-9 · Cited by 43
Metabolic Signaling in Cancer Metastasis
Krieg, S., Fernandes, S. I., Kolliopoulos, C., Liu, M., & Fendt, S. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-24-0174 · Cited by 41
Architecture of the outbred brown fat proteome defines regulators of metabolic physiology
Xiao, H., Bozi, L. H. M., Sun, Y., Riley, C. L., Philip, V. M., Chen, M., Li, J., Zhang, T., Mills, E. L., Emont, M. P., et al. (2022) · Cell · doi:10.1016/j.cell.2022.10.003 · Cited by 46
Matlac, D. M., Vanova, K. H., Bechmann, N., Richter, S., Inderhees, J., Ghayee, H. K., Ge, G., Abunimer, L., WESLEY, R. A., Aherrahrou, R., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.589451 · Cited by 40
Milliken, A. S., Nadtochiy, S. M., & Brookes, P. S. (2022) · Journal of the American Heart Association · doi:10.1161/jaha.122.026135 · Cited by 41
Type 2 diabetes and succinate: unmasking an age-old molecule
Fernández‐Veledo, S., Marsal-Beltran, A., & Vendrell, J. J. (2024) · Diabetologia · doi:10.1007/s00125-023-06063-7 · Cited by 39
Malate initiates a proton-sensing pathway essential for pH regulation of inflammation
Chen, Y., Shi, R.-C., Xiang, Y.-C., Li, F., Tang, H., He, G., Zhou, M. L., Feng, X.-Z., Tan, J.-D., Huang, P., et al. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02076-9 · Cited by 39
Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice
Jiang, J., Zhou, D., Zhang, A., Yu, W., Du, L., Yuan, H., Zhang, C., Wang, Z., Jia, X., Zhang, Z., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00751-9 · Cited by 43
Monocarboxylate transporters facilitate succinate uptake into brown adipocytes
Reddy, A. J., Winther, S., Tran, N., Xiao, H., Jakob, J., Garrity, R., Smith, A., Ordonez, M., Laznik-Bogoslavski, D., Rothstein, J. D., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-00981-5 · Cited by 36
Succinate in innate immunity: linking metabolic reprogramming to immune modulation
Atallah, R., Gindlhuber, J., & Heinemann, Á. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1661948 · Cited by 41
Aging aggravates aortic aneurysm and dissection via miR-1204-MYLK signaling axis in mice
Liu, Z.-L., Li, Y., Lin, Y.-J., Shi, M., Fu, M., Li, Z., Ning, D.-S., Zeng, X.-M., Liu, X., Cui, Q.-H., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50036-2 · Cited by 38
Dietary timing enhances exercise by modulating fat-muscle crosstalk via adipocyte AMPKα2 signaling
Chen, J., Xiang, J., Zhou, M., Huang, R., Zhang, J., Cui, Y., Jiang, X., Yang, L., Zhou, R., Xin, H., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.02.007 · Cited by 35
Extrusion of mitochondria: Garbage clearance or cell–cell communication signals?
Lyamzaev, K. G., Zinovkin, R. A., & Chernyak, B. V. (2022) · Journal of Cellular Physiology · doi:10.1002/jcp.30711 · Cited by 34
Mitochondrion-targeted antioxidant SkQ1 prevents rapid animal death caused by highly diverse shocks
Skulachev, V. P., Vyssokikh, M. Y., Chernyak, B. V., Averina, O. A., Andreev-Andrievskiy, A. A., Zinovkin, R. A., Lyamzaev, K. G., Marey, M. V., Egorov, M. V., Frolova, O. J., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-31281-9 · Cited by 36
Sabadell‐Basallote, J., Astiarraga, B., Castaño, C., Ejarque, M., Repollés-de-Dalmau, M., Quesada, I., Blanco, J., Núñez‐Roa, C., Rodríguez‐Peña, M., Martínez, L., et al. (2024) · Journal of Clinical Investigation · doi:10.1172/jci173214 · Cited by 32
Zhang, Y., Gong, H., Jin, L., Liu, P., Fan, J., Qin, X., & Zheng, Q. (2025) · Redox Biology · doi:10.1016/j.redox.2025.103576 · Cited by 32
Succinate metabolism in the retinal pigment epithelium uncouples respiration from ATP synthesis
Hass, D. T., Bisbach, C. M., Robbings, B. M., Kamat, V., Sadı́lek, M., Sweet, I. R., & Hurley, J. B. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110917 · Cited by 34
High intensity muscle stimulation activates a systemic Nrf2-mediated redox stress response
Ostrom, E. L., Valencia, A. P., Marcinek, D. J., & Traustadóttir, T. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.05.039 · Cited by 31
Hoene, M., Zhao, X., Machann, J., Birkenfeld, A. L., Heni, M., Peter, A., Niess, A. M., Moller, A., Lehmann, R., Xu, G., et al. (2022) · Metabolites · doi:10.3390/metabo13010015 · Cited by 31
Monocarboxylate Transporter 1 (MCT1) Mediates Succinate Export in the Retina
Bisbach, C. M., Hass, D. T., Thomas, E. D., Cherry, T. J., & Hurley, J. B. (2022) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.63.4.1 · Cited by 30
Emerging insights into the impact of systemic metabolic changes on tumor-immune interactions
Cote, A. L., Munger, C. J., & Ringel, A. E. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115234 · Cited by 29
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
Oncometabolites in cancer: from cancer cells to the tumor microenvironment
Chen, L., & Huang, M. (2024) · Holistic Integrative Oncology · doi:10.1007/s44178-024-00096-7 · Cited by 28
Weber, D., Ferrario, P. G., & Bub, A. (2025) · Metabolomics · doi:10.1007/s11306-025-02260-0 · Cited by 27
Kim, Y.-M., Sanborn, M. A., Vijeth, S., Gajwani, P., Wang, X., Jung, D., Vályi-Nagy, T., Chakraborty, S., Mancinelli, G. E., Tóth, P. T., et al. (2025) · Nature Cancer · doi:10.1038/s43018-025-00975-6 · Cited by 28
Signals from the Circle: Tricarboxylic Acid Cycle Intermediates as Myometabokines
Maurer, J., Hoene, M., & Weigert, C. (2021) · Metabolites · doi:10.3390/metabo11080474 · Cited by 27
der Stede, T. V., Spaas, J., de Jager, S., Brandt, J. D., Hansen, C. C., Stautemas, J., Vercammen, B., Baere, S. D., Croubels, S., Assche, C. V., et al. (2023) · Acta Physiologica · doi:10.1111/apha.14020 · Cited by 27
Succinate: A Novel Mediator to Promote Atherosclerotic Lesion Progression
Zhang, S., Liang, Y., Lü, L., Chen, Y., Wu, P., & Wei, D. (2022) · DNA and Cell Biology · doi:10.1089/dna.2021.0345 · Cited by 27
The intestine is a major contributor to circulating succinate in mice
Tong, W., Hannou, S. A., Wang, Y., Astapova, I. I., Sargsyan, A., Monn, R., Thiriveedi, V., Li, D., McCann, J. R., Rawls, J. F., et al. (2022) · The FASEB Journal · doi:10.1096/fj.202200135rr · Cited by 26
Cell selectivity in succinate receptor SUCNR1 /GPR91 signaling in skeletal muscle
Abdelmoez, A. M., Dmytriyeva, O., Zurke, Y.-X., Trauelsen, M., Marica, A. A., Savikj, M., Smith, J. A. B., Monaco, C. G., Schwartz, T. W., Krook, A., et al. (2023) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00009.2023 · Cited by 25
The blood–brain barrier—a metabolic ecosystem
Castro, M., & Potente, M. (2022) · The EMBO Journal · doi:10.15252/embj.2022111189 · Cited by 24
der Stede, T. V., de Loock, A. V., Turiel, G., Hansen, C. C., Tamariz‐Ellemann, A., Ullrich, M., Lievens, E., Spaas, J., Yigit, N., Anckaert, J., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2024.12.011 · Cited by 26
Xu, G., Yuan, Y., Luo, P., Yang, J., Zhou, J., Zhu, C., Jiang, Q., & Shu, G. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2021.808863 · Cited by 24
Exercise and Metabolic Health: The Emerging Roles of Novel Exerkines
Yazgan, B., Türkel, İ., Özerkliğ, B., ATAKAN, M. M., Aktitiz, S., & Koşar, Ş. N. (2022) · Current Protein and Peptide Science · doi:10.2174/1389203723666220629163524 · Cited by 25
Exercise-Induced Adipose Tissue Thermogenesis and Browning: How to Explain the Conflicting Findings?
Zhu, Y., Qi, Z., & Ding, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113142 · Cited by 27
Acetate and succinate benefit host muscle energetics as exercise‐associated post‐biotics
Ismaeel, A., Valentino, T. R., Burke, B. I., Goh, J. Z., Saliu, T. P., Albathi, F. A., Owen, A. M., McCarthy, J. J., & Wen, Y. (2023) · Physiological Reports · doi:10.14814/phy2.15848 · Cited by 26
Succinate-SUCNR1 induces renal tubular cell apoptosis
Pu, M., Zhang, J., Zeng, Y., Hong, F., Qi, W., Yang, X., Gao, G., & Zhou, T. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00327.2022 · Cited by 25
Casas-Benito, A., Martínez-Herrero, S., & Martínez, A. (2023) · Cancers · doi:10.3390/cancers15102862 · Cited by 26
Basic Mechanisms of Immunometabolites in Shaping the Immune Response
Ryan, D. G., Peace, C. G., & Hooftman, A. (2023) · Journal of Innate Immunity · doi:10.1159/000535452 · Cited by 22
Need for speed: Human fast-twitch mitochondria favor power over efficiency
Edman, S., Flockhart, M., Larsen, F. J., & Apró, W. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101854 · Cited by 25
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
A primer on global molecular responses to exercise in skeletal muscle: Omics in focus
Murach, K. A., & Bagley, J. R. (2025) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2025.101029 · Cited by 22
Targeting Mitochondria for Cancer Treatment
Zorova, L. D., Abramicheva, P. A., Andrianova, N. V., Babenko, V. A., Zorov, S. D., Pevzner, I. B., Popkov, V. A., Semenovich, D. S., Yakupova, E. I., Silachev, D. N., et al. (2024) · Pharmaceutics · doi:10.3390/pharmaceutics16040444 · Cited by 23
Acyl post-translational modification of proteins by metabolites in cancer cells
Wang, X., Guo, Y., Fu, Y., Zhang, C., Chen, W., Tang, X. T., Yu, Y., Chen, Y., Ding, G., & Zhang, J. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02535-4 · Cited by 20
Sweeney, H. L., Masiero, S., & Carraro, U. (2022) · European Journal of Translational Myology · doi:10.4081/ejtm.2022.10440 · Cited by 19
Gas regulation of complex II reversal via electron shunting to fumarate in the mammalian ETC
Banerjee, R. V., & Kumar, R. (2022) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2022.03.011 · Cited by 19
Metadata
- 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 (medical) › 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
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
