Genes controlling skeletal muscle glucose uptake and their regulation by endurance and resistance exercise
Open accessAbstract
Exercise improves the insulin sensitivity of glucose uptake in skeletal muscle. Due to that, exercise has become a cornerstone treatment for type 2 diabetes mellitus (T2DM). The mechanisms by which exercise improves skeletal muscle insulin sensitivity are, however, incompletely understood. We conducted a systematic review to identify all genes whose gain or loss of function alters skeletal muscle glucose uptake. We subsequently cross‐referenced these genes with recently generated data sets on exercise‐induced gene expression and signaling. Our search revealed 176 muscle glucose‐uptake genes, meaning that their genetic manipulation altered glucose uptake in skeletal muscle. Notably, exercise regulates the expression or phosphorylation of more than 50% of the glucose‐uptake genes or their protein products. This included many genes that previously have not been associated with exercise‐induced insulin sensitivity. Interestingly, endurance and resistance exercise triggered some common but mostly unique changes in expression and phosphorylation of glucose‐uptake genes or their protein products. Collectively, our work provides a resource of potentially new molecular effectors that play a role in the incompletely understood regulation of muscle insulin sensitivity by exercise.
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
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?
Systematic search found that transgenesis of Mstn, Foxc2, Fst, Ccn5, Cpt1b, Hdac3, Insr, Steap4, Igfbp3, Tnfsf11, Inpp5k, and Nos2 affects both skeletal muscle glucose uptake and promotes skeletal muscle hypertrophy in mice, confirming an overlap of underlying regulatory mechanisms.
“We found that the transgenesis of Mstn, Foxc2, Fst, Ccn5, Cpt1b, Hdac3, Insr, Steap4, Igfbp3, Tnfsf11, Inpp5k, and Nos2 affects both skeletal muscle glucose uptake and promotes skeletal muscle hypertrophy in mice, confirming an overlap of the underlying regulatory mechanisms.”
From Effects of Skeletal Muscle Hypertrophy on Fat Mass and Glucose Homeostasis in Humans and Animals: A Narrative Review with Systematic Literature Search (2025) · cites this paper as [177]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042 · see citing works
Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin
(2002) · New England Journal of Medicine · doi:10.1056/nejmoa012512 · Cited by 19,011 · cited 5× · see citing works
“16–19 In fact, these glucometabolic benefits of exercise are greater than those achieved by metformin, a widely prescribed antidiabetic drug in patients with T2DM.(20) The implications of this are important, because it indicates that the molecular mechanisms that underpin exercise‐induced skeletal muscle insulin sensi…”
BackgroundInfluentialRegulation of skeletal muscle mass in mice by a new TGF-p superfamily member
McPherron, A. C., Lawler, A. M., & Lee, S.-J. (1997) · Nature · doi:10.1038/387083a0 · Cited by 4,013 · see citing works
Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr
Janssen, I., Heymsfield, S. B., Wang, Z., & Ross, R. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.89.1.81 · Cited by 3,087 · see citing works
Utilization of the PICO framework to improve searching PubMed for clinical questions
Schardt, C., Adams, M. B., Owens, T., Keitz, S., & Fontelo, P. (2007) · BMC Medical Informatics and Decision Making · doi:10.1186/1472-6947-7-16 · Cited by 3,053 · see citing works
The Triumvirate: β-Cell, Muscle, Liver: A Collusion Responsible for NIDDM
DeFronzo, R. A. (1988) · Diabetes · doi:10.2337/diab.37.6.667 · Cited by 2,456 · see citing works
Skeletal Muscle Insulin Resistance Is the Primary Defect in Type 2 Diabetes
DeFronzo, R. A., & Tripathy, D. (2009) · Diabetes Care · doi:10.2337/dc09-s302 · Cited by 2,102 · cited 1× · see citing works
“Chronic skeletal muscle insulin resistance, therefore, strains the β‐cells of the pancreas and is considered a key risk factor for developing type 2 diabetes mellitus (T2DM).(4) Exercise increases glucose uptake into skeletal muscle of healthy and diabetic individuals.”
BackgroundBoulé, N. G., Haddad, E., Kenny, G. P., Wells, G. A., & Sigal, R. J. (2001) · JAMA · doi:10.1001/jama.286.10.1218 · Cited by 1,889 · see citing works
Aune, D., Norat, T., Leitzmann, M., Tonstad, S., & Vatten, L. J. (2015) · European Journal of Epidemiology · doi:10.1007/s10654-015-0056-z · Cited by 880 · see citing works
The Steap proteins are metalloreductases
Ohgami, R. S., Campagna, D. R., McDonald, A., & Fleming, M. D. (2006) · Blood · doi:10.1182/blood-2006-02-003681 · Cited by 744 · see citing works
Protein Phosphorylation: A Major Switch Mechanism for Metabolic Regulation
Humphrey, S. J., James, D. E., & Mann, M. (2015) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2015.09.013 · Cited by 554 · see citing works
Effective exercise modality to reduce insulin resistance in women with type 2 diabetes
Cuff, D. J., Meneilly, G. S., Martin, A., Ignaszewski, A., Tildesley, H. D., & Frohlich, J. J. (2003) · Diabetes Care · doi:10.2337/diacare.26.11.2977 · Cited by 545 · see citing works
Effect of physical exercise on sensitivity and responsiveness to insulin in humans
Mikines, K. J., Sonne, B., Farrell, P. A., Tronier, B., & Galbo, H. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.254.3.e248 · Cited by 538 · see citing works
Muscle Glucose Metabolism following Exercise in the Rat
Richter, E. A., Garetto, L. P., Goodman, M. N., & Ruderman, N. B. (1982) · Journal of Clinical Investigation · doi:10.1172/jci110517 · Cited by 510 · see citing works
Exercise-stimulated glucose uptake — regulation and implications for glycaemic control
Sylow, L., Kleinert, M., Richter, E. A., & Jensen, T. E. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.162 · Cited by 498 · see citing works
Self-citationHuman variation in skeletal muscle fiber-type proportion and enzyme activities
Simoneau, J. A., & Bouchard, C. (1989) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1989.257.4.e567 · Cited by 484 · see citing works
Feder, J. N., Tsuchihashi, Z., Irrinki, A., Lee, V. K., Mapa, F. A., Morikang, E., Prass, C. E., Starnes, S. M., Wolff, R. K., Parkkila, S., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.22.14025 · Cited by 471 · see citing works
Transcriptomic profiling of skeletal muscle adaptations to exercise and inactivity
Pillon, N. J., Gabriel, B. M., Dollet, L., Smith, J. A. B., Sardón Puig, L., Botella, J., Bishop, D. J., Krook, A., & Zierath, J. R. (2020) · Nature Communications · doi:10.1038/s41467-019-13869-w · Cited by 457 · see citing works
Self-citationHoffman, N. J., Parker, B. L., Chaudhuri, R., Fisher-Wellman, K. H., Kleinert, M., Humphrey, S. J., Yang, P., Holliday, M., Trefely, S., Fazakerley, D. J., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.09.001 · Cited by 426 · see citing works
Self-citationPospisilik, J. A., Knauf, C., Joza, N., Benit, P., Orthofer, M., Cani, P. D., Ebersberger, I., Nakashima, T., Sarao, R., Neely, G., et al. (2007) · Cell · doi:10.1016/j.cell.2007.08.047 · Cited by 404 · see citing works
Guo, T., Jou, W., Chanturiya, T., Portas, J., Gavrilova, O., & McPherron, A. C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004937 · Cited by 402 · see citing works
Considerations in the Design of Hyperinsulinemic-Euglycemic Clamps in the Conscious Mouse
Ayala, J. E., Bracy, D. P., McGuinness, O. P., & Wasserman, D. H. (2006) · Diabetes · doi:10.2337/diabetes.55.02.06.db05-0686 · Cited by 399 · see citing works
Insulin signaling and insulin sensitivity after exercise in human skeletal muscle
Wojtaszewski, J. F., Hansen, B. F., Gade, Kiens, B., Markuns, J. F., Goodyear, L. J., & Richter, E. A. (2000) · Diabetes · doi:10.2337/diabetes.49.3.325 · Cited by 382 · see citing works
The many actions of insulin in skeletal muscle, the paramount tissue determining glycemia
Sylow, L., Tokarz, V. L., Richter, E. A., & Klip, A. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.03.020 · Cited by 366 · see citing works
Effect of exercise on insulin action in human skeletal muscle
Richter, E. A., Mikines, K. J., Galbo, H., & Kiens, B. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.66.2.876 · Cited by 357 · see citing works
Enhanced Peripheral and Splanchnic Insulin Sensitivity in NIDDM Men After Single Bout of Exercise
Devlin, J. T., Hirshman, M., Horton, E. D., & Horton, E. S. (1987) · Diabetes · doi:10.2337/diab.36.4.434 · Cited by 342 · see citing works
RANKL inhibition improves muscle strength and insulin sensitivity and restores bone mass
Bonnet, N., Bourgoin, L., Biver, E., Douni, E., & Ferrari, S. (2019) · Journal of Clinical Investigation · doi:10.1172/jci125915 · Cited by 314 · see citing works
van der Berg, J. D., Stehouwer, C. D. A., Bosma, H., van der Velde, J. H. P. M., Willems, P. J. B., Savelberg, H. H. C. M., Schram, M. T., Sep, S. J. S., van der Kallen, C. J. H., Henry, R. M. A., et al. (2016) · Diabetologia · doi:10.1007/s00125-015-3861-8 · Cited by 299 · see citing works
Dela, F., Larsen, J. J., Mikines, K. J., Ploug, T., Petersen, L. N., & Galbo, H. (1995) · Diabetes · doi:10.2337/diab.44.9.1010 · Cited by 286 · see citing works
Update on GLUT4 Vesicle Traffic: A Cornerstone of Insulin Action
Jaldín‐Fincati, J. R., Pavarotti, M. A., Frendo‐Cumbo, S., Bilan, P. J., & Klip, A. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.05.002 · Cited by 276 · see citing works
Schwingshackl, L., Missbach, B., Dias, S., König, J., & Hoffmann, G. (2014) · Diabetologia · doi:10.1007/s00125-014-3303-z · Cited by 264 · see citing works
Effect of muscle glycogen depletion on in vivo insulin action in man.
Bogardus, C., Thuillez, P., Ravussin, É., Vasquez, B., Narimiga, M., & Azhar, S. (1983) · Journal of Clinical Investigation · doi:10.1172/jci111119 · Cited by 252 · see citing works
Muscle-Specific Pten Deletion Protects against Insulin Resistance and Diabetes
Wijesekara, N., Konrad, D., Eweida, M., Jefferies, C., Liadis, N., Giacca, A., Crackower, M. A., Suzuki, A., Mak, T. W., Kahn, C. R., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.3.1135-1145.2005 · Cited by 237 · see citing works
Cytosolic ROS production by NADPH oxidase 2 regulates muscle glucose uptake during exercise
Henríquez-Olguin, C., Knudsen, J. R., Raun, S. H., Li, Z., Dalbram, E., Treebak, J. T., Sylow, L., Holmdahl, R., Richter, E. A., Jaimovich, E., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12523-9 · Cited by 228 · see citing works
Wellen, K. E., Fucho, R., Gregor, M. F., Furuhashi, M., Morgan, C., Lindstad, T., Vaillancourt, E., Gorgun, C. Z., Saatcioglu, F., & Hotamisligil, G. S. (2007) · Cell · doi:10.1016/j.cell.2007.02.049 · Cited by 222 · see citing works
Lack of the architectural factor HMGA1 causes insulin resistance and diabetes in humans and mice
FOTI, D. P., CHIEFARI, E. D., Fedele, M., Iuliano, R., Brunetti, L., Paonessa, F., Manfioletti, G., Barbetti, F., Brunetti, A., Croce, C. M., et al. (2005) · Nature Medicine · doi:10.1038/nm1254 · Cited by 221 · see citing works
Effects of Prior High-Intensity Exercise on Glucose Metabolism in Normal and Insulin-resistant Men
Devlin, J. T., & Horton, E. S. (1985) · Diabetes · doi:10.2337/diab.34.10.973 · Cited by 207 · see citing works
Human Muscle Fiber Type–Specific Insulin Signaling: Impact of Obesity and Type 2 Diabetes
Albers, P. H., Pedersen, A. J. T., Birk, J. B., Steenberg, D. E., Vind, B. F., Baba, O., Nøhr, J., Højlund, K., & Wojtaszewski, J. F. P. (2014) · Diabetes · doi:10.2337/db14-0590 · Cited by 204 · see citing works
Single muscle fiber proteomics reveals unexpected mitochondrial specialization
Murgia, M., Nagaraj, N., Deshmukh, A. S., Zeiler, M., Cancellara, P., Moretti, I., Reggiani, C., Schiaffino, S., & Mann, M. (2015) · EMBO Reports · doi:10.15252/embr.201439757 · Cited by 202 · see citing works
Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity
Chadt, A., Leicht, K., Deshmukh, A. S., Jiang, L. Q., Scherneck, S., Bernhardt, U., Dreja, T., Vogel, H., Schmolz, K., Kluge, R., et al. (2008) · Nature Genetics · doi:10.1038/ng.244 · Cited by 201 · see citing works
Enhanced muscle glucose metabolism after exercise: modulation by local factors
Richter, E. A., Garetto, L. P., Goodman, M. N., & Ruderman, N. B. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.246.6.e476 · Cited by 194 · see citing works
Resistance Training and Type 2 Diabetes
Eves, N. D., & Plotnikoff, R. C. (2006) · Diabetes Care · doi:10.2337/dc05-1981 · Cited by 190 · see citing works
Boulé, N. G., Haddad, E., Kenny, G. P., Wells, G. A., & Sigal, R. J. (2002) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1034/j.1600-0838.2002.120111_3.x · Cited by 188 · see citing works
Gsh‐1, an orphan Hox gene, is required for normal pituitary development.
Li, H., Zeitler, P. S., Valerius, M. T., Small, K. M., & Potter, S. S. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00407.x · Cited by 171 · see citing works
Farese, R. V., Sajan, M. P., Yang, H., Li, P., Mastorides, S., Gower, W. R., Nimal, S., Choi, C. S., Kim, S., Shulman, G. I., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31408 · Cited by 169 · see citing works
Deshmukh, A. S., Steenberg, D. E., Hostrup, M., Birk, J. B., Larsen, J. K., Santos, A., Kjøbsted, R., Hingst, J. R., Schéele, C., Murgia, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20556-8 · Cited by 169 · see citing works
Roles of TBC1D1 and TBC1D4 in insulin- and exercise-stimulated glucose transport of skeletal muscle
Cartee, G. D. (2014) · Diabetologia · doi:10.1007/s00125-014-3395-5 · Cited by 153 · see citing works
Rac1 Is a Novel Regulator of Contraction-Stimulated Glucose Uptake in Skeletal Muscle
Sylow, L., Jensen, T. E., Kleinert, M., Mouatt, J. R., Maarbjerg, S., Jeppesen, J. F., Prats, C., Chiu, T. T., Boguslavsky, S., Klip, A., et al. (2012) · Diabetes · doi:10.2337/db12-0491 · Cited by 143 · see citing works
Self-citationGlucoregulatory and metabolic response to exercise in obese noninsulin-dependent diabetes
Minuk, H. L., Vranic, M., Marliss, E. B., Hanna, A. K., Albisser, A. M., & Zinman, B. (1981) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1981.240.5.e458 · Cited by 142 · see citing works
van Dijk, J., MANDERS, R. J. F., Tummers, K., Bonomi, A. G., Stehouwer, C. D. A., Hartgens, F., & van Loon, L. J. C. (2011) · Diabetologia · doi:10.1007/s00125-011-2380-5 · Cited by 139 · see citing works
FOTI, D. P., Iuliano, R., CHIEFARI, E. D., & Brunetti, A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.8.2720-2732.2003 · Cited by 135 · see citing works
Increased Muscle Glucose Uptake After Exercise: No Need for Insulin During Exercise
Richter, E. A., Ploug, T., & Galbo, H. (1985) · Diabetes · doi:10.2337/diab.34.10.1041 · Cited by 135 · see citing works
Kjøbsted, R., Treebak, J. T., Fentz, J., Lantier, L., Viollet, B., Birk, J. B., Schjerling, P., Björnholm, M., Zierath, J. R., & Wojtaszewski, J. F. P. (2014) · Diabetes · doi:10.2337/db14-1402 · Cited by 135 · see citing works
Ryder, J. W., Bassel‐Duby, R., Olson, E. N., & Zierath, J. R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304510200 · Cited by 130 · see citing works
Nielsen, J., Holmberg, H., Schrøder, H. D., Saltin, B., & Ørtenblad, N. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.204487 · Cited by 122 · see citing works
Keller, S. R., Davis, A. C., & Clairmont, K. B. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202037200 · Cited by 121 · see citing works
Chutkow, W. A., Samuel, V. T., Hansen, P. A., Pu, J., Valdivia, C. R., Makielski, J. C., & Burant, C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.201390398 · Cited by 117 · see citing works
Chemello, F., Bean, C., Cancellara, P., Laveder, P., Reggiani, C., & Lanfranchi, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016807 · Cited by 114 · see citing works
Dissociation of muscle insulin sensitivity from exercise endurance in mice by HDAC3 depletion
Hong, S., Zhou, W., Fang, B., Lu, W., Loro, E., Damle, M., Ding, G., Jager, J., Zhang, S., Zhang, Y., et al. (2016) · Nature Medicine · doi:10.1038/nm.4245 · Cited by 110 · see citing works
Functional Variants of the HMGA1 Gene and Type 2 Diabetes Mellitus
CHIEFARI, E. D. (2011) · JAMA · doi:10.1001/jama.2011.207 · Cited by 96 · see citing works
Impaired glucose homeostasis in insulin-like growth factor-binding protein-3-transgenic mice
Silha, J. V., Gui, Y., & Murphy, L. J. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00014.2002 · Cited by 96 · see citing works
Horst, A. K. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24340 · Cited by 92 · see citing works
Overexpression of Hexokinase II in Transgenic Mice
Chang, P., Jensen, J., Printz, R., Granner, D., Ivy, J., & Moller, D. E. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.25.14834 · Cited by 91 · see citing works
Hamada, T., Arias, E. B., & Cartee, G. D. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00416.2006 · Cited by 84 · see citing works
Is GLUT4 translocation the answer to exercise-stimulated muscle glucose uptake?
Richter, E. A. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00503.2020 · Cited by 82 · see citing works
Nelson, M. E., Parker, B. L., Burchfield, J. G., Hoffman, N. J., Needham, E. J., Cooke, K. C., Naim, T., Sylow, L., Ling, N. X. Y., Francis, D., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2019102578 · Cited by 81 · see citing works
The Rab-GTPase-activating protein TBC1D1 regulates skeletal muscle glucose metabolism
Szekeres, F. L. M., Chadt, A., Tom, R. Z., Deshmukh, A. S., Chibalin, A., Björnholm, M., Al‐Hasani, H., & Zierath, J. R. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00605.2011 · Cited by 76 · see citing works
Ropelle, E. R., Pauli, J. R., Cintra, D. E., da Silva, A. S. R., de Souza, C. T., Guadagnini, D., Carvalho, B. M., Caricilli, A. M., Katashima, C. K., Filho, C., et al. (2012) · Diabetes · doi:10.2337/db12-0339 · Cited by 73 · see citing works
Han, X., Møller, L. L. V., Groote, E. D., Bojsen-Møller, K. N., Davey, J. R., Henríquez‐Olguín, C., Li, Z., Knudsen, J. R., Jensen, T. E., Madsbad, S., et al. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12474 · Cited by 73 · see citing works
Kim, J. K., Kim, H., Park, S., Cederberg, A., Westergren, R., Nilsson, D., Higashimori, T., Cho, Y.-R., Liu, Z., Dong, J., et al. (2005) · Diabetes · doi:10.2337/diabetes.54.6.1657 · Cited by 72 · see citing works
Vigliottá, G., Miele, C., Santopietro, S., Portella, G., Perfetti, A., Maitan, M. A., Cassese, A., Oriente, F., Trencia, A., Fiory, F., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.11.5005-5015.2004 · Cited by 72 · see citing works
Iron Metabolism of the Skeletal Muscle and Neurodegeneration
Hałoń, M., Borkowska, A., Herman-Antosiewicz, A., & Antosiewicz, J. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00165 · Cited by 69 · see citing works
Transcriptional Regulation of Glucose Metabolism: The Emerging Role of the HMGA1 Chromatin Factor
CHIEFARI, E. D., FOTI, D. P., Sgarra, R., Pegoraro, S., Arcidiacono, B., Brunetti, F. S., Greco, M., Manfioletti, G., & Brunetti, A. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00357 · Cited by 65 · see citing works
Increased Insulin Action in SKIP Heterozygous Knockout Mice
Ijuin, T., Yu, Y. E., Mizutani, K., Pao, A., Tateya, S., Tamori, Y., Bradley, A., & Takenawa, T. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01990-06 · Cited by 61 · see citing works
Moller, D. E., Chang, P.-Y., Yaspelkis, B. B., Flier, J. S., Wallberg‐Henriksson, H., & Ivy, J. L. (1996) · Endocrinology · doi:10.1210/endo.137.6.8641192 · Cited by 58 · see citing works
Fatone, C., Guescini, M., Balducci, S., Battistoni, S., Settequattrini, A., Pippi, R., Stocchi, L., Mantuano, M., Stocchi, V., & De Feo, P. (2010) · Journal of Endocrinological Investigation · doi:10.1007/bf03346630 · Cited by 54 · see citing works
Functional limitations to glucose uptake in muscles comprised of different fiber types
Halseth, A. E., Bracy, D. P., & Wasserman, D. H. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.6.e994 · Cited by 51 · see citing works
Interleukin-6 mediates exercise-induced increase in insulin sensitivity in mice
Benrick, A., Wallenius, V., & Asterholm, I. W. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2012.065508 · Cited by 49 · see citing works
Transcriptomic Profiling of Skeletal Muscle Adaptations to Exercise and InactivityPreprint
Pillon, N. J., Gabriel, B. M., Dollet, L., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/813048 · Cited by 48 · see citing works
Self-citationHokken, R., Laugesen, S., Aagaard, P., Suetta, C., Frandsen, U., Ørtenblad, N., & Nielsen, J. (2020) · Acta Physiologica · doi:10.1111/apha.13561 · Cited by 45 · see citing works
Ilany, J., Bilan, P. J., Kapur, S., Caldwell, J. S., Patti, M., Marette, A., & Kahn, C. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511246103 · Cited by 44 · see citing works
Muddle, T. W. D., Colquhoun, R. J., Magrini, M. A., Luera, M. J., DeFreitas, J. M., & Jenkins, N. D. M. (2018) · Physiological Reports · doi:10.14814/phy2.13675 · Cited by 41 · see citing works
Kim, T. (2014) · Journal of Diabetes & Metabolism · doi:10.4172/2155-6156.1000401 · Cited by 40 · see citing works
Verbrugge, S. A. J., Gehlert, S., Stadhouders, L. E. M., Jacko, D., Aussieker, T., de Wit, G. M. J., Vogel, I. S. P., Offringa, C., Schönfelder, M., Jaspers, R. T., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197062 · Cited by 39 · see citing works
Self-citationFritah, A., Steel, J. H., Parker, N., Nikolopoulou, E., Christian, M., Carling, D., & Parker, M. G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032520 · Cited by 35 · see citing works
Fiber type-specific determinants ofVmaxfor insulin-stimulated muscle glucose uptake in vivo
Petersen, H. A., Fueger, P. T., Bracy, D. P., Wasserman, D. H., & Halseth, A. E. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00323.2002 · Cited by 35 · see citing works
Grünberg, J. R., Hoffmann, J. M., Hedjazifar, S., Nerstedt, A., Jenndahl, L. E., Elvin, J., Castellot, J. J., Wei, L., Movérare‐Skrtic, S., Ohlsson, C., et al. (2017) · Scientific Reports · doi:10.1038/srep43515 · Cited by 34 · see citing works
Fukatsu, Y., Noguchi, T., Hosooka, T., Ogura, T., Kotani, K., Abe, T., Shibakusa, T., Inoue, K., Sakai, M., Tobimatsu, K., et al. (2009) · Endocrinology · doi:10.1210/en.2008-1647 · Cited by 33 · see citing works
Effects of anaesthesia on insulin sensitivity and metabolic parameters in Wistar rats.
Guarino, M. P., Santos, A. I., Carmo, M. M., & Costa, P. F. (2013) · PubMed · Cited by 30 · see citing works
BIG3 inhibits insulin granule biogenesis and insulin secretion
Li, H., Wei, S., Cheng, K. K. Y., Gounko, N. V., Ericksen, R. E., Xu, A., Hong, W., & Han, W. (2014) · EMBO Reports · doi:10.1002/embr.201338181 · Cited by 29 · see citing works
Cytosolic ROS production by NADPH oxidase 2 regulates muscle glucose uptake during exercisePreprint
Henríquez‐Olguín, C., Knudsen, J. R., Raun, S. H., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/522805 · Cited by 26 · see citing works
BMP4 gene therapy enhances insulin sensitivity but not adipose tissue browning in obese mice
Hoffmann, J. M., Grünberg, J. R., Hammarstedt, A., Kroon, T., Greiner, T. U., Maurer, S., Elias, I., Pálsdóttir, V., Bosch, F., Boucher, J., et al. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.11.016 · Cited by 26 · see citing works
Minnock, D., Annibalini, G., le Roux, C. W., Contarelli, S., Krause, M. D. S., Saltarelli, R., Valli, G., Stocchi, V., Barbieri, E., & VITO, G. D. (2020) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04491-6 · Cited by 23 · see citing works
Serup, A. K., Alsted, T. J., Jordy, A. B., Schjerling, P., Holm, C., & Kiens, B. (2016) · Diabetes · doi:10.2337/db16-0655 · Cited by 21 · see citing works
Suginohara, T., Wakabayashi, K., Ato, S., & Ogasawara, R. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154419 · Cited by 20 · see citing works
Iso, T., Haruyama, H., Sunaga, H., Matsui, H., Matsui, M., Tanaka, R., Umbarawan, Y., Syamsunarno, M. R. A. A., Putri, M., Yamaguchi, A., et al. (2018) · Physiological Reports · doi:10.14814/phy2.13884 · Cited by 15 · see citing works
Hanaoka, Y., Yasuda, O., Soejima, H., Miyata, K., Yamamoto, E., Izumiya, Y., Maeda, N., Ohishi, M., Rakugi, H., Oike, Y., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094930 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dergaa, I., Saad, H. B., Omri, A. E., Glenn, J. M., Clark, C. C. T., Washif, J. A., Guelmami, N., Hammouda, O., Al-Horani, R., Reynoso-Sánchez, L. F., et al. (2023) · Biology of Sport · doi:10.5114/biolsport.2024.133661 · Cited by 133 · see citing works
Richter, E. A., Bilan, P. J., & Klip, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00033.2024 · Cited by 64 · see citing works
Peifer‐Weiß, L., Al‐Hasani, H., & Chadt, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031910 · Cited by 34 · see citing works
Gao, Y., Li, Q.-H., Finni, T. J., & Pesola, A. J. (2024) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.14628 · Cited by 22 · see citing works
Havers, T., Held, S., Schönfelder, M., Geisler, S., & Wackerhage, H. (2025) · Sports Medicine · doi:10.1007/s40279-025-02263-w · Cited by 19 · see citing works
“To identify genes and proteins that contribute to glucose uptake and muscle hypertrophy, we have systematically searched the literature for genes whose transgenesis increases glucose uptake [177] or causes skeletal muscle hypertrophy [32].”
Self-citationGhanemi, A., Yoshioka, M., & St‐Amand, J. (2023) · Diseases · doi:10.3390/diseases11010033 · Cited by 17 · see citing works
Electromyography of Sedentary Behavior: Identifying Potential for Cardiometabolic Risk Reduction
Lamberg, S., Brakenridge, C. J., Dunstan, D. W., Finni, T. J., Healy, G. N., Owen, N. G., & Pesola, A. J. (2024) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003544 · Cited by 11 · see citing works
Kuhnen, G., Russomanno, T. G., Murgia, M., Pillon, N. J., Schönfelder, M., & Wackerhage, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232112933 · Cited by 11 · see citing works
Self-citationGao, H., Ma, X., Wang, Z., Zhu, D., Guo, Y., Zhao, L., & Xiao, W. (2025) · Cells · doi:10.3390/cells14131026 · Cited by 8 · see citing works
Exercise-induced intertissue communication: adipose tissue and the heart
Blackwell, J. A., & Stanford, K. I. (2022) · Current Opinion in Physiology · doi:10.1016/j.cophys.2022.100626 · Cited by 6 · see citing works
Tsuneki, H., Sugiyama, M., Sato, K., Ito, H., Nagai, S., Kon, K., Wada, T., Kobayashi, N., Okada, T., Toyooka, N., et al. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.176190 · Cited by 6 · see citing works
Kim, C., Park, D., Lee, Y.-J., Kim, E., Oh, C.-G., Lee, D. H., & Jeon, J. Y. (2025) · Age and Ageing · doi:10.1093/ageing/afaf109 · Cited by 5 · see citing works
Sambashivaiah, S., Bhadra, R., Bhattacharya, S., & Kurpad, A. (2023) · Journal of the Indian Institute of Science · doi:10.1007/s41745-022-00349-2 · Cited by 3 · see citing works
Estrogen deficiency induces pelvic floor muscle atrophy via ERα/GLUT4 pathway
Huang, X., Zhou, M., Wang, Y., Chen, M., Xiao, Y., Li, L., Zhu, F., Chen, L., Tian, X., Wu, S., et al. (2026) · PLoS ONE · doi:10.1371/journal.pone.0349371 · Cited by 2 · see citing works
Kuhnen, G., Russomanno, T. G., Murgia, M., Pillon, N. J., Schönfelder, M., & Wackerhage, H. (2022) · Research Square · doi:10.21203/rs.3.rs-1519277/v1 · Cited by 2 · see citing works
Self-citationLin, W., & Hsu, T. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.149494 · Cited by 1 · see citing works
de Paiva, P. D. C., Marinho, T. D. S., Mandarim‐de‐Lacerda, C. A., & Águila, M. B. (2023) · International Journal of Morphology · doi:10.4067/s0717-95022023000200591
Apaflo, J. N., Narvaez, G. A., Tomy, I. J., Mossayebi, A., Fatahimeiabadi, Z., McAinch, A. J., Thyfault, J. P., Min, K., Jung, H., Wagler, A. E., et al. (2025) · European Journal of Applied Physiology · doi:10.1007/s00421-025-05907-x
Akar, E. A. (2022) · theses.fr (ABES) · doi:10.70675/a7b15e3fz84e7z4915z9447zc112181e06e4
Bhattacharjee, B., Maity, M., Bhowmick, S., Chaudhuri, T., Deb, P., Raza, A. M., & Ghosh, D. (2026) · Lecture notes in networks and systems · doi:10.1007/978-3-032-25955-4_42
Skeletal muscle biomass as an underappreciated fate of glucose
Wackerhage, H., Eggelbusch, M., Hulmi, J. J., & Mäntyselkä, S. (2026) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00295.2026
Self-citation
- Authors
- Verbrugge, S. A. J., Alhusen, J. A., Kempin, S., Pillon, N. J., Rozman, J., Wackerhage, H., & Kleinert, M.
- Affiliations
- Helmholtz Munich (DE)
- Technical University of Munich (DE)
- Karolinska Institutet (SE)
- Czech Academy of Sciences, Institute of Molecular Genetics (CZ)
- University of Copenhagen (DK)
- Corresponding author
- Verbrugge, Sander A. J.
- Wackerhage, Henning
- Kleinert, Maximilian
- ORCID
- Venue
- Journal of Cellular Biochemistry
- Publisher
- Wiley
- Published
- 2021-11-23
- Volume
- 123
- Issue
- 2
- Pages
- 202-214
- ISSN
- 0730-2312 (ISSN-L)
- 1097-4644
- OpenAlex
- W3216751011
- Cited by
- 21
- References
- 96
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 4
- FWCI
- 0.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Cellular Biochemistry (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc-nd)
- Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by-nc-nd)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
- Site cant be reached (submittedVersion, cc-by-nc-nd)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (KL 3285/2‐1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- skeletal muscle glucose uptake, insulin sensitivity, type 2 diabetes, endurance exercise, resistance training, exercise-induced gene expression, protein phosphorylation, genetic engineering
- MeSH terms
- Animals, Blood Glucose, Diabetes Mellitus, Type 2, Humans, Insulin Resistance, Physical Endurance, Muscle, Skeletal, Resistance Training
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