Additive effect of contractions and insulin on GLUT-4 translocation into the sarcolemma
Abstract
The maximal effects of insulin and muscle contractions on glucose transport are additive. GLUT-4 is the major glucose transporter isoform expressed in skeletal muscle. Muscle contraction and insulin each induce translocation of GLUT-4 from intracellular sites into the plasma membrane. The purpose of this study was to test the hypothesis that the incremental effect of contractions and insulin on glucose transport is mediated by additivity of the maximal effects of these stimuli on GLUT-4 translocation into the sarcolemma. Anesthetized rats were given insulin by intravenous infusion to raise plasma insulin to 2,635 +/- 638 microU/ml. The gastrocnemius-plantaris-soleus group was stimulated to contract via the sciatic nerve by using a protocol that maximally activates glucose transport. After treatment with insulin, contractions, or insulin plus contractions or no treatment, the gastrocnemius-plantaris-soleus muscle group was dissected out and was subjected to subcellular fractionation to separate the plasma membrane and intracellular membrane fractions. Insulin induced a 70% increase and contractions induced a 113% increase in the GLUT-4 content of the plasma membrane fraction. The effects of insulin and contractions were additive, as evidenced by a 185% increase in the GLUT-4 content of the sarcolemmal fraction. This finding provides evidence that the incremental effect of maximally effective insulin and contractile stimuli on glucose transport is mediated by additivity of their effects on GLUT-4 translocation into the sarcolemma.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Insulin is additive to contraction in stimulating glucose uptake.
“3) Insulin is additive to contraction in stimulating glucose uptake [109,110].”
From AMPK and Exercise: Glucose Uptake and Insulin Sensitivity (2013) · cites this paper as [110]
Cited by
Sorted by citations
Exercise, Glucose Transport, and Insulin Sensitivity
Goodyear, L. J., & Kahn, B. B. (1998) · Annual Review of Medicine · doi:10.1146/annurev.med.49.1.235 · Cited by 1,056 · see citing works
Cardiovascular Effects and Benefits of Exercise
Nystoriak, M. A., & Bhatnagar, A. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00135 · Cited by 881 · see citing works
Invited Review: Effects of acute exercise and exercise training on insulin resistance
Henriksen, E. J. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01219.2001 · Cited by 535 · see citing works
“The translocation mechanism for increasing plasma membrane GLUT-4 also functions in response to contractions (37, 41), hypoxia (15), nitric oxide (33), and bradykinin (2, 107).”
BackgroundLund, S., Holman, G. D., Schmitz, O., & Pedersen, O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.13.5817 · Cited by 492 · see citing works
Exercise regulation of glucose transport in skeletal muscle.
Hayashi, T., Wojtaszewski, J., & Goodyear, L. (1997) · American Journal of Physiology · doi:10.1152/ajpendo.1997.273.6.e1039 · Cited by 394 · see citing works
“Thus the results of two studies suggest that the increase in GLUT-4 at the plasma membrane is the sole mechanism for the increase in glucose transport (31, 75), whereas the two other studies raise the possibility that exercise increases glucose transporter turnover number (9, 23), a process that is frequently referred…”
BackgroundResultInfluentialAMPK and Exercise: Glucose Uptake and Insulin Sensitivity
O'Neill, H. M. (2013) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2013.37.1.1 · Cited by 295 · see citing works
“3) Insulin is additive to contraction in stimulating glucose uptake [109,110].”
BackgroundMechanisms regulating GLUT4 glucose transporter expression and glucose transport in skeletal muscle
Antonio Zorzano, A., Palacı́n, M., & Gumà, A. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2004.01380.x · Cited by 202 · see citing works
Coderre, L., Kandror, K. V., Vallega, G., & Pilch, P. F. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.46.27584 · Cited by 195 · see citing works
Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport
Cartee, G. D., & Wojtaszewski, J. F. P. (2007) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h07-026 · Cited by 183 · see citing works
“However, these stimuli use distinctive mechanisms to increase glucose transport, as evidenced by the following: (i) muscles stimulated with supramaximal insulin plus exercise/contractile activity have greater glucose transport than those stimulated with either stimulus alone (Constable et al. 1988; Gao et al. 1994); (…”
BackgroundMuscle as a consumer of lactate
Gladden, L. B. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200004000-00008 · Cited by 181 · see citing works
The regulation of carbohydrate and fat metabolism during and after exercise
Holloszy, J. O. (1998) · Frontiers in bioscience · doi:10.2741/a342 · Cited by 180 · see citing works
Self-citationLuiken, J. J. F. P., Coort, S. L., Koonen, D. P. Y., HORST, D. J. V. D., Bonen, A., Zorzano, A., & Glatz, J. F. C. (2004) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-003-1199-4 · Cited by 170 · see citing works
Mechanisms of control of heart glycolysis
Depré, C., Rider, M. H., & Hue, L. (1998) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1998.2580277.x · Cited by 164 · see citing works
“and the workload are partly additive [64, 65], thus indicating that they involve common regulatory steps located downstream of the insulin-sensitive phosphatidylinositol 3-kinase.”
BackgroundRegulation of glucose transport into skeletal muscle
Holloszy, J. O., & Hansen, P. A. (1996) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/3-540-61343-9_8 · Cited by 151 · see citing works
Self-citationHenriksen, E. J. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.04.002 · Cited by 136 · see citing works
“Muscle contractions can also stimulate glucose transport via insulin-independent mechanisms [12,13] that culminate with activation of GLUT-4 translocation [14,15].”
BackgroundTerada, S., Yokozeki, T., Kawanaka, K., Ogawa, K., Higuchi, M., Ezaki, O., & Tabata, I. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.6.2019 · Cited by 134 · see citing works
“This is evidenced by findings that the maximal effects of insulin and contractions or hypoxia on sugar transport (3, 19) and GLUT-4 translocation to the cell surface (16) are additive.”
BackgroundA forty-year memoir of research on the regulation of glucose transport into muscle
Holloszy, J. O. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00463.2002 · Cited by 135 · see citing works
“Despite the usual problem of contamination of the plasma membrane fraction with cytosolic GLUT4, Ping, with the help of Jimmy Ren and Eric Gulve, was able to show that the effects of contractions and insulin on movement of GLUT4 to the cell surface are clearly additive (30).”
BackgroundSelf-citationModulation of metabolic control by angiotensin converting enzyme (ACE) inhibition
Henriksen, E. J., & Jacob, S. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10294 · Cited by 136 · see citing works
“Like insulin, these factors activated by contraction and hypoxia ultimately signal the translocation of GLUT-4 to the plasma membrane, thereby allowing for an increase in glucose transport (Cartee et al., 1991; Goodyear et al., 1991; Gao et al., 1994).”
BackgroundRegulation of Carbohydrate and Fat Metabolism During and After Exercise
Holloszy, J. O., & Kohrt, W. M. (1996) · Annual Review of Nutrition · doi:10.1146/annurev.nu.16.070196.001005 · Cited by 129 · see citing works
Self-citationImprovement of insulin sensitivity by antagonism of the renin-angiotensin system
Henriksen, E. J. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00147.2007 · Cited by 123 · see citing works
“GLUT-4 to the plasma membrane can be elicited in response to contractions (17, 19) and hypoxia (10).”
BackgroundBergouignan, A., Latouche, C., Heywood, S., Grace, M. S., Reddy-Luthmoodoo, M., Natoli, A. K., Owen, N., Dunstan, D. W., & Kingwell, B. A. (2016) · Scientific Reports · doi:10.1038/srep32044 · Cited by 121 · see citing works
Exercise-related hypoglycemia in diabetes mellitus
Younk, L. M., Mikeladze, M., Tate, D., & Davis, S. N. (2011) · Expert Review of Endocrinology & Metabolism · doi:10.1586/eem.10.78 · Cited by 114 · see citing works
Current understanding of increased insulin sensitivity after exercise – emerging candidates
Maarbjerg, S. J., Sylow, L., & Richter, E. A. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02267.x · Cited by 104 · see citing works
“This additive effect is interesting because it parallels the additive effect of insulin and contraction on GLUT4 translocation (Gao et al. 1994b) and thereby suggests TBC1D4 as a convergent point prior to GLUT4 translocation.”
BackgroundDIET AND EXERCISE IN TYPE 2 DIABETES MELLITUS
Hamdy, O., Goodyear, L. J., & Horton, E. S. (2001) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(05)70220-6 · Cited by 102 · see citing works
Flores-Opazo, M., McGee, S. L., & Hargreaves, M. (2020) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000224 · Cited by 102 · see citing works
“Insulin and contraction/ exercise have distinct and additive effects on muscle glucose transport and GLUT4 translocation (18,26), which likely are due to differences in the upstream signaling pathways, separate GLUT4 kinetics and compartmentalization (27), and/or translocation of different pools of glucose transporter…”
BackgroundCuthbertson, D. J., Babraj, J., Mustard, K. J. W., Towler, M. C., Green, K. A., Wackerhage, H., Leese, G. P., Baar, K., Thomason-Hughes, M., Sutherland, C. D., et al. (2007) · Diabetes · doi:10.2337/db06-1716 · Cited by 100 · see citing works
“These two stimuli use distinct signaling pathways and are synergistic (2,3).”
BackgroundEfficiency of vibration exercise for glycemic control in type 2 diabetes patients
Baum, K., Votteler, T., & Schiab, J. (2007) · International Journal of Medical Sciences · doi:10.7150/ijms.4.159 · Cited by 96 · see citing works
“Secondly, a single bout of muscle contractions leads to a translocation of GLUT-4 to the sarcolemmal membrane, which acutely enhances glucose transport capacity [6,7,11].”
BackgroundThe role of the renin-angiotensin system in the development of insulin resistance in skeletal muscle
Henriksen, E. J., & Prasannarong, M. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.04.011 · Cited by 90 · see citing works
“This GLUT-4 translocation event is the primary means by which the rate of glucose transport is regulated by insulin in myocytes (Lund et al., 1993; Gao et al., 1994; Guma et al., 1995).”
BackgroundFazakerley, D. J., Holman, G. D., Marley, A. E., James, D. E., Stöckli, J., & Coster, A. C. F. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.051185 · Cited by 88 · see citing works
Regulation of hexokinase II activity and expression in human muscle by moderate exercise
Koval, J., DeFronzo, R. A., O'Doherty, R. M., Printz, R. L., Ardehali, H., Granner, D. K., & Mandarino, L. J. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.274.2.e304 · Cited by 79 · see citing works
“This increase has been attributed to an effect of exercise on the translocation of the GLUT-4 glucose transporter (4, 19, 22), hexokinase activity (14, 15, 18), or glycogen synthase activity (2, 3, 9), since electrically induced muscle contraction did not increase insulin-stimulated phosphorylation events involved in…”
BackgroundEgert, S. (1997) · Cardiovascular Research · doi:10.1016/s0008-6363(97)00133-8 · Cited by 75 · see citing works
Funai, K., & Cartee, G. D. (2009) · Diabetes · doi:10.2337/db08-1477 · Cited by 76 · see citing works
“Nevertheless, Wortmannin can clearly eliminate contractionstimulated increases in pAkt and PAS-AS160 in rat epitrochlearis muscle, which begs the question: How can activation of Akt and PAS-AS160 be important for insulinstimulated glucose transport, but not contraction-stimulated glucose transport? A similar paradox i…”
BackgroundMuscle Glycogen Resynthesis after Short Term, High Intensity Exercise and Resistance Exercise
Pascoe, D. D., & Gladden, L. B. (1996) · Sports Medicine · doi:10.2165/00007256-199621020-00003 · Cited by 74 · see citing works
Emerging role of neuregulin as a modulator of muscle metabolism
Gumà, A., Martínez-Redondo, V., López‐Soldado, I., Cantó, C., & Zorzano, A. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00541.2009 · Cited by 73 · see citing works
“To further investigate the bases for NRG additivity on insulin action, the muscle contraction pathway is reviewed here since it leads to insulin-additive effects on glucose transport (13, 22).”
Potteiger, J. A., JACOBSEN, D. J., & Donnelly, J. (2002) · International Journal of Obesity · doi:10.1038/sj.ijo.0801839 · Cited by 72 · see citing works
Richter, E. A., Jensen, P. B., Kiens, B., & Kristiansen, S. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.274.1.e89 · Cited by 71 · see citing works
The Utility of Physical Activity in the Management of Global Cardiometabolic Risk
Janiszewski, P. M., & Ross, R. (2009) · Obesity · doi:10.1038/oby.2009.382 · Cited by 71 · see citing works
“This enhanced translocation of GLUT-4 may occur due to physical activity–induced muscle contraction (71) and/or tissue hypoxia (72).”
BackgroundLund, S. A., Pryor, P. R., Østergaard, S. D., Schmitz, O., Pedersen, O. B., & Holman, G. D. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00293-2 · Cited by 67 · see citing works
Regulation of myocardial glucose uptake and transport during ischemia and energetic stress
Young, L. H., Russell, R. R., Yin, R., Caplan, M. J., Ren, J., Bergeron, R., Shulman, G. I., & Sinusas, A. J. (1999) · The American Journal of Cardiology · doi:10.1016/s0002-9149(99)00253-2 · Cited by 66 · see citing works
Self-citationTsakiridis, T. K., Vranić, M., & Klip, A. (1995) · Biochemical Journal · doi:10.1042/bj3090001 · Cited by 66 · see citing works
Effect of insulin and contraction up on glucose transport in skeletal muscle.
Pereira, L. O., & Lancha, A. (2004) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(03)00055-5 · Cited by 68 · see citing works
How muscle insulin sensitivity is regulated: testing of a hypothesis
Geiger, P. C., Han, D. H., Wright, D. C., & Holloszy, J. O. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00273.2006 · Cited by 61 · see citing works
“cation to the cell surface are additive (8, 18, 30, 32, 33, 38, 44).”
Self-citationPotteiger, J. A., JACOBSEN, D. J., Donnelly, J. E., & Hill, J. O. (2003) · Metabolism · doi:10.1016/s0026-0495(03)00146-x · Cited by 57 · see citing works
Effects of exercise and insulin on insulin signaling proteins in human skeletal muscle
Koval, J., Maezono, K., Patti, M., Pendergrass, M., DeFronzo, R. A., & Mandarino, L. J. (1999) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199907000-00012 · Cited by 51 · see citing works
An Overview of Muscle Glucose Uptake during Exercise
Wasserman, D. H., & Halseth, A. E. (1998) · Advances in experimental medicine and biology · doi:10.1007/978-1-4899-1928-1_1 · Cited by 51 · see citing works
Polonsky, K. S., & Burant, C. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-29738-7.00031-9 · Cited by 50 · see citing works
Schweitzer, G. G., Arias, E. B., & Cartee, G. D. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00619.2012 · Cited by 47 · see citing works
“Subsequently, other studies established that acute exercise can improve insulin-stimulated glucose uptake by skeletal muscle in vivo (19, 37, 44, 63, 64).”
BackgroundSavoia, A., Landi, S., Vannini, F., & Baldi, A. (2013) · Dermatology and Therapy · doi:10.1007/s13555-013-0026-x · Cited by 43 · see citing works
“Second, a single bout of muscle contractions leads to a translocation of GLUT-4 to the sarcolemma membrane, which acutely enhances glucose transport capacity [10, 11].”
BackgroundWhitfield, J., Paglialunga, S., Smith, B. K., Miotto, P. M., Simnett, G., Robson, H. L., Jain, S. S., Herbst, E. A. F., Desjardins, E. M., Dyck, D. J., et al. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.806786 · Cited by 42 · see citing works
“The effects of these metabolic stimuli are additive (1, 2), ultimately resulting in the translocation of GLUT4 from intracellular depots to the sarcolemmal membrane.”
BackgroundLi, Z., Yue, Y., Hu, F., Zhang, C., Ma, X., Li, N., Qiu, L., Fu, M., Chen, L., Yao, Z., et al. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00103.2017 · Cited by 44 · see citing works
Effect of different carbohydrate drinks on whole body carbohydrate storage after exhaustive exercise
Bowtell, J. L., Gelly, K., Jackman, M. L., Patel, A. A., Simeoni, M., & Rennie, M. J. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.88.5.1529 · Cited by 40 · see citing works
“There are thought to be one or more intracellular pools of GLUT-4 proteins, which are translocated to the sarcolemma in response to both increased insulin concentration (45) and prior exercise (26); these effects are additive (19).”
BackgroundZierath, J. R., Tsao, T., Stenbit, A. E., Ryder, J. W., Galuska, D., & Charron, M. J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.33.20910 · Cited by 39 · see citing works
Blair, D. R., Funai, K., Schweitzer, G. G., & Cartee, G. D. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.91003.2008 · Cited by 31 · see citing works
“SKELETAL MUSCLE CONTRACTION triggers increased insulin-independent glucose transport by inducing translocation of the GLUT4 glucose transporter to the cell surface (16, 23, 40), but the precise mechanisms for this effect remain incompletely understood.”
BackgroundTargeting skeletal muscle mitochondria to prevent type 2 diabetes in youth
Gordon, J. W., Dolinsky, V. W., Mughal, W., Gordon, G. R., & McGavock, J. (2015) · Biochemistry and Cell Biology · doi:10.1139/bcb-2015-0012 · Cited by 30 · see citing works
Buse, J. B., Polonsky, K. S., & Burant, C. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4377-0324-5.00031-6 · Cited by 28 · see citing works
Cartee, G. D., Arias, E. B., Yu, C. S., & Pataky, M. W. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00289.2016 · Cited by 27 · see citing works
“The increased glucose uptake in muscle tissue stimulated by either electrically stimulated contractions or in vivo exercise is attributable to redistribution of intracellular GLUT4 protein transporters to cell surface membranes (14, 19, 39).”
BackgroundCastorena, C. M., Arias, E. B., Sharma, N., Bogan, J. S., & Cartee, G. D. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00466.2014 · Cited by 27 · see citing works
Nadi, M., Marandi, S. M., Esfarjani, F., Saleki, M., & Mohammadi, M. (2017) · Advanced Biomedical Research · doi:10.4103/2277-9175.205528 · Cited by 25 · see citing works
“[21,25] In addition, doing an exercise session with muscular contractions causes the transfer of GLUT-4 to the plasma membrane, and this will increase the glucose transfer capacity into muscular and fat cells.[26,27] Insulin increases the glucose transfer to muscular cells directly and indirectly.”
BackgroundMcCarthy, O. M., Deere, R., Churm, R., Dunseath, G. J., Jones, C., Eckstein, M. L., Williams, D. M., Hayes, J., Pitt, J. P., Bain, S. C., et al. (2020) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2020.07.043 · Cited by 25 · see citing works
Exercise and Postprandial Glycemic Control in Type 2 Diabetes
Kearney, M. L., & Thyfault, J. P. (2016) · Current Diabetes Reviews · doi:10.2174/1573399811666150615112441 · Cited by 24 · see citing works
Molecular mechanisms of contraction-regulated cardiac glucose transport
Till, M., Ouwens, D. M., Kessler, A., & Eckel, J. (2000) · Biochemical Journal · doi:10.1042/bj3460841 · Cited by 24 · see citing works
Borg, M. L., Massart, J., De Castro Barbosa, T., Archilla‐Ortega, A., Smith, J. A. B., Lanner, J. T., Alsina‐Fernandez, J., Yaden, B., Culver, A. E., Karlsson, H. K. R., et al. (2021) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12746 · Cited by 23 · see citing works
“such that contraction depletes GLUT4 from transferrin receptor-positive endosomes that are not affected by insulin,(65,66) while GLUT4 trafficking to the membrane is additive in response to a combined stimulation with insulin and contraction.(67,68) An increase in total abundance of GLUT4 may not translate to an incre…”
BackgroundEzema, C. I., Omeh, E., Onyeso, O. K., Anyachukwu, C. C., Nwankwo, M. J., Amaeze, A. A., Ugwulebor, J. U., Nna, E. O., Ohotu, E. O., & Ugwuanyi, I. (2019) · Malaysian Journal of Medical Sciences · doi:10.21315/mjms2019.26.5.8 · Cited by 22 · see citing works
Gender differences in insulin action after a single bout of exercise
Perreault, L., Lavely, J. M., Bergman, B. C., & Horton, T. J. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00186.2004 · Cited by 22 · see citing works
“The relative contribution of each mechanism to net glucose uptake during and immediately after exercise is controversial; however, they are clearly synergistic (15).”
BackgroundMaternal Nutrient Restriction and Skeletal Muscle Development: Consequences for Postnatal Health
Sandoval, C., Wu, G., Smith, S. B., Dunlap, K. A., & Satterfield, M. C. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-45328-2_9 · Cited by 21 · see citing works
Regulation of Muscle Glucose Uptake In Vivo
Mandarino, L. J., Bonadonna, R. C., McGuinness, O. P., Halseth, A. E., & Wasserman, D. H. (2001) · Comprehensive physiology · doi:10.1002/cphy.cp070227 · Cited by 19 · see citing works
Cervone, D. T., & Dyck, D. J. (2017) · Physiological Reports · doi:10.14814/phy2.13320 · Cited by 20 · see citing works
“Glucose transport in skeletal muscle is mediated through distinct insulin and contraction mediated pathways, and their maximal effects can be additive (Gao et al. 1994).”
BackgroundEblenkamp, M., BÖTTCHER, U., Thomas, J., Löken, C., Ionescu, I., Rose, H., Kammermeier, H., & Fischer, Y. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00270-6 · Cited by 19 · see citing works
Fluckey, J. D., Ploug, & Galbo (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00593.x · Cited by 18 · see citing works
Skeletal Muscle Glucose Metabolism during Exercise: Implications for Health and Performance
Hargreaves, M. (1998) · Journal of science and medicine in sport · doi:10.1016/s1440-2440(09)60001-3 · Cited by 17 · see citing works
Crosstalk between exercise and galanin system alleviates insulin resistance
Fang, P., He, B., Shi, M., Zhu, Y. N., Bo, P., & Zhang, Z. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.09.012 · Cited by 16 · see citing works
Mechanisms in Exercise-Induced Increase in Glucose Disposal in Skeletal Muscle
Ojuka, E. O., & Goyaram, V. (2014) · Medicine and sport science/Medicine and sport · doi:10.1159/000357337 · Cited by 15 · see citing works
Henriksson, J., & Knol, M. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2005.01498.x · Cited by 16 · see citing works
The historical context and scientific legacy of John O. Holloszy
Hagberg, J. M., Coyle, E. F., Baldwin, K. M., Cartee, G. D., Fontana, L., Joyner, M. J., Kirwan, J. P., Seals, D. R., & Weiss, E. P. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00669.2018 · Cited by 13 · see citing works
No Acute Effect of Reduced-exertion High-intensity Interval Training (REHIT) on Insulin Sensitivity
Metcalfe, R. S., Fawkner, S. G., & Vollaard, N. B. J. (2016) · International Journal of Sports Medicine · doi:10.1055/s-0035-1564258 · Cited by 12 · see citing works
Kantor, P. F., Lopaschuk, G. D., & Opie, L. H. (2001) · Elsevier eBooks · doi:10.1016/b978-012656975-9/50034-1 · Cited by 14 · see citing works
Mechanism of hypoxia-stimulated glucose transport in rat skeletal muscle: potential role of glycogen
Reynolds, T., Brozinick, J. T., Rogers, M. A., & Cushman, S. W. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.274.5.e773 · Cited by 12 · see citing works
“Several laboratories have reported that the glucose transport response to the combined effects of insulin and contraction/hypoxia is additive (4, 26, 35) and thus have proposed that skeletal muscle contains two pools of GLUT-4, one responsive to insulin and the other responsive to contraction/hypoxia (1, 6, 10).”
BackgroundQuantitative methods for measuring the insulin-regulatable glucose transporter (Glut4).
Li, W.-M., & McNeill, J. H. (1997) · Journal of pharmacological and toxicological methods · doi:10.1016/s1056-8719(97)00036-1 · Cited by 8 · see citing works
Snook, L. A., Wright, D. C., & Holloway, G. P. (2016) · FEBS Letters · doi:10.1002/1873-3468.12260 · Cited by 8 · see citing works
McCarthy, O. M., Pitt, J. P., Churm, R., Dunseath, G. J., Jones, C., Bally, L., Nakas, C. T., Deere, R., Eckstein, M. L., Bain, S. C., et al. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2020-001577 · Cited by 6 · see citing works
Klip, A., & Marette, A. (2001) · Comprehensive physiology · doi:10.1002/cphy.cp070214 · Cited by 5 · see citing works
Lehmann-Klose, S., Beinbrech, B., R�egg, J. C., et al. (1995) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00373907 · Cited by 5 · see citing works
Zambito, J. L. (2011) · doi:10.33915/etd.3333 · Cited by 5 · see citing works
“The major mechanism by which glucose disposal is increased during exercise is through the recruitment of GLUT4.”
BackgroundInfluentialLi, W. M., Cam, M. C., Poucheret, P., & McNeill, J. H. (1998) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006847426875 · Cited by 5 · see citing works
Martineau, L. C., Chadan, S. G., & Parkhouse, W. S. (1999) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(99)00050-0 · Cited by 4 · see citing works
Kim, M., Zhang, H., Kim, T.-H., Mori, Y., Okura, T., Tanaka, K., Isobe, T., Sakae, T., & Oh, S. (2023) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph20064708 · Cited by 3 · see citing works
“Such muscle contraction increases the content of glucose transporter 4 in muscle cells and its translocation to the sarcolemmal membrane, which considerably improves glucose transport capacity [21,22].”
BackgroundTeixeira, S. A. (2010) · Cited by 3 · see citing works
Okon, I. A., Nwachukwu, D. C., Udoeyop, F. A., Uko, B. R., Umoren, E. B., Kolawole, T. A., Amadi, N. G., Owaji-Teleyem, D. M., & Owu, D. U. (2024) · Obesity Medicine · doi:10.1016/j.obmed.2024.100559 · Cited by 2 · see citing works
Ezema, C. I., Lamina, S., Onwunali, A. A., Ezugwu, U. A., Amaeze, A. A., & Nwankwo, M. (2015) · International Journal of Diabetes in Developing Countries · doi:10.1007/s13410-014-0249-0 · Cited by 1 · see citing works
10.1016/b978-1-4160-2911-3.50032-7
(2000) · Time to knit · doi:10.1016/b978-1-4160-2911-3.50032-7 · Cited by 1 · see citing works
Exercise, muscle glycogen and insulin action
Johnstone, B. R. (2004) · Figshare
Metcalfe, R. S. (2015) · The University of Bath Online Publications Store (The University of Bath) · doi:10.13140/rg.2.1.4944.0088
Ezema, C. I., Onwunali, A. A., Lamina, S., Ezugwu, U. A., Amaeze, A. A., Nwankwo, M. J., & Amaeze, F. N. (2013) · Health · doi:10.4236/health.2013.511242
Gifford, N. R. (2007) · UA Campus Repository (The University of Arizona)
Running Title: AICAR stimulation of human glucose uptake
Cuthbertson, D. J., Babraj, J., Towler, M. C., Wackerhage, H., Leese, G. P., Baar, K., Thomason-Hughes, M., Sutherland, C. D., Hardie, D. G., & Rennie, M. J. (2007)
PAULO ALEXANDRE DE CARVALHO MORAES
Paulo, S. (2007)
Duration of improved insulin sensitivity after high intensity exercise in young overweight men
Quinn, K. (2015) · doi:10.31274/etd-180810-4081
“…including; a) increases in GLUT4, a glucose transporter protein (Wallberg-Henriksson et al., 1988, Goodyear et al., 1991, Brozinick et al., 1994, Gao et al., 1994, Hansen et al., 1995, Lund et al., 1995, Kristiansen et al., 1996), b) reductions in fatty acid mobilization (Santamauro et al.,…”
Background정영수, & 구민석 (2009) · Exercise Science · doi:10.15857/ksep.2009.18.1.53
- Authors
- Gao, J., Ren, J., Gulve, E. A., & Holloszy, J. O.
- Affiliations
- Washington University in St. Louis (US)
- ORCID
- Gao, J.
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 1994-10-01
- Volume
- 77
- Issue
- 4
- Pages
- 1597-1601
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W1864159588
- Cited by
- 116
- References
- 0
- Citations by year
- 2024: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 5 · 2019: 2 · 2018: 1 · 2017: 4 · 2016: 6 · 2015: 7 · 2014: 4 · 2013: 3 · 2012: 2
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG 00078)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK20579, DK-18986, R01DK018986)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- GLUT4, glucose transporter translocation, skeletal muscle glucose transport, insulin, muscle contraction, additive effects, sarcolemma, plasma membrane, subcellular fractionation
- MeSH terms
- Animals, Cell Fractionation, Cell Membrane, Electrophoresis, Polyacrylamide Gel, Glucose, Insulin, Intracellular Membranes, Male, Monosaccharide Transport Proteins, Muscle Contraction, Muscle Proteins, Sarcolemma, Blotting, Western, Rats, Wistar, Muscle, Skeletal, Glucose Transporter Type 4, Rats
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