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Influence of muscle glycogen availability on ERK1/2 and Akt signaling after resistance exercise in human skeletal muscle
Abstract
Two pathways that have been implicated for cellular growth and development in response to muscle contraction are the extracellular signal-regulated kinase (ERK1/2) and Akt signaling pathways. Although these pathways are readily stimulated after exercise, little is known about how nutritional status may affect stimulation of these pathways in response to resistance exercise in human skeletal muscle. To investigate this, experienced cyclists performed 30 repetitions of knee extension exercise at 70% of one repetition maximum after a low (2%) or high (77%) carbohydrate (LCHO or HCHO) diet, which resulted in low or high (approximately 174 or approximately 591 mmol/kg dry wt) preexercise muscle glycogen content. Muscle biopsies were taken from the vastus lateralis before, approximately 20 s after, and 10 min after exercise. ERK1/2 and p90 ribosomal S6 kinase phosphorylation increased (P < or = 0.05) 10 min after exercise, regardless of muscle glycogen availability. Akt phosphorylation was elevated (P < 0.05) 10 min after exercise in the HCHO trial but was unaffected after exercise in the LCHO trial. Mammalian target of rapamycin phosphorylation was similar to that of Akt during each trial; however, change or lack of change was not significant. In conclusion, the ERK1/2 pathway appears to be unaffected by muscle glycogen content. However, muscle glycogen availability appears to contribute to regulation of the Akt pathway, which may influence cellular growth and adaptation in response to resistance exercise in a low-glycogen state.
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“Although the evidence is not unanimous, low levels of glycogen could inhibit the hypertrophic response to resistance training [18,19] and increase proteolysis [20,21].”
From Carbohydrate Availability and Physical Performance: Physiological Overview and Practical Recommendations (2019) · cites this paper as [19]
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BackgroundBurd, N. A., West, D. W. D., Staples, A. W., Atherton, P. J., Baker, J. M., Moore, D. R., Holwerda, A. M., Parise, G., Rennie, M. J., Baker, S. K., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012033 · Cited by 531
“Indeed, many investigations have established that Akt is transiently phosphorylated following exercise [14,41,42,43] or even no change [12,44,45].”
BackgroundExercise, MAPK, and NF-κB signaling in skeletal muscle
Kramer, H. F., & Goodyear, L. J. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00085.2007 · Cited by 375
“The magnitude of ERK1/2 phosphorylation during exercise correlates with the intensity of the protocol (87), and both endurance and resistance exercise (16, 46, 88) can increase ERK1/2 phosphorylation.”
Fyfe, J. J., Bishop, D. J., & Stepto, N. K. (2014) · Sports Medicine · doi:10.1007/s40279-014-0162-1 · Cited by 347
“For example, the availability of muscle glycogen has been reported to modulate early molecular responses to both endurance and resistance exercise in a divergent manner [82, 84, 137].”
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Coffey, V. G., Zhong, Z., Shield, A., Canny, B. J., Chibalin, A. V., Zierath, J. R., & Hawley, J. A. (2006) · The FASEB Journal · doi:10.1096/fj.05-4809fje · Cited by 336
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“It should be noted that some studies fail to demonstrate significant increases in the phosphorylation of some components of these signaling pathways, perhaps due to differences in exercise intensity (57), mode of contraction (37), and/or glycogen status (24).”
Burd, N. A., Holwerda, A. M., Selby, K. C., West, D. W. D., Staples, A. W., Cain, N. E., Cashaback, J. G. A., Potvin, J. R., Baker, S. K., & Phillips, S. M. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.192856 · Cited by 323
“Evidence suggests that members of the MAPK signalling cascades (i.e. p38, Erk1/2, p90RSK1) are phosphorylated in close temporal proximity to the resistance exercise bout (Williamson et al. 2003; Creer et al. 2005; Drummond et al. 2008; Tannerstedt et al. 2009).”
BackgroundEgan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278
Concurrent Strength and Endurance Training
Nader, G. A. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000233795.39282.33 · Cited by 254
“(10), who recently reported that low muscle-glycogen levels impaired the intracellular signaling responses to an acute bout of resistance exercise.”
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“In contrast, Creer et al. (2005) found an increase in Ser 473 phosphorylation of Akt 10 min after low”
BackgroundResultAreta, J. L., Burke, L. M., Camera, D. M., West, D. W. D., Crawshay, S., Moore, D. R., Stellingwerff, T., Phillips, S. M., Hawley, J. A., & Coffey, V. G. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00590.2013 · Cited by 227
“This finding was in contrast to our previous results (9) and those from several other groups (13, 15) when REX was undertaken in the fasted state in EB.”
ResultSpiering (2008) · doi:10.2165/00007256-200838070-00001 · Cited by 227
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“Finally, it is becoming clear that endogenous and exogenous substrate availability before and after resistance exercise can modulate the transcriptional activity of selected myogenic genes and the regulation of signalling pathways that promote the resistance-exercise-induced increase in protein synthesis (Churchley et…”
Nutritional modulation of training-induced skeletal muscle adaptations
Hawley, J. A., Burke, L. M., Phillips, S. M., & Spriet, L. L. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00949.2010 · Cited by 205
Eliasson, J., Brink-Elfegoun, T., Nilsson, J. E., Köhnke, R., Ekblom, B. T., & Blomstrand, E. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00141.2006 · Cited by 163
“Results from another study (9) indicate that changes in Akt phosphorylation are dependent on the preexercise muscle glycogen content.”
BackgroundResistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men
Hulmi, J. J., Tannerstedt, J., Selänne, H., Kainulainen, H., Kovanen, V., & Mero, A. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00087.2009 · Cited by 163
“The reason for the selection of a non-energetic placebo drink instead of isocaloric carbohydrate drink was because carbohydrates per se can have also many effects on many of the studied variables (6).”
BackgroundMascher, H., Tannerstedt, J., Brink-Elfegoun, T., Ekblom, B. T., Gustafsson, T. P., & Blomstrand, E. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00504.2007 · Cited by 165
“The choice of time points for biopsy sampling was based on previous data (10, 12, 14, 23) showing early changes in signaling proteins after a single resistance exercise session in human subjects.”
MethodEarly Time Course of Akt Phosphorylation after Endurance and Resistance Exercise
CAMERA, D. M., EDGE, J., SHORT, M. J., HAWLEY, J. A., & COFFEY, V. G. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181d964e4 · Cited by 154
Promoting training adaptations through nutritional interventions
Hawley, J. A., Tipton, K. D., & Millard-Stafford, M. L. (2006) · Journal of Sports Sciences · doi:10.1080/02640410500482727 · Cited by 157
“Creer et al. (2005) recently reported that when endurance-trained individuals performed a bout of moderate-intensity resistance exercise (similar to that likely to be undertaken by soccer players) with low (*175 mmol kg dry weight71) muscle glycogen content, phosphorylation of Akt, a critical…”
BackgroundMediators of Physical Activity Protection against ROS-Linked Skeletal Muscle Damage
Meo, S. D., Napolitano, G., & Venditti, P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20123024 · Cited by 148
“Subsequent works also showed an increase in ERK1/2 phosphorylation in response to resistance exercise [177,178].”
BackgroundStrategies to Optimize Concurrent Training of Strength and Aerobic Fitness for Rowing and Canoeing
Pallarés, J. G., & Izquierdo, M. (2011) · Sports Medicine · doi:10.2165/11539690-000000000-00000 · Cited by 151
“The interference of strength development during concurrent training has been classically explained by the following mechanisms:([47,49-51]) (i) reductions in the motor unit recruitment and decreases of rapid voluntary neural activations;([27,37,48,52]) (ii) chronic depletion of muscle glycogen stores;([53,54]) (iii) s…”
BackgroundDeldicque, L., Atherton, P. J., Patel, R. S., Theisen, D., Nielens, H., Rennie, M. J., & Francaux, M. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00873.2007 · Cited by 143
“Some studies have reported that resistance exercise activates the PKB cascade (9, 13); others have observed no changes (8, 9, 12, 14).”
BackgroundNutrient timing revisited: is there a post-exercise anabolic window?
Aragon, A. A., & Schoenfeld, B. J. (2013) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-10-5 · Cited by 139
“[15] demonstrated that changes in the phosphorylation of protein kinase B (Akt) are dependent on pre-exercise muscle glycogen content.”
BackgroundArazi, H., Eghbali, E., & Suzuki, K. (2021) · Nutrients · doi:10.3390/nu13030869 · Cited by 145
“In addition, the phosphatidylinositol 3-kinase (PI3K)–protein kinase B (AKT)–mammalian target of rapamycin (mTOR) signaling pathways are disrupted when resistance training is performed after glycogen depletion during endurance training [86,87].”
BackgroundDecrease in Akt/PKB signalling in human skeletal muscle by resistance exercise
Deldicque, L., Atherton, P. J., Patel, R. S., Theisen, D., Nielens, H., Rennie, M. J., & Francaux, M. (2008) · European Journal of Applied Physiology · doi:10.1007/s00421-008-0786-7 · Cited by 117
“ERK1/2 and p38 are also inXuenced by resistance exercise ( Creer et al. 2005; Karlsson et al. 2004), but a clear picture of the regulatory pattern has not yet emerged.”
BackgroundInfluentialConsecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle
Coffey, V. G., Pilegaard, H., Garnham, A. P., O'Brien, B. J., & Hawley, J. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91221.2008 · Cited by 116
“Moreover, Akt phosphorylation has been shown to increase after both resistance (16, 18) and endurance activities (14, 28, 41, 65) or to remain unchanged with exercise (14, 19, 42, 61, 63).”
BackgroundGlycogen availability and skeletal muscle adaptations with endurance and resistance exercise
Knuiman, P., Hopman, M. T. E., & Mensink, M. (2015) · Nutrition & Metabolism · doi:10.1186/s12986-015-0055-9 · Cited by 113
“A more recent study by Howarth et al. [82] used the stable isotope tracer methodology and therefore enabled to determine the changes in MPS and MPB.”
BackgroundInfluentialCharacterization and Regulation of Mechanical Loading‐Induced Compensatory Muscle Hypertrophy
Adams, G. R., & Bamman, M. M. (2012) · Comprehensive physiology · doi:10.1002/cphy.c110066 · Cited by 123
Mata, F., Valenzuela, P. L., Gimenez, J., Tur, C., Ferreria, D., Domínguez, R., Sanchez-Oliver, A. J., & Martínez Sanz, J. M. (2019) · Nutrients · doi:10.3390/nu11051084 · Cited by 112
“Although the evidence is not unanimous, low levels of glycogen could inhibit the hypertrophic response to resistance training [18,19] and increase proteolysis [20,21].”
BackgroundImpey, S. G., Hammond, K. M., Shepherd, S. O., Sharples, A. P., Stewart, C., Limb, M., Smith, K., Philp, A., Jeromson, S., Hamilton, D. L., et al. (2016) · Physiological Reports · doi:10.14814/phy2.12803 · Cited by 109
“…given previous data demonstrating that the post-exercise (albeit in resistance exercise) activation of Akt phosphorylation is suppressed (independent of post-exercise feeding) when muscle glycogen levels are comparable to that observed in this study, that is <150 mmol kg 1 dw (Creer et al. 2005).”
MethodCarbohydrate Availability and Training Adaptation: Effects on Cell Metabolism
Hawley, J. A., & Burke, L. M. (2010) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3181f44dd9 · Cited by 109
“There are several studies of the acute effects of commencing resistance-based exercise in the face of low muscle glycogen stores (8,12); however, the results from these investigations suggest that such a practice may have a negative impact on cellular growth and adaptation.”
ResultTerzis, G., Spengos, K., Mascher, H., Georgiadis, G., Manta, P., & Blomstrand, E. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1527-2 · Cited by 110
“Previous reports have shown both unchanged, increased or decreased Akt phosphorylation after various types of resistance exercise ( Creer et al. 2005; Deldicque et al. 2008; Eliasson et al. 2006; Mascher et al. 2008; Terzis et al. 2008).”
BackgroundResultGreene, D., Varley, B. J., Hartwig, T. B., Chapman, P., & Rigney, M. (2018) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000002904 · Cited by 109
Tannerstedt, J., Apró, W., & Blomstrand, E. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91243.2008 · Cited by 104
Heat stress enhances mTOR signaling after resistance exercise in human skeletal muscle
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“The levels of phosphorylated ERK1/2 and p38 have been shown to increase after resistance exercise in human skeletal muscle [30–32, 55].”
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“Apart from interfering with in vivo function, decreased glycogen availability may also directly or indirectly impact aspects of muscle signaling following RE (17).”
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“Regarding muscle protein synthesis (MPS) and net protein accretion, it has been concluded that they can be promoted by an early post-exercise protein consumption (Phillips, 2011).”
BackgroundInfluentialFyfe, J. J., Bishop, D. J., Zacharewicz, E., Russell, A. P., & Stepto, N. K. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00479.2015 · Cited by 87
Aerobic Exercise Alters Skeletal Muscle Molecular Responses to Resistance Exercise
LUNDBERG, T. R., FERNANDEZ-GONZALO, R., GUSTAFSSON, T., & TESCH, P. A. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318256fbe8 · Cited by 86
“Thus, although low glycogen content may blunt the anabolic signaling responses to acute RE (11), it seems the protocol and design used here ensured functional (average peak power) recovery from aerobic exercise.”
BackgroundTrappe, S. W., Creer, A., Minchev, K., Slivka, D. R., Louis, E. S., Luden, N. D., & Trappe, T. A. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00761.2007 · Cited by 89
“Low muscle glycogen levels have been shown to down regulate the typical exercise response of key signaling intermediates (Akt/mTOR) (16) and the basal expression of genes (10) that are involved with muscle growth and remodeling.”
BackgroundChurchley, E. G., Coffey, V. G., Pedersen, D. J., Shield, A., Carey, K. A., Cameron-Smith, D., & Hawley, J. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01260.2006 · Cited by 80
“(13) showed that when endurance-trained subjects commenced a bout of moderate-intensity resistance exercise with low ( 175 mmol/kg dry wt) muscle glycogen content, phosphorylation of Akt, a critical signaling mediator of cell growth and metabolism (17), was diminished compared with when subjects undertook the same wor…”
BackgroundEfficacy and consequences of very-high-protein diets for athletes and exercisers
Tipton, K. D. (2011) · Proceedings of The Nutrition Society · doi:10.1017/s0029665111000024 · Cited by 84
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“Similar to ERK1/2 phosphorylation, alterations in p90RSK phosphorylation (Ser(380) and Thr(573)) have been observed within 10 min of exercise cessation (33, 114), and p90RSK phosphorylation (Ser(380) and Thr(573)) can remain elevated for 5–24 h postexercise, depending on the phosphorylation site measured (25, 124).”
BackgroundYeo, W. K., Lessard, S. J., Chen, Z.-P., Garnham, A. P., Burke, L. M., Rivas, D. A., Kemp, B. E., & Hawley, J. A. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90540.2008 · Cited by 73
“Indeed, evidence is accumulating that nutrient manipulation can serve as a potent modulator of many of the acute responses to both endurance (15) and resistance exercise (7, 11).”
BackgroundLow muscle glycogen concentration does not suppress the anabolic response to resistance exercise
CAMERA, D. M., West, D. W. D., Burd, N. A., Phillips, S. M., GARNHAM, A. P., Hawley, J. A., & Coffey, V. G. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00395.2012 · Cited by 73
“by Creer and colleagues (11) showed an attenuation in Akt”
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“The rate of utilization of IMTG during resistance exercise appears to be in part dictated by the starting concentration such that greater IMTG content results in increased rates of IMTG degradation (92).”
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Role of Akt2 in contraction-stimulated cell signaling and glucose uptake in skeletal muscle
Sakamoto, K., Arnolds, D. E., Fujii, N., Kramer, H. F., Hirshman, M. F., & Goodyear, L. J. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00204.2006 · Cited by 63
“Although early studies suggested that Akt was not activated by either contraction (2, 25, 39) or physical exercise (26, 46, 48), more recent data from our laboratory and those of others have convincingly shown that Akt is activated by exercise and contraction in both rodent (3, 28, 30, 34, 36) and human skeletal muscl…”
ResultApró, W., & Blomstrand, E. (2010) · Acta Physiologica · doi:10.1111/j.1748-1708.2010.02151.x · Cited by 76
“These findings are in agreement with some (Coffey et al. 2006, Deshmukh et al. 2006, Eliasson et al. 2006) but no all (Creer et al. 2005, Blomstrand et al. 2006, Dreyer et al. 2006, Deldicque et al. 2008, Terzis et al. 2008) earlier studies of contractile activity on Akt phosphorylation.”
ResultHenselmans, M., Bjørnsen, T., Hedderman, R., & Vårvik, F. T. (2022) · Nutrients · doi:10.3390/nu14040856 · Cited by 89
Akt/protein kinase B in skeletal muscle physiology and pathology
Wu, M., Falasca, M., & Blough, E. R. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22353 · Cited by 60
“For example, Creer et al. (2005) showed that the degree of exercise-induced Akt serine phosphorylation is positively related to the amount of muscle glycogen.”
BackgroundMacedo, A. G., Krug, A. L. O., Herrera, N. A., Zago, A. S., Rush, J. W. E., & Amaral, S. L. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.05.010 · Cited by 55
Tipton, K. D., Jeukendrup, A. E., & Hespel, P. (2007) · Journal of Sports Sciences · doi:10.1080/02640410701607205 · Cited by 56
“Both translational (Bolster, Jefferson, & Kimball, 2004) and transcriptional (Creer et al., 2005; Psilander, Damsgaard, & Pilegaard, 2003) mechanisms are stimulated by resistance exercise, but the bulk of the increase in muscle protein synthesis is translational (Chesley, MacDougall, Tarnopolsky, Atkinson, & Smith, 19…”
BackgroundMarkworth, J. F., Vella, L. D., Figueiredo, V. C., & Cameron‐Smith, D. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01299.2013 · Cited by 59
The effect of concurrent training organisation in youth elite soccer players
Enright, K. J., Morton, J. P., Iga, J., & Drust, B. (2015) · European Journal of Applied Physiology · doi:10.1007/s00421-015-3218-5 · Cited by 57
“Whereas, completing strength training in the face of low muscle glycogen stores can have a negative impact on training performance and adaptation (Churchley et al. 2007; Creer et al. 2005).”
BackgroundResistance Exercise, Skeletal Muscle FOXO3A, and 85-Year-Old Women
Williamson, D. L., Raue, U., Slivka, D. R., & Trappe, S. W. (2010) · The Journals of Gerontology Series A · doi:10.1093/gerona/glq005 · Cited by 53
Effects of Elevated Circulating Hormones on Resistance Exercise-Induced Akt Signaling
Spiering, B. A., Kraemer, W. J., Anderson, J. M., Armstrong, L. E., Nindl, B. C., Volek, J. S., Judelson, D. A., JOSEPH, M., Vingren, J. L., Hatfield, D. L., et al. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31816722bd · Cited by 52
“Specifically, the present results contribute to a growing body of literature demonstrating that in humans, exercise-induced signaling of Akt and/or its downstream targets is modulated by ingestion of branchedchain amino acids (20), glycogen availability (10), muscle action (11,13), muscle fiber type examined (22), and…”
BackgroundResultEffects of skeletal muscle energy availability on protein turnover responses to exercise
Smiles, W. J., Hawley, J. A., & Camera, D. M. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.125104 · Cited by 48
“Of note is that the time courses of many of these intracellular events typically peak in the 3–4 h period post-exercise and have returned to pre-exercise baseline values within 24 h (Creer et al., 2005).”
Trappe, T. A., Ratchford, S. M., Brower, B. E., Liu, S. Z., Lavin, K. M., Carroll, C. C., Jemioło, B., & Trappe, S. W. (2016) · The Journals of Gerontology Series A · doi:10.1093/gerona/glv231 · Cited by 52
Shepherd, S. O., Cocks, M. S., Tipton, K. D., Witard, O. C., Ranasinghe, A. M., Barker, T. A., Wagenmakers, A. J. M., & Shaw, C. S. (2014) · Experimental Physiology · doi:10.1113/expphysiol.2014.078014 · Cited by 52
“A number of studies have previously shown that IMTG are reduced following an acute bout of resistance exercise (Essen-Gustavsson & Tesch, 1990; Creer et al. 2005; Koopman et al. 2006) and that rates of IMTG synthesis increase in the period following exercise-induced IMTG depletion (Schenk &…”
BackgroundResultHaun, C. T., Mumford, P. W., Roberson, P. A., Romero, M. A., Mobley, C. B., Kephart, W. C., Anderson, R. G., Colquhoun, R. J., Muddle, T. W. D., Luera, M. J., et al. (2017) · Physiological Reports · doi:10.14814/phy2.13457 · Cited by 48
“studies comparing acute and subchronic responses to RT have revealed strikingly similar anabolic signaling outcomes (Creer et al. 2005; Dreyer et al. 2006; Burd et al. 2010; Fry et al. 2010; Mitchell et al. 2012; Morton et al. 2016b).”
BackgroundIhalainen, J. K., Mikkonen, R. S., Ackerman, K. E., Heikura, I. A., Mjøsund, K., Valtonen, M., & Hackney, A. C. (2024) · Sports Medicine · doi:10.1007/s40279-024-02065-6 · Cited by 61
“…has been demonstrated to negatively affect cellular growth and adaptation in response to resistance exercise independently of hormonal responses [135], while exercise nutrient interactions influence cascades that affect protein regulatory systems during both exercise and recovery where energy…”
BackgroundHawley, J. A., Gibala, M. J., & Bermon, S. (2007) · Journal of Sports Sciences · doi:10.1080/02640410701607411 · Cited by 43
“…Hawley et al., 2000; Stepto et al., 2002), as well as on many of the acute regulatory processes underlying gene expression (Arkinstall, Tunstall, Cameron-Smith, & Hawley, 2004b; Cameron-Smith et al., 2003; Churchley et al., 2007; Creer et al., 2005) and cell signalling (Wojtaszewski et al., 2003).”
BackgroundSkeletal muscle signaling response to sprint exercise in men and women
Fuentes, T., Guerra, B., Ponce-González, J. G., Morales-Alamo, D., Guadalupe-Grau, A., Olmedillas, H., Rodríguez-García, L., Feijoo, D., De Pablos-Velasco, P., Fernández-Pérez, L., et al. (2012) · European Journal of Applied Physiology · doi:10.1007/s00421-011-2164-0 · Cited by 36
Paleolithic Diet—Effect on the Health Status and Performance of Athletes?
Frączek, B., Pięta, A., Burda, A., Mazur-Kurach, P., & Tyrała, F. (2021) · Nutrients · doi:10.3390/nu13031019 · Cited by 41
“For example, there is no evidence that carbohydrates are required for mTORC-1 (mammalian target of rapamycin complex-1) signaling during muscle protein synthesis [103], when dietary protein intake is sufficient [102].”
BackgroundIs sprint exercise a leptin signaling mimetic in human skeletal muscle?
Guerra, B., Olmedillas, H., Guadalupe‐Grau, A., Ponce‐González, J. G., Morales‐Álamo, D., Fuentes, T., Chapinal, E., Fernández‐Pérez, L., de Pablos-Velasco, P. L., Santana, A., et al. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00805.2010 · Cited by 34
Taylor, L. W., Wilborn, C., Kreider, R. B., & Willoughby, D. S. (2011) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e318242f92d · Cited by 34
“1 repetition maximum (1RM) of the knee extension exercise) increases ERK1/2 activity within 30 minutes of exercise (7,14,31).”
BackgroundCarrithers, J. A., Carroll, C. C., Coker, R. H., Sullivan, D. H., & Trappe, T. A. (2007) · PubMed · Cited by 32
Popov, D. V., Lysenko, E. A., Bachinin, A. V., Miller, T. F., Kurochkina, N. S., Kravchenko, I. V., Furalyov, V. A., & Vinogradova, O. L. (2015) · Muscle & Nerve · doi:10.1002/mus.24314 · Cited by 32
Effect of acute exercise on glucose tolerance following post-exercise feeding
Venables, M., Shaw, C. S., Jeukendrup, A. E., & Wagenmakers, A. J. M. (2007) · European Journal of Applied Physiology · doi:10.1007/s00421-007-0464-1 · Cited by 31
“The evidence from these studies (Creer et al. 2005; Hernandez et al. 2000) and that from the present study appears to indicate that RE followed by carbohydrate feeding to enhance glycogen re-synthesis is beneficial if not crucial to the enhancement of glucose tolerance in the post-exercise period.”
InfluentialKaragounis, L. G., Yaspelkis, B. B., Reeder, D. W., Lancaster, G. I., Hawley, J. A., & Coffey, V. G. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1427-5 · Cited by 31
“Moreover, Akt phosphorylation and activity have previously been shown to both increase/decrease (Bolster et al. 2003; Coffey et al. 2005, 2007; Creer et al. 2005; Dreyer et al. 2006; Nader and Esser 2001; Sakamoto et al. 2004 )o r remain unchanged (Coffey et al. 2005; Eliasson et al. 2006; Nader and Esser 2001; Widegr…”
BackgroundAnderson, L. J., Drust, B., Close, G. L., & Morton, J. P. (2022) · Journal of Sports Sciences · doi:10.1080/02640414.2022.2044135 · Cited by 34
“In addition, commencing strength training in conditions of low muscle glycogen (<200 mmol.kg−1 dry weight) may reduce associated mTOR signalling (Churchley et al., 2007; Creer et al., 2005).”
BackgroundMacNeil, L., Glover, E. I., Bergstra, T. G., Safdar, A., & Tarnopolsky, M. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109189 · Cited by 33
“has been suggested that the adaptive processes may interfere with one another [7,8], thereby attenuating the optimal adaptation that could be achieved from either mode individually.”
BackgroundEscobar, K. A., VanDusseldorp, T. A., & Kerksick, C. M. (2016) · British Journal Of Nutrition · doi:10.1017/s0007114516003949 · Cited by 34
“Low-CHO diets may not be as detrimental as typically espoused, as investigations have demonstrated that CHO intakes less than the moderately high recommendation does not hinder acute resistance exercise performance((30,32)) or the subsequent cellular responses responsible for adaptation, including translation initiati…”
BackgroundInfluentialRoberts, M. D., Holland, A. M., Kephart, W. C., Mobley, C. B., Mumford, P. W., Lowery, R. P., Fox, C. D., McCloskey, A. E., Shake, J. J., Mesquita, P. H. C., et al. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00837.2015 · Cited by 28
“(5) reported that 3 days of a LCKD, which decreased skeletal muscle glycogen, did not hamper intramuscular anabolic signaling (i.”
BackgroundFat and carbohydrate for exercise
Burke, L. M., & Hawley, J. A. (2006) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/01.mco.0000232911.69236.3b · Cited by 28
Zak, R., Hassenstab, B., Zuehlke, L. K., Heesch, M., Shute, R. J., Laursen, T. L., Salle, D. T. L., & Slivka, D. R. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3749-z · Cited by 26
Ochi, E., Hirose, T., Hiranuma, K., Min, S.-K., Ishii, N., & Nakazato, K. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00278.2009 · Cited by 25
Nutritional Considerations for Bouldering
Gibson-Smith, E., Storey, R., & Ranchordas, M. K. (2017) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2017-0043 · Cited by 26
Resistance Exercise–induced Regulation of Muscle Protein Synthesis to Intraset Rest
Salvador, A. F., Askow, A. T., McKenna, C. F., FANG, H.-Y., Skinner, S. K., Li, Z. A., ULANOV, A. V., Paluska, S. A., Petruzzello, S. J., Boppart, M. D., et al. (2019) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002213 · Cited by 27
Stephens, F. B., Norton, L., Jewell, K., Chokkalingam, K., Parr, T., & Tsintzas, K. (2010) · Experimental Physiology · doi:10.1113/expphysiol.2009.051367 · Cited by 20
“This was important, because muscle glycogen content is inversely related to glycogen synthase activity (Nielsen et al. 2001) and has also been suggested to affect metabolic gene expression (Pilegaard et al. 2002; Garcia-Roves et al. 2003) and Akt phosphorylation (Creer et al. 2005).”
BackgroundAltering Endogenous Carbohydrate Availability to Support Training Adaptations
Philp, A., Burke, L. M., & Baar, K. (2011) · Nestlé Nutrition Institute Workshop series · doi:10.1159/000329279 · Cited by 20
Granlund, A., Kotova, O., Benziane, B., Galuska, D., Jensen‐Waern, M., Chibalin, A., & Essén-Gustavsson, B. (2009) · Experimental Physiology · doi:10.1113/expphysiol.2009.051326 · Cited by 19
“subjects had been on a high-carbohydrate diet, resulting in high muscle glycogen levels, in comparison to a low-carbohydrate diet, resulting in low muscle glycogen levels (Creer et al. 2005).”
BackgroundNicoll, J. X., Fry, A. C., Mosier, E. M., Olsen, L. A., & Sontag, S. A. (2019) · European Journal of Applied Physiology · doi:10.1007/s00421-019-04200-y · Cited by 21
Signaling Responses After Varying Sequencing of Strength and Endurance Training in a Fed State
Jones, T. W., Walshe, I. H., Hamilton, D. L., Howatson, G., Russell, M., Price, O. J., Gibson, A. S. C., & French, D. N. (2016) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2015-0534 · Cited by 18
Ferreira, M. P., Li, R., Cooke, M. B., Kreider, R. B., & Willoughby, D. S. (2014) · Nutrition Research · doi:10.1016/j.nutres.2013.12.007 · Cited by 16
“Protein kinase B has been shown to rapidly and transiently increase in phosphorylation after exercise [32], although, Akt phosphorylation in response to RE may or may not correlate with the”
BackgroundMaughan, R. (2006) · Routledge eBooks · doi:10.4324/9780203967430 · Cited by 21
Smiles, W. J., & CAMERA, D. M. (2017) · Acta Physiologica · doi:10.1111/apha.13004 · Cited by 15
“Peak cellular signalling events manifest within 3-4 hours post-exercise and return to baseline by ~24 hours.(124) During this post-exercise ‘window’ of heightened cellular signalling and metabolism, skeletal muscle retains its sensitivity to nutrient ingestion, in particular the anabolic effects of protein ingestion.”
BackgroundTraining for Performance: Insights From Molecular Biology
Coffey, V. G., & Hawley, J. A. (2006) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.1.3.284 · Cited by 15
Gee, T., Woolrich, T. J., & Smith, M. F. (2019) · Journal of Human Kinetics · doi:10.2478/hukin-2019-0066 · Cited by 15
“…stores, thus influencing the regulation of molecular signalling pathways such as Akt and mTOR which affect cellular growth and adaptation in response to resistance exercise, and contribute to an anabolic hormonal environment by increasing insulin (Børsheim et al., 2004; Creer et al., 2005).”
BackgroundStrength and Conditioning for Competitive Rowers
Nugent, F. J., Flanagan, E. P., Wilson, F., & Warrington, G. D. (2020) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000531 · Cited by 15
“A number of mechanisms have been proposed to explain the interference between resistance and endurance training (20,37,52,76,78,89,103).”
BackgroundAl-Shanti, N., Durcan, P. J., Al-Dabbagh, S., Dimchev, G., & Stewart, C. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000356655 · Cited by 16
Effects of time of day on resistance exercise-induced anabolic signaling in skeletal muscle
Sedliak, M., Zeman, M., Buzgó, G., Cvečka, J., Hamar, D., Laczo, E., Zelko, A., Okuliarová, M., Raastad, T., Nilsen, T. S., et al. (2012) · Biological Rhythm Research · doi:10.1080/09291016.2012.740314 · Cited by 14
“It can be speculated that low muscle glycogen levels decrease resistance exercise response of Akt phosphorylation (Creer et al. 2005) and may be thus the reason for the lack of Akt responses in some individuals in the morning in the present study.”
BackgroundCooke, M. B., Bounty, P. L., Buford, T. W., Shelmadine, B., Redd, L., Hudson, G. M., & Willoughby, D. S. (2011) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-8-18 · Cited by 11
“A series of studies have demonstrated that contractile activity either positively or negatively regulates Akt activity [15,37-39], while others failed to find any change [40-42].”
BackgroundStephens, F. B., & Tsintzas, K. (2018) · Biochemical Society Transactions · doi:10.1042/bst20170198 · Cited by 11
“Indeed, glycogen depletion has been suggested to affect metabolic gene expression (42, 43) and activation of key insulin signalling proteins (44).”
BackgroundLee, M. J.-C., Caruana, N. J., Saner, N. J., Kuang, J., Stokes, T., Mcleod, J. C., Oikawa, S. Y., Bishop, D. J., Bartlett, J. D., & Phillips, S. M. (2023) · The FASEB Journal · doi:10.1096/fj.202302024r · Cited by 12
“68,81 However, in the present study, acute periods of low muscle glycogen did not attenuate MyoPS, nor mTORC1 signaling.”
BackgroundEssén-Gustavsson, B., Granlund, A., Benziane, B., Jensen‐Waern, M., & Chibalin, A. (2011) · Experimental Physiology · doi:10.1113/expphysiol.2011.057620 · Cited by 7
“A study on humans also found that pAkt Ser(473) was more elevated after exercise when subjects had been on a high-carbohydrate diet, causing high muscle glycogen levels, than when on a low-carbohydrate diet, causing low muscle glycogen levels (Creer et al. 2005).”
BackgroundMolecular Signals and Skeletal Muscle Adaptation to Exercise
Wilson, M. D. (2013) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 5
Metadata
- Authors
- Creer, A., Gallagher, P., Slivka, D., Jemiolo, B., Fink, W., & Trappe, S.
- Affiliations
- Ball State University (US)
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 2005-09
- Volume
- 99
- Issue
- 3
- Pages
- 950-956
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W2166195206
- Cited by
- 150
- References
- 47
- Citations by year
- 2025: 1 · 2024: 3 · 2023: 5 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 8 · 2018: 3 · 2017: 7 · 2016: 6 · 2015: 7 · 2014: 18 · 2013: 10 · 2012: 9
- FWCI
- 3.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG 18409, R01AG018409)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- muscle glycogen, resistance training, ERK signaling, Akt signaling, p90 ribosomal S6 kinase, mTOR, skeletal muscle, dietary carbohydrates, muscle hypertrophy, vastus lateralis, exercise adaptation
- MeSH terms
- Adult, Dietary Carbohydrates, Glycogen, Humans, Knee Joint, Male, Muscle Contraction, Physical Endurance, Proto-Oncogene Proteins, Signal Transduction, Protein Serine-Threonine Kinases, Muscle, Skeletal, Mitogen-Activated Protein Kinase 1, Mitogen-Activated Protein Kinase 3, Proto-Oncogene Proteins c-akt
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