Acute molecular responses to concurrent resistance and high-intensity interval exercise in untrained skeletal muscle

Physiological Reports

Volumn 3, Issue 4, 2015, Pages

  Pugh, Jamie K ^a   Faulkner, Steve H ^a   Jackson, Andrew P ^a   King, James A ^a   Nimmo, Myra A ^a,b  

^a LOUGHBOROUGH UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Acute responses; Cellular signaling interference; Concurrent exercise; Highintensity interval training; Human skeletal muscle

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE RING FINGER 1 PROTEIN; MYOSTATIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1;

ADULT; ARTICLE; CALORIC INTAKE; CLINICAL ARTICLE; CLINICAL TRIAL (TOPIC); CROSSOVER PROCEDURE; DOWN REGULATION; EXERCISE INTENSITY; GENE EXPRESSION; HUMAN; HUMAN EXPERIMENT; MALE; MOTOR EVOKED POTENTIAL; MUSCLE STRENGTH; NORMAL HUMAN; NUTRITIONAL ASSESSMENT; PHOSPHORYLATION; PHYSICAL ACTIVITY; PROTEIN EXPRESSION; QUALITY OF LIFE; RESISTANCE TRAINING; RNA EXTRACTION; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WESTERN BLOTTING; YOUNG ADULT;

EID: 85003671219     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12364     Document Type: Article

References (68)

1. Apró, W., L. Wang, M. Pontén, E. Blomstrand, and K. Sahlin. 2013. Resistance exercise induced mTORC1 signaling is not impaired by subsequent endurance exercise in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 305:E22–E32.
2. Arany, Z. 2008. PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr. Opin. Genet. Dev. 18:426–434.
3. Baar, K., and K. Esser. 1999. Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol. 276:C120–C127.
4. Babcock, L., M. Escano, A. D’Lugos, K. Todd, K. Murach, and N. Luden. 2012. Concurrent aerobic exercise interferes with the satellite cell response to acute resistance exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302:R1458–R1465.
5. Bamman, M. M., J. R. Shipp, J. Jiang, B. A. Gower, G. R. Hunter, A. Goodman, et al. 2001. Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am. J. Physiol. Endocrinol. Metab. 280:E383–E390.
6. Bickel, C., and J. Slade. 2005. Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J. Appl. Physiol. 98: 482–488.
7. Bickel, C. S., J. M. Slade, F. Haddad, G. R. Adams, and G. A. Dudley. 2003. Acute molecular responses of skeletal muscle to resistance exercise in able-bodied and spinal cord-injured subjects. J. Appl. Physiol. 94:2255–2262.
8. Bodine, S. C., T. N. Stitt, M. Gonzalez, W. O. Kline, G. L. Stover, R. Bauerlein, et al. 2001. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3:1014–1019.
9. Borg, G. 1998. Borg’s perceived exertion and pain scales. Human Kinetics, Champagin, IL
10. Borgenvik, M., W. Apr o, and E. Blomstrand. 2012. Intake of branched-chain amino acids influences the levels of MAFbx mRNA and MuRF-1 total protein in resting and exercising human muscle. Am. J. Physiol. Endocrinol. Metab. 302: E510–E521.
11. Browne, G. J., and C. G. Proud. 2002. Regulation of peptide- chain elongation in mammalian cells. Eur. J. Biochem. 269:5360–5368.
12. Burgomaster, K. A., K. R. Howarth, S. M. Phillips, M. Rakobowchuk, M. J. Macdonald, S. L. McGee, et al. 2008. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586:151–160.
13. Camera, D. M., D. W. D. West, S. M. Phillips, T. Rerecich, T. Stellingwerff, J. A. Hawley, et al. 2015. Protein Ingestion Increases Myofibrillar Protein Synthesis after Concurrent Exercise. Med. Sci. Sports Exerc. 47:82–91.
14. Chief Medical Office. 2011. Physical Activity Guidelines in the UK: Review and Recommendations.
15. Coffey, V. G., B. Jemiolo, J. Edge, A. P. Garnham, S. W. Trappe, and J. A. Hawley. 2009a. Effect of consecutive repeated sprint and resistance exercise bouts on acute adaptive responses in human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:R1441–R1451.
16. Coffey, V. G., H. Pilegaard, A. P. Garnham, B. J. O’Brien, and J. A. Hawley. 2009b. Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle. J. Appl. Physiol. 106:1187–1197.
17. Coyle, E. F. 2005. Very intense exercise-training is extremely potent and time efficient: a reminder. J. Appl. Physiol. 98:1983–1984.
18. Cuthbertson, D., K. Smith, J. Babraj, G. Leese, T. Waddell, P. Atherton, et al. 2005. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 19:422–424.
19. Deldicque, L., K. De Bock, M. Maris, M. Ramaekers, H. Nielens, M. Francaux, et al. 2009. Increased p70s6k phosphorylation during intake of a protein–carbohydrate drink following resistance exercise in the fasted state. Eur. J. Appl. Physiol. 108:791–800.
20. Donges, C. E., N. A. Burd, R. Duffield, G. C. Smith, D. W. D. West, M. J. Short, et al. 2012. Concurrent resistance and aerobic exercise stimulates both myofibrillar and mitochondrial protein synthesis in sedentary middle-aged men. J. Appl. Physiol. 112:1992–2001.
21. Dreyer, H. C., S. Fujita, J. G. Cadenas, D. L. Chinkes, E. Volpi, and B. B. Rasmussen. 2006. Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J. Physiol. 576:613–624.
22. Dreyer, H. C., M. J. Drummond, B. Pennings, S. Fujita, E. L. Glynn, D. L. Chinkes, et al. 2008. Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am. J. Physiol. Endocrinol. Metab. 294: E392–E400.
23. Dreyer, H. C., S. Fujita, E. L. Glynn, M. J. Drummond, E. Volpi, and B. B. Rasmussen. 2010. Resistance exercise increases leg muscle protein synthesis and mTOR signalling independent of sex. Acta Physiol. 199:71–81.
24. Egan, B., and J. R. Zierath. 2013. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17:162–184.
25. Eliasson, J., T. Elfegoun, J. Nilsson, R. K € ohnke, B. Ekblom, and E. Blomstrand. 2006. Maximal lengthening contractions increase p70 S6 kinase phosphorylation in human skeletal muscle in the absence of nutritional supply. Am. J. Physiol. Endocrinol. Metab. 291:E1197–E1205.
26. Foletta, V. C., L. J. White, A. E. Larsen, B. L eger, and A. P. Russell. 2011. The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy. Pfl € ugers Arch. 461:325–335.
27. Fujita, S., H. C. Dreyer, M. J. Drummond, E. L. Glynn, J. G. Cadenas, F. Yoshizawa, et al. 2007. Nutrient signalling in the regulation of human muscle protein synthesis. J. Physiol. 582:813–823.
28. Garber, C. E., B. Blissmer, M. R. Deschenes, B. A. Franklin, M. J. Lamonte, I.-M. Lee, et al. 2011. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med. Sci. Sports Exerc. 43:1334–1359.
29. Gibala, M. J., J. P. Little, M. van Essen, G. P. Wilkin, K. A. Burgomaster, A. Safdar, et al. 2006. Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J. Physiol. 575:901–911.
30. Gibala, M. J., J. P. Little, M. J. Macdonald, and J. A. Hawley. 2012. Physiological adaptations to low-volume, high- intensity interval training in health and disease. J. Physiol. 590:1077–1084.
31. Gillen, J. B., M. E. Percival, A. Ludzki, M. A. Tarnopolsky, and M. J. Gibala. 2013. Interval training in the fed or fasted state improves body composition and muscle oxidative capacity in overweight women. Obesity 21:2249–2255.
32. Haddad, F., and G. R. Adams. 2002. Selected contribution: acute cellular and molecular responses to resistance exercise. J. Appl. Physiol. 93:394–403.
33. Hameed, M., R. W. Orrell, M. Cobbold, G. Goldspink, and S. D. R. Harridge. 2003. Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J. Physiol. 547:247–254.
34. Harber, M., A. Konopka, B. Jemiolo, S. Trappe, T. Trappe, and P. Reidy. 2010. Muscle protein synthesis and gene expression during recovery from aerobic exercise in the fasted and fed states. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299:R1254–R1262.
35. Heydari, M., J. Freund, and S. H. Boutcher. 2012. The effect of high-intensity intermittent exercise on body composition of overweight young males. J. Obes. 480467–74:2012
36. Hickson, R. C. 1980. Interference of strength development by simultaneously training for strength and endurance. Eur. J. Appl. Physiol. 263:255–263.
37. Kapp, L. D., and J. R. Lorsch. 2004. The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73:657–704.
38. Koopman, R., B. Pennings, A. H. G. Zorenc, and L. J. C. van Loon. 2007. Protein ingestion further augments S6K1 phosphorylation in skeletal muscle following resistance type exercise in males. J. Nutr. 137:1880–1886.
39. Kraemer, W., K. Adams, E. Cafarelli, G. Dudley, C. Dooly, M. Feigenbaum, et al. 2009. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med. Sci. Sports Exerc. 41:687–708.
40. Leger, B., R. Cartoni, M. Praz, S. Lamon, O. D eriaz, A. Crettenand, et al. 2006. Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 576:923–933.
41. Leveritt, M., P. J. Abernethy, B. K. Barry, and P. A. Logan. 1999. Concurrent strength and endurance training. A review. Sports Med. 28:413–427.
42. Little, J. P., A. Safdar, G. P. Wilkin, M. A. Tarnopolsky, and M. J. Gibala. 2010. A practical model of low-volume high- intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J. Physiol. 588:1011–1022.
43. Lopez-Miranda, J., C. Williams, and D. Lairon. 2007. Dietary, physiological, genetic and pathological influences on postprandial lipid metabolism. Br. J. Nutr. 98:458–473.
44. Louis, E., U. Raue, Y. Yang, B. Jemiolo, and S. Trappe. 2007. Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 103:1744–1751.
45. Lundberg, T. R., R. Fernandez-Gonzalo, T. Gustafsson, and P. A. Tesch. 2012. Aerobic exercise alters skeletal muscle molecular responses to resistance exercise. Med. Sci. Sports Exerc. 44:1680–1688.
46. Lundberg, T. R., R. Fernandez-Gonzalo, T. Gustafsson, and P. A. Tesch. 2013. Aerobic exercise does not compromise muscle hypertrophy response to short-term resistance training. J. Appl. Physiol. 114:81–89.
47. Lundberg, T. R., R. Fernandez-Gonzalo, J. Norrbom, H. Fischer, P. A. Tesch, and T. Gustafsson. 2014. Truncated splice variant PGC-1 a 4 is not associated with exercise- induced human muscle hypertrophy. Acta Physiol. 212:142–151.
48. McGee, S. L., and M. Hargreaves. 2010. AMPK-mediated regulation of transcription in skeletal muscle. Clin. Sci. 118:507–518.
49. McPherron, A. C., A. M. Lawler, and S. J. Lee. 1997. Regulation of skeletal muscle mass in mice by a new TGF- beta superfamily member. Nature 387:83–90.
50. Mifflin, M. D., S. T. St Jeor, L. A. Hill, B. J. Scott, S. A. Daugherty, and Y. O. Koh. 1990. A new predictive equation for resting energy expenditure in healthy individuals. Am. J. Clin. Nutr. 51:241–247.
51. Miller, S. L., K. D. Tipton, D. L. Chinkes, S. E. Wolf, and R. R. Wolfe. 2003. Independent and combined effects of amino acids and glucose after resistance exercise. Med. Sci. Sports Exerc. 35:449–455.
52. Nybo, L., E. Sundstrup, M. D. Jakobsen, M. Mohr, T. Hornstrup, L. Simonsen, et al. 2010. High-intensity training versus traditional exercise interventions for promoting health. Med. Sci. Sports Exerc. 42:1951–1958.
53. Olesen, J., K. Kiilerich, and H. Pilegaard. 2010. PGC-1alpha- mediated adaptations in skeletal muscle. Pflugers Arch. 460:153–162.
54. Perry, R. L., and M. A. Rudnick. 2000. Molecular mechanisms regulating myogenic determination and differentiation. Front Biosci. 5:d750–d767.
55. Petrella, J. K., J. Kim, J. M. Cross, D. J. Kosek, and M. M. Bamman. 2006. Efficacy of myonuclear addition may explain differential myofiber growth among resistance- trained young and older men and women. Am. J. Physiol. Endocrinol. Metab. 291:E937–E946
56. Psilander, N., R. Damsgaard, and H. Pilegaard. 2003. Resistance exercise alters MRF and IGF-I mRNA content in human skeletal muscle. J. Appl. Physiol. 95:1038–1044.
57. Ruas, J. L., J. P. White, R. R. Rao, S. Kleiner, K. T. Brannan, B. C. Harrison, et al. 2012. A PGC-1 a isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151:1319–1331.
58. Sandri, M., C. Sandri, A. Gilbert, C. Skurk, E. Calabria, A. Picard, et al. 2004. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399–412.
59. Sandri, M., J. Lin, C. Handschin, W. Yang, Z. P. Arany, S. H. Lecker, et al. 2006. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy- specific gene transcription. Proc. Natl Acad. Sci. USA 103:16260–16265.
60. Stutts, W. C. 2002. Physical activity determinants in adults. Perceived benefits, barriers, and self efficacy. AAOHN J. 50:499–507.
61. Tadaishi, M., S. Miura, Y. Kai, E. Kawasaki, K. Koshinaka, K. Kawanaka, et al. 2011. Effect of exercise intensity and AICAR on isoform-specific expressions of murine skeletal muscle PGC-1 a mRNA: a role of b₂ -adrenergic receptor activation. Am. J. Physiol. Endocrinol. Metab. 300:E341–E349.
62. Tipton, K. D., A. A. Ferrando, S. M. Phillips, D. Doyle, and R. R. Wolfe. 1999. Postexercise net protein synthesis in human muscle from orally administered amino acids. Am. J. Physiol. 276:E628–E634.
63. Trapp, E. G., D. J. Chisholm, J. Freund, and S. H. Boutcher. 2008. The effects of high-intensity intermittent exercise training on fat loss and fasting insulin levels of young women. Int. J. Obes. 32:684–691.
64. Trost, S. G., N. Owen, A. E. Bauman, J. F. Sallis, and W. Brown. 2002. Correlates of adults’ participation in physical activity: review and update. Med. Sci. Sports Exerc. 34:1996–2001.
65. Welle, S., K. Burgess, and S. Mehta. 2009. Stimulation of skeletal muscle myofibrillar protein synthesis, p70 S6 kinase phosphorylation, and ribosomal protein S6 phosphorylation by inhibition of myostatin in mature mice. Am. J. Physiol. Endocrinol. Metab. 296:E567–E572.
66. Wilson, J. J. M., P. J. P. Marin, M. R. Rhea, S. M. C. Wilson, J. P. Loenneke, and J. C. Anderson. 2012. Concurrent training: a meta-analysis examining interference of aerobic and resistance exercises. J. Strength Cond. Res. 26:2293–2307.
67. Yang, Y., A. Creer, B. Jemiolo, and S. Trappe. 2005. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J. Appl. Physiol. 98:1745–1752.
68. Zanuso, S., A. Jimenez, G. Pugliese, G. Corigliano, and S. Balducci. 2010. Exercise for the management of type 2 diabetes: a review of the evidence. Acta Diabetol. 47:15–22.