Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle

Journal of Applied Physiology

Volumn 106, Issue 4, 2009, Pages 1187-1197

  Coffey, Vernon G ^a   Pilegaard, Henriette ^b   Garnham, Andrew P ^c   O'Brien, Brendan J ^d   Hawley, John A ^a  

^a RMIT UNIVERSITY   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c DEAKIN UNIVERSITY   (Australia)

^d UNIVERSITY OF BALLARAT   (Australia)

Author keywords

Acute responses; Concurrent training; Endurance; Resistance exercise

Indexed keywords

ADENYLATE KINASE; ATROGIN 1; GLUCOSE; GLYCOGEN; HEXOKINASE; HEXOKINASE 2; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MYOGENIC FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE B; PROTEIN KINASE B 1; RING FINGER PROTEIN; S6 KINASE; SOMATOMEDIN C; TUBERIN; UNCLASSIFIED DRUG; RNA;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYCLING; ENDURANCE; ENZYME PHOSPHORYLATION; EXERCISE; GLUCOSE BLOOD LEVEL; GLYCOGEN MUSCLE LEVEL; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; LACTATE BLOOD LEVEL; MALE; MUSCLE BIOPSY; MUSCLE CONTRACTILITY; NORMAL HUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REST; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; ANAEROBIC THRESHOLD; BICYCLE; BIOSYNTHESIS; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CROSSOVER PROCEDURE; DIET; FITNESS; ISOLATION AND PURIFICATION; METABOLISM; MUSCLE CONTRACTION; MUSCLE STRENGTH; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WEIGHT LIFTING; WESTERN BLOTTING;

ADULT; ANAEROBIC THRESHOLD; BICYCLING; BLOOD GLUCOSE; BLOTTING, WESTERN; CROSS-OVER STUDIES; DIET; EXERCISE; GLYCOGEN; HUMANS; LACTIC ACID; MALE; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SKELETAL; PHYSICAL ENDURANCE; PHYSICAL FITNESS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION; WEIGHT LIFTING; YOUNG ADULT;

EID: 66149104031     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.91221.2008     Document Type: Article

References (66)

1. Adams GR, Cheng DC, Haddad F, Baldwin KM. Skeletal muscle hypertrophy in response to isometric, lengthening, and shortening training bouts of equivalent duration. J Appl Physiol 96: 1613-1618, 2004. (Pubitemid 38579982)
2. Adams GR, McCue SA. Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J Appl Physiol 84: 1716-1722, 1998.
3. Atherton PJ, Babraj JA, Smith K, Singh J, Rennie MJ, Wackerhage H. Selective activation of AMPK-PGC-1α or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19: 786-788, 2005. (Pubitemid 40617384)
4. Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen M, Kelly DP, Holloszy JO. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 16: 1879-1886, 2002. (Pubitemid 35462607)
5. Bamman MM, Shipp JR, Jiang J, Gower BA, Hunter GR, Goodman A, McLafferty CL Jr, Urban RJ. Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol Endocrinol Metab 280: E383-E390, 2001. (Pubitemid 32466133)
6. Bell GJ, Syrotuik DG, Martin TP, Burnham R, Quinney HA. Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentrations in humans. Eur J Appl Physiol 81: 481-1427, 2000. (Pubitemid 30189966)
7. Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA, Adams GR. Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 98: 482-488, 2005. (Pubitemid 40129955)
8. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001. (Pubitemid 33104839)
9. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawerence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001. (Pubitemid 34428747)
10. Cai SL, Tee AR, Short JD, Bergeron JM, Kim J, Shen J, Guo R, Johnson CL, Kiguchi K, Walker CL. Activity of TSC2 is inhibited by AKT-mediated phosphorylation and membrane partitioning. J Cell Biol 173: 279-289, 2006.
11. Clark SA, Chen ZP, Murphy KT, Aughey RJ, McKenna MJ, Kemp BE, Hawley JA. Intensified exercise training does not alter AMPK signaling in human skeletal muscle. Am J Physiol Endocrinol Metab 286: E737-E743, 2004.
12. Coffey VG, Hawley JA. The molecular bases of training adaptation. Sports Med 37: 737-763, 2007.
13. Coffey VG, Shield A, Canny BJ, Carey KA, Cameron-Smith D, Hawley JA. Interaction of contractile activity and training history on mRNA abundance in skeletal muscle from trained athletes. Am J Physiol Endocrinol Metab 290: E849-E855, 2006.
14. Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, Hawley JA. Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J 20: 190-192, 2005.
15. Cohen J. Statistical Power Analysis for the Behavioral Sciences. Upper Saddle River, NJ: Lawrence Erlbaum, 1988.
16. Creer A, Gallagher P, Slivka D, Jemiolo B, Fink W, Trappe S. Influence of muscle glycogen availability on ERK1/2 and Akt signaling after resistance exercise in human skeletal muscle. J Appl Physiol 99: 950-956, 2005. (Pubitemid 41214508)
17. Daussin FN, Zoll J, Ponsot E, Dufour SP, Doutreleau S, Lonsdorfer E, Ventura-Clapier R, Mettauer B, Piquard F, Geny B, Richard R. Training at high exercise intensity promotes qualitative adaptations of mitochondrial function in human skeletal muscle. J Appl Physiol 104: 1436-1441, 2008.
18. Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB. Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol 576: 613-624, 2006. (Pubitemid 44490149)
19. Eliasson J, Elfegoun T, Nilsson J, Kohnke R, Ekblom B, Blomstrand E. 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, 2006.
20. Fry AC, Schilling BK, Staron RS, Hagerman FC, Hikida RS, Thrush JT. Muscle fiber characteristics and performance correlates of male Olympic-style weightlifters. J Strength Cond Res 17: 746-754, 2003.
21. Glowacki S, Martin S, Maurer A, Baek W, Green J, Crouse S. Effects of resistance, endurance, and concurrent exercise on training outcomes in men. Med Sci Sports Exerc 36: 2119-2127, 2004. (Pubitemid 39612855)
22. Häkkinen K, Alen M, Kraemer WJ, Gorostiaga E, Izquierdo M, Rusko H, Mikkola J, Häkkinen A, Valkeinen H, Kaarakainen E, Romu S, Erola V, Ahtiainen J, Paavolainen L. Neuromuscular adaptations during concurrent strength and endurance training versus strength training. Eur J Appl Physiol 89: 42-52, 2003. (Pubitemid 36748713)
23. Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SDR. Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance training. J Physiol 547: 247-254, 2003. (Pubitemid 36285178)
24. Hawley JA. Adaptations of skeletal muscle to prolonged, intense endurance training. Clin Exp Pharmacol Physiol 29: 218-222, 2002.
25. Hawley JA, Noakes TD. Peak power output predicts maximal oxygen uptake and performance time in trained cyclists. Eur J Appl Physiol 65: 79-83, 1992.
26. Hopkins WG. Analysis of a pre-post crossover trial with adjustment for a predictor [Online]. Sportscience Available at: http://sportsci.org/resource/ stats/xPrePostCrossover.xls.
27. Hopkins WG, Marshall SW, Batterham AM, Hanin J. Progressive statistics for studies in sports medicine and exercise science. Med Sci Sports Exerc 41: 3-13, 2009.
28. Howlett KF, Mathews A, Garnham A, Sakamoto K. The effect of exercise and insulin on AS160 phosphorylation and 14-3-3 binding capacity in human skeletal muscle. Am J Physiol Endocrinol Metab 294: E401-E407, 2008.
29. Huang J, Dibble CC, Matsuzaki M, Manning BD. The TSC1-TSC2 complex is required for proper activation of mTOR complex 2. Mol Cell Biol 28: 4104-4115, 2008.
30. Izquierdo M, Hakkinen K, Ibanez J, Kraemer WJ, Gorostiaga EM. Effects of combined resistance and cardiovascular training on strength, power, muscle cross-sectional area, and endurance markers in middle-aged men. Eur J Appl Physiol 94: 70-75, 2005. (Pubitemid 41166753)
31. Jorgensen SB, Rose AJ. How is AMPK activity regulated in skeletal muscles during exercise? Front Biosci 13: 5589-5604, 2008.
32. Karlsson HKR, Nilsson PA, Nilsson J, Chibalin AV, Zierath JR, Blomstrand E. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab 287: E1-E7, 2004. (Pubitemid 38856275)
33. Koopman R, Zorenc AHG, Gransier RJJ, Cameron-Smith D, van Loon LJC. Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. ajpendo. Am J Physiol Endocrinol Metab 290: E1245-E1252, 2006. (Pubitemid 43847910)
34. Kostek MC, Chen YW, Cuthbertson DJ, Shi R, Fedele MJ, Esser KA, Rennie MJ. Gene expression responses over 24 h to lengthening and shortening contractions in human muscle: major changes in CSRP3, MUSTN1, SIX1, and FBXO32. Physiol Genomics 31: 42-52, 2007. (Pubitemid 47443847)
35. Leick L, Wojtaszewski JFP, Johansen ST, Kiilerich K, Comes G, Hellsten Y, Hidalgo J, Pilegaard H. PGC-1α is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab 294: E463-E474, 2008.
36. Leveritt MD, Abernethy PJ, Barry B, Logan PA. Concurrent strength and endurance training: the influence of dependent variable selection. J Strength Cond Res 17: 503-508, 2003. (Pubitemid 37152351)
37. Leveritt MD, Abernethy PJ, Barry BK, Logan PA. Concurrent strength and endurance training: a review. Sports Med 28: 413-427, 1999.
38. Louis E, Raue U, Yang Y, Jemiolo B, Trappe S. Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103: 1744-1751, 2007. (Pubitemid 350033861)
39. Lowry OH, Passonneau JV. Some recent refinements of quantitative histochemical analysis. Curr Probl Clin Biochem 3: 63-84, 1971.
40. Lundby C, Nordsborg N, Kusuhara K, Kristensen K, Neufer P, Pilegaard H. Gene expression in human skeletal muscle: alternative normalization method and effect of repeated biopsies. Eur J Appl Physiol 95: 351-360, 2005. (Pubitemid 43055098)
41. Mascher H, Andersson H, Nilsson PA, Ekblom B, Blomstrand E. Changes in signalling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise. Acta Physiol Scand 191: 67-75, 2007. (Pubitemid 47221194)
42. Mascher H, Tannerstedt J, Brink-Elfegoun T, Ekblom B, Gustafsson T, Blomstrand E. Repeated resistance exercise training induces different changes in mRNA expression of MAFbx and MuRF-1 in human skeletal muscle. Am J Physiol Endocrinol Metab 294: E43-E51, 2008.
43. McCarthy JP, Agre JC, Graf BK, Pozniak MA, Vailas AC. Compatibility of adaptive responses with combining strength and endurance training. Med Sci Sports Exerc 27: 429-436, 1995.
44. McCarthy JP, Pozniak MA, Agre JC. Neuromuscular adaptations to concurrent strength and endurance training. Med Sci Sports Exerc 34: 511-519, 2002.
45. McKay BR, O'Reilly CE, Phillips SM, Tarnopolsky MA, Parise G. Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle lengthening contractions in humans. J Physiol 586: 5549-5560, 2008.
46. Musaro A, McCullagh KJA, Naya FJ, Olson EN, Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400: 581-585, 1999. (Pubitemid 29381809)
47. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344: 427-431, 1999.
48. Petrella JK, Kim Js Cross JM, Kosek DJ, Bamman MM. 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, 2006.
49. Pilegaard H, Keller C, Steensberg A, Helge JW, Pedersen BK, Saltin B, Neufer PD. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J Physiol 541: 261-271, 2002. (Pubitemid 35190197)
50. Pilegaard H, Ordway GA, Saltin B, Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000.
51. Pilegaard H, Osada T, Andersen LT, Helge JW, Saltin B, Neufer PD. Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism 54: 1048-1055, 2005. (Pubitemid 41033106)
52. Psilander N, Damsgaard R, Pilegaard H. Resistance exercise alters MRF and IGF-1 mRNA content in human skeletal muscle. J Appl Physiol 95: 1038-1044, 2003. (Pubitemid 37033999)
53. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013, 2001. (Pubitemid 34428746)
54. Rosner M, Freilinger A, Hengstschlager M. Akt regulates nuclear/cytoplasmic localization of tuberin. Oncogene 26: 521-531, 2007. (Pubitemid 46160966)
55. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N, Blenis J. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates Cap-dependent translation. J Biol Chem 282: 14056-14064, 2007. (Pubitemid 47100467)
56. Ruvinsky I, Meyuhas O. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem Sci 31: 342-348, 2006. (Pubitemid 43903237)
57. Sacheck JM, Hyatt JPK, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140-155, 2007. (Pubitemid 46052553)
58. Sacheck JM, Ohtsuka A, McLary SC, Goldberg AL. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am J Physiol Endocrinol Metab 287: E591-E601, 2004. (Pubitemid 39242684)
59. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22: 159-168, 2006.
60. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the Rictor-mTOR complex. Science 307: 1098-1101, 2005.
61. Spiering BA, Anderson JM, Armstrong LE, Nindl BC, Volek JS, Judelson DA, Joseph M, Vingren JL, Hatfield DL, Fragala MS, Ho JY, Maresh CM. Effects of elevated circulating hormones on resistance exercise-induced Akt signaling. Med Sci Sports Exerc 40: 1039-1048, 2008.
62. Tesch P, Komi P, Hakkinen K. Enzymatic adaptations consequent to long-term strength training. Int J Sports Med Suppl 8: 66-69, 1987. (Pubitemid 17042327)
63. Widegren U, Jiang XJ, Krook A, Chibalin AV, Björnholm M, Tally M, Roth RA, Henriksson J, Wallberg-Henriksson H, Zierath JR. Divergent effects of exercise on metabolic and mitogenic signaling pathways in human skeletal muscle. FASEB J 12: 1379-1389, 1998. (Pubitemid 28475579)
64. Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, Rennie MJ. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586: 3701-3717, 2008.
65. Wilson C, Hargreaves M, Howlett KF. Exercise does not alter subcellular localization, but increases phosphorylation of insulin-signaling proteins in human skeletal muscle. Am J Physiol Endocrinol Metab 290: E341-E346, 2006.
66. Yang Y, Creer A, Jemiolo B, Trappe S. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98: 1745-1752, 2005. (Pubitemid 40570785)