The order of exercise during concurrent training for rehabilitation does not alter acute genetic expression, mitochondrial enzyme activity or improvements in muscle function

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  MacNeil, Lauren G ^a   Glover, Elisa ^a   Bergstra, T Graham ^a   Safdar, Adeel ^a   Tarnopolsky, Mark A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C OXIDASE; MITOCHONDRIAL ENZYME; MUSCLE RING FINGER 1 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RHEB PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUITIN PROTEIN LIGASE NEDD4;

ADULT; AEROBIC CAPACITY; AEROBIC EXERCISE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN EXPERIMENT; KNEE BRACE; MALE; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE EXERCISE; MUSCLE FUNCTION; MUSCLE ISOMETRIC CONTRACTION; MUSCLE MASS; MUSCLE STRENGTH; NORMAL HUMAN; PROTEIN CONTENT; PROTEIN EXPRESSION; REHABILITATION; RESPIRATORY CHAIN; VASTUS LATERALIS MUSCLE; ADOLESCENT; ANATOMY AND HISTOLOGY; ENZYMOLOGY; EXERCISE; GENE EXPRESSION REGULATION; METABOLISM; MITOCHONDRIAL DYNAMICS; MUSCLE MITOCHONDRION; MUSCULOSKELETAL FUNCTION; ORGAN SIZE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIME; YOUNG ADULT;

ADOLESCENT; ADULT; EXERCISE; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; MALE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL TURNOVER; MUSCLE, SKELETAL; MUSCULOSKELETAL PHYSIOLOGICAL PHENOMENA; ORGAN SIZE; SIGNAL TRANSDUCTION; TIME FACTORS; YOUNG ADULT;

EID: 84907733041     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109189     Document Type: Article

References (66)

1. D'Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, et al. (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552: 499-511.
2. Kraemer WJ, Patton JF, Gordon SE, Harman EA, Deschenes MR, et al. (1995) Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J Appl Physiol (1985) 78: 976-989.
3. Yan Z, Lira VA, Greene NP (2012) Exercise training-induced regulation of mitochondrial quality. Exerc Sport Sci Rev 40: 159-164.
4. Di Donato DM, West DW, Churchward-Venne TA, Breen L, Baker SK, et al. (2014) Influence of aerobic exercise intensity on myofibrillar and mitochondrial protein synthesis in young men during early and late postexercise recovery. Am J Physiol Endocrinol Metab 306: E1025-1032.
5. Harber MP, Konopka AR, Douglass MD, Minchev K, Kaminsky LA, et al. (2009) Aerobic exercise training improves whole muscle and single myofiber size and function in older women. Am J Physiol Regul Integr Comp Physiol 297: R1452-1459.
6. Lundberg TR, Fernandez-Gonzalo R, Gustafsson T, Tesch PA (2012) Aerobic exercise alters skeletal muscle molecular responses to resistance exercise. Med Sci Sports Exerc 44: 1680-1688.
7. Creer A, Gallagher P, Slivka D, Jemiolo B, Fink W, et al. (2005) Influence of muscle glycogen availability on ERK1/2 and Akt signaling after resistance exercise in human skeletal muscle. J Appl Physiol (1985) 99: 950-956.
8. Hawley JA (2009) Molecular responses to strength and endurance training: are they incompatible? Appl Physiol Nutr Metab 34: 355-361.
9. Alkner BA, Tesch PA (2004) Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. Eur J Appl Physiol 93: 294-305.
10. Campbell EL, Seynnes OR, Bottinelli R, McPhee JS, Atherton PJ, et al. (2013) Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men. Biogerontology 14: 247-259.
11. Berg HE, Tesch PA (1996) Changes in muscle function in response to 10 days of lower limb unloading in humans. Acta Physiol Scand 157: 63-70.
12. Allen J, Morelli V (2011) Aging and exercise. Clin Geriatr Med 27: 661-671.
13. Baumgartner RN, Wayne SJ, Waters DL, Janssen I, Gallagher D, et al. (2004) Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res 12: 1995-2004.
14. Hvid L, Aagaard P, Justesen L, Bayer ML, Andersen JL, et al. (2010) Effects of aging on muscle mechanical function and muscle fiber morphology during shortterm immobilization and subsequent retraining. J Appl Physiol (1985) 109: 1628-1634.
15. Yasuda N, Glover EI, Phillips SM, Isfort RJ, Tarnopolsky MA (2005) Sex-based differences in skeletal muscle function and morphology with short-term limb immobilization. J Appl Physiol 99: 1085-1092.
16. de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, et al. (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585: 241-251.
17. Abadi A, Glover EI, Isfort RJ, Raha S, Safdar A, et al. (2009) Limb immobilization induces a coordinate down-regulation of mitochondrial and other metabolic pathways in men and women. PLoS One 4: e6518.
18. Adhihetty PJ, O'Leary MF, Chabi B, Wicks KL, Hood DA (2007) Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J Appl Physiol (1985) 102: 1143-1151.
19. Hakkinen K, Alen M, Kraemer WJ, Gorostiaga E, Izquierdo M, et al. (2003) Neuromuscular adaptations during concurrent strength and endurance training versus strength training. Eur J Appl Physiol 89: 42-52.
20. Hickson RC (1980) Interference of strength development by simultaneously training for strength and endurance. Eur J Appl Physiol Occup Physiol 45: 255-263.
21. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, et al. (2005) Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19: 786-788.
22. Balabinis CP, Psarakis CH, Moukas M, Vassiliou MP, Behrakis PK (2003) Early phase changes by concurrent endurance and strength training. J Strength Cond Res 17: 393-401.
23. McCarthy JP, Pozniak MA, Agre JC (2002) Neuromuscular adaptations to concurrent strength and endurance training. Med Sci Sports Exerc 34: 511-519.
24. McCarthy JP, Agre JC, Graf BK, Pozniak MA, Vailas AC (1995) Compatibility of adaptive responses with combining strength and endurance training. Med Sci Sports Exerc 27: 429-436.
25. Wilson JM, Marin PJ, Rhea MR, Wilson SM, Loenneke JP, et al. (2012) Concurrent training: a meta-analysis examining interference of aerobic and resistance exercises. J Strength Cond Res 26: 2293-2307.
26. Aagaard P, Andersen JL (2010) Effects of strength training on endurance capacity in top-level endurance athletes. Scand J Med Sci Sports 20 Suppl 2: 39-47.
27. Coffey VG, Pilegaard H, Garnham AP, O'Brien BJ, Hawley JA (2009) Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle. J Appl Physiol 106: 1187-1197.
28. Glover EI, Yasuda N, Tarnopolsky MA, Abadi A, Phillips SM (2010) Little change in markers of protein breakdown and oxidative stress in humans in immobilization-induced skeletal muscle atrophy. Appl Physiol Nutr Metab 35: 125-133.
29. Oates BR, Glover EI, West DW, Fry JL, Tarnopolsky MA, et al. (2010) Lowvolume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve 42: 539-546.
30. Coffey VG, Jemiolo B, Edge J, Garnham AP, Trappe SW, et al. (2009) 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: R1441-1451.
31. Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, et al. (2011) Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem 286: 10605-10617.
32. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, et al. (2012) A PGC- 1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151: 1319-1331.
33. Andersson U, Scarpulla RC (2001) Pgc-1-related coactivator, a novel, seruminducible coactivator of nuclear respiratory factor 1-dependent transcription in mammalian cells. Mol Cell Biol 21: 3738-3749.
34. Scarpulla RC (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14.
35. Psilander N, Wang L, Westergren J, Tonkonogi M, Sahlin K (2010) Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise. Eur J Appl Physiol 110: 597-606.
36. Wang L, Psilander N, Tonkonogi M, Ding S, Sahlin K (2009) Similar expression of oxidative genes after interval and continuous exercise. Med Sci Sports Exerc 41: 2136-2144.
37. Wang L, Mascher H, Psilander N, Blomstrand E, Sahlin K (2011) Resistance exercise enhances the molecular signaling of mitochondrial biogenesis induced by endurance exercise in human skeletal muscle. J Appl Physiol (1985) 111: 1335-1344.
38. Mathai AS, Bonen A, Benton CR, Robinson DL, Graham TE (2008) Rapid exercise-induced changes in PGC-1alpha mRNA and protein in human skeletal muscle. J Appl Physiol (1985) 105: 1098-1105.
39. Mortensen OH, Plomgaard P, Fischer CP, Hansen AK, Pilegaard H, et al. (2007) PGC-1beta is downregulated by training in human skeletal muscle: no effect of training twice every second day vs. once daily on expression of the PGC-1 family. J Appl Physiol (1985) 103: 1536-1542.
40. Hu S, Yao J, Howe AA, Menke BM, Sivitz WI, et al. (2012) Peroxisome proliferator-activated receptor gamma decouples fatty acid uptake from lipid inhibition of insulin signaling in skeletal muscle. Mol Endocrinol 26: 977-988.
41. Loviscach M, Rehman N, Carter L, Mudaliar S, Mohadeen P, et al. (2000) Distribution of peroxisome proliferator-activated receptors (PPARs) in human skeletal muscle and adipose tissue: relation to insulin action. Diabetologia 43: 304-311.
42. Park KS, Ciaraldi TP, Abrams-Carter L, Mudaliar S, Nikoulina SE, et al. (1997) PPAR-gamma gene expression is elevated in skeletal muscle of obese and type II diabetic subjects. Diabetes 46: 1230-1234.
43. Sofer A, Lei K, Johannessen CM, Ellisen LW (2005) Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol Cell Biol 25: 5834-5845.
44. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J (2002) Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 16: 1472-1487.
45. Corradetti MN, Guan KL (2006) Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 25: 6347-6360.
46. Gingras AC, Raught B, Sonenberg N (2001) Regulation of translation initiation by FRAP/mTOR. Genes Dev 15: 807-826.
47. Kimball SR, Do AN, Kutzler L, Cavener DR, Jefferson LS (2008) Rapid turnover of the mTOR complex 1 (mTORC1) repressor REDD1 and activation of mTORC1 signaling following inhibition of protein synthesis. J Biol Chem 283: 3465-3475.
48. Murakami T, Hasegawa K, Yoshinaga M (2011) Rapid induction of REDD1 expression by endurance exercise in rat skeletal muscle. Biochem Biophys Res Commun 405: 615-619.
49. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, et al. (2004) Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 18: 2893-2904.
50. Ydfors M, Fischer H, Mascher H, Blomstrand E, Norrbom J, et al. (2013) The truncated splice variants, NT-PGC-1alpha and PGC-1alpha4, increase with both endurance and resistance exercise in human skeletal muscle. Physiol Rep 1: e00140.
51. Lundberg TR, Fernandez-Gonzalo R, Norrbom J, Fischer H, Tesch PA, et al. (2014) Truncated splice variant PGC-1alpha4 is not associated with exerciseinduced human muscle hypertrophy. Acta Physiol (Oxf).
52. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, et al. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78: 761-771.
53. Favier FB, Benoit H, Freyssenet D (2008) Cellular and molecular events controlling skeletal muscle mass in response to altered use. Pflugers Arch 456: 587-600.
54. Chen YW, Gregory CM, Scarborough MT, Shi R, Walter GA, et al. (2007) Transcriptional pathways associated with skeletal muscle disuse atrophy in humans. Physiol Genomics 31: 510-520.
55. Gustafsson T, Osterlund T, Flanagan JN, von Walden F, Trappe TA, et al. (2010) Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol (1985) 109: 721-727.
56. Cunha TF, Moreira JBN, Paixao NA, Campos JC, Monteiro AWA, et al. (2012) Aerobic exercise training upregulates skeletal muscle calpain and ubiquitinproteasome systems in healthy mice. Journal of Applied Physiology 112: 1839-1846.
57. Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, 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.
58. Stefanetti RJ, Zacharewicz E, Della Gatta P, Garnham A, Russell AP, et al. (2014) Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Front Physiol 5: 30.
59. Stefanetti RJ, Lamon S, Rahbek SK, Farup J, Zacharewicz E, et al. (2014) Influence of divergent exercise contraction mode and whey protein supplementation on atrogin-1, MuRF1 and FOXO1/3A in human skeletal muscle. J Appl Physiol (1985).
60. Koncarevic A, Jackman RW, Kandarian SC (2007) The ubiquitin-protein ligase Nedd4 targets Notch1 in skeletal muscle and distinguishes the subset of atrophies caused by reduced muscle tension. FASEB J 21: 427-437.
61. Batt J, Bain J, Goncalves J, Michalski B, Plant P, et al. (2006) Differential gene expression profiling of short and long term denervated muscle. FASEB J 20: 115-117.
62. Plant PJ, Brooks D, Faughnan M, Bayley T, Bain J, et al. (2010) Cellular markers of muscle atrophy in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 42: 461-471.
63. Wang X, Blagden C, Fan J, Nowak SJ, Taniuchi I, et al. (2005) Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle. Genes Dev 19: 1715-1722.
64. Sandri M (2010) Autophagy in skeletal muscle. FEBS Lett 584: 1411-1416.
65. Wildey GM, Howe PH (2009) Runx1 is a co-activator with FOXO3 to mediate transforming growth factor beta (TGFbeta)-induced Bim transcription in hepatic cells. J Biol Chem 284: 20227-20239.
66. Suzuki N, Motohashi N, Uezumi A, Fukada S, Yoshimura T, et al. (2007) NO production results in suspension-induced muscle atrophy through dislocation of neuronal NOS. J Clin Invest 117: 2468-2476.