Acute sprint exercise transcriptome in human skeletal muscle
Autoři:
Hakan Claes Rundqvist aff001; Andreas Montelius aff001; Ted Osterlund aff001; Barbara Norman aff001; Mona Esbjornsson aff001; Eva Jansson aff001
Působiště autorů:
Division of Clinical Physiology, Karolinska Institutet, Stockholm, Sweden
aff001; Department of Laboratory Medicine, Karolinska Institutet, Stockholm, Sweden
aff002; Department of Clinical Physiology, Karolinska University Hospital, Stockholm, Sweden
aff003
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223024
Souhrn
Aim
To examine global gene expression response to profound metabolic and hormonal stress induced by acute sprint exercise.
Methods
Healthy men and women (n = 14) performed three all-out cycle sprints interspersed by 20 min recovery. Muscle biopsies were obtained before the first, and 2h and 20 min after last sprint. Microarray analysis was performed to analyse acute gene expression response and repeated blood samples were obtained.
Results
In skeletal muscle, a set of immediate early genes, FOS, NR4A3, MAFF, EGR1, JUNB were markedly upregulated after sprint exercise. Gene ontology analysis from 879 differentially expressed genes revealed predicted activation of various upstream regulators and downstream biofunctions. Gene signatures predicted an enhanced turnover of skeletal muscle mass after sprint exercise and some novel induced genes such as WNT9A, FZD7 and KLHL40 were presented. A substantial increase in circulating free fatty acids (FFA) was noted after sprint exercise, in parallel with upregulation of PGC-1A and the downstream gene PERM1 and gene signatures predicting enhanced lipid turnover. Increase in growth hormone and insulin in blood were related to changes in gene expressions and both hormones were predicted as upstream regulators.
Conclusion
This is the first study reporting global gene expression in skeletal muscle in response to acute sprint exercise and several novel findings are presented. First, in line with that muscle hypertrophy is not a typical finding after a period of sprint training, both hypertrophy and atrophy factors were regulated. Second, systemic FFA and hormonal and exposure might be involved in the sprint exercise-induced changes in gene expression.
Klíčová slova:
Blood – Exercise – Fatty acids – Gene expression – Gene regulation – Insulin – Regulator genes – Skeletal muscles
Zdroje
1. Esbjornsson-Liljedahl M, Bodin K, Jansson E. Smaller muscle ATP reduction in women than in men by repeated bouts of sprint exercise. J Appl Physiol. 2002;93(3):1075–83. doi: 10.1152/japplphysiol.00732.1999 12183505.
2. Esbjornsson M, Rundqvist HC, Mascher H, Osterlund T, Rooyackers O, Blomstrand E, et al. Sprint exercise enhances skeletal muscle p70S6k phosphorylation and more so in women than in men. Acta Physiol (Oxf). 2012;205(3):411–22. Epub 2012/01/25. doi: 10.1111/j.1748-1716.2012.02404.x 22268492.
3. Esbjornsson M, Norman B, Suchdev S, Viru M, Lindhgren A, Jansson E. Greater growth hormone and insulin response in women than in men during repeated bouts of sprint exercise. Acta Physiol (Oxf). 2009;197(2):107–15. doi: 10.1111/j.1748-1716.2009.01994.x 19432586.
4. Norman B, Nygren AT, Nowak J, Sabina RL. The effect of AMPD1 genotype on blood flow response to sprint exercise. Eur J Appl Physiol. 2008;103(2):173–80. doi: 10.1007/s00421-008-0683-0 18224333.
5. Gibala MJ, Little JP, Macdonald MJ, Hawley JA. Physiological adaptations to low-volume, high-intensity interval training in health and disease. J Physiol. 2012;590(5):1077–84. Epub 2012/02/01. doi: 10.1113/jphysiol.2011.224725 22289907.
6. Burgomaster KA, Hughes SC, Heigenhauser GJ, Bradwell SN, Gibala MJ. Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans. J Appl Physiol (1985). 2005;98(6):1985–90. doi: 10.1152/japplphysiol.01095.2004 15705728.
7. Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle. J Appl Physiol (1985). 2009;106(3):929–34. doi: 10.1152/japplphysiol.90880.2008 19112161.
8. Ross A, Leveritt M. Long-term metabolic and skeletal muscle adaptations to short-sprint training: implications for sprint training and tapering. Sports medicine (Auckland, NZ. 2001;31(15):1063–82. doi: 10.2165/00007256-200131150-00003 11735686.
9. Joanisse S, McKay BR, Nederveen JP, Scribbans TD, Gurd BJ, Gillen JB, et al. Satellite cell activity, without expansion, after nonhypertrophic stimuli. Am J Physiol-Reg I. 2015;309(9):R1101–11. doi: 10.1152/ajpregu.00249.2015 26333785.
10. Coffey VG, Moore DR, Burd NA, Rerecich T, Stellingwerff T, Garnham AP, et al. Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints. Eur J Appl Physiol. 2011;111(7):1473–83. doi: 10.1007/s00421-010-1768-0 21165642.
11. Cocks M, Shaw CS, Shepherd SO, Fisher JP, Ranasinghe AM, Barker TA, et al. Sprint interval and endurance training are equally effective in increasing muscle microvascular density and eNOS content in sedentary males. J Physiol. 2013;591(3):641–56. doi: 10.1113/jphysiol.2012.239566 22946099.
12. Hoier B, Passos M, Bangsbo J, Hellsten Y. Intense intermittent exercise provides weak stimulus for vascular endothelial growth factor secretion and capillary growth in skeletal muscle. Experimental physiology. 2013;98(2):585–97. doi: 10.1113/expphysiol.2012.067967 22962287.
13. Hoppeler H, Baum O, Lurman G, Mueller M. Molecular mechanisms of muscle plasticity with exercise. Compr Physiol. 2011;1(3):1383–412. doi: 10.1002/cphy.c100042 23733647.
14. Fluck M. Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. The Journal of experimental biology. 2006;209(Pt 12):2239–48. doi: 10.1242/jeb.02149 16731801.
15. Vissing K, Schjerling P. Simplified data access on human skeletal muscle transcriptome responses to differentiated exercise. Sci Data. 2014;1:140041. doi: 10.1038/sdata.2014.41 25984345.
16. Esbjornsson-Liljedahl M, Bodin K, Jansson E. Smaller muscle ATP reduction in women than in men by repeated bouts of sprint exercise. J Appl Physiol (1985). 2002;93(3):1075–83. doi: 10.1152/japplphysiol.00732.1999 12183505.
17. Kumar A, Davuluri G, Silva RNE, Engelen M, Ten Have GAM, Prayson R, et al. Ammonia lowering reverses sarcopenia of cirrhosis by restoring skeletal muscle proteostasis. Hepatology. 2017;65(6):2045–58. doi: 10.1002/hep.29107 28195332.
18. von Maltzahn J, Bentzinger CF, Rudnicki MA. Wnt7a-Fzd7 signalling directly activates the Akt/mTOR anabolic growth pathway in skeletal muscle. Nature cell biology. 2011;14(2):186–91. doi: 10.1038/ncb2404 22179044.
19. Bowlin KM, Embree LJ, Garry MG, Garry DJ, Shi X. Kbtbd5 is regulated by MyoD and restricted to the myogenic lineage. Differentiation. 2013;86(4–5):184–91. doi: 10.1016/j.diff.2013.08.002 24361185.
20. Hitachi K, Nakatani M, Tsuchida K. Myostatin signaling regulates Akt activity via the regulation of miR-486 expression. The international journal of biochemistry & cell biology. 2014;47:93–103. doi: 10.1016/j.biocel.2013.12.003 24342526.
21. Clasen BF, Krusenstjerna-Hafstrom T, Vendelbo MH, Thorsen K, Escande C, Moller N, et al. Gene expression in skeletal muscle after an acute intravenous GH bolus in human subjects: identification of a mechanism regulating ANGPTL4. J Lipid Res. 2013;54(7):1988–97. doi: 10.1194/jlr.P034520 23606725.
22. Huffman KM, Jessee R, Andonian B, Davis BN, Narowski R, Huebner JL, et al. Molecular alterations in skeletal muscle in rheumatoid arthritis are related to disease activity, physical inactivity, and disability. Arthritis Res Ther. 2017;19(1):12. doi: 10.1186/s13075-016-1215-7 28114971.
23. Garg A, O'Rourke J, Long C, Doering J, Ravenscroft G, Bezprozvannaya S, et al. KLHL40 deficiency destabilizes thin filament proteins and promotes nemaline myopathy. The Journal of clinical investigation. 2014;124(8):3529–39. doi: 10.1172/JCI74994 24960163.
24. Khachigian LM. Early growth response-1 in cardiovascular pathobiology. Circulation research. 2006;98(2):186–91. doi: 10.1161/01.RES.0000200177.53882.c3 16456111.
25. Freyssenet D, Irrcher I, Connor MK, Di Carlo M, Hood DA. Calcium-regulated changes in mitochondrial phenotype in skeletal muscle cells. Am J Physiol Cell Physiol. 2004;286(5):C1053–61. doi: 10.1152/ajpcell.00418.2003 15075204.
26. Lee YS, Jang HS, Kim JM, Lee JS, Lee JY, Li Kim K, et al. Adenoviral-mediated delivery of early growth response factor-1 gene increases tissue perfusion in a murine model of hindlimb ischemia. Mol Ther. 2005;12(2):328–36. doi: 10.1016/j.ymthe.2005.03.027 16043101.
27. McLean CS, Mielke C, Cordova JM, Langlais PR, Bowen B, Miranda D, et al. Gene and MicroRNA Expression Responses to Exercise; Relationship with Insulin Sensitivity. PloS one. 2015;10(5):e0127089. doi: 10.1371/journal.pone.0127089 25984722.
28. Edgett BA, Foster WS, Hankinson PB, Simpson CA, Little JP, Graham RB, et al. Dissociation of increases in PGC-1alpha and its regulators from exercise intensity and muscle activation following acute exercise. PloS one. 2013;8(8):e71623. doi: 10.1371/journal.pone.0071623 23951207.
29. van Rossum DB, Patterson RL, Cheung KH, Barrow RK, Syrovatkina V, Gessell GS, et al. DANGER, a novel regulatory protein of inositol 1,4,5-trisphosphate-receptor activity. The Journal of biological chemistry. 2006;281(48):37111–6. doi: 10.1074/jbc.M608760200 16990268.
30. Carrasco MA, Hidalgo C. Calcium microdomains and gene expression in neurons and skeletal muscle cells. Cell Calcium. 2006;40(5–6):575–83. doi: 10.1016/j.ceca.2006.08.021 17034850.
31. Carrasco MA, Jaimovich E, Kemmerling U, Hidalgo C. Signal transduction and gene expression regulated by calcium release from internal stores in excitable cells. Biol Res. 2004;37(4):701–12. doi: 10.4067/s0716-97602004000400028 15709700.
32. Wackerhage H, Schoenfeld BJ, Hamilton DL, Lehti M, Hulmi JJ. Stimuli and sensors that initiate skeletal muscle hypertrophy following resistance exercise. J Appl Physiol (1985). 2019;126(1):30–43. doi: 10.1152/japplphysiol.00685.2018 30335577.
33. Chaillou T, Jackson JR, England JH, Kirby TJ, Richards-White J, Esser KA, et al. Identification of a conserved set of upregulated genes in mouse skeletal muscle hypertrophy and regrowth. J Appl Physiol (1985). 2015;118(1):86–97. doi: 10.1152/japplphysiol.00351.2014 25554798.
34. Lamon S, Wallace MA, Russell AP. The STARS signaling pathway: a key regulator of skeletal muscle function. Pflugers Arch. 2014;466(9):1659–71. doi: 10.1007/s00424-014-1475-5 24557714.
35. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, et al. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. The Journal of biological chemistry. 2005;280(20):19587–93. doi: 10.1074/jbc.M408862200 15767263.
36. Drake JC, Wilson RJ, Yan Z. Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle. FASEB J. 2016;30(1):13–22. doi: 10.1096/fj.15-276337 26370848.
37. Hood DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. The Journal of experimental biology. 2006;209(Pt 12):2265–75. doi: 10.1242/jeb.02182 16731803.
38. Wende AR, Huss JM, Schaeffer PJ, Giguere V, Kelly DP. PGC-1alpha coactivates PDK4 gene expression via the orphan nuclear receptor ERRalpha: a mechanism for transcriptional control of muscle glucose metabolism. Molecular and cellular biology. 2005;25(24):10684–94. doi: 10.1128/MCB.25.24.10684-10694.2005 16314495.
39. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell metabolism. 2005;1(6):361–70. doi: 10.1016/j.cmet.2005.05.004 16054085.
40. Schnyder S, Handschin C. Skeletal muscle as an endocrine organ: PGC-1alpha, myokines and exercise. Bone. 2015;80:115–25. doi: 10.1016/j.bone.2015.02.008 26453501.
41. Cho Y, Hazen BC, Gandra PG, Ward SR, Schenk S, Russell AP, et al. Perm1 enhances mitochondrial biogenesis, oxidative capacity, and fatigue resistance in adult skeletal muscle. FASEB J. 2016;30(2):674–87. doi: 10.1096/fj.15-276360 26481306.
42. Cho Y, Hazen BC, Russell AP, Kralli A. Peroxisome proliferator-activated receptor gamma coactivator 1 (PGC-1)- and estrogen-related receptor (ERR)-induced regulator in muscle 1 (Perm1) is a tissue-specific regulator of oxidative capacity in skeletal muscle cells. The Journal of biological chemistry. 2013;288(35):25207–18. doi: 10.1074/jbc.M113.489674 23836911.
43. Neubauer O, Sabapathy S, Ashton KJ, Desbrow B, Peake JM, Lazarus R, et al. Time course-dependent changes in the transcriptome of human skeletal muscle during recovery from endurance exercise: from inflammation to adaptive remodeling. J Appl Physiol (1985). 2014;116(3):274–87. doi: 10.1152/japplphysiol.00909.2013 24311745.
44. Raue U, Trappe TA, Estrem ST, Qian HR, Helvering LM, Smith RC, et al. Transcriptome signature of resistance exercise adaptations: mixed muscle and fiber type specific profiles in young and old adults. J Appl Physiol (1985). 2012;112(10):1625–36. doi: 10.1152/japplphysiol.00435.2011 22302958.
45. Mahoney DJ, Tarnopolsky MA. Understanding skeletal muscle adaptation to exercise training in humans: contributions from microarray studies. Phys Med Rehabil Clin N Am. 2005;16(4):859–73, vii. doi: 10.1016/j.pmr.2005.08.018 16214048.
46. Wiik A, Gustafsson T, Esbjornsson M, Johansson O, Ekman M, Sundberg CJ, et al. Expression of oestrogen receptor alpha and beta is higher in skeletal muscle of highly endurance-trained than of moderately active men. Acta Physiol Scand. 2005;184(2):105–12. doi: 10.1111/j.1365-201X.2005.01433.x 15916670.
47. Catoire M, Alex S, Paraskevopulos N, Mattijssen F, Evers-van Gogh I, Schaart G, et al. Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(11):E1043–52. doi: 10.1073/pnas.1400889111 24591600.
48. Ferre P. The biology of peroxisome proliferator-activated receptors: relationship with lipid metabolism and insulin sensitivity. Diabetes. 2004;53 Suppl 1:S43–50. doi: 10.2337/diabetes.53.2007.s43 14749265.
49. Norheim F, Hjorth M, Langleite TM, Lee S, Holen T, Bindesboll C, et al. Regulation of angiopoietin-like protein 4 production during and after exercise. Physiol Rep. 2014;2(8). doi: 10.14814/phy2.12109 25138789.
50. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387(6628):83–90. doi: 10.1038/387083a0 9139826.
51. Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. The Journal of biological chemistry. 2002;277(51):49831–40. doi: 10.1074/jbc.M204291200 12244043.
52. Liu W, Thomas SG, Asa SL, Gonzalez-Cadavid N, Bhasin S, Ezzat S. Myostatin is a skeletal muscle target of growth hormone anabolic action. The Journal of clinical endocrinology and metabolism. 2003;88(11):5490–6. doi: 10.1210/jc.2003-030497 14602795.
53. MacKenzie MG, Hamilton DL, Pepin M, Patton A, Baar K. Inhibition of myostatin signaling through Notch activation following acute resistance exercise. PloS one. 2013;8(7):e68743. doi: 10.1371/journal.pone.0068743 23844238.
54. Sartori R, Milan G, Patron M, Mammucari C, Blaauw B, Abraham R, et al. Smad2 and 3 transcription factors control muscle mass in adulthood. Am J Physiol Cell Physiol. 2009;296(6):C1248–57. doi: 10.1152/ajpcell.00104.2009 19357234.
55. Forbes D, Jackman M, Bishop A, Thomas M, Kambadur R, Sharma M. Myostatin auto-regulates its expression by feedback loop through Smad7 dependent mechanism. Journal of cellular physiology. 2006;206(1):264–72. doi: 10.1002/jcp.20477 16110474.
56. McFarlane C, Vajjala A, Arigela H, Lokireddy S, Ge X, Bonala S, et al. Negative auto-regulation of myostatin expression is mediated by Smad3 and microRNA-27. PloS one. 2014;9(1):e87687. doi: 10.1371/journal.pone.0087687 24498167.
57. Kim JS, Petrella JK, Cross JM, Bamman MM. Load-mediated downregulation of myostatin mRNA is not sufficient to promote myofiber hypertrophy in humans: a cluster analysis. J Appl Physiol (1985). 2007;103(5):1488–95. doi: 10.1152/japplphysiol.01194.2006 17673556.
58. Matsumoto K, Miki R, Nakayama M, Tatsumi N, Yokouchi Y. Wnt9a secreted from the walls of hepatic sinusoids is essential for morphogenesis, proliferation, and glycogen accumulation of chick hepatic epithelium. Developmental biology. 2008;319(2):234–47. doi: 10.1016/j.ydbio.2008.04.021 18513713.
59. Di Padova M, Caretti G, Zhao P, Hoffman EP, Sartorelli V. MyoD acetylation influences temporal patterns of skeletal muscle gene expression. The Journal of biological chemistry. 2007;282(52):37650–9. doi: 10.1074/jbc.M707309200 17965412.
60. Cirillo F, Resmini G, Ghiroldi A, Piccoli M, Bergante S, Tettamanti G, et al. Activation of the hypoxia-inducible factor 1alpha promotes myogenesis through the noncanonical Wnt pathway, leading to hypertrophic myotubes. FASEB J. 2017;31(5):2146–56. doi: 10.1096/fj.201600878R 28188178.
61. Tipton KD, Hamilton DL, Gallagher IJ. Assessing the Role of Muscle Protein Breakdown in Response to Nutrition and Exercise in Humans. Sports medicine (Auckland, NZ. 2018;48(Suppl 1):53–64. doi: 10.1007/s40279-017-0845-5 29368185.
62. Moro T, Ebert SM, Adams CM, Rasmussen BB. Amino Acid Sensing in Skeletal Muscle. Trends Endocrinol Metab. 2016;27(11):796–806. doi: 10.1016/j.tem.2016.06.010 27444066.
63. Egerman MA, Glass DJ. Signaling pathways controlling skeletal muscle mass. Crit Rev Biochem Mol Biol. 2014;49(1):59–68. doi: 10.3109/10409238.2013.857291 24237131.
64. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013;280(17):4294–314. doi: 10.1111/febs.12253 23517348.
65. Raffaello A, Milan G, Masiero E, Carnio S, Lee D, Lanfranchi G, et al. JunB transcription factor maintains skeletal muscle mass and promotes hypertrophy. J Cell Biol. 2010;191(1):101–13. doi: 10.1083/jcb.201001136 20921137.
66. Chen YW, Nader GA, Baar KR, Fedele MJ, Hoffman EP, Esser KA. Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling. J Physiol. 2002;545(1):27–41. doi: 10.1113/jphysiol.2002.021220 12433947.
67. Liu W, Wen Y, Bi P, Lai X, Liu XS, Liu X, et al. Hypoxia promotes satellite cell self-renewal and enhances the efficiency of myoblast transplantation. Development. 2012;139(16):2857–65. doi: 10.1242/dev.079665 22764051.
68. Chan HH, Burns SF. Oxygen consumption, substrate oxidation, and blood pressure following sprint interval exercise. Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme. 2013;38(2):182–7. doi: 10.1139/apnm-2012-0136 23438230.
69. Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuk M, Macdonald MJ, McGee SL, et al. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol. 2008;586(1):151–60. doi: 10.1113/jphysiol.2007.142109 17991697.
70. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 2005;19(11):1498–500. doi: 10.1096/fj.04-3149fje 15985525.
71. Stocks B, Dent JR, Ogden HB, Zemp M, Philp A. Postexercise skeletal muscle signaling responses to moderate- to high-intensity steady-state exercise in the fed or fasted state. American journal of physiology. 2019;316(2):E230–E8. doi: 10.1152/ajpendo.00311.2018 30512989.
72. Rundqvist HC, Esbjornsson M, Rooyackers O, Osterlund T, Moberg M, Apro W, et al. Influence of nutrient ingestion on amino acid transporters and protein synthesis in human skeletal muscle after sprint exercise. J Appl Physiol (1985). 2017;123(6):1501–15. doi: 10.1152/japplphysiol.00244.2017 28860165.
73. Olfert IM, Birot O. Importance of anti-angiogenic factors in the regulation of skeletal muscle angiogenesis. Microcirculation. 2011;18(4):316–30. doi: 10.1111/j.1549-8719.2011.00092.x 21418382.
74. Olfert IM, Baum O, Hellsten Y, Egginton S. Advances and challenges in skeletal muscle angiogenesis. Am J Physiol Heart Circ Physiol. 2016;310(3):H326–36. doi: 10.1152/ajpheart.00635.2015 26608338.
75. Gustafsson T, Kraus WE. Exercise-induced angiogenesis-related growth and transcription factors in skeletal muscle, and their modification in muscle pathology. Front Biosci. 2001;6:D75–89. doi: 10.2741/gustafss 11145922.
76. Miyamoto-Mikami E, Tsuji K, Horii N, Hasegawa N, Fujie S, Homma T, et al. Gene expression profile of muscle adaptation to high-intensity intermittent exercise training in young men. Sci Rep. 2018;8(1):16811. doi: 10.1038/s41598-018-35115-x 30429512.
77. Stretch C, Khan S, Asgarian N, Eisner R, Vaisipour S, Damaraju S, et al. Effects of sample size on differential gene expression, rank order and prediction accuracy of a gene signature. PloS one. 2013;8(6):e65380. doi: 10.1371/journal.pone.0065380 23755224.
78. Friedmann-Bette B, Schwartz FR, Eckhardt H, Billeter R, Bonaterra G, Kinscherf R. Similar changes of gene expression in human skeletal muscle after resistance exercise and multiple fine needle biopsies. J Appl Physiol (1985). 2012;112(2):289–95. doi: 10.1152/japplphysiol.00959.2011 22052872.
79. Constantin-Teodosiu D, Casey A, Short AH, Hultman E, Greenhaff PL. The effect of repeated muscle biopsy sampling on ATP and glycogen resynthesis following exercise in man. European journal of applied physiology and occupational physiology. 1996;73(1–2):186–90. doi: 10.1007/bf00262830 8861690.
80. Van Thienen R, D'Hulst G, Deldicque L, Hespel P. Biochemical artifacts in experiments involving repeated biopsies in the same muscle. Physiol Rep. 2014;2(5):e00286. doi: 10.14814/phy2.286 24819751.
81. Vissing K, Andersen JL, Schjerling P. Are exercise-induced genes induced by exercise? FASEB J. 2005;19(1):94–6. doi: 10.1096/fj.04-2084fje 15516373.
82. Jansson E, Hedberg G. Skeletal muscle fibre types in teenagers: relationship to physical performance and activity. Scandinavian journal of medicine & science in sports. 1991;1(1):31–44.
83. Bar-Or O, Dotan R, Inbar O, Rothstein A, Karlsson J, Tesch P. Anaerobic Capacity and Muscle Fiber Type Distribution in Man. International journal of sports medicine. 1980;1:82–5.
84. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest. 1975;35(7):609–16. 1108172.
85. van Anken HC, Schiphorst ME. A kinetic determination of ammonia in plasma. Clinica chimica acta; international journal of clinical chemistry. 1974;56(2):151–7. doi: 10.1016/0009-8981(74)90223-x 4154813.
86. Schantz P, Billeter R, Henriksson J, Jansson E. Training-induced increase in myofibrillar ATPase intermediate fibers in human skeletal muscle. Muscle & nerve. 1982;5(8):628–36. doi: 10.1002/mus.880050807 6218405.
87. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(9):5116–21. doi: 10.1073/pnas.091062498 11309499.
88. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207–10. doi: 10.1093/nar/30.1.207 11752295.
89. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. doi: 10.1006/meth.2001.1262 11846609.
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