Acute Sprint Exercise Transcriptome in Human Skeletal Muscle

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2019 Oct 25

PMID 31647849

Citations 22

Authors

Hakan Claes Rundqvist

Andreas Montelius

Ted Osterlund

Barbara Norman

Mona Esbjornsson

Eva Jansson

Affiliations

Soon will be listed here.

Abstract

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.

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References

Forbes D, Jackman M, Bishop A, Thomas M, Kambadur R, Sharma M . Myostatin auto-regulates its expression by feedback loop through Smad7 dependent mechanism. J Cell Physiol. 2005; 206(1):264-72. DOI: 10.1002/jcp.20477. View

Miyamoto-Mikami E, Tsuji K, Horii N, Hasegawa N, Fujie S, Homma T . Gene expression profile of muscle adaptation to high-intensity intermittent exercise training in young men. Sci Rep. 2018; 8(1):16811. PMC: 6235852. DOI: 10.1038/s41598-018-35115-x. View

McPherron A, Lawler A, Lee S . Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997; 387(6628):83-90. DOI: 10.1038/387083a0. View

Lin J, Handschin C, Spiegelman B . Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005; 1(6):361-70. DOI: 10.1016/j.cmet.2005.05.004. View

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. View

Schnyder S, Handschin C . Skeletal muscle as an endocrine organ: PGC-1α, myokines and exercise. Bone. 2015; 80:115-125. PMC: 4657151. DOI: 10.1016/j.bone.2015.02.008. View

Kumar A, Davuluri G, Nascimento E Silva R, Engelen M, Ten Have G, Prayson R . Ammonia lowering reverses sarcopenia of cirrhosis by restoring skeletal muscle proteostasis. Hepatology. 2017; 65(6):2045-2058. PMC: 5444955. DOI: 10.1002/hep.29107. View

Coffey V, Moore D, Burd N, Rerecich T, Stellingwerff T, Garnham A . Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints. Eur J Appl Physiol. 2010; 111(7):1473-83. DOI: 10.1007/s00421-010-1768-0. View

Gibala M, McGee S, Garnham A, Howlett K, Snow R, 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). 2008; 106(3):929-34. DOI: 10.1152/japplphysiol.90880.2008. View

10.

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. Dev Biol. 2008; 319(2):234-47. DOI: 10.1016/j.ydbio.2008.04.021. View

11.

Clasen B, Krusenstjerna-Hafstrom T, Holm Vendelbo M, Thorsen K, Escande C, Moller N . 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. PMC: 3679400. DOI: 10.1194/jlr.P034520. View

12.

Mahoney D, Parise G, Melov S, Safdar A, Tarnopolsky M . 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. View

13.

Di Padova M, Caretti G, Zhao P, Hoffman E, Sartorelli V . MyoD acetylation influences temporal patterns of skeletal muscle gene expression. J Biol Chem. 2007; 282(52):37650-9. DOI: 10.1074/jbc.M707309200. View

14.

Edgar R, Domrachev M, Lash A . Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2001; 30(1):207-10. PMC: 99122. DOI: 10.1093/nar/30.1.207. View

15.

Sartori R, Milan G, Patron M, Mammucari C, Blaauw B, Abraham R . 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. View

16.

Joanisse S, McKay B, Nederveen J, Scribbans T, Gurd B, Gillen J . Satellite cell activity, without expansion, after nonhypertrophic stimuli. Am J Physiol Regul Integr Comp Physiol. 2015; 309(9):R1101-11. PMC: 4666950. DOI: 10.1152/ajpregu.00249.2015. View

17.

Wiik A, Gustafsson T, Esbjornsson M, Johansson O, Ekman M, Sundberg C . 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. View

18.

Moro T, Ebert S, Adams C, Rasmussen B . Amino Acid Sensing in Skeletal Muscle. Trends Endocrinol Metab. 2016; 27(11):796-806. PMC: 5075248. DOI: 10.1016/j.tem.2016.06.010. View

19.

Vissing K, Schjerling P . Simplified data access on human skeletal muscle transcriptome responses to differentiated exercise. Sci Data. 2015; 1:140041. PMC: 4432635. DOI: 10.1038/sdata.2014.41. View

20.

Olfert I, Baum O, Hellsten Y, Egginton S . Advances and challenges in skeletal muscle angiogenesis. Am J Physiol Heart Circ Physiol. 2015; 310(3):H326-36. PMC: 4796623. DOI: 10.1152/ajpheart.00635.2015. View