Repeated sprint training in hypoxia induces specific skeletal muscle adaptations through S100A protein signaling.

HIF‐1α OXPHOS RSH S100A13 exercise glycolysis

Journal

FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484

Informations de publication

Date de publication:
30 Apr 2024
Historique:
revised: 22 03 2024
received: 13 10 2023
accepted: 03 04 2024
medline: 23 4 2024
pubmed: 23 4 2024
entrez: 23 4 2024
Statut: ppublish

Résumé

Athletes increasingly engage in repeated sprint training consisting in repeated short all-out efforts interspersed by short recoveries. When performed in hypoxia (RSH), it may lead to greater training effects than in normoxia (RSN); however, the underlying molecular mechanisms remain unclear. This study aimed at elucidating the effects of RSH on skeletal muscle metabolic adaptations as compared to RSN. Sixteen healthy young men performed nine repeated sprint training sessions in either normoxia (F

Identifiants

pubmed: 38651657
doi: 10.1096/fj.202302084RR
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23615

Subventions

Organisme : University of Lausanne

Informations de copyright

© 2024 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.

Références

Buchheit M, Laursen PB. High‐intensity interval training, solutions to the programming puzzle. Sports Med. 2013;43(5):313‐338. doi:10.1007/s40279-013-0029-x
Buchheit M, Laursen PB. High‐intensity interval training, solutions to the programming puzzle. Part II: anaerobic energy, neuromuscular load and practical applications. Sports Med Auckl NZ. 2013;43(10):927‐954. doi:10.1007/s40279-013-0066-5
Linossier MT, Dormois D, Perier C, Frey J, Geyssant A, Denis C. Enzyme adaptations of human skeletal muscle during bicycle short‐sprint training and detraining. Acta Physiol Scand. 1997;161(4):439‐445. doi:10.1046/j.1365-201X.1997.00244.x
Ross A, Leveritt M. Long‐term metabolic and skeletal muscle adaptations to short‐sprint training. Sports Med. 2001;31(15):1063‐1082. doi:10.2165/00007256-200131150-00003
Saunders PU, Garvican‐Lewis LA, Schmidt WF, Gore CJ. Relationship between changes in haemoglobin mass and maximal oxygen uptake after hypoxic exposure. Br J Sports Med. 2013;47(Suppl 1):i26‐i30. doi:10.1136/bjsports-2013-092841
Kim J, Whan TI, Semenza GL, Dang CV. HIF‐1‐mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006;3(3):177‐185. doi:10.1016/j.cmet.2006.02.002
Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF‐1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 2006;3(3):187‐197. doi:10.1016/j.cmet.2006.01.012
Cartee GD, Douen AG, Ramlal T, Klip A, Holloszy JO. Stimulation of glucose transport in skeletal muscle by hypoxia. J Appl Physiol. 1991;70(4):1593‐1600. doi:10.1152/jappl.1991.70.4.1593
Ullah MS, Davies AJ, Halestrap AP. The plasma membrane lactate transporter MCT4, but not MCT1, is up‐regulated by hypoxia through a HIF‐1α‐dependent mechanism. J Biol Chem. 2006;281(14):9030‐9037. doi:10.1074/jbc.M511397200
Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia‐inducible factor 1. J Biol Chem. 1994;269(38):23757‐23763. doi:10.1016/S0021-9258(17)31580-6
Green HJ, Sutton JR, Cymerman A, Young PM, Houston CS. Operation Everest II: adaptations in human skeletal muscle. J Appl Physiol (1985). 1989;66(5):2454‐2461. doi:10.1152/jappl.1989.66.5.2454
Lundby C, Calbet JAL, Robach P. The response of human skeletal muscle tissue to hypoxia. Cell Mol Life Sci. 2009;66(22):3615‐3623. doi:10.1007/s00018-009-0146-8
Brocherie F, Girard O, Faiss R, Millet GP. Effects of repeated‐sprint training in hypoxia on sea‐level performance: a meta‐analysis. Sports Med Auckl NZ. 2017;47(8):1651‐1660. doi:10.1007/s40279-017-0685-3
Faiss R, Léger B, Vesin JM, et al. Significant molecular and systemic adaptations after repeated Sprint training in hypoxia. PLoS One. 2013;8(2):e56522. doi:10.1371/journal.pone.0056522
Brocherie F, Millet GP, D'Hulst G, Van Thienen R, Deldicque L, Girard O. Repeated maximal‐intensity hypoxic exercise superimposed to hypoxic residence boosts skeletal muscle transcriptional responses in elite team‐sport athletes. Acta Physiol. 2018;222(1):e12851. doi:10.1111/apha.12851
Robinson MM, Dasari S, Konopka AR, et al. Enhanced protein translation underlies improved metabolic and physical adaptations to different exercise training modes in Young and old humans. Cell Metab. 2017;25(3):581‐592. doi:10.1016/j.cmet.2017.02.009
Rundqvist H, Gustafsson T. Hypoxic sprint exercise as a complement to the “live high‐train low” regimen. Acta Physiol. 2018;222(1):e12989. doi:10.1111/apha.12989
Hermens HJ, Freriks B, Disselhorst‐Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000;10(5):361‐374. doi:10.1016/S1050-6411(00)00027-4
Neyroud D, Vallotton A, Millet GY, Kayser B, Place N. The effect of muscle fatigue on stimulus intensity requirements for central and peripheral fatigue quantification. Eur J Appl Physiol. 2014;114(1):205‐215. doi:10.1007/s00421-013-2760-2
Girard O, Mendez‐Villanueva A, Bishop D. Repeated‐sprint ability—part I. Sports Med. 2011;41(8):673‐694. doi:10.2165/11590550-000000000-00000
Strojnik V, Komi PV. Neuromuscular fatigue after maximal stretch‐shortening cycle exercise. J Appl Physiol. 1998;84(1):344‐350. doi:10.1152/jappl.1998.84.1.344
Place N, Maffiuletti NA, Martin A, Lepers R. Assessment of the reliability of central and peripheral fatigue after sustained maximal voluntary contraction of the quadriceps muscle. Muscle Nerve. 2007;35(4):486‐495. doi:10.1002/mus.20714
Rodriguez‐Falces J, Place N. End‐of‐fiber signals strongly influence the first and second phases of the M wave in the vastus lateralis: implications for the study of muscle excitability. Front Physiol. 2018;9:162. doi:10.3389/fphys.2018.00162
Zanou N, Dridi H, Reiken S, et al. Acute RyR1 Ca2+ leak enhances NADH‐linked mitochondrial respiratory capacity. Nat Commun. 2021;12(1):7219. doi:10.1038/s41467-021-27422-1
Wiśniewski JR, Gaugaz FZ. Fast and sensitive total protein and peptide assays for proteomic analysis. Anal Chem. 2015;87:4110‐4116. doi:10.1021/ac504689z
Kulak NA, Pichler G, Paron I, Nagaraj N, Mann M. Minimal, encapsulated proteomic‐sample processing applied to copy‐number estimation in eukaryotic cells. Nat Methods. 2014;11(3):319‐324. doi:10.1038/nmeth.2834
Meier F, Brunner AD, Koch S, et al. Online parallel accumulation–serial fragmentation (PASEF) with a novel trapped ion mobility mass spectrometer. Mol Cell Proteomics. 2018;17(12):2534‐2545. doi:10.1074/mcp.TIR118.000900
Meier F, Brunner AD, Frank M, et al. diaPASEF: parallel accumulation–serial fragmentation combined with data‐independent acquisition. Nat Methods. 2020;17(12):1229‐1236. doi:10.1038/s41592-020-00998-0
Huang T, Choi M, Tzouros M, et al. MSstatsTMT: statistical detection of differentially abundant proteins in experiments with isobaric labeling and multiple mixtures. Mol Cell Proteomics. 2020;19(10):1706‐1723. doi:10.1074/mcp.RA120.002105
Cox J, Mann M. 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high‐throughput data. BMC Bioinformatics. 2012;13(16):S12. doi:10.1186/1471-2105-13-S16-S12
Little JP, Safdar A, Bishop D, Tarnopolsky MA, Gibala MJ. An acute bout of high‐intensity interval training increases the nuclear abundance of PGC‐1α and activates mitochondrial biogenesis in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2011;300(6):R1303‐R1310. doi:10.1152/ajpregu.00538.2010
Ruas JL, White JP, Rao RR, et al. A PGC‐1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell. 2012;151(6):1319‐1331. doi:10.1016/j.cell.2012.10.050
Handschin C, Rhee J, Lin J, Tarr PT, Spiegelman BM. An autoregulatory loop controls peroxisome proliferator‐activated receptor γ coactivator 1α expression in muscle. Proc Natl Acad Sci USA. 2003;100(12):7111‐7116. doi:10.1073/pnas.1232352100
Wright DC, Geiger PC, Han DH, Jones TE, Holloszy JO. Calcium induces increases in peroxisome proliferator‐activated receptor γ coactivator‐1α and mitochondrial biogenesis by a pathway leading to p38 mitogen‐activated protein kinase activation *. J Biol Chem. 2007;282(26):18793‐18799. doi:10.1074/jbc.M611252200
Arany Z, Foo SY, Ma Y, et al. HIF‐independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC‐1α. Nature. 2008;451(7181):1008‐1012. doi:10.1038/nature06613
Toffoli S, Roegiers A, Feron O, et al. Intermittent hypoxia is an angiogenic inducer for endothelial cells: role of HIF‐1. Angiogenesis. 2009;12(1):47‐67. doi:10.1007/s10456-009-9131-y
Bloor CM. Angiogenesis during exercise and training. Angiogenesis. 2005;8(3):263‐271. doi:10.1007/s10456-005-9013-x
Chinsomboon J, Ruas J, Gupta RK, et al. The transcriptional coactivator PGC‐1α mediates exercise‐induced angiogenesis in skeletal muscle. Proc Natl Acad Sci USA. 2009;106(50):21401‐21406. doi:10.1073/pnas.0909131106
Bonen A. The expression of lactate transporters (MCT1 and MCT4) in heart and muscle. Eur J Appl Physiol. 2001;86(1):6‐11. doi:10.1007/s004210100516
Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 2013;93(3):993‐1017. doi:10.1152/physrev.00038.2012
Li Y, Li XY, Li LX, et al. S100A10 accelerates aerobic glycolysis and malignant growth by activating mTOR‐signaling pathway in gastric cancer. Front Cell Dev Biol. 2020;8:559486. doi:10.3389/fcell.2020.559486
Donato R, Cannon BR, Sorci G, et al. Functions of S100 proteins. Curr Mol Med. 2013;13(1):24‐57. doi:10.2174/156652413804486214
Gonzalez LL, Garrie K, Turner MD. Role of S100 proteins in health and disease. Biochim Biophys Acta Mol Cell Res. 2020;1867(6):118677. doi:10.1016/j.bbamcr.2020.118677
Wu M, Falasca M, Blough ER. Akt/protein kinase B in skeletal muscle physiology and pathology. J Cell Physiol. 2011;226(1):29‐36. doi:10.1002/jcp.22353
Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell. 2007;129(7):1261‐1274. doi:10.1016/j.cell.2007.06.009
Raberin A, Elmer J, Willis SJ, et al. The oxidative‐glycolytic balance influenced by sprint duration is key during repeated sprint in hypoxia. Med Sci Sports Exerc. 2023;55:245‐254. doi:10.1249/mss.0000000000003042
Granata C, Jamnick NA, Bishop DJ. Training‐induced changes in mitochondrial content and respiratory function in human skeletal muscle. Sports Med. 2018;48(8):1809‐1828. doi:10.1007/s40279-018-0936-y
Granata C, Oliveira RSF, Little JP, Renner K, Bishop DJ. Mitochondrial adaptations to high‐volume exercise training are rapidly reversed after a reduction in training volume in human skeletal muscle. FASEB J. 2016;30(10):3413‐3423. doi:10.1096/fj.201500100R
Granata C, Oliveira RSF, Little JP, Renner K, Bishop DJ. Training intensity modulates changes in PGC‐1α and p53 protein content and mitochondrial respiration, but not markers of mitochondrial content in human skeletal muscle. FASEB J. 2016;30(2):959‐970. doi:10.1096/fj.15-276907
Pasteur L. Expériences et vues nouvelles sur la nature des fermentations. C R Acad Hebd Seances Acad Sci. 1861;53:1260‐1264.
Henderson AR. Biochemistry of hypoxia: current concepts I: an introduction to biochemical pathways and their control. Br J Anaesth. 1969;41(3):245‐250. doi:10.1093/bja/41.3.245
Kierans SJ, Taylor CT. Regulation of glycolysis by the hypoxia‐inducible factor (HIF): implications for cellular physiology. J Physiol. 2021;599(1):23‐37. doi:10.1113/JP280572
Nava RC, McKenna Z, Fennel Z, et al. Repeated sprint exercise in hypoxia stimulates HIF‐1‐dependent gene expression in skeletal muscle. Eur J Appl Physiol. 2022;122(4):1097‐1107. doi:10.1007/s00421-022-04909-3
Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg CJ. Exercise‐induced expression of angiogenesis‐related transcription and growth factors in human skeletal muscle. Am J Physiol Heart Circ Physiol. 1999;276(2):H679‐H685. doi:10.1152/ajpheart.1999.276.2.H679
Krock BL, Skuli N, Simon MC. Hypoxia‐induced angiogenesis: good and evil. Genes Cancer. 2011;2(12):1117‐1133. doi:10.1177/1947601911423654

Auteurs

Clément Lanfranchi (C)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Biomedical Sciences, University of Lausanne, Lausanne, Switzerland.

Sarah J Willis (SJ)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Biological Sciences, University of Denver, Denver, Colorado, USA.

Louis Laramée (L)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.

Sonia Conde Alonso (S)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.

Vincent Pialoux (V)

Inter-University Laboratory of Human Movement Biology UR7424, University Claude Bernard Lyon 1, Lyon, France.

Bengt Kayser (B)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Biomedical Sciences, University of Lausanne, Lausanne, Switzerland.

Nicolas Place (N)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Biomedical Sciences, University of Lausanne, Lausanne, Switzerland.

Grégoire P Millet (GP)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Biomedical Sciences, University of Lausanne, Lausanne, Switzerland.

Nadège Zanou (N)

Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Biomedical Sciences, University of Lausanne, Lausanne, Switzerland.

Classifications MeSH