BMC Genomics | |
Swimming-induced exercise promotes hypertrophy and vascularization of fast skeletal muscle fibres and activation of myogenic and angiogenic transcriptional programs in adult zebrafish | |
Josep V Planas3  Herman P Spaink1  Joan Ramon Torrella4  David Rizo-Roca4  Mireia Rovira3  Arjan P Palstra2  | |
[1] Department of Molecular Cell Biology, Institute Biology, Leiden University, Leiden, The Netherlands;Institute for Marine Resources and Ecosystem Studies (IMARES), Wageningen Aquaculture, Wageningen UR, Yerseke, The Netherlands;Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Spain;Departament de Fisiologia i Immunologia, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain | |
关键词: Zebrafish; Transcriptome; Muscle; Growth; Swimming; Exercise; | |
Others : 1125708 DOI : 10.1186/1471-2164-15-1136 |
|
received in 2014-07-02, accepted in 2014-12-11, 发布年份 2014 | |
【 摘 要 】
Background
The adult skeletal muscle is a plastic tissue with a remarkable ability to adapt to different levels of activity by altering its excitability, its contractile and metabolic phenotype and its mass. We previously reported on the potential of adult zebrafish as a tractable experimental model for exercise physiology, established its optimal swimming speed and showed that swimming-induced contractile activity potentiated somatic growth. Given that the underlying exercise-induced transcriptional mechanisms regulating muscle mass in vertebrates are not fully understood, here we investigated the cellular and molecular adaptive mechanisms taking place in fast skeletal muscle of adult zebrafish in response to swimming.
Results
Fish were trained at low swimming speed (0.1 m/s; non-exercised) or at their optimal swimming speed (0.4 m/s; exercised). A significant increase in fibre cross-sectional area (1.290 ± 88 vs. 1.665 ± 106 μm2) and vascularization (298 ± 23 vs. 458 ± 38 capillaries/mm2) was found in exercised over non-exercised fish. Gene expression profiling by microarray analysis evidenced the activation of a series of complex transcriptional networks of extracellular and intracellular signaling molecules and pathways involved in the regulation of muscle mass (e.g. IGF-1/PI3K/mTOR, BMP, MSTN), myogenesis and satellite cell activation (e.g. PAX3, FGF, Notch, Wnt, MEF2, Hh, EphrinB2) and angiogenesis (e.g. VEGF, HIF, Notch, EphrinB2, KLF2), some of which had not been previously associated with exercise-induced contractile activity.
Conclusions
The results from the present study show that exercise-induced contractile activity in adult zebrafish promotes a coordinated adaptive response in fast muscle that leads to increased muscle mass by hypertrophy and increased vascularization by angiogenesis. We propose that these phenotypic adaptations are the result of extensive transcriptional changes induced by exercise. Analysis of the transcriptional networks that are activated in response to exercise in the adult zebrafish fast muscle resulted in the identification of key signaling pathways and factors for the regulation of skeletal muscle mass, myogenesis and angiogenesis that have been remarkably conserved during evolution from fish to mammals. These results further support the validity of the adult zebrafish as an exercise model to decipher the complex molecular and cellular mechanisms governing skeletal muscle mass and function in vertebrates.
【 授权许可】
2014 Palstra et al.; licensee BioMed Central.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150217024141796.pdf | 2531KB | download | |
Figure 4. | 99KB | Image | download |
Figure 3. | 114KB | Image | download |
Figure 2. | 43KB | Image | download |
Figure 1. | 69KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Gundersen K: Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 2011, 86:564-600.
- [2]Egan B, Zierath JR: Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 2013, 17:162-184.
- [3]Berchtold MW, Brinkmeier H, Muntener M: Calcium ion in skeletal muscle: Its crucial role for muscle function, plasticity, and disease. Physiol Rev 2000, 80:1215-1265.
- [4]Braun T, Gautel M: Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol 2011, 12:349-361.
- [5]Buckingham M, Rigby PWJ: Gene regulatory networksand transcriptional mechanisms that control myogenesis. Dev Cell 2014, 28:225-238.
- [6]Haskell WL, Lee I-M, Pate RR, Powell KE, Blair SN, Franklin BA, Macera CA, Heath GW, Thompson PD, Bauman A: Physical activity and public health: updated recommendation for adults from the American college of sports medicine and the American heart association. Med Sci Sports Exerc 2007, 39:1423-1434.
- [7]Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan Taber L, Albright AL, Braun B, American College of Sports Medicine, American Diabetes Association: Exercise and type 2 diabetes: the American college of sports medicine and the American diabetes association: joint position statement. Diabetes Care 2010, 33:e147-e167.
- [8]Ochi H, Westerfield M: Signaling networks that regulate muscle development: lessons from zebrafish. Dev Growth Differ 2007, 49:1-11.
- [9]Jackson HE, Ingham PW: Control of muscle fibre-type diversity during embryonic development: The zebrafish paradigm. Mech Dev 2013, 130:447-457.
- [10]Gibbs EM, Horstick EJ, Dowling JJ: Swimming into prominence: the zebrafish as a valuable tool for studying human myopathies and muscular dystrophies. FEBS J 2013, 280:4187-4197.
- [11]Berger J, Currie PD: Zebrafish models flex their muscles to shed light on muscular dystrophies. Dis Mod Mech 2012, 5:726-732.
- [12]Dou Y, Andersson-Lendahl M, Arner A: Structure and function of skeletal muscle in zebrafish early larvae. J Gen Physiol 2008, 131:445-453.
- [13]Catchen JM, Braasch I, Postlethwait JH: Conserved synteny and the zebrafish genome. Methods Cell Biol 2011, 104:259-285.
- [14]Yogev O, Williams VC, Hinits Y, Hughes SM: eIF4EBP3L acts as a gatekeeper of TORC1 in activity-dependent muscle growth by specifically regulating Mef2ca translational initiation. PLoS Biol 2013, 11:e1001679.
- [15]Johnston IA, Lee H-T, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, Kinghorn JR, Dalmay T: Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 2009, 212:1781-1793.
- [16]Hanai J-I, Cao P, Tanksale P, Imamura S, Koshimizu E, Zhao J, Kishi S, Yamashita M, Phillips PS, Sukhatme VP, Lecker SH: The muscle-specific ubiquitin ligase atrogin-1/MAFbx mediates statin-induced muscle toxicity. J Clin Invest 2007, 117:3940-3951.
- [17]Palstra AP, Tudorache C, Rovira M, Brittijn SA, Burgerhout E, Van Den Thillart GEEJM, Spaink HP, Planas JV: Establishing zebrafish as a novel exercise model: swimming economy, swimming-enhanced growth and muscle growth marker gene expression. PLoS One 2010, 5:e14483.
- [18]Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M: Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 2013, 280:4294-4314.
- [19]Davison W, Herbert NA: Swimming-enhanced growth. In Swimming Physiology of Fish. Edited by Palstra AP, Planas JV. Berlin, Heidelberg: Springer-Verlag; 2013:177-202.
- [20]Small EM, O'Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD, Richardson JA, Olson EN: Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci U S A 2010, 107:4218-4223.
- [21]Johnston IA, Bower NI, Macqueen DJ: Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 2011, 214:1617-1628.
- [22]Felip O, Ibarz A, Fernández-Borràs J, Beltrán M, Martín-Pérez M, Planas JV, Blasco J: Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C]starch and [15N]protein): effects of gelatinisation of starches and sustained swimming. Br J Nutr 2012, 107:834-844.
- [23]Magnoni LJ, Crespo D, Ibarz A, Blasco J, Fernández-Borràs J, Planas JV: Comparative biochemistry and physiology, part a. Comp Biochem Physiol A Mol Integr Physiol 2013, 166:1-12.
- [24]Sandri M: Signaling in muscle atrophy and hypertrophy. Physiology 2008, 23:160-170.
- [25]Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL: Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004, 117:399-412.
- [26]Paul PK, Gupta SK, Bhatnagar S, Panguluri SK, Darnay BG, Choi Y, Kumar A: Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice. J Cell Biol 2010, 191:1395-1411.
- [27]Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP: Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 2006, 576:923-933.
- [28]Lee S-J, Lee Y-S, Zimmers TA, Soleimani A, Matzuk MM, Tsuchida K, Cohn RD, Barton ER: Regulation of muscle mass by follistatin and activins. Mol Endocrinol 2010, 24:1998-2008.
- [29]McPherron AC, Lawler AM, Lee SJ: Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387:83-90.
- [30]Xu C, Wu G, Zohar Y, Du S-J: Analysis of myostatin gene structure, expression and function in zebrafish. J Exp Biol 2003, 206:4067-4079.
- [31]Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ: Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 2009, 296:C1258-C1270.
- [32]Sartori R, Schirwis E, Blaauw B, Bortolanza S, Zhao J, Enzo E, Stantzou A, Mouisel E, Toniolo L, Ferry A, Stricker S, Goldberg AL, Dupont S, Piccolo S, Amthor H, Sandri M: BMP signaling controls muscle mass. Nat Genet 2013, 45:1309-1318.
- [33]Winbanks CE, Chen JL, Qian H, Liu Y, Bernardo BC, Beyer C, Watt KI, Thomson RE, Connor T, Turner BJ, McMullen JR, Larsson L, McGee SL, Harrison CA, Gregorevic P: The bone morphogenetic protein axis is a positive regulator of skeletal muscle mass. J Cell Biol 2013, 203:345-357.
- [34]Wagers AJ, Conboy IM: Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 2005, 122:659-667.
- [35]McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, Srikuea R, Lawson BA, Grimes B, Keller C, Van Zant G, Campbell KS, Esser KA, Dupont-Versteegden EE, Peterson CA: Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 2011, 138:3657-3666.
- [36]Blaauw B, Canato M, Agatea L, Toniolo L, Mammucari C, Masiero E, Abraham R, Sandri M, Schiaffino S, Reggiani C: Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J 2009, 23:3896-3905.
- [37]Lee S-J, Huynh TV, Lee Y-S, Sebald SM, Wilcox-Adelman SA, Iwamori N, Lepper C, Matzuk MM, Fan C-M: Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway. Proc Natl Acad Sci U S A 2012, 109:E2353-E2360.
- [38]Petrella JK, Kim JS, Mayhew DL, Cross JM, Bamman MM: Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol 2008, 104:1736-1742.
- [39]Rescan P-Y, Montfort J, Fautrel A, Rallière C, Lebret V: Gene expression profiling of the hyperplastic growth zones of the late trout embryo myotome using laser capture microdissection and microarray analysis. BMC Genomics 2013, 14:173. BioMed Central Full Text
- [40]Thalacker-Mercer A, Stec M, Cui X, Cross J, Windham S, Bamman M: Cluster analysis reveals differential transcript profiles associated with resistance training-induced human skeletal muscle hypertrophy. Physiol Genomics 2013, 45:499-507.
- [41]Keller P, Vollaard NBJ, Gustafsson T, Gallagher IJ, Sundberg CJ, Rankinen T, Britton SL, Bouchard C, Koch LG, Timmons JA: A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J Appl Physiol 2011, 110:46-59.
- [42]Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA: A temporal switch from Notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008, 2:50-59.
- [43]Zhang H, Anderson JE: Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio). J Exp Biol 2014, 217:1910-1917.
- [44]Alexander MS, Kawahara G, Kho AT, Howell MH, Pusack TJ, Myers JA, Montanaro F, Zon LI, Guyon JR, Kunkel LM: Isolation and transcriptome analysis of adult zebrafish cells enriched for skeletal muscle progenitors. Muscle Nerve 2011, 43:741-750.
- [45]Montarras D, L'honoré A, Buckingham M: Lying low but ready for action: the quiescent muscle satellite cell. FEBS J 2013, 280:4036-4050.
- [46]Potthoff MJ, Olson EN: MEF2: a central regulator of diverse developmental programs. Development 2007, 134:4131-4140.
- [47]Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, DiMaio JM, Olson EN, Bassel-Duby R, Williams RS: Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 2001, 20:6414-6423.
- [48]Ticho BS, Stainier DY, Fishman MC, Breitbart RE: Three zebrafish MEF2 genes delineate somitic and cardiac muscle development in wild-type and mutant embryos. Mech Dev 1996, 59:205-218.
- [49]Hinits Y, Hughes SM: Mef2s are required for thick filament formation in nascent muscle fibres. Development 2007, 134:2511-2519.
- [50]Guerci A, Lahoute C, Hébrard S, Collard L, Graindorge D, Favier M, Cagnard N, Batonnet-Pichon S, Précigout G, Garcia L, Tuil D, Daegelen D, Sotiropoulos A: Srf-dependent paracrine signals produced by myofibers control satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 2012, 15:25-37.
- [51]Puri PL, Iezzi S, Stiegler P, Chen TT, Schiltz RL, Muscat GE, Giordano A, Kedes L, Wang JY, Sartorelli V: Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol Cell 2001, 8:885-897.
- [52]Egginton S: Invited review: activity-induced angiogenesis. Pflugers Arch 2008, 457:963-977.
- [53]Plyley MJ, Olmstead BJ, Noble EG: Time course of changes in capillarization in hypertrophied rat plantaris muscle. J Appl Physiol 1998, 84:902-907.
- [54]Ibarz A, Felip O, Fernández-Borràs J, Martín-Pérez M, Blasco J, Torrella JR: Sustained swimming improves muscle growth and cellularity in gilthead sea bream. J Comp Physiol B 2010, 181:209-217.
- [55]Pelster B, Sänger AM, Siegele M, Schwerte T: Influence of swim training on cardiac activity, tissue capillarization, and mitochondrial density in muscle tissue of zebrafish larvae. Am J Physiol Regul Integr Comp Physiol 2003, 285:R339-R347.
- [56]Sänger AM: Effects of training on axial muscle of two cyprinid species: Chondrostoma nasus (L.) and Leuciscus cephalus (L.). J Fish Biol 1992, 40:637-646.
- [57]Davie PS, Wells RM, Tetens V: Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isozymes: evidence for increased aerobic capacity of white muscle. J Exp Zool 1986, 237:159-171.
- [58]Prior BM: What makes vessels grow with exercise training? J Appl Physiol 2004, 97:1119-1128.
- [59]Adams RH, Alitalo K: Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007, 8:464-478.
- [60]Potente M, Gerhardt H, Carmeliet P: Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
- [61]Chung AS, Ferrara N: Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol 2011, 27:563-584.
- [62]Gore AV, Monzo K, Cha YR, Pan W, Weinstein BM: Vascular development in the zebrafish. Cold Spring Harb Perspect Med 2012, 2:a006684-a006684.
- [63]Hong CC, Peterson QP, Hong J-Y, Peterson RT: Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr Biol 2006, 16:1366-1372.
- [64]Herbert SP, Huisken J, Kim TN, Feldman ME, Houseman BT, Wang RA, Shokat KM, Stainier DYR: Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science 2009, 326:294-298.
- [65]Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND: MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 2010, 464:1196-1200.
- [66]Hoier B, Hellsten Y: Exercise induced capillary growth in human skeletal muscle and the dynamics of VEGF. Microcirculation 2014, 21:301-314.
- [67]Gaudel C, Schwartz C, Giordano C, Abumrad NA, Grimaldi PA: Pharmacological activation of PPARbeta promotes rapid and calcineurin-dependent fiber remodeling and angiogenesis in mouse skeletal muscle. Am J Physiol Endocrinol Metab 2008, 295:E297-E304.
- [68]Arany Z, Foo S-Y, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM: HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 2008, 451:1008-1012.
- [69]Kopp R, Köblitz L, Egg M, Pelster B: HIF signaling and overall gene expression changes during hypoxia and prolonged exercise differ considerably. Physiol Genomics 2011, 43:506-516.
- [70]McClelland GB, Craig PM, Dhekney K, Dipardo S: Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol 2006, 577:739-751.
- [71]LeMoine CMR, Craig PM, Dhekney K, Kim JJ, McClelland GB: Temporal and spatial patterns of gene expression in skeletal muscles in response to swim training in adult zebrafish (Danio rerio). J Comp Physiol B 2010, 180:151-160.
- [72]van der Meulen T, Schipper H, van den Boogaart JGM, Huising MO, Kranenbarg S, van Leeuwen JL: Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 2006, 291:R1040-R1048.
- [73]Mathieu-Costello O, Agey PJ, Wu L, Hang J, Adair TH: Capillary-to-fiber surface ratio in rat fast-twitch hindlimb muscles after chronic electrical stimulation. J Appl Physiol 1996, 80:904-909.
- [74]Phillips BE, Williams JP, Gustafsson T, Bouchard C, Rankinen T, Knudsen S, Smith K, Timmons JA, Atherton PJ: Molecular Networks of human muscle adaptation to exercise and Age. PLoS Genet 2013, 9:e1003389.
- [75]Nachlas MM, Tsou KC, De Souza E, Cheng CS, Seligman AM: Cytochemical demonstration of succinic dehydrogenase by the use of a new p-nitrophenyl substituted ditetrazole. J Histochem Cytochem 1957, 5:420-436.
- [76]Fouces V, Torrella JR, Palomeque J, Viscor G: A histochemical ATPase method for the demonstration of the muscle capillary network. J Histochem Cytochem 1993, 41:283-289.
- [77]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, 25:402-408.