Characterization of the equine skeletal muscle transcriptome identifies novel functional responses to exercise training.
Abstract: Digital gene expression profiling was used to characterize the assembly of genes expressed in equine skeletal muscle and to identify the subset of genes that were differentially expressed following a ten-month period of exercise training. The study cohort comprised seven Thoroughbred racehorses from a single training yard. Skeletal muscle biopsies were collected at rest from the gluteus medius at two time points: T(1) - untrained, (9 +/- 0.5 months old) and T(2) - trained (20 +/- 0.7 months old). Results: The most abundant mRNA transcripts in the muscle transcriptome were those involved in muscle contraction, aerobic respiration and mitochondrial function. A previously unreported over-representation of genes related to RNA processing, the stress response and proteolysis was observed. Following training 92 tags were differentially expressed of which 74 were annotated. Sixteen genes showed increased expression, including the mitochondrial genes ACADVL, MRPS21 and SLC25A29 encoded by the nuclear genome. Among the 58 genes with decreased expression, MSTN, a negative regulator of muscle growth, had the greatest decrease.Functional analysis of all expressed genes using FatiScan revealed an asymmetric distribution of 482 Gene Ontology (GO) groups and 18 KEGG pathways. Functional groups displaying highly significant (P < 0.0001) increased expression included mitochondrion, oxidative phosphorylation and fatty acid metabolism while functional groups with decreased expression were mainly associated with structural genes and included the sarcoplasm, laminin complex and cytoskeleton. Conclusions: Exercise training in Thoroughbred racehorses results in coordinate changes in the gene expression of functional groups of genes related to metabolism, oxidative phosphorylation and muscle structure.
Publication Date: 2010-06-23 PubMed ID: 20573200PubMed Central: PMC2900271DOI: 10.1186/1471-2164-11-398Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research looks into identifying the changes in equine muscle genes that occur as a result of exercise training. It was found that there were significant changes in genes related to metabolism, oxidative phosphorylation, and muscle structure in Thoroughbred racehorses after a period of training.
Research Objective and Methodology
- The study aimed at identifying the changes that occur in the genetic composition of horse muscles due to training. To do this, they compared the gene expressions in a group of seven Thoroughbred racehorses at resting state before and after a ten-month training period. The researchers analyzed the genes in the gluteus medius muscle, an important muscle involved in movement.
- To collect data, muscle biopsies were taken from the horses before the training period (when the horses were about 9 months old) and after the training period (when the horses were about 20 months old). The data from these biopsies were then used for digital gene expression profiling to identify which genes were expressed and how their expression changed due to training.
Research Results
- The genes most prominently expressed in the muscle tissues were related to muscle contraction, aerobic respiration, and mitochondrial function. They also found an over-expression of genes related to RNA processing, stress response and proteolysis, which had not been reported in earlier studies.
- Of the genes expressed, they found that 92 of them behaved differently after the horses were trained. Some genes showed an increase in expression after training. For instance, genes ACADVL, MRPS21, and SLC25A29, which are connected with mitochondrial function and are encoded by the nuclear genome, showed an increase.
- Conversely, 58 genes showed a decrease in their expression, among which was MSTN, a gene that negatively regulates muscle growth.
- FatiScan, used for functional analysis of gene expressions, revealed an asymmetric distribution of 482 Gene Ontology groups and 18 KEGG pathways that led to significant changes in functional groups. Notably, the functions related to mitochondrion, oxidative phosphorylation, and fatty acid metabolism showed increased expression while those associated with structural genes like sarcoplasm, laminin complex, and cytoskeleton displayed diminished expression.
Research Conclusion
- This research concludes that exercise training influences significant changes in the genetic composition of muscle tissues in Thoroughbred racehorses. These changes impact the functional groups of genes associated with metabolism, oxidative phosphorylation, and muscle structure, suggesting that the body adapts to exercise at a molecular level as well as a physical level.
Cite This Article
APA
McGivney BA, McGettigan PA, Browne JA, Evans AC, Fonseca RG, Loftus BJ, Lohan A, MacHugh DE, Murphy BA, Katz LM, Hill EW.
(2010).
Characterization of the equine skeletal muscle transcriptome identifies novel functional responses to exercise training.
BMC Genomics, 11, 398.
https://doi.org/10.1186/1471-2164-11-398 Publication
Researcher Affiliations
- Animal Genomics Laboratory, UCD School of Agriculture, Food Science and Veterinary Medicine, College of Life Sciences, University College Dublin, Belfield, Dublin 4, Ireland.
MeSH Terms
- Animals
- Female
- Gene Expression Profiling / methods
- Gene Library
- Horses / genetics
- Horses / physiology
- Humans
- Male
- Mice
- Muscle, Skeletal / metabolism
- Muscle, Skeletal / physiology
- Physical Conditioning, Animal
- Reproducibility of Results
- Reverse Transcriptase Polymerase Chain Reaction
- Time Factors
References
This article includes 124 references
- Saltin B, Hartley LH, Kilbom A, Astrand I. Physical training in sedentary middle-aged and older men. II. Oxygen uptake, heart rate, and blood lactate concentration at submaximal and maximal exercise.. Scand J Clin Lab Invest 1969 Dec;24(4):323-34.
- Adhihetty PJ, Irrcher I, Joseph AM, Ljubicic V, Hood DA. Plasticity of skeletal muscle mitochondria in response to contractile activity.. Exp Physiol 2003 Jan;88(1):99-107.
- Holloszy JO, Rennie MJ, Hickson RC, Conlee RK, Hagberg JM. Physiological consequences of the biochemical adaptations to endurance exercise.. Ann N Y Acad Sci 1977;301:440-50.
- Hartman JW, Moore DR, Phillips SM. Resistance training reduces whole-body protein turnover and improves net protein retention in untrained young males.. Appl Physiol Nutr Metab 2006 Oct;31(5):557-64.
- Yarasheski KE, Zachwieja JJ, Bier DM. Acute effects of resistance exercise on muscle protein synthesis rate in young and elderly men and women.. Am J Physiol 1993 Aug;265(2 Pt 1):E210-4.
- Nader GA, Esser KA. Intracellular signaling specificity in skeletal muscle in response to different modes of exercise.. J Appl Physiol (1985) 2001 May;90(5):1936-42.
- Ronéus M, Essén-Gustavsson B, Lindholm A, Persson SG. Skeletal muscle characteristics in young trained and untrained standardbred trotters.. Equine Vet J 1992 Jul;24(4):292-4.
- Ronéus M. Muscle characteristics in standardbreds of different ages and sexes.. Equine Vet J 1993 Mar;25(2):143-6.
- Katz LM, Bayly WM, Hines MT, Sides RH. Differences in the ventilatory responses of horses and ponies to exercise of varying intensities.. Equine Vet J Suppl 1999 Jul;(30):49-51.
- Serrano AL, Quiroz-Rothe E, Rivero JL. Early and long-term changes of equine skeletal muscle in response to endurance training and detraining.. Pflugers Arch 2000 Dec;441(2-3):263-74.
- Hinchcliff KW, Lauderdale MA, Dutson J, Geor RJ, Lacombe VA, Taylor LE. High intensity exercise conditioning increases accumulated oxygen deficit of horses.. Equine Vet J 2002 Jan;34(1):9-16.
- McGowan CM, Golland LC, Evans DL, Hodgson DR, Rose RJ. Effects of prolonged training, overtraining and detraining on skeletal muscle metabolites and enzymes.. Equine Vet J Suppl 2002 Sep;(34):257-63.
- Rivero JL, Ruz A, Marti-Korfft S, Lindner A. Contribution of exercise intensity and duration to training-linked myosin transitions in thoroughbreds.. Equine Vet J Suppl 2006 Aug;(36):311-5.
- Yamano S, Eto D, Sugiura T, Kai M, Hiraga A, Tokuriki M, Miyata H. Effect of growth and training on muscle adaptation in Thoroughbred horses.. Am J Vet Res 2002 Oct;63(10):1408-12.
- Eto D, Yamano S, Mukai K, Sugiura T, Nasu T, Tokuriki M, Miyata H. Effect of high intensity training on anaerobic capacity of middle gluteal muscle in Thoroughbred horses.. Res Vet Sci 2004 Apr;76(2):139-44.
- Rivero JL, Sporleder HP, Quiroz-Rothe E, Vervuert I, Coenen M, Harmeyer J. Oral L-carnitine combined with training promotes changes in skeletal muscle.. Equine Vet J Suppl 2002 Sep;(34):269-74.
- Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA, Adams GR. Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise.. J Appl Physiol (1985) 2005 Feb;98(2):482-8.
- Neufer PD, Dohm GL. Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle.. Am J Physiol 1993 Dec;265(6 Pt 1):C1597-603.
- Yang Y, Creer A, Jemiolo B, Trappe S. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle.. J Appl Physiol (1985) 2005 May;98(5):1745-52.
- Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle.. J Physiol 2003 Feb 1;546(Pt 3):851-8.
- 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 Sep;19(11):1498-500.
- Schmutz S, Däpp C, Wittwer M, Vogt M, Hoppeler H, Flück M. Endurance training modulates the muscular transcriptome response to acute exercise.. Pflugers Arch 2006 Feb;451(5):678-87.
- Klossner S, Däpp C, Schmutz S, Vogt M, Hoppeler H, Flück M. Muscle transcriptome adaptations with mild eccentric ergometer exercise.. Pflugers Arch 2007 Dec;455(3):555-62.
- Puntschart A, Claassen H, Jostarndt K, Hoppeler H, Billeter R. mRNAs of enzymes involved in energy metabolism and mtDNA are increased in endurance-trained athletes.. Am J Physiol 1995 Sep;269(3 Pt 1):C619-25.
- Stepto NK, Coffey VG, Carey AL, Ponnampalam AP, Canny BJ, Powell D, Hawley JA. Global gene expression in skeletal muscle from well-trained strength and endurance athletes.. Med Sci Sports Exerc 2009 Mar;41(3):546-65.
- Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H. 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 2005 May;19(7):786-8.
- Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, Hawley JA. Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans.. FASEB J 2006 Jan;20(1):190-2.
- Coffey VG, Pilegaard H, Garnham AP, O'Brien BJ, Hawley JA. Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle.. J Appl Physiol (1985) 2009 Apr;106(4):1187-97.
- Coffey VG, Reeder DW, Lancaster GI, Yeo WK, Febbraio MA, Yaspelkis BB 3rd, Hawley JA. Effect of high-frequency resistance exercise on adaptive responses in skeletal muscle.. Med Sci Sports Exerc 2007 Dec;39(12):2135-44.
- Nader GA. Concurrent strength and endurance training: from molecules to man.. Med Sci Sports Exerc 2006 Nov;38(11):1965-70.
- Hickson RC. Interference of strength development by simultaneously training for strength and endurance.. Eur J Appl Physiol Occup Physiol 1980;45(2-3):255-63.
- Sale DG, Jacobs I, MacDougall JD, Garner S. Comparison of two regimens of concurrent strength and endurance training.. Med Sci Sports Exerc 1990 Jun;22(3):348-56.
- McCarthy JP, Agre JC, Graf BK, Pozniak MA, Vailas AC. Compatibility of adaptive responses with combining strength and endurance training.. Med Sci Sports Exerc 1995 Mar;27(3):429-36.
- Shaw BS, Shaw I. Compatibility of concurrent aerobic and resistance training on maximal aerobic capacity in sedentary males.. Cardiovasc J Afr 2009 Mar-Apr;20(2):104-6.
- Davis WJ, Wood DT, Andrews RG, Elkind LM, Davis WB. Concurrent training enhances athletes' strength, muscle endurance, and other measures.. J Strength Cond Res 2008 Sep;22(5):1487-502.
- Poole D. Current concepts of oxygen transport during exercise.. Equine and Comparative Exercise Physiology 2003;1:5–22.
- Young LE, Marlin DJ, Deaton C, Brown-Feltner H, Roberts CA, Wood JL. Heart size estimated by echocardiography correlates with maximal oxygen uptake.. Equine Vet J Suppl 2002 Sep;(34):467-71.
- Jones JH, Longworth KE, Lindholm A, Conley KE, Karas RH, Kayar SR, Taylor CR. Oxygen transport during exercise in large mammals. I. Adaptive variation in oxygen demand.. J Appl Physiol (1985) 1989 Aug;67(2):862-70.
- Banister EW, Purvis AD. Exercise electrocardiography in the horse by radiotelemetry.. J Am Vet Med Assoc 1968 Apr 1;152(7):1004-8.
- Marsland WP. Heart rate response to submaximal exercise in the Standardbred horse.. J Appl Physiol 1968 Jan;24(1):98-101.
- Asheim A, Knudsen O, Lindholm A, Rülcker C, Saltin B. Heart rates and blood lactate concentrations of standardbred horses during training and racing.. J Am Vet Med Assoc 1970 Aug 1;157(3):304-12.
- Hall MC, Steel JD, Stewart GA. Cardiac monitoring during exercise tests in the horse. 2. Heart rate responses to exercise.. Aust Vet J 1976 Jan;52(1):1-5.
- Kayar SR, Hoppeler H, Lindstedt SL, Claassen H, Jones JH, Essen-Gustavsson B, Taylor CR. Total muscle mitochondrial volume in relation to aerobic capacity of horses and steers.. Pflugers Arch 1989 Feb;413(4):343-7.
- Hargreaves BJ, Kronfeld DS, Naylor JR. Ambient temperature and relative humidity influenced packed cell volume, total plasma protein and other variables in horses during an incremental submaximal field exercise test.. Equine Vet J 1999 Jul;31(4):314-8.
- Guthrie AJ, Lund RJ. Thermoregulation. Base mechanisms and hyperthermia.. Vet Clin North Am Equine Pract 1998 Apr;14(1):45-59.
- Gunn HM. Muscle, bone and fat proportions and muscle distribution of Thoroughbreds and other horses. JR Gillespie and NE Robinson, Editors, Equine exercise physiology 2 Davis, ICEEP, CA. 1987. pp. 253–264.
- McGivney BA, Eivers SS, MacHugh DE, MacLeod JN, O'Gorman GM, Park SD, Katz LM, Hill EW. Transcriptional adaptations following exercise in thoroughbred horse skeletal muscle highlights molecular mechanisms that lead to muscle hypertrophy.. BMC Genomics 2009 Dec 30;10:638.
- Mienaltowski MJ, Huang L, Frisbie DD, McIlwraith CW, Stromberg AJ, Bathke AC, Macleod JN. Transcriptional profiling differences for articular cartilage and repair tissue in equine joint surface lesions.. BMC Med Genomics 2009 Sep 14;2:60.
- Bright LA, Burgess SC, Chowdhary B, Swiderski CE, McCarthy FM. Structural and functional-annotation of an equine whole genome oligoarray.. BMC Bioinformatics 2009 Oct 8;10 Suppl 11(Suppl 11):S8.
- Morrissy S, Zhao Y, Delaney A, Asano J, Dhalla N, Li I, McDonald H, Pandoh P, Prabhu AL, Tam A, Hirst M, Marra M. Digital gene expression by tag sequencing on the illumina genome analyzer.. Curr Protoc Hum Genet 2010 Apr;Chapter 11:Unit 11.11.1-36.
- Serteyn D, Piquemal D, Vanderheyden L, Lejeune JP, Verwilghen D, Sandersen C. Gene expression profiling from leukocytes of horses affected by osteochondrosis.. J Orthop Res 2010 Jul;28(7):965-70.
- Asmann YW, Klee EW, Thompson EA, Perez EA, Middha S, Oberg AL, Therneau TM, Smith DI, Poland GA, Wieben ED, Kocher JP. 3' tag digital gene expression profiling of human brain and universal reference RNA using Illumina Genome Analyzer.. BMC Genomics 2009 Nov 16;10:531.
- Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. Serial analysis of gene expression.. Science 1995 Oct 20;270(5235):484-7.
- Coleman SJ, Zeng Z, Mienaltowske M, Liu J, MacLeod JN. Analysis Of Equine Structural Gene Annotation By RNA Sequencing.. Plant & Animal Genomes XVII Conference 2009; San Diego, CA. 2009.
- Oshlack A, Wakefield MJ. Transcript length bias in RNA-seq data confounds systems biology.. Biol Direct 2009 Apr 16;4:14.
- Welle S, Bhatt K, Thornton CA. Inventory of high-abundance mRNAs in skeletal muscle of normal men.. Genome Res 1999 May;9(5):506-13.
- Payne RM, Strauss AW. Expression of the mitochondrial creatine kinase genes.. Mol Cell Biochem 1994 Apr-May;133-134:235-43.
- Ventura-Clapier R, Kuznetsov A, Veksler V, Boehm E, Anflous K. Functional coupling of creatine kinases in muscles: species and tissue specificity.. Mol Cell Biochem 1998 Jul;184(1-2):231-47.
- Gellerich FN, Khuchua ZA, Kuznetsov AV. Influence of the mitochondrial outer membrane and the binding of creatine kinase to the mitochondrial inner membrane on the compartmentation of adenine nucleotides in the intermembrane space of rat heart mitochondria.. Biochim Biophys Acta 1993 Jan 8;1140(3):327-34.
- Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis.. Biochem J 1992 Jan 1;281 ( Pt 1)(Pt 1):21-40.
- Gu J, MacHugh DE, McGivney BA, Park SD, Katz LM, Hill EW. Association of sequence variants in CKM (creatine kinase, muscle) and COX4I2 (cytochrome c oxidase, subunit 4, isoform 2) genes with racing performance in Thoroughbred horses.. Equine Vet J Suppl 2010 Nov;(38):569-75.
- Gu J, Orr N, Park SD, Katz LM, Sulimova G, MacHugh DE, Hill EW. A genome scan for positive selection in thoroughbred horses.. PLoS One 2009 Jun 2;4(6):e5767.
- MacLeod JN. Analysis Of Equine Gene Expression By RNA Sequencing.. Plant & Animal Genome Conference XVIII 2009; San Diego, CA, USA. 2009.
- Rivero JL, Galisteo AM, Agüera E, Miró F. Skeletal muscle histochemistry in male and female Andalusian and Arabian horses of different ages.. Res Vet Sci 1993 Mar;54(2):160-9.
- Sekoguchi E, Sato N, Yasui A, Fukada S, Nimura Y, Aburatani H, Ikeda K, Matsuura A. A novel mitochondrial carnitine-acylcarnitine translocase induced by partial hepatectomy and fasting.. J Biol Chem 2003 Oct 3;278(40):38796-802.
- Orii KO, Aoyama T, Souri M, Orii KE, Kondo N, Orii T, Hashimoto T. Genomic DNA organization of human mitochondrial very-long-chain acyl-CoA dehydrogenase and mutation analysis.. Biochem Biophys Res Commun 1995 Dec 26;217(3):987-92.
- Matthews CE, Ockene IS, Freedson PS, Rosal MC, Merriam PA, Hebert JR. Moderate to vigorous physical activity and risk of upper-respiratory tract infection.. Med Sci Sports Exerc 2002 Aug;34(8):1242-8.
- Gleeson M. Mucosal immune responses and risk of respiratory illness in elite athletes.. Exerc Immunol Rev 2000;6:5-42.
- Bouwman FG, van Ginneken MM, Noben JP, Royackers E, de Graaf-Roelfsema E, Wijnberg ID, van der Kolk JH, Mariman EC, van Breda E. Differential expression of equine muscle biopsy proteins during normal training and intensified training in young standardbred horses using proteomics technology.. Comp Biochem Physiol Part D Genomics Proteomics 2010 Mar;5(1):55-64.
- Stefansson S, Yepes M, Gorlatova N, Day DE, Moore EG, Zabaleta A, McMahon GA, Lawrence DA. Mutants of plasminogen activator inhibitor-1 designed to inhibit neutrophil elastase and cathepsin G are more effective in vivo than their endogenous inhibitors.. J Biol Chem 2004 Jul 16;279(29):29981-7.
- Dufaux B, Order U. Plasma elastase-alpha 1-antitrypsin, neopterin, tumor necrosis factor, and soluble interleukin-2 receptor after prolonged exercise.. Int J Sports Med 1989 Dec;10(6):434-8.
- Pyne DB. Regulation of neutrophil function during exercise.. Sports Med 1994 Apr;17(4):245-58.
- Shephard RJ, Shek PN. Immune responses to inflammation and trauma: a physical training model.. Can J Physiol Pharmacol 1998 May;76(5):469-72.
- Moldoveanu AI, Shephard RJ, Shek PN. The cytokine response to physical activity and training.. Sports Med 2001 Feb;31(2):115-44.
- Niess AM, Dickhuth HH, Northoff H, Fehrenbach E. Free radicals and oxidative stress in exercise--immunological aspects.. Exerc Immunol Rev 1999;5:22-56.
- Dousset E, Avela J, Ishikawa M, Kallio J, Kuitunen S, Kyröláinen H, Linnamo V, Komi PV. Bimodal recovery pattern in human skeletal muscle induced by exhaustive stretch-shortening cycle exercise.. Med Sci Sports Exerc 2007 Mar;39(3):453-60.
- Phillips SM, Tipton KD, Ferrando AA, Wolfe RR. Resistance training reduces the acute exercise-induced increase in muscle protein turnover.. Am J Physiol 1999 Jan;276(1):E118-24.
- Tipton KD, Ferrando AA, Phillips SM, Doyle D Jr, Wolfe RR. Postexercise net protein synthesis in human muscle from orally administered amino acids.. Am J Physiol 1999 Apr;276(4):E628-34.
- Reppert SM, Weaver DR. Coordination of circadian timing in mammals.. Nature 2002 Aug 29;418(6901):935-41.
- Oishi K, Sakamoto K, Okada T, Nagase T, Ishida N. Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats.. Biochem Biophys Res Commun 1998 Dec 18;253(2):199-203.
- Atkinson G, Edwards B, Reilly T, Waterhouse J. Exercise as a synchroniser of human circadian rhythms: an update and discussion of the methodological problems.. Eur J Appl Physiol 2007 Mar;99(4):331-41.
- Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding.. Science 2001 Jan 19;291(5503):490-3.
- Edgar DM, Dement WC. Regularly scheduled voluntary exercise synchronizes the mouse circadian clock.. Am J Physiol 1991 Oct;261(4 Pt 2):R928-33.
- Piccione G, Grasso F, Fazio F, Giudice E. The effect of physical exercise on the daily rhythm of platelet aggregation and body temperature in horses.. Vet J 2008 May;176(2):216-20.
- Murphy BA, Vick MM, Sessions DR, Cook RF, Fitzgerald BP. Evidence of an oscillating peripheral clock in an equine fibroblast cell line and adipose tissue but not in peripheral blood.. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2006 Jul;192(7):743-51.
- Souissi N, Gauthier A, Sesboüé B, Larue J, Davenne D. Effects of regular training at the same time of day on diurnal fluctuations in muscular performance.. J Sports Sci 2002 Nov;20(11):929-37.
- Reilly T, Atkinson G, Edwards B, Waterhouse J, Farrelly K, Fairhurst E. Diurnal variation in temperature, mental and physical performance, and tasks specifically related to football (soccer).. Chronobiol Int 2007;24(3):507-19.
- Brisswalter J, Bieuzen F, Giacomoni M, Tricot V, Falgairette G. Morning-to-evening differences in oxygen uptake kinetics in short-duration cycling exercise.. Chronobiol Int 2007;24(3):495-506.
- Morris C, Atkinson G, Drust B, Marrin K, Gregson W. Human core temperature responses during exercise and subsequent recovery: an important interaction between diurnal variation and measurement site.. Chronobiol Int 2009 Apr;26(3):560-75.
- Suter E, Hoppeler H, Claassen H, Billeter R, Aebi U, Horber F, Jaeger P, Marti B. Ultrastructural modification of human skeletal muscle tissue with 6-month moderate-intensity exercise training.. Int J Sports Med 1995 Apr;16(3):160-6.
- Desplanches D, Hoppeler H, Linossier MT, Denis C, Claassen H, Dormois D, Lacour JR, Geyssant A. Effects of training in normoxia and normobaric hypoxia on human muscle ultrastructure.. Pflugers Arch 1993 Nov;425(3-4):263-7.
- Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans.. Pflugers Arch 1985 Apr;403(4):369-76.
- Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER. Endurance training in humans: aerobic capacity and structure of skeletal muscle.. J Appl Physiol (1985) 1985 Aug;59(2):320-7.
- MacArthur DG, North KN. ACTN3: A genetic influence on muscle function and athletic performance.. Exerc Sport Sci Rev 2007 Jan;35(1):30-4.
- Hewitt JE. Abnormal glycosylation of dystroglycan in human genetic disease.. Biochim Biophys Acta 2009 Sep;1792(9):853-61.
- Cohn RD. Dystroglycan: important player in skeletal muscle and beyond.. Neuromuscul Disord 2005 Mar;15(3):207-17.
- Chin ER. Role of Ca2+/calmodulin-dependent kinases in skeletal muscle plasticity.. J Appl Physiol (1985) 2005 Aug;99(2):414-23.
- Michel RN, Chin ER, Chakkalakal JV, Eibl JK, Jasmin BJ. Ca2+/calmodulin-based signalling in the regulation of the muscle fibre phenotype and its therapeutic potential via modulation of utrophin A and myostatin expression.. Appl Physiol Nutr Metab 2007 Oct;32(5):921-9.
- Tentori L, Graziani G. Doping with growth hormone/IGF-1, anabolic steroids or erythropoietin: is there a cancer risk?. Pharmacol Res 2007 May;55(5):359-69.
- Saugy M, Robinson N, Saudan C, Baume N, Avois L, Mangin P. Human growth hormone doping in sport.. Br J Sports Med 2006 Jul;40 Suppl 1(Suppl 1):i35-9.
- Firth SM, Baxter RC. Cellular actions of the insulin-like growth factor binding proteins.. Endocr Rev 2002 Dec;23(6):824-54.
- Ren H, Yin P, Duan C. IGFBP-5 regulates muscle cell differentiation by binding to IGF-II and switching on the IGF-II auto-regulation loop.. J Cell Biol 2008 Sep 8;182(5):979-91.
- Kuemmerle JF, Zhou H. Insulin-like growth factor-binding protein-5 (IGFBP-5) stimulates growth and IGF-I secretion in human intestinal smooth muscle by Ras-dependent activation of p38 MAP kinase and Erk1/2 pathways.. J Biol Chem 2002 Jun 7;277(23):20563-71.
- McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member.. Nature 1997 May 1;387(6628):83-90.
- Roth SM, Martel GF, Ferrell RE, Metter EJ, Hurley BF, Rogers MA. Myostatin gene expression is reduced in humans with heavy-resistance strength training: a brief communication.. Exp Biol Med (Maywood) 2003 Jun;228(6):706-9.
- Kim JS, Cross JM, Bamman MM. Impact of resistance loading on myostatin expression and cell cycle regulation in young and older men and women.. Am J Physiol Endocrinol Metab 2005 Jun;288(6):E1110-9.
- Catipović B. Myostatin mutation associated with gross muscle hypertrophy in a child.. N Engl J Med 2004 Sep 2;351(10):1030-1; author reply 1030-1.
- Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Ménissier F, Massabanda J, Fries R, Hanset R, Georges M. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle.. Nat Genet 1997 Sep;17(1):71-4.
- McPherron AC, Lee SJ. Double muscling in cattle due to mutations in the myostatin gene.. Proc Natl Acad Sci U S A 1997 Nov 11;94(23):12457-61.
- Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh CS, Parker HG, Ostrander EA. A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs.. PLoS Genet 2007 May 25;3(5):e79.
- Schuelke M, Wagner KR, Stolz LE, Hübner C, Riebel T, Kömen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child.. N Engl J Med 2004 Jun 24;350(26):2682-8.
- Hill EW, Gu J, Eivers SS, Fonseca RG, McGivney BA, Govindarajan P, Orr N, Katz LM, MacHugh DE. A sequence polymorphism in MSTN predicts sprinting ability and racing stamina in thoroughbred horses.. PLoS One 2010 Jan 20;5(1):e8645.
- Lindholm A, Piehl K. Fibre composition, enzyme activity and concentrations of metabolites and electrolytes in muscles of standardbred horses.. Acta Vet Scand 1974;15(3):287-309.
- Dingboom EG, Dijkstra G, Enzerink E, van Oudheusden HC, Weijs WA. Postnatal muscle fibre composition of the gluteus medius muscle of Dutch Warmblood foals; maturation and the influence of exercise.. Equine Vet J Suppl 1999 Nov;(31):95-100.
- Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, Brent S, Chen Y, Clapham P, Clarke L, Coates G, Fairley S, Fitzgerald S, Fernandez-Banet J, Gordon L, Graf S, Haider S, Hammond M, Holland R, Howe K, Jenkinson A, Johnson N, Kahari A, Keefe D, Keenan S, Kinsella R, Kokocinski F, Kulesha E, Lawson D, Longden I, Megy K, Meidl P, Overduin B, Parker A, Pritchard B, Rios D, Schuster M, Slater G, Smedley D, Spooner W, Spudich G, Trevanion S, Vilella A, Vogel J, White S, Wilder S, Zadissa A, Birney E, Cunningham F, Curwen V, Durbin R, Fernandez-Suarez XM, Herrero J, Kasprzyk A, Proctor G, Smith J, Searle S, Flicek P. Ensembl 2009.. Nucleic Acids Res 2009 Jan;37(Database issue):D690-7.
- Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, Diekhans M, Giardine B, Harte RA, Hinrichs AS, Hsu F, Kober KM, Miller W, Pedersen JS, Pohl A, Raney BJ, Rhead B, Rosenbloom KR, Smith KE, Stanke M, Thakkapallayil A, Trumbower H, Wang T, Zweig AS, Haussler D, Kent WJ. The UCSC Genome Browser Database: 2008 update.. Nucleic Acids Res 2008 Jan;36(Database issue):D773-9.
- Robinson MD, Smyth GK. Moderated statistical tests for assessing differences in tag abundance.. Bioinformatics 2007 Nov 1;23(21):2881-7.
- Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery.. Genome Biol 2003;4(5):P3.
- Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.. Nat Protoc 2009;4(1):44-57.
- Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE.. Genome Biol 2003;4(10):R70.
- Al-Shahrour F, Arbiza L, Dopazo H, Huerta-Cepas J, Mínguez P, Montaner D, Dopazo J. From genes to functional classes in the study of biological systems.. BMC Bioinformatics 2007 Apr 3;8:114.
- Al-Shahrour F, Minguez P, Tárraga J, Montaner D, Alloza E, Vaquerizas JM, Conde L, Blaschke C, Vera J, Dopazo J. BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments.. Nucleic Acids Res 2006 Jul 1;34(Web Server issue):W472-6.
- Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing.. Journal of the Royal Statistical Society Series B-Methodological 1995;57(1):289–300.
- Cappelli K, Felicetti M, Capomaccio S, Spinsanti G, Silvestrelli M, Supplizi AV. Exercise induced stress in horses: selection of the most stable reference genes for quantitative RT-PCR normalization.. BMC Mol Biol 2008 May 19;9:49.
Citations
This article has been cited 39 times.- Han H, McGivney BA, Allen L, Bai D, Corduff LR, Davaakhuu G, Davaasambuu J, Dorjgotov D, Hall TJ, Hemmings AJ, Holtby AR, Jambal T, Jargalsaikhan B, Jargalsaikhan U, Kadri NK, MacHugh DE, Pausch H, Readhead C, Warburton D, Dugarjaviin M, Hill EW. Common protein-coding variants influence the racing phenotype in galloping racehorse breeds. Commun Biol 2022 Dec 13;5(1):1320.
- Pan J, Purev C, Zhao H, Zhang Z, Wang F, Wendoule N, Qi G, Liu Y, Zhou H. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse. Open Life Sci 2022;17(1):1269-1281.
- Dzięgielewska A, Dunislawska A. Mitochondrial Dysfunctions and Potential Molecular Markers in Sport Horses. Int J Mol Sci 2022 Aug 4;23(15).
- Zhang M, Guo Y, Su R, Corazzin M, Li J, Huang H, Zhang Y, Yao D, Su L, Zhao L, Jin Y. Effects of physical exercise on muscle metabolism and meat quality characteristics of Mongolian sheep. Food Sci Nutr 2022 May;10(5):1494-1509.
- Klein DJ, McKeever KH, Mirek ET, Anthony TG. Metabolomic Response of Equine Skeletal Muscle to Acute Fatiguing Exercise and Training. Front Physiol 2020;11:110.
- Farries G, Bryan K, McGivney CL, McGettigan PA, Gough KF, Browne JA, MacHugh DE, Katz LM, Hill EW. Expression Quantitative Trait Loci in Equine Skeletal Muscle Reveals Heritable Variation in Metabolism and the Training Responsive Transcriptome. Front Genet 2019;10:1215.
- Kim DH, Lee HG, Sp N, Kang DY, Jang KJ, Lee HK, Cho BW, Yang YM. Validation of exercise-response genes in skeletal muscle cells of Thoroughbred racing horses. Asian-Australas J Anim Sci 2021 Jan 1;34(1):134-142.
- Zhang C, Ni P, Ahmad HI, Gemingguli M, Baizilaitibei A, Gulibaheti D, Fang Y, Wang H, Asif AR, Xiao C, Chen J, Ma Y, Liu X, Du X, Zhao S. Detecting the Population Structure and Scanning for Signatures of Selection in Horses (Equus caballus) From Whole-Genome Sequencing Data. Evol Bioinform Online 2018;14:1176934318775106.
- Padilha FGF, El-Jaick KB, de Castro L, Moreira ADS, Ferreira AMR. Effect of selection for eventing on the MSTN gene in Brazilian sport horses. J Equine Sci 2018;29(1):21-24.
- McGivney BA, Griffin ME, Gough KF, McGivney CL, Browne JA, Hill EW, Katz LM. Evaluation of microRNA expression in plasma and skeletal muscle of thoroughbred racehorses in training. BMC Vet Res 2017 Nov 22;13(1):347.
- Bryan K, McGivney BA, Farries G, McGettigan PA, McGivney CL, Gough KF, MacHugh DE, Katz LM, Hill EW. Equine skeletal muscle adaptations to exercise and training: evidence of differential regulation of autophagosomal and mitochondrial components. BMC Genomics 2017 Aug 9;18(1):595.
- Dube S, Chionuma H, Matoq A, Alshiekh-Nasany R, Abbott L, Poiesz BJ, Dube DK. Expression of various sarcomeric tropomyosin isoforms in equine striated muscles. Open Vet J 2017;7(2):180-191.
- Ropka-Molik K, Stefaniuk-Szmukier M, Żukowski K, Piórkowska K, Gurgul A, Bugno-Poniewierska M. Transcriptome profiling of Arabian horse blood during training regimens. BMC Genet 2017 Apr 5;18(1):31.
- Tozaki T, Kikuchi M, Kakoi H, Hirota KI, Mukai K, Aida H, Nakamura S, Nagata SI. Profiling of exercise-induced transcripts in the peripheral blood cells of Thoroughbred horses. J Equine Sci 2016;27(4):157-164.
- Chanda M, Srikuea R, Cherdchutam W, Chairoungdua A, Piyachaturawat P. Modulating effects of exercise training regimen on skeletal muscle properties in female polo ponies. BMC Vet Res 2016 Nov 4;12(1):245.
- Goljanek-Whysall K, Iwanejko LA, Vasilaki A, Pekovic-Vaughan V, McDonagh B. Ageing in relation to skeletal muscle dysfunction: redox homoeostasis to regulation of gene expression. Mamm Genome 2016 Aug;27(7-8):341-57.
- Do KT, Cho HW, Badrinath N, Park JW, Choi JY, Chung YH, Lee HK, Song KD, Cho BW. Molecular Characterization and Expression Analysis of Creatine Kinase Muscle (CK-M) Gene in Horse. Asian-Australas J Anim Sci 2015 Dec;28(12):1680-5.
- Stefaniuk M, Ropka-Molik K. RNA sequencing as a powerful tool in searching for genes influencing health and performance traits of horses. J Appl Genet 2016 May;57(2):199-206.
- Pacholewska A, Drögemüller M, Klukowska-Rötzler J, Lanz S, Hamza E, Dermitzakis ET, Marti E, Gerber V, Leeb T, Jagannathan V. The transcriptome of equine peripheral blood mononuclear cells. PLoS One 2015;10(3):e0122011.
- Gim JA, Hong CP, Kim DS, Moon JW, Choi Y, Eo J, Kwon YJ, Lee JR, Jung YD, Bae JH, Choi BH, Ko J, Song S, Ahn K, Ha HS, Yang YM, Lee HK, Park KD, Do KT, Han K, Yi JM, Cha HJ, Ayarpadikannan S, Cho BW, Bhak J, Kim HS. Genome-wide analysis of DNA methylation before-and after exercise in the thoroughbred horse with MeDIP-Seq. Mol Cells 2015 Mar;38(3):210-20.
- Levian C, Ruiz E, Yang X. The pathogenesis of obesity from a genomic and systems biology perspective. Yale J Biol Med 2014 Jun;87(2):113-26.
- Moreton J, Malla S, Aboobaker AA, Tarlinton RE, Emes RD. Characterisation of the horse transcriptome from immunologically active tissues. PeerJ 2014;2:e382.
- Park W, Kim J, Kim HJ, Choi J, Park JW, Cho HW, Kim BW, Park MH, Shin TS, Cho SK, Park JK, Kim H, Hwang JY, Lee CK, Lee HK, Cho S, Cho BW. Investigation of de novo unique differentially expressed genes related to evolution in exercise response during domestication in Thoroughbred race horses. PLoS One 2014;9(3):e91418.
- Mukherjee K, Edgett BA, Burrows HW, Castro C, Griffin JL, Schwertani AG, Gurd BJ, Funk CD. Whole blood transcriptomics and urinary metabolomics to define adaptive biochemical pathways of high-intensity exercise in 50-60 year old masters athletes. PLoS One 2014;9(3):e92031.
- Gutiérrez-Aguilar M, Baines CP. Physiological and pathological roles of mitochondrial SLC25 carriers. Biochem J 2013 Sep 15;454(3):371-86.
- Kim H, Lee T, Park W, Lee JW, Kim J, Lee BY, Ahn H, Moon S, Cho S, Do KT, Kim HS, Lee HK, Lee CK, Kong HS, Yang YM, Park J, Kim HM, Kim BC, Hwang S, Bhak J, Burt D, Park KD, Cho BW, Kim H. Peeling back the evolutionary layers of molecular mechanisms responsive to exercise-stress in the skeletal muscle of the racing horse. DNA Res 2013 Jun;20(3):287-98.
- Freeman TC, Ivens A, Baillie JK, Beraldi D, Barnett MW, Dorward D, Downing A, Fairbairn L, Kapetanovic R, Raza S, Tomoiu A, Alberio R, Wu C, Su AI, Summers KM, Tuggle CK, Archibald AL, Hume DA. A gene expression atlas of the domestic pig. BMC Biol 2012 Nov 15;10:90.
- Park KD, Park J, Ko J, Kim BC, Kim HS, Ahn K, Do KT, Choi H, Kim HM, Song S, Lee S, Jho S, Kong HS, Yang YM, Jhun BH, Kim C, Kim TH, Hwang S, Bhak J, Lee HK, Cho BW. Whole transcriptome analyses of six thoroughbred horses before and after exercise using RNA-Seq. BMC Genomics 2012 Sep 12;13:473.
- Votion DM, Gnaiger E, Lemieux H, Mouithys-Mickalad A, Serteyn D. Physical fitness and mitochondrial respiratory capacity in horse skeletal muscle. PLoS One 2012;7(4):e34890.
- Bower MA, McGivney BA, Campana MG, Gu J, Andersson LS, Barrett E, Davis CR, Mikko S, Stock F, Voronkova V, Bradley DG, Fahey AG, Lindgren G, MacHugh DE, Sulimova G, Hill EW. The genetic origin and history of speed in the Thoroughbred racehorse. Nat Commun 2012 Jan 24;3:643.
- Hill EW, McGivney BA, Gu J, Whiston R, Machugh DE. A genome-wide SNP-association study confirms a sequence variant (g.66493737C>T) in the equine myostatin (MSTN) gene as the most powerful predictor of optimum racing distance for Thoroughbred racehorses. BMC Genomics 2010 Oct 11;11:552.
- Wang T, Li M, Ren W, Meng J, Yao X, Chu H, Yao R, Zhai M, Zeng Y. Multi-Omics Analysis Reveals Biaxial Regulatory Mechanisms of Cardiac Adaptation by Specialized Racing Training in Yili Horses. Biology (Basel) 2025 Nov 17;14(11).
- Takahashi K, Mukai K, Takahashi Y, Ebisuda Y, Sugiyama F, Hatta H, Kitaoka Y. Effects of hypoxia and hyperoxia on exercise-induced metabolomic and transcriptomic profiles in equine skeletal muscle. J Exp Biol 2025 Dec 15;228(24).
- Austin MMP, Ivey JLZ, Shepherd EA, Myer PR. Methodologies to Identify Metabolic Pathway Differences Between Emaciated and Moderately Conditioned Horses: A Review of Multiple Gene Expression Techniques. Animals (Basel) 2025 Oct 10;15(20).
- Ferrari P, Bertolini A, Garavaldi A, Faeti V, Bergamaschi M, Loffi C, Pinna A, Virgili R. Effect of Space Allowance on Pig Performance, Carcass Traits and Meat Quality in Italian Heavy Pigs Reared Under Two Housing Systems. Foods 2025 Aug 14;14(16).
- Kinanti RG, Weningtyas A, Ariesaka KM, Puspitasari ST, Arsani NL, Liao HE. Identification of differentially expressed genes in resting human skeletal muscle of sedentary versus strength and endurance- trained individuals using bioinformatics analysis and in vitro validation. Narra J 2025 Apr;5(1):e1764.
- Stefaniuk-Szmukier M, Szmatoła T, Ropka-Molik K. Molecular Signatures of Exercise Adaptation in Arabian Racing Horses: Transcriptomic Insights from Blood and Muscle. Genes (Basel) 2025 Apr 4;16(4).
- Yang L, Li P, Huang X, Wang C, Zeng Y, Wang J, Yao X, Meng J. Effects of Combined Transcriptome and Metabolome Analysis Training on Athletic Performance of 2-Year-Old Trot-Type Yili Horses. Genes (Basel) 2025 Feb 4;16(2).
- Stefaniuk-Szmukier M, Szmatoła T, Pustelnik A, Ropka-Molik K. First transcriptomic insight into the working muscles of racing pigeons during a competition flight. Mol Biol Rep 2024 May 8;51(1):625.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists