Gallop Racing Shifts Mature mRNA towards Introns: Does Exercise-Induced Stress Enhance Genome Plasticity?
Abstract: Physical exercise is universally recognized as stressful. Among the "sport species", the horse is probably the most appropriate model for investigating the genomic response to stress due to the homogeneity of its genetic background. The aim of this work is to dissect the whole transcription modulation in Peripheral Blood Mononuclear Cells (PBMCs) after exercise with a time course framework focusing on unexplored regions related to introns and intergenic portions. PBMCs NGS from five 3 year old Sardinian Anglo-Arab racehorses collected at rest and after a 2000 m race was performed. Apart from differential gene expression ascertainment between the two time points the complexity of transcription for alternative transcripts was identified. Interestingly, we noted a transcription shift from the coding to the non-coding regions. We further investigated the possible causes of this phenomenon focusing on genomic repeats, using a differential expression approach and finding a strong general up-regulation of repetitive elements such as LINE. Since their modulation is also associated with the "exonization", the recruitment of repeats that act with regulatory functions, suggesting that there might be an active regulation of this transcriptional shift. Thanks to an innovative bioinformatic approach, our study could represent a model for the transcriptomic investigation of stress.
Publication Date: 2020-04-09 PubMed ID: 32283859PubMed Central: PMC7230505DOI: 10.3390/genes11040410Google 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 study investigates how physical exercise stress impacts the genomic response in racehorses. Specifically, it examines how this stress influences certain not previously studied regions of the horse genome tied to introns and intergenic portions.
Objective and Method
- This research aims to explore the overall transcriptional changes in Peripheral Blood Mononuclear Cells (PBMCs) due to exercise stress over time, with a particular focus on previously unexplored areas linked with introns and intergenic portions.
- The study employed Next-Generation Sequencing (NGS) on PBMCs from five 3-year old Sardinian Anglo-Arab racehorses, collected before and after a 2000 m race to detect any possible changes in gene expression between the two moments.
Results and Findings
- Interestingly, the researchers found a shift from coding to the non-coding regions in the transcription activity after the race.
- In trying to explain what could cause this shift, they focused on genomic repeats by using a differential expression approach. This process revealed a significantly up-regulated expression of repetitive elements like LINE.
- The researchers also found that these changes in repetitive elements are related with “exonization”, a process that turns sequences from intronic or intergenic regions into exons. This suggests the presence of active regulation causing the shift in transcription.
Conclusion and Significance
- This study offers new insights into how exercise-induced stress can influence genome plasticity, increasing our understanding of how genomes adapt to stress situations.
- The findings highlight the importance of genomic repeats and their possible regulatory role in stress response.
- Technologically, the innovative bioinformatics approach applied in this research could serve as a model for future studies on the transcriptomic investigation of stress.
Cite This Article
APA
Cappelli K, Mecocci S, Gioiosa S, Giontella A, Silvestrelli M, Cherchi R, Valentini A, Chillemi G, Capomaccio S.
(2020).
Gallop Racing Shifts Mature mRNA towards Introns: Does Exercise-Induced Stress Enhance Genome Plasticity?
Genes (Basel), 11(4), 410.
https://doi.org/10.3390/genes11040410 Publication
Researcher Affiliations
- Dipartimento di Medicina Veterinaria, University of Perugia, 06126 Perugia, Italy.
- Centro di Ricerca sul Cavallo Sportivo, University of Perugia, 06126 Perugia, Italy.
- Dipartimento di Medicina Veterinaria, University of Perugia, 06126 Perugia, Italy.
- Centro di Ricerca sul Cavallo Sportivo, University of Perugia, 06126 Perugia, Italy.
- SCAI-Super Computing Applications and Innovation Department, CINECA, 00185 Rome, Italy.
- Dipartimento di Medicina Veterinaria, University of Perugia, 06126 Perugia, Italy.
- Centro di Ricerca sul Cavallo Sportivo, University of Perugia, 06126 Perugia, Italy.
- Dipartimento di Medicina Veterinaria, University of Perugia, 06126 Perugia, Italy.
- Centro di Ricerca sul Cavallo Sportivo, University of Perugia, 06126 Perugia, Italy.
- AGRIS, Servizio Ricerca Qualitu00e0 e Valorizzazione delle Produzioni Equine, Ozieri, 09127 Sassari, Italy.
- Dipartimento per l'Innovazione Nei Sistemi Biologici, Agroalimentari e Forestali, Universitu00e0 della Tuscia, 01100 Tuscia, Italy.
- Dipartimento per l'Innovazione Nei Sistemi Biologici, Agroalimentari e Forestali, Universitu00e0 della Tuscia, 01100 Tuscia, Italy.
- Institute of Biomembranes, Bioenergetics and Molecular Biotechnologies, IBIOM, CNR, 70126 Bari, Italy.
- Dipartimento di Medicina Veterinaria, University of Perugia, 06126 Perugia, Italy.
- Centro di Ricerca sul Cavallo Sportivo, University of Perugia, 06126 Perugia, Italy.
MeSH Terms
- Animals
- Female
- Gene Expression Regulation
- Genome
- Horses
- Introns / genetics
- Leukocytes, Mononuclear / metabolism
- Male
- Physical Conditioning, Animal
- RNA, Messenger / genetics
- Stress, Physiological
- Transcriptome
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 62 references
- Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Ru00f6der M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See LH, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigu00f3 R, Gingeras TR. Landscape of transcription in human cells.. Nature 2012 Sep 6;489(7414):101-8.
- Giuffra E, Tuggle CK. Functional Annotation of Animal Genomes (FAANG): Current Achievements and Roadmap.. Annu Rev Anim Biosci 2019 Feb 15;7:65-88.
- de Hoon M, Shin JW, Carninci P. Paradigm shifts in genomics through the FANTOM projects.. Mamm Genome 2015 Oct;26(9-10):391-402.
- Visscher PM, Wray NR, Zhang Q, Sklar P, McCarthy MI, Brown MA, Yang J. 10 Years of GWAS Discovery: Biology, Function, and Translation.. Am J Hum Genet 2017 Jul 6;101(1):5-22.
- Kline H., Foreman J. Heart and spleen weights as a function of breed and somatotype. Equine Exerc Physiol. 1991;3:17u201321.
- Barrey E, Galloux P, Valette JP, Auvinet B, Wolter R. Stride characteristics of overground versus treadmill locomotion in the saddle horse.. Acta Anat (Basel) 1993;146(2-3):90-4.
- 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.
- Cappelli K, Felicetti M, Capomaccio S, Nocelli C, Silvestrelli M, Verini-Supplizi A. Effect of training status on immune defence related gene expression in Thoroughbred: are genes ready for the sprint?. Vet J 2013 Mar;195(3):373-6.
- Ohmura H, Mukai K, Takahashi T, Aida H, Jones JH. Cardiorespiratory function in Thoroughbreds during locomotion on a treadmill at an incline or decline.. Am J Vet Res 2017 Mar;78(3):340-349.
- Rivero JL, van Breda E, Rogers CW, Lindner A, van Oldruitenborgh-Oosterbaan MM. Unexplained underperformance syndrome in sport horses: classification, potential causes and recognition.. Equine Vet J 2008 Sep;40(6):611-8.
- Cappelli K., Supplizi A.V., Capomaccio S., Albertini E., Silvestrelli M. Analysis Of Peripheral Blood Mononuclear Cells Gene Expression in Endurance Horses. Town & Country Convention Center; San Diego, CA, USA: 2005.
- Cappelli K, Verini-Supplizi A, Capomaccio S, Silvestrelli M. Analysis of peripheral blood mononuclear cells gene expression in endurance horses by cDNA-AFLP technique.. Res Vet Sci 2007 Jun;82(3):335-43.
- 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.
- Cappelli K, Felicetti M, Capomaccio S, Pieramati C, Silvestrelli M, Verini-Supplizi A. Exercise-induced up-regulation of MMP-1 and IL-8 genes in endurance horses.. BMC Physiol 2009 Jun 24;9:12.
- Capomaccio S, Cappelli K, Barrey E, Felicetti M, Silvestrelli M, Verini-Supplizi A. Microarray analysis after strenuous exercise in peripheral blood mononuclear cells of endurance horses.. Anim Genet 2010 Dec;41 Suppl 2:166-75.
- Capomaccio S, Cappelli K, Spinsanti G, Mencarelli M, Muscettola M, Felicetti M, Verini Supplizi A, Bonifazi M. Athletic humans and horses: comparative analysis of interleukin-6 (IL-6) and IL-6 receptor (IL-6R) expression in peripheral blood mononuclear cells in trained and untrained subjects at rest.. BMC Physiol 2011 Jan 21;11:3.
- Capomaccio S, Vitulo N, Verini-Supplizi A, Barcaccia G, Albiero A, D'Angelo M, Campagna D, Valle G, Felicetti M, Silvestrelli M, Cappelli K. RNA sequencing of the exercise transcriptome in equine athletes.. PLoS One 2013;8(12):e83504.
- Jacob AG, Smith CWJ. Intron retention as a component of regulated gene expression programs.. Hum Genet 2017 Sep;136(9):1043-1057.
- Braunschweig U, Barbosa-Morais NL, Pan Q, Nachman EN, Alipanahi B, Gonatopoulos-Pournatzis T, Frey B, Irimia M, Blencowe BJ. Widespread intron retention in mammals functionally tunes transcriptomes.. Genome Res 2014 Nov;24(11):1774-86.
- Elbarbary RA, Lucas BA, Maquat LE. Retrotransposons as regulators of gene expression.. Science 2016 Feb 12;351(6274):aac7247.
- Capomaccio S, Verini-Supplizi A, Galla G, Vitulo N, Barcaccia G, Felicetti M, Silvestrelli M, Cappelli K. Transcription of LINE-derived sequences in exercise-induced stress in horses.. Anim Genet 2010 Dec;41 Suppl 2:23-7.
- Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
- Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements.. Nat Methods 2015 Apr;12(4):357-60.
- Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
- Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features.. Bioinformatics 2010 Mar 15;26(6):841-2.
- Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features.. Bioinformatics 2014 Apr 1;30(7):923-30.
- Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
- Benjamini Y., Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B Methodol. 1995;57:289u2013300. doi: 10.1111/j.2517-6161.1995.tb02031.x.
- Anders S, Reyes A, Huber W. Detecting differential usage of exons from RNA-seq data.. Genome Res 2012 Oct;22(10):2008-17.
- Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ. The UCSC Table Browser data retrieval tool.. Nucleic Acids Res 2004 Jan 1;32(Database issue):D493-6.
- Kuhn RM, Haussler D, Kent WJ. The UCSC genome browser and associated tools.. Brief Bioinform 2013 Mar;14(2):144-61.
- Vilborg A, Steitz JA. Readthrough transcription: How are DoGs made and what do they do?. RNA Biol 2017 May 4;14(5):632-636.
- Fernandes JCR, Acuu00f1a SM, Aoki JI, Floeter-Winter LM, Muxel SM. Long Non-Coding RNAs in the Regulation of Gene Expression: Physiology and Disease.. Noncoding RNA 2019 Feb 17;5(1).
- Pecinka A, Mittelsten Scheid O. Stress-induced chromatin changes: a critical view on their heritability.. Plant Cell Physiol 2012 May;53(5):801-8.
- Biamonti G, Caceres JF. Cellular stress and RNA splicing.. Trends Biochem Sci 2009 Mar;34(3):146-53.
- Kaer K, Branovets J, Hallikma A, Nigumann P, Speek M. Intronic L1 retrotransposons and nested genes cause transcriptional interference by inducing intron retention, exonization and cryptic polyadenylation.. PLoS One 2011;6(10):e26099.
- Sznajder u0141J, Thomas JD, Carrell EM, Reid T, McFarland KN, Cleary JD, Oliveira R, Nutter CA, Bhatt K, Sobczak K, Ashizawa T, Thornton CA, Ranum LPW, Swanson MS. Intron retention induced by microsatellite expansions as a disease biomarker.. Proc Natl Acad Sci U S A 2018 Apr 17;115(16):4234-4239.
- Muotri AR, Marchetto MC, Coufal NG, Gage FH. The necessary junk: new functions for transposable elements.. Hum Mol Genet 2007 Oct 15;16 Spec No. 2:R159-67.
- Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ. Deciphering the splicing code.. Nature 2010 May 6;465(7294):53-9.
- Long JC, Caceres JF. The SR protein family of splicing factors: master regulators of gene expression.. Biochem J 2009 Jan 1;417(1):15-27.
- Lee Y, Rio DC. Mechanisms and Regulation of Alternative Pre-mRNA Splicing.. Annu Rev Biochem 2015;84:291-323.
- Dvinge H. Regulation of alternative mRNA splicing: old players and new perspectives.. FEBS Lett 2018 Sep;592(17):2987-3006.
- Herzel L, Neugebauer KM. Quantification of co-transcriptional splicing from RNA-Seq data.. Methods 2015 Sep 1;85:36-43.
- Blencowe BJ. Alternative splicing: new insights from global analyses.. Cell 2006 Jul 14;126(1):37-47.
- Zheng CL, Fu XD, Gribskov M. Characteristics and regulatory elements defining constitutive splicing and different modes of alternative splicing in human and mouse.. RNA 2005 Dec;11(12):1777-87.
- Garg K, Green P. Differing patterns of selection in alternative and constitutive splice sites.. Genome Res 2007 Jul;17(7):1015-22.
- Shalgi R, Hurt JA, Lindquist S, Burge CB. Widespread inhibition of posttranscriptional splicing shapes the cellular transcriptome following heat shock.. Cell Rep 2014 Jun 12;7(5):1362-1370.
- Ninomiya K, Adachi S, Natsume T, Iwakiri J, Terai G, Asai K, Hirose T. LncRNA-dependent nuclear stress bodies promote intron retention through SR protein phosphorylation.. EMBO J 2020 Feb 3;39(3):e102729.
- Anufrieva KS, Shender Vu041e, Arapidi GP, Pavlyukov MS, Shakhparonov MI, Shnaider PV, Butenko IO, Lagarkova MA, Govorun VM. Therapy-induced stress response is associated with downregulation of pre-mRNA splicing in cancer cells.. Genome Med 2018 Jun 27;10(1):49.
- Brady LK, Wang H, Radens CM, Bi Y, Radovich M, Maity A, Ivan C, Ivan M, Barash Y, Koumenis C. Transcriptome analysis of hypoxic cancer cells uncovers intron retention in EIF2B5 as a mechanism to inhibit translation.. PLoS Biol 2017 Sep;15(9):e2002623.
- Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann Y, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blu00f6cker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowki J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, Szustakowki J. Initial sequencing and analysis of the human genome.. Nature 2001 Feb 15;409(6822):860-921.
- Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blu00f6cker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Della Valle G, Fryc S, Guu00e9rin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Ru00f8ed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvu00e4nen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Lander ES, Lindblad-Toh K. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009 Nov 6;326(5954):865-7.
- Crichton JH, Dunican DS, Maclennan M, Meehan RR, Adams IR. Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline.. Cell Mol Life Sci 2014 May;71(9):1581-605.
- Richardson SR, Doucet AJ, Kopera HC, Moldovan JB, Garcia-Perez JL, Moran JV. The Influence of LINE-1 and SINE Retrotransposons on Mammalian Genomes.. Microbiol Spectr 2015 Apr;3(2):MDNA3-0061-2014.
- Aporntewan C, Phokaew C, Piriyapongsa J, Ngamphiw C, Ittiwut C, Tongsima S, Mutirangura A. Hypomethylation of intragenic LINE-1 represses transcription in cancer cells through AGO2.. PLoS One 2011 Mar 15;6(3):e17934.
- Wongpaiboonwattana W, Tosukhowong P, Dissayabutra T, Mutirangura A, Boonla C. Oxidative stress induces hypomethylation of LINE-1 and hypermethylation of the RUNX3 promoter in a bladder cancer cell line.. Asian Pac J Cancer Prev 2013;14(6):3773-8.
- Miousse IR, Koturbash I. The Fine LINE: Methylation Drawing the Cancer Landscape.. Biomed Res Int 2015;2015:131547.
- Scott EC, Devine SE. The Role of Somatic L1 Retrotransposition in Human Cancers.. Viruses 2017 May 31;9(6).
- Kroutter EN, Belancio VP, Wagstaff BJ, Roy-Engel AM. The RNA polymerase dictates ORF1 requirement and timing of LINE and SINE retrotransposition.. PLoS Genet 2009 Apr;5(4):e1000458.
- Ostertag EM, Kazazian HH Jr. Biology of mammalian L1 retrotransposons.. Annu Rev Genet 2001;35:501-38.
- Pizarro JG, Cristofari G. Post-Transcriptional Control of LINE-1 Retrotransposition by Cellular Host Factors in Somatic Cells.. Front Cell Dev Biol 2016;4:14.
- Mackinnon LT. Chronic exercise training effects on immune function.. Med Sci Sports Exerc 2000 Jul;32(7 Suppl):S369-76.
Citations
This article has been cited 6 times.- Foury A, Mach N, Ruet A, Lansade L, Moisan MP. Transcriptomic signature related to poor welfare of sport horses.. Compr Psychoneuroendocrinol 2023 Nov;16:100201.
- Bartolomu00e9 E, Perdomo-Gonzu00e1lez DI, Ripollu00e9s-Lobo M, Valera M. Basal Reactivity Evaluated by Infrared Thermography in the "Caballo de Deporte Espau00f1ol" Horse Breed According to Its Coat Color.. Animals (Basel) 2022 Sep 21;12(19).
- Karagianni AE, Kurian D, Cillu00e1n-Garcia E, Eaton SL, Wishart TM, Pirie RS. Training associated alterations in equine respiratory immunity using a multiomics comparative approach.. Sci Rep 2022 Jan 10;12(1):427.
- Cappelli K, Mecocci S, Capomaccio S, Beccati F, Palumbo AR, Tognoloni A, Pepe M, Chiaradia E. Circulating Transcriptional Profile Modulation in Response to Metabolic Unbalance Due to Long-Term Exercise in Equine Athletes: A Pilot Study.. Genes (Basel) 2021 Dec 9;12(12).
- Bartolomu00e9 E, Perdomo-Gonzu00e1lez DI, Su00e1nchez-Guerrero MJ, Valera M. Genetic Parameters of Effort and Recovery in Sport Horses Assessed with Infrared Thermography.. Animals (Basel) 2021 Mar 16;11(3).
- Cappelli K, Amadori M, Mecocci S, Miglio A, Antognoni MT, Razzuoli E. Immune Response in Young Thoroughbred Racehorses under Training.. Animals (Basel) 2020 Oct 5;10(10).