RNA sequencing of the exercise transcriptome in equine athletes

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Capomaccio, Stefano ^a   Vitulo, Nicola ^b   Verini Supplizi, Andrea ^a   Barcaccia, Gianni ^b   Albiero, Alessandro ^b   D'Angelo, Michela ^b   Campagna, Davide ^b   Valle, Giorgio ^b   Felicetti, Michela ^a   Silvestrelli, Maurizio ^a   Cappelli, Katia ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 22; UNTRANSLATED RNA;

3' UNTRANSLATED REGION; ADAPTIVE IMMUNITY; ARTICLE; ATHLETE; CONTROLLED STUDY; DOWN REGULATION; ENDURANCE SPORT; EQUIDAE; EXERCISE; GENE EXPRESSION; GENE MAPPING; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; INTRON; PHYSICAL STRESS; PROTEIN SYNTHESIS; RNA SEQUENCE; RNA SPLICING; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSPOSON; UPREGULATION;

ANIMALS; GENE EXPRESSION; GENE REGULATORY NETWORKS; HORSES; MULTIGENE FAMILY; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL EXERTION; RNA SPLICE SITES; SEQUENCE ANALYSIS, RNA; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84896697227     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083504     Document Type: Article

References (57)

1. Purvis D, Gonsalves S, Deuster PA (2010) Physiological and Psychological Fatigue in Extreme Conditions: Overtraining and Elite Athletes. PM&R 2: 442-450. doi:10.1016/j.pmrj.2010.03.025.
2. De Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12: 833-845. doi:10.1038/nrg3055.
3. Art T, Franck T, Gangl M, Votion D, Kohnen S, et al. (2006) Plasma concentrations of myeloperoxidase in endurance and 3-day event horses after a competition. Equine Vet J Suppl: 298-302.
4. Capomaccio S, Cappelli K, Barrey E, Felicetti M, Silvestrelli M, et al. (2010) Microarray analysis after strenuous exercise in peripheral blood mononuclear cells of endurance horses. Anim Genet 41: 166-175.
5. Capomaccio S, Verini-Supplizi A, Galla G, Vitulo N, Barcaccia G, et al. (2010) Transcription of LINE-derived sequences in exercise-induced stress in horses. Anim Genet 41: 23-27.
6. Cappelli K, Verini-Supplizi A, Capomaccio S, Silvestrelli M (2007) Analysis of peripheral blood mononuclear cells gene expression in endurance horses by cDNA-AFLP technique. Res Vet Sci 82: 335-343. (Pubitemid 46554815)
7. Cappelli K, Felicetti M, Capomaccio S, Pieramati C, Silvestrelli M, et al. (2009) Exercise-induced up-regulation of MMP-1 and IL-8 genes in endurance horses. BMC Physiol 9: 12. doi:10.1186/1472-6793-9-12.
8. Cappelli K, Felicetti M, Capomaccio S, Nocelli C, Silvestrelli M, et al. (2013) Effect of training status on immune defence related gene expression in Thoroughbred: Are genes ready for the sprint? Vet J 195: 373-376. doi:10.1016/j.tvjl.2012.07.021.
9. Consortium TEP (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74. doi:10.1038/nature11247.
10. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, et al. (2012) Landscape of transcription in human cells. Nature 489: 101-108. doi:10.1038/nature11233.
11. Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12: 87-98. doi:10.1038/nrg2934.
12. Jacquier A (2009) The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs. Nat Rev Genet 10: 833-844. doi:10.1038/nrg2683.
13. Klevebring D, Bjursell M, Emanuelsson O, Lundeberg J (2010) In-Depth Transcriptome Analysis Reveals Novel TARs and Prevalent Antisense Transcription in Human Cell Lines. PLoS ONE 5: e9762. doi:10.1371/journal.pone.0009762.
14. Morrissy AS, Griffith M, Marra MA (2011) Extensive relationship between antisense transcription and alternative splicing in the human genome. Genome Res 21: 1203-1212. doi:10.1101/gr.113431.110.
15. Numata K, Kiyosawa H (2012) Genome-wide impact of endogenous antisense transcripts in eukaryotes. Front Biosci J Virtual Libr 17: 300.
16. Werner A, Carlile M, Swan D (2009) What do natural antisense transcripts regulate. RNA Biol 6: 43-48.
17. Su W-Y, Xiong H, Fang J-Y (2010) Natural antisense transcripts regulate gene expression in an epigenetic manner. Biochem Biophys Res Commun 396: 177-181. doi:10.1016/j.bbrc.2010.04.147.
18. Kalsotra A, Cooper TA (2011) Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 12: 715-729. doi:10.1038/nrg3052.
19. Pandey R, Mandal AK, Jha V, Mukerji M (2011) Heat shock factor binding in Alu repeats expands its involvement in stress through an antisense mechanism. Genome Biol 12: R117. doi:10.1186/gb-2011-12-11-r117.
20. Park S-J, Huh J-W, Kim Y-H, Kim H-S, Chang K-T (2012) Intron Retention and TE Exonization Events in ZRANB2. Comp Funct Genomics 2012. Available: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3384923/. Accessed 25 July 2012.
21. Bowman TV, McCooey AJ, Merchant AA, Ramos CA, Fonseca P, et al. (2006) Differential mRNA Processing in Hematopoietic Stem Cells. STEM CELLS 24: 662-670. doi:10.1634/stemcells.2005-0552. (Pubitemid 44464770)
22. Sela N, Mersch B, Hotz-Wagenblatt A, Ast G (2010) Characteristics of Transposable Element Exonization within Human and Mouse. PLoS ONE 5: e10907. doi:10.1371/journal.pone.0010907.
23. Cooper TA, Wan L, Dreyfuss G (2009) RNA and Disease. Cell 136: 777-793. doi:10.1016/j.cell.2009.02.011.
24. Cappelli K, Felicetti M, Capomaccio S, Spinsanti G, Silvestrelli M, et al. (2008) Exercise induced stress in horses: selection of the most stable reference genes for quantitative RT-PCR normalization. BMC Mol Biol 9: 49. doi:10.1186/1471-2199-9-49.
25. Rieder S, Taourit S, Mariat D, Langlois B, Guerin G (2001) Mutations in the agouti (ASIP), the extension (MC1R), and the brown (TYRP1) loci and their association to coat color phenotypes in horses (Equus caballus). Mamm Genome 12: 450-455. (Pubitemid 32463738)
26. Campagna D, Albiero A, Bilardi A, Caniato E, Forcato C, et al. (2009) PASS: a program to align short sequences. Bioinforma Oxf Engl 25: 967-968. doi:10.1093/bioinformatics/btp087.
27. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515. doi:10.1038/nbt.1621.
28. Bu D, Yu K, Sun S, Xie C, Skogerbø G, et al. (2011) NONCODE v3.0: integrative annotation of long noncoding RNAs. Nucleic Acids Res. Available: http://nar.oxfordjournals.org/content/early/2011/11/30/nar.gkr1175. Accessed 21 November 2012.
29. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140. doi:10.1093/bioinformatics/btp616.
30. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics 21: 3448-3449. doi:10.1093/bioinformatics/bti551. (Pubitemid 41222459)
31. Tariq MA, Kim HJ, Jejelowo O, Pourmand N (2011) Whole-transcriptome RNAseq analysis from minute amount of total RNA. Nucleic Acids Res 39: e120-e120. doi:10.1093/nar/gkr547.
32. Schmitz J, Brosius J (2011) Exonization of transposed elements: A challenge and opportunity for evolution. Biochimie 93: 1928-1934. doi:10.1016/j.biochi.2011.07.014.
33. Fernandes JMO, MacKenzie MG, Kinghorn JR, Johnston IA (2007) FoxK1 splice variants show developmental stage-specific plasticity of expression with temperature in the tiger pufferfish. J Exp Biol 210: 3461-3472. doi:10.1242/jeb.009183. (Pubitemid 350057244)
34. Nurmi JT, Puolakkainen PA, Rautonen NE (2005) Intron 1 retaining cyclooxygenase 1 splice variant is induced by osmotic stress in human intestinal epithelial cells. Prostaglandins Leukot Essent Fatty Acids 73: 343-350. doi:10.1016/j.plefa.2005.07.004. (Pubitemid 41375629)
35. Yang N, Kazazian HH (2006) L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 13: 763-771. doi:10.1038/nsmb1141. (Pubitemid 44338769)
36. Guttman M, Amit I, Garber M, French C, Lin MF, et al. (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458: 223. doi:10.1038/nature07672.
37. Ebisuya M, Yamamoto T, Nakajima M, Nishida E (2008) Ripples from neighbouring transcription. Nat Cell Biol 10: 1106. doi:10.1038/ncb1771.
38. Struhl K (2007) Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol 14: 103. doi:10.1038/nsmb0207-103.
39. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, et al. (2012) The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Res 22: 1775-1789. doi:10.1101/gr.132159.111.
40. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, et al. (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300. doi:10.1038/nature10398.
41. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10: 155-159. doi:10.1038/nrg2521.
42. König D, Wagner KH, Elmadfa I, Berg A (2001) Exercise and oxidative stress: significance of antioxidants with reference to inflammatory, muscular, and systemic stress. Exerc Immunol Rev 7: 108-133. (Pubitemid 32911045)
43. Neubauer O, Reichhold S, Nersesyan A, König D, Wagner KH (2008) Exercise-induced DNA damage: is there a relationship with inflammatory responses. Exerc Immunol Rev 14: 51-72.
44. Mastorakos G, Ilias I (2006) Interleukin-6. Ann N Y Acad Sci 1088: 373-381. doi:10.1196/annals.1366.021.
45. Müller-Werdan U, Werdan K (2003) [End-organ damage in inflammation and sepsis]. Internist 44: 864-871.
46. Crujeiras AB, Parra D, Milagro FI, Goyenechea E, Larrarte E, et al. (2008) Differential expression of oxidative stress and inflammation related genes in peripheral blood mononuclear cells in response to a low-calorie diet: a nutrigenomics study. Omics J Integr Biol 12: 251-261. doi:10.1089/omi.2008. 0001. (Pubitemid 352773935)
47. Gleeson M (2007) Immune function in sport and exercise. J Appl Physiol 103: 693-699. doi:10.1152/japplphysiol.00008.2007.
48. Nakamura S, Kobayashi M, Sugino T, Kajimoto O, Matoba R, et al. (2010) Effect of exercise on gene expression profile in unfractionated peripheral blood leukocytes. Biochem Biophys Res Commun 391: 846-851. doi:10.1016/j.bbrc.2009. 11.150.
49. Radom-Aizik S, Zaldivar F, Leu S-Y, Cooper DM (2009) Brief Bout of Exercise Alters Gene Expression in Peripheral Blood Mononuclear Cells of Early- and Late-Pubertal Males. Pediatr Res 65: 447-452. doi:10.1203/PDR. 0b013e3181993473.
50. Hashimoto K, Honda A, Hayashi Y, Inuzuka T, Satoh M, et al. (2009) DNA microarray analysis of transcriptional responses of mouse spinal cords to physical exercise. J Toxicol Sci 34: 445-448.
51. Lira FS, Koyama CH, Yamashita AS, Rosa JC, Zanchi NE, et al. (2009) Chronic exercise decreases cytokine production in healthy rat skeletal muscle. Cell Biochem Funct 27: 458-461. doi:10.1002/cbf.1594.
52. Fischer CP (2006) Interleukin-6 in acute exercise and training: what is the biological relevance? Exerc Immunol Rev 12: 6-33.
53. Pedersen BK, Febbraio MA (2008) Muscle as an Endocrine Organ: Focus on Muscle-Derived Interleukin-6. Physiol Rev 88: 1379-1406. doi:10.1152/ physrev.90100.2007.
54. Petersen AMW, Pedersen BK (2006) The role of IL-6 in mediating the anti-inflammatory effects of exercise. J Physiol Pharmacol Off J Pol Physiol Soc 57 Suppl 10: 43-51. (Pubitemid 46548766)
55. Ki SH, Park O, Zheng M, Morales-Ibanez O, Kolls JK, et al. (2010) Interleukin-22 treatment ameliorates alcoholic liver injury in a murine model of chronic-binge ethanol feeding: Role of signal transducer and activator of transcription 3. Hepatology 52: 1291-1300. doi:10.1002/hep.23837.
56. Beyeen AD, Adzemovic MZ, Öckinger J, Stridh P, Becanovic K, et al. (2010) IL-22RA2 Associates with Multiple Sclerosis and Macrophage Effector Mechanisms in Experimental Neuroinflammation. J Immunol 185: 6883-6890. doi:10.4049/jimmunol.1001392.
57. Lakier Smith L (2003) Overtraining, excessive exercise, and altered immunity: is this a T helper-1 versus T helper-2 lymphocyte response? Sports Med Auckl NZ 33: 347-364.