FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Pflugers Arch / Exercise regulates shelterin genes and microRNAs implicated ...
Pflugers Archiv : European journal of physiology2022; 474(11); 1159-1169; doi: 10.1007/s00424-022-02745-0

Exercise regulates shelterin genes and microRNAs implicated in ageing in Thoroughbred horses.

Abstract: Ageing causes a gradual deterioration of bodily functions and telomere degradation. Excessive telomere shortening leads to cellular senescence and decreases tissue vitality. Six proteins, called shelterin, protect telomere integrity and control telomere length through telomerase-dependent mechanisms. Exercise training appears to maintain telomeres in certain somatic cells, although the underlying molecular mechanisms are incompletely understood. Here, we examined the influence of a single bout of vigorous exercise training on leukocyte telomerase reverse transcriptase (TERT) and shelterin gene expression, and the abundance of three microRNAs (miRNAs) implicated in biological ageing (miRNA-143, -223 and -486-5p) in an elite athlete and large animal model, Thoroughbred horses. Gene and miRNA expression were analysed using primer-based and TaqMan Assay qPCR. Leukocyte TRF1, TRF2 and POT1 expression were all significantly increased whilst miR-223 and miR-486-5p were decreased immediately after vigorous exercise (all p < 0.05), and tended to return to baseline levels 24 h after training. Relative to the young horses (~ 3.9 years old), middle-aged horses (~ 14.8 years old) exhibited reduced leukocyte TERT gene expression, and increased POT1 and miR-223 abundance (all p < 0.05). These data demonstrate that genes transcribing key components of the shelterin-telomere complex are influenced by ageing and dynamically regulated by a single bout of vigorous exercise in a large, athletic mammal - Thoroughbred horses. Our findings also implicate TERT and shelterin gene transcripts as potential targets of miR-223 and miR-486-5p, which are modulated by exercise and may have a role in the telomere maintenance and genomic stability associated with long-term aerobic training.
© 2022. The Author(s).
Get Full Text
Publication Date: 2022-09-09 PubMed ID: 36085194PubMed Central: PMC9560944DOI: 10.1007/s00424-022-02745-0Google 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.
LinkedInCopy
  • 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.

This research investigates how vigorous exercise affects certain genes and microRNAs that are linked to aging in thoroughbred horses. The study sheds light on the ways in which exercise might help maintain telomere length and cellular vitality, and thus contribute to delaying the aging process.

Introduction to Telomeres, Shelterin Proteins, and MicroRNAs

  • Ageing involves gradual wear and tear of body functions and degradation of telomeres, which are DNA-protein structures that protect the ends of chromosomes. When telomeres shorten excessively, it results in cellular aging and decreased tissue vitality.
  • Shelterin is a complex of six proteins that protect the integrity and length of telomeres through mechanisms dependent on an enzyme called telomerase.
  • MicroRNAs (miRNAs) are small RNA molecules associated with biological aging. They regulate gene expression and help control cellular processes.

Study Focus-Exercise and Telomere Maintenance

  • The research focuses on the influence of vigorous exercise training on the expression of shelterin gene and telomerase reverse transcriptase (TERT). Also targeted were three specific miRNAs (miRNA-143, miRNA-223 and miRNA-486-5p) known to be involved in aging.
  • The study was conducted among Thoroughbred horses, as an athletic mammal model. This involved analyses of gene and miRNA expressions using primer-based and TaqMan Assay qPCR techniques.

Noteworthy Findings

  • Increased expression of shelterin were noted in the horse’s leukocytes (white blood cells) immediately after they engaged in vigorous exercise.
  • The concentrations of miR-223 and miR-486-5p were found to be significantly lower directly after exercise.
  • Around 24 hours after training, the levels of shelterin and miRNAs started trending back towards their baseline pre-exercise levels.
  • In comparison to younger horses, the middle-aged ones exhibited lower TERT gene expression and higher amounts of POT1 (a shelterin component) and miR-223.

Implications and Conclusion

  • Results indicate that genes associated with the shelterin-telomere complex are impacted both by aging and vigorous exercise.
  • The action of exercise may regulate key components of the shelterin-telomere complex, in part, through modulation of miR-223 and miR-486-5p molecules.
  • This provides insights regarding the potential role of miR-223 and miR-486-5p in genomic stability and telomere maintenance, via exercise, which could in turn influence the process of ageing.
  • Although the research is carried out in horses, the results could have implications for humans since the cellular ageing process is a shared biological mechanism.

Cite This Article

APA
Mandal S, Denham MM, Spencer SJ, Denham J. (2022). Exercise regulates shelterin genes and microRNAs implicated in ageing in Thoroughbred horses. Pflugers Arch, 474(11), 1159-1169. https://doi.org/10.1007/s00424-022-02745-0

Publication

Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
NlmUniqueID: 0154720
Country: Germany
Language: English
Volume: 474
Issue: 11
Pages: 1159-1169

Researcher Affiliations

Mandal, Shama
  • School of Health and Biomedical Sciences, RMIT University, Melbourne, VIC, Australia.
Denham, Michele M
  • Jubilee Stud, Freshwater Creek, Victoria, Australia.
Spencer, Sarah J
  • School of Health and Biomedical Sciences, RMIT University, Melbourne, VIC, Australia.
  • ARC Centre of Excellence for Nanoscale Biophotonics, RMIT University, Melbourne, VIC, Australia.
Denham, Joshua
  • School of Health and Biomedical Sciences, RMIT University, Melbourne, VIC, Australia. josh.denham@usq.edu.au.
  • School of Health and Medical Sciences, University of Southern Queensland, Ipswich, QLD, 4305, Australia. josh.denham@usq.edu.au.
  • School of Science and Technology, University of New England, Armidale, NSW, Australia. josh.denham@usq.edu.au.

MeSH Terms

  • Aging / genetics
  • Animals
  • Horses / genetics
  • Mammals / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Shelterin Complex
  • Telomerase / genetics
  • Telomerase / metabolism
  • Telomere / genetics
  • Telomere / metabolism

Conflict of Interest Statement

M. D. owns and operates a Thoroughbred horse stud.

References

This article includes 52 references
  1. Andersen SL, Sebastiani P, Dworkis DA, Feldman L, Perls TT. Health span approximates life span among many supercentenarians: compression of morbidity at the approximate limit of life span.. J Gerontol A Biol Sci Med Sci 2012 Apr;67(4):395-405.
    doi: 10.1093/gerona/glr223pmc: PMC3309876pubmed: 22219514google scholar: lookup
  2. Aoi W, Ichikawa H, Mune K, Tanimura Y, Mizushima K, Naito Y, Yoshikawa T. Muscle-enriched microRNA miR-486 decreases in circulation in response to exercise in young men.. Front Physiol 2013;4:80.
    doi: 10.3389/fphys.2013.00080pmc: PMC3622901pubmed: 23596423google scholar: lookup
  3. Bandaria JN, Qin P, Berk V, Chu S, Yildiz A. Shelterin Protects Chromosome Ends by Compacting Telomeric Chromatin.. Cell 2016 Feb 11;164(4):735-46.
    doi: 10.1016/j.cell.2016.01.036pmc: PMC4762449pubmed: 26871633google scholar: lookup
  4. Bond SL, Greco-Otto P, Sides R, Kwong GPS, Léguillette R, Bayly WM. Assessment of two methods to determine the relative contributions of the aerobic and anaerobic energy systems in racehorses.. J Appl Physiol (1985) 2019 May 1;126(5):1390-1398.
    doi: 10.1152/japplphysiol.00983.2018pubmed: 30763162google scholar: lookup
  5. 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.
    doi: 10.1186/1471-2199-9-49pmc: PMC2412902pubmed: 18489742google scholar: lookup
  6. Chilton WL, Marques FZ, West J, Kannourakis G, Berzins SP, O'Brien BJ, Charchar FJ. Acute exercise leads to regulation of telomere-associated genes and microRNA expression in immune cells.. PLoS One 2014;9(4):e92088.
    doi: 10.1371/journal.pone.0092088pmc: PMC3994003pubmed: 24752326google scholar: lookup
  7. Colgin LM, Baran K, Baumann P, Cech TR, Reddel RR. Human POT1 facilitates telomere elongation by telomerase.. Curr Biol 2003 May 27;13(11):942-6.
    doi: 10.1016/s0960-9822(03)00339-7pubmed: 12781132google scholar: lookup
  8. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP. A DNA damage checkpoint response in telomere-initiated senescence.. Nature 2003 Nov 13;426(6963):194-8.
    doi: 10.1038/nature02118pubmed: 14608368google scholar: lookup
  9. Denham J, Denham MM. Leukocyte telomere length in the Thoroughbred racehorse.. Anim Genet 2018 Oct;49(5):452-456.
    doi: 10.1111/age.12681pubmed: 30051918google scholar: lookup
  10. Denham J, Prestes PR. Muscle-Enriched MicroRNAs Isolated from Whole Blood Are Regulated by Exercise and Are Potential Biomarkers of Cardiorespiratory Fitness.. Front Genet 2016;7:196.
    doi: 10.3389/fgene.2016.00196pmc: PMC5108773pubmed: 27895662google scholar: lookup
  11. Denham J, Sellami M. Exercise training increases telomerase reverse transcriptase gene expression and telomerase activity: A systematic review and meta-analysis.. Ageing Res Rev 2021 Sep;70:101411.
    doi: 10.1016/j.arr.2021.101411pubmed: 34284150google scholar: lookup
  12. Denham J, O'Brien BJ, Prestes PR, Brown NJ, Charchar FJ. Increased expression of telomere-regulating genes in endurance athletes with long leukocyte telomeres.. J Appl Physiol (1985) 2016 Jan 15;120(2):148-58.
    doi: 10.1152/japplphysiol.00587.2015pubmed: 26586905google scholar: lookup
  13. Denham J, Marques FZ, O'Brien BJ, Charchar FJ. Exercise: putting action into our epigenome.. Sports Med 2014 Feb;44(2):189-209.
    doi: 10.1007/s40279-013-0114-1pubmed: 24163284google scholar: lookup
  14. Denham J, O'Brien BJ, Charchar FJ. Telomere Length Maintenance and Cardio-Metabolic Disease Prevention Through Exercise Training.. Sports Med 2016 Sep;46(9):1213-37.
    doi: 10.1007/s40279-016-0482-4pubmed: 26914269google scholar: lookup
  15. Denham J, Stevenson K, Denham MM. Age-associated telomere shortening in Thoroughbred horses.. Exp Gerontol 2019 Nov;127:110718.
    doi: 10.1016/j.exger.2019.110718pubmed: 31479729google scholar: lookup
  16. D'Souza RF, Woodhead JST, Zeng N, Blenkiron C, Merry TL, Cameron-Smith D, Mitchell CJ. Circulatory exosomal miRNA following intense exercise is unrelated to muscle and plasma miRNA abundances.. Am J Physiol Endocrinol Metab 2018 Oct 1;315(4):E723-E733.
    doi: 10.1152/ajpendo.00138.2018pubmed: 29969318google scholar: lookup
  17. Ehtesham N, Shahrbanian S, Valadiathar M, Mowla SJ. Modulations of obesity-related microRNAs after exercise intervention: a systematic review and bioinformatics analysis.. Mol Biol Rep 2021 Mar;48(3):2817-2831.
    doi: 10.1007/s11033-021-06275-3pubmed: 33772703google scholar: lookup
  18. Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs.. Annu Rev Biochem 2010;79:351-79.
    doi: 10.1146/annurev-biochem-060308-103103pubmed: 20533884google scholar: lookup
  19. Hagman M, Werner C, Kamp K, Fristrup B, Hornstrup T, Meyer T, Böhm M, Laufs U, Krustrup P. Reduced telomere shortening in lifelong trained male football players compared to age-matched inactive controls.. Prog Cardiovasc Dis 2020 Nov-Dec;63(6):738-749.
    doi: 10.1016/j.pcad.2020.05.009pubmed: 32497584google scholar: lookup
  20. Hemann MT, Greider CW. Wild-derived inbred mouse strains have short telomeres.. Nucleic Acids Res 2000 Nov 15;28(22):4474-8.
    doi: 10.1093/nar/28.22.4474pmc: PMC113886pubmed: 11071935google scholar: lookup
  21. Holohan B, Wright WE, Shay JW. Cell biology of disease: Telomeropathies: an emerging spectrum disorder.. J Cell Biol 2014 May 12;205(3):289-99.
    doi: 10.1083/jcb.201401012pmc: PMC4018777pubmed: 24821837google scholar: lookup
  22. Karlseder J, Smogorzewska A, de Lange T. Senescence induced by altered telomere state, not telomere loss.. Science 2002 Mar 29;295(5564):2446-9.
    doi: 10.1126/science.1069523pubmed: 11923537google scholar: lookup
  23. Laye MJ, Solomon TP, Karstoft K, Pedersen KK, Nielsen SD, Pedersen BK. Increased shelterin mRNA expression in peripheral blood mononuclear cells and skeletal muscle following an ultra-long-distance running event.. J Appl Physiol (1985) 2012 Mar;112(5):773-81.
    doi: 10.1152/japplphysiol.00997.2011pubmed: 22162529google scholar: lookup
  24. Loayza D, De Lange T. POT1 as a terminal transducer of TRF1 telomere length control.. Nature 2003 Jun 26;423(6943):1013-8.
    doi: 10.1038/nature01688pubmed: 12768206google scholar: lookup
  25. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging.. Cell 2013 Jun 6;153(6):1194-217.
    doi: 10.1016/j.cell.2013.05.039pmc: PMC3836174pubmed: 23746838google scholar: lookup
  26. Lu H, Buchan RJ, Cook SA. MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism.. Cardiovasc Res 2010 Jun 1;86(3):410-20.
    doi: 10.1093/cvr/cvq010pubmed: 20080987google scholar: lookup
  27. Ludlow AT, Witkowski S, Marshall MR, Wang J, Lima LC, Guth LM, Spangenburg EE, Roth SM. Chronic exercise modifies age-related telomere dynamics in a tissue-specific fashion.. J Gerontol A Biol Sci Med Sci 2012 Sep;67(9):911-26.
    doi: 10.1093/gerona/gls002pmc: PMC3436090pubmed: 22389464google scholar: lookup
  28. Ludlow AT, Gratidão L, Ludlow LW, Spangenburg EE, Roth SM. Acute exercise activates p38 MAPK and increases the expression of telomere-protective genes in cardiac muscle.. Exp Physiol 2017 Apr 1;102(4):397-410.
    doi: 10.1113/EP086189pmc: PMC5378631pubmed: 28166612google scholar: lookup
  29. Mach N, Plancade S, Pacholewska A, Lecardonnel J, Rivière J, Moroldo M, Vaiman A, Morgenthaler C, Beinat M, Nevot A, Robert C, Barrey E. Integrated mRNA and miRNA expression profiling in blood reveals candidate biomarkers associated with endurance exercise in the horse.. Sci Rep 2016 Mar 10;6:22932.
    doi: 10.1038/srep22932pmc: PMC4785432pubmed: 26960911google scholar: lookup
  30. McGowan TW, Pinchbeck G, Phillips CJ, Perkins N, Hodgson DR, McGowan CM. A survey of aged horses in Queensland, Australia. Part 1: management and preventive health care.. Aust Vet J 2010 Nov;88(11):420-7.
    doi: 10.1111/j.1751-0813.2010.00637.xpubmed: 20958281google scholar: lookup
  31. Mundstock E, Zatti H, Louzada FM, Oliveira SG, Guma FT, Paris MM, Rueda AB, Machado DG, Stein RT, Jones MH, Sarria EE, Barbé-Tuana FM, Mattiello R. Effects of physical activity in telomere length: Systematic review and meta-analysis.. Ageing Res Rev 2015 Jul;22:72-80.
    doi: 10.1016/j.arr.2015.02.004pubmed: 25956165google scholar: lookup
  32. Nandakumar J, Bell CF, Weidenfeld I, Zaug AJ, Leinwand LA, Cech TR. The TEL patch of telomere protein TPP1 mediates telomerase recruitment and processivity.. Nature 2012 Dec 13;492(7428):285-9.
    doi: 10.1038/nature11648pmc: PMC3521872pubmed: 23103865google scholar: lookup
  33. Nielsen S, Åkerström T, Rinnov A, Yfanti C, Scheele C, Pedersen BK, Laye MJ. The miRNA plasma signature in response to acute aerobic exercise and endurance training.. PLoS One 2014;9(2):e87308.
    doi: 10.1371/journal.pone.0087308pmc: PMC3929352pubmed: 24586268google scholar: lookup
  34. O'Connor MS, Safari A, Xin H, Liu D, Songyang Z. A critical role for TPP1 and TIN2 interaction in high-order telomeric complex assembly.. Proc Natl Acad Sci U S A 2006 Aug 8;103(32):11874-9.
    doi: 10.1073/pnas.0605303103pmc: PMC1567669pubmed: 16880378google scholar: lookup
  35. Ohmura H, Matsui A, Hada T, Jones JH. Physiological responses of young thoroughbred horses to intermittent high-intensity treadmill training.. Acta Vet Scand 2013 Aug 17;55(1):59.
    doi: 10.1186/1751-0147-55-59pmc: PMC3765425pubmed: 23957961google scholar: lookup
  36. Rusanova I, Diaz-Casado ME, Fernández-Ortiz M, Aranda-Martínez P, Guerra-Librero A, García-García FJ, Escames G, Mañas L, Acuña-Castroviejo D. Analysis of Plasma MicroRNAs as Predictors and Biomarkers of Aging and Frailty in Humans.. Oxid Med Cell Longev 2018;2018:7671850.
    doi: 10.1155/2018/7671850pmc: PMC6079380pubmed: 30116492google scholar: lookup
  37. Schmidt JC, Dalby AB, Cech TR. Identification of human TERT elements necessary for telomerase recruitment to telomeres.. Elife 2014 Oct 1;3.
    pmc: PMC4359370pubmed: 25271372doi: 10.7554/eLife.03563google scholar: lookup
  38. Schoenhofen EA, Wyszynski DF, Andersen S, Pennington J, Young R, Terry DF, Perls TT. Characteristics of 32 supercentenarians.. J Am Geriatr Soc 2006 Aug;54(8):1237-40.
    doi: 10.1111/j.1532-5415.2006.00826.xpmc: PMC2895458pubmed: 16913991google scholar: lookup
  39. Sfeir A, de Lange T. Removal of shelterin reveals the telomere end-protection problem.. Science 2012 May 4;336(6081):593-7.
    doi: 10.1126/science.1218498pmc: PMC3477646pubmed: 22556254google scholar: lookup
  40. Shaheen F, Grammatopoulos DK, Müller J, Zammit VA, Lehnert H. Extra-nuclear telomerase reverse transcriptase (TERT) regulates glucose transport in skeletal muscle cells.. Biochim Biophys Acta 2014 Sep;1842(9):1762-9.
    doi: 10.1016/j.bbadis.2014.06.018pubmed: 24970747google scholar: lookup
  41. Silva GJJ, Bye A, El Azzouzi H, Wisløff U. MicroRNAs as Important Regulators of Exercise Adaptation.. Prog Cardiovasc Dis 2017 Jun-Jul;60(1):130-151.
    doi: 10.1016/j.pcad.2017.06.003pubmed: 28666746google scholar: lookup
  42. Soriano-Arroquia A, McCormick R, Molloy AP, McArdle A, Goljanek-Whysall K. Age-related changes in miR-143-3p:Igfbp5 interactions affect muscle regeneration.. Aging Cell 2016 Apr;15(2):361-9.
    doi: 10.1111/acel.12442pmc: PMC4783349pubmed: 26762731google scholar: lookup
  43. Steptoe A, Hamer M, Lin J, Blackburn EH, Erusalimsky JD. The Longitudinal Relationship Between Cortisol Responses to Mental Stress and Leukocyte Telomere Attrition.. J Clin Endocrinol Metab 2017 Mar 1;102(3):962-969.
    doi: 10.1210/jc.2016-3035pmc: PMC5460695pubmed: 27967317google scholar: lookup
  44. Teteloshvili N, Kluiver J, van der Geest KS, van der Lei RJ, Jellema P, Pawelec G, Brouwer E, Kroesen BJ, Boots AM, van den Berg A. Age-Associated Differences in MiRNA Signatures Are Restricted to CD45RO Negative T Cells and Are Associated with Changes in the Cellular Composition, Activation and Cellular Ageing.. PLoS One 2015;10(9):e0137556.
    doi: 10.1371/journal.pone.0137556pmc: PMC4567287pubmed: 26360056google scholar: lookup
  45. Thompson CAH, Wong JMY. Non-canonical Functions of Telomerase Reverse Transcriptase: Emerging Roles and Biological Relevance.. Curr Top Med Chem 2020;20(6):498-507.
    doi: 10.2174/1568026620666200131125110pubmed: 32003692google scholar: lookup
  46. Treiber T, Treiber N, Meister G. Regulation of microRNA biogenesis and function.. Thromb Haemost 2012 Apr;107(4):605-10.
    doi: 10.1160/TH11-12-0836pubmed: 22318703google scholar: lookup
  47. Valente C, Andrade R, Alvarez L, Rebelo-Marques A, Stamatakis E, Espregueira-Mendes J. Effect of physical activity and exercise on telomere length: Systematic review with meta-analysis.. J Am Geriatr Soc 2021 Nov;69(11):3285-3300.
    doi: 10.1111/jgs.17334pubmed: 34161613google scholar: lookup
  48. Wang F, Podell ER, Zaug AJ, Yang Y, Baciu P, Cech TR, Lei M. The POT1-TPP1 telomere complex is a telomerase processivity factor.. Nature 2007 Feb 1;445(7127):506-10.
    doi: 10.1038/nature05454pubmed: 17237768google scholar: lookup
  49. Werner C, Hanhoun M, Widmann T, Kazakov A, Semenov A, Pöss J, Bauersachs J, Thum T, Pfreundschuh M, Müller P, Haendeler J, Böhm M, Laufs U. Effects of physical exercise on myocardial telomere-regulating proteins, survival pathways, and apoptosis.. J Am Coll Cardiol 2008 Aug 5;52(6):470-82.
    doi: 10.1016/j.jacc.2008.04.034pubmed: 18672169google scholar: lookup
  50. Werner C, Fürster T, Widmann T, Pöss J, Roggia C, Hanhoun M, Scharhag J, Büchner N, Meyer T, Kindermann W, Haendeler J, Böhm M, Laufs U. Physical exercise prevents cellular senescence in circulating leukocytes and in the vessel wall.. Circulation 2009 Dec 15;120(24):2438-47.
    doi: 10.1161/CIRCULATIONAHA.109.861005pubmed: 19948976google scholar: lookup
  51. Whittemore K, Vera E, Martínez-Nevado E, Sanpera C, Blasco MA. Telomere shortening rate predicts species life span.. Proc Natl Acad Sci U S A 2019 Jul 23;116(30):15122-15127.
    doi: 10.1073/pnas.1902452116pmc: PMC6660761pubmed: 31285335google scholar: lookup
  52. Yang L, Li Y, Wang X, Mu X, Qin D, Huang W, Alshahrani S, Nieman M, Peng J, Essandoh K, Peng T, Wang Y, Lorenz J, Soleimani M, Zhao ZQ, Fan GC. Overexpression of miR-223 Tips the Balance of Pro- and Anti-hypertrophic Signaling Cascades toward Physiologic Cardiac Hypertrophy.. J Biol Chem 2016 Jul 22;291(30):15700-13.
    doi: 10.1074/jbc.M116.715805pmc: PMC4957053pubmed: 27226563google scholar: lookup

Citations

This article has been cited 6 times.
  1. Abdolmaleky HM, Zhou JR. Underlying Mechanisms of Brain Aging and Neurodegenerative Diseases as Potential Targets for Preventive or Therapeutic Strategies Using Phytochemicals. Nutrients 2023 Aug 4;15(15).
    doi: 10.3390/nᔕ3456pubmed: 37571393google scholar: lookup
  2. Denham J. Canonical and extra-telomeric functions of telomerase: Implications for healthy ageing conferred by endurance training. Aging Cell 2023 Jun;22(6):e13836.
    doi: 10.1111/acel.13836pubmed: 37041671google scholar: lookup
  3. Castanheira CIGD, Taylor S, Skiöldebrand E, Rubio-Martinez LM, Hackl M, Clegg PD, Peffers MJ. Synovial Fluid and Serum MicroRNA Signatures in Equine Osteoarthritis. Int J Mol Sci 2025 Nov 19;26(22).
    doi: 10.3390/ijms262211190pubmed: 41303673google scholar: lookup
  4. Ma S, Ren W, Li Z, Li L, Wang R, Su Y, Huang Q, Dehaxi S, Wang J. Comparative analysis of miRNA expression in Yili horses pre- and post-5000-m race. Front Genet 2025;16:1676558.
    doi: 10.3389/fgene.2025.1676558pubmed: 41098164google scholar: lookup
  5. Ding W, Gong W, Bou T, Shi L, Lin Y, Wu H, Dugarjaviin M, Bai D. Pilot Study on the Profiling and Functional Analysis of mRNA, miRNA, and lncRNA in the Skeletal Muscle of Mongolian Horses, Xilingol Horses, and Grassland-Thoroughbreds. Animals (Basel) 2025 Apr 13;15(8).
    doi: 10.3390/ani15081123pubmed: 40281957google scholar: lookup
  6. Iskandar M, Xiao Barbero M, Jaber M, Chen R, Gomez-Guevara R, Cruz E, Westerheide S. A Review of Telomere Attrition in Cancer and Aging: Current Molecular Insights and Future Therapeutic Approaches. Cancers (Basel) 2025 Jan 14;17(2).
    doi: 10.3390/cancers17020257pubmed: 39858038google scholar: lookup
Subscribe to our newsletter
Join 99,383 horse owners like you who receive our email updates on horse health and nutrition.