FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / BMC Vet Res / Molecular characterization of the apoptosis-related SH3RF1 a...
BMC veterinary research2018; 14(1); 237; doi: 10.1186/s12917-018-1567-0

Molecular characterization of the apoptosis-related SH3RF1 and SH3RF2 genes and their association with exercise performance in Arabian horses.

Abstract: Apoptosis plays an important role in the regulation of healthy tissue growth and development as well as in controlling the maintenance of homeostasis in exercising muscles. During an intensive physical effort, the regulation of cell death by apoptosis results in the replacement of unaccustomed muscle cells by new cells that are better suited to exercise. The aim of this study was to determine the expression of two genes (SH3FR1 and SH3RF2) that control apoptosis in muscle tissues during training periods characterized by different intensities. The gene expression levels were estimated using real-time PCR method in skeletal muscle biopsies collected from 15 Arabian horses (untrained, after an intense gallop phase, and at the end of the racing season). An association study was performed on 250 Arabian horses to assess the effect of the SH3RF2:c.796 T > C (p.Ser266Pro) variant on race performance traits in flat gallop-racing. Results: A gene expression analysis confirmed a significant decrease (p  C missense variant was associated with selected racing performance traits, which is important information during the evaluation of horses' exercise predisposition. The association results and frequencies of the CT and TT genotypes suggest the possibility of using SH3RF2 variant in selection to improve the racing performance of Arabian horses.
Get Full Text
Publication Date: 2018-08-14 PubMed ID: 30107803PubMed Central: PMC6092840DOI: 10.1186/s12917-018-1567-0Google 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

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 examines the relationship between two apoptosis-related genes, SH3RF1 and SH3RF2, and the performance of Arabian racehorses during different periods of exercise intensity. Findings indicate that variations in the SH3RF2 gene can impact race performance and could potentially be used in selection criteria to improve the performance of these horses.

About the Research

  • The researchers studied the role of apoptosis – a process of programmed cell death – in the context of exercise performance in Arabian horses. Apoptosis helps maintain homeostasis in muscles during exercise. It enables unaccustomed muscle cells to be replaced by new cells that are better adapted to exercise.
  • The focus of the study was on the expression of two genes associated with apoptosis (SH3RF1 and SH3RF2) in muscle tissues during different phases of training.
  • Gene expression levels were gauged using real-time PCR methods, taking samples from skeletal muscle biopsies from 15 Arabian horses at various stages: untrained, after an intense gallop phase, and at the end of the racing season.
  • Another component of the study involved an association assessment performed on 250 Arabian horses to examine the influence of specific variants of the SH3RF2 gene on racing performance outcomes in flat gallop-racing.

Key Findings

  • Results revealed a significant decrease in the expression of the SH3RF2 gene (which is anti-apoptotic) during various training intensities – the highest expression being in untrained horses and the lowest at the end of the racing season in trained horses. However, there was no significant change in the SH3RF1 gene.
  • A particular variant of the SH3RF2 gene (specifically, a serine substitution by proline at amino acid position 266, denoted by the CC genotype) correlated negatively with the probability of winning races, the number of races participated in, and the monetary value of prizes. In contrast, horses carrying the TT genotype had the highest financial success both in total winnings and per race.

Conclusions and Implications

  • This study illustrates the potential regulation mechanism of apoptosis induced by exercise on a molecular level in horses.
  • The discovered SH3RF2 gene variant (c.796 T > C) was found to be associated with selected racing performance traits, which is crucial for analyzing a horse’s exercise predisposition.
  • The research findings suggest the possibility of using SH3RF2 gene variation for selection purposes, which could lead to an improved performance of Arabian racehorses.

Cite This Article

APA
Ropka-Molik K, Stefaniuk-Szmukier M, Piórkowska K, Szmatoła T, Bugno-Poniewierska M. (2018). Molecular characterization of the apoptosis-related SH3RF1 and SH3RF2 genes and their association with exercise performance in Arabian horses. BMC Vet Res, 14(1), 237. https://doi.org/10.1186/s12917-018-1567-0

Publication

BMC veterinary research
ISSN: 1746-6148
NlmUniqueID: 101249759
Country: England
Language: English
Volume: 14
Issue: 1
Pages: 237
PII: 237

Researcher Affiliations

Ropka-Molik, K
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Kraków, Poland. katarzyna.ropka@izoo.krakow.pl.
  • Laboratory of Genomics, National Research Institute of Animal Production, Krakowska 1, 32-083, Balice, Poland. katarzyna.ropka@izoo.krakow.pl.
Stefaniuk-Szmukier, M
  • Department of Horse Breeding, Institute of Animal Science, the University of Agriculture in Cracow, Kraków, Poland.
Piórkowska, K
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Kraków, Poland.
Szmatoła, T
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Kraków, Poland.
Bugno-Poniewierska, M
  • Institute of Veterinary Sciences University of Agriculture in Krakow, Kraków, Poland.

MeSH Terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Gene Expression
  • Genotype
  • Horses / genetics
  • Horses / physiology
  • Muscle, Skeletal / metabolism
  • Physical Conditioning, Animal / physiology
  • Physical Fitness / physiology
  • Polymorphism, Single Nucleotide
  • Running / physiology

Grant Funding

  • 2014/15/D/NZ9/05256 / Narodowym Centrum Nauki

Conflict of Interest Statement

ETHICS APPROVAL: The protocol was approved by the Animal Care and Use Committee of the Institute of Pharmacology, Polish Academy of Sciences in Cracow (no. 1173/2015). The horses’ owners gave consent to be part of this study and allowed for maintaining all research procedures on animals. The constant was obtained verbally which approved by Ethics Committee. CONSENT FOR PUBLICATION: Not applicable. COMPETING INTERESTS: The authors declare that they have no competing interests. PUBLISHER’S NOTE: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

This article includes 34 references
  1. Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation.. Cell Metab 2013 Feb 5;17(2):162-84.
    doi: 10.1016/j.cmet.2012.12.012pubmed: 23395166google scholar: lookup
  2. Ferraro E, Giammarioli AM, Chiandotto S, Spoletini I, Rosano G. Exercise-induced skeletal muscle remodeling and metabolic adaptation: redox signaling and role of autophagy.. Antioxid Redox Signal 2014 Jul 1;21(1):154-76.
    doi: 10.1089/ars.2013.5773pmc: PMC4048572pubmed: 24450966google scholar: lookup
  3. Bazgir B, Fathi R, Rezazadeh Valojerdi M, Mozdziak P, Asgari A. Satellite Cells Contribution to Exercise Mediated Muscle Hypertrophy and Repair.. Cell J 2017 Winter;18(4):473-484.
    pmc: PMC5086326pubmed: 28042532doi: 10.22074/cellj.2016.4714google scholar: lookup
  4. Antonio J, Gonyea WJ. Skeletal muscle fiber hyperplasia.. Med Sci Sports Exerc 1993 Dec;25(12):1333-45.
    doi: 10.1249/00005768-199312000-00004pubmed: 8107539google scholar: lookup
  5. Yan Z, Okutsu M, Akhtar YN, Lira VA. Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle.. J Appl Physiol (1985) 2011 Jan;110(1):264-74.
    doi: 10.1152/japplphysiol.00993.2010pmc: PMC3253006pubmed: 21030673google scholar: lookup
  6. Carraro U, Franceschi C. Apoptosis of skeletal and cardiac muscles and physical exercise.. Aging (Milano) 1997 Feb-Apr;9(1-2):19-34.
    doi: 10.1007/BF03340125pubmed: 9177583google scholar: lookup
  7. Phaneuf S, Leeuwenburgh C. Apoptosis and exercise.. Med Sci Sports Exerc 2001 Mar;33(3):393-6.
    doi: 10.1097/00005768-200103000-00010pubmed: 11252065google scholar: lookup
  8. Siu PM, Bryner RW, Martyn JK, Alway SE. Apoptotic adaptations from exercise training in skeletal and cardiac muscles.. FASEB J 2004 Jul;18(10):1150-2.
    doi: 10.1096/fj.03-1291fjepubmed: 15132982google scholar: lookup
  9. Boffi FM, Cittar J, Balskus G, Muriel M, Desmaras E. Training-induced apoptosis in skeletal muscle.. Equine Vet J Suppl 2002 Sep;(34):275-8.
    doi: 10.1111/j.2042-3306.2002.tb05432.xpubmed: 12405700google scholar: lookup
  10. Ropka-Molik K, Stefaniuk-Szmukier M, Z Ukowski K, Piórkowska K, Bugno-Poniewierska M. Exercise-induced modification of the skeletal muscle transcriptome in Arabian horses.. Physiol Genomics 2017 Jun 1;49(6):318-326.
    doi: 10.1152/physiolgenomics.00130.2016pubmed: 28455310google scholar: lookup
  11. Wilhelm M, Kukekov NV, Schmit TL, Biagas KV, Sproul AA, Gire S, Maes ME, Xu Z, Greene LA. Sh3rf2/POSHER protein promotes cell survival by ring-mediated proteasomal degradation of the c-Jun N-terminal kinase scaffold POSH (Plenty of SH3s) protein.. J Biol Chem 2012 Jan 13;287(3):2247-56.
    doi: 10.1074/jbc.M111.269431pmc: PMC3265902pubmed: 22128169google scholar: lookup
  12. Lennox AL, Stronach B. POSH misexpression induces caspase-dependent cell death in Drosophila.. Dev Dyn 2010 Feb;239(2):651-64.
    doi: 10.1002/dvdy.22186pmc: PMC4083821pubmed: 20014406google scholar: lookup
  13. de Bock CE, Hughes MR, Snyder K, Alley S, Sadeqzadeh E, Dun MD, McNagny KM, Molloy TJ, Hondermarck H, Thorne RF. Protein interaction screening identifies SH3RF1 as a new regulator of FAT1 protein levels.. FEBS Lett 2017 Feb;591(4):667-678.
    doi: 10.1002/1873-3468.12569pubmed: 28129444google scholar: lookup
  14. Stefaniuk M, Ropka-Molik K, Piórkowska K, Bereta A, Szpar P, Czerwonka Z, Podstawski Z. Evaluation of minimally invasive muscle biopsy method for genetic analysis in horse. Ann of Anim Sci 2015;15(3):621–627.
    doi: 10.1515/aoas-2015-0017google scholar: lookup
  15. Knych HK, Harrison LM, Steinmetz SJ, Chouicha N, Kass PH. Differential expression of skeletal muscle genes following administration of clenbuterol to exercised horses.. BMC Genomics 2016 Aug 9;17:596.
    doi: 10.1186/s12864-016-2945-2pmc: PMC4979108pubmed: 27506674google scholar: lookup
  16. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR.. Nucleic Acids Res 2001 May 1;29(9):e45.
    doi: 10.1093/nar/29.9.e45pmc: PMC55695pubmed: 11328886google scholar: lookup
  17. Hachija J, Kazui H. Studies of histological and molecular biologicalchanges after graded periods of ischemia-reperfusion in mouse skeletal muscle. Basic Appl Myol 1996;6:302.
  18. Kim TW, Kang YK, Park ZY, Kim YH, Hong SW, Oh SJ, Sohn HA, Yang SJ, Jang YJ, Lee DC, Kim SY, Yoo HS, Kim E, Yeom YI, Park KC. SH3RF2 functions as an oncogene by mediating PAK4 protein stability.. Carcinogenesis 2014 Mar;35(3):624-34.
    doi: 10.1093/carcin/bgt338pubmed: 24130170google scholar: lookup
  19. Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, von Mering C. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible.. Nucleic Acids Res 2017 Jan 4;45(D1):D362-D368.
    doi: 10.1093/nar/gkw937pmc: PMC5210637pubmed: 27924014google scholar: lookup
  20. Chen CY, Lai NS, Yang JJ, Huang HL, Hung WC, Li C, Lin TH, Huang HB. FLJ23654 encodes a heart protein phosphatase 1-binding protein (Hepp1).. Biochem Biophys Res Commun 2010 Jan 1;391(1):698-702.
    doi: 10.1016/j.bbrc.2009.11.123pubmed: 19945436google scholar: lookup
  21. Gesing A, Masternak MM, Wang F, Lewinski A, Karbownik-Lewinska M, Bartke A. Decreased expression level of apoptosis-related genes and/or proteins in skeletal muscles, but not in hearts, of growth hormone receptor knockout mice.. Exp Biol Med (Maywood) 2011 Feb;236(2):156-68.
    doi: 10.1258/ebm.2010.010202pmc: PMC3703836pubmed: 21321312google scholar: lookup
  22. Liu TR, Su X, Qiu WS, Chen WC, Men QQ, Zou L, Li ZQ, Fu XY, Yang AK. Thyroid-stimulating hormone receptor affects metastasis and prognosis in papillary thyroid carcinoma.. Eur Rev Med Pharmacol Sci 2016 Sep;20(17):3582-91.
    pubmed: 27649658
  23. Schlessinger J. SH2/SH3 signaling proteins.. Curr Opin Genet Dev 1994 Feb;4(1):25-30.
    doi: 10.1016/0959-437X(94)90087-6pubmed: 8193536google scholar: lookup
  24. Kozlowski LP, Bujnicki JM. MetaDisorder: a meta-server for the prediction of intrinsic disorder in proteins.. BMC Bioinformatics 2012 May 24;13:111.
    doi: 10.1186/1471-2105-13-111pmc: PMC3465245pubmed: 22624656google scholar: lookup
  25. Dor O, Zhou Y. Real-SPINE: an integrated system of neural networks for real-value prediction of protein structural properties.. Proteins 2007 Jul 1;68(1):76-81.
    doi: 10.1002/prot.21408pubmed: 17397056google scholar: lookup
  26. Adamczak R, Porollo A, Meller J. Combining prediction of secondary structure and solvent accessibility in proteins.. Proteins 2005 May 15;59(3):467-75.
    doi: 10.1002/prot.20441pubmed: 15768403google scholar: lookup
  27. Eisenberg D, McLachlan AD. Solvation energy in protein folding and binding.. Nature 1986 Jan 16-22;319(6050):199-203.
    doi: 10.1038/319199a0pubmed: 3945310google scholar: lookup
  28. Chong SH, Ham S. Dynamics of Hydration Water Plays a Key Role in Determining the Binding Thermodynamics of Protein Complexes.. Sci Rep 2017 Aug 18;7(1):8744.
    doi: 10.1038/s41598-017-09466-wpmc: PMC5562873pubmed: 28821854google scholar: lookup
  29. Rubin CJ, Zody MC, Eriksson J, Meadows JR, Sherwood E, Webster MT, Jiang L, Ingman M, Sharpe T, Ka S, Hallböök F, Besnier F, Carlborg O, Bed'hom B, Tixier-Boichard M, Jensen P, Siegel P, Lindblad-Toh K, Andersson L. Whole-genome resequencing reveals loci under selection during chicken domestication.. Nature 2010 Mar 25;464(7288):587-91.
    doi: 10.1038/nature08832pubmed: 20220755google scholar: lookup
  30. Hanotte O, Ronin Y, Agaba M, Nilsson P, Gelhaus A, Horstmann R, Sugimoto Y, Kemp S, Gibson J, Korol A, Soller M, Teale A. Mapping of quantitative trait loci controlling trypanotolerance in a cross of tolerant West African N'Dama and susceptible East African Boran cattle.. Proc Natl Acad Sci U S A 2003 Jun 24;100(13):7443-8.
    doi: 10.1073/pnas.1232392100pmc: PMC164605pubmed: 12805560google scholar: lookup
  31. Boitard S, Rocha D. Detection of signatures of selective sweeps in the Blonde d'Aquitaine cattle breed.. Anim Genet 2013 Aug;44(5):579-83.
    doi: 10.1111/age.12042pubmed: 23647053google scholar: lookup
  32. Kim SW, Lee JH, Park TS. Functional analysis of SH3 domain containing ring finger 2 during the myogenic differentiation of quail myoblast cells.. Asian-Australas J Anim Sci 2017 Aug;30(8):1183-1189.
    doi: 10.5713/ajas.16.0865pmc: PMC5494493pubmed: 28111446google scholar: lookup
  33. Ricard A, Bruns E, Cunningham EP. Genetics of performance traits. In: Bowling AT, Ruvinsky A, editors. Genetics of the horse: CABI Publishing, New York; 2000. p. 411–38.
  34. Barrey E. Reviewe: Genetics and genomics in equine exercise physiology: an overview of the new applications of molecular biology as positive and negative markers of performance and health.. Equine Vet J Suppl 2010 Nov;(38):561-8.
    doi: 10.1111/j.2042-3306.2010.00299.xpubmed: 21059061google scholar: lookup

Citations

This article has been cited 8 times.
  1. Ropka-Molik K, Stefaniuk-Szmukier M, Musiał AD, Velie BD. The Genetics of Racing Performance in Arabian Horses. Int J Genomics 2019;2019:9013239.
    doi: 10.1155/2019/9013239pubmed: 31565654google scholar: lookup
  2. Stefaniuk-Szmukier M, Szmatoła T, Łątka J, Długosz B, Ropka-Molik K. The Blood and Muscle Expression Pattern of the Equine TCAP Gene during the Race Track Training of Arabian Horses. Animals (Basel) 2019 Aug 18;9(8).
    doi: 10.3390/ani9080574pubmed: 31426609google scholar: lookup
  3. Kim SW, Jo A, Im J, Lee HE, Kim HS. Expression analysis of miR-221-3p and its target genes in horses. Genes Genomics 2019 Apr;41(4):459-465.
    doi: 10.1007/s13258-018-00778-3pubmed: 30604147google scholar: lookup
  4. Jafari H, Abebe BK, Cong L, Ahmed Z, Zhaofei W, Sun M, Muhatai G, Chuzhao L, Dang R. Review: Genomic insights into the adaptive traits and stress resistance in modern horses. Stress Biol 2026 Jan 12;6(1):5.
    doi: 10.1007/s44154-025-00274-1pubmed: 41521281google scholar: lookup
  5. Wilson EP, Broadaway KA, Parsons VA, Vadlamudi S, Narisu N, Brotman SM, Currin KW, Stringham HM, Erdos MR, Welch R, Holtzman JK, Lakka TA, Laakso M, Tuomilehto J, Boehnke M, Koistinen HA, Collins FS, Parker SCJ, Scott LJ, Mohlke KL. Skeletal muscle eQTL meta-analysis implicates genes in the genetic architecture of muscular and cardiometabolic traits. Am J Hum Genet 2025 Nov 6;112(11):2693-2707.
    doi: 10.1016/j.ajhg.2025.09.003pubmed: 40992379google scholar: lookup
  6. 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).
    doi: 10.3390/genes16040431pubmed: 40282391google scholar: lookup
  7. Herrera-Sánchez MP, Rodríguez-Hernández R, Rondón-Barragán IS. Comparative Transcriptome Analysis of Hens' Livers in Conventional Cage vs. Cage-Free Egg Production Systems. Vet Med Int 2025;2025:3041254.
    doi: 10.1155/vmi/3041254pubmed: 40160973google scholar: lookup
  8. Myćka G, Ropka-Molik K, Cywińska A, Stefaniuk-Szmukier M. Endurance Effort Affected Expression of Actinin 3 and Klotho Different Isoforms Basing on the Arabian Horses Model. Genes (Basel) 2024 Dec 18;15(12).
    doi: 10.3390/genes15121618pubmed: 39766885google scholar: lookup
Subscribe to our newsletter
Join 99,359 horse owners like you who receive our email updates on horse health and nutrition.