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Cells2022; 11(12); 1917; doi: 10.3390/cells11121917

Methylation Status of Gene Bodies of Selected microRNA Genes Associated with Neoplastic Transformation in Equine Sarcoids.

Abstract: Horses are of great importance in recreation, livestock production, as working animals in poorly developed countries, and for equine-assisted therapy. Equine sarcoids belong to the most commonly diagnosed tumors in this species. They may cause discomfort, pain, and can lead to the permanent impairment of motor function. The molecular bases of their formation are still under investigation. Our previous studies revealed altered microRNA (miRNA) expression and DNA methylation levels in sarcoid tumors. Abnormal patterns of methylation may be responsible for changes in gene expression levels, including microRNAs. Recently, the DNA methylation of gene bodies has also been shown to have an impact on gene expression. Thus, the aim of the study was to investigate the methylation pattern of gene bodies of chosen miRNAs identified in sarcoid tissue (miR-101, miR-10b, miR-200a, and miR-338-3p), which have also been established to play roles in neoplastic transformation. To this end, we applied qRT-PCR, Bisulfite Sequencing PCR (BSP), and Mquant methods. As a result, we identified the statistically significant downregulation of pri-mir-101-1, pri-mir-10b, and pri-mir-200a in the sarcoid samples in comparison to the control. The DNA methylation analysis revealed their hypermethylation. This suggests that DNA methylation may be one mechanism responsible for the downregulation of theses miRNAs. However, the identified differences in the methylation levels are not very high, which implies that other mechanisms may also underlie the downregulation of the expression of these miRNAs in equine sarcoids. For the first time, the results obtained shed light on microRNA expression regulation by gene body methylation in equine sarcoids and provide bases for further deeper studies on other mechanisms influencing the miRNA repertoire.
Publication Date: 2022-06-14 PubMed ID: 35741046PubMed Central: PMC9221590DOI: 10.3390/cells11121917Google Scholar: Lookup
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  • 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 explores the impact of DNA methylation on the gene expressions of selected microRNAs in equine sarcoids, common tumors in horses. It suggests that DNA methylation might be one mechanism responsible for reducing microRNA expressions, but other factors might be at play given the slight differences in methylation levels.

Introduction to Equine Sarcoids and DNA Methylation

  • The research’s focus is equine sarcoids, a prevalent type of tumours in horses. These tumors can cause discomfort, pain, and impair motor functions permanently.
  • Despite their prevalence, the molecular basis for the development of these tumors is not fully understood, prompting the need for further research.
  • DNA methylation is one of the mechanisms investigated in this study. DNA methylation refers to a process wherein a methyl group is added to DNA molecules, influencing their functions, notably gene expression. The impact of DNA methylation on gene bodies has recently been discovered to affect gene expression as well.

Study Aim

  • The study aims to understand the patterns of methylation in certain microRNAs (miRNAs)— specifically miR-101, miR-10b, miR-200a, and miR-338-3p— identified in sarcoid tissues. miRNAs are small non-coding RNA molecules that play essential roles in gene expression regulation.
  • These chosen miRNAs are believed to have a significant role in neoplastic transformation— a process where normal cells are transformed into cancerous or tumorous cells.

Methodology

  • The researchers used qRT-PCR, Bisulfite Sequencing PCR (BSP), and Mquant methods to investigate the methylation pattern of the selected miRNAs.

Findings

  • The results showed a significant decrease in the level of pri-mir-101-1, pri-mir-10b, and pri-mir-200a in the sarcoid samples when compared to the controls.
  • DNA methylation analysis revealed an increase in methylation in these microRNAs. This suggests that DNA methylation might be linked to a reduction in these microRNAs’ expression.
  • However, the differences in methylation levels were not significantly high, suggesting other mechanisms could also influence the downregulation of these miRNAs.

Conclusion & Future Direction

  • The study indicates that DNA methylation could be one possible mechanism regulating the expression of microRNA in equine sarcoids. However, the relatively small differences in methylation call for further investigation into other potential underlying mechanisms.
  • This research is a step towards understanding the molecular basis of equine sarcoid formation and may guide future studies on the different mechanisms influencing the microRNA repertoire.

Cite This Article

APA
Pawlina-Tyszko K, Semik-Gurgul E, Ząbek T, Witkowski M. (2022). Methylation Status of Gene Bodies of Selected microRNA Genes Associated with Neoplastic Transformation in Equine Sarcoids. Cells, 11(12), 1917. https://doi.org/10.3390/cells11121917

Publication

ISSN: 2073-4409
NlmUniqueID: 101600052
Country: Switzerland
Language: English
Volume: 11
Issue: 12
PII: 1917

Researcher Affiliations

Pawlina-Tyszko, Klaudia
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Krakowska 1 St., 32-083 Balice, Poland.
Semik-Gurgul, Ewelina
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Krakowska 1 St., 32-083 Balice, Poland.
Ząbek, Tomasz
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Krakowska 1 St., 32-083 Balice, Poland.
Witkowski, Maciej
  • Institute of Veterinary Medicine, University Centre of Veterinary Medicine JU-AU, Al. Mickiewicza 24/28, 30-059 Cracow, Poland.
  • Horse Clinic Służewiec, Puławska 266 St., 02-684 Warsaw, Poland.

MeSH Terms

  • Animals
  • Cell Transformation, Neoplastic / genetics
  • DNA Methylation / genetics
  • Down-Regulation
  • Gene Expression Regulation, Neoplastic
  • Horses / genetics
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / veterinary

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 52 references
  1. Jackson C. The incidence and pathology of tumours of domesticated animals in South Africa.. Onderstepoort J. Vet. Sci. Anim. Ind. 1936;6:378–385.
  2. Bogaert L, Martens A, Depoorter P, Gasthuys F. Equine sarcoids-Part 1: Clinical presentation and epidemiology.. Vlaams Diergeneeskd. Tijdschr. 2008;77:2–9.
  3. Ogłuszka M, Starzyński RR, Pierzchała M, Otrocka-Domagała I, Raś A. Equine Sarcoids-Causes, Molecular Changes, and Clinicopathologic Features: A Review.. Vet Pathol 2021 May;58(3):472-482.
    doi: 10.1177/0300985820985114pubmed: 33461443google scholar: lookup
  4. Broström H. Equine sarcoids. A clinical and epidemiological study in relation to equine leucocyte antigens (ELA).. Acta Vet Scand 1995;36(2):223-36.
    doi: 10.1186/BF03547691pmc: PMC8095413pubmed: 7484549google scholar: lookup
  5. Chambers G, Ellsmore VA, O'Brien PM, Reid SWJ, Love S, Campo MS, Nasir L. Association of bovine papillomavirus with the equine sarcoid.. J Gen Virol 2003 May;84(Pt 5):1055-1062.
    doi: 10.1099/vir.0.18947-0pubmed: 12692268google scholar: lookup
  6. Semik-Gurgul E. Molecular approaches to equine sarcoids.. Equine Vet J 2021 Mar;53(2):221-230.
    doi: 10.1111/evj.13322pubmed: 32654178google scholar: lookup
  7. Knottenbelt DC. The Equine Sarcoid: Why Are There so Many Treatment Options?. Vet Clin North Am Equine Pract 2019 Aug;35(2):243-262.
    doi: 10.1016/j.cveq.2019.03.006pubmed: 31097356google scholar: lookup
  8. Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS. Post-transcriptional gene silencing by siRNAs and miRNAs.. Curr Opin Struct Biol 2005 Jun;15(3):331-41.
    doi: 10.1016/j.sbi.2005.05.006pubmed: 15925505google scholar: lookup
  9. Meister G, Tuschl T. Mechanisms of gene silencing by double-stranded RNA.. Nature 2004 Sep 16;431(7006):343-9.
    doi: 10.1038/nature02873pubmed: 15372041google scholar: lookup
  10. Elson-Schwab I, Lorentzen A, Marshall CJ. MicroRNA-200 family members differentially regulate morphological plasticity and mode of melanoma cell invasion.. PLoS One 2010 Oct 4;5(10).
  11. Muralidhar GG, Barbolina MV. The miR-200 Family: Versatile Players in Epithelial Ovarian Cancer.. Int J Mol Sci 2015 Jul 24;16(8):16833-47.
    doi: 10.3390/ijms160816833pmc: PMC4581173pubmed: 26213923google scholar: lookup
  12. Pedroza-Torres A, López-Urrutia E, García-Castillo V, Jacobo-Herrera N, Herrera LA, Peralta-Zaragoza O, López-Camarillo C, De Leon DC, Fernández-Retana J, Cerna-Cortés JF, Pérez-Plasencia C. MicroRNAs in cervical cancer: evidences for a miRNA profile deregulated by HPV and its impact on radio-resistance.. Molecules 2014 May 16;19(5):6263-81.
    doi: 10.3390/molecules19056263pmc: PMC6271743pubmed: 24840898google scholar: lookup
  13. Pawlina K, Gurgul A, Szmatoła T, Koch C, Mählmann K, Witkowski M, Bugno-Poniewierska M. Comprehensive characteristics of microRNA expression profile of equine sarcoids.. Biochimie 2017 Jun;137:20-28.
    doi: 10.1016/j.biochi.2017.02.017pubmed: 28259757google scholar: lookup
  14. Robertson KD, Jones PA. DNA methylation: past, present and future directions.. Carcinogenesis 2000 Mar;21(3):461-7.
    doi: 10.1093/carcin/21.3.461pubmed: 10688866google scholar: lookup
  15. Watson RE, Curtin GM, Doolittle DJ, Goodman JI. Progressive alterations in global and GC-rich DNA methylation during tumorigenesis.. Toxicol Sci 2003 Oct;75(2):289-99.
    doi: 10.1093/toxsci/kfg190pubmed: 12883089google scholar: lookup
  16. Arechederra M, Daian F, Yim A, Bazai SK, Richelme S, Dono R, Saurin AJ, Habermann BH, Maina F. Hypermethylation of gene body CpG islands predicts high dosage of functional oncogenes in liver cancer.. Nat Commun 2018 Aug 8;9(1):3164.
    doi: 10.1038/s41467-018-05550-5pmc: PMC6082886pubmed: 30089774google scholar: lookup
  17. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond.. Nat Rev Genet 2012 May 29;13(7):484-92.
    doi: 10.1038/nrg3230pubmed: 22641018google scholar: lookup
  18. Murtha M, Esteller M. Extraordinary Cancer Epigenomics: Thinking Outside the Classical Coding and Promoter Box.. Trends Cancer 2016 Oct;2(10):572-584.
    doi: 10.1016/j.trecan.2016.08.004pubmed: 28741488google scholar: lookup
  19. Suzuki H, Maruyama R, Yamamoto E, Kai M. Epigenetic alteration and microRNA dysregulation in cancer.. Front Genet 2013 Dec 3;4:258.
    doi: 10.3389/fgene.2013.00258pmc: PMC3847369pubmed: 24348513google scholar: lookup
  20. Semik E, Ząbek T, Gurgul A, Fornal A, Szmatoła T, Pawlina K, Wnuk M, Klukowska-Rötzler J, Koch C, Mählmann K, Bugno-Poniewierska M. Comparative analysis of DNA methylation patterns of equine sarcoid and healthy skin samples.. Vet Comp Oncol 2018 Mar;16(1):37-46.
    doi: 10.1111/vco.12308pubmed: 28220614google scholar: lookup
  21. Altamura G, Strazzullo M, Corteggio A, Francioso R, Roperto F, D'Esposito M, Borzacchiello G. O(6)-methylguanine-DNA methyltransferase in equine sarcoids: molecular and epigenetic analysis.. BMC Vet Res 2012 Nov 10;8:218.
    doi: 10.1186/1746-6148-8-218pmc: PMC3512464pubmed: 23140380google scholar: lookup
  22. Strazzullo M, Corteggio A, Altamura G, Francioso R, Roperto F, D'Esposito M, Borzacchiello G. Molecular and epigenetic analysis of the fragile histidine triad tumour suppressor gene in equine sarcoids.. BMC Vet Res 2012 Mar 16;8:30.
    doi: 10.1186/1746-6148-8-30pmc: PMC3361464pubmed: 22424615google scholar: lookup
  23. Semik-Gurgul E, Ząbek T, Fornal A, Wnuk M, Pawlina-Tyszko K, Gurgul A, Klukowska-Rötzler J, Koch C, Mählmann K, Bugno-Poniewierska M. DNA methylation patterns of the S100A14, POU2F3 and SFN genes in equine sarcoid tissues.. Res Vet Sci 2018 Aug;119:302-307.
    doi: 10.1016/j.rvsc.2018.07.006pubmed: 30086514google scholar: lookup
  24. Verma M, Srivastava S. Epigenetyka nowotworów: Implikacje dla wczesnego wykrywania i zapobiegania.. Lancet Oncol. 2003;2:121–131.
  25. Burri N, Shaw P, Bouzourene H, Sordat I, Sordat B, Gillet M, Schorderet D, Bosman FT, Chaubert P. Methylation silencing and mutations of the p14ARF and p16INK4a genes in colon cancer.. Lab Invest 2001 Feb;81(2):217-29.
    doi: 10.1038/labinvest.3780230pubmed: 11232644google scholar: lookup
  26. Costello JF, Frühwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, Wright FA, Feramisco JD, Peltomäki P, Lang JC, Schuller DE, Yu L, Bloomfield CD, Caligiuri MA, Yates A, Nishikawa R, Su Huang H, Petrelli NJ, Zhang X, O'Dorisio MS, Held WA, Cavenee WK, Plass C. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns.. Nat Genet 2000 Feb;24(2):132-8.
    doi: 10.1038/72785pubmed: 10655057google scholar: lookup
  27. Bogaert L, Van Poucke M, De Baere C, Dewulf J, Peelman L, Ducatelle R, Gasthuys F, Martens A. Bovine papillomavirus load and mRNA expression, cell proliferation and p53 expression in four clinical types of equine sarcoid.. J Gen Virol 2007 Aug;88(Pt 8):2155-2161.
    doi: 10.1099/vir.0.82876-0pubmed: 17622617google scholar: lookup
  28. 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
  29. Bogaert L, Van Poucke M, De Baere C, Peelman L, Gasthuys F, Martens A. Selection of a set of reliable reference genes for quantitative real-time PCR in normal equine skin and in equine sarcoids.. BMC Biotechnol 2006 Apr 27;6:24.
    doi: 10.1186/1472-6750-6-24pmc: PMC1484482pubmed: 16643647google scholar: lookup
  30. Andersen CL, Jensen JL, Ørntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets.. Cancer Res 2004 Aug 1;64(15):5245-50.
    doi: 10.1158/0008-5472.CAN-04-0496pubmed: 15289330google scholar: lookup
  31. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA. Primer3Plus, an enhanced web interface to Primer3.. Nucleic Acids Res 2007 Jul;35(Web Server issue):W71-4.
    doi: 10.1093/nar/gkm306pmc: PMC1933133pubmed: 17485472google scholar: lookup
  32. BLAST . Joseph Bedell, Ian Korf and Mark Yandell. OReilly & Associates; Sebastopol, CA, USA: 2003.
  33. Cunningham F, Allen JE, Allen J, Alvarez-Jarreta J, Amode MR, Armean IM, Austine-Orimoloye O, Azov AG, Barnes I, Bennett R, Berry A, Bhai J, Bignell A, Billis K, Boddu S, Brooks L, Charkhchi M, Cummins C, Da Rin Fioretto L, Davidson C, Dodiya K, Donaldson S, El Houdaigui B, El Naboulsi T, Fatima R, Giron CG, Genez T, Martinez JG, Guijarro-Clarke C, Gymer A, Hardy M, Hollis Z, Hourlier T, Hunt T, Juettemann T, Kaikala V, Kay M, Lavidas I, Le T, Lemos D, Marugán JC, Mohanan S, Mushtaq A, Naven M, Ogeh DN, Parker A, Parton A, Perry M, Piližota I, Prosovetskaia I, Sakthivel MP, Salam AIA, Schmitt BM, Schuilenburg H, Sheppard D, Pérez-Silva JG, Stark W, Steed E, Sutinen K, Sukumaran R, Sumathipala D, Suner MM, Szpak M, Thormann A, Tricomi FF, Urbina-Gómez D, Veidenberg A, Walsh TA, Walts B, Willhoft N, Winterbottom A, Wass E, Chakiachvili M, Flint B, Frankish A, Giorgetti S, Haggerty L, Hunt SE, IIsley GR, Loveland JE, Martin FJ, Moore B, Mudge JM, Muffato M, Perry E, Ruffier M, Tate J, Thybert D, Trevanion SJ, Dyer S, Harrison PW, Howe KL, Yates AD, Zerbino DR, Flicek P. Ensembl 2022.. Nucleic Acids Res 2022 Jan 7;50(D1):D988-D995.
    doi: 10.1093/nar/gkab1049pmc: PMC8728283pubmed: 34791404google scholar: lookup
  34. Leakey TI, Zielinski J, Siegfried RN, Siegel ER, Fan CY, Cooney CA. A simple algorithm for quantifying DNA methylation levels on multiple independent CpG sites in bisulfite genomic sequencing electropherograms.. Nucleic Acids Res 2008 Jun;36(11):e64.
    doi: 10.1093/nar/gkn210pmc: PMC2441810pubmed: 18480118google scholar: lookup
  35. R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2020.
  36. Mallona I, Díez-Villanueva A, Peinado MA. Methylation plotter: a web tool for dynamic visualization of DNA methylation data.. Source Code Biol Med 2014;9:11.
    doi: 10.1186/1751-0473-9-11pmc: PMC4066318pubmed: 25260021google scholar: lookup
  37. Lund AH. miR-10 in development and cancer.. Cell Death Differ 2010 Feb;17(2):209-14.
    doi: 10.1038/cdd.2009.58pubmed: 19461655google scholar: lookup
  38. Moghbeli M. Molecular interactions of miR-338 during tumor progression and metastasis.. Cell Mol Biol Lett 2021 Apr 7;26(1):13.
    doi: 10.1186/s11658-021-00257-wpmc: PMC8028791pubmed: 33827418google scholar: lookup
  39. Wang CZ, Deng F, Li H, Wang DD, Zhang W, Ding L, Tang JH. MiR-101: a potential therapeutic target of cancers.. Am J Transl Res 2018;10(11):3310-3321.
    pmc: PMC6291716pubmed: 30662588
  40. Ehrlich M. DNA methylation in cancer: too much, but also too little.. Oncogene 2002 Aug 12;21(35):5400-13.
    doi: 10.1038/sj.onc.1205651pubmed: 12154403google scholar: lookup
  41. Kim K, Lee HC, Park JL, Kim M, Kim SY, Noh SM, Song KS, Kim JC, Kim YS. Epigenetic regulation of microRNA-10b and targeting of oncogenic MAPRE1 in gastric cancer.. Epigenetics 2011 Jun;6(6):740-51.
    doi: 10.4161/epi.6.6.15874pubmed: 21562367google scholar: lookup
  42. Yu M, Xu Y, Pan L, Feng Y, Luo K, Mu Q, Luo G. miR-10b Downregulated by DNA Methylation Acts as a Tumor Suppressor in HPV-Positive Cervical Cancer via Targeting Tiam1.. Cell Physiol Biochem 2018;51(4):1763-1777.
    doi: 10.1159/000495680pubmed: 30504727google scholar: lookup
  43. Sheedy P, Medarova Z. The fundamental role of miR-10b in metastatic cancer.. Am J Cancer Res 2018;8(9):1674-1688.
    pmc: PMC6176190pubmed: 30323962
  44. Gan L, Denecke B. Profiling Pre-MicroRNA and Mature MicroRNA Expressions Using a Single Microarray and Avoiding Separate Sample Preparation.. Microarrays (Basel) 2013 Mar 14;2(1):24-33.
    doi: 10.3390/microarrays2010024pmc: PMC5003435pubmed: 27605179google scholar: lookup
  45. Jazdzewski K, Murray EL, Franssila K, Jarzab B, Schoenberg DR, de la Chapelle A. Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma.. Proc Natl Acad Sci U S A 2008 May 20;105(20):7269-74.
    doi: 10.1073/pnas.0802682105pmc: PMC2438239pubmed: 18474871google scholar: lookup
  46. Pawlina-Tyszko K, Semik-Gurgul E, Gurgul A, Oczkowicz M, Szmatoła T, Bugno-Poniewierska M. Application of the targeted sequencing approach reveals the single nucleotide polymorphism (SNP) repertoire in microRNA genes in the pig genome.. Sci Rep 2021 May 10;11(1):9848.
    doi: 10.1038/s41598-021-89363-5pmc: PMC8110958pubmed: 33972633google scholar: lookup
  47. Davalos V, Moutinho C, Villanueva A, Boque R, Silva P, Carneiro F, Esteller M. Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis.. Oncogene 2012 Apr 19;31(16):2062-74.
    doi: 10.1038/onc.2011.383pmc: PMC3330264pubmed: 21874049google scholar: lookup
  48. Ceppi P, Mudduluru G, Kumarswamy R, Rapa I, Scagliotti GV, Papotti M, Allgayer H. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer.. Mol Cancer Res 2010 Sep;8(9):1207-16.
    doi: 10.1158/1541-7786.MCR-10-0052pubmed: 20696752google scholar: lookup
  49. Suzuki H, Maruyama R, Yamamoto E, Kai M. DNA methylation and microRNA dysregulation in cancer.. Mol Oncol 2012 Dec;6(6):567-78.
  50. Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B, Laxman B, Cao X, Jing X, Ramnarayanan K, Brenner JC, Yu J, Kim JH, Han B, Tan P, Kumar-Sinha C, Lonigro RJ, Palanisamy N, Maher CA, Chinnaiyan AM. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer.. Science 2008 Dec 12;322(5908):1695-9.
    doi: 10.1126/science.1165395pmc: PMC2684823pubmed: 19008416google scholar: lookup
  51. Wei X, Xiang T, Ren G, Tan C, Liu R, Xu X, Wu Z. miR-101 is down-regulated by the hepatitis B virus x protein and induces aberrant DNA methylation by targeting DNA methyltransferase 3A.. Cell Signal 2013 Feb;25(2):439-46.
    doi: 10.1016/j.cellsig.2012.10.013pubmed: 23124077google scholar: lookup
  52. Huang D, Wang X, Zhuang C, Shi W, Liu M, Tu Q, Zhang D, Hu L. Reciprocal negative feedback loop between EZH2 and miR-101-1 contributes to miR-101 deregulation in hepatocellular carcinoma.. Oncol Rep 2016 Feb;35(2):1083-90.
    doi: 10.3892/or.2015.4467pubmed: 26718325google scholar: lookup

Citations

This article has been cited 1 times.
  1. Semik-Gurgul E, Gurgul A, Szmatoła T. Transcriptome and methylome sequencing reveals altered long non-coding RNA genes expression and their aberrant DNA methylation in equine sarcoids. Funct Integr Genomics 2023 Aug 8;23(3):268.
    doi: 10.1007/s10142-023-01200-2pubmed: 37552338google scholar: lookup