Analyze Diet
Journal of veterinary internal medicine2021; 35(1); 610-619; doi: 10.1111/jvim.16027

Diagnostic potential of three serum microRNAs as biomarkers for equine sarcoid disease in horses and donkeys.

Abstract: MicroRNAs (miRNAs) are potential biomarkers for equine sarcoids (ES). Objective: To assess eca-miR-331, eca-miR-100, and eca-miR-1 as serum biomarkers for ES disease. Methods: Sixty-eight ES cases (56 horses, 12 donkeys), 69 tumor-free controls (60 horses, 9 donkeys), and 20 horses with other skin tumors. Methods: For this case-control study, expression of serum eca-miR-331, eca-miR-100, and eca-miR-1 in ES-affected equids was compared to tumor-free age-, sex-, and breed-matched control horses and donkeys with other skin tumors using reverse transcription quantitative PCR (polymerase chain reaction) for relative miRNA quantification. Biological, preanalytical, and clinical variable influences on miRNA expression were examined. Receiver operator characteristic (ROC) curve analyses were used to determine differences in miRNA expression between groups. Results: The expression of eca-miR-100 was affected by age (P = .003) and expression of eca-miR-100 and eca-miR-1 were affected by hemolysis (both P < .001). Eca-miR-331 was unaffected by biological variation, hemolysis, ES type, and disease severity. Eca-miR-331 concentrations were higher in ES-affected compared to tumor-free controls (P = .002). The ROC curve analysis indicated an area under the curve of 0.65 (P = .002) with a sensitivity of 60%, specificity of 71%, and positive and negative likelihood ratios of 2.1 and 0.56, respectively, to diagnose ES. Eca-miR-331 expression did not discriminate between horses with ES and other skin tumors. Expression of eca-miR-100 and eca-miR-1 was not different between groups. Conclusions: Serum eca-miR-331 expression is neither sensitive nor specific enough as a single ES biomarker. If combined with other miRNAs, it may be helpful for ES diagnosis.
Publication Date: 2021-01-07 PubMed ID: 33415768PubMed Central: PMC7848377DOI: 10.1111/jvim.16027Google 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

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 project examined the potential of three specific microRNAs to serve as indicators of equine sarcoid (ES) disease in horses and donkeys. The researchers found that while one of these microRNAs showed increased presence in ES-affected animals, it wasn’t distinct enough to serve as a reliable standalone biomarker for the disease.

Objective and Methodology

  • The research sought to investigate the potential of three specific microRNAs, specifically eca-miR-331, eca-miR-100, and eca-miR-1, as biomarkers for ES disease.
  • A case-control study was conducted involving 68 ES cases (56 horses and 12 donkeys), 69 tumor-free controls (60 horses, 9 donkeys), and 20 horses with other types of skin tumors.
  • The study used reverse transcription quantitative PCR (polymerase chain reaction) for relative microRNA quantification, comparing microRNA expression in ES-affected equids with that in tumor-free controls and donkeys with other skin tumors.
  • The research also examined the influence of biological, preanalytical, and clinical variables on microRNA expression.

Results

  • The expression of eca-miR-100 was found to be affected by age and hemolysis, while both eca-miR-100 and eca-miR-1 were influenced by hemolysis.
  • Concentration of eca-miR-331 was higher in ES-affected equids compared to tumor-free controls.
  • The area under the receiver operator characteristic (ROC) curve for eca-miR-331 was 0.65, with 60% sensitivity and 71% specificity in diagnosing ES. This indicates that it is only moderately effective as a standalone biomarker.
  • The measurement of eca-miR-331’s expression did not distinguish between horses with ES and those with other skin tumors.
  • No significant differences were found in the expression of eca-miR-100 and eca-miR-1 between ES-affected equids and controls or between ES-affected equids and those with other skin tumors.

Conclusions

  • The research concluded that the expression of serum eca-miR-331 alone isn’t sensitive or specific enough to reliably diagnose ES.
  • However, if it is combined with the analysis of other microRNAs, it may assist in diagnosing ES.

Cite This Article

APA
Unger L, Abril C, Gerber V, Jagannathan V, Koch C, Hamza E. (2021). Diagnostic potential of three serum microRNAs as biomarkers for equine sarcoid disease in horses and donkeys. J Vet Intern Med, 35(1), 610-619. https://doi.org/10.1111/jvim.16027

Publication

ISSN: 1939-1676
NlmUniqueID: 8708660
Country: United States
Language: English
Volume: 35
Issue: 1
Pages: 610-619

Researcher Affiliations

Unger, Lucia
  • Department of Clinical Veterinary Medicine, Swiss Institute of Equine Medicine (ISME), Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Switzerland.
Abril, Carlos
  • Institute of Virology and Immunology, University of Bern, Bern, Switzerland.
Gerber, Vinzenz
  • Department of Clinical Veterinary Medicine, Swiss Institute of Equine Medicine (ISME), Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Switzerland.
Jagannathan, Vidhya
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Koch, Christoph
  • Department of Clinical Veterinary Medicine, Swiss Institute of Equine Medicine (ISME), Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Switzerland.
Hamza, Eman
  • Department of Clinical Veterinary Medicine, Swiss Institute of Equine Medicine (ISME), Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Switzerland.

MeSH Terms

  • Animals
  • Biomarkers
  • Biomarkers, Tumor
  • Case-Control Studies
  • Equidae
  • Horse Diseases / diagnosis
  • Horses
  • MicroRNAs / genetics
  • ROC Curve

Grant Funding

  • Swiss Institute of Equine Medicine Research funds

Conflict of Interest Statement

Authors declare no conflict of interest.

References

This article includes 76 references
  1. Knowles EJ, Tremaine WH, Pearson GR, Mair TS. A database survey of equine tumours in the United Kingdom.. Equine Vet J 2016 May;48(3):280-4.
    pubmed: 25594351doi: 10.1111/evj.12421google scholar: lookup
  2. Davis CR, Valentine BA, Gordon E, McDonough SP, Schaffer PA, Allen AL, Pesavento P. Neoplasia in 125 donkeys (Equus asinus): literature review and a survey of five veterinary schools in the United States and Canada.. J Vet Diagn Invest 2016 Nov;28(6):662-670.
    pubmed: 27698162doi: 10.1177/1040638716665659google scholar: lookup
  3. 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.
    pubmed: 12692268doi: 10.1099/vir.0.18947-0google scholar: lookup
  4. Yuan Z, Gault EA, Campo MS, Nasir L. Different contribution of bovine papillomavirus type 1 oncoproteins to the transformation of equine fibroblasts.. J Gen Virol 2011 Apr;92(Pt 4):773-83.
    pubmed: 21177927doi: 10.1099/vir.0.028191-0google scholar: lookup
  5. Martens A, De Moor A, Demeulemeester J, Ducatelle R. Histopathological characteristics of five clinical types of equine sarcoid.. Res Vet Sci 2000 Dec;69(3):295-300.
    pubmed: 11124103doi: 10.1053/rvsc.2000.0432google scholar: lookup
  6. Knottenbelt DC, Kelly DF. The diagnosis and treatment of periorbital sarcoid in the horse: 445 cases from 1974 to 1999.. Vet Ophthalmol 2000;3(2-3):169-191.
  7. Epperson ED, Castleman WL. Bovine Papillomavirus DNA and S100 Profiles in Sarcoids and Other Cutaneous Spindle Cell Tumors in Horses.. Vet Pathol 2017 Jan;54(1):44-52.
    pubmed: 27312364doi: 10.1177/0300985816653169google scholar: lookup
  8. Koch C, Martens A, Hainisch EK, Schüpbach G, Gerber V, Haspeslagh M. The clinical diagnosis of equine sarcoids - Part 1: Assessment of sensitivity and specificity using a multicentre case-based online examination.. Vet J 2018 Dec;242:77-82.
    pubmed: 30195623doi: 10.1016/j.tvjl.2018.08.009google scholar: lookup
  9. Haspeslagh M, Gerber V, Knottenbelt DC, Schüpbach G, Martens A, Koch C. The clinical diagnosis of equine sarcoids-Part 2: Assessment of case features typical of equine sarcoids and validation of a diagnostic protocol to guide equine clinicians in the diagnosis of equine sarcoids.. Vet J 2018 Oct;240:14-18.
    pubmed: 30268326doi: 10.1016/j.tvjl.2018.08.010google scholar: lookup
  10. Martens A, De Moor A, Ducatelle R. PCR detection of bovine papilloma virus DNA in superficial swabs and scrapings from equine sarcoids.. Vet J 2001 May;161(3):280-6.
    pubmed: 11352485doi: 10.1053/tvjl.2000.0524google scholar: lookup
  11. Bogaert L, Martens A, Van Poucke M, Ducatelle R, De Cock H, Dewulf J, De Baere C, Peelman L, Gasthuys F. High prevalence of bovine papillomaviral DNA in the normal skin of equine sarcoid-affected and healthy horses.. Vet Microbiol 2008 May 25;129(1-2):58-68.
    pubmed: 18093754doi: 10.1016/j.vetmic.2007.11.008google scholar: lookup
  12. Li L, Xiao B, Tong H, Xie F, Zhang Z, Xiao GG. Regulation of breast cancer tumorigenesis and metastasis by miRNAs.. Expert Rev Proteomics 2012 Dec;9(6):615-25.
    pubmed: 23256672doi: 10.1586/epr.12.64google scholar: lookup
  13. Yin Y, Song M, Gu B, Qi X, Hu Y, Feng Y, Liu H, Zhou L, Bian Z, Zhang J, Zuo X, Huang Z. Systematic analysis of key miRNAs and related signaling pathways in colorectal tumorigenesis.. Gene 2016 Mar 10;578(2):177-84.
    pubmed: 26692142doi: 10.1016/j.gene.2015.12.015google scholar: lookup
  14. Matsuyama H, Suzuki HI. Systems and Synthetic microRNA Biology: From Biogenesis to Disease Pathogenesis.. Int J Mol Sci 2019 Dec 24;21(1).
    pmc: PMC6981965pubmed: 31878193doi: 10.3390/ijms21010132google scholar: lookup
  15. Turchinovich A, Samatov TR, Tonevitsky AG, Burwinkel B. Circulating miRNAs: cell-cell communication function?. Front Genet 2013;4:119.
    pmc: PMC3695387pubmed: 23825476doi: 10.3389/fgene.2013.00119google scholar: lookup
  16. Pardini B, Sabo AA, Birolo G, Calin GA. Noncoding RNAs in Extracellular Fluids as Cancer Biomarkers: The New Frontier of Liquid Biopsies.. Cancers (Basel) 2019 Aug 14;11(8).
    pmc: PMC6721601pubmed: 31416190doi: 10.3390/cancers11081170google scholar: lookup
  17. 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.
    pubmed: 28259757doi: 10.1016/j.biochi.2017.02.017google scholar: lookup
  18. Bogedale K, Jagannathan V, Gerber V, Unger L. Differentially expressed microRNAs, including a large microRNA cluster on chromosome 24, are associated with equine sarcoid and squamous cell carcinoma.. Vet Comp Oncol 2019 Jun;17(2):155-164.
    pubmed: 30684296doi: 10.1111/vco.12458google scholar: lookup
  19. Terron-Canedo N, Weir W, Nicolson L, Britton C, Nasir L. Differential expression of microRNAs in bovine papillomavirus type 1 transformed equine cells.. Vet Comp Oncol 2017 Sep;15(3):764-774.
    pubmed: 27039895doi: 10.1111/vco.12216google scholar: lookup
  20. Unger L, Jagannathan V, Pacholewska A, Leeb T, Gerber V. Differences in miRNA differential expression in whole blood between horses with sarcoid regression and progression.. J Vet Intern Med 2019 Jan;33(1):241-250.
    pmc: PMC6335546pubmed: 30506726doi: 10.1111/jvim.15375google scholar: lookup
  21. Unger L, Gerber V, Pacholewska A, Leeb T, Jagannathan V. MicroRNA fingerprints in serum and whole blood of sarcoid-affected horses as potential non-invasive diagnostic biomarkers.. Vet Comp Oncol 2019 Mar;17(1):107-117.
    pubmed: 30430738doi: 10.1111/vco.12451google scholar: lookup
  22. Mählmann K, Hamza E, Marti E, Dolf G, Klukowska J, Gerber V, Koch C. Increased FOXP3 expression in tumour-associated tissues of horses affected with equine sarcoid disease.. Vet J 2014 Dec;202(3):516-21.
    pubmed: 25266649doi: 10.1016/j.tvjl.2014.09.003google scholar: lookup
  23. Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration.. Ann Intern Med 2007 Oct 16;147(8):W163-94.
  24. Angelos J, Oppenheim Y, Rebhun W, Mohammed H, Antczak DF. Evaluation of breed as a risk factor for sarcoid and uveitis in horses.. Anim Genet 1988;19(4):417-25.
  25. Mair TS, Walmsley JP, Phillips TJ. Surgical treatment of 45 horses affected by squamous cell carcinoma of the penis and prepuce.. Equine Vet J 2000 Sep;32(5):406-10.
    pubmed: 11037262doi: 10.2746/042516400777591093google scholar: lookup
  26. van den Top JG, de Heer N, Klein WR, Ensink JM. Penile and preputial tumours in the horse: a retrospective study of 114 affected horses.. Equine Vet J 2008 Sep;40(6):528-32.
    pubmed: 18487101doi: 10.2746/042516408x281180google scholar: lookup
  27. Wobeser BK, Davies JL, Hill JE, Jackson ML, Kidney BA, Mayer MN, Townsend HG, Allen AL. Epidemiology of equine sarcoids in horses in western Canada.. Can Vet J 2010 Oct;51(10):1103-8.
    pmc: PMC2942047pubmed: 21197201
  28. Martens A, De Moor A, Vlaminck L, Pille F, Steenhaut M. Evaluation of excision, cryosurgery and local BCG vaccination for the treatment of equine sarcoids.. Vet Rec 2001 Dec 1;149(22):665-9.
    pubmed: 11765322doi: 10.1136/vr.149.22.665google scholar: lookup
  29. Tamzali Y, Borde L, Rols MP, Golzio M, Lyazrhi F, Teissie J. Successful treatment of equine sarcoids with cisplatin electrochemotherapy: a retrospective study of 48 cases.. Equine Vet J 2012 Mar;44(2):214-20.
  30. Fleury C, Bérard F, Leblond A, Faure C, Ganem N, Thomas L. The study of cutaneous melanomas in Camargue-type gray-skinned horses (2): epidemiological survey.. Pigment Cell Res 2000 Feb;13(1):47-51.
  31. Unger L, Fouché N, Leeb T, Gerber V, Pacholewska A. Optimized methods for extracting circulating small RNAs from long-term stored equine samples.. Acta Vet Scand 2016 Jun 29;58(1):44.
    pmc: PMC4928274pubmed: 27356979doi: 10.1186/s13028-016-0224-5google scholar: lookup
  32. Lee S, Hwang S, Yu HJ, Oh D, Choi YJ, Kim MC, Kim Y, Ryu DY. Expression of microRNAs in Horse Plasma and Their Characteristic Nucleotide Composition.. PLoS One 2016;11(1):e0146374.
  33. Le Carré J, Lamon S, Léger B. Validation of a multiplex reverse transcription and pre-amplification method using TaqMan(®) MicroRNA assays.. Front Genet 2014;5:413.
    pmc: PMC4244598pubmed: 25505484doi: 10.3389/fgene.2014.00413google scholar: lookup
  34. Pfaffl MW. Relative quantification. In: Dorak T, ed. Real‐Time PCR. 1st ed. San Diego, California: International University Line; 2001:63‐82.
  35. Eusebi P. Diagnostic accuracy measures.. Cerebrovasc Dis 2013;36(4):267-72.
    pubmed: 24135733doi: 10.1159/000353863google scholar: lookup
  36. Kitchen RR, Kubista M, Tichopad A. Statistical aspects of quantitative real-time PCR experiment design.. Methods 2010 Apr;50(4):231-6.
    pubmed: 20109551doi: 10.1016/j.ymeth.2010.01.025google scholar: lookup
  37. Pacholewska A, Mach N, Mata X, Vaiman A, Schibler L, Barrey E, Gerber V. Novel equine tissue miRNAs and breed-related miRNA expressed in serum.. BMC Genomics 2016 Oct 26;17(1):831.
    pmc: PMC5080802pubmed: 27782799doi: 10.1186/s12864-016-3168-2google scholar: lookup
  38. Barrey E, Bonnamy B, Barrey EJ, Mata X, Chaffaux S, Guerin G. Muscular microRNA expressions in healthy and myopathic horses suffering from polysaccharide storage myopathy or recurrent exertional rhabdomyolysis.. Equine Vet J Suppl 2010 Nov;(38):303-10.
  39. Meder B, Backes C, Haas J, Leidinger P, Stähler C, Großmann T, Vogel B, Frese K, Giannitsis E, Katus HA, Meese E, Keller A. Influence of the confounding factors age and sex on microRNA profiles from peripheral blood.. Clin Chem 2014 Sep;60(9):1200-8.
    pubmed: 24987111doi: 10.1373/clinchem.2014.224238google scholar: lookup
  40. Ameling S, Kacprowski T, Chilukoti RK, Malsch C, Liebscher V, Suhre K, Pietzner M, Friedrich N, Homuth G, Hammer E, Völker U. Associations of circulating plasma microRNAs with age, body mass index and sex in a population-based study.. BMC Med Genomics 2015 Oct 14;8:61.
    pmc: PMC4604724pubmed: 26462558doi: 10.1186/s12920-015-0136-7google scholar: lookup
  41. Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies.. Cancer Prev Res (Phila) 2012 Mar;5(3):492-497.
  42. Kirschner MB, Kao SC, Edelman JJ, Armstrong NJ, Vallely MP, van Zandwijk N, Reid G. Haemolysis during sample preparation alters microRNA content of plasma.. PLoS One 2011;6(9):e24145.
  43. Blondal T, Jensby Nielsen S, Baker A, Andreasen D, Mouritzen P, Wrang Teilum M, Dahlsveen IK. Assessing sample and miRNA profile quality in serum and plasma or other biofluids.. Methods 2013 Jan;59(1):S1-6.
    pubmed: 23036329doi: 10.1016/j.ymeth.2012.09.015google scholar: lookup
  44. McGivney BA, Griffin ME, Gough KF, McGivney CL, Browne JA, Hill EW, Katz LM. Evaluation of microRNA expression in plasma and skeletal muscle of thoroughbred racehorses in training.. BMC Vet Res 2017 Nov 22;13(1):347.
    pmc: PMC5700565pubmed: 29166903doi: 10.1186/s12917-017-1277-zgoogle scholar: lookup
  45. Kirschner MB, Edelman JJ, Kao SC, Vallely MP, van Zandwijk N, Reid G. The Impact of Hemolysis on Cell-Free microRNA Biomarkers.. Front Genet 2013;4:94.
    pmc: PMC3663194pubmed: 23745127doi: 10.3389/fgene.2013.00094google scholar: lookup
  46. Krepelkova I, Mrackova T, Izakova J, Dvorakova B, Chalupova L, Mikulik R, Slaby O, Bartos M, Ruzicka V. Evaluation of miRNA detection methods for the analytical characteristic necessary for clinical utilization.. Biotechniques 2019 Jun;66(6):277-284.
    pubmed: 31124705doi: 10.2144/btn-2019-0021google scholar: lookup
  47. de Planell-Saguer M, Rodicio MC. Detection methods for microRNAs in clinic practice.. Clin Biochem 2013 Jul;46(10-11):869-78.
  48. Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M. A practical approach to RT-qPCR-Publishing data that conform to the MIQE guidelines.. Methods 2010 Apr;50(4):S1-5.
    pubmed: 20215014doi: 10.1016/j.ymeth.2010.01.005google scholar: lookup
  49. Ståhlberg A, Håkansson J, Xian X, Semb H, Kubista M. Properties of the reverse transcription reaction in mRNA quantification.. Clin Chem 2004 Mar;50(3):509-15.
    pubmed: 14726469doi: 10.1373/clinchem.2003.026161google scholar: lookup
  50. Kappel A, Backes C, Huang Y, Zafari S, Leidinger P, Meder B, Schwarz H, Gumbrecht W, Meese E, Staehler CF, Keller A. MicroRNA in vitro diagnostics using immunoassay analyzers.. Clin Chem 2015 Apr;61(4):600-7.
    pubmed: 25617425doi: 10.1373/clinchem.2014.232165google scholar: lookup
  51. Bachmann LM, Puhan MA, ter Riet G, Bossuyt PM. Sample sizes of studies on diagnostic accuracy: literature survey.. BMJ 2006 May 13;332(7550):1127-9.
    pmc: PMC1459608pubmed: 16627488doi: 10.1136/bmj.38793.637789.2fgoogle scholar: lookup
  52. Zhang J, Coombes KR. Sources of variation in false discovery rate estimation include sample size, correlation, and inherent differences between groups.. BMC Bioinformatics 2012;13 Suppl 13(Suppl 13):S1.
    pmc: PMC3426804pubmed: 23320794doi: 10.1186/1471-2105-13-s13-s1google scholar: lookup
  53. Ioannidis JP, Panagiotou OA. Comparison of effect sizes associated with biomarkers reported in highly cited individual articles and in subsequent meta-analyses.. JAMA 2011 Jun 1;305(21):2200-10.
    pubmed: 21632484doi: 10.1001/jama.2011.713google scholar: lookup
  54. Ammerlaan W, Betsou F. Intraindividual Temporal miRNA Variability in Serum, Plasma, and White Blood Cell Subpopulations.. Biopreserv Biobank 2016 Oct;14(5):390-397.
    pubmed: 27096687doi: 10.1089/bio.2015.0125google scholar: lookup
  55. Heegaard NH, Carlsen AL, Lilje B, Ng KL, Rønne ME, Jørgensen HL, Sennels H, Fahrenkrug J. Diurnal Variations of Human Circulating Cell-Free Micro-RNA.. PLoS One 2016;11(8):e0160577.
  56. Guo X, Guo L, Ji J, Zhang J, Zhang J, Chen X, Cai Q, Li J, Gu Q, Liu B, Zhu Z, Yu Y. miRNA-331-3p directly targets E2F1 and induces growth arrest in human gastric cancer.. Biochem Biophys Res Commun 2010 Jul 16;398(1):1-6.
    pubmed: 20510161doi: 10.1016/j.bbrc.2010.05.082google scholar: lookup
  57. Liu XH, Sun M, Nie FQ, Ge YB, Zhang EB, Yin DD, Kong R, Xia R, Lu KH, Li JH, De W, Wang KM, Wang ZX. Lnc RNA HOTAIR functions as a competing endogenous RNA to regulate HER2 expression by sponging miR-331-3p in gastric cancer.. Mol Cancer 2014 Apr 28;13:92.
    pmc: PMC4021402pubmed: 24775712doi: 10.1186/1476-4598-13-92google scholar: lookup
  58. Epis MR, Giles KM, Barker A, Kendrick TS, Leedman PJ. miR-331-3p regulates ERBB-2 expression and androgen receptor signaling in prostate cancer.. J Biol Chem 2009 Sep 11;284(37):24696-704.
    pmc: PMC2757173pubmed: 19584056doi: 10.1074/jbc.m109.030098google scholar: lookup
  59. Epis MR, Barker A, Giles KM, Beveridge DJ, Leedman PJ. The RNA-binding protein HuR opposes the repression of ERBB-2 gene expression by microRNA miR-331-3p in prostate cancer cells.. J Biol Chem 2011 Dec 2;286(48):41442-41454.
    pmc: PMC3308856pubmed: 21971048doi: 10.1074/jbc.m111.301481google scholar: lookup
  60. Feng DD, Zhang H, Zhang P, Zheng YS, Zhang XJ, Han BW, Luo XQ, Xu L, Zhou H, Qu LH, Chen YQ. Down-regulated miR-331-5p and miR-27a are associated with chemotherapy resistance and relapse in leukaemia.. J Cell Mol Med 2011 Oct;15(10):2164-75.
  61. Epis MR, Giles KM, Candy PA, Webster RJ, Leedman PJ. miR-331-3p regulates expression of neuropilin-2 in glioblastoma.. J Neurooncol 2014 Jan;116(1):67-75.
    pmc: PMC3889298pubmed: 24142150doi: 10.1007/s11060-013-1271-7google scholar: lookup
  62. Zhao D, Sui Y, Zheng X. MiR-331-3p inhibits proliferation and promotes apoptosis by targeting HER2 through the PI3K/Akt and ERK1/2 pathways in colorectal cancer.. Oncol Rep 2016 Feb;35(2):1075-82.
    pubmed: 26718987doi: 10.3892/or.2015.4450google scholar: lookup
  63. Chen L, Ma G, Cao X, An X, Liu X. MicroRNA-331 Inhibits Proliferation and Invasion of Melanoma Cells by Targeting Astrocyte-Elevated Gene-1.. Oncol Res 2018 Oct 17;26(9):1429-1437.
  64. Chen X, Luo H, Li X, Tian X, Peng B, Liu S, Zhan T, Wan Y, Chen W, Li Y, Lu Z, Huang X. miR-331-3p functions as an oncogene by targeting ST7L in pancreatic cancer.. Carcinogenesis 2018 Jul 30;39(8):1006-1015.
    pubmed: 29850766doi: 10.1093/carcin/bgy074google scholar: lookup
  65. Cao Y, Chen J, Wang D, Peng H, Tan X, Xiong D, Huang A, Tang H. Upregulated in Hepatitis B virus-associated hepatocellular carcinoma cells, miR-331-3p promotes proliferation of hepatocellular carcinoma cells by targeting ING5.. Oncotarget 2015 Nov 10;6(35):38093-106.
    pmc: PMC4741986pubmed: 26497554doi: 10.18632/oncotarget.5642google scholar: lookup
  66. Fujii T, Shimada K, Asano A, Tatsumi Y, Yamaguchi N, Yamazaki M, Konishi N. MicroRNA-331-3p Suppresses Cervical Cancer Cell Proliferation and E6/E7 Expression by Targeting NRP2.. Int J Mol Sci 2016 Aug 18;17(8).
    pmc: PMC5000747pubmed: 27548144doi: 10.3390/ijms17081351google scholar: lookup
  67. Chen L, Chu F, Cao Y, Shao J, Wang F. Serum miR-182 and miR-331-3p as diagnostic and prognostic markers in patients with hepatocellular carcinoma.. Tumour Biol 2015 Sep;36(10):7439-47.
    pubmed: 25903466doi: 10.1007/s13277-015-3430-2google scholar: lookup
  68. Sun Q, Li J, Jin B, Wang T, Gu J. Evaluation of miR-331-3p and miR-23b-3p as serum biomarkers for hepatitis c virus-related hepatocellular carcinoma at early stage.. Clin Res Hepatol Gastroenterol 2020 Feb;44(1):21-28.
    pubmed: 31053500doi: 10.1016/j.clinre.2019.03.011google scholar: lookup
  69. Gu J, Zhang J, Zheng L, Ajani JA, Wu X, Ye Y. Serum miR-331-3p predicts tumor recurrence in esophageal adenocarcinoma.. Sci Rep 2018 Sep 18;8(1):14006.
    pmc: PMC6143616pubmed: 30228315doi: 10.1038/s41598-018-32282-9google scholar: lookup
  70. McAnena P, Tanriverdi K, Curran C, Gilligan K, Freedman JE, Brown JAL, Kerin MJ. Circulating microRNAs miR-331 and miR-195 differentiate local luminal a from metastatic breast cancer.. BMC Cancer 2019 May 10;19(1):436.
    pmc: PMC6511137pubmed: 31077182doi: 10.1186/s12885-019-5636-ygoogle scholar: lookup
  71. Haider BA, Baras AS, McCall MN, Hertel JA, Cornish TC, Halushka MK. A critical evaluation of microRNA biomarkers in non-neoplastic disease.. PLoS One 2014;9(2):e89565.
  72. Backes C, Meese E, Keller A. Specific miRNA Disease Biomarkers in Blood, Serum and Plasma: Challenges and Prospects.. Mol Diagn Ther 2016 Dec;20(6):509-518.
    pubmed: 27378479doi: 10.1007/s40291-016-0221-4google scholar: lookup
  73. Weiland M, Gao XH, Zhou L, Mi QS. Small RNAs have a large impact: circulating microRNAs as biomarkers for human diseases.. RNA Biol 2012 Jun;9(6):850-9.
    pubmed: 22699556doi: 10.4161/rna.20378google scholar: lookup
  74. Grasedieck S, Schöler N, Bommer M, Niess JH, Tumani H, Rouhi A, Bloehdorn J, Liebisch P, Mertens D, Döhner H, Buske C, Langer C, Kuchenbauer F. Impact of serum storage conditions on microRNA stability.. Leukemia 2012 Nov;26(11):2414-6.
    pubmed: 22504138doi: 10.1038/leu.2012.106google scholar: lookup
  75. White SD. Donkey dermatology.. Vet Clin North Am Equine Pract 2013 Dec;29(3):703-8.
    pubmed: 24267685doi: 10.1016/j.cveq.2013.08.002google scholar: lookup
  76. Li SC, Chan WC, Hu LY, Lai CH, Hsu CN, Lin WC. Identification of homologous microRNAs in 56 animal genomes.. Genomics 2010 Jul;96(1):1-9.
    pubmed: 20347954doi: 10.1016/j.ygeno.2010.03.009google scholar: lookup

Citations

This article has been cited 6 times.
  1. Hamza E, Cosandey J, Gerber V, Koch C, Unger L. The potential of three whole blood microRNAs to predict outcome and monitor treatment response in sarcoid-bearing equids. Vet Res Commun 2023 Jan;47(1):87-98.
    doi: 10.1007/s11259-022-09930-7pubmed: 35484337google scholar: lookup
  2. Cosandey J, Hamza E, Gerber V, Ramseyer A, Leeb T, Jagannathan V, Blaszczyk K, Unger L. Diagnostic and prognostic potential of eight whole blood microRNAs for equine sarcoid disease. PLoS One 2021;16(12):e0261076.
    doi: 10.1371/journal.pone.0261076pubmed: 34941894google scholar: lookup
  3. Ibrahim S, Hedia M, Taqi MO, Derbala MK, Mahmoud KGM, Ahmed Y, Ismail S, El-Belely M. Alterations in the Expression Profile of Serum miR-155, miR-223, miR-17, miR-200a, miR-205, as well as Levels of Interleukin 6, and Prostaglandins during Endometritis in Arabian Mares. Vet Sci 2021 Jun 4;8(6).
    doi: 10.3390/vetsci8060098pubmed: 34199703google scholar: lookup
  4. Ostendarp C, Barton AK. Intraocular Tumors in Horses: Diagnosis, Tumor Classification, Oncologic Assessment and Therapy. Vet Sci 2025 Oct 17;12(10).
    doi: 10.3390/vetsci12101006pubmed: 41150147google scholar: lookup
  5. Beermann A, Hamza E, Reinhard S, Koch C, Oberhänsli T, Unger L. Selected microRNAs as biomarkers in sarcoid-affected horses under immunotherapy with a mistletoe extract. J Vet Diagn Invest 2026 Jan;38(1):33-40.
    doi: 10.1177/10406387251362820pubmed: 41039872google scholar: lookup
  6. Walters M, Skovgaard K, Heegaard PMH, Fang Y, Kharaz YA, Bundgaard L, Skovgaard LT, Jensen HE, Andersen PH, Peffers MJ, Jacobsen S. Identification and characterisation of temporal abundance of microRNAs in synovial fluid from an experimental equine model of osteoarthritis. Equine Vet J 2025 Jul;57(4):1138-1150.
    doi: 10.1111/evj.14456pubmed: 39775906google scholar: lookup