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Journal of veterinary internal medicine2018; 33(1); 241-250; doi: 10.1111/jvim.15375

Differences in miRNA differential expression in whole blood between horses with sarcoid regression and progression.

Abstract: Currently no methods are available to predict the clinical outcome of individual horses with equine sarcoid (ES) disease. Objective: To investigate if whole blood microRNA (miRNA) profiles can predict the long-term development of ES tumors. Methods: Five horses with regression and 5 with progression of ES lesions monitored over 5-7 years and 5 control horses free of ES for at least 5 years. Methods: For this cohort study, RNA extracted from whole blood samples from the regression, progression, and control groups was used for high throughput sequencing. Known and novel miRNAs were identified using miRDeep2 and differential expression analysis was carried out by the DESeq2 algorithm. Target gene and pathway prediction as well as enrichment and network analyses were conducted using TarBase, mirPath, and metaCore from GeneGo. Results: Fourteen miRNAs were differentially expressed between regression and progression groups after accounting for the control condition: 4 miRNAs (28.6%) were upregulated and 10 miRNAs (71.4%) were downregulated with >2-fold change. Seven of the 10 downregulated miRNAs are encoded in an miRNA cluster on equine chromosome 24, homologous to the well-known 14q32 cluster in humans. Their target genes show enrichment for pathways involved in viral carcinogenesis. Conclusions: Whole blood miRNA expression profiles are associated with long-term ES growth in horses and warrant further validation as prognostic biomarkers in a larger study cohort. Deregulation of miRNAs on equine chromosome 24 might represent a trigger for ES development.
© 2018 The Authors. Journal of Veterinary Internal Medicine published by Wiley Periodicals, Inc. on behalf of the American College of Veterinary Internal Medicine.
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Publication Date: 2018-12-02 PubMed ID: 30506726PubMed Central: PMC6335546DOI: 10.1111/jvim.15375Google Scholar: Lookup
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  • 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.

The researchers of this study investigated if profiles of a type of genetic material called miRNA found in the blood of horses could be used to predict the development of equine sarcoid (ES) tumors. They discovered differences in the expression of certain miRNAs between horses whose ES tumors were regressing or progressing, suggesting that these might be useful as prognostic biomarkers.

Study Objective and Methodology

  • The aim of the study was to determine if whole blood miRNA profiles could help predict the long-term development of equine sarcoid (ES) tumors, a condition currently without reliable predictive methods.
  • A cohort study was conducted on a group of fifteen horses. It consisted of horses with ES tumors either progressing or regressing over 5-7 years, and healthy control horses which had been free of ES for at least 5 years.
  • RNA, which includes miRNA, was extracted from blood samples of these horse groups and subjected to high throughput sequencing.
  • Identification of known and novel miRNAs was done using a data analysis software called miRDeep2. The DESeq2 algorithm was used to perform differential expression analysis.
  • Predictions were made for target genes and pathways using TarBase and mirPath. Network analyses were then conducted using metaCore from GeneGo for functional enrichment.

Research Findings

  • 14 miRNAs were found to be differentially expressed between the regression and progression horse groups. Of these, 4 miRNAs were upregulated and 10 miRNAs were downregulated by at least 2-fold.
  • Seven of the ten downregulated miRNAs are located in a cluster on equine chromosome 24, similar to a well-known miRNA cluster in humans on chromosome 14q32.
  • The target genes of these downregulated miRNAs are involved in pathways that play a role in causing cancer, particularly viral carcinogenesis.

Conclusions and Future Directions

  • The findings highlight potential of whole blood miRNA expression profiles as prognostic biomarkers for long-term ES growth in horses, however, further validation in a larger study cohort is needed.
  • The study also suggests that deregulation of miRNAs on chromosome 24 in horses might initiate ES development. Future studies could investigate this in more detail.

Cite This Article

APA
Unger L, Jagannathan V, Pacholewska A, Leeb T, Gerber V. (2018). Differences in miRNA differential expression in whole blood between horses with sarcoid regression and progression. J Vet Intern Med, 33(1), 241-250. https://doi.org/10.1111/jvim.15375

Publication

Journal of veterinary internal medicine
ISSN: 1939-1676
NlmUniqueID: 8708660
Country: United States
Language: English
Volume: 33
Issue: 1
Pages: 241-250

Researcher Affiliations

Unger, Lucia
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Jagannathan, Vidhya
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Pacholewska, Alicja
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Leeb, Tosso
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Gerber, Vinzenz
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, Bern, Switzerland.

MeSH Terms

  • Animals
  • Biomarkers, Tumor / blood
  • Disease Progression
  • Female
  • Horse Diseases / blood
  • Horse Diseases / pathology
  • Horses / blood
  • Horses / genetics
  • Male
  • MicroRNAs / blood
  • MicroRNAs / genetics
  • Sequence Analysis, RNA / veterinary
  • Skin Neoplasms / blood
  • Skin Neoplasms / pathology
  • Skin Neoplasms / veterinary

Grant Funding

  • ismequine.ch / Swiss Institute Research Funds
  • Swiss Institute of Equine Medicine
  • University of Bern
  • Swiss Institute of Equine Medicine
  • University of Bern

References

This article includes 67 references
  1. Schaffer PA, Wobeser B, Martin LE, Dennis MM, Duncan CG. Cutaneous neoplastic lesions of equids in the central United States and Canada: 3,351 biopsy specimens from 3,272 equids (2000-2010).. J Am Vet Med Assoc 2013 Jan 1;242(1):99-104.
    pubmed: 23234288doi: 10.2460/javma.242.1.99google scholar: lookup
  2. Valentine BA. Survey of equine cutaneous neoplasia in the Pacific Northwest.. J Vet Diagn Invest 2006 Jan;18(1):123-6.
    pubmed: 16566271doi: 10.1177/104063870601800121google scholar: lookup
  3. Lazary S, Marti E, Szalai G, Gaillard C, Gerber H. Studies on the frequency and associations of equine leucocyte antigens in sarcoid and summer dermatitis.. Anim Genet 1994 Jun;25 Suppl 1:75-80.
    pubmed: 7943987doi: 10.1111/j.1365-2052.1994.tb00406.xgoogle 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.
    pmc: PMC8095413pubmed: 7484549doi: 10.1186/bf03547691google scholar: lookup
  5. Broström H, Fahlbrink E, Dubath ML, Lazary S. Association between equine leucocyte antigens (ELA) and equine sarcoid tumors in the population of Swedish halfbreds and some of their families.. Vet Immunol Immunopathol 1988 Oct;19(3-4):215-23.
    pubmed: 3252614doi: 10.1016/0165-2427(88)90109-2google scholar: lookup
  6. Christen G, Gerber V, Dolf G, Burger D, Koch C. Inheritance of equine sarcoid disease in Franches-Montagnes horses.. Vet J 2014 Jan;199(1):68-71.
    pubmed: 24152383doi: 10.1016/j.tvjl.2013.09.053google scholar: lookup
  7. Staiger EA, Tseng CT, Miller D, Cassano JM, Nasir L, Garrick D, Brooks SA, Antczak DF. Host genetic influence on papillomavirus-induced tumors in the horse.. Int J Cancer 2016 Aug 15;139(4):784-92.
    pubmed: 27037728doi: 10.1002/ijc.30120google scholar: lookup
  8. Jandova V, Klukowska-Rötzler J, Dolf G, Janda J, Roosje P, Marti E, Koch C, Gerber V, Swinburne J. Whole genome scan identifies several chromosomal regions linked to equine sarcoids.. Schweiz Arch Tierheilkd 2012 Jan;154(1):19-25.
    pubmed: 22222899doi: 10.1024/0036-7281/a000288google scholar: lookup
  9. Berruex F, Gerber V, Wohlfender FD, Burger D, Koch C. Clinical course of sarcoids in 61 Franches-Montagnes horses over a 5-7 year period.. Vet Q 2016 Dec;36(4):189-196.
    pubmed: 27327513doi: 10.1080/01652176.2016.1204483google scholar: lookup
  10. Knottenbelt DC. A suggested clinical classification for the equine sarcoid.. Pferdeheilkunde 2006;22:479‐480.
  11. McConaghy FF, Davis RE, Reppas GP, Rawlinson R J, McClintock SA, Hutchins DR, Hodgson DR. Management of equine sarcoids: 1975-93.. N Z Vet J 1994 Oct;42(5):180-4.
    pubmed: 16031776doi: 10.1080/00480169.1994.35816google scholar: lookup
  12. Taylor S, Haldorson G. A review of equine sarcoid.. Equine Vet Educ 2013;25:210‐216.
  13. 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
  14. 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.
    pubmed: 17622617doi: 10.1099/vir.0.82876-0google scholar: lookup
  15. 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
  16. 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.
    pubmed: 28220614doi: 10.1111/vco.12308google scholar: lookup
  17. Croce CM. Causes and consequences of microRNA dysregulation in cancer.. Nat Rev Genet 2009 Oct;10(10):704-14.
    pmc: PMC3467096pubmed: 19763153doi: 10.1038/nrg2634google scholar: lookup
  18. Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review.. EMBO Mol Med 2012 Mar;4(3):143-59.
    pmc: PMC3376845pubmed: 22351564doi: 10.1002/emmm.201100209google 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. 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
  21. Gao G, Gay HA, Chernock RD, Zhang TR, Luo J, Thorstad WL, Lewis JS Jr, Wang X. A microRNA expression signature for the prognosis of oropharyngeal squamous cell carcinoma.. Cancer 2013 Jan 1;119(1):72-80.
    pmc: PMC3461127pubmed: 22736309doi: 10.1002/cncr.27696google scholar: lookup
  22. Wong N, Khwaja SS, Baker CM, Gay HA, Thorstad WL, Daly MD, Lewis JS Jr, Wang X. Prognostic microRNA signatures derived from The Cancer Genome Atlas for head and neck squamous cell carcinomas.. Cancer Med 2016 Jul;5(7):1619-28.
    pmc: PMC4944889pubmed: 27109697doi: 10.1002/cam4.718google scholar: lookup
  23. Hui AB, Lin A, Xu W, Waldron L, Perez-Ordonez B, Weinreb I, Shi W, Bruce J, Huang SH, O'Sullivan B, Waldron J, Gullane P, Irish JC, Chan K, Liu FF. Potentially prognostic miRNAs in HPV-associated oropharyngeal carcinoma.. Clin Cancer Res 2013 Apr 15;19(8):2154-62.
    pubmed: 23459718doi: 10.1158/1078-0432.ccr-12-3572google scholar: lookup
  24. Kok MGM, de Ronde MWJ, Moerland PD, Ruijter JM, Creemers EE, Pinto-Sietsma SJ. Small sample sizes in high-throughput miRNA screens: A common pitfall for the identification of miRNA biomarkers.. Biomol Detect Quantif 2018 May;15:1-5.
    pmc: PMC5737945pubmed: 29276692doi: 10.1016/j.bdq.2017.11.002google scholar: lookup
  25. 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
  26. Andrews S. FastQC: a quality control tool for high throughput sequence data.. 2010.
  27. Martin M. Cutadapt removes adapter sequences from high‐throughput sequencing reads.. EMBnet.journal 2011;17:10‐12.
  28. Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades.. Nucleic Acids Res 2012 Jan;40(1):37-52.
    pmc: PMC3245920pubmed: 21911355doi: 10.1093/nar/gkr688google scholar: lookup
  29. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.. Genome Biol 2009;10(3):R25.
    pmc: PMC2690996pubmed: 19261174doi: 10.1186/gb-2009-10-3-r25google scholar: lookup
  30. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature.. Nucleic Acids Res 2006 Jan 1;34(Database issue):D140-4.
    pmc: PMC1347474pubmed: 16381832doi: 10.1093/nar/gkj112google scholar: lookup
  31. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features.. Bioinformatics 2010 Mar 15;26(6):841-2.
    pmc: PMC2832824pubmed: 20110278doi: 10.1093/bioinformatics/btq033google scholar: lookup
  32. Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor.. Nat Protoc 2013 Sep;8(9):1765-86.
    pubmed: 23975260doi: 10.1038/nprot.2013.099google scholar: lookup
  33. Pantano L. DEGreport: Report of DEG analysis.. 2017.
  34. Tabas-Madrid D, Nogales-Cadenas R, Pascual-Montano A. GeneCodis3: a non-redundant and modular enrichment analysis tool for functional genomics.. Nucleic Acids Res 2012 Jul;40(Web Server issue):W478-83.
    pmc: PMC3394297pubmed: 22573175doi: 10.1093/nar/gks402google scholar: lookup
  35. Nogales-Cadenas R, Carmona-Saez P, Vazquez M, Vicente C, Yang X, Tirado F, Carazo JM, Pascual-Montano A. GeneCodis: interpreting gene lists through enrichment analysis and integration of diverse biological information.. Nucleic Acids Res 2009 Jul;37(Web Server issue):W317-22.
    pmc: PMC2703901pubmed: 19465387doi: 10.1093/nar/gkp416google scholar: lookup
  36. Carmona-Saez P, Chagoyen M, Tirado F, Carazo JM, Pascual-Montano A. GENECODIS: a web-based tool for finding significant concurrent annotations in gene lists.. Genome Biol 2007;8(1):R3.
    pmc: PMC1839127pubmed: 17204154doi: 10.1186/gb-2007-8-1-r3google scholar: lookup
  37. Vlachos IS, Paraskevopoulou MD, Karagkouni D, Georgakilas G, Vergoulis T, Kanellos I, Anastasopoulos IL, Maniou S, Karathanou K, Kalfakakou D, Fevgas A, Dalamagas T, Hatzigeorgiou AG. DIANA-TarBase v7.0: indexing more than half a million experimentally supported miRNA:mRNA interactions.. Nucleic Acids Res 2015 Jan;43(Database issue):D153-9.
    pmc: PMC4383989pubmed: 25416803doi: 10.1093/nar/gkሕgoogle scholar: lookup
  38. Vlachos IS, Zagganas K, Paraskevopoulou MD, Georgakilas G, Karagkouni D, Vergoulis T, Dalamagas T, Hatzigeorgiou AG. DIANA-miRPath v3.0: deciphering microRNA function with experimental support.. Nucleic Acids Res 2015 Jul 1;43(W1):W460-6.
    pmc: PMC4489228pubmed: 25977294doi: 10.1093/nar/gkv403google scholar: lookup
  39. Kim MC, Lee SW, Ryu DY, Cui FJ, Bhak J, Kim Y. Identification and characterization of microRNAs in normal equine tissues by Next Generation Sequencing.. PLoS One 2014;9(4):e93662.
    pmc: PMC3973549pubmed: 24695583doi: 10.1371/journal.pone.0093662google scholar: lookup
  40. Yue P, Turkson J. Targeting STAT3 in cancer: how successful are we?. Expert Opin Investig Drugs 2009 Jan;18(1):45-56.
    pmc: PMC2610472pubmed: 19053881doi: 10.1517/13543780802565791google scholar: lookup
  41. Zehavi L, Avraham R, Barzilai A, Bar-Ilan D, Navon R, Sidi Y, Avni D, Leibowitz-Amit R. Silencing of a large microRNA cluster on human chromosome 14q32 in melanoma: biological effects of mir-376a and mir-376c on insulin growth factor 1 receptor.. Mol Cancer 2012 Jul 2;11:44.
    pmc: PMC3444916pubmed: 22747855doi: 10.1186/1476-4598-11-44google scholar: lookup
  42. Lavon I, Zrihan D, Granit A, Einstein O, Fainstein N, Cohen MA, Cohen MA, Zelikovitch B, Shoshan Y, Spektor S, Reubinoff BE, Felig Y, Gerlitz O, Ben-Hur T, Smith Y, Siegal T. Gliomas display a microRNA expression profile reminiscent of neural precursor cells.. Neuro Oncol 2010 May;12(5):422-33.
    pmc: PMC2940621pubmed: 20406893doi: 10.1093/neuonc/nop061google scholar: lookup
  43. Thayanithy V, Sarver AL, Kartha RV, Li L, Angstadt AY, Breen M, Steer CJ, Modiano JF, Subramanian S. Perturbation of 14q32 miRNAs-cMYC gene network in osteosarcoma.. Bone 2012 Jan;50(1):171-81.
    pmc: PMC3755949pubmed: 22037351doi: 10.1016/j.bone.2011.10.012google scholar: lookup
  44. Haller F, von Heydebreck A, Zhang JD, Gunawan B, Langer C, Ramadori G, Wiemann S, Sahin O. Localization- and mutation-dependent microRNA (miRNA) expression signatures in gastrointestinal stromal tumours (GISTs), with a cluster of co-expressed miRNAs located at 14q32.31.. J Pathol 2010 Jan;220(1):71-86.
    pubmed: 19768731doi: 10.1002/path.2610google scholar: lookup
  45. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells.. Cancer Cell 2006 Jun;9(6):435-43.
    pubmed: 16766263doi: 10.1016/j.ccr.2006.04.020google scholar: lookup
  46. Kelly AD, Haibe-Kains B, Janeway KA, Hill KE, Howe E, Goldsmith J, Kurek K, Perez-Atayde AR, Francoeur N, Fan JB, April C, Schneider H, Gebhardt MC, Culhane A, Quackenbush J, Spentzos D. MicroRNA paraffin-based studies in osteosarcoma reveal reproducible independent prognostic profiles at 14q32.. Genome Med 2013;5(1):2.
    pmc: PMC3706900pubmed: 23339462doi: 10.1186/gm406google scholar: lookup
  47. Sarver AL, Thayanithy V, Scott MC, Cleton-Jansen AM, Hogendoorn PC, Modiano JF, Subramanian S. MicroRNAs at the human 14q32 locus have prognostic significance in osteosarcoma.. Orphanet J Rare Dis 2013 Jan 11;8:7.
    pmc: PMC3566973pubmed: 23311495doi: 10.1186/1750-1172-8-7google scholar: lookup
  48. Zhang L, Volinia S, Bonome T, Calin GA, Greshock J, Yang N, Liu CG, Giannakakis A, Alexiou P, Hasegawa K, Johnstone CN, Megraw MS, Adams S, Lassus H, Huang J, Kaur S, Liang S, Sethupathy P, Leminen A, Simossis VA, Sandaltzopoulos R, Naomoto Y, Katsaros D, Gimotty PA, DeMichele A, Huang Q, Bützow R, Rustgi AK, Weber BL, Birrer MJ, Hatzigeorgiou AG, Croce CM, Coukos G. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer.. Proc Natl Acad Sci U S A 2008 May 13;105(19):7004-9.
    pmc: PMC2383982pubmed: 18458333doi: 10.1073/pnas.0801615105google scholar: lookup
  49. Nadal E, Zhong J, Lin J, Reddy RM, Ramnath N, Orringer MB, Chang AC, Beer DG, Chen G. A MicroRNA cluster at 14q32 drives aggressive lung adenocarcinoma.. Clin Cancer Res 2014 Jun 15;20(12):3107-17.
    pubmed: 24833665doi: 10.1158/1078-0432.ccr-13-3348google scholar: lookup
  50. Luk JM, Burchard J, Zhang C, Liu AM, Wong KF, Shek FH, Lee NP, Fan ST, Poon RT, Ivanovska I, Philippar U, Cleary MA, Buser CA, Shaw PM, Lee CN, Tenen DG, Dai H, Mao M. DLK1-DIO3 genomic imprinted microRNA cluster at 14q32.2 defines a stemlike subtype of hepatocellular carcinoma associated with poor survival.. J Biol Chem 2011 Sep 2;286(35):30706-30713.
    pmc: PMC3162431pubmed: 21737452doi: 10.1074/jbc.m111.229831google scholar: lookup
  51. Costa FF, Bischof JM, Vanin EF, Lulla RR, Wang M, Sredni ST, Rajaram V, Bonaldo Mde F, Wang D, Goldman S, Tomita T, Soares MB. Identification of microRNAs as potential prognostic markers in ependymoma.. PLoS One 2011;6(10):e25114.
    pmc: PMC3203863pubmed: 22053178doi: 10.1371/journal.pone.0025114google scholar: lookup
  52. Wentzensen N, Vinokurova S, von Knebel Doeberitz M. Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract.. Cancer Res 2004 Jun 1;64(11):3878-84.
    pubmed: 15172997doi: 10.1158/0008-5472.can-04-0009google scholar: lookup
  53. Lajer CB, Garnæs E, Friis-Hansen L, Norrild B, Therkildsen MH, Glud M, Rossing M, Lajer H, Svane D, Skotte L, Specht L, Buchwald C, Nielsen FC. The role of miRNAs in human papilloma virus (HPV)-associated cancers: bridging between HPV-related head and neck cancer and cervical cancer.. Br J Cancer 2012 Apr 24;106(9):1526-34.
    pmc: PMC3341860pubmed: 22472886doi: 10.1038/bjc.2012.109google scholar: lookup
  54. Lajer CB, Nielsen FC, Friis-Hansen L, Norrild B, Borup R, Garnæs E, Rossing M, Specht L, Therkildsen MH, Nauntofte B, Dabelsteen S, von Buchwald C. Different miRNA signatures of oral and pharyngeal squamous cell carcinomas: a prospective translational study.. Br J Cancer 2011 Mar 1;104(5):830-40.
    pmc: PMC3048216pubmed: 21326242doi: 10.1038/bjc.2011.29google scholar: lookup
  55. McKenna DJ, Patel D, McCance DJ. miR-24 and miR-205 expression is dependent on HPV onco-protein expression in keratinocytes.. Virology 2014 Jan 5;448:210-6.
    pmc: PMC3865362pubmed: 24314651doi: 10.1016/j.virol.2013.10.014google scholar: lookup
  56. Harden ME, Prasad N, Griffiths A, Munger K. Modulation of microRNA-mRNA Target Pairs by Human Papillomavirus 16 Oncoproteins.. mBio 2017 Jan 3;8(1).
    pmc: PMC5210503pubmed: 28049151doi: 10.1128/mbio.02170-16google scholar: lookup
  57. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, Li Q, Li X, Wang W, Zhang Y, Wang J, Jiang X, Xiang Y, Xu C, Zheng P, Zhang J, Li R, Zhang H, Shang X, Gong T, Ning G, Wang J, Zen K, Zhang J, Zhang CY. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases.. Cell Res 2008 Oct;18(10):997-1006.
    pubmed: 18766170doi: 10.1038/cr.2008.282google scholar: lookup
  58. 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.
    pmc: PMC4186243pubmed: 22158052doi: 10.1158/1940-6207.capr-11-0370google scholar: lookup
  59. Patnaik SK, Yendamuri S, Kannisto E, Kucharczuk JC, Singhal S, Vachani A. MicroRNA expression profiles of whole blood in lung adenocarcinoma.. PLoS One 2012;7(9):e46045.
    pmc: PMC3460960pubmed: 23029380doi: 10.1371/journal.pone.0046045google scholar: lookup
  60. 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.
    pmc: PMC3164711pubmed: 21909417doi: 10.1371/journal.pone.0024145google scholar: lookup
  61. Häusler SF, Keller A, Chandran PA, Ziegler K, Zipp K, Heuer S, Krockenberger M, Engel JB, Hönig A, Scheffler M, Dietl J, Wischhusen J. Whole blood-derived miRNA profiles as potential new tools for ovarian cancer screening.. Br J Cancer 2010 Aug 24;103(5):693-700.
    pmc: PMC2938264pubmed: 20683447doi: 10.1038/sj.bjc.6605833google scholar: lookup
  62. Becker C, Hammerle-Fickinger A, Riedmaier I, Pfaffl MW. mRNA and microRNA quality control for RT-qPCR analysis.. Methods 2010 Apr;50(4):237-43.
    pubmed: 20079844doi: 10.1016/j.ymeth.2010.01.010google scholar: lookup
  63. Ibberson D, Benes V, Muckenthaler MU, Castoldi M. RNA degradation compromises the reliability of microRNA expression profiling.. BMC Biotechnol 2009 Dec 21;9:102.
    pmc: PMC2805631pubmed: 20025722doi: 10.1186/1472-6750-9-102google scholar: lookup
  64. Jung M, Schaefer A, Steiner I, Kempkensteffen C, Stephan C, Erbersdobler A, Jung K. Robust microRNA stability in degraded RNA preparations from human tissue and cell samples.. Clin Chem 2010 Jun;56(6):998-1006.
    pubmed: 20378769doi: 10.1373/clinchem.2009.141580google scholar: lookup
  65. Hall JS, Taylor J, Valentine HR, Irlam JJ, Eustace A, Hoskin PJ, Miller CJ, West CM. Enhanced stability of microRNA expression facilitates classification of FFPE tumour samples exhibiting near total mRNA degradation.. Br J Cancer 2012 Aug 7;107(4):684-94.
    pmc: PMC3419950pubmed: 22805332doi: 10.1038/bjc.2012.294google scholar: lookup
  66. 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
  67. 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

Citations

This article has been cited 8 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. Unger L, Abril C, Gerber V, Jagannathan V, Koch C, Hamza E. Diagnostic potential of three serum microRNAs as biomarkers for equine sarcoid disease in horses and donkeys. J Vet Intern Med 2021 Jan;35(1):610-619.
    doi: 10.1111/jvim.16027pubmed: 33415768google scholar: lookup
  4. Podstawski P, Witarski W, Szmatoła T, Bugno-Poniewierska M, Ropka-Molik K. Mobility and Invasion Related Gene Expression Patterns in Equine Sarcoid. Animals (Basel) 2020 May 19;10(5).
    doi: 10.3390/ani10050880pubmed: 32438542google scholar: lookup
  5. Zhang H, Liu X, Yang X, Wu H, Zhu J, Zhang H. miRNA-mRNA Integrated Analysis Reveals Roles for miRNAs in a Typical Halophyte, Reaumuria soongorica, during Seed Germination under Salt Stress. Plants (Basel) 2020 Mar 10;9(3).
    doi: 10.3390/plants9030351pubmed: 32164348google scholar: lookup
  6. 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
  7. Ohlsson Å, Hanås S, Holst BS, Lorent J, Andersson G, Höglund K, Tidholm A, Ljungvall I, Häggström J. Profiling of the microRNA transcriptome in feline whole blood. Sci Rep 2025 Jul 31;15(1):27962.
    doi: 10.1038/s41598-025-09478-xpubmed: 40745193google scholar: lookup
  8. 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
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