Genes2020; 11(10); 1143; doi: 10.3390/genes11101143

An Integrative miRNA-mRNA Expression Analysis Reveals Striking Transcriptomic Similarities between Severe Equine Asthma and Specific Asthma Endotypes in Humans.

Abstract: Severe equine asthma is an incurable obstructive respiratory condition affecting 10-15% of horses in temperate climates. Upon exposure to airborne antigens from hay feeding, affected horses show neutrophilic airway inflammation and bronchoconstriction, leading to increased respiratory effort. The resulting implications range from welfare concerns to economic impacts on equestrian sports and horse breeding. Immunological and pathophysiological characteristics of severe equine asthma show important parallels with allergic and severe neutrophilic human asthma. Our study aimed at investigating regulatory networks underlying the pathophysiology of the disease by profiling miRNA and mRNA expression in lung tissue samples from asthmatic horses compared with healthy controls. We sequenced small RNAs and mRNAs from lungs of seven asthmatic horses in exacerbation, five affected horses in remission, and eight healthy control horses. Our comprehensive differential expression analyses, combined with the miRNA-mRNA negative correlation approach, revealed a strong similarity on the transcriptomic level between severe equine asthma and severe neutrophilic asthma in humans, potentially through affecting Th17 cell differentiation. This study also showed that several dysregulated miRNAs and mRNAs are involved in airway remodeling. These results present a starting point for a better transcriptomic understanding of severe equine asthma and its similarities to asthma in humans.
Publication Date: 2020-09-28 PubMed ID: 32998415PubMed Central: PMC7600650DOI: 10.3390/genes11101143Google Scholar: Lookup
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  • Comparative Study
  • 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 research article focuses on a comparative study between Severe Equine Asthma and certain types of asthma in humans, specifically by measuring miRNA and mRNA expression. It finds substantial transcriptomic similarities between these two forms of asthma, furthering our understanding of both diseases.

Research Objectives

  • The main objective of the study was to explore the regulatory networks underlying the pathophysiology of severe equine asthma. This was accomplished by profiling miRNA and mRNA expression in lung tissue samples from asthmatic and healthy horses.
  • The researchers also wanted to compare these findings with human instances of asthma, particularly severe neutrophilic asthma.

Methods

  • The study used lung tissue samples from a variety of horses, including seven horses that were actively experiencing asthma, five horses in remission from asthma, and eight healthy horses.
  • The researchers sequenced small RNAs and mRNAs from these samples to study their differential expression.

Findings

  • Through differential expression analysis and related studies focused on the negative correlation between miRNA and mRNA, the researchers discovered that severe equine asthma and severe neutrophilic human asthma exhibit a strong transcriptomic similarity.
  • This similarity was particularly evident in the impact on Th17 cell differentiation.
  • The study found that several dysregulated miRNAs and mRNAs are involved in causing structural changes in the airways, a process known as “airway remodeling”.

Implications

  • The results of this research provide a foundation for a deeper transcriptomic understanding of severe equine asthma and its similarities to human asthma.
  • This could potentially lead to new therapeutic strategies that could benefit both horses and humans suffering from specific asthma endotypes.
  • The study further reinforces the importance of comparative medicine in identifying disease patterns across species, thereby enabling more targeted and effective treatments.

Cite This Article

APA
Hulliger MF, Pacholewska A, Vargas A, Lavoie JP, Leeb T, Gerber V, Jagannathan V. (2020). An Integrative miRNA-mRNA Expression Analysis Reveals Striking Transcriptomic Similarities between Severe Equine Asthma and Specific Asthma Endotypes in Humans. Genes (Basel), 11(10), 1143. https://doi.org/10.3390/genes11101143

Publication

ISSN: 2073-4425
NlmUniqueID: 101551097
Country: Switzerland
Language: English
Volume: 11
Issue: 10
PII: 1143

Researcher Affiliations

Hulliger, Matthias F
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
Pacholewska, Alicja
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
Vargas, Amandine
  • Faculty of Veterinary Medicine, University of Montreal, 3200 rue Sicotte, St-Hyacinthe, QC J2S 2M2, Canada.
Lavoie, Jean-Pierre
  • Faculty of Veterinary Medicine, University of Montreal, 3200 rue Sicotte, St-Hyacinthe, QC J2S 2M2, Canada.
Leeb, Tosso
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
Gerber, Vincent
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
Jagannathan, Vidhya
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.

MeSH Terms

  • Animals
  • Asthma / genetics
  • Asthma / metabolism
  • Asthma / pathology
  • Computational Biology / methods
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Horse Diseases / genetics
  • Horse Diseases / metabolism
  • Horse Diseases / pathology
  • Horses
  • Humans
  • MicroRNAs / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcriptome

Grant Funding

  • PJT-148807 / Canadian institute of health research

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 86 references
  1. Hotchkiss JW, Reid SW, Christley RM. A survey of horse owners in Great Britain regarding horses in their care. Part 2: Risk factors for recurrent airway obstruction.. Equine Vet J 2007 Jul;39(4):301-8.
    doi: 10.2746/042516407X180129pubmed: 17722720google scholar: lookup
  2. Leclere M, Lavoie-Lamoureux A, Lavoie JP. Heaves, an asthma-like disease of horses.. Respirology 2011 Oct;16(7):1027-46.
  3. Setlakwe EL, Lemos KR, Lavoie-Lamoureux A, Duguay JD, Lavoie JP. Airway collagen and elastic fiber content correlates with lung function in equine heaves.. Am J Physiol Lung Cell Mol Physiol 2014 Aug 1;307(3):L252-60.
    doi: 10.1152/ajplung.00019.2014pubmed: 24879055google scholar: lookup
  4. Bullone M, Lavoie JP. Asthma "of horses and men"--how can equine heaves help us better understand human asthma immunopathology and its functional consequences?. Mol Immunol 2015 Jul;66(1):97-105.
    doi: 10.1016/j.molimm.2014.12.005pubmed: 25547716google scholar: lookup
  5. Bond S, Lu00e9guillette R, Richard EA, Couetil L, Lavoie JP, Martin JG, Pirie RS. Equine asthma: Integrative biologic relevance of a recently proposed nomenclature.. J Vet Intern Med 2018 Nov;32(6):2088-2098.
    doi: 10.1111/jvim.15302pmc: PMC6271326pubmed: 30294851google scholar: lookup
  6. To T, Stanojevic S, Moores G, Gershon AS, Bateman ED, Cruz AA, Boulet LP. Global asthma prevalence in adults: findings from the cross-sectional world health survey.. BMC Public Health 2012 Mar 19;12:204.
    doi: 10.1186/1471-2458-12-204pmc: PMC3353191pubmed: 22429515google scholar: lookup
  7. Bahadori K, Doyle-Waters MM, Marra C, Lynd L, Alasaly K, Swiston J, FitzGerald JM. Economic burden of asthma: a systematic review.. BMC Pulm Med 2009 May 19;9:24.
    doi: 10.1186/1471-2466-9-24pmc: PMC2698859pubmed: 19454036google scholar: lookup
  8. Moran G., Folch H. Recurrent airway obstruction in horses - An allergic inflammation: A review. Vet. Med. (Praha) 2011;56:1u201313. doi: 10.17221/1566-VETMED.
    doi: 10.17221/1566-VETMEDgoogle scholar: lookup
  9. Pacholewska A, Jagannathan V, Dru00f6gemu00fcller M, Klukowska-Ru00f6tzler J, Lanz S, Hamza E, Dermitzakis ET, Marti E, Leeb T, Gerber V. Impaired Cell Cycle Regulation in a Natural Equine Model of Asthma.. PLoS One 2015;10(8):e0136103.
  10. Niedzwiedz A, Jaworski Z, Tykalowski B, Smialek M. Neutrophil and macrophage apoptosis in bronchoalveolar lavage fluid from healthy horses and horses with recurrent airway obstruction (RAO).. BMC Vet Res 2014 Jan 24;10:29.
    doi: 10.1186/1746-6148-10-29pmc: PMC3903020pubmed: 24460911google scholar: lookup
  11. Pacholewska A, Kraft MF, Gerber V, Jagannathan V. Differential Expression of Serum MicroRNAs Supports CD4u207a T Cell Differentiation into Th2/Th17 Cells in Severe Equine Asthma.. Genes (Basel) 2017 Dec 12;8(12).
    doi: 10.3390/genes8120383pmc: PMC5748701pubmed: 29231896google scholar: lookup
  12. Pirie RS. Recurrent airway obstruction: a review.. Equine Vet J 2014 May;46(3):276-88.
    doi: 10.1111/evj.12204pubmed: 24164473google scholar: lookup
  13. Lavoie JP, Maghni K, Desnoyers M, Taha R, Martin JG, Hamid QA. Neutrophilic airway inflammation in horses with heaves is characterized by a Th2-type cytokine profile.. Am J Respir Crit Care Med 2001 Oct 15;164(8 Pt 1):1410-3.
    doi: 10.1164/ajrccm.164.8.2012091pubmed: 11704587google scholar: lookup
  14. Cordeau ME, Joubert P, Dewachi O, Hamid Q, Lavoie JP. IL-4, IL-5 and IFN-gamma mRNA expression in pulmonary lymphocytes in equine heaves.. Vet Immunol Immunopathol 2004 Jan;97(1-2):87-96.
    doi: 10.1016/j.vetimm.2003.08.013pubmed: 14700540google scholar: lookup
  15. Horohov DW, Beadle RE, Mouch S, Pourciau SS. Temporal regulation of cytokine mRNA expression in equine recurrent airway obstruction.. Vet Immunol Immunopathol 2005 Oct 18;108(1-2):237-45.
    doi: 10.1016/j.vetimm.2005.07.013pubmed: 16098607google scholar: lookup
  16. Klukowska-Ru00f6tzler J, Swinburne JE, Dru00f6gemu00fcller C, Dolf G, Janda J, Leeb T, Gerber V. The interleukin 4 receptor gene and its role in recurrent airway obstruction in Swiss Warmblood horses.. Anim Genet 2012 Aug;43(4):450-3.
  17. Giguu00e8re S, Viel L, Lee E, MacKay RJ, Hernandez J, Franchini M. Cytokine induction in pulmonary airways of horses with heaves and effect of therapy with inhaled fluticasone propionate.. Vet Immunol Immunopathol 2002 Mar;85(3-4):147-58.
    doi: 10.1016/S0165-2427(01)00420-2pubmed: 11943316google scholar: lookup
  18. Ainsworth DM, Gru00fcnig G, Matychak MB, Young J, Wagner B, Erb HN, Antczak DF. Recurrent airway obstruction (RAO) in horses is characterized by IFN-gamma and IL-8 production in bronchoalveolar lavage cells.. Vet Immunol Immunopathol 2003 Nov 15;96(1-2):83-91.
    doi: 10.1016/S0165-2427(03)00142-9pubmed: 14522137google scholar: lookup
  19. Beadle RE, Horohov DW, Gaunt SD. Interleukin-4 and interferon-gamma gene expression in summer pasture-associated obstructive pulmonary disease affected horses.. Equine Vet J 2002 Jul;34(4):389-94.
    doi: 10.2746/042516402776249119pubmed: 12117112google scholar: lookup
  20. Papi A, Brightling C, Pedersen SE, Reddel HK. Asthma.. Lancet 2018 Feb 24;391(10122):783-800.
    doi: 10.1016/S0140-6736(17)33311-1pubmed: 29273246google scholar: lookup
  21. Kuruvilla ME, Lee FE, Lee GB. Understanding Asthma Phenotypes, Endotypes, and Mechanisms of Disease.. Clin Rev Allergy Immunol 2019 Apr;56(2):219-233.
    doi: 10.1007/s12016-018-8712-1pmc: PMC6411459pubmed: 30206782google scholar: lookup
  22. Tessier L, Cu00f4tu00e9 O, Clark ME, Viel L, Diaz-Mu00e9ndez A, Anders S, Bienzle D. Gene set enrichment analysis of the bronchial epithelium implicates contribution of cell cycle and tissue repair processes in equine asthma.. Sci Rep 2018 Nov 6;8(1):16408.
    doi: 10.1038/s41598-018-34636-9pmc: PMC6219531pubmed: 30401798google scholar: lookup
  23. Bullone M, Joubert P, Gagnu00e9 A, Lavoie JP, Hu00e9lie P. Bronchoalveolar lavage fluid neutrophilia is associated with the severity of pulmonary lesions during equine asthma exacerbations.. Equine Vet J 2018 Sep;50(5):609-615.
    doi: 10.1111/evj.12806pubmed: 29341228google scholar: lookup
  24. Andrews S. FASTQCu2014A Quality Control Tool for High Throughput Sequence Data. [(accessed on 1 June 2020)]; Available online: www.bioinformatics.babraham.ac.uk/projects/fastqc.
  25. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet.J. 2011;17:10. doi: 10.14806/ej.17.1.200.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  26. Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
    doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
  27. Friedlu00e4nder 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.
    doi: 10.1093/nar/gkr688pmc: PMC3245920pubmed: 21911355google scholar: lookup
  28. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data.. Nucleic Acids Res 2011 Jan;39(Database issue):D152-7.
    doi: 10.1093/nar/gkq1027pmc: PMC3013655pubmed: 21037258google scholar: lookup
  29. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  30. 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.
    doi: 10.1093/nar/gkv403pmc: PMC4489228pubmed: 25977294google scholar: lookup
  31. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner.. Bioinformatics 2013 Jan 1;29(1):15-21.
  32. Anders S, Pyl PT, Huber W. HTSeq--a Python framework to work with high-throughput sequencing data.. Bioinformatics 2015 Jan 15;31(2):166-9.
  33. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A. PANTHER: a library of protein families and subfamilies indexed by function.. Genome Res 2003 Sep;13(9):2129-41.
    doi: 10.1101/gr.772403pmc: PMC403709pubmed: 12952881google scholar: lookup
  34. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks.. Genome Res 2003 Nov;13(11):2498-504.
  35. Kutmon M, Kelder T, Mandaviya P, Evelo CT, Coort SL. CyTargetLinker: a cytoscape app to integrate regulatory interactions in network analysis.. PLoS One 2013;8(12):e82160.
  36. Vila-Casadesu00fas M, Gironella M, Lozano JJ. MiRComb: An R Package to Analyse miRNA-mRNA Interactions. Examples across Five Digestive Cancers.. PLoS One 2016;11(3):e0151127.
  37. Chalmin F, Mignot G, Bruchard M, Chevriaux A, Vu00e9gran F, Hichami A, Ladoire S, Derangu00e8re V, Vincent J, Masson D, Robson SC, Eberl G, Pallandre JR, Borg C, Ryffel B, Apetoh L, Ru00e9bu00e9 C, Ghiringhelli F. Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression.. Immunity 2012 Mar 23;36(3):362-73.
    doi: 10.1016/j.immuni.2011.12.019pubmed: 22406269google scholar: lookup
  38. Maes T, Cobos FA, Schleich F, Sorbello V, Henket M, De Preter K, Bracke KR, Conickx G, Mesnil C, Vandesompele J, Lahousse L, Bureau F, Mestdagh P, Joos GF, Ricciardolo FL, Brusselle GG, Louis R. Asthma inflammatory phenotypes show differential microRNA expression in sputum.. J Allergy Clin Immunol 2016 May;137(5):1433-46.
    doi: 10.1016/j.jaci.2016.02.018pubmed: 27155035google scholar: lookup
  39. Simpson JL, Phipps S, Baines KJ, Oreo KM, Gunawardhana L, Gibson PG. Elevated expression of the NLRP3 inflammasome in neutrophilic asthma.. Eur Respir J 2014 Apr;43(4):1067-76.
    doi: 10.1183/09031936.00105013pubmed: 24136334google scholar: lookup
  40. Baines KJ, Simpson JL, Wood LG, Scott RJ, Fibbens NL, Powell H, Cowan DC, Taylor DR, Cowan JO, Gibson PG. Sputum gene expression signature of 6 biomarkers discriminates asthma inflammatory phenotypes.. J Allergy Clin Immunol 2014 Apr;133(4):997-1007.
    doi: 10.1016/j.jaci.2013.12.1091pubmed: 24582314google scholar: lookup
  41. Padoan E, Ferraresso S, Pegolo S, Castagnaro M, Barnini C, Bargelloni L. Real time RT-PCR analysis of inflammatory mediator expression in recurrent airway obstruction-affected horses.. Vet Immunol Immunopathol 2013 Dec 15;156(3-4):190-9.
    doi: 10.1016/j.vetimm.2013.09.020pubmed: 24176614google scholar: lookup
  42. Hansen S, Otten ND, Birch K, Skovgaard K, Hopster-Iversen C, Fjeldborg J. Bronchoalveolar lavage fluid cytokine, cytology and IgE allergen in horses with equine asthma.. Vet Immunol Immunopathol 2020 Feb;220:109976.
    doi: 10.1016/j.vetimm.2019.109976pubmed: 31786444google scholar: lookup
  43. Pietra M, Peli A, Bonato A, Ducci A, Cinotti S. Equine bronchoalveolar lavage cytokines in the development of recurrent airway obstruction.. Vet Res Commun 2007 Aug;31 Suppl 1:313-6.
    doi: 10.1007/s11259-007-0055-ypubmed: 17682903google scholar: lookup
  44. Sun W, Shen W, Yang S, Hu F, Li H, Zhu TH. miR-223 and miR-142 attenuate hematopoietic cell proliferation, and miR-223 positively regulates miR-142 through LMO2 isoforms and CEBP-u03b2.. Cell Res 2010 Oct;20(10):1158-69.
    doi: 10.1038/cr.2010.134pubmed: 20856265google scholar: lookup
  45. Dorhoi A, Iannaccone M, Farinacci M, Fau00e9 KC, Schreiber J, Moura-Alves P, Nouailles G, Mollenkopf HJ, Oberbeck-Mu00fcller D, Ju00f6rg S, Heinemann E, Hahnke K, Lu00f6we D, Del Nonno F, Goletti D, Capparelli R, Kaufmann SH. MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment.. J Clin Invest 2013 Nov;123(11):4836-48.
    doi: 10.1172/JCI67604pmc: PMC3809781pubmed: 24084739google scholar: lookup
  46. Ifergan I, Chen S, Zhang B, Miller SD. Cutting Edge: MicroRNA-223 Regulates Myeloid Dendritic Cell-Driven Th17 Responses in Experimental Autoimmune Encephalomyelitis.. J Immunol 2016 Feb 15;196(4):1455-1459.
    doi: 10.4049/jimmunol.1501965pmc: PMC4744529pubmed: 26783338google scholar: lookup
  47. Tabet F, Vickers KC, Cuesta Torres LF, Wiese CB, Shoucri BM, Lambert G, Catherinet C, Prado-Lourenco L, Levin MG, Thacker S, Sethupathy P, Barter PJ, Remaley AT, Rye KA. HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells.. Nat Commun 2014 Feb 28;5:3292.
    doi: 10.1038/ncomms4292pmc: PMC4189962pubmed: 24576947google scholar: lookup
  48. Curtale G, Rubino M, Locati M. MicroRNAs as Molecular Switches in Macrophage Activation.. Front Immunol 2019;10:799.
    doi: 10.3389/fimmu.2019.00799pmc: PMC6478758pubmed: 31057539google scholar: lookup
  49. Bartel S, Carraro G, Alessandrini F, Krauss-Etschmann S, Ricciardolo FLM, Bellusci S. miR-142-3p is associated with aberrant WNT signaling during airway remodeling in asthma.. Am J Physiol Lung Cell Mol Physiol 2018 Aug 1;315(2):L328-L333.
    doi: 10.1152/ajplung.00113.2018pubmed: 29722559google scholar: lookup
  50. Wang Y, Liang J, Qin H, Ge Y, Du J, Lin J, Zhu X, Wang J, Xu J. Elevated expression of miR-142-3p is related to the pro-inflammatory function of monocyte-derived dendritic cells in SLE.. Arthritis Res Ther 2016 Nov 16;18(1):263.
    doi: 10.1186/s13075-016-1158-zpmc: PMC5112667pubmed: 27852285google scholar: lookup
  51. Naqvi AR, Fordham JB, Ganesh B, Nares S. miR-24, miR-30b and miR-142-3p interfere with antigen processing and presentation by primary macrophages and dendritic cells.. Sci Rep 2016 Sep 9;6:32925.
    doi: 10.1038/srep32925pmc: PMC5017188pubmed: 27611009google scholar: lookup
  52. Liu Y, Song X, Meng S, Jiang M. Downregulated expression of miR-142-3p in macrophages contributes to increased IL-6 levels in aged mice.. Mol Immunol 2016 Dec;80:11-16.
    doi: 10.1016/j.molimm.2016.10.009pubmed: 27788393google scholar: lookup
  53. Naqvi AR, Fordham JB, Nares S. miR-24, miR-30b, and miR-142-3p regulate phagocytosis in myeloid inflammatory cells.. J Immunol 2015 Feb 15;194(4):1916-27.
    doi: 10.4049/jimmunol.1401893pmc: PMC4323870pubmed: 25601927google scholar: lookup
  54. He Q, Li F, Li J, Li R, Zhan G, Li G, Du W, Tan H. MicroRNA-26a-interleukin (IL)-6-IL-17 axis regulates the development of non-alcoholic fatty liver disease in a murine model.. Clin Exp Immunol 2017 Jan;187(1):174-184.
    doi: 10.1111/cei.12838pmc: PMC5167023pubmed: 27377869google scholar: lookup
  55. Zhang R, Tian A, Wang J, Shen X, Qi G, Tang Y. miR26a modulates Th17/T reg balance in the EAE model of multiple sclerosis by targeting IL6.. Neuromolecular Med 2015 Mar;17(1):24-34.
    doi: 10.1007/s12017-014-8335-5pubmed: 25362566google scholar: lookup
  56. Shi T, Xie Y, Fu Y, Zhou Q, Ma Z, Ma J, Huang Z, Zhang J, Chen J. The signaling axis of microRNA-31/interleukin-25 regulates Th1/Th17-mediated inflammation response in colitis.. Mucosal Immunol 2017 Jul;10(4):983-995.
    doi: 10.1038/mi.2016.102pubmed: 27901018google scholar: lookup
  57. Nakahama T, Hanieh H, Nguyen NT, Chinen I, Ripley B, Millrine D, Lee S, Nyati KK, Dubey PK, Chowdhury K, Kawahara Y, Kishimoto T. Aryl hydrocarbon receptor-mediated induction of the microRNA-132/212 cluster promotes interleukin-17-producing T-helper cell differentiation.. Proc Natl Acad Sci U S A 2013 Jul 16;110(29):11964-9.
    doi: 10.1073/pnas.1311087110pmc: PMC3718186pubmed: 23818645google scholar: lookup
  58. Pollari S, Leivonen SK, Peru00e4lu00e4 M, Fey V, Ku00e4ku00f6nen SM, Kallioniemi O. Identification of microRNAs inhibiting TGF-u03b2-induced IL-11 production in bone metastatic breast cancer cells.. PLoS One 2012;7(5):e37361.
  59. Dai X, Chen X, Chen Q, Shi L, Liang H, Zhou Z, Liu Q, Pang W, Hou D, Wang C, Zen K, Yuan Y, Zhang CY, Xia L. MicroRNA-193a-3p Reduces Intestinal Inflammation in Response to Microbiota via Down-regulation of Colonic PepT1.. J Biol Chem 2015 Jun 26;290(26):16099-115.
    doi: 10.1074/jbc.M115.659318pmc: PMC4481212pubmed: 25931122google scholar: lookup
  60. Nong W. Long non-coding RNA NEAT1/miR-193a-3p regulates LPS-induced apoptosis and inflammatory injury in WI-38 cells through TLR4/NF-u03baB signaling.. Am J Transl Res 2019;11(9):5944-5955.
    pmc: PMC6789249pubmed: 31632562
  61. O'Reilly S, Ciechomska M, Fullard N, Przyborski S, van Laar JM. IL-13 mediates collagen deposition via STAT6 and microRNA-135b: a role for epigenetics.. Sci Rep 2016 Apr 26;6:25066.
    doi: 10.1038/srep25066pmc: PMC4844987pubmed: 27113293google scholar: lookup
  62. Matsuyama H, Suzuki HI, Nishimori H, Noguchi M, Yao T, Komatsu N, Mano H, Sugimoto K, Miyazono K. miR-135b mediates NPM-ALK-driven oncogenicity and renders IL-17-producing immunophenotype to anaplastic large cell lymphoma.. Blood 2011 Dec 22;118(26):6881-92.
    doi: 10.1182/blood-2011-05-354654pubmed: 22042699google scholar: lookup
  63. Newcomb DC, Peebles RS Jr. Th17-mediated inflammation in asthma.. Curr Opin Immunol 2013 Dec;25(6):755-60.
    doi: 10.1016/j.coi.2013.08.002pmc: PMC3855890pubmed: 24035139google scholar: lookup
  64. Korn A, Miller D, Dong L, Buckles EL, Wagner B, Ainsworth DM. Differential Gene Expression Profiles and Selected Cytokine Protein Analysis of Mediastinal Lymph Nodes of Horses with Chronic Recurrent Airway Obstruction (RAO) Support an Interleukin-17 Immune Response.. PLoS One 2015;10(11):e0142622.
  65. Frodella C.M., Thomas K.A., Bowser J.E., Mochal C.A., Eddy A.L., Claude A., Swiderski C.E. The lung transcriptome of horses with pasture-associated severe equine asthma identifies a Th17-high Th2-low phenotype. J. Equine Vet. Sci. 2019;76:61. doi: 10.1016/j.jevs.2019.03.062.
  66. Debrue M, Hamilton E, Joubert P, Lajoie-Kadoch S, Lavoie JP. Chronic exacerbation of equine heaves is associated with an increased expression of interleukin-17 mRNA in bronchoalveolar lavage cells.. Vet Immunol Immunopathol 2005 May 1;105(1-2):25-31.
    doi: 10.1016/j.vetimm.2004.12.013pubmed: 15797472google scholar: lookup
  67. Swinburne JE, Bogle H, Klukowska-Ru00f6tzler J, Dru00f6gemu00fcller M, Leeb T, Temperton E, Dolf G, Gerber V. A whole-genome scan for recurrent airway obstruction in Warmblood sport horses indicates two positional candidate regions.. Mamm Genome 2009 Aug;20(8):504-15.
    doi: 10.1007/s00335-009-9214-5pubmed: 19760324google scholar: lookup
  68. Kamsteeg M, Bergers M, de Boer R, Zeeuwen PL, Hato SV, Schalkwijk J, Tjabringa GS. Type 2 helper T-cell cytokines induce morphologic and molecular characteristics of atopic dermatitis in human skin equivalent.. Am J Pathol 2011 May;178(5):2091-9.
  69. Walker JK, Ahumada A, Frank B, Gaspard R, Berman K, Quackenbush J, Schwartz DA. Multistrain genetic comparisons reveal CCR5 as a receptor involved in airway hyperresponsiveness.. Am J Respir Cell Mol Biol 2006 Jun;34(6):711-8.
    doi: 10.1165/rcmb.2005-0314OCpmc: PMC2644233pubmed: 16474097google scholar: lookup
  70. Madigan LA, Wong GS, Gordon EM, Chen WS, Balenga N, Koziol-White CJ, Panettieri RA Jr, Levine SJ, Druey KM. RGS4 Overexpression in Lung Attenuates Airway Hyperresponsiveness in Mice.. Am J Respir Cell Mol Biol 2018 Jan;58(1):89-98.
    doi: 10.1165/rcmb.2017-0109OCpmc: PMC5800898pubmed: 28853915google scholar: lookup
  71. Balenga NA, Jester W, Jiang M, Panettieri RA Jr, Druey KM. Loss of regulator of G protein signaling 5 promotes airway hyperresponsiveness in the absence of allergic inflammation.. J Allergy Clin Immunol 2014 Aug;134(2):451-9.
    doi: 10.1016/j.jaci.2014.01.019pmc: PMC4119844pubmed: 24666695google scholar: lookup
  72. Scisciani C, Vossio S, Guerrieri F, Schinzari V, De Iaco R, D'Onorio de Meo P, Cervello M, Montalto G, Pollicino T, Raimondo G, Levrero M, Pediconi N. Transcriptional regulation of miR-224 upregulated in human HCCs by NFu03baB inflammatory pathways.. J Hepatol 2012 Apr;56(4):855-61.
    doi: 10.1016/j.jhep.2011.11.017pubmed: 22178270google scholar: lookup
  73. Bureau F, Delhalle S, Bonizzi G, Fiu00e9vez L, Dognu00e9 S, Kirschvink N, Vanderplasschen A, Merville MP, Bours V, Lekeux P. Mechanisms of persistent NF-kappa B activity in the bronchi of an animal model of asthma.. J Immunol 2000 Nov 15;165(10):5822-30.
    doi: 10.4049/jimmunol.165.10.5822pubmed: 11067942google scholar: lookup
  74. Bureau F, Bonizzi G, Kirschvink N, Delhalle S, Desmecht D, Merville MP, Bours V, Lekeux P. Correlation between nuclear factor-kappaB activity in bronchial brushing samples and lung dysfunction in an animal model of asthma.. Am J Respir Crit Care Med 2000 Apr;161(4 Pt 1):1314-21.
    doi: 10.1164/ajrccm.161.4.9907010pubmed: 10764329google scholar: lookup
  75. Haag M, Leusink-Muis T, Le Bouquin R, Nijkamp FP, Lugnier A, Frossard N, Folkerts G, Pons F. Increased expression and decreased activity of cytochrome P450 1A1 in a murine model of toluene diisocyanate-induced asthma.. Arch Toxicol 2002 Nov;76(11):621-7.
    doi: 10.1007/s00204-002-0393-zpubmed: 12415424google scholar: lookup
  76. Zordoky BN, El-Kadi AO. Role of NF-kappaB in the regulation of cytochrome P450 enzymes.. Curr Drug Metab 2009 Feb;10(2):164-78.
    doi: 10.2174/138920009787522151pubmed: 19275551google scholar: lookup
  77. Polekhina G, House CM, Traficante N, Mackay JP, Relaix F, Sassoon DA, Parker MW, Bowtell DD. Siah ubiquitin ligase is structurally related to TRAF and modulates TNF-alpha signaling.. Nat Struct Biol 2002 Jan;9(1):68-75.
    doi: 10.1038/nsb743pubmed: 11742346google scholar: lookup
  78. Comer BS, Camoretti-Mercado B, Kogut PC, Halayko AJ, Solway J, Gerthoffer WT. MicroRNA-146a and microRNA-146b expression and anti-inflammatory function in human airway smooth muscle.. Am J Physiol Lung Cell Mol Physiol 2014 Nov 1;307(9):L727-34.
    doi: 10.1152/ajplung.00174.2014pmc: PMC4217003pubmed: 25217662google scholar: lookup
  79. McGeachie MJ, Davis JS, Kho AT, Dahlin A, Sordillo JE, Sun M, Lu Q, Weiss ST, Tantisira KG. Asthma remission: Predicting future airways responsiveness using an miRNA network.. J Allergy Clin Immunol 2017 Aug;140(2):598-600.e8.
    doi: 10.1016/j.jaci.2017.01.023pmc: PMC5546990pubmed: 28238746google scholar: lookup
  80. Kho AT, McGeachie MJ, Moore KG, Sylvia JM, Weiss ST, Tantisira KG. Circulating microRNAs and prediction of asthma exacerbation in childhood asthma.. Respir Res 2018 Jun 26;19(1):128.
    doi: 10.1186/s12931-018-0828-6pmc: PMC6020199pubmed: 29940952google scholar: lookup
  81. Han TS, Voon DC, Oshima H, Nakayama M, Echizen K, Sakai E, Yong ZWE, Murakami K, Yu L, Minamoto T, Ock CY, Jenkins BJ, Kim SJ, Yang HK, Oshima M. Interleukin 1 Up-regulates MicroRNA 135b to Promote Inflammation-Associated Gastric Carcinogenesis in Mice.. Gastroenterology 2019 Mar;156(4):1140-1155.e4.
    doi: 10.1053/j.gastro.2018.11.059pubmed: 30508510google scholar: lookup
  82. Barton AK, Shety T, Bondzio A, Einspanier R, Gehlen H. Corrigendum to "Metalloproteinases and Their Tissue Inhibitors in Comparison between Different Chronic Pneumopathies in the Horse".. Mediators Inflamm 2017;2017:7825942.
    doi: 10.1155/2017/7825942pmc: PMC5742512pubmed: 29375199google scholar: lookup
  83. Zhang B, Zhang J, Xu ZY, Xie HL. Expression of RECK and matrix metalloproteinase-2 in ameloblastoma.. BMC Cancer 2009 Dec 8;9:427.
    doi: 10.1186/1471-2407-9-427pmc: PMC2794878pubmed: 19995435google scholar: lookup
  84. Al-Alawi M, Hassan T, Chotirmall SH. Transforming growth factor u03b2 and severe asthma: a perfect storm.. Respir Med 2014 Oct;108(10):1409-23.
    doi: 10.1016/j.rmed.2014.08.008pubmed: 25240764google scholar: lookup
  85. Ma Z, Liu T, Huang W, Liu H, Zhang HM, Li Q, Chen Z, Guo AY. MicroRNA regulatory pathway analysis identifies miR-142-5p as a negative regulator of TGF-u03b2 pathway via targeting SMAD3.. Oncotarget 2016 Nov 1;7(44):71504-71513.
    doi: 10.18632/oncotarget.12229pmc: PMC5342096pubmed: 27683030google scholar: lookup
  86. Schurch NJ, Schofield P, Gierliu0144ski M, Cole C, Sherstnev A, Singh V, Wrobel N, Gharbi K, Simpson GG, Owen-Hughes T, Blaxter M, Barton GJ. How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use?. RNA 2016 Jun;22(6):839-51.
    doi: 10.1261/rna.053959.115pmc: PMC4878611pubmed: 27022035google scholar: lookup

Citations

This article has been cited 5 times.
  1. Woodrow JS, Sheats MK, Cooper B, Bayless R. Asthma: The Use of Animal Models and Their Translational Utility.. Cells 2023 Apr 5;12(7).
    doi: 10.3390/cells12071091pubmed: 37048164google scholar: lookup
  2. Sage SE, Nicholson P, Leeb T, Gerber V, Jagannathan V. Long-Read Transcriptome of Equine Bronchoalveolar Cells.. Genes (Basel) 2022 Sep 25;13(10).
    doi: 10.3390/genes13101722pubmed: 36292607google scholar: lookup
  3. Klier J, Fuchs S, Winter G, Gehlen H. Inhalative Nanoparticulate CpG Immunotherapy in Severe Equine Asthma: An Innovative Therapeutic Concept and Potential Animal Model for Human Asthma Treatment.. Animals (Basel) 2022 Aug 16;12(16).
    doi: 10.3390/ani12162087pubmed: 36009677google scholar: lookup
  4. Simu00f5es J, Batista M, Tilley P. The Immune Mechanisms of Severe Equine Asthma-Current Understanding and What Is Missing.. Animals (Basel) 2022 Mar 16;12(6).
    doi: 10.3390/ani12060744pubmed: 35327141google scholar: lookup
  5. Karagianni AE, Eaton SL, Kurian D, Cillu00e1n-Garcia E, Twynam-Perkins J, Raper A, Wishart TM, Pirie RS. Application across species of a one health approach to liquid sample handling for respiratory based -omics analysis.. Sci Rep 2021 Jul 12;11(1):14292.
    doi: 10.1038/s41598-021-93839-9pubmed: 34253818google scholar: lookup