FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Cells2024; 13(22); 1926; doi: 10.3390/cells13221926

Distinct Molecular Profiles Underpin Mild-To-Moderate Equine Asthma Cytological Profiles.

Abstract: A state-of-the-art multi-omics approach was applied to improve our understanding of the aetio-pathogenesis of a highly prevalent, performance-limiting disorder of racehorses: mild-to-moderate equine asthma (MMEA). This is a prerequisite to improving prophylactic, management, and therapeutic options for this condition. Although a number of risk factors have been identified, options for intervention are limited. This study applied a multi-omic approach to reveal key inflammatory pathways involved in inflammatory cell recruitment to the lower airways and highlight distinct MMEA inflammatory profiles. We compared bronchoalveolar lavage fluid (BALF) cell gene and protein expression data from horses with non-inflammatory BALF cytology with those isolated from horses with neutrophilic, mastocytic, mixed neutrophilic/mastocytic, and eosinophilic/mastocytic inflammation. The analyses on transcriptomic/proteomic data derived from BALF from horses with neutrophilic cytology showed enrichment in classical inflammatory pathways, and horses with mastocytic inflammation showed enrichment in pathways involved in hypersensitivity reactions related to nonclassical inflammation potentially mimicking a Th2-immune response. The mixed eosinophilic/mastocytic group also presented with a nonclassical inflammatory profile, whereas the mixed neutrophilic/mastocytic group revealed profiles consistent with both neutrophilic inflammation and hypersensitivity. Our adopted multi-omics approach provided a holistic assessment of the immunological status of the lower airways associated with the different cytological profiles of equine asthma.
Get Full Text
Publication Date: 2024-11-20 PubMed ID: 39594673PubMed Central: PMC11593015DOI: 10.3390/cells13221926Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research focuses on identifying the molecular profiles connected to mild-to-moderate equine asthma (MMEA) – a common disorder in racehorses using a combined approach of genomics and proteomics. The study found different types of inflammatory pathways associated with various types of airway inflammation, which may lead to new methods to prevent, manage, and treat this condition.

Objective of the Research

  • The primary objective of the research was to enhance our comprehension of the underlying causes and pathogenesis of mild-to-moderate equine asthma (MMEA), a commonly occurring disorder impacting the performance of racehorses.
  • Such understanding is essential to develop better preventive measures, management practices, and therapeutic treatments for this condition.
  • Despite several identified risk factors, intervention options have been insufficient, necessitating a refined research approach.

Methodology

  • The methodology involved a multi-omic strategy, integrating genomics and proteomics, aiming to reveal key inflammatory pathways responsible for immune cell recruitment into the lower respiratory tract.
  • This study, comparatively analyzing bronchoalveolar lavage fluid (BALF) cell gene and protein expression data, sought to identify distinct inflammatory profiles for MMEA.
  • The study compared horses with non-inflammatory BALF cytology with those exhibiting different types of inflammation, ranging from neutrophilic, mastocytic, mixed neutrophilic/mastocytic, and eosinophilic/mastocytic inflammation.

Findings

  • The analysis of transcriptomic/proteomic data derived from horses with neutrophilic cytology showed an enrichment in classical inflammatory pathways.
  • On the other hand, horses with mastocytic inflammation displayed an enrichment in pathways involved in hypersensitivity reactions associated with non-classical inflammation, potentially mimicking a Th2-immune response.
  • The mixed eosinophilic/mastocytic group also showed a non-classical inflammatory profile, while the mixed neutrophilic/mastocytic group revealed profiles consistent with both neutrophilic inflammation and hypersensitivity.

Conclusion

  • The multi-omics approach used in the research provided a comprehensive evaluation of the immunological status of the lower airways associated with the different cytological profiles of equine asthma.
  • This holistic approach has enhanced our understanding of MMEA by revealing distinct inflammatory profiles. These findings may potentially lead to more effective methods for prevention, management, and treatment of the condition.

Cite This Article

APA
Karagianni AE, Richard EA, Toquet MP, Hue ES, Courouce-Malblanc A, McGorum B, Kurian D, Aguilar J, Mazeri S, Wishart TM, Pirie RS. (2024). Distinct Molecular Profiles Underpin Mild-To-Moderate Equine Asthma Cytological Profiles. Cells, 13(22), 1926. https://doi.org/10.3390/cells13221926

Publication

Cells
ISSN: 2073-4409
NlmUniqueID: 101600052
Country: Switzerland
Language: English
Volume: 13
Issue: 22
PII: 1926

Researcher Affiliations

Karagianni, Anna E
  • School of Veterinary Medicine, Faculty of Health and Medical Sciences, VSM Building, University of Surrey, Daphne Jackson Road, Guildford, Surrey GU2 7AL, UK.
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.
Richard, Eric A
  • LABÉO, 14280 Saint-Contest, France.
  • Université de Caen Normandie, BIOTARGEN UR7450, Normandie Univ, 14000 Caen, France.
Toquet, Marie-Pierre
  • LABÉO, 14280 Saint-Contest, France.
  • Université de Caen Normandie, BIOTARGEN UR7450, Normandie Univ, 14000 Caen, France.
Hue, Erika S
  • LABÉO, 14280 Saint-Contest, France.
  • Université de Caen Normandie, BIOTARGEN UR7450, Normandie Univ, 14000 Caen, France.
Courouce-Malblanc, Anne
  • Centre International de Santé du Cheval d'Oniris (CISCO), Route de Gachet, 44307 Nantes, France.
McGorum, Bruce
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.
Kurian, Dominic
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.
Aguilar, Judit
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.
Mazeri, Stella
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.
Wishart, Thomas M
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.
  • Centre for Systems Health and Integrated Metabolic Research, Nottingham Trent University, Nottingham NG1 4GG, UK.
Pirie, Robert Scott
  • The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9PS, UK.

MeSH Terms

  • Horses
  • Animals
  • Asthma / pathology
  • Asthma / genetics
  • Asthma / immunology
  • Bronchoalveolar Lavage Fluid / cytology
  • Horse Diseases / pathology
  • Horse Diseases / immunology
  • Horse Diseases / metabolism
  • Neutrophils / metabolism
  • Neutrophils / immunology
  • Mast Cells / metabolism
  • Mast Cells / pathology
  • Transcriptome / genetics
  • Proteomics / methods
  • Inflammation / pathology
  • Eosinophils / metabolism
  • Eosinophils / pathology
  • Gene Expression Profiling

Grant Funding

  • R45502/3138 / Horserace Betting Levy Board
  • RB1005/ 338DCD / Hong Kong Jockey Club
  • BBS/E/D/10002071 / Biotechnology and Biological Sciences Research Council

Conflict of Interest Statement

None of the co-authors have any conflict of interest.

References

This article includes 57 references
  1. Wood J.L.N., Newton J.R., Chanter N., Mumford J.A.. Inflammatory airway disease, nasal discharge and respiratory infections in young British racehorses.. Equine Vet. J. 2005;37:236–242.
    doi: 10.2746/0425164054530579pubmed: 15892233google scholar: lookup
  2. Allen K.J., Tremaine W.H., Franklin S.H.. Prevalence of inflammatory airway disease in national hunt horses referred for investigation of poor athletic performance.. Equine Vet. J. Suppl. 2006;38:529–534.
    doi: 10.1111/j.2042-3306.2006.tb05599.xpubmed: 17402478google scholar: lookup
  3. Ivester K.M., Couetil L.L., Moore G.E.. An observational study of environmental exposures, airway cytology, and performance in racing thoroughbreds.. J. Vet. Intern. Med. 2018;32:1754–1762.
    doi: 10.1111/jvim.15226pmc: PMC6189343pubmed: 30222207google scholar: lookup
  4. Couetil L., Cardwell J.M., Leguillette R., Mazan M., Richard E., Bienzle D., Bullone M., Gerber V., Ivester K., Lavoie J.P.. Equine Asthma: Current Understanding and Future Directions.. Front. Vet. Sci. 2020;7:450.
    doi: 10.3389/fvets.2020.00450pmc: PMC7438831pubmed: 32903600google scholar: lookup
  5. Davis K.U., Sheats M.K.. Differential gene expression and Ingenuity Pathway Analysis of bronchoalveolar lavage cells from horses with mild/moderate neutrophilic or mastocytic inflammation on BAL cytology.. Vet. Immunol. Immunopathol. 2021;234:110195.
    doi: 10.1016/j.vetimm.2021.110195pmc: PMC8132494pubmed: 33588285google scholar: lookup
  6. Simões J., Batista M., Tilley P.. The Immune Mechanisms of Severe Equine Asthma-Current Understanding and What Is Missing.. Animals 2022;12:744.
    doi: 10.3390/ani12060744pmc: PMC8944511pubmed: 35327141google scholar: lookup
  7. Leduc L., Leclère M., Lavoie J.P.. Towards personalized medicine for the treatment of equine asthma.. Vet. J. 2024;305:106125.
    doi: 10.1016/j.tvjl.2024.106125pubmed: 38704018google scholar: lookup
  8. Hughes K.J., Nicolson L., Da Costa N., Franklin S.H., Allen K.J., Dunham S.P.. Evaluation of cytokine mRNA expression in bronchoalveolar lavage cells from horses with inflammatory airway disease.. Vet. Immunol. Immunopathol. 2011;140:82–89.
    doi: 10.1016/j.vetimm.2010.11.018pubmed: 21194756google scholar: lookup
  9. Lavoie J.P., Cesarini C., Lavoie-Lamoureux A., Moran K., Lutz S., Picandet V., Jean D., Marcoux M.. Bronchoalveolar Lavage Fluid Cytology and Cytokine Messenger Ribonucleic Acid Expression of Racehorses with Exercise Intolerance and Lower Airway Inflammation.. J. Vet. Intern. Med. 2011;25:322–329.
    doi: 10.1111/j.1939-1676.2010.0664.xpubmed: 21281348google scholar: lookup
  10. Beekman L., Tohver T., Léguillette R.. Comparison of cytokine mRNA expression in the bronchoalveolar lavage fluid of horses with inflammatory airway disease and bronchoalveolar lavage mastocytosis or neutrophilia using REST software analysis.. J. Vet. Intern. Med./Am. Coll. Vet. Intern. Med. 2012;26:153–161.
    doi: 10.1111/j.1939-1676.2011.00847.xpubmed: 22168153google scholar: lookup
  11. Richard E.A., Depecker M., Defontis M., Leleu C., Fortier G., Pitel P.H., Courouce-Malblanc A.. Cytokine concentrations in bronchoalveolar lavage fluid from horses with neutrophilic inflammatory airway disease.. J. Vet. Intern. Med. 2014;28:1838–1844.
    doi: 10.1111/jvim.12464pmc: PMC4895612pubmed: 25269933google scholar: lookup
  12. Karagianni A.E., Kurian D., Cillán-Garcia E., Eaton S.L., Wishart T.M., Pirie R.S.. Training associated alterations in equine respiratory immunity using a multiomics comparative approach.. Sci. Rep. 2022;12:427.
    doi: 10.1038/s41598-021-04137-3pmc: PMC8748960pubmed: 35013475google scholar: lookup
  13. Bedenice D., Mazan M.R., Hoffman A.M.. Association between cough and cytology of bronchoalveolar lavage fluid and pulmonary function in horses diagnosed with inflammatory airway disease.. J. Vet. Intern. Med./Am. Coll. Vet. Intern. Med. 2008;22:1022–1028.
    doi: 10.1111/j.1939-1676.2008.0109.xpubmed: 18498325google scholar: lookup
  14. Couëtil L.L., Cardwell J.M., Gerber V., Lavoie J.P., Léguillette R., Richard E.A.. Inflammatory Airway Disease of Horses--Revised Consensus Statement.. J. Vet. Intern. Med. 2016;30:503–515.
    doi: 10.1111/jvim.13824pmc: PMC4913592pubmed: 26806374google scholar: lookup
  15. Lemonnier L.C., Couroucé A., Cessans M., Petit L., Cardwell J.M., Barbazanges P., Toquet M., Richard E.A.. Detection of fungi in the airways of horses according to the sample site: A methodological study.. Vet. Res. Commun. 2024;48:345–355.
    doi: 10.1007/s11259-023-10213-ypubmed: 37704768google scholar: lookup
  16. Kilkenny C., Browne W.J., Cuthill I.C., Emerson M., Altman D.G.. Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research.. PLoS Biol. 2010;8:e1000412.
    doi: 10.1371/journal.pbio.1000412pmc: PMC2893951pubmed: 20613859google scholar: lookup
  17. Depecker M., Richard E.A., Pitel P.-H., Fortier G., Leleu C., Couroucé-Malblanc A.. Bronchoalveolar lavage fluid in Standardbred racehorses: Influence of unilateral/bilateral profiles and cut-off values on lower airway disease diagnosis.. Vet. J. 2014;199:150–156.
    doi: 10.1016/j.tvjl.2013.10.013pubmed: 24225534google scholar: lookup
  18. Karagianni A.E., Kapetanovic R., McGorum B.C., Hume D.A., Pirie S.R.. The equine alveolar macrophage: Functional and phenotypic comparisons with peritoneal macrophages.. Vet. Immunol. Immunopathol. 2013;155:219–228.
    doi: 10.1016/j.vetimm.2013.07.003pmc: PMC3795452pubmed: 23978307google scholar: lookup
  19. Ewels P., Magnusson M., Lundin S., Kaller M.. MultiQC: Summarize analysis results for multiple tools and samples in a single report.. Bioinformatics 2016;32:3047–3048.
    doi: 10.1093/bioinformatics/btw354pmc: PMC5039924pubmed: 27312411google scholar: lookup
  20. Love M.I., Huber W., Anders S.. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol. 2014;15:550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  21. Ramery E., Fraipont A., Richard E.A., Art T., Pirottin D., van Delm W., Bureau F., Lekeux P.. Expression microarray as a tool to identify differentially expressed genes in horses suffering from inflammatory airway disease.. Vet. Clin. Pathol. 2015;44:37–46.
    doi: 10.1111/vcp.12216pubmed: 25488254google scholar: lookup
  22. Livak K.J., Schmittgen T.D.. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.. Methods 2001;25:402–408.
    doi: 10.1006/meth.2001.1262pubmed: 11846609google scholar: lookup
  23. Karagianni A.E., Eaton S.L., Kurian D., Cillán-Garcia E., Twynam-Perkins J., Raper A., Wishart T.M., Pirie R.S.. Application across species of a one health approach to liquid sample handling for respiratory based -omics analysis.. Sci. Rep. 2021;11:14292.
    doi: 10.1038/s41598-021-93839-9pmc: PMC8275668pubmed: 34253818google scholar: lookup
  24. Eaton S.L., Roche S.L., Llavero Hurtado M., Oldknow K.J., Farquharson C., Gillingwater T.H., Wishart T.M.. Total protein analysis as a reliable loading control for quantitative fluorescent Western blotting.. PLoS ONE 2013;8:e72457.
    doi: 10.1371/journal.pone.0072457pmc: PMC3758299pubmed: 24023619google scholar: lookup
  25. HaileMariam M., Eguez R.V., Singh H., Bekele S., Ameni G., Pieper R., Yu Y.. S-Trap, an Ultrafast Sample-Preparation Approach for Shotgun Proteomics.. J. Proteome Res. 2018;17:2917–2924.
    doi: 10.1021/acs.jproteome.8b00505pubmed: 30114372google scholar: lookup
  26. Aguilan J.T., Kulej K., Sidoli S.. Guide for protein fold change and p-value calculation for non-experts in proteomics.. Mol. Omics 2020;16:573–582.
    doi: 10.1039/D0MO00087Fpubmed: 32968743google scholar: lookup
  27. Huang D.W., Sherman B.T., Lempicki R.A.. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.. Nat. Protoc. 2009;4:44–57.
    doi: 10.1038/nprot.2008.211pubmed: 19131956google scholar: lookup
  28. Ogata H., Goto S., Sato K., Fujibuchi W., Bono H., Kanehisa M.. KEGG: Kyoto Encyclopedia of Genes and Genomes.. Nucleic Acids Res. 1999;27:29–34.
    doi: 10.1093/nar/27.1.29pmc: PMC148090pubmed: 9847135google scholar: lookup
  29. Sherman B.T., Hao M., Qiu J., Jiao X., Baseler M.W., Lane H.C., Imamichi T., Chang W.. DAVID: A web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res. 2022;50:W216–W221.
    doi: 10.1093/nar/gkac194pmc: PMC9252805pubmed: 35325185google scholar: lookup
  30. Kramer A., Green J., Pollard J., Jr., Tugendreich S.. Causal analysis approaches in Ingenuity Pathway Analysis.. Bioinformatics 2014;30:523–530.
    doi: 10.1093/bioinformatics/btt703pmc: PMC3928520pubmed: 24336805google scholar: lookup
  31. Karagianni A.E., Summers K.M., Couroucé A., Depecker M., McGorum B.C., Hume D.A., Pirie R.S.. The Effect of Race Training on the Basal Gene Expression of Alveolar Macrophages Derived from Standardbred Racehorses.. J. Equine Vet. Sci. 2019;75:48–54.
    doi: 10.1016/j.jevs.2019.01.010pubmed: 31002092google scholar: lookup
  32. Meyer K.C., Raghu G., Baughman R.P., Brown K.K., Costabel U., du Bois R.M., Drent M., Haslam P.L., Kim D.S., Nagai S.. An official American Thoracic Society clinical practice guideline: The clinical utility of bronchoalveolar lavage cellular analysis in interstitial lung disease.. Am. J. Respir. Crit. Care Med. 2012;185:1004–1014.
    doi: 10.1164/rccm.201202-0320STpubmed: 22550210google scholar: lookup
  33. Allen K.J., Tennant K.V., Franklin S.H.. Effect of inclusion or exclusion of epithelial cells in equine respiratory cytology analysis.. Vet. J. 2019;254:105405.
    doi: 10.1016/j.tvjl.2019.105405pubmed: 31836172google scholar: lookup
  34. Hinchcliff K.W., Couetil L.L., Knight P.K., Morley P.S., Robinson N.E., Sweeney C.R., van Erck E.. Exercise induced pulmonary hemorrhage in horses: American College of Veterinary Internal Medicine consensus statement.. J. Vet. Intern. Med. 2015;29:743–758.
    doi: 10.1111/jvim.12593pmc: PMC4895427pubmed: 25996660google scholar: lookup
  35. Baruah S., Murthy S., Keck K., Galvan I., Prichard A., Allen L.H., Farrelly M., Klesney-Tait J.. TREM-1 regulates neutrophil chemotaxis by promoting NOX-dependent superoxide production.. J. Leukoc. Biol. 2019;105:1195–1207.
    doi: 10.1002/JLB.3VMA0918-375Rpmc: PMC6708376pubmed: 30667543google scholar: lookup
  36. Bullone M., Lavoie J.P.. Asthma “of horses and men”—How can equine heaves help us better understand human asthma immunopathology and its functional consequences?. Mol. Immunol. 2015;66:97–105.
    doi: 10.1016/j.molimm.2014.12.005pubmed: 25547716google scholar: lookup
  37. Woodrow J.S., Hines M., Sommardahl C., Flatland B., Lo Y., Wang Z., Sheats M.K., Lennon E.M.. Initial investigation of molecular phenotypes of airway mast cells and cytokine profiles in equine asthma.. Front. Vet. Sci. 2022;9:997139.
    doi: 10.3389/fvets.2022.997139pmc: PMC9875299pubmed: 36713876google scholar: lookup
  38. Kuruvilla M.E., Lee F.E., Lee G.B.. Understanding Asthma Phenotypes, Endotypes, and Mechanisms of Disease.. Clin. Rev. Allergy Immunol. 2019;56:219–233.
    doi: 10.1007/s12016-018-8712-1pmc: PMC6411459pubmed: 30206782google scholar: lookup
  39. Ramery E., Closset R., Art T., Bureau F., Lekeux P.. Expression microarrays in equine sciences.. Vet. Immunol. Immunopathol. 2009;127:197–202.
    doi: 10.1016/j.vetimm.2008.10.314pubmed: 19027176google scholar: lookup
  40. Shim J.J., Dabbagh K., Ueki I.F., Dao-Pick T., Burgel P.R., Takeyama K., Tam D.C., Nadel J.A.. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils.. Am. J. Physiol. Lung Cell Mol. Physiol. 2001;280:L134–L140.
    doi: 10.1152/ajplung.2001.280.1.L134pubmed: 11133503google scholar: lookup
  41. Zu Y.-L., Qi J., Gilchrist A., Fernandez G.A., Vazquez-Abad D., Kreutzer D.L., Huang C.-K., Sha’afi R.I.. p38 Mitogen-Activated Protein Kinase Activation Is Required for Human Neutrophil Function Triggered by TNF-α or FMLP Stimulation.. J. Immunol. 1998;160:1982–1989.
    doi: 10.4049/jimmunol.160.4.1982pubmed: 9469462google scholar: lookup
  42. Vuoristo M.-S., Kellokumpu-Lehtinen P., Laine S., Soppi E.. Serum Levels of Interleukins 2, 6 and 8, Soluble Interleukin-2 Receptor and Intercellular Adhesion Molecule-1 During Treatment with Interleukin-2 Plus Interferon-Alfa.. Immunopharmacol. Immunotoxicol. 1996;18:337–354.
    doi: 10.3109/08923979609052740pubmed: 8872489google scholar: lookup
  43. Kaur R., Chupp G.. Phenotypes and endotypes of adult asthma: Moving toward precision medicine.. J. Allergy Clin. Immunol. 2019;144:1–12.
    doi: 10.1016/j.jaci.2019.05.031pubmed: 31277742google scholar: lookup
  44. Méndez-Enríquez E., Hallgren J.. Mast Cells and Their Progenitors in Allergic Asthma.. Front. Immunol. 2019;10:821.
    doi: 10.3389/fimmu.2019.00821pmc: PMC6548814pubmed: 31191511google scholar: lookup
  45. Varricchi G., Brightling C.E., Grainge C., Lambrecht B.N., Chanez P.. Airway remodelling in asthma and the epithelium: On the edge of a new era.. Eur. Respir. J. 2024;63:2301619.
    doi: 10.1183/13993003.01619-2023pmc: PMC11024394pubmed: 38609094google scholar: lookup
  46. Tsai M., Valent P., Galli S.J.. KIT as a master regulator of the mast cell lineage.. J. Allergy Clin. Immunol. 2022;149:1845–1854.
    doi: 10.1016/j.jaci.2022.04.012pmc: PMC9177781pubmed: 35469840google scholar: lookup
  47. Tran N.Q.V., Le M.-K., Nakamura Y., Kondo T., Nakao A.. A link between KIT expression, mast cell abundance and activity, and Th2-high endotype in asthmatic airways.. Allergy 2024;79:1338–1342.
    doi: 10.1111/all.15954pubmed: 37984459google scholar: lookup
  48. Michaeloudes C., Abubakar-Waziri H., Lakhdar R., Raby K., Dixey P., Adcock I.M., Mumby S., Bhavsar P.K., Chung K.F.. Molecular mechanisms of oxidative stress in asthma.. Mol. Asp. Med. 2022;85:101026.
    doi: 10.1016/j.mam.2021.101026pubmed: 34625291google scholar: lookup
  49. Murphy R.C., Hallstrand T.S.. Exploring the origin and regulatory role of mast cells in asthma.. Curr. Opin. Allergy Clin. Immunol. 2021;21:71–78.
    doi: 10.1097/ACI.0000000000000703pmc: PMC10038756pubmed: 33369571google scholar: lookup
  50. Dougherty R.H., Sidhu S.S., Raman K., Solon M., Solberg O.D., Caughey G.H., Woodruff P.G., Fahy J.V.. Accumulation of intraepithelial mast cells with a unique protease phenotype in T(H)2-high asthma.. J. Allergy Clin. Immunol. 2010;125:1046–1053.e1048.
    doi: 10.1016/j.jaci.2010.03.003pmc: PMC2918406pubmed: 20451039google scholar: lookup
  51. Chai O.H., Han E.H., Lee H.K., Song C.H.. Mast cells play a key role in Th2 cytokine-dependent asthma model through production of adhesion molecules by liberation of TNF-α.. Exp. Mol. Med. 2011;43:35–43.
    doi: 10.3858/emm.2011.43.1.004pmc: PMC3041936pubmed: 21169725google scholar: lookup
  52. Cahill K.N., Katz H.R., Cui J., Lai J., Kazani S., Crosby-Thompson A., Garofalo D., Castro M., Jarjour N., DiMango E.. KIT Inhibition by Imatinib in Patients with Severe Refractory Asthma.. N. Engl. J. Med. 2017;376:1911–1920.
    doi: 10.1056/NEJMoa1613125pmc: PMC5568669pubmed: 28514613google scholar: lookup
  53. Chelombitko M.A., Fedorov A.V., Ilyinskaya O.P., Zinovkin R.A., Chernyak B.V.. Role of Reactive Oxygen Species in Mast Cell Degranulation.. Biochemistry 2016;81:1564–1577.
    doi: 10.1134/S000629791612018Xpubmed: 28259134google scholar: lookup
  54. Hammad H., Lambrecht B.N.. The basic immunology of asthma.. Cell 2021;184:1469–1485.
    doi: 10.1016/j.cell.2021.02.016pubmed: 33711259google scholar: lookup
  55. Rasmussen S.M., Halvard Hansen E.S., Stensrud T., Radon K., Wolfarth B., Kurowski M., Bousquet J., Bonini S., Bonini M., Delgado L.. Asthma endotypes in elite athletes: A cross-sectional study of European athletes participating in the Olympic Games.. Allergy 2022;77:2250–2253.
    doi: 10.1111/all.15313pubmed: 35426975google scholar: lookup
  56. Frellstedt L., Gosset P., Kervoaze G., Hans A., Desmet C., Pirottin D., Bureau F., Lekeux P., Art T.. The innate immune response of equine bronchial epithelial cells is altered by training.. Vet. Res. 2015;46:3.
    doi: 10.1186/s13567-014-0126-3pmc: PMC4297379pubmed: 25595212google scholar: lookup
  57. Kippelen P., Anderson S.D.. Airway injury during high-level exercise.. Br. J. Sports Med. 2012;46:385–390.
    doi: 10.1136/bjsports-2011-090819pubmed: 22247295google scholar: lookup

Citations

This article has been cited 1 times.
  1. Jiang C, Wang X, Li R, Ni L, Liu X. Increased LOXL2 facilitates tissue remodeling in eosinophilic chronic rhinosinusitis with nasal polyps. World Allergy Organ J 2025 Oct;18(10):101126.
    doi: 10.1016/j.waojou.2025.101126pubmed: 41143091google scholar: lookup
Subscribe to our newsletter
Join 99,970 horse owners like you who receive our email updates on horse health and nutrition.