Profile of immune response during nasal challenge with dermatophagoides pteronyssinus in subjects with allergic airway diseases.

Allergy Asthma House dust mite Interleukin Nasal challenge Rhinitis

Journal

Journal of inflammation (London, England)

ISSN: 1476-9255

Titre abrégé: J Inflamm (Lond)

Pays: England

ID NLM: 101232234

Informations de publication

Date de publication:
31 Oct 2024

Historique:

received: 18 12 2023

accepted: 20 10 2024

medline: 1 11 2024

pubmed: 1 11 2024

entrez: 1 11 2024

Statut: epublish

Résumé

T lymphocyte helper (Th) 2 plays the main role in pathogenesis of allergic airway diseases (AAD). Recent studies showed that interleukin (IL) 33, Th17 and Th22 also may be involved in allergic inflammation. The aim is to evaluate cytokine level before and after nasal challenge with Dermatophagoides pteronyssinus in patients with AAD. Patients with persistent allergic rhinitis (AR) with or without allergic asthma (AA) allergic to house dust mite and healthy individuals underwent nasal challenge with Dermatophagoides pteronyssinus. Measurements of IL-13, IL-17, IL-22 and IL-33 in serum and nasal lavage were performed before, 2 and 22 h after nasal challenge by ELISA. . Ten patients with AR only, 6 patients with AR and AA and 7 healthy individuals were involved in the study. Serum IL-22 level significantly increased in patients with AR and AA and nasal lavage IL-22 tended to increase in patients with AAD after nasal challenge. Serum IL-13 level tended to increase in patients with AR and AA. IL-13 level in nasal lavage fluid decreased at 22 h after nasal challenge in patients with AR only. IL-17 level in serum and nasal lavage decreased in patients with AAD. Serum IL-33 tended to increase after nasal challenge whereas IL-33 in nasal lavage significantly decreased. Cytokine profile differs between local and systemic compartments and between patients with allergic rhinitis only and patients with allergic rhinitis and asthma after nasal challenge.

Sections du résumé

BACKGROUND BACKGROUND

METHODS METHODS

Patients with persistent allergic rhinitis (AR) with or without allergic asthma (AA) allergic to house dust mite and healthy individuals underwent nasal challenge with Dermatophagoides pteronyssinus. Measurements of IL-13, IL-17, IL-22 and IL-33 in serum and nasal lavage were performed before, 2 and 22 h after nasal challenge by ELISA.

RESULTS RESULTS

. Ten patients with AR only, 6 patients with AR and AA and 7 healthy individuals were involved in the study. Serum IL-22 level significantly increased in patients with AR and AA and nasal lavage IL-22 tended to increase in patients with AAD after nasal challenge. Serum IL-13 level tended to increase in patients with AR and AA. IL-13 level in nasal lavage fluid decreased at 22 h after nasal challenge in patients with AR only. IL-17 level in serum and nasal lavage decreased in patients with AAD. Serum IL-33 tended to increase after nasal challenge whereas IL-33 in nasal lavage significantly decreased.

CONCLUSION CONCLUSIONS

Cytokine profile differs between local and systemic compartments and between patients with allergic rhinitis only and patients with allergic rhinitis and asthma after nasal challenge.

Identifiants

DOI: 10.1186/s12950-024-00415-9 PMID: 39482718

pubmed: 39482718

doi: 10.1186/s12950-024-00415-9

pii: 10.1186/s12950-024-00415-9

doi:

Types de publication

Journal Article

Langues

eng

Pagination

Informations de copyright

Références

Global Initiative for Asthma. Global Strategy for Asthma Management and Prevention, 2023. Updated July 2023. www.ginasthma.org

Blaiss MS, Hammerby E, Robinson S, Kennedy-Martin T, Buchs S. The burden of allergic rhinitis and allergic rhinoconjunctivitis on adolescents: a literature review. Ann Allergy Asthma Immunol. 2018;121(1):43–e523.

pubmed: 29626629 doi: 10.1016/j.anai.2018.03.028

Meltzer EO. Allergic rhinitis: Burden of Illness, Quality of Life, Comorbidities, and control. Immunol Allergy Clin North Am. 2016;36(2):235–48.

pubmed: 27083099 doi: 10.1016/j.iac.2015.12.002

Lee LK, Obi E, Paknis B, Kavati A, Chipps B. Asthma control and disease burden in patients with asthma and allergic comorbidities. J Asthma. 2018;55(2):208–19.

pubmed: 28586296 doi: 10.1080/02770903.2017.1316394

Broek JL, Bousquet J, Baena-Cagnani CE, Bonini S, Canonica GW, Casale TB, et al. Allergic Rhinitis and its impact on Asthma (ARIA) guidelines: 2010 revision. J Allergy Clin Immunol. 2010;126(3):466–76.

doi: 10.1016/j.jaci.2010.06.047

Passali D, Cingi C, Staffa P, Passali F, Muluk NB, Bellussi ML. The International Study of the allergic Rhinitis Survey: outcomes from 4 geographical regions. 2018;8(1):1–15.

Akdis CA, Hellings PW, Agache I. Global atlas of allergic rhinitis and chronic rhinosinusitis. Eur Acad Allergy Clin Immunol. 2015.

Hellings PW, Klimek L, Cingi C, Agache I, Akdis C, Bachert C, et al. Non-allergic rhinitis: position paper of the European Academy of Allergy and Clinical Immunology. Allergy Eur J Allergy Clin Immunol. 2017;72(11):1657–65.

doi: 10.1111/all.13200

Global Initiative for Asthma. Global Strategy for Asthma Management and Prevention. 2020. www.ginasthma.org

Valls-Mateus M, Marino-Sanchez F, Ruiz-Echevarría K, Cardenas-Escalante P, Jiménez-Feijoo R, Blasco-Lozano J, et al. Nasal obstructive disorders impair health-related quality of life in adolescents with persistent allergic rhinitis: a real-life study. Pediatr Allergy Immunol. 2017;28(5):438–45.

pubmed: 28423474 doi: 10.1111/pai.12724

Maspero J, Lee BW, Katelaris CH, Potter PC, Cingi C, Lopatin A, et al. Quality of life and control of allergic rhinitis in patients from regions beyond western Europe and the United States. Clin Exp Allergy. 2012;42(12):1684–96.

pubmed: 23181786 doi: 10.1111/j.1365-2222.2012.04025.x

Annunziato F, Romagnani C, Romagnani S. The 3 major types of innate and adaptive cell-mediated effector immunity. J Allergy Clin Immunol. 2015;135(3):626–35.

pubmed: 25528359 doi: 10.1016/j.jaci.2014.11.001

Hong H, Liao S, Chen F, Yang Q, Wang D-Y. Role of IL-25, IL-33, and TSLP in triggering united airway diseases toward type 2 inflammation. Allergy. 2020;75(11):2794–804.

pubmed: 32737888 doi: 10.1111/all.14526

De Greve G, Hellings PW, Fokkens WJ, Pugin B, Steelant B, Seys SF. Endotype-driven treatment in chronic upper airway diseases. Clin Transl Allergy. 2017;7:22.

pubmed: 28706720 pmcid: 5506670 doi: 10.1186/s13601-017-0157-8

Giavina-Bianchi P, Aun MV, Takejima P, Kalil J, Agondi RC. United airway disease: current perspectives. J Asthma Allergy. 2016;9:93–100.

pubmed: 27257389 pmcid: 4872272 doi: 10.2147/JAA.S81541

Licari A, Castagnoli R, Denicolò CF, Rossini L, Marseglia A, Marseglia GL. The nose and the lung: United Airway Disease? Front Pediatr. 2017;5:44.

pubmed: 28316969 pmcid: 5334318 doi: 10.3389/fped.2017.00044

Augé J, Vent J, Agache I, Airaksinen L, Campo Mozo P, Chaker A, et al. EAACI position paper on the standardization of nasal allergen challenges. Allergy. 2018;73(8):1597–608.

pubmed: 29377177 doi: 10.1111/all.13416

Doran E, Cai F, Holweg CTJ, Wong K, Brumm J, Arron JR. Interleukin-13 in Asthma and other Eosinophilic disorders. Front Med. 2017;4:139.

doi: 10.3389/fmed.2017.00139

Gour N, Wills-Karp M. IL-4 and IL-13 signaling in allergic airway disease. Cytokine. 2015;75(1):68–78.

pubmed: 26070934 pmcid: 4532591 doi: 10.1016/j.cyto.2015.05.014

Marone G, Granata F, Pucino V, Pecoraro A, Heffler E, Loffredo S, et al. The Intriguing Role of Interleukin 13 in the pathophysiology of Asthma. Front Pharmacol. 2019;10:1387.

pubmed: 31866859 pmcid: 6908970 doi: 10.3389/fphar.2019.01387

Bagnasco D, Ferrando M, Varricchi G, Passalacqua G, Canonica GW. A critical evaluation of Anti-IL-13 and Anti-IL-4 strategies in severe asthma. Int Arch Allergy Immunol. 2016;170(2):122–31.

pubmed: 27637004 doi: 10.1159/000447692

Matsunaga MC, Yamauchi PS. IL-4 and IL-13 inhibition in atopic dermatitis. J Drugs Dermatol. 2016;15(8):925–9.

pubmed: 27537991

Baumann R, Rabaszowski M, Stenin I, Gaertner-Akerboom M, Scheckenbach K, Wiltfang J, et al. The release of IL-31 and IL-13 after nasal allergen challenge and their relation to nasal symptoms. Clin Transl Allergy. 2012;2(1):13.

pubmed: 22853438 pmcid: 3509028 doi: 10.1186/2045-7022-2-13

Alasandagutti ML, Ansari MSS, Sagurthi SR, Valluri V, Gaddam S. Role of IL-13 genetic variants in Signalling of Asthma. Inflammation. 2017;40(2):566–77.

pubmed: 28083766 doi: 10.1007/s10753-016-0503-3

Berry MA, Parker D, Neale N, Woodman L, Morgan A, Monk P, et al. Sputum and bronchial submucosal IL-13 expression in asthma and eosinophilic bronchitis. J Allergy Clin Immunol. 2004;114(5):1106–9.

pubmed: 15536417 doi: 10.1016/j.jaci.2004.08.032

Prieto J, Lensmar C, Roquet A, van der Ploeg I, Gigliotti D, Eklund A, et al. Increased interleukin-13 mRNA expression in bronchoalveolar lavage cells of atopic patients with mild asthma after repeated low-dose allergen provocations. Respir Med. 2000;94(8):806–14.

pubmed: 10955758 doi: 10.1053/rmed.2000.0826

Kalinauskaite-Zukauske V, Janulaityte I, Januskevicius A, Malakauskas K. Serum levels of epithelial-derived mediators and interleukin-4/interleukin-13 signaling after bronchial challenge with Dermatophagoides pteronyssinus in patients with allergic asthma. Scand J Immunol. 2019;90(5):e12820.

pubmed: 31486098 doi: 10.1111/sji.12820

Campion NJ, Villazala-Merino S, Thwaites RS, Stanek V, Killick H, Pertsinidou E et al. Nasal IL-13 production identifies patients with late-phase allergic responses. J Allergy Clin Immunol. 2023;1:S0091-6749(23)00971-5.

Erin EM, Leaker BR, Zacharasiewicz AS, Higgins LA, Williams TJ, Boyce MJ, et al. Single dose topical corticosteroid inhibits IL-5 and IL-13 in nasal lavage following grass pollen challenge. Allergy. 2005;60(12):1524–9.

pubmed: 16266385 doi: 10.1111/j.1398-9995.2005.00928.x

Kamali AN, Noorbakhsh SM, Hamedifar H, Jadidi-Niaragh F, Yazdani R, Bautista JM, et al. A role for Th1-like Th17 cells in the pathogenesis of inflammatory and autoimmune disorders. Mol Immunol. 2019;105:107–15.

pubmed: 30502718 doi: 10.1016/j.molimm.2018.11.015

Maddur MS, Miossec P, Kaveri SV, Bayry J. Th17 cells: Biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol. 2012;181(1):8–18.

pubmed: 22640807 doi: 10.1016/j.ajpath.2012.03.044

Bae JS, Kim JH, Kim EH, Mo JH. The role of IL-17 in a Lipopolysaccharide-Induced Rhinitis Model. Allergy Asthma Immunol Res. 2017;9(2):169–76.

pubmed: 28102062 pmcid: 5266111 doi: 10.4168/aair.2017.9.2.169

Ricciardolo FLM, Sorbello V, Folino A, Gallo F, Massaglia GM, Favatà G, et al. Identification of IL-17F/frequent exacerbator endotype in asthma. J Allergy Clin Immunol. 2017;140(2):395–406.

pubmed: 27931975 doi: 10.1016/j.jaci.2016.10.034

Jirmo AC, Busse M, Happle C, Skuljec J, Dalüge K, Habener A, et al. IL-17 regulates DC migration to the peribronchial LNs and allergen presentation in experimental allergic asthma. Eur J Immunol. 2020;50(7):1019–33.

pubmed: 32142593 doi: 10.1002/eji.201948409

Chen JH, Qin L, Shi YY, Feng JT, Zheng YL, Wan YF, et al. IL-17 protein levels in both induced sputum and plasma are increased in stable but not acute asthma individuals with obesity. Respir Med. 2016;121:48–58.

pubmed: 27888992 doi: 10.1016/j.rmed.2016.10.018

Bullone M, Carriero V, Bertolini F, Folino A, Mannelli A, Stefano A, Di, et al. Elevated serum IgE, oral corticosteroid dependence and IL-17/22 expression in highly neutrophilic asthma. Eur Respir J. 2019;54(5):1900068.

pubmed: 31439682 doi: 10.1183/13993003.00068-2019

Amin K, Issa SM, Ali KM, Aziz MI, Hama Amieen HM, Bystrom J et al. Evidence for eosinophil and IL-17 mediated inflammation in allergic rhinitis. Clin Mol Allergy. 2020.

Degirmenci PB, Aksun S, Altin Z, Bilgir F, Arslan IB, Colak H, et al. Allergic rhinitis and its relationship with IL-10, IL-17, TGF-β, IFN-γ, IL 22, and IL-35. Dis Markers. 2018;18:6.

Erkan K, Bozkurt MK, Artaç H, Özdemir H, Ünlü A, Korucu EN, et al. The role of regulatory T cells in allergic rhinitis and their correlation with IL-10, IL-17 and neopterin levels in serum and nasal lavage fluid. Eur Arch Oto-Rhino-Laryngology. 2020;277(4):1109–14.

doi: 10.1007/s00405-020-05811-4

Baumann R, Rabaszowski M, Stenin I, Tilgner L, Scheckenbach K, Wiltfang J, et al. Comparison of the nasal release of IL-4, IL-10, IL-17, CCL13/MCP-4, and CCL26/eotaxin-3 in allergic rhinitis during season and after allergen challenge. Am J Rhinol Allergy. 2013;27(4):266–72.

pubmed: 23883806 doi: 10.2500/ajra.2013.27.3913

Ramezanpour M, Moraitis S, Smith JL, Wormald PJ, Vreugde S. Th17 cytokines disrupt the Airway Mucosal Barrier in Chronic Rhinosinusitis. Mediators Inflamm. 2016;2016:9798206.

pubmed: 26903715 pmcid: 4745600 doi: 10.1155/2016/9798206

Foray AP, Dietrich C, Pecquet C, Machavoine F, Chatenoud L, Leite-de-Moraes M. IL-4 and IL-17 are required for House Dust Mite-Driven Airway Hyperresponsiveness in Autoimmune Diabetes-Prone non-obese Diabetic mice. Front Immunol. 2021;11:595003.

pubmed: 33643284 pmcid: 7904896 doi: 10.3389/fimmu.2020.595003

Murrison LB, Brandt EB, Myers JB, Khurana Hershey GK. Environmental exposures and mechanisms in allergy and asthma development. J Clin Invest. 2019;129(4):1504–15.

pubmed: 30741719 pmcid: 6436881 doi: 10.1172/JCI124612

Baumann R, Rabaszowski M, Stenin I, Tilgner L, Gaertner-Akerboom M, Scheckenbach K, et al. Nasal levels of soluble IL-33R ST2 and IL-16 in allergic rhinitis: inverse correlation trends with disease severity. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2013;43(10):1134–43.

doi: 10.1111/cea.12148

Fang P, Zhou L, Zhou Y, Kolls JK, Zheng T, Zhu Z. Immune modulatory effects of IL-22 on allergen-induced pulmonary inflammation. PLoS ONE. 2014;9(9):e107454.

pubmed: 25254361 pmcid: 4177833 doi: 10.1371/journal.pone.0107454

Taube C, Tertilt C, Gyülveszi G, Dehzad N, Kreymborg K, Schneeweiss K, et al. IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS ONE. 2011;6(7):e21799.

pubmed: 21789181 pmcid: 3138740 doi: 10.1371/journal.pone.0021799

Besnard A-G, Sabat R, Dumoutier L, Renauld J-C, Willart M, Lambrecht B, et al. Dual role of IL-22 in allergic airway inflammation and its cross-talk with IL-17A. Am J Respir Crit Care Med. 2011;183(9):1153–63.

pubmed: 21297073 doi: 10.1164/rccm.201008-1383OC

Hakemi M, Eskandari N, Yazdani R, Farahani R, Sherkat R. Cytokines (interleukin-9, IL-17, IL-22, IL-25 and IL-33) and asthma. Adv Biomed Res. 2014;3:127.

pubmed: 24949298 pmcid: 4063088 doi: 10.4103/2277-9175.133249

Shahsavan S, Pirayesh A, Samani OZ, Shirzad H, Zamani MA, Amani S, et al. The relationship between IL-17A and IL-22 expression and clinical severity in patients with moderate/severe persistent allergic rhinitis. Am J Otolaryngol - Head Neck Med Surg. 2019;40(2):173–8.

Zhu J, Cao Y, Li K, Wang Z, Zuo P, Xiong W, et al. Increased expression of aryl hydrocarbon receptor and interleukin 22 in patients with allergic asthma. Asian Pac J Allergy Immunol. 2011;29(3):266–72.

pubmed: 22053597

Zhao Y, Yang J, Gao YD, Guo W. Th17 immunity in patients with allergic asthma. Int Arch Allergy Immunol. 2010;151(4):297–307.

pubmed: 19844129 doi: 10.1159/000250438

Farfariello V, Amantini C, Nabissi M, Morelli MB, Aperio C, Caprodossi S, et al. IL-22 mRNA in peripheral blood mononuclear cells from allergic rhinitic and asthmatic pediatric patients. Pediatr Allergy Immunol. 2011;22(4):419–23.

pubmed: 21535180 doi: 10.1111/j.1399-3038.2010.01116.x