Key role of the epithelium in chronic upper airways diseases.
Allergic rhinitis
chronic rhinitis
respiratory epithelium
Journal
Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology
ISSN: 1365-2222
Titre abrégé: Clin Exp Allergy
Pays: England
ID NLM: 8906443
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
16
08
2019
revised:
15
11
2019
accepted:
15
11
2019
pubmed:
21
11
2019
medline:
10
6
2021
entrez:
21
11
2019
Statut:
ppublish
Résumé
The respiratory epithelium of the upper airways is a first-line defence against inhaled irritants, pathogens and allergens. It ensures a physical barrier provided by apical junctions and mucociliary clearance to avoid excessive activation of the immune system. The epithelium also forms a chemical and immunological barrier, extensively equipped to protect the airways against external aggressions before the adaptive immune system is required. Under normal circumstances, the epithelium is capable of recovering rapidly after damage. This manuscript reviews these main properties of the upper airway epithelium as well as its reported impairments in chronic inflammatory diseases. The knowledge on normal epithelial functions and their dysregulation in upper airway diseases should help to design new epithelial-targeted treatments.
Substances chimiques
Allergens
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
135-146Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Meltzer EO. Quality of life in adults and children with allergic rhinitis. J Allergy Clin Immunol. 2001;108(1 Suppl):S45-53.
Schmitt J, Stadler E, Kuster D, Wustenberg EG. Medical care and treatment of allergic rhinitis: A population-based cohort study based on routine healthcare utilization data. Allergy. 2016;71(6):850-858.
Ozdoganoglu T, Songu M. The burden of allergic rhinitis and asthma. Ther Adv Respir Dis. 2012;6(1):11-23.
Hastan D, Fokkens WJ, Bachert C, et al. Chronic rhinosinusitis in Europe-an underestimated disease. A GA(2)LEN study. Allergy. 2011;66(9):1216-1223.
Rudmik L. Economics of Chronic Rhinosinusitis. Curr Allergy Asthma Rep. 2017;17(4):20.
Pawankar R. Allergic rhinitis and asthma: are they manifestations of one syndrome? Clinical Exp Allergy. 2006;36(1):1-4.
Fokkens WJ, Lund VJ, Mullol J, et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. Rhinology. 2012;50(1):1-12.
Bachert C, Van Bruaene N, Toskala E, et al. Important research questions in allergy and related diseases: 3-chronic rhinosinusitis and nasal polyposis - a GALEN study. Allergy. 2009;64(4):520-533.
Tomassen P, Vandeplas G, Van Zele T, et al. Inflammatory endotypes of chronic rhinosinusitis based on cluster analysis of biomarkers. J Allergy Clin Immunol. 2016;137(5): 1449-1456.e4.
Knight DA, Holgate ST. The airway epithelium: Structural and functional properties in health and disease. Respirology. 2003;8(4):432-446.
Rock JR, Randell SH, Hogan BL. Airway basal stem cells: A perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech. 2010;3(9-10):545-556.
Gohy ST, Hupin C, Pilette C, Ladjemi MZ. Chronic inflammatory airway diseases: the central role of the epithelium revisited. Clinical Exp Allergy. 2016;46(4):529-542.
Finger TE, Bottger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL. Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA. 2003;100(15):8981-8986.
Kohanski MA, Workman AD, Patel NN, et al. Solitary chemosensory cells are a primary epithelial source of IL-25 in patients with chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol. 2018;142(2):pp. 460-469 e467.
Lee RJ, Kofonow JM, Rosen PL, et al. Bitter and sweet taste receptors regulate human upper respiratory innate immunity. J Clin Investig. 2014;124(3):1393-1405.
Holgate ST. Epithelium dysfunction in asthma. Journal of Allergy and Clinical Immunology. 2007;120(6):1233-1244.
Ordovas-Montanes J, Dwyer DF, Nyquist SK, et al. Allergic inflammatory memory in human respiratory epithelial progenitor cells. Nature. 2018;560(7720):649-654.
Gohy SHC, Fregimilika C, Detry B. Bouzin C, Gaide Chevronnay H, Lecocs M, Weynand B, Ladjemi MZ, Pierreux C, Brienmbaut P, Polette M and Pilette C. Imprinting of the COPD airway epithelium for dedifferentiation and mesenchymal transition. The European respiratory journal. 2014:Accepted.
Shin H-W, Cho K, Kim DW, et al. Hypoxia-inducible factor 1 mediates nasal polypogenesis by inducing epithelial-to-mesenchymal transition. Am J Respir Crit Care Med. 2012;185(9):944-954.
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.
Hallstrand TS, Hackett TL, Altemeier WA, Matute-Bello G, Hansbro PM, Knight DA. Airway epithelial regulation of pulmonary immune homeostasis and inflammation. Clin Immunol. 2014;151(1):1-15.
Suzuki H, Nishizawa T, Tani K, et al. Crystal structure of a claudin provides insight into the architecture of tight junctions. Science. 2014;344(6181):304-307.
Schneeberger EE, Lynch RD. The tight junction: A multifunctional complex. Am J Physiol Cell Physiol. 2004;286(6):C1213-1228.
Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2001;2(4):285-293.
Ganesan S, Comstock AT, Sajjan US. Barrier function of airway tract epithelium. Tissue barriers. 2013;1(4):e24997.
Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR. E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. The EMBO journal. 2004;23(8):1739-1748.
Gottardi CJ, Gumbiner BM. Distinct molecular forms of beta-catenin are targeted to adhesive or transcriptional complexes. J Cell Biol. 2004;167(2):339-349.
Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med. 2008;178(12):1271-1281.
Kim JY, Sajjan US, Krasan GP, LiPuma JJ. Disruption of tight junctions during traversal of the respiratory epithelium by Burkholderia cenocepacia. Infect Immun. 2005;73(11):7107-7112.
Runswick S, Mitchell T, Davies P, Robinson C, Garrod DR. Pollen proteolytic enzymes degrade tight junctions. Respirology. 2007;12(6):834-842.
Lee H-J, Kim B, Im N-R, et al. Decreased expression of E-cadherin and ZO-1 in the nasal mucosa of patients with allergic rhinitis: Altered regulation of E-cadherin by IL-4, IL-5, and TNF-alpha. Am J Rhinol Allergy. 2016;30(3):173-178.
Steelant B, Farré R, Wawrzyniak P, et al. Impaired barrier function in patients with house dust mite-induced allergic rhinitis is accompanied by decreased occludin and zonula occludens-1 expression. J Allergy Clin Immunol. 2016;137(4): 1043-1053.e5.
Henriquez OA, Den Beste K, Hoddeson EK, Parkos CA, Nusrat A, Wise SK. House dust mite allergen Der p 1 effects on sinonasal epithelial tight junctions. International forum of allergy & rhinology. 2013;3(8):630-635.
Meng J, Zhou P, Liu Y, et al. The development of nasal polyp disease involves early nasal mucosal inflammation and remodelling. PLoS ONE. 2013;8(12):e82373.
Soyka MB, Wawrzyniak P, Eiwegger T, et al. Defective epithelial barrier in chronic rhinosinusitis: The regulation of tight junctions by IFN-gamma and IL-4. J Allergy Clin Immunol. 2012;130(5):1087-1096 e10.
Zuckerman JD, Lee WY, DelGaudio JM, et al. Pathophysiology of nasal polyposis: The role of desmosomal junctions. American journal of rhinology. 2008;22(6):589-597.
Sánchez de Medina F, Romero-Calvo I, Mascaraque C, Martinez-Augustin O. Intestinal inflammation and mucosal barrier function. Inflamm Bowel Dis. 2014;20(12):2394-2404.
Han H, Roan F, Ziegler SF. The atopic march: Current insights into skin barrier dysfunction and epithelial cell-derived cytokines. Immunol Rev. 2017;278(1):116-130.
Loxham M, Davies DE. Phenotypic and genetic aspects of epithelial barrier function in asthmatic patients. J Allergy Clin Immunol. 2017;139(6):1736-1751.
Grainge CL, Davies DE. Epithelial injury and repair in airways diseases. Chest. 2013;144(6):1906-1912.
Erjefalt JS, Erjefalt I, Sundler F, Persson CG. In vivo restitution of airway epithelium. Cell Tissue Res. 1995;281(2):305-316.
Puchelle E, Zahm JM, Tournier JM, Coraux C. Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2006;3(8):726-733.
Rock JR, Onaitis MW, Rawlins EL, et al. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA. 2009;106(31):12771-12775.
Lazard DS, Moore A, Hupertan V, et al. Muco-ciliary differentiation of nasal epithelial cells is decreased after wound healing in vitro. Allergy. 2009;64(8):1136-1143.
Valera FCP, Ruffin M, Adam D, et al. Staphylococcus aureus impairs sinonasal epithelial repair: Effects in patients with chronic rhinosinusitis with nasal polyps and control subjects. J Allergy Clin Immunol. 2019;143(2):pp. 591-603 e593.
Mynatt RG, Do J, Janney C, Sindwani R. Squamous metaplasia and chronic rhinosinusitis: A clinicopathological study. American journal of rhinology. 2008;22(6):602-605.
Yee KK, Pribitkin EA, Cowart BJ, et al. Smoking-associated squamous metaplasia in olfactory mucosa of patients with chronic rhinosinusitis. Toxicol Pathol. 2009;37(5):594-598.
Vachier I, Vignola AM, Chiappara G, et al. Inflammatory features of nasal mucosa in smokers with and without COPD. Thorax. 2004;59(4):303-307.
Staudt MR, Buro-Auriemma LJ, Walters MS, et al. Airway Basal stem/progenitor cells have diminished capacity to regenerate airway epithelium in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;190(8):955-958.
Pain M, Bermudez O, Lacoste P, et al. Tissue remodelling in chronic bronchial diseases: From the epithelial to mesenchymal phenotype. Eur Respir Rev. 2014;23(131):118-130.
Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest. 2003;112(12):1776-1784.
Hupin C, Gohy S, Bouzin C, Lecocq M, Polette M, Pilette C. Features of mesenchymal transition in the airway epithelium from chronic rhinosinusitis. Allergy. 2014;69(11):1540-1549.
Lee M, Kim DW, Yoon H, et al. Sirtuin 1 attenuates nasal polypogenesis by suppressing epithelial-to-mesenchymal transition. J Allergy Clin Immunol. 2016;137(1): 87-98.e7.
Tyner JW, Kim EY, Ide K, et al. Blocking airway mucous cell metaplasia by inhibiting EGFR antiapoptosis and IL-13 transdifferentiation signals. J Clin Investig. 2006;116(2):309-321.
Li CW, Shi LI, Zhang KK, et al. Role of p63/p73 in epithelial remodeling and their response to steroid treatment in nasal polyposis. J Allergy Clin Immunol. 2011;127(3): 765-772.e2.
Ding GQ, Zheng CQ. The expression of MUC5AC and MUC5B mucin genes in the mucosa of chronic rhinosinusitis and nasal polyposis. American journal of rhinology. 2007;21(3):359-366.
Du J, Ba L, Li BO, et al. Distinct expression of NK2 homeobox 1 (NKX2-1) and goblet cell hyperplasia in nasal polyps with different endotypes. Int Forum Allergy Rhinol. 2017;7(7):690-698.
Widdicombe JH, Widdicombe JG. Regulation of human airway surface liquid. Respir Physiol. 1995;99(1):3-12.
Al-Rawi MM, Edelstein DR, Erlandson RA. Changes in nasal epithelium in patients with severe chronic sinusitis: A clinicopathologic and electron microscopic study. The Laryngoscope. 1998;108(12):1816-1823.
Li YY, Li CW, Chao SS, et al. Impairment of cilia architecture and ciliogenesis in hyperplastic nasal epithelium from nasal polyps. J Allergy Clin Immunol. 2014;134(6):1282-1292.
Rose MC, Voynow JA. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev. 2006;86(1):245-278.
Fahy JV, Dickey BF. Airway mucus function and dysfunction. N Engl J Med. 2010;363(23):2233-2247.
Corfield AP. Mucins: A biologically relevant glycan barrier in mucosal protection. Biochem Biophys Acta. 2014;1850(1):236-252.
Burgel P-R, Escudier E, Coste A, et al. Relation of epidermal growth factor receptor expression to goblet cell hyperplasia in nasal polyps. J Allergy Clin Immunol. 2000;106(4):705-712.
Martinez-Anton A, deBolos C, Garrido M, et al. Mucin genes have different expression patterns in healthy and diseased upper airway mucosa. Clin Exp Allergy. 2006;36(4):448-457.
Cole AM, Liao HI, Stuchlik O, Tilan J, Pohl J, Ganz T. Cationic polypeptides are required for antibacterial activity of human airway fluid. J Immunol. 2002;169(12):6985-6991.
Kalfa VC, Spector SL, Ganz T, Cole AM. Lysozyme levels in the nasal secretions of patients with perennial allergic rhinitis and recurrent sinusitis. Ann Allergy Asthma Immunol. 2004;93(3):288-292.
Psaltis AJ, Bruhn MA, Ooi EH, Tan LW, Wormald PJ. Nasal mucosa expression of lactoferrin in patients with chronic rhinosinusitis. Laryngoscope. 2007;117(11):2030-2035.
Fukami M, Stierna P, Veress B, Carlsoo B. Lysozyme and lactoferrin in human maxillary sinus mucosa during chronic sinusitis. An immunohistochemical study. Eur Arch Otorhinolaryngology. 1993;250(3):133-139.
Woods CM, Lee VS, Hussey DJ, et al. Lysozyme expression is increased in the sinus mucosa of patients with chronic rhinosinusitis. Rhinology. 2012;50(2):147-156.
Wei YI, Xia W, Ye X, et al. The antimicrobial protein short palate, lung, and nasal epithelium clone 1 (SPLUNC1) is differentially modulated in eosinophilic and noneosinophilic chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol. 2014;133(2):420-428.
Sallenave JM. Secretory leukocyte protease inhibitor and elafin/trappin-2: Versatile mucosal antimicrobials and regulators of immunity. Am J Respir Cell Mol Biol. 2010;42(6):635-643.
Hiemstra PS, Maassen RJ, Stolk J, Heinzel-Wieland R, Steffens GJ, Dijkman JH. Antibacterial activity of antileukoprotease. Infect Immun. 1996;64(11):4520-4524.
Xu W, He B, Chiu A, et al. Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat Immunol. 2007;8(3):294-303.
Samsom JN, van der Marel APJ, van Berkel LA, et al. Secretory leukoprotease inhibitor in mucosal lymph node dendritic cells regulates the threshold for mucosal tolerance. Journal of immunology. 2007;179(10):6588-6595.
Tomazic PV, Birner-Gruenberger R, Leitner A, Obrist B, Spoerk S, Lang-Loidolt D. Nasal mucus proteomic changes reflect altered immune responses and epithelial permeability in patients with allergic rhinitis. Journal of Allergy and Clinical Immunology. 2014;133(3):741-750.
Westin U, Lundberg E, Wihl JA, Ohlsson K. The effect of immediate-hypersensitivity reactions on the level of SLPI, granulocyte elastase, alpha1-antitrypsin, and albumin in nasal secretions, by the method of unilateral antigen challenge. Allergy. 1999;54(8):857-864.
Dong D, Yulin Z, Yan X, Hongyan Z, Shitao Z, Jia W. Enhanced expressions of lysozyme, SLPI and glycoprotein 340 in biofilm-associated chronic rhinosinusitis. Eur Arch Otorhinolaryngology. 2014;271(6):1563-1571.
Williams SE, Brown TI, Roghanian A, Sallenave JM. SLPI and elafin: One glove, many fingers. Clin Sci. 2006;110(1):21-35.
Tieu DD, Kern RC, Schleimer RP. Alterations in epithelial barrier function and host defense responses in chronic rhinosinusitis. J Allergy Clin Immunol. 2009;124(1):37-42.
Perez-Novo CA, Watelet JB, Claeys C, Van Cauwenberge P, Bachert C. Prostaglandin, leukotriene, and lipoxin balance in chronic rhinosinusitis with and without nasal polyposis. J Allergy Clin Immunol. 2005;115(6):1189-1196.
Holgate ST, Peters-Golden M, Panettieri RA, Henderson WR. Roles of cysteinyl leukotrienes in airway inflammation, smooth muscle function, and remodeling. J Allergy Clin Immunol. 2003;111(1):S18-S36.
Barnes PJ. Mediators of chronic obstructive pulmonary disease. Pharmacol Rev. 2004;56(4):515-548.
Shimizu S, Ogawa T, Seno S, Kouzaki H, Shimizu T. Pro-resolution mediator lipoxin A4 and its receptor in upper airway inflammation. Ann Otol Rhinol Laryngol. 2013;122(11):683-689.
Kowalski ML, Agache I, Bavbek S, et al. Diagnosis and management of NSAID-exacerbated respiratory disease (N-ERD)-a EAACI position paper. Allergy. 2019;74(1):28-39.
Steelant B, Seys SF, Van Gerven L, et al. Histamine and T helper cytokine-driven epithelial barrier dysfunction in allergic rhinitis. J Allergy Clin Immunol. 2018;141(3): 951-963.e8.
Nagarkar DR, Poposki JA, Tan BK, et al. Thymic stromal lymphopoietin activity is increased in nasal polyps of patients with chronic rhinosinusitis. J Allergy Clin Immunol. 2013;132(3): 593-600.e12.
Lam M, Hull L, Imrie A, et al. Interleukin-25 and interleukin-33 as mediators of eosinophilic inflammation in chronic rhinosinusitis. Am J Rhinol Allergy. 2015;29(3):175-181.
Lund S, Walford HH, Doherty TA. Type 2 Innate Lymphoid Cells in Allergic Disease. Curr Immunol Rev. 2013;9(4):214-221.
Liu T, Zhao F, Xie C, et al. Role of thymic stromal lymphopoietin in the pathogenesis of nasal polyposis. Am J Med Sci. 2011;341(1):40-47.
Soumelis V, Reche PA, Kanzler H, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 2002;3(7):673-680.
Kamekura R, Kojima T, Koizumi J-I, et al. Thymic stromal lymphopoietin enhances tight-junction barrier function of human nasal epithelial cells. Cell Tissue Res. 2009;338(2):283-293.
Talabot-Ayer D, Lamacchia C, Gabay C, Palmer G. Interleukin-33 is biologically active independently of caspase-1 cleavage. J Biol Chem. 2009;284(29):19420-19426.
Song W, Wang C, Zhou J, Pan S, Lin S. IL-33 Expression in chronic rhinosinusitis with nasal polyps and its relationship with clinical severity. ORL J.Otorhinolaryngol Relat Spec. 2017;79(6):323-330.
Kim D-K, Jin HR, Eun KM, et al. The role of interleukin-33 in chronic rhinosinusitis. Thorax. 2017;72(7):635-645.
Chen F, Hong H, Sun Y, et al. Nasal interleukin 25 as a novel biomarker for patients with chronic rhinosinusitis with nasal polyps and airway hypersensitiveness: A pilot study. Ann Allergy Asthma Immunol. 2017;119(4): 310-316.e2.
Hong H, Chen F, Sun Y, et al. Nasal IL-25 predicts the response to oral corticosteroids in chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol. 2018;141(5):1890-1892.
Fantuzzi G, Dinarello CA. Interleukin-18 and interleukin-1 beta: Two cytokine substrates for ICE (caspase-1). J Clin Immunol. 1999;19(1):1-11.
Verhaeghe B, Gevaert P, Holtappels G, et al. Up-regulation of IL-18 in allergic rhinitis. Allergy. 2002;57(9):825-830.
Mullou J, Xaubet A, Gaya A, et al. Cytokine gene expression and release from epithelial cells. A comparison study between healthy nasal mucosa and nasal polyps. Clin Exp Allergy. 1995;25(7):607-615.
Peric A, Spadijer-Mirkovic C, Matkovic-Jozin S, Jovancevic L, Vojvodic D. Granulocyte-macrophage colony-stimulating factor production and tissue eosinophilia in chronic rhinitis. Int Arch Otorhinolaryngol. 2016;20(4):364-369.
De Corso E, Baroni S, Lucidi D, et al. Nasal lavage levels of granulocyte-macrophage colony-stimulating factor and chronic nasal hypereosinophilia. Int Forum Allergy Rhinology. 2015;5(6):557-562.
Van Zele T, Claeys S, Gevaert P, et al. Differentiation of chronic sinus diseases by measurement of inflammatory mediators. Allergy. 2006;61(11):1280-1289.
Watelet JB, Claeys C, Perez-Novo C, Gevaert P, Van Cauwenberge P, Bachert C. Transforming growth factor beta1 in nasal remodeling: Differences between chronic rhinosinusitis and nasal polyposis. Am J Rhinol. 2004;18(5):267-272.
Roberts N, Al Mubarak R, Francisco D, Kraft M, Chu HW. Comparison of paired human nasal and bronchial airway epithelial cell responses to rhinovirus infection and IL-13 treatment. Clin Transl Med. 2018;7(1):13.
Bals R, Hiemstra PS. Innate immunity in the lung: How epithelial cells fight against respiratory pathogens. Eur Respir J. 2004;23(2):327-333.
Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34(5):637-650.
Lane AP, Truong-Tran QA, Myers A, Bickel C, Schleimer RP. Serum amyloid A, properdin, complement 3, and toll-like receptors are expressed locally in human sinonasal tissue. Am J Rhinol. 2006;20(1):117-123.
Lin CF, Tsai CH, Cheng CH, Chen YS, Tournier F, Yeh TH. Expression of toll-like receptors in cultured nasal epithelial cells. Acta Otolaryngol. 2007;127(4):395-402.
Wang J, Matsukura S, Watanabe S, Adachi M, Suzaki H. Involvement of Toll-like receptors in the immune response of nasal polyp epithelial cells. Clin Immunol. 2007;124(3):345-352.
van Tongeren J, Röschmann KIL, Reinartz SM, et al. Expression profiling and functional analysis of Toll-like receptors in primary healthy human nasal epithelial cells shows no correlation and a refractory LPS response. Clin Transl Allergy. 2015;5:42.
Hirschberg A, Kiss M, Kadocsa E, et al. Different activations of toll-like receptors and antimicrobial peptides in chronic rhinosinusitis with or without nasal polyposis. Eur Arch Otorhinolaryngology. 2016;273(7):1779-1788.
Ramanathan M Jr, Lee WK, Dubin MG, Lin S, Spannhake EW, Lane AP. Sinonasal epithelial cell expression of toll-like receptor 9 is decreased in chronic rhinosinusitis with polyps. Am J Rhinol. 2007;21(1):110-116.
Claeys S, de Belder T, Holtappels G, et al. Human beta-defensins and toll-like receptors in the upper airway. Allergy. 2003;58(8):748-753.
Renkonen J, Toppila-Salmi S, Joenväärä S, et al. Expression of Toll-like receptors in nasal epithelium in allergic rhinitis. APMIS. 2015;123(8):716-725.
Fransson M, Adner M, Erjefalt J, Jansson L, Uddman R, Cardell LO. Up-regulation of Toll-like receptors 2, 3 and 4 in allergic rhinitis. Respir Res. 2005;6:100.
Paris G, Pozharskaya T, Asempa T, Lane AP. Damage-associated molecular patterns stimulate interleukin-33 expression in nasal polyp epithelial cells. Int Forum Allergy Rhinology. 2014;4(1):15-21.
Ramanathan M Jr, Lee WK, Spannhake EW, Lane AP. Th2 cytokines associated with chronic rhinosinusitis with polyps down-regulate the antimicrobial immune function of human sinonasal epithelial cells. Am J Rhinol. 2008;22(2):115-121.
Pilette C, Durham SR, Vaerman JP, Sibille Y. Mucosal immunity in asthma and chronic obstructive pulmonary disease: a role for immunoglobulin A? Proc Am Thorac Soc. 2004;1(2):125-135.
Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol. 2008;1(1):11-22.
Kato A, Xiao H, Chustz RT, Liu MC, Schleimer RP. Local release of B cell-activating factor of the TNF family after segmental allergen challenge of allergic subjects. J Allergy Clin Immunol. 2009;123(2):369-375.e2.
Kato A, Peters A, Suh L, et al. Evidence of a role for B cell-activating factor of the TNF family in the pathogenesis of chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol. 2008;121(6):1385-1392.
Hupin C, Rombaux P, Bowen H, Gould H, Lecocq M, Pilette C. Downregulation of polymeric immunoglobulin receptor and secretory IgA antibodies in eosinophilic upper airway diseases. Allergy. 2013;68(12):1589-1597.
Gohy ST, Detry BR, Lecocq M, et al. Polymeric immunoglobulin receptor down-regulation in chronic obstructive pulmonary disease. persistence in the cultured epithelium and role of transforming growth Factor-beta. Am J Respir Crit Care Med. 2014;190(5):509-521.
Ladjemi MZ, Lecocq M, Weynand B, et al. Increased IgA production by B-cells in COPD via lung epithelial interleukin-6 and TACI pathways. Eur Resp J. 2015;45(4):980-993.
Burton OT, Oettgen HC. Beyond immediate hypersensitivity: Evolving roles for IgE antibodies in immune homeostasis and allergic diseases. Immunol Rev. 2011;242(1):128-143.
Palaniyandi S, Tomei E, Li Z, Conrad DH, Zhu X. CD23-dependent transcytosis of IgE and immune complex across the polarized human respiratory epithelial cells. J Immunol. 2011;186(6):3484-3496.
Vachier I, Chiappara G, Vignola A, et al. Glucocorticoid receptors in bronchial epithelial cells in asthma. Am J Respir Crit Care Med. 1998;158(3):963-970.
Aversa S, Ondolo C, Abbadessa G, et al. Steroid resistance in nasal polyposis: Role of glucocorticoid receptor and TGF-beta1. Rhinology. 2012;50(4):427-435.
de Borja Callejas F, Martínez-Antón A, Picado C, et al. Corticosteroid treatment regulates mucosal remodeling in chronic rhinosinusitis with nasal polyps. The Laryngoscope. 2015;125(5):E158-167.
Spadijer-Mirkovic C, Peric A, Belic B, Vojvodic D. Clara cell protein 16 and eosinophil cationic protein production in chronically inflamed sinonasal mucosa. International forum of allergy & rhinology. 2016;6(5):529-536.
Hellings PW, Fokkens WJ, Akdis C, et al. Uncontrolled allergic rhinitis and chronic rhinosinusitis: Where do we stand today? Allergy. 2013;68(1):1-7.
Tsabouri S, Tseretopoulou X, Priftis K, Ntzani EE. Omalizumab for the treatment of inadequately controlled allergic rhinitis: A systematic review and meta-analysis of randomized clinical trials. J Allergy Clin Immunol Pract. 2014;2(3):332-340 e331.
Gevaert P, Van Bruaene N, Cattaert T, et al. Mepolizumab, a humanized anti-IL-5 mAb, as a treatment option for severe nasal polyposis. J Allergy Clin Immunol. 2011;128(5): 989-995.e8.
Gevaert P, Langloidolt D, Lackner A, et al. Nasal IL-5 levels determine the response to anti-IL-5 treatment in patients with nasal polyps. J Allergy Clin Immunol. 2006;118(5):1133-1141.
Gevaert P, Calus L, Van Zele T, et al. Omalizumab is effective in allergic and nonallergic patients with nasal polyps and asthma. J Allergy Clin Immunol. 2013;131(1): 110-116.e1.
Bachert C, Mannent L, Naclerio RM, et al. Effect of subcutaneous dupilumab on nasal polyp burden in patients with chronic sinusitis and nasal polyposis: A randomized clinical trial. JAMA. 2016;315(5):469-479.
Zhang F, Huang G, Hu B, Song Y, Shi Y. A soluble thymic stromal lymphopoietin (TSLP) antagonist, TSLPR-immunoglobulin, reduces the severity of allergic disease by regulating pulmonary dendritic cells. Clin Exp Immunol. 2011;164(2):256-264.
Kim YH, Yang TY, Park C-S, et al. Anti-IL-33 antibody has a therapeutic effect in a murine model of allergic rhinitis. Allergy. 2012;67(2):183-190.
Steelant B, Wawrzyniak P, Martens K, et al. Blocking histone deacetylase activity as a novel target for epithelial barrier defects in allergic rhinitis. J Allergy Clin Immunol. 2019.
Rennard SI, Fogarty C, Kelsen S, et al. The safety and efficacy of infliximab in moderate to severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007;175(9):926-934.
Mahler DA, Huang S, Tabrizi M, Bell GM. Efficacy and safety of a monoclonal antibody recognizing interleukin-8 in COPD: a pilot study. Chest. 2004;126(3):926-934.
Busse WW, Holgate S, Kerwin E, et al. Randomized, double-blind, placebo-controlled study of brodalumab, a human anti-IL-17 receptor monoclonal antibody, in moderate to severe asthma. Am J Respir Crit Care Med. 2013;188(11):1294-1302.
Wang M, Zhang W, Shang J, Yang J, Zhang L, Bachert C. Immunomodulatory effects of IL-23 and IL-17 in a mouse model of allergic rhinitis. Clin Exp Allergy. 2013;43(8):956-966.
Liu W, Liu S, Verma M, et al. Mechanism of TH2/TH17-predominant and neutrophilic TH2/TH17-low subtypes of asthma. J Allergy Clin Immunol. 2017;139(5): 1548-1558.e4.
Amali A, Saedi B, Rahavi-Ezabadi S, Ghazavi H, Hassanpoor N. Long-term postoperative azithromycin in patients with chronic rhinosinusitis: A randomized clinical trial. Am J Rhinol Allergy. 2015;29(6):421-424.
Videler WJ, Badia L, Harvey RJ, et al. Lack of efficacy of long-term, low-dose azithromycin in chronic rhinosinusitis: a randomized controlled trial. Allergy. 2011;66(11):1457-1468.
Huang Z, Zhou B. Clarithromycin for the treatment of adult chronic rhinosinusitis: a systematic review and meta-analysis. Int Forum Allergy Rhinology. 2019;9(5):545-555.
Takabayashi T, Kato A, Peters AT, et al. Glandular mast cells with distinct phenotype are highly elevated in chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol. 2012;130(2): 410-420.e5.