188
Views
4
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

EGF Protects Epithelial Cells from Barrier Damage in Chronic Rhinosinusitis with Nasal Polyps

, , , , &
Pages 439-450 | Published online: 19 Jan 2022

References

  • Hastan D, Fokkens WJ, Bachert C, et al. Chronic rhinosinusitis in Europe–an underestimated disease. A GA(2)LEN study. Allergy. 2011;66:1216–1223. doi:10.1111/j.1398-9995.2011.02646.x
  • Shi JB, Fu QL, Zhang H, et al. Epidemiology of chronic rhinosinusitis: results from a cross-sectional survey in seven Chinese cities. Allergy. 2015;70:533–539. doi:10.1111/all.12577
  • Wang X, Zhang N, Bo M, et al. Diversity of TH cytokine profiles in patients with chronic rhinosinusitis: a multicenter study in Europe, Asia, and Oceania. J Allergy Clin Immunol. 2016;138:1344–1353. doi:10.1016/j.jaci.2016.05.041
  • Workman AD, Kohanski MA, Cohen NA. Biomarkers in chronic rhinosinusitis with nasal polyps. Immunol Allergy Clin North Am. 2018;38:679–692. doi:10.1016/j.iac.2018.06.006
  • Cao PP, Li H-B, Wang B-F, et al. Distinct immunopathologic characteristics of various types of chronic rhinosinusitis in adult Chinese. J Allergy Clin Immunol. 2009;124:478–484, e471–e472. doi:10.1016/j.jaci.2009.05.017
  • Akdis CA, Bachert C, Cingi C, et al. Endotypes and phenotypes of chronic rhinosinusitis: a PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol. 2013;131:1479–1490. doi:10.1016/j.jaci.2013.02.036
  • Meltzer EO, Hamilos DL, Hadley JA, et al. Rhinosinusitis: establishing definitions for clinical research and patient care. Otolaryngol Head Neck Surg. 2004;131:S1–S62. doi:10.1016/j.otohns.2004.09.067
  • Fokkens WJ, Lund VJ, Mullol J, et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology. 2012;50:1–12. doi:10.4193/Rhino12.000
  • Bachert C, Marple B, Schlosser RJ, et al. Adult chronic rhinosinusitis. Nat Rev Dis Primers. 2020;6:86. doi:10.1038/s41572-020-00218-1
  • Rosenfeld RM, Piccirillo JF, Chandrasekhar SS, et al. Clinical practice guideline (update): adult sinusitis. Otolaryngol Head Neck Surg. 2015;152:S1–S39. doi:10.1177/0194599815572097
  • Seshadri S, Lin DC, Rosati M, et al. Reduced expression of antimicrobial PLUNC proteins in nasal polyp tissues of patients with chronic rhinosinusitis. Allergy. 2012;67:920–928. doi:10.1111/j.1398-9995.2012.02848.x
  • Tantilipikorn P, Sompornrattanaphan M, Suwanwech T, Ngaotepprutaram P. Chronic rhinosinusitis and allergy: increased allergen sensitization versus real allergic rhinitis multimorbidity: a systematic review. Curr Allergy Asthma Rep. 2020;20:19. doi:10.1007/s11882-020-00913-9
  • Stevens WW, Schleimer RP, Kern RC. Chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol Pract. 2016;4:565–572. doi:10.1016/j.jaip.2016.04.012
  • 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;130:1087–1096 e1010. doi:10.1016/j.jaci.2012.05.052
  • Tieu DD, Kern RC, Schleimer RP. Alterations in epithelial barrier function and host defense responses in chronic rhinosinusitis. J Allergy Clin Immunol. 2009;124:37–42. doi:10.1016/j.jaci.2009.04.045
  • Kao SS, Ramezanpour M, Bassiouni A, et al. Barrier disruptive effects of mucus isolated from chronic rhinosinusitis patients. Allergy. 2020;75:200–203. doi:10.1111/all.13964
  • Schleimer RP. Immunopathogenesis of chronic rhinosinusitis and nasal polyposis. Annu Rev Pathol. 2017;12:331–357. doi:10.1146/annurev-pathol-052016-100401
  • Zhang N, Van Crombruggen K, Gevaert E, Bachert C. Barrier function of the nasal mucosa in health and type-2 biased airway diseases. Allergy. 2016;71:295–307. doi:10.1111/all.12809
  • Schleimer RP, Kato A, Kern R, Kuperman D, Avila PC. Epithelium: at the interface of innate and adaptive immune responses. J Allergy Clin Immunol. 2007;120:1279–1284. doi:10.1016/j.jaci.2007.08.046
  • Van Bruaene N, Bachert C. Tissue remodeling in chronic rhinosinusitis. Curr Opin Allergy Clin Immunol. 2011;11:8–11. doi:10.1097/ACI.0b013e32834233ef
  • Barham HP, Osborn JL, Snidvongs K, et al. Remodeling changes of the upper airway with chronic rhinosinusitis. Int Forum Allergy Rhinol. 2015;5:565–572. doi:10.1002/alr.21546
  • Kern RC, Conley DB, Walsh W, et al. Perspectives on the etiology of chronic rhinosinusitis: an immune barrier hypothesis. Am J Rhinol. 2008;22:549–559. doi:10.2500/ajr.2008.22.3228
  • 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:e82373. doi:10.1371/journal.pone.0082373
  • Brozek JL, Bousquet J, Agache I, et al. Allergic rhinitis and its impact on asthma (ARIA) guidelines-2016 revision. J Allergy Clin Immunol. 2017;140:950–958. doi:10.1016/j.jaci.2017.03.050
  • Jang YJ, Kim HG, Koo TW, Chung PS. Localization of ZO-1 and E-cadherin in the nasal polyp epithelium. Eur Arch Otorhinolaryngol. 2002;259:465–469. doi:10.1007/s00405-002-0500-z
  • Rogers GA, Beste KD, Parkos CA, et al. Epithelial tight junction alterations in nasal polyposis. Int Forum Allergy Rhinol. 2011;1:50–54. doi:10.1002/alr.20014
  • Barmeyer C, Schulzke JD, Fromm M. Claudin-related intestinal diseases. Semin Cell Dev Biol. 2015;42:30–38. doi:10.1016/j.semcdb.2015.05.006
  • Shahana S, Jaunmuktane Z, Asplund MS, Roomans GM. Ultrastructural investigation of epithelial damage in asthmatic and non-asthmatic nasal polyps. Respir Med. 2006;100:2018–2028. doi:10.1016/j.rmed.2006.02.012
  • Loxham M, Davies DE. Phenotypic and genetic aspects of epithelial barrier function in asthmatic patients. J Allergy Clin Immunol. 2017;139:1736–1751. doi:10.1016/j.jaci.2017.04.005
  • Georas SN, Rezaee F. Epithelial barrier function: at the front line of asthma immunology and allergic airway inflammation. J Allergy Clin Immunol. 2014;134:509–520. doi:10.1016/j.jaci.2014.05.049
  • Yu XM, Li CW, Chao SS, et al. Reduced growth and proliferation dynamics of nasal epithelial stem/progenitor cells in nasal polyps in vitro. Sci Rep. 2014;4:4619. doi:10.1038/srep04619
  • Yu XM, Li CW, Li YY, et al. Down-regulation of EMP1 is associated with epithelial hyperplasia and metaplasia in nasal polyps. Histopathology. 2013;63:686–695. doi:10.1111/his.12211
  • Wang W, Gao Z, Wang H, et al. Transcriptome analysis reveals distinct gene expression profiles in eosinophilic and noneosinophilic chronic rhinosinusitis with nasal polyps. Sci Rep. 2016;6:26604. doi:10.1038/srep26604
  • Ma Y, Zheng C, Shi L. The kinase LRRK2 is differently expressed in chronic rhinosinusitis with and without nasal polyps. Clin Transl Allergy. 2018;8:8. doi:10.1186/s13601-018-0194-y
  • Nian JB, Zeng M, Zheng J, et al. Epithelial cells expressed IL-33 to promote degranulation of mast cells through inhibition on ST2/PI3K/mTOR-mediated autophagy in allergic rhinitis. Cell Cycle. 2020;19:1132–1142. doi:10.1080/15384101.2020.1749402
  • Wlodarska M, Thaiss C, Nowarski R, et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell. 2014;156:1045–1059. doi:10.1016/j.cell.2014.01.026
  • Buque A, Bloy N, Perez-Lanzón M, et al. Immunoprophylactic and immunotherapeutic control of hormone receptor-positive breast cancer. Nat Commun. 2020;11:3819. doi:10.1038/s41467-020-17644-0
  • Lai X, Li X, Chang L, et al. IL-19 up-regulates mucin 5AC production in patients with chronic rhinosinusitis via STAT3 pathway. Front Immunol. 2019;10:1682. doi:10.3389/fimmu.2019.01682
  • Cheng J, Chen J, Zhao Y, et al. MicroRNA-761 suppresses remodeling of nasal mucosa and epithelial-mesenchymal transition in mice with chronic rhinosinusitis through LCN2. Stem Cell Res Ther. 2020;11:151. doi:10.1186/s13287-020-01598-7
  • Shi S, Han Y, Wang D, et al. PD-L1 and PD-1 expressed in trigeminal ganglia may inhibit pain in an acute migraine model. Cephalalgia. 2020;40:288–298. doi:10.1177/0333102419883374
  • Parra ER, Villalobos P, Behrens C, et al. Effect of neoadjuvant chemotherapy on the immune microenvironment in non-small cell lung carcinomas as determined by multiplex immunofluorescence and image analysis approaches. J Immunother Cancer. 2018;6:48. doi:10.1186/s40425-018-0368-0
  • Van Bruaene N, Pérez-Novo CA, Basinski TM, et al. T-cell regulation in chronic paranasal sinus disease. J Allergy Clin Immunol. 2008;121:1435–1441, e1431–e1433. doi:10.1016/j.jaci.2008.02.018
  • Bachert C, Zhang N, Holtappels G, et al. Presence of IL-5 protein and IgE antibodies to staphylococcal enterotoxins in nasal polyps is associated with comorbid asthma. J Allergy Clin Immunol. 2010;126:962–968, e961–e966. doi:10.1016/j.jaci.2010.07.007
  • Tan BK, Klingler AI, Poposki JA, et al. Heterogeneous inflammatory patterns in chronic rhinosinusitis without nasal polyps in Chicago, Illinois. J Allergy Clin Immunol. 2017;139:699–703 e697. doi:10.1016/j.jaci.2016.06.063
  • Thanasumpun T, Batra PS. Endoscopically-derived bacterial cultures in chronic rhinosinusitis: a systematic review. Am J Otolaryngol. 2015;36:686–691. doi:10.1016/j.amjoto.2015.04.010
  • Zhang Z, Adappa ND, Doghramji LJ, et al. Different clinical factors associated with Staphylococcus aureus and Pseudomonas aeruginosa in chronic rhinosinusitis. Int Forum Allergy Rhinol. 2015;5:724–733. doi:10.1002/alr.21532
  • Corriveau MN, Zhang N, Holtappels G, Van Roy N, Bachert C. Detection of Staphylococcus aureus in nasal tissue with peptide nucleic acid-fluorescence in situ hybridization. Am J Rhinol Allergy. 2009;23:461–465. doi:10.2500/ajra.2009.23.3367
  • Tan NC, Foreman A, Jardeleza C, et al. Intracellular Staphylococcus aureus: the Trojan horse of recalcitrant chronic rhinosinusitis? Int Forum Allergy Rhinol. 2013;3:261–266. doi:10.1002/alr.21154
  • Kim RJ, Yin T, Chen C-J-J, et al. The interaction between bacteria and mucosal immunity in chronic rhinosinusitis: a prospective cross-sectional analysis. Am J Rhinol Allergy. 2013;27:e183–e189. doi:10.2500/ajra.2013.27.3974
  • 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;143:591–603 e593. doi:10.1016/j.jaci.2018.05.035
  • Tan NC, Cooksley CM, Roscioli E, et al. Small-colony variants and phenotype switching of intracellular Staphylococcus aureus in chronic rhinosinusitis. Allergy. 2014;69:1364–1371. doi:10.1111/all.12457
  • Kohanski MA, Lane AP. Sinonasal epithelial cell response to Staphylococcus aureus burden in chronic rhinosinusitis. JAMA Otolaryngol Head Neck Surg. 2015;141:341–349. doi:10.1001/jamaoto.2014.3550
  • Gevaert E, Zhang N, Krysko O, et al. Extracellular eosinophilic traps in association with Staphylococcus aureus at the site of epithelial barrier defects in patients with severe airway inflammation. J Allergy Clin Immunol. 2017;139:1849–1860 e1846. doi:10.1016/j.jaci.2017.01.019
  • Teufelberger AR, Nordengrün M, Braun H, et al. The IL-33/ST2 axis is crucial in type 2 airway responses induced by Staphylococcus aureus-derived serine protease-like protein D. J Allergy Clin Immunol. 2018;141:549–559 e547. doi:10.1016/j.jaci.2017.05.004
  • Malik Z, Roscioli E, Murphy J, et al. Staphylococcus aureus impairs the airway epithelial barrier in vitro. Int Forum Allergy Rhinol. 2015;5(6):551–556. doi:10.1002/alr.21517
  • Kim CS, Jeon S-Y, Min Y-G, et al. Effects of beta-toxin of Staphylococcus aureus on ciliary activity of nasal epithelial cells. Laryngoscope. 2000;110:2085–2088. doi:10.1097/00005537-200012000-00021
  • Eiffler I, Behnke J, Ziesemer S, Muller C, Hildebrandt JP. Staphylococcus aureus alpha-toxin-mediated cation entry depolarizes membrane potential and activates p38 MAP kinase in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2016;311:L676–L685. doi:10.1152/ajplung.00090.2016
  • Hermann I, Räth S, Ziesemer S, et al. Staphylococcus aureus hemolysin A disrupts cell–matrix adhesions in human airway epithelial cells. Am J Respir Cell Mol Biol. 2015;52:14–24. doi:10.1165/rcmb.2014-0082OC
  • LeMessurier KS, Tiwary M, Morin NP, Samarasinghe AE. Respiratory barrier as a safeguard and regulator of defense against influenza A virus and Streptococcus pneumoniae. Front Immunol. 2020;11:3. doi:10.3389/fimmu.2020.00003
  • Burgel PR, Nadel JA. Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax. 2004;59:992–996. doi:10.1136/thx.2003.018879
  • Jacob M, Bin Khalaf D, Alhissi S, et al. Quantitative profiling of cytokines and chemokines in DOCK8-deficient and atopic dermatitis patients. Allergy. 2019;74:370–379. doi:10.1111/all.13610
  • Pastore S, Mascia F, Mariani V, Girolomoni G. The epidermal growth factor receptor system in skin repair and inflammation. J Invest Dermatol. 2008;128:1365–1374. doi:10.1038/sj.jid.5701184
  • Sinha A, Nightingale J, West KP, Berlanga-Acosta J, Playford RJ. Epidermal growth factor enemas with oral mesalamine for mild-to-moderate left-sided ulcerative colitis or proctitis. N Engl J Med. 2003;349:350–357. doi:10.1056/NEJMoa013136
  • Brown GL, Nanney LB, Griffen J, et al. Enhancement of wound healing by topical treatment with epidermal growth factor. N Engl J Med. 1989;321:76–79. doi:10.1056/NEJM198907133210203
  • Duan C, Li CW, Zhao L, et al. Differential expression patterns of EGF, EGFR, and ERBB4 in nasal polyp epithelium. PLoS One. 2016;11:e0156949. doi:10.1371/journal.pone.0156949
  • Ding GQ, Zheng CQ, Bagga SS. Up-regulation of the mucosal epidermal growth factor receptor gene in chronic rhinosinusitis and nasal polyposis. Arch Otolaryngol Head Neck Surg. 2007;133:1097–1103. doi:10.1001/archotol.133.11.1097
  • Marinas AE, Ciurea P, Margaritescu C, Cotoi OS. Expression of epidermal growth factor (EGF) and its receptors (EGFR1 and EGFR2) in chronic bronchitis. Rom J Morphol Embryol. 2012;53:957–966.
  • Sheng W, Shi X, Lin Y, et al. Musashi2 promotes EGF-induced EMT in pancreatic cancer via ZEB1-ERK/MAPK signaling. J Exp Clin Cancer Res. 2020;39:16. doi:10.1186/s13046-020-1521-4
  • Okuyama M, Fujiwara Y, Tanigawa T, et al. Roles of ZO-1 and epidermal growth factor in esophageal epithelial defense against acid. Digestion. 2007;75:135–141. doi:10.1159/000106454
  • Kugler MC, Joyner AL, Loomis CA, Munger JS. Sonic hedgehog signaling in the lung. From development to disease. Am J Respir Cell Mol Biol. 2015;52:1–13. doi:10.1165/rcmb.2014-0132TR
  • Konigshoff M, Balsara N, Pfaff E-M, et al. Functional Wnt signaling is increased in idiopathic pulmonary fibrosis. PLoS One. 2008;3:e2142. doi:10.1371/journal.pone.0002142
  • Choy DF, Modrek B, Abbas AR, et al. Gene expression patterns of Th2 inflammation and intercellular communication in asthmatic airways. J Immunol. 2011;186:1861–1869. doi:10.4049/jimmunol.1002568
  • Chilosi M, Poletti V, Zamò A, et al. Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am J Pathol. 2003;162:1495–1502. doi:10.1016/s0002-9440(10)64282-4
  • Aumiller V, Balsara N, Wilhelm J, Gunther A, Konigshoff M. WNT/beta-catenin signaling induces IL-1beta expression by alveolar epithelial cells in pulmonary fibrosis. Am J Respir Cell Mol Biol. 2013;49:96–104. doi:10.1165/rcmb.2012-0524OC
  • Konigshoff M, Kramer M, Balsara N, et al. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest. 2009;119:772–787. doi:10.1172/JCI33950
  • Konigshoff M, Eickelberg O. WNT signaling in lung disease: a failure or a regeneration signal? Am J Respir Cell Mol Biol. 2010;42:21–31. doi:10.1165/rcmb.2008-0485TR
  • Halleskog C, Mulder J, Dahlström J, et al. WNT signaling in activated microglia is proinflammatory. Glia. 2011;59:119–131. doi:10.1002/glia.21081
  • Sen M, Lauterbach K, El-Gabalawy H, et al. Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2000;97:2791–2796. doi:10.1073/pnas.050574297
  • Blumenthal A, Ehlers S, Lauber J, et al. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood. 2006;108:965–973. doi:10.1182/blood-2005-12-5046
  • Boscke R, Vladar EK, Könnecke M, et al. Wnt signaling in chronic rhinosinusitis with nasal polyps. Am J Respir Cell Mol Biol. 2017;56:575–584. doi:10.1165/rcmb.2016-0024OC
  • Whyte JL, Smith AA, Helms JA. Wnt signaling and injury repair. Cold Spring Harb Perspect Biol. 2012;4:a008078. doi:10.1101/cshperspect.a008078
  • Fatehullah A, Tan SH, Barker N. Organoids as an in vitro model of human development and disease. Nat Cell Biol. 2016;18:246–254. doi:10.1038/ncb3312
  • Hsu YC, Li L, Fuchs E. Emerging interactions between skin stem cells and their niches. Nat Med. 2014;20:847–856. doi:10.1038/nm.3643
  • Lindemans CA, Calafiore M, Mertelsmann AM, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature. 2015;528:560–564. doi:10.1038/nature16460
  • Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–1007. doi:10.1038/nature06196
  • Sato T, van Es JH, Snippert HJ, et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 2011;469:415–418. doi:10.1038/nature09637
  • Bielefeld KA, Amini-Nik S, Alman BA. Cutaneous wound healing: recruiting developmental pathways for regeneration. Cell Mol Life Sci. 2013;70:2059–2081. doi:10.1007/s00018-012-1152-9
  • Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453:314–321. doi:10.1038/nature07039
  • Knight C, James S, Kuntin D, et al. Epidermal growth factor can signal via beta-catenin to control proliferation of mesenchymal stem cells independently of canonical Wnt signalling. Cell Signal. 2019;53:256–268. doi:10.1016/j.cellsig.2018.09.021