Influence of interleukin-33 gene expression on clinical and morphological characteristics of the nasal mucosa in allergic rhinitis

Abstract

The high incidence of allergic rhinitis and the association of allergic rhinitis with an increased risk of other allergic diseases, as well as the limited effectiveness of treatment methods make it extremely relevant to study the molecular mechanisms of allergic inflammation of the nasal mucosa. After the discovery of the IL-33 molecule a number of scientific papers about the role of IL-33 in the allergic inflammatory response and etiopathogenesis of various diseases were published. To date, research of IL-33 role in bronchial asthma pathogenesis has made significant progress, including the development of monoclonal antibodies against IL-33 for the treatment and control of the disease. Similar progress can be expected in the near future in studies of IL-33 in the pathogenesis of allergic rhinitis. The particular interest of modern allergology research lies in the field of the relationship between the production of IL-33 and pathomorphological changes in the nasal mucosa. Despite the limited number of publications devoted to this issue, literature analysis suggests that interleukin-33 significantly affects changes in the nasal mucosa and mediates clinical manifestations of allergic rhinitis.

Keywords:allergic rhinitis; interleukin-33; gene expression; cytokines; immunogenetics; Th cells; review

For citation: Gusniev S.A., Polner S.A., Mikhaleva L.M., Ilina N.I., Esakova A.P., Kurbacheva O.M., Shilovskiy I.P., Khaitov M.R. Influence of interleukin-33 gene expression on clinical and morphological characteristics of the nasal mucosa in allergic rhinitis. Immunologiya. 2021; 42 (1): 68-79. DOI: https://doi.org/10.33029/0206-4952-2021-42-1-68-79 (in Russian)

Funding. The work was supported by the Russian Science Foundation grant No. 19-15-00272.

Coninflict of interests. The authors declare no conflict of interests.

References

1. Il'ina N.I., Fedenko E.S., Kurbacheva O.M. Allergic rhinitis: a guide for general practitioners and pharmacists. Rossiyskiy allergologicheskiy zhurnal. 2004; 3: 1–12. (in Russian)

2. Akdis C.A., Hellings P.W., Agache I.; European Academy of Allergy and Clinical Immunology (eds). Global Atlas of Allergic Rhinitis and Chronic Rhinosinusitis. Zurich, Switzerland: European Academy of Allergy and Clinical Immunology; 2015: 422 p.

3. Passali D., Cingi C., Staffa P., Passali F., Muluk N.B., Bellussi M.L. The International Study of the Allergic Rhinitis Survey: outcomes from 4 geographical regions. Asia Pac. Allergy. 2018; 8 (1): e7.

4. Elisyutina O.G., Fedenko E.S., Boldyreva M.N., Gudima G.O. Genetic aspects of immunopathogenesis of atopic dermatitis. Immunologiya. 2015; 36 (2): 122–8. (in Russian)

5. Bousquet J., Khaltaev N., Cruz A.A., Denburg J., Fokkens W.J., Togias A., Zuberbier T., Baena-Cagnani C.E., Canonica G.W., van Weel C., Agache I., Aït-Khaled N., Bachert C., Blaiss M.S., Bonini S., Boulet L.-P., Bousquet P.-J., Camargos P., Carlsen K.-H., Chen Y., Custovic A., Dahl R., Demoly P., Douagui H., Durham S.R., van Wijk R.G., Kalayci O., Kaliner M.A., Kim Y.-Y., Kowalski M.L., Kuna P., Le L.T.T., Lemiere C., Li J., Lockey R.F., Mavale-Manuel S., Meltzer E.O., Mohammad Y., Mullol J., Naclerio R., O’Hehir R.E., Ohta K., Ouedraogo S., Palkonen S., Papadopoulos N., Passalacqua G., Pawankar R., Popov T.A., Rabe K.F., Rosado-Pinto J., Scadding G.K., Simons F.E.R., Toskala E., Valovirta E., van Cauwenberge P., Wang D.-Y., Wickman M., Yawn B.P., Yorgancioglu A., Yusuf O.M., Zar H., Annesi-Maesano I., Bateman E.D., Ben Kheder A., Boakye D.A., Bouchard J., Burney P., Busse W.W., Chan-Yeung M., Chavannes N.H., Chuchalin A., Dolen W.K., Emuzyte R., Grouse L., Humbert M., Jackson C., Johnston S.L., Keith P.K., Kemp J.P., Klossek J.-M., Larenas-Linnemann D., Lipworth B., Malo J.-L., Marshall G.D., Naspitz C., Nekam K., Niggemann B., Nizankowska-Mogilnicka E., Okamoto Y., Orru M.P., Potter P., Price D., Stoloff S.W., Vandenplas O., Viegi G., Williams D.; World Health Organization, GA(2)LEN, AllerGen. Allergic Rhinitis and its Impact on Asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA(2)LEN and AllerGen). Allergy. 2008; 63 (suppl 86): 8–160.

6. Gushchin I.S. Allergy – late product of the immune system evolution. Immunologiya. 2019; 40 (2): 43–57. DOI: https://doi.org/10.24411/0206-4952-2019-12007 (in Russian)

7. Creticos P.S., Peters S.P., Adkinson N.F., Naclerio R.M., Hayes E.C., Norman P.S., Lichtenstein L.M. Peptide leukotriene release after antigen challenge in patients sensitive to ragweed. N. Engl. J. Med. 1984; 310 (25): 1626–30.

8. Varney V.A., Jacobson M.R., Sudderick R.M., Robinson D.S., Irani A.M., Schwartz L.B., Mackay I.S., Kay A.B., Durham S.R. Immunohistology of the nasal mucosa following allergen-induced rhinitis. Identification of activated T lymphocytes, eosinophils, and neutrophils. Am. Rev. Respir. Dis. 1992; 146 (1): 170–6.

9. Fokkens W.J., Godthelp T., Holm A.F., Blom H., Mulder P.G., Vroom T.M., Rijntjes E. Dynamics of mast cells in the nasal mucosa of patients with allergic rhinitis and non-allergic controls: a biopsy study. Clin. Exp. Allergy. 1992; 22 (7): 701–10.

10. Sizyakina L.P., Andreeva I.I., Semenova N.I. Immunoregulatory mechanisms of progression of seasonal allergic rhinitis. Immunologiya. 2018; 39 (5–6): 276–81. DOI: DOI: http://doi.org/10.18821/0206-4952-2018-39-5-6-276-281 (in Russian)

11. Jutel M., Akdis M., Akdis C.A. Histamine, histamine receptors and their role in immune pathology. Clin. Exp. Allergy. 2009; 39 (12): 1786–800.

12. Ueda T., Takeno S., Furukido K., Hirakawa K., Yajin K. Leukotriene receptor antagonist pranlukast suppresses eosinophil infiltration and cytokine production in human nasal mucosa of perennial allergic rhinitis. Ann. Otol. Rhinol. Laryngol. 2003; 112 (11): 955–61.

13. Dobrina A., Menegazzi R., Carlos T.M., Nardon E., Cramer R., Zacchi T., Harlan J.M., Patriarca P. Mechanisms of eosinophil adherence to cultured vascular endothelial cells. Eosinophils bind to the cytokine-induced ligand vascular cell adhesion molecule-1 via the very late activation antigen-4 integrin receptor. J. Clin. Invest. 1991; 88 (1): 20–6.

14. Flood-Page P.T., Menzies-Gow A.N., Kay A.B., Robinson D.S. Eosinophil’s role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am. J. Respir. Crit. Care Med. 2003; 167 (2): 199–204.

15. Terada N., Nomura T., Kim W.J., Otsuka Y., Takahashi R., Kishi H., Yamashita T., Sugawara N., Fukuda S., Ikeda-Ito T., Konno A. Expression of C-C chemokine TARC in human nasal mucosa and its regulation by cytokines. Clin. Exp. Allergy. 2001; 31 (12): 1923–31.

16. Weller P.F., Lee C.W., Foster D.W., Corey E.J., Austen K.F., Lewis R.A. Generation and metabolism of 5-lipoxygenase pathway leukotrienes by human eosinophils: predominant production of leukotriene C4. Proc. Natl Acad. Sci. USA. 1983; 80 (24): 7626–30.

17. Ayars G.H., Altman L.C., McManus M.M., Agosti J.M., Baker C., Luchtel D.L., Loegering D.A., Gleich G.J. Injurious effect of the eosinophil peroxide-hydrogen peroxide-halide system and major basic protein on human nasal epithelium in vitro. Am. Rev. Respir. Dis. 1989; 140 (1): 125–31.

18. Jacoby D.B., Gleich G.J., Fryer A.D. Human eosinophil major basic protein is an endogenous allosteric antagonist at the inhibitory muscarinic M2 receptor. J. Clin. Invest. 1993; 91 (4): 1314–8.

19. Canonica G.W., Bousquet J., Mullol J., Scadding G.K., Virchow J.C. A survey of the burden of allergic rhinitis in Europe. Allergy. 2007; 62 (suppl 85): 17–25.

20. Kakli H.A., Riley T.D. Allergic rhinitis. Prim. Care. 2016; 43 (3): 465–75.

21. Wick G., Grundtman C., Mayerl C., Wimpissinger T.-F., Feichtinger J., Zelger B., Sgonc R., Wolfram D. The immunology of fibrosis. Annu. Rev. Immunol. 2013; 31 (1): 107–35.

22. Morimoto Y., Hirahara K., Kiuchi M., Wada T., Ichikawa T., Kanno T., Okano M., Kokubo K., Onodera A., Sakurai D., Okamoto Y., Nakayama T. Amphiregulin-producing pathogenic memory T helper 2 cells instruct eosinophils to secrete osteopontin and facilitate airway fibrosis. Immunity. 2018; 49 (1): 134–50.e6.

23. Poole J.A., Nordgren T.M., Heires A.J., Nelson A.J., Katafiasz D., Bailey K.L., Romberger D.J. Amphiregulin modulates murine lung recovery and fibroblast function following exposure to agriculture organic dust. Am. J. Physiol. Lung Cell. Mol. Physiol. 2020; 318 (1): L180–91.

24. Nagata Y., Maruoka S., Gon Y., Mizumura K., Kishi H., Nomura Y., Hikichi M., Hashimoto S., Oshima T. Expression of IL-25, IL-33, and thymic stromal lymphopoietin in nasal polyp gland duct epithelium in patients with chronic rhinosinusitis. Am. J. Rhinol. Allergy. 2019; 33 (4): 378–87.

25. Schmitz J., Owyang A., Oldham E., Song Y., Murphy E., McClanahan T.K., Zurawski G., Moshrefi M., Qin J., Li X., Gorman D.M., Bazan J.F., Kastelein R.A. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity. 2005; 23 (5): 479–90.

26. Liu H.-C., Liao Y., Liu C.-Q. miR-487b mitigates allergic rhinitis through inhibition of the IL-33/ST2 signaling pathway. Eur. Rev. Med. Pharmacol. Sci. 2018; 22 (23): 8076–83.

27. Derendorf H., Meltzer E.O. Molecular and clinical pharmacology of intranasal corticosteroids: clinical and therapeutic implications. Allergy. 2008; 63 (10): 1292–300.

28. Dykewicz M.S., Hamilos D.L. Rhinitis and sinusitis. J. Allergy Clin. Immunol. 2010; 125 (2 suppl 2): S103–15.

29. Oliphant C.J., Barlow J.L., McKenzie A.N.J. Insights into the initiation of type 2 immune responses. Immunology. 2011; 134 (4): 378–85.

30. Shilovsky I.P., Dyneva M.E., Kurbacheva O.M., Kudlay D.A., Khaitov M. R. The role of interleukin-37 in the pathogenesis of allergic diseases. Acta Naturae. 2019; 11 (4 (43)): 54–64. (in Russian)

31. Khaitov M.R., Gaysina A.R., Shilovsky I.P., Smirnov V.V., Ramenskaya G.V., Nikonova A.A., Khaitov R.M. Role of interleukin-33 in pathogenesis of asthma. New experimental data. Biokhimiya. 2018; 83 (1): 19–33. (in Russian)

32. Hsu C.-L., Neilsen C.V., Bryce P.J. IL-33 is produced by mast cells and regulates IgE-dependent inflammation. PLoS One. 2010; 5(8): e11944.

33. Galitskaya M.A., Kurbacheva O.M., Shilovsky I.P., Nikol'sky A.A., Nikonova A.A., Dyneva M.E., Khaitov M.R. Several features of inflammation at the patients with atopic bronchial asthma when exposed to respiratory viruses. Immunologiya. 2019; 41 (2): 154–63. DOI: https://doi.org/10.33029/0206-4952-2020-41-2-154-163 (in Russian)

34. Castillo J.R., Peters S.P., Busse W.W. Asthma exacerbations: pathogenesis, prevention, and treatment. J. Allergy Clin. Immunol. Pract. 2017; 5 (4): 918–27.

35. Galitskaya M.A., Kurbacheva O.M. The modern view of the role of innate and adaptive immunity in bronchial asthma. Rossiyskiy allergologicheskiy zhurnal. 2018; 15 (6): 7–17. (in Russian)

36. Galitskaya M.A., Shilovskiy I.P., Nikonova A.A., Gaisina A.R., Zhernov Y.V., Kurbacheva O.M., Khaitov M.R. Increased IL‐33 expression in atopic bronchial asthma patients with confirmed viral respiratory infection. Allergy Eur. J. Allergy Clin. Immunol. Suppl. 2018; 73 (S105): 298.

37. Lüthi A.U., Cullen S.P., McNeela E.A., Duriez P.J., Afonina I.S., Sheridan C., Brumatti G., Taylor R.C., Kersse K., Vandenabeele P., Lavelle E.C., Martin S.J. Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity. 2009; 31 (1): 84–98.

38. Lefrançais E., Roga S., Gautier V., Gonzalez-de-Peredo A., Monsarrat B., Girard J.-P., Cayrol C. IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc. Natl Acad. Sci. USA. 2012; 109 (5): 1673–8.

39. Glück J., Rymarczyk B., Rogala B. Serum IL-33 but not ST2 level is elevated in intermittent allergic rhinitis and is a marker of the disease severity. Inflamm. Res. 2012; 61 (6): 547–50.

40. Haenuki Y., Matsushita K., Futatsugi-Yumikura S., Ishii K.J., Kawagoe T., Imoto Y., Fujieda S., Yasuda M., Hisa Y., Akira S., Nakanishi K., Yoshimoto T. A critical role of IL-33 in experimental allergic rhinitis. J. Allergy Clin. Immunol. 2012; 130 (1): 184–94.e11.

41. Huang R., Mao W., Wang G., et al. Synergistic relationship between TSLP and IL-33/ST2 signaling pathways in allergic rhinitis and the effects of hypoxia. Int. Forum Allergy Rhinol. 2020; 10 (4): 511–20. DOI: https://doi.org/10.1002/alr.22504

42. Sakashita M., Yoshimoto T., Hirota T., Harada M., Okubo K., Osawa Y., Fujieda S., Nakamura Y., Yasuda K., Nakanishi K., Tamari M. Association of serum interleukin-33 level and the interleukin-33 genetic variant with Japanese cedar pollinosis. Clin. Exp. Allergy. 2008; 38 (12): 1875–81.

43. Khaitov M.R., Akimov V.S. Genetic predisposition to the development of bronchial asthma and atopy. Approaches to identifying new genes associated with the development of bronchial asthma and atopy. Rossiyskiy allergologicheskiy zhurnal. 2004; (3): 67–74. (in Russian)

44. Liew F.Y., Girard J.-P., Turnquist H.R. Interleukin-33 in health and disease. Nat. Rev. Immunol. 2016; 16 (11): 676–89.

45. Korppi M., Teräsjärvi J., Lauhkonen E., Huhtala H., Nuolivirta K., He Q. IL33 rs1342326 gene variation is associated with allergic rhinitis at school age after infant bronchiolitis. Acta Paediatr. 2020; 109 (10): 2112–6.

46. Waage J., Standl M., Curtin J.A., Jessen L.E., Thorsen J., Tian C., Schoettler N., Flores C., Abdellaoui A., Ahluwalia T.S., Alves A.C., Amaral A.F.S., Antó J.M., Arnold A., Barreto-Luis A., Baurecht H., van Beijsterveldt C.E.M., Bleecker E.R., Bonàs-Guarch S., Boomsma D.I., Brix S., Bunyavanich S., Burchard E.G., Chen Z., Curjuric I., Custovic A., den Dekker H.T., Dharmage S.C., Dmitrieva J., Duijts L., Ege M.J., Gauderman W.J., Georges M., Gieger C., Gilliland F., Granell R., Gui H., Hansen T., Heinrich J., Henderson J., Hernandez-Pacheco N., Holt P., Imboden M., Jaddoe V.W.V., Jarvelin M.-R., Jarvis D.L., Jensen K.K., Jónsdóttir I., Kabesch M., Kaprio J., Kumar A., Lee Y.-A., Levin A.M., Li X., Lorenzo-Diaz F., Melén E., Mercader J.M., Meyers D.A., Myers R., Nicolae D.L., Nohr E.A., Palviainen T., Paternoster L., Pennell C.E., Pershagen G., Pino-Yanes M., Probst-Hensch N.M., Rüschendorf F., Simpson A., Stefansson K., Sunyer J., Sveinbjornsson G., Thiering E., Thompson P.J., Torrent M., Torrents D., Tung J.Y., Wang C.A., Weidinger S., Weiss S., Willemsen G., Williams L.K., Ober C., Hinds D.A., Ferreira M.A., Bisgaard H., Strachan D.P., Bonnelykke K.; 23andMe Research Team, AAGC collaborators. Genome-wide association and HLA fine-mapping studies identify risk loci and genetic pathways underlying allergic rhinitis. Nat. Genet. 2018; 50 (8): 1072–80.

47. Gao Y., Li J., Zhang Y., Zhang L. Replication study of susceptibility variants associated with allergic rhinitis and allergy in Han Chinese. Allergy Asthma Clin. Immunol. 2020; 16: 13.

48. Schröder P.C., Casaca V.I., Illi S., Schieck M., Michel S., Böck A., Roduit C., Frei R., Lluis A., Genuneit J., Pfefferle P., Roponen M., Weber J., Braun-Fahrländer C., Riedler J., Lauener R., Vuitton D.A., Dalphin J.-C., Pekkanen J., von Mutius E., Kabesch M., Schaub B.; PASTURE Study group. IL-33 polymorphisms are associated with increased risk of hay fever and reduced regulatory T cells in a birth cohort. Pediatr. Allergy Immunol. 2016; 27 (7): 687–95.

49. Ohno T., Morita H., Arae K., Matsumoto K., Nakae S. Interleukin-33 in allergy. Allergy. 2012; 67 (10): 1203–14.

50. Solelhac G., Charpin D. Management of allergic rhinitis. F1000Prime Rep. 2014; 6: 94.

51. Bernstein J.A. Evaluating the effectiveness of medications in the treatment of allergic rhinitis. Ann. Allergy Asthma Immunol. 2010; 105 (2): 189.

52. Demoly P., Bousquet P.J., Mesbah K., Bousquet J., Devillier P. Visual analogue scale in patients treated for allergic rhinitis: an observational prospective study in primary care: asthma and rhinitis. Clin. Exp. Allergy. 2013; 43 (8): 881–8.

53. Valovirta E., Myrseth S.-E., Palkonen S. The voice of the patients: allergic rhinitis is not a trivial disease. Curr. Opin. Allergy Clin. Immunol. 2008; 8 (1): 1–9.

54. Rondon C., Campo P., Eguiluz-Gracia I., Plaza C., Bogas G., Galindo P., Mayorga C., Torres M.J. Local allergic rhinitis is an independent rhinitis phenotype: the results of a 10-year follow-up study. Allergy. 2018; 73 (2): 470–8.

55. Jakalski M., Bozek A., Canonica G.W. Responders and nonresponders to pharmacotherapy and allergen immunotherapy. Hum. Vaccines Immunother. 2019; 15 (12): 2896–902.

56. Klimek L., Sperl A., Becker S., Mösges R., Tomazic P.V. Current therapeutical strategies for allergic rhinitis. Expert Opin. Pharmacother. 2019; 20 (1): 83–9.

57. Issahaku A.R., Agoni C., Soremekun O.S., Kubi P.A., Kumi R.O., Olotu F.A., Soliman M.E.S. Same target, different therapeutic outcomes: the case of CAY10471 and fevipiprant on CRTh2 receptor in treatment of allergic rhinitis and asthma. Comb. Chem. High Throughput Screen. 2019; 22 (8): 521–33.

58. Yang J., Zhong W., Xue K., Wang Z. Epigenetic changes: an emerging potential pharmacological target in allergic rhinitis. Int. Immunopharmacol. 2019; 71: 76–83.

59. Steelant B., Wawrzyniak P., Martens K., Jonckheere A.-C., Pugin B., Schrijvers R., Bullens D.M., Vanoirbeek J.A., Krawczyk K., Dreher A., Akdis C.A., Hellings P.W. Blocking histone deacetylase activity as a novel target for epithelial barrier defects in patients with allergic rhinitis. J. Allergy Clin. Immunol. 2019; 144 (5): 1242–53.e7.

60. Chen Y.-L., Gutowska-Owsiak D., Hardman C.S., Westmoreland M., MacKenzie T., Cifuentes L., Waithe D., Lloyd-Lavery A., Marquette A., Londei M., Ogg G. Proof-of-concept clinical trial of etokimab shows a key role for IL-33 in atopic dermatitis pathogenesis. Sci. Transl. Med. 2019; 11 (515): eaax2945.

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