Immune mechanisms of neutrophilic inflammation in asthma
DOI: 10.32364/2587-6821-2024-8-8-2
N.A. Kuzubova, E.S. Lebedeva
Pavlov First Saint Petersburg State Medical University, St. Petersburg, Russian Federation
This review presents an analysis of scientific publications in recent years devoted to the study of cellular and molecular mechanisms of neutrophilic airway inflammation as potential therapeutic targets in the treatment of severe, poorly controlled asthma of the neutrophil phenotype, the presence of which is still debated and there is no generally accepted definition. The conditional term "neutrophilic asthma" implies the existence of a certain asthma endotype, in which neutrophils are the main type of cells mediating the pathophysiology and disease symptoms. The involvement of the inverted protein response associated with endoplasmic reticulum (ER) stress and the sensory signal transduction protein in the endoplasmic reticulum membrane in the deregulation of the T helper 17 (Th17) cells function and neutrophilic airway inflammation is considered. Polarization and activation of M1 macrophages play an important role in the neutrophilic inflammation immunopathogenesis, in particular, in asthma associated with obesity. Soluble suppression of tumorigenicity 2 protein is considered as a receptor that promotes neutrophil activation and neutrophilic inflammation. The involvement of neutrophil extracellular traps and the respiratory tract microbiome in the neutrophilic inflammation progression, in particular, the role of bacterial outer membrane vesicles, is discussed.
Keywords: neutrophils, neutrophilic inflammation, asthma, Th17 cells, M1 macrophages, suppression of tumorigenicity 2 protein, neutrophil extracellular traps, respiratory tract microbiome.
For citation: Kuzubova N.A., Lebedeva E.S. Immune mechanisms of neutrophilic inflammation in asthma. Russian Medical Inquiry. 2024;8(8):453–458 (in Russ.). DOI: 10.32364/2587-6821-2024-8-8-2.
Natalia A. Kuzubova — Dr. Sc. (Med.), Deputy Director of Science, National Research Institute of Pulmonology of the Pavlov First Saint Petersburg State Medical University; 6-8, Lev Tolstoy str., St. Petersburg, 197022, Russian Federation; ORCID iD 0000-0002-1166-9717.
Elena S. Lebedeva — C. Sc. (Bio.), Leading Researcher, National Research Institute of Pulmonology of the Pavlov First Saint Petersburg State Medical University; 6-8, Lev Tolstoy str., St. Petersburg, 197022, Russian Federation; ORCID iD 0000-0001-6887-0166.
Contact information: Natalia A. Kuzubova, е-mail: kuzubova@ mail.ru.
Financial Disclosure: no authors have a financial or property interest in any material or method mentioned.
There is no conflict of interest.
Received 10.07.2024.
Revised 02.08.2024.
Accepted 27.08.2024.
References
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32. Watanabe M., Nakamoto K., Inui T. et al. Serum sST2 levels predict severe exacerbation of asthma. Respir Res. 2018;19(1):169. DOI: 10.1186/s12931-018-0872-2.
33. Allinne J., Scott G., Lim W.K. et al. IL-33 blockade affects mediators of persistence and exacerbation in a model of chronic airway inflammation. J Allergy Clin Immunol. 2019;144(6):1624–1637.e10. DOI: 10.1016/j.jaci.2019.08.039.
34. Kelsen S.G., Agache I.O., Soong W. et al. Astegolimab (anti-ST2) efficacy and safety in adults with severe asthma: a randomized clinical trial. J Allergy Clin Immunol. 2021;148(3):790–798. DOI: 10.1016/j.jaci.2021.03.044.
35. Crim C., Stone S., Millar V. et al. IL-33 receptor inhibition in subjects with uncontrolled asthma: a randomized, placebo-controlled trial. J Allergy Clin Immunol Glob. 2022;1(4):198–208. DOI: 10.1016/j.jacig.2022.07.002.
36. Stojkov D., Yousefi S., Simon H.U. NETs: Important players in asthma? J Allergy Clin Immunol. 2024;153(1):100–102. DOI: 10.1016/j.jaci.2023.09.031.
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44. Zhang J., Zhu Z., Zuo X. et al. The role of NTHi colonization and infection in the pathogenesis of neutrophilic asthma. Respir Res. 2020;21(1):170. DOI: 10.1186/s12931-020-01438-5.
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46. Vanaja S.K., Russo A.J., Behl B. et al. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and Caspase-11 activation. Cells. 2016;165(5):1106–1119. DOI: 10.1016/j.cell.2016.04.015.
47. Eltobgy M.M., Zani A., Kenney A.D. et al. Caspase-4/11 exacerbates disease severity in SARS-CoV-2 infection by promoting inflammation and immunothrombosis. Proc Natl Acad Sci USA. 2022;119(21):e2202012119. DOI: 10.1073/pnas.2202012119.
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49. Busse W.W., 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. DOI: 10.1164/rccm.201212-2318OC.
50. Kirsten A., Watz H., Pedersen F. et al. The anti-IL-17A antibody secukinumab does not attenuate ozone-induced airway neutrophilia in healthy volunteers. Eur Respir J. 2013;41:239–241. DOI: 10.1183/09031936.00123612.
2. Nair P., Surette M.G., Virchow J.C. Neutrophilic asthma: Misconception or misnomer? Lancet Respir Med. 2021;9(5):441–443. DOI: 10.1016/S2213-2600(21)00023-0.
3. Nair P., Prabhavalkar K.S. Neutrophilic asthma and potentially related target therapies. Curr Drug Targets. 2020;21(4):374–388. DOI: 10.2174/1389450120666191011162526.
4. Nabe T. Steroid-resistant asthma and neutrophils. Biol Pharm Bull. 2020;43(1):31–35. DOI: 10.1248/bpb.b19-00095.
5. Crisford H., Sapey E., Rogers G.B. et al. Neutrophils in asthma: The good, the bad and the bacteria. Thorax. 2021;76(8):835–844. DOI: 10.1136/thoraxjnl-2020-215986.
6. He L.X., Deng K., Wang J. et al. Clinical subtypes of neuyrophilic asthma: A cluster analysis from Australasian severe asthma network. J Allergy Clin Immunol Pract. 2024;12(3):686–698.e8. DOI: 10.1016/j.jaip.2023.09.023.
7. Syabbalo N. Severe neutrophilic asthma: Pathogenesis and treatment. J Thorac Dis Cardiothorac Surg. 2022;3(1). DOI: 10.31579/2693-2156/030.
8. Yan Q., Zhang X., Xie Y. et al. Bronchial epithelial transcriptomics and experimental validation reveal asthma severity-related neutrophilic signatures and potential treatments. Commun Biol. 2024;7(1):181. DOI: 10.1038/s42003-024-05837-y.
9. Chung K.F. Asthma phenotyping: A necessity for improved therapeutic precision and new targeted therapies. J Intern Med. 2016;279(2):192–204. DOI: 10.1111/joim.12382.
10. Ray A., Kolls J.K. Neutrophilic inflammation in asthma and association with disease severity. Trends Immunol. 2017;38(12):942–954. DOI: 10.1016/j.it.2017.07.003.
11. Habib N., Pasha M.A., Tang D.D. Current understanding of asthma pathogenesis and biomarkers. Cells. 2022;11(17):2764. DOI: 10.3390/cells11172764.
12. Wang E., Wechsler M.E., Tran T.N. et al. Characterization of severe asthma worldwide: data from the international severe asthma registry. Chest. 2020;157(4):790–804. DOI: 10.1016/j.chest.2019.10.053.
13. Plavsic A., Bonaci-Nikolic B., Milenkovic B. et al. Asthma inflammatory phenotypes: How can we distinguish them? J Clin Med. 2024;13(2):526. DOI: 10.3390/jcm13020526.
14. Peri F., Amaddeo A., Badina L. et al. T2-low asthma: A discussed but still orphan disease. Biomedicines. 2023;11(4):1226. DOI: 10.3390/biomedicines11041226.
15. Kyriakopoulos C., Gogali A., Bartziokas K., Kostikas K. Identification and treatment of T2-low asthma in the era of biologics. ERJ Open Res. 2021;7(2):00309–02020. DOI: 10.1183/23120541.00309-2020.
16. Hynes G.M., Hinks T.S.C. The role of interleukin-17 in asthma: a protective response? ERJ Open Res. 2020;6(2):00364–02019. DOI: 10.1183/23120541.00364-2019.
17. Gauvreau G.M., Sehmi R., Ambrose C.S., Griffiths J.M. Thymic stromal lymphopoietin: Its role and potential as a therapeutic target in asthma. Expert Opin Ther Targets. 2020;24(8):777–792. DOI: 10.1080/14728222.2020.1783242.
18. Menzies-Gow A., Wechsler M.E., Brightling C.E. Unmet need in severe, uncontrolled asthma: Can anti-TSLP therapy with tezepelumab provide a valuable new treatment option? Respir Res. 2020;21(1):268. DOI: 10.1186/s12931-020-01505-x.
19. Yamasaki A., Okazaki R., Harada T. Neutrophils and asthma. Diagnostics (Basel). 2022;12(5):1175. DOI: 10.3390/diagnostics12051175.
20. Liu D., Tan Y., Bajinka O. et al. Th17/IL-17 axis regulated by airway microbes get involved in the development of asthma. Curr Allergy Asthma Rep. 2020;20(4):11. DOI: 10.1007/s11882-020-00903-x.
21. Wu D., Zhang X., Zimmerly K.M. et al. Unconventional activation of IRE1 enhances TH17 responses and promote airway neutrophilia. Am J Respir Cell Mol Biol. 2024;71(2):169–181. DOI: 10.1165/rcmb.2023-0424OC.
22. Singhania A., Wallington J.C., Smith C.G. et al. Multitissue transcriptomics delineates the diversity of airway T cell functions in asthma. Am J Respir Cell Mol Biol. 2018;58(2):261–270. DOI: 10.1165/rcmb.2017-0162OC.
23. Sze E., Bhalla A., Nair P. Mechanisms and therapeutic strategies for non-T2 asthma. Allergy. 2019;75(2):311–325. DOI: 10.1111/all.13985.
24. Kim J., Chang Y., Bae B. et al. Innate immune crosstalk in asthmatic airways: Innate lymphoid cells coordinate polarization of lung macrophages. J Allergy Clin Immunol. 2019;143(5):1769–1782.e11. DOI: 10.1016/j.jaci.2018.10.040.
25. Van der Veen T.A., de Groot L.E., Melgert B.N. The different faces of the macrophage in asthma. Curr Opin Pulm Med. 2020;26(1):62–68. DOI: 10.1097/MCP.0000000000000647.
26. Quoc Q.L., Cao T.B.T., Jang J.-H. et al. ST2-mediated neutrophilic airway inflammation: A therapeutic target for patients with uncontrolled asthma. Allergy Asthma Immunol Res. 2024;16(1):22–41. DOI: 10.4168/aair.2024.16.1.22.
27. Quoc Q.L., Choi Y., Thi Bich T.C. et al. S100A9 in adult asthmatic patients: a biomarker for neutrophilic asthma. Exp Mol Med. 2021;53(7):1170–1179. DOI: 10.1038/s12276-021-00652-5.
28. Wang Y., Wan R., Hu C. Leptin/obR signaling exacerbates obesity-related neutrophilic airway inflammation through inflammatory M1 macrophages. Mol Med. 2023;29(1):100. DOI: 10.1186/s10020-023-00702-w.
29. Chang С., Chen G., Wu W. et al. Exogenous IL-25 ameliorates airway neutrophilia via suppressing macrophage M1 polarization and the expression of IL-12 and IL-23 in asthma. Respir Res. 2023;24(1):260. DOI: 10.1186/s12931-023-02557-5.
30. Choi Y., Kim Y.M., Lee H.R. et al. Eosinophil extracellular traps activate type 2 innate lymphoid cells through stimulating airway epithelium in severe asthma. Allergy. 2020;75(1):95–103. DOI: 10.1111/all.13997.
31. Kim S.R. Next-generation therapeutic approaches for uncontrolled asthma: Insights into heterogeneity of non-type 2 inflammation. Allergy Asthma Immunol Res. 2024;16(1):1–5. DOI: 10.4168/aair.2024.16.1.1.
32. Watanabe M., Nakamoto K., Inui T. et al. Serum sST2 levels predict severe exacerbation of asthma. Respir Res. 2018;19(1):169. DOI: 10.1186/s12931-018-0872-2.
33. Allinne J., Scott G., Lim W.K. et al. IL-33 blockade affects mediators of persistence and exacerbation in a model of chronic airway inflammation. J Allergy Clin Immunol. 2019;144(6):1624–1637.e10. DOI: 10.1016/j.jaci.2019.08.039.
34. Kelsen S.G., Agache I.O., Soong W. et al. Astegolimab (anti-ST2) efficacy and safety in adults with severe asthma: a randomized clinical trial. J Allergy Clin Immunol. 2021;148(3):790–798. DOI: 10.1016/j.jaci.2021.03.044.
35. Crim C., Stone S., Millar V. et al. IL-33 receptor inhibition in subjects with uncontrolled asthma: a randomized, placebo-controlled trial. J Allergy Clin Immunol Glob. 2022;1(4):198–208. DOI: 10.1016/j.jacig.2022.07.002.
36. Stojkov D., Yousefi S., Simon H.U. NETs: Important players in asthma? J Allergy Clin Immunol. 2024;153(1):100–102. DOI: 10.1016/j.jaci.2023.09.031.
37. Tsai C.H., Lai A.C., Lin Y.C. et al. Neutrophil extracellular trap production and CCL4L2 expression influence corticosteroid response in asthma. Sci Transl Med. 2023;15(699):eadf3843. DOI: 10.1126/scitranslmed.adf3843.
38. Kim S.H., Jung H.W., Kim M. et al. Ceramide/sphingosine-1-phosphate imbalance is associated with distinct inflammatory phenotypes of uncontrolled asthma. Allergy. 2020;75(8):1991–2004. DOI: 10.1111/all.14236.
39. Poto R., Shamji M., Marone G. et al. Neutrophil extracellular traps in asthma: friends or foes? Cells. 2022;11(21):3521. DOI: 10.3390/cells11213521.
40. Kang N., Song W.J. Discovering biomarkers of neutrophilic asthma: a clinician's perspective. Allergy Asthma Immunol Res. 2022;14(1):1–4. DOI: 10.4168/aair.2022.14.1.1.
41. Taylor S.L., Leong L.E.X., Choo J.M. et al. Inflammatory phenotypes in patients with severe asthma are associated with distinct airway microbiology. J Allergy Clin Immunol. 2018;141(1):94–103.e15. DOI: 10.1016/j.jaci.2017.03.044.
42. Kozik A.J., Huang Y.J. The microbiome in asthma: Role in pathogenesis, phenotype, and response to treatment. Ann Allergy Asthma Immunol. 2019;122(3):270–275. DOI: 10.1016/j.anai.2018.12.005.
43. Abdel-Aziz M.I., Brinkman P., Vijverberg S.J.H. et al. Sputum microbiome profiles identify severe asthma phenotypes of relative stability at 12 to 18 months. J Allergy Clin Immunol. 2021;147(1):123–134. DOI: 10.1016/j.jaci.2020.04.018.
44. Zhang J., Zhu Z., Zuo X. et al. The role of NTHi colonization and infection in the pathogenesis of neutrophilic asthma. Respir Res. 2020;21(1):170. DOI: 10.1186/s12931-020-01438-5.
45. Zhang Y., Wang H., Zhang Y. et al. Aerosolization inhalation of non-typeable Haemophilus influenzae outer membrane vesicles contributing to neutrophilic asthma. Front Microbiol. 2023;14:1226633. DOI: 10.3389/fmicb.2023.1226633.
46. Vanaja S.K., Russo A.J., Behl B. et al. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and Caspase-11 activation. Cells. 2016;165(5):1106–1119. DOI: 10.1016/j.cell.2016.04.015.
47. Eltobgy M.M., Zani A., Kenney A.D. et al. Caspase-4/11 exacerbates disease severity in SARS-CoV-2 infection by promoting inflammation and immunothrombosis. Proc Natl Acad Sci USA. 2022;119(21):e2202012119. DOI: 10.1073/pnas.2202012119.
48. Шишкина В.В., Мошуров И.П., Герасимова О.А. и др. Cемейство каспаз: молекулярные основы взаимодействия при апоптозе и пироптозе. Гены и клетки. 2024;19(1):153–168. DOI: 10.17816/gc569246.Shishkina V.V., Moshurov I.P., Gerasimova O.A. et al. The caspase family: molecular bases of interaction in apoptosis and pyroptosis. Genes & Cells. 2024;19(1):153–168 (in Russ.). DOI: 10.17816/gc569246.
49. Busse W.W., 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. DOI: 10.1164/rccm.201212-2318OC.
50. Kirsten A., Watz H., Pedersen F. et al. The anti-IL-17A antibody secukinumab does not attenuate ozone-induced airway neutrophilia in healthy volunteers. Eur Respir J. 2013;41:239–241. DOI: 10.1183/09031936.00123612.
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