Skip to main content
Top
Published in: Inflammation 1/2024

22-09-2023 | Bronchial Asthma | RESEARCH

Interplay of IL-33 and IL-35 Modulates Th2/Th17 Responses in Cigarette Smoke Exposure HDM-Induced Asthma

Authors: Jing Liu, Beiting Su, Peizhi Tao, Xuena Yang, Li Zheng, Yusen Lin, Xiaoling Zou, Hailing Yang, Wenbin Wu, Tiantuo Zhang, Hongtao Li

Published in: Inflammation | Issue 1/2024

Login to get access

Abstract

Cigarette smoke (CS) facilitates adverse effects on the airway inflammation and treatment of asthma. Here, we investigated the mechanisms by which CS exacerbates asthma. The roles of IL-33 and IL-35 in asthma development were examined by treatment with IL-33 knockout (IL-33 KO) or transfection of adenovirus encoding IL-35 (Ad-IL-35) in a murine model of cigarette smoke-exposure asthma. Furthermore, the involvement of IL-33 and IL-35 in regulating DCs and Th2/Th17 cells was examined in a coculture system of DCs with CD4+ T cells. Additionally, we observed the effect of CpG-ODNs on the balance of IL-33 and IL-35. We show that CS and house dust mite (HDM) exposure induced IL-33 and suppressed IL-35 levels in cigarette smoke-exposure asthma in vivo and in vitro. Treatment with IL-33 KO or Ad-IL-35 significantly attenuated airway hyperreactivity, goblet hyperplasia, airway remodelling, and eosinophil and neutrophil infiltration in the lung tissues from asthmatic mice. Furthermore, we demonstrated reciprocal regulation between CS and HDM-modulated IL-33 and IL-35. Mechanistically, IL-33 KO (or anti-ST2) and Ad-IL-35 attenuated Th2- and Th17-associated inflammation by downregulating TSLP-DC signalling. Finally, administration of CpG-ODNs suppressed the expression of IL-33/ST2 and elevated the levels of IL-35, which is mainly derived from CD4+Foxp+ Tregs, to alleviate Th2- and Th17-associated inflammation by inhibiting the activation of BMDCs. Taken together, the IL-33/ST2 pathway drives the DC-Th2 and Th17 responses of cigarette smoke-exposure asthma, while IL-35 has the opposite effect. CpG-ODNs represent a potential therapeutic strategy for modulating the balance of IL-33 and IL-35 to suppress allergic airway inflammation.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference El-Husseini, Z.W., R. Gosens, F. Dekker, and G.H. Koppelman. 2020. The genetics of asthma and the promise of genomics-guided drug target discovery. The Lancet Respiratory Medicine 8: 1045–1056.PubMedCrossRef El-Husseini, Z.W., R. Gosens, F. Dekker, and G.H. Koppelman. 2020. The genetics of asthma and the promise of genomics-guided drug target discovery. The Lancet Respiratory Medicine 8: 1045–1056.PubMedCrossRef
3.
go back to reference Wang, J., C. Janson, R. Jogi, B. Forsberg, T. Gislason, M. Holm, et al. 2021. A prospective study on the role of smoking, environmental tobacco smoke, indoor painting and living in old or new buildings on asthma, rhinitis and respiratory symptoms. Environmental Research 192: 110269. PubMedCrossRef Wang, J., C. Janson, R. Jogi, B. Forsberg, T. Gislason, M. Holm, et al. 2021. A prospective study on the role of smoking, environmental tobacco smoke, indoor painting and living in old or new buildings on asthma, rhinitis and respiratory symptoms. Environmental Research 192: 110269. PubMedCrossRef
4.
go back to reference Coogan, P.F., N. Castro-Webb, J. Yu, G.T. O’Connor, J.R. Palmer, and L. Rosenberg. 2015. Active and passive smoking and the incidence of asthma in the Black Women’s Health Study. American Journal of Respiratory and Critical Care Medicine 191: 168–176. PubMedPubMedCentralCrossRef Coogan, P.F., N. Castro-Webb, J. Yu, G.T. O’Connor, J.R. Palmer, and L. Rosenberg. 2015. Active and passive smoking and the incidence of asthma in the Black Women’s Health Study. American Journal of Respiratory and Critical Care Medicine 191: 168–176. PubMedPubMedCentralCrossRef
5.
go back to reference Lajunen, T.K., J.J. Jaakkola, and M.S. Jaakkola. 2013. The synergistic effect of heredity and exposure to second-hand smoke on adult-onset asthma. American Journal of Respiratory and Critical Care Medicine 188: 776–782. PubMedCrossRef Lajunen, T.K., J.J. Jaakkola, and M.S. Jaakkola. 2013. The synergistic effect of heredity and exposure to second-hand smoke on adult-onset asthma. American Journal of Respiratory and Critical Care Medicine 188: 776–782. PubMedCrossRef
6.
go back to reference Polosa, R., and N.C. Thomson. 2013. Smoking and asthma: Dangerous liaisons. European Respiratory Journal 41: 716–726. PubMedCrossRef Polosa, R., and N.C. Thomson. 2013. Smoking and asthma: Dangerous liaisons. European Respiratory Journal 41: 716–726. PubMedCrossRef
7.
go back to reference Kiljander, T., T. Poussa, T. Helin, A. Jaakkola, K. Venho, and L. Lehtimäki. 2020. Symptom control among asthmatics with a clinically significant smoking history: A cross-sectional study in Finland. BMC Pulmonary Medicine 20: 88.PubMedPubMedCentralCrossRef Kiljander, T., T. Poussa, T. Helin, A. Jaakkola, K. Venho, and L. Lehtimäki. 2020. Symptom control among asthmatics with a clinically significant smoking history: A cross-sectional study in Finland. BMC Pulmonary Medicine 20: 88.PubMedPubMedCentralCrossRef
8.
go back to reference Polosa, R., C. Russo, P. Caponnetto, G. Bertino, M. Sarvà, T. Antic, et al. 2011. Greater severity of new onset asthma in allergic subjects who smoke: A 10-year longitudinal study. Respiratory Research 12: 16.PubMedPubMedCentralCrossRef Polosa, R., C. Russo, P. Caponnetto, G. Bertino, M. Sarvà, T. Antic, et al. 2011. Greater severity of new onset asthma in allergic subjects who smoke: A 10-year longitudinal study. Respiratory Research 12: 16.PubMedPubMedCentralCrossRef
10.
go back to reference Savenije, O.E., John J. Mahachie, M., Granell R., Kerkhof M., Dijk F. N., de Jongste J. C., et al. 2014. Association of IL33-IL-1 receptor-like 1 (IL1RL1) pathway polymorphisms with wheezing phenotypes and asthma in childhood. The Journal of Allergy and Clinical Immunology 134: 170–177.PubMedCrossRef Savenije, O.E., John J. Mahachie, M., Granell R., Kerkhof M., Dijk F. N., de Jongste J. C., et al. 2014. Association of IL33-IL-1 receptor-like 1 (IL1RL1) pathway polymorphisms with wheezing phenotypes and asthma in childhood. The Journal of Allergy and Clinical Immunology 134: 170–177.PubMedCrossRef
11.
go back to reference Cayrol, C., and J.P. Girard. 2018. Interleukin-33 (IL-33): A nuclear cytokine from the IL-1 family. Immunological Reviews 281: 154–168.PubMedCrossRef Cayrol, C., and J.P. Girard. 2018. Interleukin-33 (IL-33): A nuclear cytokine from the IL-1 family. Immunological Reviews 281: 154–168.PubMedCrossRef
12.
go back to reference Lee, J.H., K.L. Hailey, S.A. Vitorino, P.A. Jennings, T.D. Bigby, and E.C. Breen. 2019. Cigarette smoke triggers IL-33-associated inflammation in a model of late-stage chronic obstructive pulmonary disease. American Journal of Respiratory Cell and Molecular Biology 61: 567–574.PubMedPubMedCentralCrossRef Lee, J.H., K.L. Hailey, S.A. Vitorino, P.A. Jennings, T.D. Bigby, and E.C. Breen. 2019. Cigarette smoke triggers IL-33-associated inflammation in a model of late-stage chronic obstructive pulmonary disease. American Journal of Respiratory Cell and Molecular Biology 61: 567–574.PubMedPubMedCentralCrossRef
13.
go back to reference Hu, D. 2017. Role of anti-inflammatory cytokines IL-35 and IL-37 in asthma. Inflammation 40: 697–707.PubMedCrossRef Hu, D. 2017. Role of anti-inflammatory cytokines IL-35 and IL-37 in asthma. Inflammation 40: 697–707.PubMedCrossRef
14.
go back to reference Collison, L.W., C.J. Workman, T.T. Kuo, K. Boyd, Y. Wang, K.M. Vignali, et al. 2007. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 450: 566–569.PubMedCrossRef Collison, L.W., C.J. Workman, T.T. Kuo, K. Boyd, Y. Wang, K.M. Vignali, et al. 2007. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 450: 566–569.PubMedCrossRef
15.
go back to reference Collison, L.W., V. Chaturvedi, A.L. Henderson, P.R. Giacomin, C. Guy, J. Bankoti, et al. 2010. IL-35-mediated induction of a potent regulatory T cell population. Nature Immunology 11: 1093–1101.PubMedPubMedCentralCrossRef Collison, L.W., V. Chaturvedi, A.L. Henderson, P.R. Giacomin, C. Guy, J. Bankoti, et al. 2010. IL-35-mediated induction of a potent regulatory T cell population. Nature Immunology 11: 1093–1101.PubMedPubMedCentralCrossRef
16.
go back to reference Teymouri, M., M. Pirro, F. Fallarino, M. Gargaro, and A. Sahebkar. 2018. IL-35, a hallmark of immune-regulation in cancer progression, chronic infections and inflammatory diseases. International Journal of Cancer 143: 2105–2115.PubMedCrossRef Teymouri, M., M. Pirro, F. Fallarino, M. Gargaro, and A. Sahebkar. 2018. IL-35, a hallmark of immune-regulation in cancer progression, chronic infections and inflammatory diseases. International Journal of Cancer 143: 2105–2115.PubMedCrossRef
17.
go back to reference Wang, R.X., C.R. Yu, I.M. Dambuza, R.M. Mahdi, M.B. Dolinska, Y.V. Sergeev, et al. 2014. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nature Medicine 20: 633–641.PubMedPubMedCentralCrossRef Wang, R.X., C.R. Yu, I.M. Dambuza, R.M. Mahdi, M.B. Dolinska, Y.V. Sergeev, et al. 2014. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nature Medicine 20: 633–641.PubMedPubMedCentralCrossRef
18.
go back to reference Liu, S., Y. Li, L. Xia, H. Shen, and J. Lu. 2019. IL-35 prevent bone loss through promotion of bone formation and angiogenesis in rheumatoid arthritis. Clinical and Experimental Rheumatology 37: 820–825.PubMed Liu, S., Y. Li, L. Xia, H. Shen, and J. Lu. 2019. IL-35 prevent bone loss through promotion of bone formation and angiogenesis in rheumatoid arthritis. Clinical and Experimental Rheumatology 37: 820–825.PubMed
19.
go back to reference Peng, W., L. Wang, H. Zhang, Z. Zhang, and X. Chen. 2021. Effects of recombinant IL-35-BCG on Treg/Th17 cell imbalance and inflammatory response in asthmatic newborn mice induced by RSV. Inflammation 44: 2476–2485.PubMedCrossRef Peng, W., L. Wang, H. Zhang, Z. Zhang, and X. Chen. 2021. Effects of recombinant IL-35-BCG on Treg/Th17 cell imbalance and inflammatory response in asthmatic newborn mice induced by RSV. Inflammation 44: 2476–2485.PubMedCrossRef
20.
go back to reference Chen, C., Y. Deng, H. Chen, X. Wu, S. Cheng, Y. Xu, et al. 2014. Decreased concentration of IL-35 in plasma of patients with asthma and COPD. Asian Pacific Journal of Allergy and Immunology 32: 211–217.PubMed Chen, C., Y. Deng, H. Chen, X. Wu, S. Cheng, Y. Xu, et al. 2014. Decreased concentration of IL-35 in plasma of patients with asthma and COPD. Asian Pacific Journal of Allergy and Immunology 32: 211–217.PubMed
21.
go back to reference Jiang, S., F. Shan, Y. Zhang, L. Jiang, and Z. Cheng. 2018. Increased serum IL-17 and decreased serum IL-10 and IL-35 levels correlate with the progression of COPD. International Journal of Chronic Obstructive Pulmonary Disease 13: 2483–2494.PubMedPubMedCentralCrossRef Jiang, S., F. Shan, Y. Zhang, L. Jiang, and Z. Cheng. 2018. Increased serum IL-17 and decreased serum IL-10 and IL-35 levels correlate with the progression of COPD. International Journal of Chronic Obstructive Pulmonary Disease 13: 2483–2494.PubMedPubMedCentralCrossRef
22.
go back to reference Hanagata, N. 2017. CpG oligodeoxynucleotide nanomedicines for the prophylaxis or treatment of cancers, infectious diseases, and allergies. International Journal of Nanomedicine 12: 515–531.PubMedPubMedCentralCrossRef Hanagata, N. 2017. CpG oligodeoxynucleotide nanomedicines for the prophylaxis or treatment of cancers, infectious diseases, and allergies. International Journal of Nanomedicine 12: 515–531.PubMedPubMedCentralCrossRef
23.
go back to reference Sabatel, C., C. Radermecker, L. Fievez, G. Paulissen, S. Chakarov, C. Fernandes, et al. 2017. Exposure to bacterial CpG DNA protects from airway allergic inflammation by expanding regulatory lung interstitial macrophages. Immunity 46: 457–473.PubMedCrossRef Sabatel, C., C. Radermecker, L. Fievez, G. Paulissen, S. Chakarov, C. Fernandes, et al. 2017. Exposure to bacterial CpG DNA protects from airway allergic inflammation by expanding regulatory lung interstitial macrophages. Immunity 46: 457–473.PubMedCrossRef
24.
go back to reference Okajima, T., S. Shigemori, F. Namai, T. Ogita, T. Sato, and T. Shimosato. 2021. Free feeding of CpG-oligodeoxynucleotide particles prophylactically attenuates allergic airway inflammation and hyperresponsiveness in mice. Frontiers in Immunology 12: 738041. PubMedPubMedCentralCrossRef Okajima, T., S. Shigemori, F. Namai, T. Ogita, T. Sato, and T. Shimosato. 2021. Free feeding of CpG-oligodeoxynucleotide particles prophylactically attenuates allergic airway inflammation and hyperresponsiveness in mice. Frontiers in Immunology 12: 738041. PubMedPubMedCentralCrossRef
25.
go back to reference Mohammadi-Shahrokhi, V., A. Rezaei, A. Andalib, A. Rahnama, A. Jafarzadeh, and N. Eskandari. 2017. Immunomodulatory effects of adjuvants CPG, MPLA, and BCG on the Derp2-induced acute asthma at early life in an animal model of BALB/c mice. Inflammation 40: 259–274.PubMedCrossRef Mohammadi-Shahrokhi, V., A. Rezaei, A. Andalib, A. Rahnama, A. Jafarzadeh, and N. Eskandari. 2017. Immunomodulatory effects of adjuvants CPG, MPLA, and BCG on the Derp2-induced acute asthma at early life in an animal model of BALB/c mice. Inflammation 40: 259–274.PubMedCrossRef
26.
go back to reference Beeh, K.M., F. Kanniess, F. Wagner, C. Schilder, I. Naudts, A. Hammann-Haenni, et al. 2013. The novel TLR-9 agonist QbG10 shows clinical efficacy in persistent allergic asthma. The Journal of Allergy and Clinical Immunology 131: 866–874.PubMedCrossRef Beeh, K.M., F. Kanniess, F. Wagner, C. Schilder, I. Naudts, A. Hammann-Haenni, et al. 2013. The novel TLR-9 agonist QbG10 shows clinical efficacy in persistent allergic asthma. The Journal of Allergy and Clinical Immunology 131: 866–874.PubMedCrossRef
27.
go back to reference Krieg, A.M. 2006. Therapeutic potential of Toll-like receptor 9 activation. Nature Reviews Drug Discovery 5: 471–484.PubMedCrossRef Krieg, A.M. 2006. Therapeutic potential of Toll-like receptor 9 activation. Nature Reviews Drug Discovery 5: 471–484.PubMedCrossRef
28.
go back to reference Li, H.T., Z.G. Chen, Y.S. Lin, H. Liu, J. Ye, X.L. Zou, et al. 2018. CpG-ODNs and budesonide act synergistically to improve allergic responses in combined allergic rhinitis and asthma syndrome induced by chronic exposure to ovalbumin by modulating the TSLP-DC-OX40L axis. Inflammation 41: 1304–1320.PubMedCrossRef Li, H.T., Z.G. Chen, Y.S. Lin, H. Liu, J. Ye, X.L. Zou, et al. 2018. CpG-ODNs and budesonide act synergistically to improve allergic responses in combined allergic rhinitis and asthma syndrome induced by chronic exposure to ovalbumin by modulating the TSLP-DC-OX40L axis. Inflammation 41: 1304–1320.PubMedCrossRef
29.
go back to reference Li, H.T., Y.S. Lin, Q.M. Ye, X.N. Yang, X.L. Zou, H.L. Yang, et al. 2020. Airway inflammation and remodeling of cigarette smoking exposure ovalbumin-induced asthma is alleviated by CpG oligodeoxynucleotides via affecting dendritic cell-mediated Th17 polarization. International Immunopharmacology 82: 106361. PubMedCrossRef Li, H.T., Y.S. Lin, Q.M. Ye, X.N. Yang, X.L. Zou, H.L. Yang, et al. 2020. Airway inflammation and remodeling of cigarette smoking exposure ovalbumin-induced asthma is alleviated by CpG oligodeoxynucleotides via affecting dendritic cell-mediated Th17 polarization. International Immunopharmacology 82: 106361. PubMedCrossRef
30.
go back to reference Ramaprakash, H., T. Shibata, K.E. Duffy, U.B. Ismailoglu, R.M. Bredernitz, A.P. Moreira, et al. 2011. Targeting ST2L potentiates CpG-mediated therapeutic effects in a chronic fungal asthma model. American Journal of Pathology 179: 104–115.PubMedPubMedCentralCrossRef Ramaprakash, H., T. Shibata, K.E. Duffy, U.B. Ismailoglu, R.M. Bredernitz, A.P. Moreira, et al. 2011. Targeting ST2L potentiates CpG-mediated therapeutic effects in a chronic fungal asthma model. American Journal of Pathology 179: 104–115.PubMedPubMedCentralCrossRef
31.
go back to reference Thio, C.L., A.C. Lai, P.Y. Chi, G. Webster, and Y.J. Chang. 2019. Toll-like receptor 9-dependent interferon production prevents group 2 innate lymphoid cell-driven airway hyperreactivity. The Journal of Allergy and Clinical Immunology 144: 682-697.e689.PubMedCrossRef Thio, C.L., A.C. Lai, P.Y. Chi, G. Webster, and Y.J. Chang. 2019. Toll-like receptor 9-dependent interferon production prevents group 2 innate lymphoid cell-driven airway hyperreactivity. The Journal of Allergy and Clinical Immunology 144: 682-697.e689.PubMedCrossRef
32.
go back to reference Tan, Y.Y., H.Q. Zhou, Y.J. Lin, L.T. Yi, Z.G. Chen, Q.D. Cao, et al. 2022. FGF2 is overexpressed in asthma and promotes airway inflammation through the FGFR/MAPK/NF-κB pathway in airway epithelial cells. Military Medical Research 9: 7.PubMedPubMedCentralCrossRef Tan, Y.Y., H.Q. Zhou, Y.J. Lin, L.T. Yi, Z.G. Chen, Q.D. Cao, et al. 2022. FGF2 is overexpressed in asthma and promotes airway inflammation through the FGFR/MAPK/NF-κB pathway in airway epithelial cells. Military Medical Research 9: 7.PubMedPubMedCentralCrossRef
33.
go back to reference Li, H.T., Q.M. Ye, Y.S. Lin, X.N. Yang, X.L. Zou, H.L. Yang, et al. 2021. CpG oligodeoxynucleotides attenuate RORγt-mediated Th17 response by restoring histone deacetylase-2 in cigarette smoke-exposure asthma. Cell & Bioscience 11: 92.CrossRef Li, H.T., Q.M. Ye, Y.S. Lin, X.N. Yang, X.L. Zou, H.L. Yang, et al. 2021. CpG oligodeoxynucleotides attenuate RORγt-mediated Th17 response by restoring histone deacetylase-2 in cigarette smoke-exposure asthma. Cell & Bioscience 11: 92.CrossRef
34.
go back to reference Zhang, H., S.L. Qiu, Q.Y. Tang, X. Zhou, J.Q. Zhang, Z.Y. He, et al. 2019. Erythromycin suppresses neutrophil extracellular traps in smoking-related chronic pulmonary inflammation. Cell Death & Disease 10: 678.CrossRef Zhang, H., S.L. Qiu, Q.Y. Tang, X. Zhou, J.Q. Zhang, Z.Y. He, et al. 2019. Erythromycin suppresses neutrophil extracellular traps in smoking-related chronic pulmonary inflammation. Cell Death & Disease 10: 678.CrossRef
35.
go back to reference Myou, S., A.R. Leff, S. Myo, E. Boetticher, J. Tong, A.Y. Meliton, et al. 2003. Blockade of inflammation and airway hyperresponsiveness in immune-sensitized mice by dominant-negative phosphoinositide 3-kinase-TAT. Journal of Experimental Medicine 198: 1573–1582.PubMedPubMedCentralCrossRef Myou, S., A.R. Leff, S. Myo, E. Boetticher, J. Tong, A.Y. Meliton, et al. 2003. Blockade of inflammation and airway hyperresponsiveness in immune-sensitized mice by dominant-negative phosphoinositide 3-kinase-TAT. Journal of Experimental Medicine 198: 1573–1582.PubMedPubMedCentralCrossRef
36.
go back to reference Le, A.V., J.Y. Cho, M. Miller, S. McElwain, K. Golgotiu, and D.H. Broide. 2007. Inhibition of allergen-induced airway remodeling in Smad 3-deficient mice. The Journal of Immunology 178: 7310–7316.PubMedCrossRef Le, A.V., J.Y. Cho, M. Miller, S. McElwain, K. Golgotiu, and D.H. Broide. 2007. Inhibition of allergen-induced airway remodeling in Smad 3-deficient mice. The Journal of Immunology 178: 7310–7316.PubMedCrossRef
37.
go back to reference Lambrecht, B.N., and H. Hammad. 2017. The immunology of the allergy epidemic and the hygiene hypothesis. Nature Immunology 18: 1076–1083.PubMedCrossRef Lambrecht, B.N., and H. Hammad. 2017. The immunology of the allergy epidemic and the hygiene hypothesis. Nature Immunology 18: 1076–1083.PubMedCrossRef
38.
go back to reference Han, Y., C. Yu, Y. Yu, and L. Bi. 2022. CD25+ B cells produced IL-35 and alleviated local inflammation during experimental periodontitis. Oral Diseases 28: 2248–2257.PubMedCrossRef Han, Y., C. Yu, Y. Yu, and L. Bi. 2022. CD25+ B cells produced IL-35 and alleviated local inflammation during experimental periodontitis. Oral Diseases 28: 2248–2257.PubMedCrossRef
39.
40.
go back to reference Lanckacker, E.A., K.G. Tournoy, H. Hammad, G. Holtappels, B.N. Lambrecht, G.F. Joos, et al. 2013. Short cigarette smoke exposure facilitates sensitisation and asthma development in mice. European Respiratory Journal 41: 1189–1199.PubMedCrossRef Lanckacker, E.A., K.G. Tournoy, H. Hammad, G. Holtappels, B.N. Lambrecht, G.F. Joos, et al. 2013. Short cigarette smoke exposure facilitates sensitisation and asthma development in mice. European Respiratory Journal 41: 1189–1199.PubMedCrossRef
41.
go back to reference Boonpiyathad, T., Z.C. Sözener, P. Satitsuksanoa, and C.A. Akdis. 2019. Immunologic mechanisms in asthma. Seminars in Immunology 46: 101333. PubMedCrossRef Boonpiyathad, T., Z.C. Sözener, P. Satitsuksanoa, and C.A. Akdis. 2019. Immunologic mechanisms in asthma. Seminars in Immunology 46: 101333. PubMedCrossRef
42.
go back to reference Dang, X., B. He, Q. Ning, Y. Liu, J. Guo, G. Niu, et al. 2020. Alantolactone suppresses inflammation, apoptosis and oxidative stress in cigarette smoke-induced human bronchial epithelial cells through activation of Nrf2/HO-1 and inhibition of the NF-κB pathways. Respiratory Research 21: 95.PubMedPubMedCentralCrossRef Dang, X., B. He, Q. Ning, Y. Liu, J. Guo, G. Niu, et al. 2020. Alantolactone suppresses inflammation, apoptosis and oxidative stress in cigarette smoke-induced human bronchial epithelial cells through activation of Nrf2/HO-1 and inhibition of the NF-κB pathways. Respiratory Research 21: 95.PubMedPubMedCentralCrossRef
43.
go back to reference Zi, Y., X. Wang, Y. Zi, H. Yu, Y. Lan, Y. Fan, et al. 2023. Cigarette smoke induces the ROS accumulation and iNOS activation through deactivation of Nrf-2/SIRT3 axis to mediate the human bronchial epithelium ferroptosis. Free Radical Biology & Medicine 200: 73–86.CrossRef Zi, Y., X. Wang, Y. Zi, H. Yu, Y. Lan, Y. Fan, et al. 2023. Cigarette smoke induces the ROS accumulation and iNOS activation through deactivation of Nrf-2/SIRT3 axis to mediate the human bronchial epithelium ferroptosis. Free Radical Biology & Medicine 200: 73–86.CrossRef
44.
go back to reference Moffatt, M.F., I.G. Gut, F. Demenais, D.P. Strachan, E. Bouzigon, S. Heath, et al. 2010. A large-scale, consortium-based genomewide association study of asthma. New England Journal of Medicine 363: 1211–1221.PubMedCrossRef Moffatt, M.F., I.G. Gut, F. Demenais, D.P. Strachan, E. Bouzigon, S. Heath, et al. 2010. A large-scale, consortium-based genomewide association study of asthma. New England Journal of Medicine 363: 1211–1221.PubMedCrossRef
45.
go back to reference Wang, W., P. Li, Y.F. Chen, and J. Yang. 2015. A potential immunopathogenic role for reduced IL-35 expression in allergic asthma. Journal of Asthma 52: 763–771.CrossRef Wang, W., P. Li, Y.F. Chen, and J. Yang. 2015. A potential immunopathogenic role for reduced IL-35 expression in allergic asthma. Journal of Asthma 52: 763–771.CrossRef
46.
go back to reference Huang, Q., C.D. Li, Y.R. Yang, X.F. Qin, J.J. Wang, X. Zhang, et al. 2021. Role of the IL-33/ST2 axis in cigarette smoke-induced airways remodelling in chronic obstructive pulmonary disease. Thorax thoraxjnl-2020-214712. Huang, Q., C.D. Li, Y.R. Yang, X.F. Qin, J.J. Wang, X. Zhang, et al. 2021. Role of the IL-33/ST2 axis in cigarette smoke-induced airways remodelling in chronic obstructive pulmonary disease. Thorax thoraxjnl-2020-214712.
47.
go back to reference Kim, M.H., J.W. Kwon, J.H. Hahn, M. Kim, H.S. Chang, J.S. Park, et al. 2022. Circulating IL-32 and IL-33 levels in patients with asthma and COPD: A retrospective cross-sectional study. Journal of Thoracic Disease 14: 2437–2439.PubMedPubMedCentralCrossRef Kim, M.H., J.W. Kwon, J.H. Hahn, M. Kim, H.S. Chang, J.S. Park, et al. 2022. Circulating IL-32 and IL-33 levels in patients with asthma and COPD: A retrospective cross-sectional study. Journal of Thoracic Disease 14: 2437–2439.PubMedPubMedCentralCrossRef
48.
go back to reference Wechsler, M.E., M.K. Ruddy, I.D. Pavord, E. Israel, K.F. Rabe, L.B. Ford, et al. 2021. Efficacy and safety of itepekimab in patients with moderate-to-severe asthma. New England Journal of Medicine 385: 1656–1668.PubMedCrossRef Wechsler, M.E., M.K. Ruddy, I.D. Pavord, E. Israel, K.F. Rabe, L.B. Ford, et al. 2021. Efficacy and safety of itepekimab in patients with moderate-to-severe asthma. New England Journal of Medicine 385: 1656–1668.PubMedCrossRef
49.
go back to reference Whitehead Gregory S., Rhonda H. Wilson, Keiko Nakano, Lauranell H. Burch, Hideki Nakano, Donald N. Cook. 2012. IL-35 production by inducible costimulator (ICOS)-positive regulatory T cells reverses established IL-17-dependent allergic airways disease. Journal of Allergy and Clinical Immunology 129: 207–215.e201–205. Whitehead Gregory S., Rhonda H. Wilson, Keiko Nakano, Lauranell H. Burch, Hideki Nakano, Donald N. Cook. 2012. IL-35 production by inducible costimulator (ICOS)-positive regulatory T cells reverses established IL-17-dependent allergic airways disease. Journal of Allergy and Clinical Immunology 129: 207–215.e201–205.
50.
go back to reference Li, Y., X. Pan, X. Peng, S. Li, Y. Zhou, X. Zheng, et al. 2015. Adenovirus-mediated interleukin-35 gene transfer suppresses allergic airway inflammation in a murine model of asthma. Inflammation Research 64: 767–774.PubMedCrossRef Li, Y., X. Pan, X. Peng, S. Li, Y. Zhou, X. Zheng, et al. 2015. Adenovirus-mediated interleukin-35 gene transfer suppresses allergic airway inflammation in a murine model of asthma. Inflammation Research 64: 767–774.PubMedCrossRef
51.
go back to reference Dong, J., C.K. Wong, Z. Cai, D. Jiao, M. Chu, and C.W. Lam. 2015. Amelioration of allergic airway inflammation in mice by regulatory IL-35 through dampening inflammatory dendritic cells. Allergy 70: 921–932.PubMedCrossRef Dong, J., C.K. Wong, Z. Cai, D. Jiao, M. Chu, and C.W. Lam. 2015. Amelioration of allergic airway inflammation in mice by regulatory IL-35 through dampening inflammatory dendritic cells. Allergy 70: 921–932.PubMedCrossRef
52.
go back to reference Pan, X., K. Xu, Y. Li, X. Wang, X. Peng, M. Li, et al. 2019. Interleukin-35 expression protects against cigarette smoke-induced lung inflammation in mice. Biomedicine & Pharmacotherapy 110: 727–732.CrossRef Pan, X., K. Xu, Y. Li, X. Wang, X. Peng, M. Li, et al. 2019. Interleukin-35 expression protects against cigarette smoke-induced lung inflammation in mice. Biomedicine & Pharmacotherapy 110: 727–732.CrossRef
53.
go back to reference Faustino, L.D., J.W. Griffith, R.A. Rahimi, K. Nepal, D.L. Hamilos, J.L. Cho, et al. 2020. Interleukin-33 activates regulatory T cells to suppress innate γδ T cell responses in the lung. Nature Immunology 21: 1371–1383.PubMedPubMedCentralCrossRef Faustino, L.D., J.W. Griffith, R.A. Rahimi, K. Nepal, D.L. Hamilos, J.L. Cho, et al. 2020. Interleukin-33 activates regulatory T cells to suppress innate γδ T cell responses in the lung. Nature Immunology 21: 1371–1383.PubMedPubMedCentralCrossRef
54.
go back to reference Kohlgruber, A.C., S.T. Gal-Oz, N.M. LaMarche, M. Shimazaki, D. Duquette, H.F. Koay, et al. 2018. γδ T cells producing interleukin-17A regulate adipose regulatory T cell homeostasis and thermogenesis. Nature Immunology 19: 464–474.PubMedPubMedCentralCrossRef Kohlgruber, A.C., S.T. Gal-Oz, N.M. LaMarche, M. Shimazaki, D. Duquette, H.F. Koay, et al. 2018. γδ T cells producing interleukin-17A regulate adipose regulatory T cell homeostasis and thermogenesis. Nature Immunology 19: 464–474.PubMedPubMedCentralCrossRef
55.
go back to reference Guo, X.J., P. Dash, J.C. Crawford, E.K. Allen, A.E. Zamora, D.F. Boyd, et al. 2018. Lung γδ T cells mediate protective responses during neonatal influenza infection that are associated with type 2 immunity. Immunity 49: 531-544.e536.PubMedPubMedCentralCrossRef Guo, X.J., P. Dash, J.C. Crawford, E.K. Allen, A.E. Zamora, D.F. Boyd, et al. 2018. Lung γδ T cells mediate protective responses during neonatal influenza infection that are associated with type 2 immunity. Immunity 49: 531-544.e536.PubMedPubMedCentralCrossRef
56.
go back to reference Nie, M., Q. Zeng, L. Xi, Y. Tang, R. Luo, and W. Liu. 2021. The effect of IL-35 on the expression of nasal epithelial-derived proinflammatory cytokines. Mediators of Inflammation 2021: 1110671.PubMedPubMedCentralCrossRef Nie, M., Q. Zeng, L. Xi, Y. Tang, R. Luo, and W. Liu. 2021. The effect of IL-35 on the expression of nasal epithelial-derived proinflammatory cytokines. Mediators of Inflammation 2021: 1110671.PubMedPubMedCentralCrossRef
57.
go back to reference Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 2013. The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annual Review of Immunology 31: 563–604.PubMedCrossRef Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 2013. The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annual Review of Immunology 31: 563–604.PubMedCrossRef
58.
go back to reference Jaligama, S., V.S. Patel, P. Wang, A. Sallam, J. Harding, M. Kelley, et al. 2018. Radical containing combustion derived particulate matter enhance pulmonary Th17 inflammation via the aryl hydrocarbon receptor. Particle and Fibre Toxicology 15: 20.PubMedPubMedCentralCrossRef Jaligama, S., V.S. Patel, P. Wang, A. Sallam, J. Harding, M. Kelley, et al. 2018. Radical containing combustion derived particulate matter enhance pulmonary Th17 inflammation via the aryl hydrocarbon receptor. Particle and Fibre Toxicology 15: 20.PubMedPubMedCentralCrossRef
59.
go back to reference Hammad, H., and B.N. Lambrecht. 2015. Barrier epithelial cells and the control of type 2 immunity. Immunity 43: 29–40.PubMedCrossRef Hammad, H., and B.N. Lambrecht. 2015. Barrier epithelial cells and the control of type 2 immunity. Immunity 43: 29–40.PubMedCrossRef
60.
go back to reference Roan, F., K. Obata-Ninomiya, and S.F. Ziegler. 2019. Epithelial cell-derived cytokines: More than just signaling the alarm. The Journal of Clinical Investigation 129: 1441–1451.PubMedPubMedCentralCrossRef Roan, F., K. Obata-Ninomiya, and S.F. Ziegler. 2019. Epithelial cell-derived cytokines: More than just signaling the alarm. The Journal of Clinical Investigation 129: 1441–1451.PubMedPubMedCentralCrossRef
61.
go back to reference Deckers, J., D. Sichien, M. Plantinga, J. Van Moorleghem, M. Vanheerswynghels, E. Hoste, et al. 2017. Epicutaneous sensitization to house dust mite allergen requires interferon regulatory factor 4-dependent dermal dendritic cells. The Journal of Allergy and Clinical Immunology 140: 1364-1377.e1362.PubMedCrossRef Deckers, J., D. Sichien, M. Plantinga, J. Van Moorleghem, M. Vanheerswynghels, E. Hoste, et al. 2017. Epicutaneous sensitization to house dust mite allergen requires interferon regulatory factor 4-dependent dermal dendritic cells. The Journal of Allergy and Clinical Immunology 140: 1364-1377.e1362.PubMedCrossRef
62.
go back to reference Agalioti, T., E.J. Villablanca, S. Huber, and N. Gagliani. 2018. T(H)17 cell plasticity: The role of dendritic cells and molecular mechanisms. Journal of Autoimmunity 87: 50–60.PubMedCrossRef Agalioti, T., E.J. Villablanca, S. Huber, and N. Gagliani. 2018. T(H)17 cell plasticity: The role of dendritic cells and molecular mechanisms. Journal of Autoimmunity 87: 50–60.PubMedCrossRef
63.
go back to reference Van Dyken, S.J., J.C. Nussbaum, J. Lee, A.B. Molofsky, H.E. Liang, J.L. Pollack, et al. 2016. A tissue checkpoint regulates type 2 immunity. Nature Immunology 17: 1381–1387.PubMedPubMedCentralCrossRef Van Dyken, S.J., J.C. Nussbaum, J. Lee, A.B. Molofsky, H.E. Liang, J.L. Pollack, et al. 2016. A tissue checkpoint regulates type 2 immunity. Nature Immunology 17: 1381–1387.PubMedPubMedCentralCrossRef
64.
go back to reference Willart, M.A., K. Deswarte, P. Pouliot, H. Braun, R. Beyaert, B.N. Lambrecht, et al. 2012. Interleukin-1α controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. Journal of Experimental Medicine 209: 1505–1517.PubMedPubMedCentralCrossRef Willart, M.A., K. Deswarte, P. Pouliot, H. Braun, R. Beyaert, B.N. Lambrecht, et al. 2012. Interleukin-1α controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. Journal of Experimental Medicine 209: 1505–1517.PubMedPubMedCentralCrossRef
65.
go back to reference Vocca, L., C. Di Sano, C.G. Uasuf, A. Sala, L. Riccobono, S. Gangemi, et al. 2015. IL-33/ST2 axis controls Th2/IL-31 and Th17 immune response in allergic airway diseases. Immunobiology 220: 954–963.PubMedCrossRef Vocca, L., C. Di Sano, C.G. Uasuf, A. Sala, L. Riccobono, S. Gangemi, et al. 2015. IL-33/ST2 axis controls Th2/IL-31 and Th17 immune response in allergic airway diseases. Immunobiology 220: 954–963.PubMedCrossRef
66.
go back to reference Huang, C.H., E.X. Loo, I.C. Kuo, G.H. Soh, D.L. Goh, B.W. Lee, et al. 2011. Airway inflammation and IgE production induced by dust mite allergen-specific memory/effector Th2 cell line can be effectively attenuated by IL-35. The Journal of Immunology 187: 462–471.PubMedCrossRef Huang, C.H., E.X. Loo, I.C. Kuo, G.H. Soh, D.L. Goh, B.W. Lee, et al. 2011. Airway inflammation and IgE production induced by dust mite allergen-specific memory/effector Th2 cell line can be effectively attenuated by IL-35. The Journal of Immunology 187: 462–471.PubMedCrossRef
68.
go back to reference Krieg, A.M., A.K. Yi, S. Matson, T.J. Waldschmidt, G.A. Bishop, R. Teasdale, et al. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546–549.PubMedCrossRef Krieg, A.M., A.K. Yi, S. Matson, T.J. Waldschmidt, G.A. Bishop, R. Teasdale, et al. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546–549.PubMedCrossRef
69.
go back to reference Kline, J.N., and Z.K. Ballas. 2002. DNA immunomodulation of asthma. Clinical Allergy and Immunology 16: 551–564.PubMed Kline, J.N., and Z.K. Ballas. 2002. DNA immunomodulation of asthma. Clinical Allergy and Immunology 16: 551–564.PubMed
70.
go back to reference Wirtz, S., C. Becker, M.C. Fantini, E.E. Nieuwenhuis, I. Tubbe, P.R. Galle, et al. 2005. EBV-induced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-kappa B activation. The Journal of Immunology 174: 2814–2824.PubMedCrossRef Wirtz, S., C. Becker, M.C. Fantini, E.E. Nieuwenhuis, I. Tubbe, P.R. Galle, et al. 2005. EBV-induced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-kappa B activation. The Journal of Immunology 174: 2814–2824.PubMedCrossRef
71.
go back to reference Kim, D.H., J.H. Sohn, H.J. Park, J.H. Lee, J.W. Park, and J.M. Choi. 2016. CpG oligodeoxynucleotide inhibits cockroach-induced asthma via induction of IFN-γ+ Th1 cells or Foxp3+ regulatory T cells in the lung. Allergy, Asthma & Immunology Research 8: 264–275.CrossRef Kim, D.H., J.H. Sohn, H.J. Park, J.H. Lee, J.W. Park, and J.M. Choi. 2016. CpG oligodeoxynucleotide inhibits cockroach-induced asthma via induction of IFN-γ+ Th1 cells or Foxp3+ regulatory T cells in the lung. Allergy, Asthma & Immunology Research 8: 264–275.CrossRef
72.
go back to reference Senti, G., P. Johansen, Susanne Haug, C. Bull, C. Gottschaller, P. Müller et al. 2009. Use of A-type CpG oligodeoxynucleotides as an adjuvant in allergen-specific immunotherapy in humans: A phase I/IIa clinical trial. Clinical and Experimental Allergy 39: 562–570.PubMedCrossRef Senti, G., P. Johansen, Susanne Haug, C. Bull, C. Gottschaller, P. Müller et al. 2009. Use of A-type CpG oligodeoxynucleotides as an adjuvant in allergen-specific immunotherapy in humans: A phase I/IIa clinical trial. Clinical and Experimental Allergy 39: 562–570.PubMedCrossRef
Metadata
Title
Interplay of IL-33 and IL-35 Modulates Th2/Th17 Responses in Cigarette Smoke Exposure HDM-Induced Asthma
Authors
Jing Liu
Beiting Su
Peizhi Tao
Xuena Yang
Li Zheng
Yusen Lin
Xiaoling Zou
Hailing Yang
Wenbin Wu
Tiantuo Zhang
Hongtao Li
Publication date
22-09-2023
Publisher
Springer US
Published in
Inflammation / Issue 1/2024
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-023-01902-6

Other articles of this Issue 1/2024

Inflammation 1/2024 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine
Webinar | 06-02-2024 | 20:00 (CET)

Mastering chronic pancreatitis pain: A multidisciplinary approach and practical solutions

Severe pain is the most common symptom of chronic pancreatitis. In this webinar, experts share the latest insights in pain management for chronic pancreatitis patients. Experts from a range of disciplines discuss pertinent cases and provide practical suggestions for use within clinical practice.

Sponsored by: Viatris

Developed by: Springer Healthcare