دورية أكاديمية

IL-17A both initiates, via IFNγ suppression, and limits the pulmonary type-2 immune response to nematode infection.

التفاصيل البيبلوغرافية
العنوان: IL-17A both initiates, via IFNγ suppression, and limits the pulmonary type-2 immune response to nematode infection.
المؤلفون: Ajendra J; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK., Chenery AL; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK., Parkinson JE; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK., Chan BHK; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK., Pearson S; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK., Colombo SAP; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK.; Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK., Boon L; Bioceros, Member of Polpharma Biologics, Yalelaan 46, 3584, CM, Utrecht, The Netherlands., Grencis RK; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK., Sutherland TE; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK. tara.sutherland@manchester.ac.uk., Allen JE; Lydia Becker Institute for Immunology & Infection, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK. judi.allen@manchester.ac.uk.; Wellcome Centre for Cell-Matrix Research, Manchester, M13 9PT, UK. judi.allen@manchester.ac.uk.
المصدر: Mucosal immunology [Mucosal Immunol] 2020 Nov; Vol. 13 (6), pp. 958-968. Date of Electronic Publication: 2020 Jul 07.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Elsevier Country of Publication: United States NLM ID: 101299742 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1935-3456 (Electronic) Linking ISSN: 19330219 NLM ISO Abbreviation: Mucosal Immunol Subsets: MEDLINE
أسماء مطبوعة: Publication: 2023- : [New York, NY] : Elsevier
Original Publication: New York, NY : Nature Pub. Group, c2008-
مواضيع طبية MeSH: Interleukin-17/*metabolism , Lung/*immunology , Nippostrongylus/*physiology , Strongylida Infections/*immunology , Th2 Cells/*immunology, Animals ; Cells, Cultured ; Female ; Immune Tolerance ; Immunity, Innate ; Interferon-gamma/metabolism ; Interleukin-17/genetics ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout
مستخلص: Nippostrongylus brasiliensis is a well-defined model of type-2 immunity but the early lung-migrating phase is dominated by innate IL-17A production. In this study, we confirm previous observations that Il17a-KO mice infected with N. brasiliensis exhibit an impaired type-2 immune response. Transcriptional profiling of the lung on day 2 of N. brasiliensis infection revealed an increased Ifng signature in Il17a-KO mice confirmed by enhanced IFNγ protein production in lung lymphocyte populations. Depletion of early IFNγ rescued type-2 immune responses in the Il17a-KO mice demonstrating that IL-17A-mediated suppression of IFNγ promotes type-2 immunity. Notably, later in infection, once the type-2 response was established, IL-17A limited the magnitude of the type-2 response. IL-17A regulation of type-2 immunity was lung-specific and infection with Trichuris muris revealed that IL-17A promotes a type-2 immune response in the lung even when infection is restricted to the intestine. Together our data reveal IL-17A as a major regulator of pulmonary type-2 immunity such that IL-17A supports early development of a protective type-2 response by suppression of IFNγ but subsequently limits excessive type-2 responses. A failure of this feedback loop may contribute to conditions such as severe asthma, characterised by combined elevation of IL-17 and type-2 cytokines.
التعليقات: Comment in: Mucosal Immunol. 2020 Nov;13(6):849-851. (PMID: 32728131)
References: Papotto, P. H., Ribot, J. C. & Silva-Santos, B. IL-17 + γδ T cells as kick-starters of inflammation. Nat. Immunol. 18, 604–611 (2017). (PMID: 28518154)
Iwakura, Y., Ishigame, H., Saijo, S. & Nakae, S. Functional specialization of interleukin-17 family members. Immunity 34, 149–162 (2011). (PMID: 21349428)
Allen, J. E. & Maizels, R. M. Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 11, 375–388 (2011). (PMID: 21610741)
Mbow, M. et al. T-helper 17 cells are associated with pathology in human schistosomiasis. J. Infect. Dis. 207, 186–195 (2013). (PMID: 23087431)
Rutitzky, L. I. & Stadecker, M. J. Exacerbated egg-induced immunopathology in murine Schistosoma mansoni infection is primarily mediated by IL-17 and restrained by IFN-γ. Eur. J. Immunol. 41, 2677–2687 (2011). (PMID: 216609333679923)
Katawa, G. et al. Hyperreactive onchocerciasis is characterized by a combination of Th17-Th2 immune responses and reduced regulatory T cells. PLoS Negl. Trop. Dis. 9, e3414 (2015). (PMID: 255692104288720)
Choy, D. F. et al. TH2 and TH17 inflammatory pathways are reciprocally regulated in asthma. Sci. Transl. Med. 7, 301ra129 (2015). (PMID: 26290411)
Sutherland, T. E. et al. Chitinase-like proteins promote IL-17-mediated neutrophilia in a tradeoff between nematode killing and host damage. Nat. Immunol. 15, 1116–1125 (2014). (PMID: 2532675125326751)
Molofsky, A. B. et al. Interleukin-33 and interferon-γ counter-regulate group 2 innate lymphoid cell activation during immune perturbation. Immunity 43, 161–174 (2015). (PMID: 260924694512852)
Newcomb, D. C. et al. A Functional IL-13 receptor is expressed on polarized murine CD4 + Th17 cells and IL-13 signaling attenuates Th17 cytokine production. J. Immunol. 182, 5317–5321 (2009). (PMID: 193807783711250)
Chen, F. et al. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat. Immunol. 15, 938–946 (2014). (PMID: 251733464479254)
Nakajima, S. et al. IL-17A as an inducer for Th2 immune responses in murine atopic dermatitis models. J. Invest. Dermatol. 134, 2122–2130 (2014). (PMID: 24480880)
Nakae, S. et al. Antigen-specific T cell sensitization is impaired in Il-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17, 375–387 (2002). (PMID: 12354389)
Chenuet, P. et al. Neutralization of either IL-17A or IL-17F is sufficient to inhibit house dust mite induced allergic asthma in mice. Clin. Sci. 131, 2533–2548 (2017).
Campbell, L. et al. ILC2s mediate systemic innate protection by priming mucus production at distal mucosal sites. J. Exp. Med. 216, 2714–2723 (2019). (PMID: 315824166888984)
Minutti, C. M. et al. Epidermal growth factor receptor expression licenses type-2 Helper T cells to function in a T cell receptor-independent fashion. Immunity 47, 710–722.e6 (2017). (PMID: 290459025654729)
Redpath, S. A. et al. ICOS controls Foxp3+ regulatory T-cell expansion, maintenance and IL-10 production during helminth infection. Eur. J. Immunol. 43, 705–715 (2013). (PMID: 233192953615169)
Terrazas, L. I., Montero, D., Terrazas, C. A., Reyes, J. L. & Rodríguez-Sosa, M. Role of the programmed Death-1 pathway in the suppressive activity of alternatively activated macrophages in experimental cysticercosis. Int. J. Parasitol. 35, 1349–1358 (2005). (PMID: 16126211)
Ardain, A. et al. Group 3 innate lymphoid cells mediate early protective immunity against tuberculosis. Nature 570, 528–532 (2019). (PMID: 311680926626542)
Osborne, L. C. et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science. 345, 578–582 (2014). (PMID: 250827044548887)
Ribot, J. C. et al. CD27 is a thymic determinant of the balance between interferon-γ- and interleukin 17-producing γδ T cell subsets. Nat. Immunol. 10, 427–436 (2009). (PMID: 192707124167721)
Bancroft, A. J., McKenzie, A. N. & Grencis, R. K. A critical role for IL-13 in resistance to intestinal nematode infection. J. Immunol. 160, 3453–3461 (1998). (PMID: 9531306)
Bancroft, A. J., Else, K. J. & Grencis, R. K. Low‐level infection with Trichuris muris significantly affects the polarization of the CD4 response. Eur. J. Immunol. 24, 3113–3118 (1994). (PMID: 7805740)
Filbey, K. J. et al. Intestinal helminth infection promotes IL-5- and CD4 + T cell-dependent immunity in the lung against migrating parasites. Mucosal Immunol. 12, 352–362 (2019). (PMID: 30401814)
Lajoie, S. et al. Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat. Immunol. 11, 928–935 (2010). (PMID: 208024842943538)
Díaz, A. & Allen, J. E. Mapping immune response profiles: The emerging scenario from helminth immunology. Eur. J. Immunol. 37, 3319–3326 (2007). (PMID: 18000958)
Wakashin, H., Hirose, K., Iwamoto, I. & Nakajima, H. Role of IL-23-Th17 cell axis in allergic airway inflammation. Int. Arch. Allergy Immunol. 149 Suppl 1, 108–112 (2009). (PMID: 19494515)
Wang, X. et al. IL-17 constrains natural killer cell activity by restraining IL-15-driven cell maturation via SOCS3. Proc. Natl Acad. Sci. USA. 116, 17409–17418 (2019). (PMID: 31405974)
Moroda, M., Takamoto, M., Iwakura, Y., Nakayama, J. & Aosai, F. Interleukin-17 adeficient mice are highly susceptible to Toxoplasma gondii infection due to excessively induced T. gondii HSP70 and interferon gamma production. Infect. Immun. 85, e00399–17 (2017). (PMID: 288939135695131)
Ritter, M. et al. Absence of IL-17A in Litomosoides sigmodontis-infected mice influences worm development and drives elevated filarial-specific IFN-γ. Parasitol. Res. 117, 2665–2675 (2018). (PMID: 299313946061040)
Zhang, Y. et al. Lack of IL-17 signaling decreases liver fibrosis in murine schistosomiasis japonica. Int. Immunol. 27, 317–325 (2015). (PMID: 25840437)
Li, L. et al. IL-17 produced by neutrophils regulates IFN-γ-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J. Clin. Invest. 120, 331–342 (2010). (PMID: 20038794)
Lin, Y. et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31, 799–810 (2009). (PMID: 198534812789998)
Taylor, B. C. et al. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J. Exp. Med. 206, 655–667 (2009). (PMID: 1927362619273626)
Newcomb, D. C. et al. IL-13 regulates Th17 secretion of IL-17A in an IL-10–dependent manner. J. Immunol. 188, 1027–1035 (2012). (PMID: 22210911)
Dyken, S. J. Van et al. Chitin activates parallel immune modules that direct distinct inflammatory responses via innate lymphoid type 2 and γδ T cells. Immunity 40, 414–424 (2014). (PMID: 246311574019510)
Chen, F. et al. An essential role for T H 2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 18, 260–266 (2012). (PMID: 222457793274634)
Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 1–8 (2001).
Hirota, K. et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12, 255–263 (2011). (PMID: 212787373040235)
Lawrence, R. A., Gray, C. A., Osborne, J. & Maizels, R. M. Nippostrongylus brasiliensis: cytokine responses and nematode expulsion in normal and IL-4 deficient mice. Exp. Parasitol. 84, 65–73 (1996). (PMID: 8888733)
Holland, M. J., Harcus, Y. M., Riches, P. L. & Maizels, R. M. Proteins secreted by the parasitic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses. Eur. J. Immunol. 30, 1977–1987 (2000). (PMID: 10940887)
Hayes, K. S. et al. Chronic trichuris muris infection causes neoplastic change in the intestine and exacerbates tumour formation in APC min/+ mice. PLoS Negl. Trop. Dis. 11, e0005708 (2017). (PMID: 286509855501682)
Ritchie, M. E. et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015). (PMID: 2560579225605792)
معلومات مُعتمدة: MR/K01207X/2 United Kingdom MRC_ Medical Research Council; 103132/Z/13/Z United Kingdom WT_ Wellcome Trust; MR/K01207X/1 United Kingdom MRC_ Medical Research Council; United Kingdom WT_ Wellcome Trust; 106898/A/15/Z United Kingdom WT_ Wellcome Trust; Z10661/Z/18/Z United Kingdom WT_ Wellcome Trust; MRFAUK-2015-302 United Kingdom MRC_ Medical Research Council; MRF_MRF-009-0002-RG-SUTHE United Kingdom MRF MRF
المشرفين على المادة: 0 (Interleukin-17)
82115-62-6 (Interferon-gamma)
تواريخ الأحداث: Date Created: 20200709 Date Completed: 20210712 Latest Revision: 20240306
رمز التحديث: 20240306
مُعرف محوري في PubMed: PMC7567645
DOI: 10.1038/s41385-020-0318-2
PMID: 32636457
قاعدة البيانات: MEDLINE
الوصف
تدمد:1935-3456
DOI:10.1038/s41385-020-0318-2