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IL-27 is produced by mononuclear phagocytes and unfolds pleiotropic immune-modulatory functions through ligation to IL-27 receptor \u03b1 (IL-27RA). Although IL-27 is known to contribute to immunity and to limit inflammation after various infections, its relevance for host defense against multicellular parasites is still poorly defined. Here, we investigated the role of IL-27 during infection with the soil-transmitted hookworm, Nippostrongylus brasiliensis, in its early host intrapulmonary life cycle. IL-27(p28) was detectable in bronchoalveolar lavage fluid of C57BL\/6J wild-type mice on day 1 after s.c. inoculation. IL-27RA expression was most abundant on lung-invading \u03b3\u03b4 T cells. Il27ra\u2212\/\u2212 mice showed increased lung parasite burden together with aggravated pulmonary hemorrhage and higher alveolar total protein leakage as a surrogate for epithelial\u2013vascular barrier disruption. Conversely, injections of recombinant mouse (rm)IL-27 into wild-type mice reduced lung injury and parasite burden. In multiplex screens, higher airway accumulations of IL-6, TNF-\u03b1, and MCP-3 (CCL7) were observed in Il27ra\u2212\/\u2212 mice, whereas rmIL-27 treatment showed a reciprocal effect. Importantly, \u03b3\u03b4 T cell numbers in airways were enhanced by endogenous or administered IL-27. Further analysis revealed a direct antihelminthic function of IL-27 on \u03b3\u03b4 T cells as adoptive intratracheal transfer of rmIL-27\u2013treated \u03b3\u03b4 T cells during primary N. brasiliensis lung infection conferred protection in mice. In summary, this report demonstrates protective functions of IL-27 to control the early lung larval stage of hookworm infection.<\/jats:p>","DOI":"10.4049\/jimmunol.2000945","type":"journal-article","created":{"date-parts":[[2022,3,30]],"date-time":"2022-03-30T13:25:20Z","timestamp":1648646720000},"page":"2008-2018","source":"Crossref","is-referenced-by-count":6,"title":["IL-27 Enhances \u03b3\u03b4 T Cell\u2013Mediated Innate Resistance to Primary Hookworm Infection in the Lungs"],"prefix":"10.1093","volume":"208","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5705-5470","authenticated-orcid":false,"given":"Arjun","family":"Sharma","sequence":"first","affiliation":[{"name":"Pulmonary Center, Department of Medicine, Boston University School of Medicine , Boston, Massachusetts"},{"name":"Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University Mainz , Mainz,","place":["Germany"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jason B","family":"Noon","sequence":"additional","affiliation":[{"name":"Pulmonary Center, Department of Medicine, Boston University School of Medicine , Boston, Massachusetts"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9593-505X","authenticated-orcid":false,"given":"Konstantinos","family":"Kontodimas","sequence":"additional","affiliation":[{"name":"Pulmonary Center, Department of Medicine, Boston University School of Medicine , Boston, Massachusetts"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5369-1958","authenticated-orcid":false,"given":"Lucien P","family":"Garo","sequence":"additional","affiliation":[{"name":"Pulmonary Center, Department of Medicine, Boston University School of Medicine , Boston, Massachusetts"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8054-5726","authenticated-orcid":false,"given":"Johannes","family":"Platten","sequence":"additional","affiliation":[{"name":"Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University Mainz , Mainz,","place":["Germany"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1938-2507","authenticated-orcid":false,"given":"Lee J","family":"Quinton","sequence":"additional","affiliation":[{"name":"Pulmonary Center, Department of Medicine, Boston University School of Medicine , Boston, Massachusetts"},{"name":"Division of Infectious Disease and Immunology, Department of Medicine, University of Massachusetts Chan Medical School , Worcester, MA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1590-8869","authenticated-orcid":false,"suffix":"Jr.","given":"Joseph F","family":"Urban","sequence":"additional","affiliation":[{"name":"Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory and Beltsville Human Nutrition Research Center, Diet, Genomics, and Immunology Laboratory, U.S. Department of Agriculture , Beltsville, MD"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0696-2636","authenticated-orcid":false,"given":"Christoph","family":"Reinhardt","sequence":"additional","affiliation":[{"name":"Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University Mainz , Mainz,","place":["Germany"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2773-1033","authenticated-orcid":false,"given":"Markus","family":"Bosmann","sequence":"additional","affiliation":[{"name":"Pulmonary Center, Department of Medicine, Boston University School of Medicine , Boston, Massachusetts"},{"name":"Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University Mainz , Mainz,","place":["Germany"]},{"name":"Research Center for Immunotherapy, University Medical Center of the Johannes Gutenberg-University Mainz , Mainz,","place":["Germany"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2022,4,15]]},"reference":[{"key":"2025021009024678700_r1","doi-asserted-by":"crossref","first-page":"16088","DOI":"10.1038\/nrdp.2016.88","article-title":"Hookworm infection","volume":"2","author":"Loukas","year":"2016","journal-title":"Nat. Rev. Dis. Primers"},{"key":"2025021009024678700_r2","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1186\/1756-3305-7-37","article-title":"Global numbers of infection and disease burden of soil transmitted helminth infections in 2010","volume":"7","author":"Pullan","year":"2014","journal-title":"Parasit. Vectors"},{"key":"2025021009024678700_r3","doi-asserted-by":"crossref","first-page":"e0005424","DOI":"10.1371\/journal.pntd.0005424","article-title":"The Global Burden of Disease Study 2013: what does it mean for the NTDs?","volume":"11","author":"Herricks","year":"2017","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2025021009024678700_r4","doi-asserted-by":"crossref","first-page":"e291","DOI":"10.1371\/journal.pntd.0000291","article-title":"Hookworm-related anaemia among pregnant women: a systematic review","volume":"2","author":"Brooker","year":"2008","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2025021009024678700_r5","doi-asserted-by":"crossref","first-page":"776","DOI":"10.1111\/j.1365-3156.2010.02542.x","article-title":"Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review","volume":"15","author":"Smith","year":"2010","journal-title":"Trop. Med. Int. Health"},{"key":"2025021009024678700_r6","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1056\/NEJMra032492","article-title":"Hookworm infection","volume":"351","author":"Hotez","year":"2004","journal-title":"N. Engl. J. Med."},{"key":"2025021009024678700_r7","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.hoc.2015.11.002","article-title":"The global burden of anemia","volume":"30","author":"Kassebaum","year":"2016","journal-title":"Hematol. Oncol. Clin. North Am."},{"key":"2025021009024678700_r8","first-page":"467","volume-title":"Disease Control Priorities in Developing Countries.","author":"Hotez","year":"2006","edition":"2nd"},{"key":"2025021009024678700_r9","doi-asserted-by":"crossref","first-page":"20130435","DOI":"10.1098\/rstb.2013.0435","article-title":"The coverage and frequency of mass drug administration required to eliminate persistent transmission of soil-transmitted helminths","volume":"369","author":"Anderson","year":"2014","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"2025021009024678700_r10","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1016\/S0140-6736(06)68653-4","article-title":"Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm","volume":"367","author":"Bethony","year":"2006","journal-title":"Lancet"},{"key":"2025021009024678700_r11","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1017\/S003118201700138X","article-title":"Recombinant subunit vaccines for soil-transmitted helminths","volume":"144","author":"Noon","year":"2017","journal-title":"Parasitology"},{"key":"2025021009024678700_r12","doi-asserted-by":"crossref","DOI":"10.1002\/0471142735.im1912s55","article-title":"Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus","volume-title":"Curr. Protoc. 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Immunol."},{"key":"2025021009024678700_r15","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1038\/nature23469","article-title":"Neuronal regulation of type 2 innate lymphoid cells via neuromedin U","volume":"549","author":"Cardoso","year":"2017","journal-title":"Nature"},{"key":"2025021009024678700_r16","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1038\/ni.2984","article-title":"Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion","volume":"15","author":"Chen","year":"2014","journal-title":"Nat. Immunol."},{"key":"2025021009024678700_r17","doi-asserted-by":"crossref","first-page":"74","DOI":"10.3389\/fimmu.2013.00074","article-title":"Development of CD4 T cell dependent immunity against N. brasiliensis infection","volume":"4","author":"Harvie","year":"2013","journal-title":"Front. 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Nanotechnol."},{"key":"2025021009024678700_r22","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1016\/S1074-7613(02)00324-2","article-title":"IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4+ T cells","volume":"16","author":"Pflanz","year":"2002","journal-title":"Immunity"},{"key":"2025021009024678700_r23","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1038\/nature06306","article-title":"The inhibitory cytokine IL-35 contributes to regulatory T-cell function","volume":"450","author":"Collison","year":"2007","journal-title":"Nature"},{"key":"2025021009024678700_r24","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.bbrc.2018.12.101","article-title":"The pituitary gland prevents shock-associated death by controlling multiple inflammatory mediators","volume":"509","author":"Sharma","year":"2019","journal-title":"Biochem. Biophys. Res. 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Redox Signal."},{"key":"2025021009024678700_r29","doi-asserted-by":"crossref","first-page":"1384","DOI":"10.1038\/mi.2016.20","article-title":"IL-27 suppresses type 2 immune responses in vivo via direct effects on group 2 innate lymphoid cells","volume":"9","author":"Mchedlidze","year":"2016","journal-title":"Mucosal Immunol."},{"key":"2025021009024678700_r30","doi-asserted-by":"crossref","first-page":"5626","DOI":"10.4049\/jimmunol.173.9.5626","article-title":"The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity","volume":"173","author":"Artis","year":"2004","journal-title":"J. Immunol."},{"key":"2025021009024678700_r31","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1038\/ni.3309","article-title":"Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses","volume":"17","author":"Moro","year":"2016","journal-title":"Nat. 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