{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,26]],"date-time":"2026-08-26T07:16:07Z","timestamp":1787728567279,"version":"build-2784847793"},"reference-count":56,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2020,12,1]],"date-time":"2020-12-01T00:00:00Z","timestamp":1606780800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/100000038","name":"U.S. Food and Drug Administration","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,12,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>No licensed vaccine exists against visceral leishmaniasis (VL), a disease caused by the Leishmania donovani parasite. We have previously reported both macrophages and dendritic cells play important role in the protection induced by a live attenuated centrin gene\u2013deleted L. donovani (LdCen\u2212\/\u2212) parasite vaccine. The role of neutrophils in orchestrating the initial innate response to pathogens is widely recognized. To investigate the early interaction of LdCen\u2212\/\u2212 with neutrophils, we immunized mice intradermally in the ear pinna with LdCen\u2212\/\u2212. Compared with LdWT infection, LdCen\u2212\/\u2212 parasites induced higher recruitment of neutrophils to the ear dermis and ear draining lymph nodes (dLN) as early as 6\u201318 h after immunization, which were predominantly proinflammatory in nature. Neutrophils from ear dLN of LdCen\u2212\/\u2212-immunized mice exhibited heightened expression of costimulatory molecules and attenuated expression of coinhibitory molecules necessary for higher T cell activation. Further phenotypic characterization revealed heterogeneous neutrophil populations containing N\u03b1 and N\u03b2 subtypes in the ear dLN. Of the two, the parasitized N\u03b1 subset from LdCen\u2212\/\u2212-immunized mice exhibited much stronger Ag-specific CD4+ T cell proliferation ex vivo. Adoptive transfer of neutrophils bearing LdCen\u2212\/\u2212 parasites induced an increased Th1 response in naive mice. Importantly, neutrophil depletion significantly abrogated Ag-specific CD4+ T cell proliferation in LdCen\u2212\/\u2212-immunized mice and impaired protection against virulent challenge. Conversely, replenishing of neutrophils significantly restored the LdCen\u2212\/\u2212 -induced host-protective response. These results suggest that neutrophils are indispensable for protective immunity induced by LdCen\u2212\/\u2212 parasite vaccine.<\/jats:p>","DOI":"10.4049\/jimmunol.2000829","type":"journal-article","created":{"date-parts":[[2020,11,11]],"date-time":"2020-11-11T19:35:24Z","timestamp":1605123324000},"page":"3333-3347","source":"Crossref","is-referenced-by-count":19,"title":["Essential Role of Neutrophils in the Protective Immune Response Induced by a Live Attenuated <i>Leishmania<\/i> Vaccine"],"prefix":"10.1093","volume":"205","author":[{"given":"Parna","family":"Bhattacharya","sequence":"first","affiliation":[{"name":"Division of Emerging and Transfusion Transmitted Disease, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0069-7867","authenticated-orcid":false,"given":"Ranadhir","family":"Dey","sequence":"additional","affiliation":[{"name":"Division of Emerging and Transfusion Transmitted Disease, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ankit","family":"Saxena","sequence":"additional","affiliation":[{"name":"Flow Cytometry Core, National Heart, Lung, and Blood Institute, National Institutes of Health , Bethesda, MD 20892"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6288-7335","authenticated-orcid":false,"given":"Subir","family":"Karmakar","sequence":"additional","affiliation":[{"name":"Division of Emerging and Transfusion Transmitted Disease, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0294-8834","authenticated-orcid":false,"given":"Nevien","family":"Ismail","sequence":"additional","affiliation":[{"name":"Division of Emerging and Transfusion Transmitted Disease, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6557-8220","authenticated-orcid":false,"given":"Sreenivas","family":"Gannavaram","sequence":"additional","affiliation":[{"name":"Division of Emerging and Transfusion Transmitted Disease, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pradeep K","family":"Dagur","sequence":"additional","affiliation":[{"name":"Flow Cytometry Core, National Heart, Lung, and Blood Institute, National Institutes of Health , Bethesda, MD 20892"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monika","family":"Satoskar","sequence":"additional","affiliation":[{"name":"Northeast Ohio Medical University , Rootstown, OH 44272"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sanika","family":"Satoskar","sequence":"additional","affiliation":[{"name":"Northeast Ohio Medical University , Rootstown, OH 44272"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia","family":"De Paoli","sequence":"additional","affiliation":[{"name":"Office of Blood Research and Review, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kazuyo","family":"Takeda","sequence":"additional","affiliation":[{"name":"Microscopy and Imaging Core Facility, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8118-5275","authenticated-orcid":false,"suffix":"Jr.","given":"John Philip","family":"McCoy","sequence":"additional","affiliation":[{"name":"Flow Cytometry Core, National Heart, Lung, and Blood Institute, National Institutes of Health , Bethesda, MD 20892"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4941-1620","authenticated-orcid":false,"given":"Hira L","family":"Nakhasi","sequence":"additional","affiliation":[{"name":"Division of Emerging and Transfusion Transmitted Disease, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration , Silver Spring, MD 20993"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,12,15]]},"reference":[{"key":"2025030417510090200_r1","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/s13071-017-1974-2","article-title":"Review of \u201cMathematical models for neglected tropical diseases: essential tools for control and elimination, part B\u201d edited by Maria-Gloria Basanez and Roy M. Anderson","volume":"10","author":"Spear","year":"2017","journal-title":"Parasit Vectors"},{"key":"2025030417510090200_r2","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0003131","article-title":"Visceral leishmaniasis in Ethiopia: an evolving disease","volume":"8","author":"Leta","year":"2014","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2025030417510090200_r3","doi-asserted-by":"crossref","DOI":"10.1155\/2018\/8463097","article-title":"Incidence and trends of leishmaniasis and its risk factors in Humera, Western Tigray","volume":"2018","author":"Gebremichael Tedla","year":"2018","journal-title":"J. Parasitol. Res."},{"key":"2025030417510090200_r4","doi-asserted-by":"crossref","first-page":"3966","DOI":"10.1128\/IAI.00770-13","article-title":"Leishmania amazonensis amastigotes trigger neutrophil activation but resist neutrophil microbicidal mechanisms","volume":"81","author":"Carlsen","year":"2013","journal-title":"Infect. Immun."},{"key":"2025030417510090200_r5","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1126\/science.1159194","article-title":"In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. [Published erratum appears in 2008 Science 322: 1634.]","volume":"321","author":"Peters","year":"2008","journal-title":"Science"},{"key":"2025030417510090200_r6","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1038\/nri3399","article-title":"Neutrophil recruitment and function in health and inflammation","volume":"13","author":"Kolaczkowska","year":"2013","journal-title":"Nat. Rev. Immunol."},{"key":"2025030417510090200_r7","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.pt.2016.02.003","article-title":"Different leishmania species drive distinct neutrophil functions","volume":"32","author":"Hurrell","year":"2016","journal-title":"Trends Parasitol."},{"key":"2025030417510090200_r8","doi-asserted-by":"crossref","first-page":"508","DOI":"10.3389\/fimmu.2014.00508","article-title":"Neutrophil-derived cytokines: facts beyond expression","volume":"5","author":"Tecchio","year":"2014","journal-title":"Front. Immunol."},{"key":"2025030417510090200_r9","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1016\/j.it.2009.07.007","article-title":"Polymorphonuclear neutrophils and T lymphocytes: strange bedfellows or brothers in arms?","volume":"30","author":"M\u00fcller","year":"2009","journal-title":"Trends Immunol."},{"key":"2025030417510090200_r10","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1038\/nri3024","article-title":"Neutrophils in the activation and regulation of innate and adaptive immunity","volume":"11","author":"Mantovani","year":"2011","journal-title":"Nat. Rev. Immunol."},{"key":"2025030417510090200_r11","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1002\/eji.201344195","article-title":"When neutrophils meet T cells: beginnings of a tumultuous relationship with underappreciated potential","volume":"44","author":"Kalyan","year":"2014","journal-title":"Eur. J. Immunol."},{"key":"2025030417510090200_r12","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1016\/j.it.2007.06.002","article-title":"Neutrophil granules: a library of innate immunity proteins","volume":"28","author":"Borregaard","year":"2007","journal-title":"Trends Immunol."},{"key":"2025030417510090200_r13","doi-asserted-by":"crossref","first-page":"E1333","DOI":"10.1073\/pnas.1424341112","article-title":"NF\u03baB activation by modified vaccinia virus as a novel strategy to enhance neutrophil migration and HIV-specific T-cell responses","volume":"112","author":"Di Pilato","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030417510090200_r14","doi-asserted-by":"crossref","first-page":"898","DOI":"10.3389\/fmicb.2016.00898","article-title":"The role of neutrophils in the induction of specific Th1 and Th17 during vaccination against tuberculosis","volume":"7","author":"Trentini","year":"2016","journal-title":"Front. Microbiol."},{"key":"2025030417510090200_r15","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1016\/j.immuni.2012.07.015","article-title":"Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8+ T cells. [Published erratum appears in 2012 Immunity 37: 1145.]","volume":"37","author":"Duffy","year":"2012","journal-title":"Immunity"},{"key":"2025030417510090200_r16","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1000484","article-title":"Vector transmission of leishmania abrogates vaccine-induced protective immunity","volume":"5","author":"Peters","year":"2009","journal-title":"PLoS Pathog."},{"key":"2025030417510090200_r17","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/s00005-008-0010-9","article-title":"Live attenuated Leishmania vaccines: a potential strategic alternative","volume":"56","author":"Silvestre","year":"2008","journal-title":"Arch. Immunol. Ther. Exp. (Warsz.)"},{"key":"2025030417510090200_r18","doi-asserted-by":"crossref","first-page":"25703","DOI":"10.1074\/jbc.M402794200","article-title":"Centrin gene disruption impairs stage-specific basal body duplication and cell cycle progression in Leishmania","volume":"279","author":"Selvapandiyan","year":"2004","journal-title":"J. Biol. Chem."},{"key":"2025030417510090200_r19","doi-asserted-by":"crossref","first-page":"1813","DOI":"10.4049\/jimmunol.0900276","article-title":"Intracellular replication-deficient Leishmania donovani induces long lasting protective immunity against visceral leishmaniasis","volume":"183","author":"Selvapandiyan","year":"2009","journal-title":"J. Immunol."},{"key":"2025030417510090200_r20","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1016\/j.vaccine.2013.01.048","article-title":"Induction of immunogenicity by live attenuated Leishmania donovani centrin deleted parasites in dogs","volume":"31","author":"Fiuza","year":"2013","journal-title":"Vaccine"},{"key":"2025030417510090200_r21","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.vaccine.2014.11.039","article-title":"Vaccination using live attenuated Leishmania donovani centrin deleted parasites induces protection in dogs against Leishmania infantum","volume":"33","author":"Fiuza","year":"2015","journal-title":"Vaccine"},{"key":"2025030417510090200_r22","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0004322","article-title":"Intradermal immunization of leishmania donovani centrin knock-out parasites in combination with salivary protein LJM19 from sand fly vector induces a durable protective immune response in hamsters","volume":"10","author":"Fiuza","year":"2016","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2025030417510090200_r23","doi-asserted-by":"crossref","first-page":"3800","DOI":"10.1128\/IAI.00184-15","article-title":"Genetically modified live attenuated leishmania donovani parasites induce innate immunity through classical activation of macrophages that direct the Th1 response in mice","volume":"83","author":"Bhattacharya","year":"2015","journal-title":"Infect. Immun."},{"key":"2025030417510090200_r24","doi-asserted-by":"crossref","first-page":"4319","DOI":"10.4049\/jimmunol.1000893","article-title":"Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps","volume":"185","author":"Gabriel","year":"2010","journal-title":"J. Immunol."},{"key":"2025030417510090200_r25","doi-asserted-by":"crossref","first-page":"1531","DOI":"10.1093\/infdis\/jiw394","article-title":"A subset of neutrophils expressing markers of antigen-presenting cells in human visceral leishmaniasis","volume":"214","author":"Sharma","year":"2016","journal-title":"J. Infect. Dis."},{"key":"2025030417510090200_r26","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1189\/jlb.0706440","article-title":"Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection","volume":"82","author":"Charmoy","year":"2007","journal-title":"J. Leukoc. Biol."},{"key":"2025030417510090200_r27","doi-asserted-by":"crossref","DOI":"10.1155\/2010\/719361","article-title":"The prominent role of neutrophils during the initial phase of infection by Leishmania parasites","volume":"2010","author":"Charmoy","year":"2010","journal-title":"J. Biomed. Biotechnol."},{"key":"2025030417510090200_r28","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1111\/j.1365-2958.2010.07214.x","article-title":"Characterization of a Leishmania stage-specific mitochondrial membrane protein that enhances the activity of cytochrome c oxidase and its role in virulence","volume":"77","author":"Dey","year":"2010","journal-title":"Mol. Microbiol."},{"key":"2025030417510090200_r29","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1003923","article-title":"Lundep, a sand fly salivary endonuclease increases Leishmania parasite survival in neutrophils and inhibits XIIa contact activation in human plasma","volume":"10","author":"Chagas","year":"2014","journal-title":"PLoS Pathog."},{"key":"2025030417510090200_r30","doi-asserted-by":"crossref","first-page":"43253","DOI":"10.1074\/jbc.M106806200","article-title":"Expression of a mutant form of Leishmania donovani centrin reduces the growth of the parasite","volume":"276","author":"Selvapandiyan","year":"2001","journal-title":"J. Biol. Chem."},{"key":"2025030417510090200_r31","doi-asserted-by":"crossref","first-page":"6748","DOI":"10.1073\/pnas.0900226106","article-title":"Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps","volume":"106","author":"Guimar\u00e3es-Costa","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030417510090200_r32","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1002536","article-title":"Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response","volume":"8","author":"Ribeiro-Gomes","year":"2012","journal-title":"PLoS Pathog."},{"key":"2025030417510090200_r33","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1006\/expr.2001.4656","article-title":"A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation","volume":"99","author":"Sp\u00e4th","year":"2001","journal-title":"Exp. Parasitol."},{"key":"2025030417510090200_r34","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1016\/j.it.2015.07.007","article-title":"The role of tissue resident cells in neutrophil recruitment","volume":"36","author":"Kim","year":"2015","journal-title":"Trends Immunol."},{"key":"2025030417510090200_r35","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1016\/j.cell.2014.01.006","article-title":"Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium","volume":"156","author":"Schiwon","year":"2014","journal-title":"Cell"},{"key":"2025030417510090200_r36","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1182\/blood-2009-11-254490","article-title":"CCR7 is involved in the migration of neutrophils to lymph nodes","volume":"117","author":"Beauvillain","year":"2011","journal-title":"Blood"},{"key":"2025030417510090200_r37","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.4049\/jimmunol.165.5.2628","article-title":"An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB\/c mice infected with Leishmania major","volume":"165","author":"Tacchini-Cottier","year":"2000","journal-title":"J. Immunol."},{"key":"2025030417510090200_r38","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1002\/eji.201546015","article-title":"The Nlrp3 inflammasome, IL-1\u03b2, and neutrophil recruitment are required for susceptibility to a nonhealing strain of Leishmania major in C57BL\/6 mice","volume":"46","author":"Charmoy","year":"2016","journal-title":"Eur. J. Immunol."},{"key":"2025030417510090200_r39","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1128\/IAI.01388-07","article-title":"Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani","volume":"76","author":"McFarlane","year":"2008","journal-title":"Infect. Immun."},{"key":"2025030417510090200_r40","doi-asserted-by":"crossref","first-page":"59","DOI":"10.3389\/fcimb.2012.00059","article-title":"The influence of early neutrophil-Leishmania interactions on the host immune response to infection","volume":"2","author":"Ribeiro-Gomes","year":"2012","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"2025030417510090200_r41","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1128\/IAI.70.2.826-835.2002","article-title":"Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors","volume":"70","author":"Laufs","year":"2002","journal-title":"Infect. Immun."},{"key":"2025030417510090200_r42","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0007533","article-title":"Leishmania major degrades murine CXCL1 - an immune evasion strategy","volume":"13","author":"Yorek","year":"2019","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2025030417510090200_r43","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1038\/ni957","article-title":"Antigen presentation to naive CD4 T cells in the lymph node","volume":"4","author":"Itano","year":"2003","journal-title":"Nat. Immunol."},{"key":"2025030417510090200_r44","doi-asserted-by":"crossref","first-page":"4308","DOI":"10.4049\/jimmunol.180.6.4308","article-title":"Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways","volume":"180","author":"De Filippo","year":"2008","journal-title":"J. Immunol."},{"key":"2025030417510090200_r45","doi-asserted-by":"crossref","first-page":"4930","DOI":"10.1182\/blood-2013-02-486217","article-title":"Mast cell and macrophage chemokines CXCL1\/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation","volume":"121","author":"De Filippo","year":"2013","journal-title":"Blood"},{"key":"2025030417510090200_r46","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1000755","article-title":"Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice","volume":"6","author":"Charmoy","year":"2010","journal-title":"PLoS Pathog."},{"key":"2025030417510090200_r47","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.imlet.2008.02.008","article-title":"Murine neutrophils present class II restricted antigen","volume":"118","author":"Culshaw","year":"2008","journal-title":"Immunol. Lett."},{"key":"2025030417510090200_r48","doi-asserted-by":"crossref","first-page":"1991","DOI":"10.1182\/blood-2016-10-744441","article-title":"Neutrophils acquire the capacity for antigen presentation to memory CD4+ T cells in vitro and ex vivo","volume":"129","author":"Vono","year":"2017","journal-title":"Blood"},{"key":"2025030417510090200_r49","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1093\/intimm\/dxr007","article-title":"Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation","volume":"23","author":"Abi Abdallah","year":"2011","journal-title":"Int. Immunol."},{"key":"2025030417510090200_r50","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1046\/j.1365-2567.2000.00140.x","article-title":"Polymorphonuclear neutrophils as accessory cells for T-cell activation: major histocompatibility complex class II restricted antigen-dependent induction of T-cell proliferation","volume":"101","author":"Radsak","year":"2000","journal-title":"Immunology"},{"key":"2025030417510090200_r51","doi-asserted-by":"crossref","first-page":"7110","DOI":"10.4049\/jimmunol.1100001","article-title":"Lung neutrophils facilitate activation of naive antigen-specific CD4+ T cells during Mycobacterium tuberculosis infection","volume":"186","author":"Blomgran","year":"2011","journal-title":"J. Immunol."},{"key":"2025030417510090200_r52","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1186\/s12964-019-0471-y","article-title":"The regulatory roles of neutrophils in adaptive immunity","volume":"17","author":"Li","year":"2019","journal-title":"Cell Commun. Signal."},{"key":"2025030417510090200_r53","doi-asserted-by":"crossref","first-page":"7139","DOI":"10.1038\/ncomms8139","article-title":"Microbe-dependent lymphatic migration of neutrophils modulates lymphocyte proliferation in lymph nodes","volume":"6","author":"Hampton","year":"2015","journal-title":"Nat. Commun."},{"key":"2025030417510090200_r54","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.immuni.2008.07.012","article-title":"Dynamics of neutrophil migration in lymph nodes during infection. [Published erratum appears in 2008 Immunity 29: 661.]","volume":"29","author":"Chtanova","year":"2008","journal-title":"Immunity"},{"key":"2025030417510090200_r55","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1002\/JLB.4MIR0220-574RR","article-title":"Neutrophils at the crossroads of innate and adaptive immunity","volume":"108","author":"Rosales","year":"2020","journal-title":"J. Leukoc. Biol."},{"key":"2025030417510090200_r56","doi-asserted-by":"crossref","first-page":"3513","DOI":"10.4049\/jimmunol.1303145","article-title":"Characterization of cross-protection by genetically modified live-attenuated Leishmania donovani parasites against Leishmania mexicana","volume":"193","author":"Dey","year":"2014","journal-title":"J. Immunol."}],"container-title":["The Journal of Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/205\/12\/3333\/61879325\/ji2000829.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/205\/12\/3333\/61879325\/ji2000829.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,4]],"date-time":"2025-03-04T18:10:48Z","timestamp":1741111848000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jimmunol\/article\/205\/12\/3333\/7943761"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12]]},"references-count":56,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2020,12,15]]}},"URL":"https:\/\/doi.org\/10.4049\/jimmunol.2000829","relation":{},"ISSN":["0022-1767","1550-6606"],"issn-type":[{"value":"0022-1767","type":"print"},{"value":"1550-6606","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,12]]},"published":{"date-parts":[[2020,12]]}}}