{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T07:18:41Z","timestamp":1791098321337,"version":"4.1.0"},"reference-count":56,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2013,11,13]],"date-time":"2013-11-13T00:00:00Z","timestamp":1384300800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/100017540","name":"Division of Intramural Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100017540","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"NIAID","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"U.S. National Institutes of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013,11,13]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Yersinia pestis, the bacterial agent of plague, is transmitted by fleas. The bite of an infected flea deposits Y. pestis into the dermis and triggers recruitment of innate immune cells, including phagocytic PMNs. Y. pestis can subvert this PMN response and survive at the flea-bite site, disseminate, and persist in the host. Although its genome encodes a number of antiphagocytic virulence factors, phagocytosis of Y. pestis by PMNs has been observed. This study tests the hypotheses that Y. pestis, grown at the ambient temperature of the flea vector (21\u00b0C), where the major antiphagocytic virulence factors are not produced, can survive and replicate within human PMNs and can use PMNs as a route to infect macrophages subsequently. We show that Y. pestis is localized within PMN phagosomes, predominately as individual bacteria, and that intracellular bacteria can survive and replicate. Within 12 h of infection, \u223c70% of infected PMNs had PS on their surface and were plausibly competent for efferocytosis. With the use of live cell confocal imaging, we show that autologous HMDMs recognize and internalize infected PMNs and that Y. pestis survives and replicates within these HMDMs following efferocytosis. Addition of HMDMs to infected PMNs resulted in decreased secretion of inflammatory cytokines (compared with HMDMs incubated directly with pCD1\u2212Y. pestis) and increased secretion of the anti-inflammatory cytokine IL-1ra. Thus, Y. pestis can survive and replicate within PMNs, and infected PMNs may be a route for noninflammatory infection of macrophages.<\/jats:p>","DOI":"10.1189\/jlb.1112551","type":"journal-article","created":{"date-parts":[[2013,11,14]],"date-time":"2013-11-14T04:31:48Z","timestamp":1384403508000},"page":"389-398","source":"Crossref","is-referenced-by-count":69,"title":["<i>Yersinia pestis<\/i>survival and replication within human neutrophil phagosomes and uptake of infected neutrophils by macrophages"],"prefix":"10.1093","volume":"95","author":[{"given":"Justin L","family":"Spinner","sequence":"first","affiliation":[{"name":"Laboratories of Zoonotic Pathogens, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seth","family":"Winfree","sequence":"additional","affiliation":[{"name":"Intracellular Parasites, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tregei","family":"Starr","sequence":"additional","affiliation":[{"name":"Intracellular Parasites, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey G","family":"Shannon","sequence":"additional","affiliation":[{"name":"Laboratories of Zoonotic Pathogens, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vinod","family":"Nair","sequence":"additional","affiliation":[{"name":"Electron Microscopy Unit, Research Technologies Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivia","family":"Steele-Mortimer","sequence":"additional","affiliation":[{"name":"Intracellular Parasites, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B Joseph","family":"Hinnebusch","sequence":"additional","affiliation":[{"name":"Laboratories of Zoonotic Pathogens, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Hamilton, Montana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2013,11,13]]},"reference":[{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1111\/j.1600-065X.2007.00550.x","article-title":"How human neutrophils kill and degrade microbes: an integrated view","volume":"219","author":"Nauseef","year":"2007","journal-title":"Immunol. 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Pathol."},{"key":"2023032709544556300_","first-page":"156","article-title":"Pathology of experimental pneumonic plague produced by fraction 1-positive and fraction 1-negative Yersinia pestis in African green monkeys","volume":"120","author":"Davis","year":"1996","journal-title":"(Cercopithecus aethiops). Arch. Pathol. Lab. Med."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"17786","DOI":"10.1073\/pnas.0506840102","article-title":"Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity","volume":"102","author":"Lathem","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1128\/IAI.00403-06","article-title":"Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice","volume":"75","author":"Bubeck","year":"2007","journal-title":"Infect. 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Dis."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1128\/IAI.70.3.1453-1460.2002","article-title":"Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis","volume":"70","author":"Du","year":"2002","journal-title":"Infect. Immun."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/978-1-4614-3561-7_20","article-title":"The life stage of Yersinia pestis in the flea vector confers increased resistance to phagocytosis and killing by murine polymorphonuclear leukocytes","volume":"954","author":"Spinner","year":"2012","journal-title":"Adv. Exp. Med. Biol."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"7142","DOI":"10.1128\/IAI.73.11.7142-7150.2005","article-title":"Pathogenesis of Yersinia pestis infection in BALB\/c mice: effects on host macrophages and neutrophils","volume":"73","author":"Lukaszewski","year":"2005","journal-title":"Infect. 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Immun."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1128\/iai.45.3.649-654.1984","article-title":"Growth in mouse peritoneal macrophages of Yersinia pestis lacking established virulence determinants","volume":"45","author":"Straley","year":"1984","journal-title":"Infect. Immun."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"e42211","DOI":"10.1371\/journal.pone.0042211","article-title":"Yersinia pestis intracellular parasitism of macrophages from hosts exhibiting high and low severity of plague","volume":"7","author":"Ponnusamy","year":"2012","journal-title":"PLoS One"},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1128\/IAI.00718-09","article-title":"Ywsinia pestis two-component gene regulatory systems promote survival in human neutrophils","volume":"78","author":"O'Loughlin","year":"2010","journal-title":"Infect. 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Med."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.clim.2004.07.013","article-title":"Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae","volume":"114","author":"Pujol","year":"2005","journal-title":"Clin. Immunol."},{"key":"2023032709544556300_","doi-asserted-by":"crossref","first-page":"4041","DOI":"10.1128\/IAI.00648-13","article-title":"Role of Yersinia pestis toxin complex family proteins in resistance to phagocytosis by polymorphonuclear leukocytes","volume":"81","author":"Spinner","year":"2013","journal-title":"Infect. 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