Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.

<h4>Background/aims</h4>Arthropod-borne pathogens are transmitted into a unique intradermal microenvironment that includes the saliva of their vectors. Immunomodulatory factors in the saliva can enhance infectivity; however, in some cases the immune response that develops to saliva from...

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Autores principales: Christopher F Bosio, Austin K Viall, Clayton O Jarrett, Donald Gardner, Michael P Rood, B Joseph Hinnebusch
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Publicado: Public Library of Science (PLoS) 2014
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spelling oai:doaj.org-article:e78b5ff4487a465498c61bdff09ba5bd2021-11-25T06:31:59ZEvaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.1935-27271935-273510.1371/journal.pntd.0003196https://doaj.org/article/e78b5ff4487a465498c61bdff09ba5bd2014-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pntd.0003196https://doaj.org/toc/1935-2727https://doaj.org/toc/1935-2735<h4>Background/aims</h4>Arthropod-borne pathogens are transmitted into a unique intradermal microenvironment that includes the saliva of their vectors. Immunomodulatory factors in the saliva can enhance infectivity; however, in some cases the immune response that develops to saliva from prior uninfected bites can inhibit infectivity. Most rodent reservoirs of Yersinia pestis experience fleabites regularly, but the effect this has on the dynamics of flea-borne transmission of plague has never been investigated. We examined the innate and acquired immune response of mice to bites of Xenopsylla cheopis and its effects on Y. pestis transmission and disease progression in both naïve mice and mice chronically exposed to flea bites.<h4>Methods/principal findings</h4>The immune response of C57BL/6 mice to uninfected flea bites was characterized by flow cytometry, histology, and antibody detection methods. In naïve mice, flea bites induced mild inflammation with limited recruitment of neutrophils and macrophages to the bite site. Infectivity and host response in naïve mice exposed to flea bites followed immediately by intradermal injection of Y. pestis did not differ from that of mice infected with Y. pestis without prior flea feeding. With prolonged exposure, an IgG1 antibody response primarily directed to the predominant component of flea saliva, a family of 36-45 kDa phosphatase-like proteins, occurred in both laboratory mice and wild rats naturally exposed to X. cheopis, but a hypersensitivity response never developed. The incidence and progression of terminal plague following challenge by infective blocked fleas were equivalent in naïve mice and mice sensitized to flea saliva by repeated exposure to flea bites over a 10-week period.<h4>Conclusions</h4>Unlike what is observed with many other blood-feeding arthropods, the murine immune response to X. cheopis saliva is mild and continued exposure to flea bites leads more to tolerance than to hypersensitivity. The immune response to flea saliva had no detectable effect on Y. pestis transmission or plague pathogenesis in mice.Christopher F BosioAustin K ViallClayton O JarrettDonald GardnerMichael P RoodB Joseph HinnebuschPublic Library of Science (PLoS)articleArctic medicine. Tropical medicineRC955-962Public aspects of medicineRA1-1270ENPLoS Neglected Tropical Diseases, Vol 8, Iss 9, p e3196 (2014)
institution DOAJ
collection DOAJ
language EN
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Christopher F Bosio
Austin K Viall
Clayton O Jarrett
Donald Gardner
Michael P Rood
B Joseph Hinnebusch
Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.
description <h4>Background/aims</h4>Arthropod-borne pathogens are transmitted into a unique intradermal microenvironment that includes the saliva of their vectors. Immunomodulatory factors in the saliva can enhance infectivity; however, in some cases the immune response that develops to saliva from prior uninfected bites can inhibit infectivity. Most rodent reservoirs of Yersinia pestis experience fleabites regularly, but the effect this has on the dynamics of flea-borne transmission of plague has never been investigated. We examined the innate and acquired immune response of mice to bites of Xenopsylla cheopis and its effects on Y. pestis transmission and disease progression in both naïve mice and mice chronically exposed to flea bites.<h4>Methods/principal findings</h4>The immune response of C57BL/6 mice to uninfected flea bites was characterized by flow cytometry, histology, and antibody detection methods. In naïve mice, flea bites induced mild inflammation with limited recruitment of neutrophils and macrophages to the bite site. Infectivity and host response in naïve mice exposed to flea bites followed immediately by intradermal injection of Y. pestis did not differ from that of mice infected with Y. pestis without prior flea feeding. With prolonged exposure, an IgG1 antibody response primarily directed to the predominant component of flea saliva, a family of 36-45 kDa phosphatase-like proteins, occurred in both laboratory mice and wild rats naturally exposed to X. cheopis, but a hypersensitivity response never developed. The incidence and progression of terminal plague following challenge by infective blocked fleas were equivalent in naïve mice and mice sensitized to flea saliva by repeated exposure to flea bites over a 10-week period.<h4>Conclusions</h4>Unlike what is observed with many other blood-feeding arthropods, the murine immune response to X. cheopis saliva is mild and continued exposure to flea bites leads more to tolerance than to hypersensitivity. The immune response to flea saliva had no detectable effect on Y. pestis transmission or plague pathogenesis in mice.
format article
author Christopher F Bosio
Austin K Viall
Clayton O Jarrett
Donald Gardner
Michael P Rood
B Joseph Hinnebusch
author_facet Christopher F Bosio
Austin K Viall
Clayton O Jarrett
Donald Gardner
Michael P Rood
B Joseph Hinnebusch
author_sort Christopher F Bosio
title Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.
title_short Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.
title_full Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.
title_fullStr Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.
title_full_unstemmed Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis.
title_sort evaluation of the murine immune response to xenopsylla cheopis flea saliva and its effect on transmission of yersinia pestis.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/e78b5ff4487a465498c61bdff09ba5bd
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