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Defective innate cell response and lymph node infiltration specify Yersinia pestis infection.

Guinet F, Avé P, Jones L, Huerre M, Carniel E - PLoS ONE (2008)

Bottom Line: Clustering and multiple correspondence analyses showed that the DLN pathologies induced by the two species were statistically significantly different and identified the most discriminating elementary lesions.Therefore, Y. pestis exceptional virulence is not due to its recently acquired portal of entry into the host, but is associated with a distinct ability to massively infiltrate the DLN, without inducing in this organ an organized polymorphonuclear cell reaction.These results shed light on pathophysiological processes that draw the line between a virulent and a hypervirulent pathogen.

View Article: PubMed Central - PubMed

Affiliation: Unité des Yersinia, Institut Pasteur, Paris, France. fguinet@pasteur.fr

ABSTRACT
Since its recent emergence from the enteropathogen Yersinia pseudotuberculosis, Y. pestis, the plague agent, has acquired an intradermal (id) route of entry and an extreme virulence. To identify pathophysiological events associated with the Y. pestis high degree of pathogenicity, we compared disease progression and evolution in mice after id inoculation of the two Yersinia species. Mortality studies showed that the id portal was not in itself sufficient to provide Y. pseudotuberculosis with the high virulence power of its descendant. Surprisingly, Y. pseudotuberculosis multiplied even more efficiently than Y. pestis in the dermis, and generated comparable histological lesions. Likewise, Y. pseudotuberculosis translocated to the draining lymph node (DLN) and similar numbers of the two bacterial species were found at 24 h post infection (pi) in this organ. However, on day 2 pi, bacterial loads were higher in Y. pestis-infected than in Y. pseudotuberculosis-infected DLNs. Clustering and multiple correspondence analyses showed that the DLN pathologies induced by the two species were statistically significantly different and identified the most discriminating elementary lesions. Y. pseudotuberculosis infection was accompanied by abscess-type polymorphonuclear cell infiltrates containing the infection, while Y. pestis-infected DLNs exhibited an altered tissue density and a vascular congestion, and were typified by an invasion of the tissue by free floating bacteria. Therefore, Y. pestis exceptional virulence is not due to its recently acquired portal of entry into the host, but is associated with a distinct ability to massively infiltrate the DLN, without inducing in this organ an organized polymorphonuclear cell reaction. These results shed light on pathophysiological processes that draw the line between a virulent and a hypervirulent pathogen.

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Bacterial loads at injection site and in draining lymph node.Data are means of log10 of cfu numbers recovered from 77 mice infected over six independent experiments. Bars = Standard Errors. Stars indicate that the data are significantly different between the two Yersinia species (p≤0.0001). The dashed line shows the detection limit (10 cfu). The cross symbol indicates that most Y. pestis-infected mice died between days 2 and 3.
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pone-0001688-g001: Bacterial loads at injection site and in draining lymph node.Data are means of log10 of cfu numbers recovered from 77 mice infected over six independent experiments. Bars = Standard Errors. Stars indicate that the data are significantly different between the two Yersinia species (p≤0.0001). The dashed line shows the detection limit (10 cfu). The cross symbol indicates that most Y. pestis-infected mice died between days 2 and 3.

Mentions: Y. pseudotuberculosis was able to survive and to proliferate in the dermis during the first two days pi. Its growth rate over the first 24 h pi was even higher than that of Y. pestis (Figure 1). Furthermore, Y. pseudotuberculosis was found in the proximal lymph node, and similar numbers of both Yersinia species were present in the DLN at 24 h (p = 0.39). On the following day, however, Y. pestis numbers in the DLN were significantly higher than those of Y. pseudotuberculosis. Over extended observation periods of 7 days, DLN Y. pseudotuberculosis loads reached a plateau from day 3 on (Fig. 1 and data not shown). Therefore, both species were able to multiply at the inoculation site and to reach the proximal lymph node but while, in the DLN, Y. pseudotuberculosis growth was contained, Y. pestis multiplication was not controlled and the animals started to die between days 2 and 3.


Defective innate cell response and lymph node infiltration specify Yersinia pestis infection.

Guinet F, Avé P, Jones L, Huerre M, Carniel E - PLoS ONE (2008)

Bacterial loads at injection site and in draining lymph node.Data are means of log10 of cfu numbers recovered from 77 mice infected over six independent experiments. Bars = Standard Errors. Stars indicate that the data are significantly different between the two Yersinia species (p≤0.0001). The dashed line shows the detection limit (10 cfu). The cross symbol indicates that most Y. pestis-infected mice died between days 2 and 3.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2244809&req=5

pone-0001688-g001: Bacterial loads at injection site and in draining lymph node.Data are means of log10 of cfu numbers recovered from 77 mice infected over six independent experiments. Bars = Standard Errors. Stars indicate that the data are significantly different between the two Yersinia species (p≤0.0001). The dashed line shows the detection limit (10 cfu). The cross symbol indicates that most Y. pestis-infected mice died between days 2 and 3.
Mentions: Y. pseudotuberculosis was able to survive and to proliferate in the dermis during the first two days pi. Its growth rate over the first 24 h pi was even higher than that of Y. pestis (Figure 1). Furthermore, Y. pseudotuberculosis was found in the proximal lymph node, and similar numbers of both Yersinia species were present in the DLN at 24 h (p = 0.39). On the following day, however, Y. pestis numbers in the DLN were significantly higher than those of Y. pseudotuberculosis. Over extended observation periods of 7 days, DLN Y. pseudotuberculosis loads reached a plateau from day 3 on (Fig. 1 and data not shown). Therefore, both species were able to multiply at the inoculation site and to reach the proximal lymph node but while, in the DLN, Y. pseudotuberculosis growth was contained, Y. pestis multiplication was not controlled and the animals started to die between days 2 and 3.

Bottom Line: Clustering and multiple correspondence analyses showed that the DLN pathologies induced by the two species were statistically significantly different and identified the most discriminating elementary lesions.Therefore, Y. pestis exceptional virulence is not due to its recently acquired portal of entry into the host, but is associated with a distinct ability to massively infiltrate the DLN, without inducing in this organ an organized polymorphonuclear cell reaction.These results shed light on pathophysiological processes that draw the line between a virulent and a hypervirulent pathogen.

View Article: PubMed Central - PubMed

Affiliation: Unité des Yersinia, Institut Pasteur, Paris, France. fguinet@pasteur.fr

ABSTRACT
Since its recent emergence from the enteropathogen Yersinia pseudotuberculosis, Y. pestis, the plague agent, has acquired an intradermal (id) route of entry and an extreme virulence. To identify pathophysiological events associated with the Y. pestis high degree of pathogenicity, we compared disease progression and evolution in mice after id inoculation of the two Yersinia species. Mortality studies showed that the id portal was not in itself sufficient to provide Y. pseudotuberculosis with the high virulence power of its descendant. Surprisingly, Y. pseudotuberculosis multiplied even more efficiently than Y. pestis in the dermis, and generated comparable histological lesions. Likewise, Y. pseudotuberculosis translocated to the draining lymph node (DLN) and similar numbers of the two bacterial species were found at 24 h post infection (pi) in this organ. However, on day 2 pi, bacterial loads were higher in Y. pestis-infected than in Y. pseudotuberculosis-infected DLNs. Clustering and multiple correspondence analyses showed that the DLN pathologies induced by the two species were statistically significantly different and identified the most discriminating elementary lesions. Y. pseudotuberculosis infection was accompanied by abscess-type polymorphonuclear cell infiltrates containing the infection, while Y. pestis-infected DLNs exhibited an altered tissue density and a vascular congestion, and were typified by an invasion of the tissue by free floating bacteria. Therefore, Y. pestis exceptional virulence is not due to its recently acquired portal of entry into the host, but is associated with a distinct ability to massively infiltrate the DLN, without inducing in this organ an organized polymorphonuclear cell reaction. These results shed light on pathophysiological processes that draw the line between a virulent and a hypervirulent pathogen.

Show MeSH
Related in: MedlinePlus