Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine

Penelope Barnes, Molly A. Bergman, Joan Mecsas, Ralph R. Isberg

Research output: Contribution to journalArticle

95 Citations (Scopus)

Abstract

Dissemination of Yersinia pseudotuberculosis within mice after oral inoculation was analyzed. Y. pseudotuberculosis translocated to organs such as the liver and spleen shortly after oral inoculation, but was quickly cleared. In contrast, a second temporally distinct bacterial translocation event resulted in successful hepatosplenic replication of the bacteria. Replicating pools of bacteria could be established in these organs in mouse mutants that lacked Peyer's patches. These animals frequently had sterile mesenteric lymph nodes, a finding consistent with translocation taking place independently of regional lymph node colonization. In further contradiction to accepted models for dissemination of enteropathogens, clonal analysis revealed that bacteria causing disease in the spleen and liver of C57BL/6J mice were derived from populations located outside the intestinal lymph nodes. Replication of bacteria in the intestine before translocation appeared critical for dissemination, as transient selective suppression by streptomycin of bacterial growth in the intestine delayed dissemination of Y. pseudotuberculosis. These results collectively indicate that hepatosplenic colonization appears intimately connected with the ability of Y. pseudotuberculosis to successfully establish replication in the intestinal lumen and does not result from ordered spread leading from the intestine to regional lymph nodes before dissemination. JEM

Original languageEnglish (US)
Pages (from-to)1591-1601
Number of pages11
JournalJournal of Experimental Medicine
Volume203
Issue number6
DOIs
StatePublished - Jun 12 2006
Externally publishedYes

Fingerprint

Yersinia pseudotuberculosis
Intestines
Lymph Nodes
Bacteria
Spleen
Bacterial Translocation
Peyer's Patches
Liver
Streptomycin
Inbred C57BL Mouse
Growth
Population

ASJC Scopus subject areas

  • Immunology

Cite this

Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. / Barnes, Penelope; Bergman, Molly A.; Mecsas, Joan; Isberg, Ralph R.

In: Journal of Experimental Medicine, Vol. 203, No. 6, 12.06.2006, p. 1591-1601.

Research output: Contribution to journalArticle

Barnes, Penelope ; Bergman, Molly A. ; Mecsas, Joan ; Isberg, Ralph R. / Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. In: Journal of Experimental Medicine. 2006 ; Vol. 203, No. 6. pp. 1591-1601.
@article{d829eeb5b77c4f03a1b6fd4527dfe162,
title = "Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine",
abstract = "Dissemination of Yersinia pseudotuberculosis within mice after oral inoculation was analyzed. Y. pseudotuberculosis translocated to organs such as the liver and spleen shortly after oral inoculation, but was quickly cleared. In contrast, a second temporally distinct bacterial translocation event resulted in successful hepatosplenic replication of the bacteria. Replicating pools of bacteria could be established in these organs in mouse mutants that lacked Peyer's patches. These animals frequently had sterile mesenteric lymph nodes, a finding consistent with translocation taking place independently of regional lymph node colonization. In further contradiction to accepted models for dissemination of enteropathogens, clonal analysis revealed that bacteria causing disease in the spleen and liver of C57BL/6J mice were derived from populations located outside the intestinal lymph nodes. Replication of bacteria in the intestine before translocation appeared critical for dissemination, as transient selective suppression by streptomycin of bacterial growth in the intestine delayed dissemination of Y. pseudotuberculosis. These results collectively indicate that hepatosplenic colonization appears intimately connected with the ability of Y. pseudotuberculosis to successfully establish replication in the intestinal lumen and does not result from ordered spread leading from the intestine to regional lymph nodes before dissemination. JEM",
author = "Penelope Barnes and Bergman, {Molly A.} and Joan Mecsas and Isberg, {Ralph R.}",
year = "2006",
month = "6",
day = "12",
doi = "10.1084/jem.20060905",
language = "English (US)",
volume = "203",
pages = "1591--1601",
journal = "Journal of Experimental Medicine",
issn = "0022-1007",
publisher = "Rockefeller University Press",
number = "6",

}

TY - JOUR

T1 - Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine

AU - Barnes, Penelope

AU - Bergman, Molly A.

AU - Mecsas, Joan

AU - Isberg, Ralph R.

PY - 2006/6/12

Y1 - 2006/6/12

N2 - Dissemination of Yersinia pseudotuberculosis within mice after oral inoculation was analyzed. Y. pseudotuberculosis translocated to organs such as the liver and spleen shortly after oral inoculation, but was quickly cleared. In contrast, a second temporally distinct bacterial translocation event resulted in successful hepatosplenic replication of the bacteria. Replicating pools of bacteria could be established in these organs in mouse mutants that lacked Peyer's patches. These animals frequently had sterile mesenteric lymph nodes, a finding consistent with translocation taking place independently of regional lymph node colonization. In further contradiction to accepted models for dissemination of enteropathogens, clonal analysis revealed that bacteria causing disease in the spleen and liver of C57BL/6J mice were derived from populations located outside the intestinal lymph nodes. Replication of bacteria in the intestine before translocation appeared critical for dissemination, as transient selective suppression by streptomycin of bacterial growth in the intestine delayed dissemination of Y. pseudotuberculosis. These results collectively indicate that hepatosplenic colonization appears intimately connected with the ability of Y. pseudotuberculosis to successfully establish replication in the intestinal lumen and does not result from ordered spread leading from the intestine to regional lymph nodes before dissemination. JEM

AB - Dissemination of Yersinia pseudotuberculosis within mice after oral inoculation was analyzed. Y. pseudotuberculosis translocated to organs such as the liver and spleen shortly after oral inoculation, but was quickly cleared. In contrast, a second temporally distinct bacterial translocation event resulted in successful hepatosplenic replication of the bacteria. Replicating pools of bacteria could be established in these organs in mouse mutants that lacked Peyer's patches. These animals frequently had sterile mesenteric lymph nodes, a finding consistent with translocation taking place independently of regional lymph node colonization. In further contradiction to accepted models for dissemination of enteropathogens, clonal analysis revealed that bacteria causing disease in the spleen and liver of C57BL/6J mice were derived from populations located outside the intestinal lymph nodes. Replication of bacteria in the intestine before translocation appeared critical for dissemination, as transient selective suppression by streptomycin of bacterial growth in the intestine delayed dissemination of Y. pseudotuberculosis. These results collectively indicate that hepatosplenic colonization appears intimately connected with the ability of Y. pseudotuberculosis to successfully establish replication in the intestinal lumen and does not result from ordered spread leading from the intestine to regional lymph nodes before dissemination. JEM

UR - http://www.scopus.com/inward/record.url?scp=33745027147&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33745027147&partnerID=8YFLogxK

U2 - 10.1084/jem.20060905

DO - 10.1084/jem.20060905

M3 - Article

C2 - 16754724

AN - SCOPUS:33745027147

VL - 203

SP - 1591

EP - 1601

JO - Journal of Experimental Medicine

JF - Journal of Experimental Medicine

SN - 0022-1007

IS - 6

ER -