Murine neonates infected with yersinia enterocolitica develop rapid and robust proinflammatory responses in intestinal lymphoid tissues

David Siefker, Andrea Echeverry, Roberta Brambill, Masayuki Fukat, Kurt Schesser, Becky Adkins

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Neonatal animals are generally very susceptible to infection with bacterial pathogens. However, we recently reported that neonatal mice are highly resistant to orogastric infection with Yersinia enterocolitica. Here, we show that proinflammatory responses greatly exceeding those in adults arise very rapidly in the mesenteric lymph nodes (MLN) of neonates. High-level induction of proinflammatory gene expression occurred in the neonatal MLN as early as 18 h postinfection. Marked innate phagocyte recruitment was subsequently detected at 24 h postinfection. Enzyme-linked immunosorbent spot assay (ELISPOT) analyses indicated that enhanced inflammation in neonatal MLN is contributed to, in part, by an increased frequency of proinflammatory cytokinesecreting cells. Moreover, both CD11b+ and CD11b- cell populations appeared to play a role in proinflammatory gene expression. The level of inflammation in neonatal MLN was also dependent on key bacterial components. Y. enterocolitica lacking the virulence plasmid failed to induce innate phagocyte recruitment. In contrast, tumor necrosis factor alpha (TNF-α) protein expression and neutrophil recruitment were strikingly higher in neonatal MLN after infection with a yopP-deficient strain than with wild-type Y. enterocolitica, whereas only modest increases occurred in adults. This hyperinflammatory response was associated with greater colonization of the spleen and higher mortality in neonates, while there was no difference in mortality among adults. This model highlights the dynamic levels of inflammation in the intestinal lymphoid tissues and reveals the protective (wild-type strain) versus harmful (yopP-deficient strain) consequences of inflammation in neonates. Moreover, these results reveal that the neonatal intestinal lymphoid tissues have great potential to rapidly mobilize innate components in response to infection with bacterial enteropathogens.

Original languageEnglish (US)
Pages (from-to)762-772
Number of pages11
JournalInfection and Immunity
Volume82
Issue number2
DOIs
StatePublished - Feb 1 2014

Fingerprint

Yersinia enterocolitica
Lymphoid Tissue
Lymph Nodes
Inflammation
Phagocytes
Bacterial Infections
Newborn Animals
Gene Expression
Neutrophil Infiltration
Mortality
Infection
Virulence
Plasmids
Spleen
Tumor Necrosis Factor-alpha
Enzyme-Linked Immunosorbent Assay
Population
Proteins

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

Murine neonates infected with yersinia enterocolitica develop rapid and robust proinflammatory responses in intestinal lymphoid tissues. / Siefker, David; Echeverry, Andrea; Brambill, Roberta; Fukat, Masayuki; Schesser, Kurt; Adkins, Becky.

In: Infection and Immunity, Vol. 82, No. 2, 01.02.2014, p. 762-772.

Research output: Contribution to journalArticle

Siefker, David ; Echeverry, Andrea ; Brambill, Roberta ; Fukat, Masayuki ; Schesser, Kurt ; Adkins, Becky. / Murine neonates infected with yersinia enterocolitica develop rapid and robust proinflammatory responses in intestinal lymphoid tissues. In: Infection and Immunity. 2014 ; Vol. 82, No. 2. pp. 762-772.
@article{f58bc8f4f81d449186fd9e625abdc6e1,
title = "Murine neonates infected with yersinia enterocolitica develop rapid and robust proinflammatory responses in intestinal lymphoid tissues",
abstract = "Neonatal animals are generally very susceptible to infection with bacterial pathogens. However, we recently reported that neonatal mice are highly resistant to orogastric infection with Yersinia enterocolitica. Here, we show that proinflammatory responses greatly exceeding those in adults arise very rapidly in the mesenteric lymph nodes (MLN) of neonates. High-level induction of proinflammatory gene expression occurred in the neonatal MLN as early as 18 h postinfection. Marked innate phagocyte recruitment was subsequently detected at 24 h postinfection. Enzyme-linked immunosorbent spot assay (ELISPOT) analyses indicated that enhanced inflammation in neonatal MLN is contributed to, in part, by an increased frequency of proinflammatory cytokinesecreting cells. Moreover, both CD11b+ and CD11b- cell populations appeared to play a role in proinflammatory gene expression. The level of inflammation in neonatal MLN was also dependent on key bacterial components. Y. enterocolitica lacking the virulence plasmid failed to induce innate phagocyte recruitment. In contrast, tumor necrosis factor alpha (TNF-α) protein expression and neutrophil recruitment were strikingly higher in neonatal MLN after infection with a yopP-deficient strain than with wild-type Y. enterocolitica, whereas only modest increases occurred in adults. This hyperinflammatory response was associated with greater colonization of the spleen and higher mortality in neonates, while there was no difference in mortality among adults. This model highlights the dynamic levels of inflammation in the intestinal lymphoid tissues and reveals the protective (wild-type strain) versus harmful (yopP-deficient strain) consequences of inflammation in neonates. Moreover, these results reveal that the neonatal intestinal lymphoid tissues have great potential to rapidly mobilize innate components in response to infection with bacterial enteropathogens.",
author = "David Siefker and Andrea Echeverry and Roberta Brambill and Masayuki Fukat and Kurt Schesser and Becky Adkins",
year = "2014",
month = "2",
day = "1",
doi = "10.1128/IAI.01489-13",
language = "English (US)",
volume = "82",
pages = "762--772",
journal = "Infection and Immunity",
issn = "0019-9567",
publisher = "American Society for Microbiology",
number = "2",

}

TY - JOUR

T1 - Murine neonates infected with yersinia enterocolitica develop rapid and robust proinflammatory responses in intestinal lymphoid tissues

AU - Siefker, David

AU - Echeverry, Andrea

AU - Brambill, Roberta

AU - Fukat, Masayuki

AU - Schesser, Kurt

AU - Adkins, Becky

PY - 2014/2/1

Y1 - 2014/2/1

N2 - Neonatal animals are generally very susceptible to infection with bacterial pathogens. However, we recently reported that neonatal mice are highly resistant to orogastric infection with Yersinia enterocolitica. Here, we show that proinflammatory responses greatly exceeding those in adults arise very rapidly in the mesenteric lymph nodes (MLN) of neonates. High-level induction of proinflammatory gene expression occurred in the neonatal MLN as early as 18 h postinfection. Marked innate phagocyte recruitment was subsequently detected at 24 h postinfection. Enzyme-linked immunosorbent spot assay (ELISPOT) analyses indicated that enhanced inflammation in neonatal MLN is contributed to, in part, by an increased frequency of proinflammatory cytokinesecreting cells. Moreover, both CD11b+ and CD11b- cell populations appeared to play a role in proinflammatory gene expression. The level of inflammation in neonatal MLN was also dependent on key bacterial components. Y. enterocolitica lacking the virulence plasmid failed to induce innate phagocyte recruitment. In contrast, tumor necrosis factor alpha (TNF-α) protein expression and neutrophil recruitment were strikingly higher in neonatal MLN after infection with a yopP-deficient strain than with wild-type Y. enterocolitica, whereas only modest increases occurred in adults. This hyperinflammatory response was associated with greater colonization of the spleen and higher mortality in neonates, while there was no difference in mortality among adults. This model highlights the dynamic levels of inflammation in the intestinal lymphoid tissues and reveals the protective (wild-type strain) versus harmful (yopP-deficient strain) consequences of inflammation in neonates. Moreover, these results reveal that the neonatal intestinal lymphoid tissues have great potential to rapidly mobilize innate components in response to infection with bacterial enteropathogens.

AB - Neonatal animals are generally very susceptible to infection with bacterial pathogens. However, we recently reported that neonatal mice are highly resistant to orogastric infection with Yersinia enterocolitica. Here, we show that proinflammatory responses greatly exceeding those in adults arise very rapidly in the mesenteric lymph nodes (MLN) of neonates. High-level induction of proinflammatory gene expression occurred in the neonatal MLN as early as 18 h postinfection. Marked innate phagocyte recruitment was subsequently detected at 24 h postinfection. Enzyme-linked immunosorbent spot assay (ELISPOT) analyses indicated that enhanced inflammation in neonatal MLN is contributed to, in part, by an increased frequency of proinflammatory cytokinesecreting cells. Moreover, both CD11b+ and CD11b- cell populations appeared to play a role in proinflammatory gene expression. The level of inflammation in neonatal MLN was also dependent on key bacterial components. Y. enterocolitica lacking the virulence plasmid failed to induce innate phagocyte recruitment. In contrast, tumor necrosis factor alpha (TNF-α) protein expression and neutrophil recruitment were strikingly higher in neonatal MLN after infection with a yopP-deficient strain than with wild-type Y. enterocolitica, whereas only modest increases occurred in adults. This hyperinflammatory response was associated with greater colonization of the spleen and higher mortality in neonates, while there was no difference in mortality among adults. This model highlights the dynamic levels of inflammation in the intestinal lymphoid tissues and reveals the protective (wild-type strain) versus harmful (yopP-deficient strain) consequences of inflammation in neonates. Moreover, these results reveal that the neonatal intestinal lymphoid tissues have great potential to rapidly mobilize innate components in response to infection with bacterial enteropathogens.

UR - http://www.scopus.com/inward/record.url?scp=84892972718&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84892972718&partnerID=8YFLogxK

U2 - 10.1128/IAI.01489-13

DO - 10.1128/IAI.01489-13

M3 - Article

VL - 82

SP - 762

EP - 772

JO - Infection and Immunity

JF - Infection and Immunity

SN - 0019-9567

IS - 2

ER -