Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut

Javier Santander, Jacquelyn Kilbourne, Jie Yeun Park, Taylor Martin, Amanda Loh, Ignacia Diaz, Robert Rojas, Cristopher Segovia, Dale Denardo, Roy Curtiss

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Bacterial lipopolysaccharides (LPS) are structural components of the outer membranes of Gram-negative bacteria and also are potent inducers of inflammation in mammals. Higher vertebrates are extremely sensitive to LPS, but lower vertebrates, like fish, are resistant to their systemic toxic effects. However, the effects of LPS on the fish intestinal mucosa remain unknown. Edwardsiella ictaluri is a primitive member of the Enterobacteriaceae family that causes enteric septicemia in channel catfish (Ictalurus punctatus). E. ictaluri infects and colonizes deep lymphoid tissues upon oral or immersion infection. Both gut and olfactory organs are the primary sites of invasion. At the systemic level, E. ictaluri pathogenesis is relatively well characterized, but our knowledge about E. ictaluri intestinal interaction is limited. Recently, we observed that E. ictaluri oligo-polysaccharide (O-PS) LPS mutants have differential effects on the intestinal epithelia of orally inoculated catfish. Here we evaluate the effects of E. ictaluri O-PS LPS mutants by using a novel catfish intestinal loop model and compare it to the rabbit ileal loop model inoculated with Salmonella enterica serovar Typhimurium LPS. We found evident differences in rabbit ileal loop and catfish ileal loop responses to E. ictaluri and S. Typhimurium LPS. We determined that catfish respond to E. ictaluri LPS but not to S. Typhimurium LPS. We also determined that E. ictaluri inhibits cytokine production and induces disruption of the intestinal fish epithelia in an O-PS-dependent fashion. The E. ictaluri wild type and ΔwibT LPS mutant caused intestinal tissue damage and inhibited proinflammatory cytokine synthesis, in contrast to E. ictaluri Δgne and Δugd LPS mutants. We concluded that the E. ictaluri O-PS subunits play a major role during pathogenesis, since they influence the recognition of the LPS by the intestinal mucosal immune system of the catfish. The LPS structure of E. ictaluri mutants is needed to understand the mechanism of interaction.

Original languageEnglish (US)
Pages (from-to)3394-3404
Number of pages11
JournalInfection and Immunity
Volume82
Issue number8
DOIs
StatePublished - 2014

Fingerprint

Edwardsiella ictaluri
Catfishes
Lipopolysaccharides
Polysaccharides
Intestinal Mucosa
Ictaluridae
Fishes
Vertebrates
Cytokines
Rabbits
Salmonella enterica
Poisons

ASJC Scopus subject areas

  • Immunology
  • Microbiology
  • Parasitology
  • Infectious Diseases

Cite this

Santander, J., Kilbourne, J., Park, J. Y., Martin, T., Loh, A., Diaz, I., ... Curtiss, R. (2014). Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut. Infection and Immunity, 82(8), 3394-3404. https://doi.org/10.1128/IAI.01697-14

Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut. / Santander, Javier; Kilbourne, Jacquelyn; Park, Jie Yeun; Martin, Taylor; Loh, Amanda; Diaz, Ignacia; Rojas, Robert; Segovia, Cristopher; Denardo, Dale; Curtiss, Roy.

In: Infection and Immunity, Vol. 82, No. 8, 2014, p. 3394-3404.

Research output: Contribution to journalArticle

Santander, J, Kilbourne, J, Park, JY, Martin, T, Loh, A, Diaz, I, Rojas, R, Segovia, C, Denardo, D & Curtiss, R 2014, 'Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut', Infection and Immunity, vol. 82, no. 8, pp. 3394-3404. https://doi.org/10.1128/IAI.01697-14
Santander, Javier ; Kilbourne, Jacquelyn ; Park, Jie Yeun ; Martin, Taylor ; Loh, Amanda ; Diaz, Ignacia ; Rojas, Robert ; Segovia, Cristopher ; Denardo, Dale ; Curtiss, Roy. / Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut. In: Infection and Immunity. 2014 ; Vol. 82, No. 8. pp. 3394-3404.
@article{6f6850cdfb0c496cadef5fbffc0c10b0,
title = "Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut",
abstract = "Bacterial lipopolysaccharides (LPS) are structural components of the outer membranes of Gram-negative bacteria and also are potent inducers of inflammation in mammals. Higher vertebrates are extremely sensitive to LPS, but lower vertebrates, like fish, are resistant to their systemic toxic effects. However, the effects of LPS on the fish intestinal mucosa remain unknown. Edwardsiella ictaluri is a primitive member of the Enterobacteriaceae family that causes enteric septicemia in channel catfish (Ictalurus punctatus). E. ictaluri infects and colonizes deep lymphoid tissues upon oral or immersion infection. Both gut and olfactory organs are the primary sites of invasion. At the systemic level, E. ictaluri pathogenesis is relatively well characterized, but our knowledge about E. ictaluri intestinal interaction is limited. Recently, we observed that E. ictaluri oligo-polysaccharide (O-PS) LPS mutants have differential effects on the intestinal epithelia of orally inoculated catfish. Here we evaluate the effects of E. ictaluri O-PS LPS mutants by using a novel catfish intestinal loop model and compare it to the rabbit ileal loop model inoculated with Salmonella enterica serovar Typhimurium LPS. We found evident differences in rabbit ileal loop and catfish ileal loop responses to E. ictaluri and S. Typhimurium LPS. We determined that catfish respond to E. ictaluri LPS but not to S. Typhimurium LPS. We also determined that E. ictaluri inhibits cytokine production and induces disruption of the intestinal fish epithelia in an O-PS-dependent fashion. The E. ictaluri wild type and ΔwibT LPS mutant caused intestinal tissue damage and inhibited proinflammatory cytokine synthesis, in contrast to E. ictaluri Δgne and Δugd LPS mutants. We concluded that the E. ictaluri O-PS subunits play a major role during pathogenesis, since they influence the recognition of the LPS by the intestinal mucosal immune system of the catfish. The LPS structure of E. ictaluri mutants is needed to understand the mechanism of interaction.",
author = "Javier Santander and Jacquelyn Kilbourne and Park, {Jie Yeun} and Taylor Martin and Amanda Loh and Ignacia Diaz and Robert Rojas and Cristopher Segovia and Dale Denardo and Roy Curtiss",
year = "2014",
doi = "10.1128/IAI.01697-14",
language = "English (US)",
volume = "82",
pages = "3394--3404",
journal = "Infection and Immunity",
issn = "0019-9567",
publisher = "American Society for Microbiology",
number = "8",

}

TY - JOUR

T1 - Inflammatory effects of Edwardsiella ictaluri lipopolysaccharide modifications in catfish gut

AU - Santander, Javier

AU - Kilbourne, Jacquelyn

AU - Park, Jie Yeun

AU - Martin, Taylor

AU - Loh, Amanda

AU - Diaz, Ignacia

AU - Rojas, Robert

AU - Segovia, Cristopher

AU - Denardo, Dale

AU - Curtiss, Roy

PY - 2014

Y1 - 2014

N2 - Bacterial lipopolysaccharides (LPS) are structural components of the outer membranes of Gram-negative bacteria and also are potent inducers of inflammation in mammals. Higher vertebrates are extremely sensitive to LPS, but lower vertebrates, like fish, are resistant to their systemic toxic effects. However, the effects of LPS on the fish intestinal mucosa remain unknown. Edwardsiella ictaluri is a primitive member of the Enterobacteriaceae family that causes enteric septicemia in channel catfish (Ictalurus punctatus). E. ictaluri infects and colonizes deep lymphoid tissues upon oral or immersion infection. Both gut and olfactory organs are the primary sites of invasion. At the systemic level, E. ictaluri pathogenesis is relatively well characterized, but our knowledge about E. ictaluri intestinal interaction is limited. Recently, we observed that E. ictaluri oligo-polysaccharide (O-PS) LPS mutants have differential effects on the intestinal epithelia of orally inoculated catfish. Here we evaluate the effects of E. ictaluri O-PS LPS mutants by using a novel catfish intestinal loop model and compare it to the rabbit ileal loop model inoculated with Salmonella enterica serovar Typhimurium LPS. We found evident differences in rabbit ileal loop and catfish ileal loop responses to E. ictaluri and S. Typhimurium LPS. We determined that catfish respond to E. ictaluri LPS but not to S. Typhimurium LPS. We also determined that E. ictaluri inhibits cytokine production and induces disruption of the intestinal fish epithelia in an O-PS-dependent fashion. The E. ictaluri wild type and ΔwibT LPS mutant caused intestinal tissue damage and inhibited proinflammatory cytokine synthesis, in contrast to E. ictaluri Δgne and Δugd LPS mutants. We concluded that the E. ictaluri O-PS subunits play a major role during pathogenesis, since they influence the recognition of the LPS by the intestinal mucosal immune system of the catfish. The LPS structure of E. ictaluri mutants is needed to understand the mechanism of interaction.

AB - Bacterial lipopolysaccharides (LPS) are structural components of the outer membranes of Gram-negative bacteria and also are potent inducers of inflammation in mammals. Higher vertebrates are extremely sensitive to LPS, but lower vertebrates, like fish, are resistant to their systemic toxic effects. However, the effects of LPS on the fish intestinal mucosa remain unknown. Edwardsiella ictaluri is a primitive member of the Enterobacteriaceae family that causes enteric septicemia in channel catfish (Ictalurus punctatus). E. ictaluri infects and colonizes deep lymphoid tissues upon oral or immersion infection. Both gut and olfactory organs are the primary sites of invasion. At the systemic level, E. ictaluri pathogenesis is relatively well characterized, but our knowledge about E. ictaluri intestinal interaction is limited. Recently, we observed that E. ictaluri oligo-polysaccharide (O-PS) LPS mutants have differential effects on the intestinal epithelia of orally inoculated catfish. Here we evaluate the effects of E. ictaluri O-PS LPS mutants by using a novel catfish intestinal loop model and compare it to the rabbit ileal loop model inoculated with Salmonella enterica serovar Typhimurium LPS. We found evident differences in rabbit ileal loop and catfish ileal loop responses to E. ictaluri and S. Typhimurium LPS. We determined that catfish respond to E. ictaluri LPS but not to S. Typhimurium LPS. We also determined that E. ictaluri inhibits cytokine production and induces disruption of the intestinal fish epithelia in an O-PS-dependent fashion. The E. ictaluri wild type and ΔwibT LPS mutant caused intestinal tissue damage and inhibited proinflammatory cytokine synthesis, in contrast to E. ictaluri Δgne and Δugd LPS mutants. We concluded that the E. ictaluri O-PS subunits play a major role during pathogenesis, since they influence the recognition of the LPS by the intestinal mucosal immune system of the catfish. The LPS structure of E. ictaluri mutants is needed to understand the mechanism of interaction.

UR - http://www.scopus.com/inward/record.url?scp=84904719647&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84904719647&partnerID=8YFLogxK

U2 - 10.1128/IAI.01697-14

DO - 10.1128/IAI.01697-14

M3 - Article

C2 - 24866806

AN - SCOPUS:84904719647

VL - 82

SP - 3394

EP - 3404

JO - Infection and Immunity

JF - Infection and Immunity

SN - 0019-9567

IS - 8

ER -