Prebiotic oligosaccharides potentiate host protective responses against L. Monocytogenes infection

Poyin Chen, Taylor Reiter, Bihua Huang, Nguyet Kong, Bart C Weimer

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Prebiotic oligosaccharides are used to modulate enteric pathogens and reduce pathogen shedding. The interactions with prebiotics that alter Listeria monocytogenes infection are not yet clearly delineated. L. monocytogenes cellular invasion requires a concerted manipulation of host epithelial cell membrane receptors to initiate internalization and infection often via receptor glycosylation. Bacterial interactions with host glycans are intimately involved in modulating cellular responses through signaling cascades at the membrane and in intracellular compartments. Characterizing the mechanisms underpinning these modulations is essential for predictive use of dietary prebiotics to diminish pathogen association. We demonstrated that human milk oligosaccharide (HMO) pretreatment of colonic epithelial cells (Caco-2) led to a 50% decrease in Listeria association, while Biomos pretreatment increased host association by 150%. L. monocytogenes-induced gene expression changes due to oligosaccharide pretreatment revealed global alterations in host signaling pathways that resulted in differential subcellular localization of L. monocytogenes during early infection. Ultimately, HMO pretreatment led to bacterial clearance in Caco-2 cells via induction of the unfolded protein response and eIF2 signaling, while Biomos pretreatment resulted in the induction of host autophagy and L. monocytogenes vacuolar escape earlier in the infection progression. This study demonstrates the capacity of prebiotic oligosaccharides to minimize infection through induction of host-intrinsic protective responses.

Original languageEnglish (US)
Pages (from-to)1-25
Number of pages25
JournalPathogens
Volume6
Issue number4
DOIs
StatePublished - Dec 19 2017

Fingerprint

Prebiotics
Listeria monocytogenes
Oligosaccharides
Infection
Human Milk
Epithelial Cells
Unfolded Protein Response
Listeriosis
Intracellular Membranes
Listeria
Caco-2 Cells
Autophagy
Glycosylation
Polysaccharides
Cell Membrane
Gene Expression

Keywords

  • Autophagy
  • C-di-AMP
  • Cell-mediated immunity (CMI)
  • eIF2 signaling
  • ER stress
  • Human milk oligosaccharide
  • Prebiotic oligosaccharide
  • Unfolded protein response

ASJC Scopus subject areas

  • Immunology and Microbiology(all)
  • Infectious Diseases
  • Microbiology (medical)
  • Immunology and Allergy
  • Molecular Biology

Cite this

Prebiotic oligosaccharides potentiate host protective responses against L. Monocytogenes infection. / Chen, Poyin; Reiter, Taylor; Huang, Bihua; Kong, Nguyet; Weimer, Bart C.

In: Pathogens, Vol. 6, No. 4, 19.12.2017, p. 1-25.

Research output: Contribution to journalArticle

Chen, Poyin ; Reiter, Taylor ; Huang, Bihua ; Kong, Nguyet ; Weimer, Bart C. / Prebiotic oligosaccharides potentiate host protective responses against L. Monocytogenes infection. In: Pathogens. 2017 ; Vol. 6, No. 4. pp. 1-25.
@article{9e02defd5f684d24b9653e7dbc007934,
title = "Prebiotic oligosaccharides potentiate host protective responses against L. Monocytogenes infection",
abstract = "Prebiotic oligosaccharides are used to modulate enteric pathogens and reduce pathogen shedding. The interactions with prebiotics that alter Listeria monocytogenes infection are not yet clearly delineated. L. monocytogenes cellular invasion requires a concerted manipulation of host epithelial cell membrane receptors to initiate internalization and infection often via receptor glycosylation. Bacterial interactions with host glycans are intimately involved in modulating cellular responses through signaling cascades at the membrane and in intracellular compartments. Characterizing the mechanisms underpinning these modulations is essential for predictive use of dietary prebiotics to diminish pathogen association. We demonstrated that human milk oligosaccharide (HMO) pretreatment of colonic epithelial cells (Caco-2) led to a 50{\%} decrease in Listeria association, while Biomos pretreatment increased host association by 150{\%}. L. monocytogenes-induced gene expression changes due to oligosaccharide pretreatment revealed global alterations in host signaling pathways that resulted in differential subcellular localization of L. monocytogenes during early infection. Ultimately, HMO pretreatment led to bacterial clearance in Caco-2 cells via induction of the unfolded protein response and eIF2 signaling, while Biomos pretreatment resulted in the induction of host autophagy and L. monocytogenes vacuolar escape earlier in the infection progression. This study demonstrates the capacity of prebiotic oligosaccharides to minimize infection through induction of host-intrinsic protective responses.",
keywords = "Autophagy, C-di-AMP, Cell-mediated immunity (CMI), eIF2 signaling, ER stress, Human milk oligosaccharide, Prebiotic oligosaccharide, Unfolded protein response",
author = "Poyin Chen and Taylor Reiter and Bihua Huang and Nguyet Kong and Weimer, {Bart C}",
year = "2017",
month = "12",
day = "19",
doi = "10.3390/pathogens6040068",
language = "English (US)",
volume = "6",
pages = "1--25",
journal = "Pathogens",
issn = "2076-0817",
publisher = "MDPI AG",
number = "4",

}

TY - JOUR

T1 - Prebiotic oligosaccharides potentiate host protective responses against L. Monocytogenes infection

AU - Chen, Poyin

AU - Reiter, Taylor

AU - Huang, Bihua

AU - Kong, Nguyet

AU - Weimer, Bart C

PY - 2017/12/19

Y1 - 2017/12/19

N2 - Prebiotic oligosaccharides are used to modulate enteric pathogens and reduce pathogen shedding. The interactions with prebiotics that alter Listeria monocytogenes infection are not yet clearly delineated. L. monocytogenes cellular invasion requires a concerted manipulation of host epithelial cell membrane receptors to initiate internalization and infection often via receptor glycosylation. Bacterial interactions with host glycans are intimately involved in modulating cellular responses through signaling cascades at the membrane and in intracellular compartments. Characterizing the mechanisms underpinning these modulations is essential for predictive use of dietary prebiotics to diminish pathogen association. We demonstrated that human milk oligosaccharide (HMO) pretreatment of colonic epithelial cells (Caco-2) led to a 50% decrease in Listeria association, while Biomos pretreatment increased host association by 150%. L. monocytogenes-induced gene expression changes due to oligosaccharide pretreatment revealed global alterations in host signaling pathways that resulted in differential subcellular localization of L. monocytogenes during early infection. Ultimately, HMO pretreatment led to bacterial clearance in Caco-2 cells via induction of the unfolded protein response and eIF2 signaling, while Biomos pretreatment resulted in the induction of host autophagy and L. monocytogenes vacuolar escape earlier in the infection progression. This study demonstrates the capacity of prebiotic oligosaccharides to minimize infection through induction of host-intrinsic protective responses.

AB - Prebiotic oligosaccharides are used to modulate enteric pathogens and reduce pathogen shedding. The interactions with prebiotics that alter Listeria monocytogenes infection are not yet clearly delineated. L. monocytogenes cellular invasion requires a concerted manipulation of host epithelial cell membrane receptors to initiate internalization and infection often via receptor glycosylation. Bacterial interactions with host glycans are intimately involved in modulating cellular responses through signaling cascades at the membrane and in intracellular compartments. Characterizing the mechanisms underpinning these modulations is essential for predictive use of dietary prebiotics to diminish pathogen association. We demonstrated that human milk oligosaccharide (HMO) pretreatment of colonic epithelial cells (Caco-2) led to a 50% decrease in Listeria association, while Biomos pretreatment increased host association by 150%. L. monocytogenes-induced gene expression changes due to oligosaccharide pretreatment revealed global alterations in host signaling pathways that resulted in differential subcellular localization of L. monocytogenes during early infection. Ultimately, HMO pretreatment led to bacterial clearance in Caco-2 cells via induction of the unfolded protein response and eIF2 signaling, while Biomos pretreatment resulted in the induction of host autophagy and L. monocytogenes vacuolar escape earlier in the infection progression. This study demonstrates the capacity of prebiotic oligosaccharides to minimize infection through induction of host-intrinsic protective responses.

KW - Autophagy

KW - C-di-AMP

KW - Cell-mediated immunity (CMI)

KW - eIF2 signaling

KW - ER stress

KW - Human milk oligosaccharide

KW - Prebiotic oligosaccharide

KW - Unfolded protein response

UR - http://www.scopus.com/inward/record.url?scp=85040943816&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85040943816&partnerID=8YFLogxK

U2 - 10.3390/pathogens6040068

DO - 10.3390/pathogens6040068

M3 - Article

AN - SCOPUS:85040943816

VL - 6

SP - 1

EP - 25

JO - Pathogens

JF - Pathogens

SN - 2076-0817

IS - 4

ER -