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Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems

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Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems. / Al-Nedawi, Khalid; Mian, M Firoz; Hossain, Nazia; Karimi, Khalil; Mao, Yu-Kang; Forsythe, Paul; Min, Kevin K; Stanisz, Andrew M; Kunze, Wolfgang A; Bienenstock, John.

In: FASEB J, Vol. 29, No. 2, 02.2015, p. 684-95.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Al-Nedawi, K, Mian, MF, Hossain, N, Karimi, K, Mao, Y-K, Forsythe, P, Min, KK, Stanisz, AM, Kunze, WA & Bienenstock, J 2015, 'Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems', FASEB J, vol. 29, no. 2, pp. 684-95. https://doi.org/10.1096/fj.14-259721

APA

Al-Nedawi, K., Mian, M. F., Hossain, N., Karimi, K., Mao, Y-K., Forsythe, P., Min, K. K., Stanisz, A. M., Kunze, W. A., & Bienenstock, J. (2015). Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems. FASEB J, 29(2), 684-95. https://doi.org/10.1096/fj.14-259721

Vancouver

Al-Nedawi K, Mian MF, Hossain N, Karimi K, Mao Y-K, Forsythe P et al. Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems. FASEB J. 2015 Feb;29(2):684-95. https://doi.org/10.1096/fj.14-259721

Bibtex

@article{19ada81f530642febaf251f151c143e4,
title = "Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems",
abstract = "Ingestion of a commensal bacteria, Lactobacillus rhamnosus JB-1, has potent immunoregulatory effects, and changes nerve-dependent colon migrating motor complexes (MMCs), enteric nerve function, and behavior. How these alterations occur is unknown. JB-1 microvesicles (MVs) are enriched for heat shock protein components such as chaperonin 60 heat-shock protein isolated from Escherichia coli (GroEL) and reproduce regulatory and neuronal effects in vitro and in vivo. Ingested labeled MVs were detected in murine Peyer's patch (PP) dendritic cells (DCs) within 18 h. After 3 d, PP and mesenteric lymph node DCs assumed a regulatory phenotype and increased functional regulatory CD4(+)25(+)Foxp3+ T cells. JB-1, MVs, and GroEL similarly induced phenotypic change in cocultured DCs via multiple pathways including C-type lectin receptors specific intercellular adhesion molecule-3 grabbing non-integrin-related 1 and Dectin-1, as well as TLR-2 and -9. JB-1 and MVs also decreased the amplitude of neuronally dependent MMCs in an ex vivo model of peristalsis. Gut epithelial, but not direct neuronal application of, MVs, replicated functional effects of JB-1 on in situ patch-clamped enteric neurons. GroEL and anti-TLR-2 were without effect in this system, suggesting the importance of epithelium neuron signaling and discrimination between pathways for bacteria-neuron and -immune communication. Together these results offer a mechanistic explanation of how Gram-positive commensals and probiotics may influence the host's immune and nervous systems.",
keywords = "Animals, Bone Marrow Cells, CD4-Positive T-Lymphocytes, Chaperonin 60, Coculture Techniques, Dendritic Cells, Enteric Nervous System, Forkhead Transcription Factors, Gastrointestinal Tract, Immune System, Interleukin-2 Receptor alpha Subunit, Lactobacillus rhamnosus, Lectins, C-Type, Lymph Nodes, Male, Mice, Mice, Inbred BALB C, Neurons, Peristalsis, Peyer's Patches, Phenotype, Probiotics, Proteomics, Signal Transduction",
author = "Khalid Al-Nedawi and Mian, {M Firoz} and Nazia Hossain and Khalil Karimi and Yu-Kang Mao and Paul Forsythe and Min, {Kevin K} and Stanisz, {Andrew M} and Kunze, {Wolfgang A} and John Bienenstock",
note = "{\textcopyright} FASEB.",
year = "2015",
month = feb,
doi = "10.1096/fj.14-259721",
language = "English",
volume = "29",
pages = "684--95",
journal = "FASEB J",
issn = "0892-6638",
publisher = "FASEB",
number = "2",

}

RIS

TY - JOUR

T1 - Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems

AU - Al-Nedawi, Khalid

AU - Mian, M Firoz

AU - Hossain, Nazia

AU - Karimi, Khalil

AU - Mao, Yu-Kang

AU - Forsythe, Paul

AU - Min, Kevin K

AU - Stanisz, Andrew M

AU - Kunze, Wolfgang A

AU - Bienenstock, John

N1 - © FASEB.

PY - 2015/2

Y1 - 2015/2

N2 - Ingestion of a commensal bacteria, Lactobacillus rhamnosus JB-1, has potent immunoregulatory effects, and changes nerve-dependent colon migrating motor complexes (MMCs), enteric nerve function, and behavior. How these alterations occur is unknown. JB-1 microvesicles (MVs) are enriched for heat shock protein components such as chaperonin 60 heat-shock protein isolated from Escherichia coli (GroEL) and reproduce regulatory and neuronal effects in vitro and in vivo. Ingested labeled MVs were detected in murine Peyer's patch (PP) dendritic cells (DCs) within 18 h. After 3 d, PP and mesenteric lymph node DCs assumed a regulatory phenotype and increased functional regulatory CD4(+)25(+)Foxp3+ T cells. JB-1, MVs, and GroEL similarly induced phenotypic change in cocultured DCs via multiple pathways including C-type lectin receptors specific intercellular adhesion molecule-3 grabbing non-integrin-related 1 and Dectin-1, as well as TLR-2 and -9. JB-1 and MVs also decreased the amplitude of neuronally dependent MMCs in an ex vivo model of peristalsis. Gut epithelial, but not direct neuronal application of, MVs, replicated functional effects of JB-1 on in situ patch-clamped enteric neurons. GroEL and anti-TLR-2 were without effect in this system, suggesting the importance of epithelium neuron signaling and discrimination between pathways for bacteria-neuron and -immune communication. Together these results offer a mechanistic explanation of how Gram-positive commensals and probiotics may influence the host's immune and nervous systems.

AB - Ingestion of a commensal bacteria, Lactobacillus rhamnosus JB-1, has potent immunoregulatory effects, and changes nerve-dependent colon migrating motor complexes (MMCs), enteric nerve function, and behavior. How these alterations occur is unknown. JB-1 microvesicles (MVs) are enriched for heat shock protein components such as chaperonin 60 heat-shock protein isolated from Escherichia coli (GroEL) and reproduce regulatory and neuronal effects in vitro and in vivo. Ingested labeled MVs were detected in murine Peyer's patch (PP) dendritic cells (DCs) within 18 h. After 3 d, PP and mesenteric lymph node DCs assumed a regulatory phenotype and increased functional regulatory CD4(+)25(+)Foxp3+ T cells. JB-1, MVs, and GroEL similarly induced phenotypic change in cocultured DCs via multiple pathways including C-type lectin receptors specific intercellular adhesion molecule-3 grabbing non-integrin-related 1 and Dectin-1, as well as TLR-2 and -9. JB-1 and MVs also decreased the amplitude of neuronally dependent MMCs in an ex vivo model of peristalsis. Gut epithelial, but not direct neuronal application of, MVs, replicated functional effects of JB-1 on in situ patch-clamped enteric neurons. GroEL and anti-TLR-2 were without effect in this system, suggesting the importance of epithelium neuron signaling and discrimination between pathways for bacteria-neuron and -immune communication. Together these results offer a mechanistic explanation of how Gram-positive commensals and probiotics may influence the host's immune and nervous systems.

KW - Animals

KW - Bone Marrow Cells

KW - CD4-Positive T-Lymphocytes

KW - Chaperonin 60

KW - Coculture Techniques

KW - Dendritic Cells

KW - Enteric Nervous System

KW - Forkhead Transcription Factors

KW - Gastrointestinal Tract

KW - Immune System

KW - Interleukin-2 Receptor alpha Subunit

KW - Lactobacillus rhamnosus

KW - Lectins, C-Type

KW - Lymph Nodes

KW - Male

KW - Mice

KW - Mice, Inbred BALB C

KW - Neurons

KW - Peristalsis

KW - Peyer's Patches

KW - Phenotype

KW - Probiotics

KW - Proteomics

KW - Signal Transduction

U2 - 10.1096/fj.14-259721

DO - 10.1096/fj.14-259721

M3 - SCORING: Journal article

C2 - 25392266

VL - 29

SP - 684

EP - 695

JO - FASEB J

JF - FASEB J

SN - 0892-6638

IS - 2

ER -