Cited by 178Gastrointestinal motility and disordersProbiotics and Fermented FoodsGut microbiota and health

Bacteroides fragilis polysaccharide A is necessary and sufficient for acute activation of intestinal sensory neurons

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Mao, Yu-Kang, Kasper, Dennis L., Wang, Bingxian, Forsythe, Paul, Bienenstock, John, Kunze, Wolfgang A.·2013·Nature Communications

Abstract

Symbionts or probiotics are known to affect the nervous system. To understand the mechanisms involved, it is important to measure sensory neuron responses and identify molecules responsible for this interaction. Here we test the effects of adding Lactobacillus rhamnosus (JB-1) and Bacteroides fragilis to the epithelium while making voltage recordings from intestinal primary afferent neurons. Sensory responses are recorded within 8 s of applying JB-1 and excitability facilitated within 15 min. Bacteroides fragilis produces similar results, as does its isolated, capsular exopolysaccharide, polysaccharide A. Lipopolysaccharide-free polysaccharide A completely mimics the neuronal effects of the parent organism. Experiments with a mutant Bacteroides fragilis devoid of polysaccharide A shows that polysaccharide A is necessary and sufficient for the neuronal effects. Complex carbohydrates have not been reported before as candidates for such signalling between symbionts and the host. These observations indicate new neuronal targets and invite further study of bacterial carbohydrates as inter-kingdom signalling molecules between beneficial bacteria and sensory neurons.

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  • Bacteroides fragilis, likely via its capsular exopolysaccharide, can influence ENS function, while L. rhamnosus strain JB-1 does so via a G-protein-coupled receptor-mediated pathway.

    “Bacteroides (B.) fragilis for example, likely as a consequence of its capsular exopolysaccharide, can influence ENS function while an L. rhamnosus strain (JB-1) does so via a G-protein-coupled receptor-mediated pathway (Mao et al., 2013).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Mao et al., 2013

    The Abstract and Discussion report that B. fragilis affects intestinal sensory neurons and that its capsular polysaccharide A is necessary and sufficient for the observed effects. In “Short latency orthodromic responses to the bacteria and PSA” (page unavailable), a G-protein inhibitor abolished JB-1’s effect on neuronal excitability. That supports G-protein involvement, but the paper does not establish a specific G-protein-coupled receptor-mediated pathway for JB-1. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Different bacterial strains differentially influence enteric nerve activity and may do so by different mechanisms.

    “different bacterial strains differentially influence enteric nerve activity but that they may do so by different mechanisms (Mao et al., 2013).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Mao et al., 2013

  • The effects of L. rhamnosus JB-1 on the ENS are not dependent on diffusion of molecules from the epithelium to the myenteric neurons.

    “the authors show that the effects on the ENS are not dependent on diffusion of molecules from the epithelium to the myenteric neurons.”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Mao et al., 2013

  • Intrinsic primary afferent neurons are cellular targets of neuroactive bacteria and transmit microbial messages to the brain via the vagus nerve.

    “Intrinsic primary afferent neurons (IPANs) are cellular targets of neuroactive bacteria and transmit microbial messages to the brain via the vagus nerve.135,136”

    From The Gut Microbiome and the Brain (2014) · cites this paper as [136]

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Research works printed but not linked: 1

  1. Kunze, W., Mao, Y., Forsythe, P. & Bienenstock, J. Effect of Lactobacillus sp. (Lb) probiotic ingestion on membrane properties of intrinsic sensory neurons in rat colon. Gastroenterology 130, A401 (2006).

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Authors
Mao, Y.-K., Kasper, D. L., Wang, B., Forsythe, P., Bienenstock, J., & Kunze, W. A.
Affiliations
  • Harvard University (US)
  • McMaster University (CA)
  • St. Joseph’s Healthcare Hamilton (CA)
Corresponding author
Kunze, Wolfgang A.
Venue
Nature Communications
Published
2013-02-12
Volume
4
Issue
1
Pages
1465-1465
ISSN
2041-1723 (ISSN-L)
OpenAlex
W2104319202
Cited by
178
References
54
Citations by year
2026: 8 · 2025: 13 · 2024: 20 · 2023: 11 · 2022: 16 · 2021: 12 · 2020: 16 · 2019: 18 · 2018: 9 · 2017: 15 · 2016: 16 · 2015: 9 · 2014: 11 · 2013: 4
FWCI
12.57
Type
journal article
Language
en
Open access
Locations
  • Nature Communications (publishedVersion)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • Crohn's and Colitis Foundation of America
  • Leona M. and Harry B. Helmsley Charitable Trust
  • McMaster University
  • Crohn's and Colitis Foundation
Topics
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
Bacteroides fragilis, polysaccharide A, Lactobacillus rhamnosus, sensory neuron excitability, gut-brain axis, bacterial carbohydrates, myenteric plexus, commensal bacteria, enteric nervous system, symbiotic bacteria
MeSH terms
Action Potentials, Animals, Bacteroides fragilis, Dissection, Epithelium, Intestinal Mucosa, Intestines, Polysaccharides, Bacterial, Pyrazoles, Sensory Receptor Cells, Patch-Clamp Techniques, Mice, Intermediate-Conductance Calcium-Activated Potassium Channels, Lacticaseibacillus rhamnosus, In Vitro Techniques

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