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Cited by 783Gastrointestinal motility and disordersMast cells and histaminePain Mechanisms and Treatments

Mast Cell-Dependent Excitation of Visceral-Nociceptive Sensory Neurons in Irritable Bowel Syndrome

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Barbara, Giovanni, Wang, Bingxian, Stanghellini, Vincenzo, de Giorgio, Roberto, Cremon, Cesare, Di Nardo, Giovanni, Trevisani, Marcello, Campi, Barbara +5 more·2007·Gastroenterology
DOI 10.1053/j.gastro.2006.11.039
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Abstract

Background & aims Intestinal mast cell infiltration may participate to abdominal pain in irritable bowel syndrome (IBS) patients. However, the underlying mechanisms remain unknown. We assessed the effect of mast cell mediators released from the colonic mucosa of IBS patients on the activation of rat sensory neurons in vitro.Methods Colonic mast cell infiltration and mediator release were assessed with quantitative immunofluorescence and immunoenzymatic assays. The effect of mucosal mediators was tested on mesenteric sensory nerve firing and Ca(2+) mobilization in dorsal root ganglia in rats.Results Mediators from IBS patients, but not controls, markedly enhanced the firing of mesenteric nerves (14.7 +/- 3.2 imp/sec vs 2.8 +/- 1.5 imp/sec; P < .05) and stimulated mobilization of Ca(2+) in dorsal root ganglia neurons (29% +/- 4% vs 11% +/- 4%; P < .05). On average, 64% of dorsal root ganglia responsive to mediators were capsaicin-sensitive, known to mediate nociception. Histamine and tryptase were mainly localized to mucosal mast cells. IBS-dependent nerve firing and Ca(2+) mobilization were correlated with the area of the colonic lamina propria occupied by mast cells (r = 0.74; P < .01, and r = 0.78; P < .01, respectively). IBS-dependent excitation of dorsal root ganglia was inhibited by histamine H(1) receptor blockade and serine protease inactivation (inhibition of 51.7%; P < .05 and 74.5%; P < .05; respectively).Conclusions Mucosal mast cell mediators from IBS patients excite rat nociceptive visceral sensory nerves. These results provide new insights into the mechanism underlying visceral hypersensitivity in IBS.

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Crossref · 10.1053/j.gastro.2006.11.039

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  • Patients with IBS have increased concentrations of inflammatory/immune cells in intestinal tissue compared with controls.

    “Evidence supporting this hypothesis includes increased concentrations of inflammatory/immune cells in intestinal tissue from IBS patients, altered levels of pro- and anti-inflammatory cytokines in the GI tract and peripheral blood of patients with IBS (Table 1) (11, 13, 24, 36, 46, 50, 51, 62, 73, 75, 89, 90, 94, 98, 102, 118, 121–124, 168, 174, 185, 187), and IBS-associated polymorphisms in genes”

    From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [13]

  • Some studies demonstrated an increase in activated mast cells in biopsies from specific regions of the GI tract (cecum and terminal ileum) but not from other regions, whereas other studies found activated mast cells in the descending colon.

    “Notably, some studies demonstrated an increase in activated mast cells in biopsies from specific regions of the GI tract (i.e., cecum and terminal ileum) but not from other regions (e.g., ascending colon, descending colon, rectum) (89, 121, 187), whereas other studies have found activated mast cells in the descending colon (11, 13).”

    From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [13]

  • Patients with IBS have altered levels of pro- and anti-inflammatory cytokines in the GI tract and peripheral blood compared with controls.

    “Evidence supporting this hypothesis includes increased concentrations of inflammatory/immune cells in intestinal tissue from IBS patients, altered levels of pro- and anti-inflammatory cytokines in the GI tract and peripheral blood of patients with IBS (Table 1) (11, 13, 24, 36, 46, 50, 51, 62, 73, 75, 89, 90, 94, 98, 102, 118, 121–124, 168, 174, 185, 187), and IBS-associated polymorphisms in genes”

    From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [13]

  • Other studies have reported elevated levels of histamine and tryptase release in patients with IBS compared with controls.

    “Other studies have reported elevated levels of histamine and tryptase release in patients with IBS compared with controls (11, 13, 35, 73).”

    From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [13]

  • Several studies have demonstrated increased concentrations of activated mast cells in patients with IBS compared with controls.

    “Several studies have demonstrated increased concentrations of activated mast cells in patients with IBS compared with controls (11, 13, 24, 46, 89, 94, 121, 187).”

    From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [13]

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Research works printed but not linked: 1

  1. [13]13. Metcalfe DD, Baram D, Mekori YA. Mast cells. Physiol Rev 1997; 77:1033-1079.

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Authors
Barbara, G., Wang, B., Stanghellini, V., de Giorgio, R., Cremon, C., Di Nardo, G., Trevisani, M., Campi, B., Geppetti, P., Tonini, M., Bunnett, N. W., Grundy, D., & Corinaldesi, R.
Affiliations
  • IRCCS Azienda Ospedliero-Universitaria di Bologna Policlinico di Sant'Orsola (IT)
  • University of Tübingen (DE)
  • University of Bologna (IT)
  • University of Ferrara (IT)
  • University of Pavia (IT)
  • University of California, San Francisco (US)
  • University of Sheffield (GB)
Corresponding author
Barbara, Giovanni
ORCID
Venue
Gastroenterology
Publisher
Elsevier BV
Published
2007-01
Volume
132
Issue
1
Pages
26-37
ISSN
0016-5085 (ISSN-L)
DOI
10.1053/j.gastro.2006.11.039
OpenAlex
W2158148601
Cited by
783
References
41
Citations by year
2026: 30 · 2025: 23 · 2024: 37 · 2023: 43 · 2022: 33 · 2021: 36 · 2020: 43 · 2019: 24 · 2018: 49 · 2017: 41 · 2016: 48 · 2015: 34 · 2014: 40 · 2013: 49 · 2012: 49
FWCI
42.78
Type
journal article
Language
en
Open access
Licence
Locations
  • Gastroenterology (publishedVersion)
  • PubMed (publishedVersion)
  • Florence Research (University of Florence) (submittedVersion, other-oa)
  • Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
  • Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
Funders
  • Alexander von Humboldt-Stiftung
  • Ministero dell’Istruzione, dell’Università e della Ricerca (2002052573)
  • Università di Bologna
  • National Institutes of Health (DK39957, DK43207, DK57480)
Topics
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
  • Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
  • Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Keywords
irritable bowel syndrome, mast cells, visceral nociception, visceral hypersensitivity, visceral pain, colonic mucosa, sensory neurons, dorsal root ganglia, histamine, tryptase, histamine H1 receptor, serine protease, capsaicin-sensitive neurons, lamina propria, mast cell mediators
MeSH terms
Adult, Aged, Animals, Biopsy, Calcium, Cell Communication, Colon, Female, Ganglia, Spinal, Humans, Intestinal Mucosa, Male, Mast Cells, Middle Aged, Neurons, Afferent, Nociceptors, Rats, Sprague-Dawley, Enteric Nervous System, Visceral Afferents, Inflammation Mediators, Irritable Bowel Syndrome, Rats

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