Serotonin 5-HT7 receptor is critically involved in acute and chronic inflammation of the gastrointestinal tract

Inflamm Bowel Dis. 2014 Sep;20(9):1516-29. doi: 10.1097/MIB.0000000000000150.

Abstract

Background: Intestinal inflammation is often associated with an increased level of serotonin (5-HT), an important gastrointestinal signaling molecule involved in gut homeostasis through stimulation of specific receptors. In this study, we investigated the role of 5-HT7 receptor (5-HT7R) in the induction and development of intestinal inflammation using a mouse model of acute and chronic colitis and human patients with Crohn's disease (CD).

Methods: Acute colitis was induced through administration of dextran sodium sulfate to wild-type, 5-HT7R-deficient mice and hematopoietic bone marrow chimera. Chronic colitis was induced in interleukin 10-deficient mice. The role of 5-HT7R in gut inflammation was assessed using agonist/antagonist treatment. We investigated expression and distribution of 5-HT7R, extent of gut inflammation with magnetic resonance imaging and histological analysis, survival rate, and disease activity index. Finally, biopsies from the large intestine of patients with CD were analyzed.

Results: Under basal conditions, 5-HT7R is expressed both in enteric neurons and CD11c cells of the large intestine. Expression of 5-HT7R significantly increased after induction of colitis in mice and in inflamed intestinal regions of patients with CD in CD11c/CD86 double-positive cells. Pharmacological blockade or genetic ablation of 5-HT7R resulted in increased severity of both acute and chronic dextran sodium sulfate-induced colitis, whereas receptor stimulation showed an anti-inflammatory effect. Analysis of bone marrow chimera indicated importance of 5-HT7R expressed by hematopoietic cells in intestinal inflammation.

Conclusions: The 5-HT7R expressed on CD11c/CD86-positive myeloid cells modulates the severity of intestinal inflammation in an acute and chronic colitis and thus represents a potential therapeutic target for the treatment of inflammatory disorders such as CD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Disease
  • Adolescent
  • Adult
  • Animals
  • Blotting, Western
  • Chronic Disease
  • Colitis / chemically induced
  • Colitis / metabolism
  • Colitis / pathology*
  • Crohn Disease / metabolism
  • Crohn Disease / pathology*
  • Dextran Sulfate / toxicity
  • Disease Models, Animal
  • Female
  • Follow-Up Studies
  • Gastrointestinal Tract / drug effects
  • Gastrointestinal Tract / metabolism
  • Gastrointestinal Tract / pathology*
  • Humans
  • Immunoenzyme Techniques
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammation / pathology*
  • Interleukin-10 / physiology
  • Male
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Prognosis
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Serotonin / chemistry
  • Receptors, Serotonin / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Serotonin / metabolism
  • Young Adult

Substances

  • IL10 protein, mouse
  • RNA, Messenger
  • Receptors, Serotonin
  • serotonin 7 receptor
  • Interleukin-10
  • Serotonin
  • Dextran Sulfate