Pharmacological reduction of mucosal but not neuronal serotonin opposes inflammation in mouse intestine

Gut. 2014 Jun;63(6):928-37. doi: 10.1136/gutjnl-2013-304901. Epub 2013 Jun 7.

Abstract

Objective: Enterochromaffin cell-derived serotonin (5-HT) promotes intestinal inflammation. We tested hypotheses that peripheral tryptophan hydroxylase (TPH) inhibitors, administered orally, block 5-HT biosynthesis and deplete 5-HT from enterochromaffin cells sufficiently to ameliorate intestinal inflammation; moreover, peripheral TPH inhibitors fail to enter the murine enteric nervous system (ENS) or central nervous systems and thus do not affect constitutive gastrointestinal motility.

Design: Two peripheral TPH inhibitors, LP-920540 and telotristat etiprate (LX1032; LX1606) were given orally to mice. Effects were measured on 5-HT levels in the gut, blood and brain, 5-HT immunoreactivity in the ENS, gastrointestinal motility and severity of trinitrobenzene sulfonic acid (TNBS)-induced colitis. Quantitation of clinical scores, histological damage and intestinal expression of inflammation-associated cytokines and chemokines with focused microarrays and real-time reverse transcriptase PCR were employed to evaluate the severity of intestinal inflammation.

Results: LP-920540 and LX1032 reduced 5-HT significantly in the gut and blood but not in the brain. Neither LP-920540 nor LX1032 decreased 5-HT immunoreactive neurons or fibres in the myenteric plexus and neither altered total gastrointestinal transit time, colonic motility or gastric emptying in mice. In contrast, oral LP-920540 and LX1032 reduced the severity of TNBS-induced colitis; the expression of 24% of 84 genes encoding inflammation-related cytokines and chemokines was lowered at least fourfold and the reduced expression of 17% was statistically significant.

Conclusions: Observations suggest that that peripheral TPH inhibitors uncouple the positive linkage of enterochromaffin cell-derived 5-HT to intestinal inflammation. Because peripheral TPH inhibitors evidently do not enter the murine ENS, they lack deleterious effects on constitutive intestinal motility in mice.

Keywords: Enteric Nervous System; Experimental Colitis; Gastrointestinal Transit; Neurogastroenterology; Serotonin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / metabolism
  • Colitis / chemically induced
  • Colitis / metabolism*
  • Colitis / pathology
  • Cytokines / genetics
  • Down-Regulation / drug effects*
  • Enzyme Inhibitors / pharmacology*
  • Gastrointestinal Motility / drug effects
  • Gene Expression / drug effects*
  • Intestinal Mucosa / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Myenteric Plexus / metabolism
  • Neurons / metabolism*
  • Phenylalanine / analogs & derivatives
  • Phenylalanine / pharmacology
  • Pyrimidines / pharmacology
  • Serotonin / biosynthesis*
  • Serotonin / blood
  • Severity of Illness Index
  • Trinitrobenzenesulfonic Acid
  • Tryptophan Hydroxylase / antagonists & inhibitors

Substances

  • Cytokines
  • Enzyme Inhibitors
  • Pyrimidines
  • ethyl 2-amino-3-(4-(2-amino-6-(2,2,2-trifluoro-1-(3'-fluorobiphenyl-4-yl)ethoxy)pyrimidin-4-yl)phenyl)propanoic acid
  • Serotonin
  • telotristat
  • Phenylalanine
  • Trinitrobenzenesulfonic Acid
  • Tryptophan Hydroxylase