Intestinal upregulation of melanin-concentrating hormone in TNBS-induced enterocolitis in adult zebrafish

PLoS One. 2013 Dec 20;8(12):e83194. doi: 10.1371/journal.pone.0083194. eCollection 2013.

Abstract

Background: Melanin-concentrating hormone (MCH), an evolutionarily conserved appetite-regulating neuropeptide, has been recently implicated in the pathogenesis of inflammatory bowel disease (IBD). Expression of MCH is upregulated in inflamed intestinal mucosa in humans with colitis and MCH-deficient mice treated with trinitrobenzene-sulfonic acid (TNBS) develop an attenuated form of colitis compared to wild type animals. Zebrafish have emerged as a new animal model of IBD, although the majority of the reported studies concern zebrafish larvae. Regulation MCH expression in the adult zebrafish intestine remains unknown.

Methods: In the present study we induced enterocolitis in adult zebrafish by intrarectal administration of TNBS. Follow-up included survival analysis, histological assessment of changes in intestinal architecture, and assessment of intestinal infiltration by myeloperoxidase positive cells and cytokine transcript levels.

Results: Treatment with TNBS dose-dependently reduced fish survival. This response required the presence of an intact microbiome, since fish pre-treated with vancomycin developed less severe enterocolitis. At 6 hours post-challenge, we detected a significant influx of myeloperoxidase positive cells in the intestine and upregulation of both proinflammatory and anti-inflammatory cytokines. Most importantly, and in analogy to human IBD and TNBS-induced mouse experimental colitis, we found increased intestinal expression of MCH and its receptor in TNBS-treated zebrafish.

Conclusions: Taken together these findings not only establish a model of chemically-induced experimental enterocolitis in adult zebrafish, but point to effects of MCH in intestinal inflammation that are conserved across species.

Publication types

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

MeSH terms

  • Administration, Rectal
  • Animals
  • Cell Movement
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Enterocolitis / chemically induced
  • Enterocolitis / genetics*
  • Enterocolitis / mortality
  • Enterocolitis / pathology
  • Fish Proteins / genetics*
  • Fish Proteins / metabolism
  • Gene Expression Regulation
  • Humans
  • Hypothalamic Hormones / genetics*
  • Hypothalamic Hormones / metabolism
  • Intestinal Mucosa / metabolism*
  • Intestines / microbiology
  • Intestines / pathology
  • Male
  • Melanins / genetics*
  • Melanins / metabolism
  • Microbiota / drug effects
  • Peroxidase / genetics
  • Peroxidase / metabolism
  • Pituitary Hormones / genetics*
  • Pituitary Hormones / metabolism
  • Receptors, Pituitary Hormone / genetics*
  • Receptors, Pituitary Hormone / metabolism
  • Survival Analysis
  • Trinitrobenzenesulfonic Acid
  • Vancomycin / pharmacology
  • Zebrafish

Substances

  • Cytokines
  • Fish Proteins
  • Hypothalamic Hormones
  • Melanins
  • Pituitary Hormones
  • Receptors, Pituitary Hormone
  • melanin-concentrating hormone receptor
  • melanin-concentrating hormone
  • Vancomycin
  • Trinitrobenzenesulfonic Acid
  • Peroxidase