Activation of the 5-hydroxytryptamine 4 receptor ameliorates tight junction barrier dysfunction in the colon of type 1 diabetic mice

Acta Biochim Biophys Sin (Shanghai). 2023 Dec 25;55(12):1874-1883. doi: 10.3724/abbs.2023137.

Abstract

Hyperglycemia drives dysfunction of the intestinal barrier. 5-Hydroxytryptaine 4 receptor (5-HT 4R) agonists have been considered therapeutics for constipation in clnic. However, the roles of 5-HT 4R activation in mucosa should be fully realized. Here, we investigate the effects of 5-HT 4R activation on diabetes-induced disruption of the tight junction (TJ) barrier in the colon. Not surprisingly, the TJ barrier in diabetic mice with or without 5-HT 4R is tremendously destroyed, as indicated by increased serum fluorescein isothiocyanate (FITC)-dextran and decreased transepithelial electrical resistance (TER). Simultaneously, decreased expressions of TJ proteins are shown in both wild-type (WT) and 5-HT 4R knockout (KO) mice with diabetes. Notably, chronic treatment with intraperitoneal injection of a 5-HT 4R agonist in WT mice with diabetes repairs the TJ barrier and promotes TJ protein expressions, including occludin, claudin-1 and ZO-1, in the colon, whereas a 5-HT 4R agonist does not improve TJ barrier function or TJ protein expressions in 5-HT 4R KO mice with diabetes. Furthermore, stimulation of 5-HT 4R inhibits diabetes-induced upregulation of myosin light chain kinase (MLCK), Rho-associated coiled coil protein kinase 1 (ROCK1), and phosphorylated myosin light chain (p-MLC), which are key molecules that regulate TJ integrity, in the colonic mucosa of WT mice. However, such action induced by a 5-HT 4R agonist is not observed in 5-HT 4R KO mice with diabetes. These findings indicate that 5-HT 4R activation may restore TJ integrity by inhibiting the expressions of MLCK, ROCK1 and p-MLC, improving epithelial barrier function in diabetes.

Keywords: 5-HTR; MLCK; ROCK1; diabetes; tight junction barrier.

MeSH terms

  • Animals
  • Colon / metabolism
  • Diabetes Mellitus, Experimental* / metabolism
  • Diabetes Mellitus, Type 1* / metabolism
  • Intestinal Mucosa / metabolism
  • Mice
  • Receptors, Serotonin, 5-HT4* / genetics
  • Receptors, Serotonin, 5-HT4* / metabolism
  • Serotonin / metabolism
  • Serotonin / pharmacology
  • Tight Junction Proteins / genetics
  • Tight Junction Proteins / metabolism
  • Tight Junctions

Substances

  • fluorescein isothiocyanate dextran
  • Receptors, Serotonin, 5-HT4
  • Serotonin
  • Tight Junction Proteins

Grants and funding

This work was supported by the grants from the National Natural Science Foundation of China (No. 81770355 to G.Z.), the Natural Science Foundation of Shanghai (No. 23ZR1457700 to H.H.), the Shanghai Tongi Hospital (No. GJPY2123 to H.H.), and the Innovative Research Team of High-Level Local Universities in Shanghai (No. SHSMU-ZDCX20211102 to G.Z).