The role of 5-HT2B receptors in mitral valvulopathy: bone marrow mobilization of endothelial progenitors

Br J Pharmacol. 2017 Nov;174(22):4123-4139. doi: 10.1111/bph.13981. Epub 2017 Oct 15.

Abstract

Background and purpose: Valvular heart disease (VHD) is highly prevalent in industrialized countries. Chronic use of anorexigens, amphetamine or ergot derivatives targeting the 5-HT system is associated with VHD. Here, we investigated the contribution of 5-HT receptors in a model of valve degeneration induced by nordexfenfluramine, the main metabolite of the anorexigens, dexfenfluramine and benfluorex.

Experimental approach: Nordexfenfluramine was infused chronically (28 days) in mice ((WT and transgenic Htr2B -/- , Htr2A -/- , and Htr2B/2A -/- ) to induce mitral valve lesions. Bone marrow transplantation was also carried out. Haemodynamics were measured with echocardiography; tissues and cells were analysed by histology, immunocytochemistry, flow cytometry and RT -qPCR. Samples of human prolapsed mitral valves were also analysed.

Key results: Chronic treatment of mice with nordexfenfluramine activated 5-HT2B receptors and increased valve thickness and cell density in a thick extracellular matrix, mimicking early steps of mitral valve remodelling. Lesions were prevented by 5-HT2A or 5-HT2B receptor antagonists and in transgenic Htr2B -/- or Htr2A/2B -/- mice. Surprisingly, valve lesions were mainly formed by numerous non-proliferative CD34+ endothelial progenitors. These progenitors originated from bone marrow (BM) as revealed by BM transplantation. The initial steps of mitral valve remodelling involved mobilization of BM-derived CD34+ CD31+ cells by 5-HT2B receptor stimulation. Analysis of human prolapsed mitral valves showing spontaneous degenerative lesions, demonstrated the presence of non-proliferating CD34+ /CD309+ /NOS3+ endothelial progenitors expressing 5-HT2B receptors.

Conclusions and implications: BM-derived endothelial progenitor cells make a crucial contribution to the remodelling of mitral valve tissue. Our data describe a new and important mechanism underlying human VHD.

MeSH terms

  • Animals
  • Bone Marrow Transplantation
  • Endothelial Progenitor Cells* / metabolism
  • Heart Valve Diseases / metabolism*
  • Heart Valve Diseases / pathology
  • Male
  • Mice, Transgenic
  • Mitral Valve / drug effects
  • Mitral Valve / metabolism*
  • Mitral Valve / pathology
  • Norfenfluramine / pharmacology
  • Receptor, Serotonin, 5-HT2A / genetics
  • Receptor, Serotonin, 5-HT2B / genetics
  • Receptor, Serotonin, 5-HT2B / metabolism*
  • Serotonin 5-HT2 Receptor Antagonists / pharmacology

Substances

  • Receptor, Serotonin, 5-HT2A
  • Receptor, Serotonin, 5-HT2B
  • Serotonin 5-HT2 Receptor Antagonists
  • Norfenfluramine