Serotonin-induced smooth muscle hyperplasia in various forms of human pulmonary hypertension

Circ Res. 2004 May 14;94(9):1263-70. doi: 10.1161/01.RES.0000126847.27660.69. Epub 2004 Apr 1.

Abstract

Hyperplasia of pulmonary artery smooth muscle cells (PA-SMCs) is a hallmark pathological feature of pulmonary hypertension (PH). Serotonin (5-HT) is involved in the hyperplasia through its interactions with specific receptors and internalization by a specific plasma membrane transporter. We investigated the expression and role of the 5-HT transporter (5-HTT) and 5-HT1B, 5-HT2A, and 5-HT2B receptors in lungs and isolated PA-SMCs from patients with primary PH (n=14), pulmonary veno-occlusive disease (n=4), or secondary PH (SPH, n=8) and nonpulmonary hypertensive control subjects. Whereas strong immunostaining for the three receptor types and 5-HTT was seen in remodeled pulmonary vessels from patients in all PH categories, only 5-HTT expression was increased in lungs and cultured PA-SMCs from patients versus controls. The increased growth response of PA-SMCs from patients with primary PH, pulmonary veno-occlusive disease, or SPH to 5-HT or serum was entirely attributable to 5-HTT overexpression, because 5-HTT inhibitors but not 5-HT receptor antagonists abolished 5-HT mitogenic activity and reduced the serum-induced growth response to similar levels in patients as in controls. The L-allelic variant of the 5-HTT gene promoter, which is associated with 5-HTT overexpression, was present homozygously in 14 of 25 (56%) lung transplantation patients with SPH but in only 27% of controls. Polymorphism of the 5-HTT gene promoter was only partly responsible for the increased 5-HTT expression in PH, because PA-SMCs from patients exhibited higher 5-HTT levels than same-genotype cells from controls and no additional promoter sequence alterations were found. We conclude that 5-HTT overexpression is a common pathogenic mechanism in various forms of PH.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Alleles
  • Carrier Proteins / antagonists & inhibitors
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology*
  • Cell Division
  • Cells, Cultured / pathology
  • Culture Media, Serum-Free / pharmacology
  • Female
  • Gene Expression
  • Genetic Predisposition to Disease
  • Genotype
  • Humans
  • Hyperplasia
  • Hypertension, Pulmonary / etiology
  • Hypertension, Pulmonary / genetics*
  • Hypertension, Pulmonary / pathology
  • Hypertension, Pulmonary / surgery
  • Introns / genetics
  • Lung Diseases / complications
  • Lung Diseases / pathology
  • Lung Transplantation
  • Male
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Membrane Transport Proteins*
  • Middle Aged
  • Muscle, Smooth, Vascular / pathology*
  • Myocytes, Smooth Muscle / pathology
  • Nerve Tissue Proteins / antagonists & inhibitors
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / physiology*
  • Platelet-Derived Growth Factor / pharmacology
  • Polymorphism, Genetic
  • Promoter Regions, Genetic / genetics
  • Pulmonary Artery / pathology*
  • Pulmonary Veno-Occlusive Disease / genetics
  • Pulmonary Veno-Occlusive Disease / pathology
  • Pulmonary Veno-Occlusive Disease / surgery
  • RNA, Messenger / biosynthesis
  • Receptors, Serotonin / genetics
  • Receptors, Serotonin / physiology
  • Serotonin / physiology*
  • Serotonin Antagonists / pharmacology
  • Serotonin Plasma Membrane Transport Proteins
  • Tunica Media / chemistry
  • Tunica Media / pathology

Substances

  • Carrier Proteins
  • Culture Media, Serum-Free
  • Membrane Glycoproteins
  • Membrane Transport Proteins
  • Nerve Tissue Proteins
  • Platelet-Derived Growth Factor
  • RNA, Messenger
  • Receptors, Serotonin
  • SLC6A4 protein, human
  • Serotonin Antagonists
  • Serotonin Plasma Membrane Transport Proteins
  • Serotonin