Targeting 5-Hydroxytryptamine Receptor 1A in the Portal Vein to Decrease Portal Hypertension

Gastroenterology. 2024 Oct;167(5):993-1007. doi: 10.1053/j.gastro.2024.06.007. Epub 2024 Jun 19.

Abstract

Background & aims: Portal hypertension (PH) is one of the most frequent complications of chronic liver disease. The peripheral 5-hydroxytryptamine (5-HT) level was increased in cirrhotic patients. We aimed to elucidate the function and mechanism of 5-HT receptor 1A (HTR1A) in the portal vein (PV) on PH.

Methods: PH models were induced by thioacetamide injection, bile duct ligation, or partial PV ligation. HTR1A expression was detected using real-time polymerase chain reaction, in situ hybridization, and immunofluorescence staining. In situ intraportal infusion was used to assess the effects of 5-HT, the HTR1A agonist 8-OH-DPAT, and the HTR1A antagonist WAY-100635 on portal pressure (PP). Htr1a-knockout (Htr1a-/-) rats and vascular smooth muscle cell (VSMC)-specific Htr1a-knockout (Htr1aΔVSMC) mice were used to confirm the regulatory role of HTR1A on PP.

Results: HTR1A expression was significantly increased in the hypertensive PV of PH model rats and cirrhotic patients. Additionally, 8-OH-DPAT increased, but WAY-100635 decreased, the PP in rats without affecting liver fibrosis and systemic hemodynamics. Furthermore, 5-HT or 8-OH-DPAT directly induced the contraction of isolated PVs. Genetic deletion of Htr1a in rats and VSMC-specific Htr1a knockout in mice prevented the development of PH. Moreover, 5-HT triggered adenosine 3',5'-cyclic monophosphate pathway-mediated PV smooth muscle cell contraction via HTR1A in the PV. We also confirmed alverine as an HTR1A antagonist and demonstrated its capacity to decrease PP in rats with thioacetamide-, bile duct ligation-, and partial PV ligation-induced PH.

Conclusions: Our findings reveal that 5-HT promotes PH by inducing the contraction of the PV and identify HTR1A as a promising therapeutic target for attenuating PH. As an HTR1A antagonist, alverine is expected to become a candidate for clinical PH treatment.

Keywords: 5-Hydroxytryptamine; Alverine; HTR1A; Portal Hypertension; Portal Vein Smooth Muscle Cells.

MeSH terms

  • 8-Hydroxy-2-(di-n-propylamino)tetralin / pharmacology
  • Animals
  • Cyclic AMP / metabolism
  • Disease Models, Animal
  • Female
  • Humans
  • Hypertension, Portal* / etiology
  • Hypertension, Portal* / genetics
  • Hypertension, Portal* / metabolism
  • Hypertension, Portal* / physiopathology
  • Ligation
  • Liver Cirrhosis / genetics
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology
  • Liver Cirrhosis, Experimental / chemically induced
  • Liver Cirrhosis, Experimental / genetics
  • Liver Cirrhosis, Experimental / metabolism
  • Liver Cirrhosis, Experimental / pathology
  • Liver Cirrhosis, Experimental / physiopathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / pathology
  • Piperazines / pharmacology
  • Portal Pressure* / drug effects
  • Portal Vein* / metabolism
  • Pyridines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Wistar
  • Receptor, Serotonin, 5-HT1A* / genetics
  • Receptor, Serotonin, 5-HT1A* / metabolism
  • Serotonin / metabolism
  • Serotonin / pharmacology
  • Serotonin 5-HT1 Receptor Agonists* / pharmacology
  • Serotonin 5-HT1 Receptor Antagonists / pharmacology
  • Signal Transduction
  • Thioacetamide / toxicity

Substances

  • 8-Hydroxy-2-(di-n-propylamino)tetralin
  • Cyclic AMP
  • N-(2-(4-(2-methoxyphenyl)-1-piperazinyl)ethyl)-N-(2-pyridinyl)cyclohexanecarboxamide
  • Piperazines
  • Pyridines
  • Receptor, Serotonin, 5-HT1A
  • Serotonin
  • Serotonin 5-HT1 Receptor Agonists
  • Serotonin 5-HT1 Receptor Antagonists
  • Thioacetamide
  • HTR1A protein, human
  • Htr1a protein, mouse