Pumilio-1 mediated translational control of claudin-5 at the blood-brain barrier

Fluids Barriers CNS. 2024 Jun 19;21(1):52. doi: 10.1186/s12987-024-00553-5.

Abstract

Claudin-5 is one of the most essential tight junction proteins at the blood-brain barrier. A single nucleotide polymorphism rs10314 is located in the 3'-untranslated region of claudin-5 and has been shown to be a risk factor for schizophrenia. Here, we show that the pumilio RNA-binding protein, pumilio-1, is responsible for rs10314-mediated claudin-5 regulation. The RNA sequence surrounding rs10314 is highly homologous to the canonical pumilio-binding sequence and claudin-5 mRNA with rs10314 produces 25% less protein due to its inability to bind to pumilio-1. Pumilio-1 formed cytosolic granules under stress conditions and claudin-5 mRNA appeared to preferentially accumulate in these granules. Added to this, we observed granular pumilio-1 in endothelial cells in human brain tissues from patients with psychiatric disorders or epilepsy with increased/accumulated claudin-5 mRNA levels, suggesting translational claudin-5 suppression may occur in a brain-region specific manner. These findings identify a key regulator of claudin-5 translational processing and how its dysregulation may be associated with neurological and neuropsychiatric disorders.

Keywords: Claudin-5; Pumilio; Tight junction; Translational regulation.

MeSH terms

  • Animals
  • Blood-Brain Barrier* / metabolism
  • Claudin-5* / genetics
  • Claudin-5* / metabolism
  • Endothelial Cells / metabolism
  • Humans
  • Polymorphism, Single Nucleotide
  • Protein Biosynthesis / physiology
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins* / genetics
  • RNA-Binding Proteins* / metabolism

Substances

  • Claudin-5
  • RNA-Binding Proteins
  • RNA, Messenger
  • CLDN5 protein, human