Low molecular weight hyaluronan inhibits lung epithelial ion channels by activating the calcium-sensing receptor

Matrix Biol. 2023 Feb:116:67-84. doi: 10.1016/j.matbio.2023.02.002. Epub 2023 Feb 8.

Abstract

Herein, we tested the hypothesis that low molecular weight hyaluronan (LMW-HA) inhibits lung epithelial ions transport in-vivo, ex-vivo, and in-vitro by activating the calcium-sensing receptor (CaSR). Twenty-four hours post intranasal instillation of 50-150 µg/ml LMW-HA to C57BL/6 mice, there was a 75% inhibition of alveolar fluid clearance (AFC), a threefold increase in the epithelial lining fluid (ELF) depth, and a 20% increase in lung wet/dry (W/D) ratio. Incubation of human and mouse precision cut lung slices with 150 µg/ml LMW-HA reduced the activity and the open probability (Po) of epithelial sodium channel (ENaC) in alveolar epithelial type 2 (ATII) cells, and in mouse tracheal epithelial cells (MTEC) monolayers as early as 4 h. The Cl- current through cystic fibrosis transmembrane conductance regulator (CFTR) and the activity of Na,K-ATPase were both inhibited by more than 66% at 24 h. The inhibitory effects of LMW-HA on ion channels were reversed by 1 µM NPS-2143, or 150 µg/ml high molecular weight hyaluronan (HMW-HA). In HEK-293 cells expressing the calcium-sensitive Cl- channel TMEM16-A, CaSR was required for the activation of the Cl- current by LMW-HA. This is the first demonstration of lung ions and water transport inhibition by LMW-HA, and its mediation through the activation of CaSR.

Keywords: Calcium-sensing receptor; Epithelial ion channels; Hyaluronan; Lung edema; Lung injury.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • HEK293 Cells
  • Humans
  • Hyaluronic Acid* / pharmacology
  • Lung / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Molecular Weight
  • Receptors, Calcium-Sensing*
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Sodium-Potassium-Exchanging ATPase / pharmacology

Substances

  • Receptors, Calcium-Sensing
  • Hyaluronic Acid
  • Sodium-Potassium-Exchanging ATPase