Superoxide-induced Type I collagen secretion depends on prolyl 4-hydroxylases

Biochem Biophys Res Commun. 2020 Sep 3;529(4):1011-1017. doi: 10.1016/j.bbrc.2020.07.002. Epub 2020 Jul 30.

Abstract

Reactive oxygen species (ROS) including superoxide (O2•-) play an important role in a variety of diseases, including Alzheimer's Disease, cancer, and atherosclerosis. Early reports showed that O2•- is a stimulant for collagen synthesis. However, the mechanism remains incompletely understood. Here we showed that LY83583 (6-anilinoquinoline-5,8-quinone), a substance known to induce O2•- production by smooth muscle cell (SMC), increases Type I collagen secretion. This effect could be blocked by treating the cells with Tiron, a scavenger for O2•-. LY83583-induced Type I collagen secretion required P4HA1 and P4HA2. Knockout of either P4ha1 or P4ha2 greatly reduced LY83583-stimulated Type I collagen maturation whereas silencing of both P4ha1 and P4ha2 completely blocked LY83583-induced Type I collagen maturation. Although significantly more hydroxyproline on purified Type I collagen was detected from LY83583 treated mouse embryonic fibroblast (MEF) cells by mass spectrometry, the level of prolyl 4-hydroxylases was not altered. Thus, LY83583 might increase the enzymatic activity of prolyl 4-hydroxylases to increase Type I collagen maturation. In addition, we found that LY83583 activated prolyl 4-hydrolases differed from ascorbate-activated prolyl 4-hydroxylase in two aspects: (1) LY83583 activated both P4HA1 and P4HA2 involved in collagen maturation whereas ascorbate mainly stimulated P4HA1 in collagen maturation; (2) LY83583 did not induce N259 glycosylation on P4HA1 as ascorbate did. The mechanisms remain to be investigated.

Keywords: Prolyl 4-hydroxylases; Reactive oxygen species (ROS); Superoxide; Type I collagen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminoquinolines / pharmacology
  • Animals
  • Aorta / cytology
  • Collagen Type I / genetics
  • Collagen Type I / metabolism*
  • Embryo, Mammalian / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Glycosylation
  • Hydroxylation
  • Mice
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • Peptides / metabolism
  • Proline / metabolism
  • Prolyl Hydroxylases / metabolism*
  • Superoxides / metabolism*
  • Transcription, Genetic / drug effects

Substances

  • Aminoquinolines
  • Collagen Type I
  • Peptides
  • Superoxides
  • 6-anilino-5,8-quinolinedione
  • Proline
  • Prolyl Hydroxylases