Reactive oxygen species-dependent RhoA activation mediates collagen synthesis in hyperoxic lung fibrosis

Free Radic Biol Med. 2011 Jun 1;50(11):1689-98. doi: 10.1016/j.freeradbiomed.2011.03.020. Epub 2011 Mar 23.

Abstract

Lung fibrosis is an ultimate consequence of pulmonary oxygen toxicity in human and animal models. Excessive production and deposition of extracellular matrix proteins, e.g., collagen-I, is the most important feature of pulmonary fibrosis in hyperoxia-induced lung injury. In this study, we investigated the roles of RhoA and reactive oxygen species (ROS) in collagen-I synthesis in hyperoxic lung fibroblasts and in a mouse model of oxygen toxicity. Exposure of human lung fibroblasts to hyperoxia resulted in RhoA activation and an increase in collagen-I synthesis and cell proliferation. Inhibition of RhoA by C3 transferase CT-04, dominant-negative RhoA mutant T19N, or RhoA siRNA prevented hyperoxia-induced collagen-I synthesis. The constitutively active RhoA mutant Q63L mimicked the effect of hyperoxia on collagen-I expression. Moreover, the Rho kinase inhibitor Y27632 inhibited collagen-I synthesis in hyperoxic lung fibroblasts and fibrosis in mouse lungs after oxygen toxicity. Furthermore, the ROS scavenger tiron attenuated hyperoxia-induced increases in RhoA activation and collagen-I synthesis in lung fibroblasts and mouse lungs after oxygen toxicity. More importantly, we found that hyperoxia induced separation of guanine nucleotide dissociation inhibitor (GDI) from RhoA in lung fibroblasts and mouse lungs. Further, tiron prevented the separation of GDI from RhoA in hyperoxic lung fibroblasts and mouse lungs with oxygen toxicity. Together, these results indicate that ROS-induced separation of GDI from RhoA leads to RhoA activation with oxygen toxicity. ROS-dependent RhoA activation is responsible for the increase in collagen-I synthesis in hyperoxic lung fibroblasts and mouse lungs.

Publication types

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

MeSH terms

  • 1,2-Dihydroxybenzene-3,5-Disulfonic Acid Disodium Salt / pharmacology
  • Animals
  • Cell Proliferation / drug effects
  • Collagen Type I / biosynthesis*
  • Collagen Type I / genetics
  • Disease Models, Animal
  • Enzyme Activation / drug effects
  • Enzyme Activation / genetics
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Free Radical Scavengers / pharmacology
  • Humans
  • Hyperoxia / drug therapy
  • Hyperoxia / genetics
  • Hyperoxia / metabolism*
  • Hyperoxia / pathology
  • Hyperoxia / physiopathology
  • Lung / drug effects
  • Lung / metabolism*
  • Lung / pathology
  • Mice
  • Mutation / genetics
  • Pulmonary Fibrosis
  • RNA, Small Interfering / genetics
  • Reactive Oxygen Species / metabolism
  • Transgenes / genetics
  • rhoA GTP-Binding Protein / genetics
  • rhoA GTP-Binding Protein / metabolism*

Substances

  • Collagen Type I
  • Free Radical Scavengers
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • 1,2-Dihydroxybenzene-3,5-Disulfonic Acid Disodium Salt
  • rhoA GTP-Binding Protein