Relaxin protects rat lungs from ischemia-reperfusion injury via inducible NO synthase: role of ERK-1/2, PI3K, and forkhead transcription factor FKHRL1

PLoS One. 2013 Sep 30;8(9):e75592. doi: 10.1371/journal.pone.0075592. eCollection 2013.

Abstract

Introduction: Early allograft dysfunction following lung transplantation is mainly an ischemia/reperfusion (IR) injury. We showed that relaxin-2 (relaxin) exerts a protective effect in lung IR, attributable to decreases in endothelin-1 (ET-1) production, leukocyte recruitment, and free radical generation. Here, we summarize our investigations into relaxin's signalling.

Materials and methods: Isolated rat lungs were perfused with vehicle or 5 nM relaxin (n = 6-10 each). Thereafter, experiments were conducted in the presence of relaxin plus vehicle, the protein kinase A inhibitors H-89 and KT-5720, the NO synthase (NOS) inhibitor L-NAME, the iNOS inhibitor 1400W, the nNOS inhibitor SMTC, the extracellular signal-regulated kinase-1/2 (ERK-1/2) inhibitor PD-98059, the phosphatidylinositol-3 kinase (PI3K) inhibitor wortmannin, the endothelin type-B (ETB) antagonist A-192621, or the glucocorticoid receptor (GR) antagonist RU-486. After 90 min ischemia and 90 min reperfusion we determined wet-to-dry (W/D) weight ratio, mean pulmonary arterial pressure (MPAP), vascular release of ET-1, neutrophil elastase (NE), myeloperoxidase (MPO), and malondialdehyde (MDA). Primary rat pulmonary vascular cells were similarly treated.

Results: IR lungs displayed significantly elevated W/D ratios, MPAP, as well as ET-1, NE, MDA, and MPO. In the presence of relaxin, all of these parameters were markedly improved. This protective effect was completely abolished by L-NAME, 1400W, PD-98059, and wortmannin whereas neither PKA and nNOS inhibition nor ETB and GR antagonism were effective. Analysis of NOS gene expression and activity revealed that the relaxin-induced early and moderate iNOS stimulation is ERK-1/2-dependent and counter-balanced by PI3K. Relaxin-PI3K-related phosphorylation of a forkhead transcription factor, FKHRL1, paralleled this regulation. In pulmonary endothelial and smooth muscle cells, FKHRL1 was essential to relaxin-PI3K signalling towards iNOS.

Conclusion: In this short-time experimental setting, relaxin protects against IR-induced lung injury via early and moderate iNOS induction, dependent on balanced ERK-1/2 and PI3K-FKHRL1 stimulation. These findings render relaxin a candidate drug for lung preservation.

Publication types

  • Evaluation Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Pressure / drug effects
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Regulation / drug effects*
  • Leukocyte Elastase / metabolism
  • Lung / drug effects*
  • Lung / pathology
  • MAP Kinase Signaling System / physiology
  • Malondialdehyde / metabolism
  • Nitric Oxide Synthase / metabolism*
  • Peroxidase / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Pulmonary Artery / drug effects
  • Rats
  • Relaxin / metabolism
  • Relaxin / pharmacology*
  • Reperfusion Injury / prevention & control*
  • Vascular Resistance / drug effects

Substances

  • FOXO3 protein, rat
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors
  • Malondialdehyde
  • Relaxin
  • Peroxidase
  • Nitric Oxide Synthase
  • Leukocyte Elastase

Grants and funding

The work was funded by institutional grants to KA and MW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.