The antiangiogenic insulin receptor substrate-1 antisense oligonucleotide aganirsen impairs AU-rich mRNA stability by reducing 14-3-3β-tristetraprolin protein complex, reducing inflammation and psoriatic lesion size in patients

J Pharmacol Exp Ther. 2014 Apr;349(1):107-17. doi: 10.1124/jpet.113.209346. Epub 2014 Feb 6.

Abstract

Increased inflammation and aberrant angiogenesis underlie psoriasis. Here, we report that the inhibition of insulin receptor substrate-1 (IRS-1) expression with aganirsen resulted in a dose-dependent reduction (P < 0.0001) in IRS-1 protein in the cytoplasm, while IRS-1 protein remained quantitatively unchanged in the perinuclear environment. Aganirsen induced a dose-dependent increase in serine-phosphorylated IRS-1 in the soluble perinuclear-nuclear fraction, inducing IRS-1-14-3-3β protein association (P < 0.001), thereby impairing 14-3-3β-tristetraprolin protein complex and AU-rich mRNA's stability (P < 0.001). Accordingly, aganirsen inhibited (P < 0.001) in vitro the expression of interleukin-8 (IL-8), IL-12, IL-22, and tumor necrosis factor alpha (TNFα), four inflammatory mediators containing mRNA with AU-rich regions. To demonstrate the clinical relevance of this pathway, we tested the efficacy of aganirsen by topical application in a pilot, double-blind, randomized, dose-ranging study in 12 psoriatic human patients. After 6 weeks of treatment, least square mean differences with placebo were -38.9% (95% confidence interval, -75.8 to -2.0%) and -37.4% (-74.3 to -0.5%) at the doses of 0.86 and 1.72 mg/g, respectively. Lesion size reduction was associated with reduced expression of IRS-1 (P < 0.01), TNFα (P < 0.0001), and vascular endothelial growth factor (P < 0.01); reduced keratinocyte proliferation (P < 0.01); and the restoration (P < 0.02) of normal levels of infiltrating CD4(+) and CD3(+) lymphocytes in psoriatic skin lesions. These results suggest that aganirsen is a first-in-class of a new generation of antiangiogenic medicines combining anti-inflammatory activities. Aganirsen-induced downregulation of inflammatory mediators characterized by AU-rich mRNA likely underlies its beneficial clinical outcome in psoriasis. These results justify further large-scale clinical studies to establish the dose of aganirsen and its long-term efficacy in psoriasis.

Publication types

  • Randomized Controlled Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • AU Rich Elements
  • Administration, Topical
  • Angiogenesis Inhibitors / administration & dosage
  • Angiogenesis Inhibitors / adverse effects
  • Angiogenesis Inhibitors / therapeutic use*
  • Cytokines / antagonists & inhibitors
  • Cytokines / immunology
  • Dose-Response Relationship, Drug
  • Double-Blind Method
  • Female
  • Humans
  • Insulin Receptor Substrate Proteins / antagonists & inhibitors*
  • Male
  • Microvessels / drug effects
  • Microvessels / metabolism
  • Middle Aged
  • Oligonucleotides / administration & dosage
  • Oligonucleotides / adverse effects
  • Oligonucleotides / therapeutic use*
  • Pilot Projects
  • Psoriasis / drug therapy*
  • Psoriasis / immunology
  • Psoriasis / metabolism
  • Psoriasis / pathology
  • RNA Stability / drug effects*
  • RNA, Messenger / genetics
  • RNA, Messenger / physiology*
  • Skin / blood supply
  • Skin / drug effects
  • Skin / immunology
  • Skin / pathology
  • Treatment Outcome
  • Tristetraprolin / metabolism*

Substances

  • Angiogenesis Inhibitors
  • Cytokines
  • GS 101
  • IRS1 protein, human
  • Insulin Receptor Substrate Proteins
  • Oligonucleotides
  • RNA, Messenger
  • Tristetraprolin
  • ZFP36 protein, human