S-nitrosylation of endogenous protein tyrosine phosphatases in endothelial insulin signaling

Free Radic Biol Med. 2016 Oct:99:199-213. doi: 10.1016/j.freeradbiomed.2016.08.012. Epub 2016 Aug 10.

Abstract

Nitric oxide (NO) exerts its biological function through S-nitrosylation of cellular proteins. Due to the labile nature of this modification under physiological condition, identification of S-nitrosylated residue in enzymes involved in signaling regulation remains technically challenging. The present study investigated whether intrinsic NO produced in endothelium-derived MS-1 cells response to insulin stimulation might target endogenous protein tyrosine phosphatases (PTPs). For this, we have developed an approach using a synthetic reagent that introduces a phenylacetamidyl moiety on S-nitrosylated Cys, followed by detection with anti-phenylacetamidyl Cys (PAC) antibody. Coupling with sequential blocking of free thiols with multiple iodoacetyl-based Cys-reactive chemicals, we employed this PAC-switch method to show that endogenous SHP-2 and PTP1B were S-nitrosylated in MS-1 cells exposed to insulin. The mass spectrometry detected a phenylacetamidyl moiety specifically present on the active-site Cys463 of SHP-2. Focusing on the regulatory role of PTP1B, we showed S-nitrosylation to be the principal Cys reversible redox modification in endothelial insulin signaling. The PAC-switch method in an imaging format illustrated that a pool of S-nitrosylated PTP1B was colocalized with activated insulin receptor to the cell periphery, and that such event was endothelial NO synthase (eNOS)-dependent. Moreover, ectopic expression of the C215S mutant of PTP1B that mimics the active-site Cys215 S-nitrosylated form restored insulin responsiveness in eNOS-ablated cells, which was otherwise insensitive to insulin stimulation. This work not only introduces a new method that explores the role of physiological NO in regulating signal transduction, but also highlights a positive NO effect on promoting insulin responsiveness through S-nitrosylation of PTP1B's active-site Cys215.

Keywords: Endothelial cell; Insulin signaling; New method; Nitric oxide; PTP1B; S-nitrosylation; SHP-2.

MeSH terms

  • Acetanilides / chemistry
  • Animals
  • Antibodies / chemistry
  • COS Cells
  • Catalytic Domain
  • Cell Line
  • Chlorocebus aethiops
  • Cysteine / metabolism*
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Gene Expression
  • Indicators and Reagents / chemistry
  • Insulin / pharmacology*
  • Mice
  • Nitric Oxide Synthase Type III / deficiency
  • Nitric Oxide Synthase Type III / genetics
  • Nitroso Compounds / metabolism*
  • Protein Processing, Post-Translational*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1 / metabolism*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / metabolism*
  • Receptor, Insulin / genetics
  • Receptor, Insulin / metabolism
  • Signal Transduction
  • Staining and Labeling / methods

Substances

  • Acetanilides
  • Antibodies
  • Indicators and Reagents
  • Insulin
  • Nitroso Compounds
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Receptor, Insulin
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Ptpn1 protein, mouse
  • Cysteine