Protein-tyrosine phosphatase Shp2 positively regulates macrophage oxidative burst

J Biol Chem. 2015 Feb 13;290(7):3894-909. doi: 10.1074/jbc.M114.614057. Epub 2014 Dec 23.

Abstract

Macrophages are vital to innate immunity and express pattern recognition receptors and integrins for the rapid detection of invading pathogens. Stimulation of Dectin-1 and complement receptor 3 (CR3) activates Erk- and Akt-dependent production of reactive oxygen species (ROS). Shp2, a protein-tyrosine phosphatase encoded by Ptpn11, promotes activation of Ras-Erk and PI3K-Akt and is crucial for hematopoietic cell function; however, no studies have examined Shp2 function in particulate-stimulated ROS production. Maximal Dectin-1-stimulated ROS production corresponded kinetically to maximal Shp2 and Erk phosphorylation. Bone marrow-derived macrophages (BMMs) from mice with a conditionally deleted allele of Ptpn11 (Shp2(flox/flox);Mx1Cre+) produced significantly lower ROS levels compared with control BMMs. Although YFP-tagged phosphatase dead Shp2-C463A was strongly recruited to the early phagosome, its expression inhibited Dectin-1- and CR3-stimulated phospho-Erk and ROS levels, placing Shp2 phosphatase function and Erk activation upstream of ROS production. Further, BMMs expressing gain of function Shp2-D61Y or Shp2-E76K and peritoneal exudate macrophages from Shp2D61Y/+;Mx1Cre+ mice produced significantly elevated levels of Dectin-1- and CR3-stimulated ROS, which was reduced by pharmacologic inhibition of Erk. SIRPα (signal regulatory protein α) is a myeloid inhibitory immunoreceptor that requires tyrosine phosphorylation to exert its inhibitory effect. YFP-Shp2C463A-expressing cells have elevated phospho-SIRPα levels and an increased Shp2-SIRPα interaction compared with YFP-WT Shp2-expressing cells. Collectively, these findings indicate that Shp2 phosphatase function positively regulates Dectin-1- and CR3-stimulated ROS production in macrophages by dephosphorylating and thus mitigating the inhibitory function of SIRPα and by promoting Erk activation.

Keywords: Macrophage; NADPH Oxidase; Pattern Recognition Receptor (PRR); Phagocytosis; Tyrosine-Protein Phosphatase (Tyrosine Phosphatase).

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • Fluorescent Antibody Technique
  • Immunoprecipitation
  • Integrases / metabolism
  • Lectins, C-Type / metabolism
  • Macrophages / cytology
  • Macrophages / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Phagocytosis
  • Phosphorylation
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / physiology*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Reactive Oxygen Species / metabolism*
  • Respiratory Burst / physiology*
  • Signal Transduction
  • Tyrosine / metabolism

Substances

  • Lectins, C-Type
  • Reactive Oxygen Species
  • dectin 1
  • Tyrosine
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases
  • Cre recombinase
  • Integrases
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Ptpn11 protein, mouse