Frontline Science: TNF-α and GM-CSF1 priming augments the role of SOS1/2 in driving activation of Ras, PI3K-γ, and neutrophil proinflammatory responses

J Leukoc Biol. 2019 Oct;106(4):815-822. doi: 10.1002/JLB.2HI0918-359RR. Epub 2019 Feb 5.

Abstract

Circulating neutrophils are, by necessity, quiescent and relatively unresponsive to acute stimuli. In regions of inflammation, mediators can prime neutrophils to react to acute stimuli with stronger proinflammatory, pathogen-killing responses. In neutrophils G protein-coupled receptor (GPCR)-driven proinflammatory responses, such as reactive oxygen species (ROS) formation and accumulation of the key intracellular messenger phosphatidylinositol (3,4,5)-trisphosphate (PIP3 ), are highly dependent on PI3K-γ, a Ras-GTP, and Gβγ coincidence detector. In unprimed cells, the major GPCR-triggered activator of Ras is the Ras guanine nucleotide exchange factor (GEF), Ras guanine nucleotide releasing protein 4 (RasGRP4). Although priming is known to increase GPCR-PIP3 signaling, the mechanisms underlying this augmentation remain unclear. We used genetically modified mice to address the role of the 2 RasGEFs, RasGRP4 and son of sevenless (SOS)1/2, in neutrophil priming. We found that following GM-CSF/TNFα priming, RasGRP4 had only a minor role in the enhanced responses. In contrast, SOS1/2 acquired a substantial role in ROS formation, PIP3 accumulation, and ERK activation in primed cells. These results suggest that SOS1/2 signaling plays a key role in determining the responsiveness of neutrophils in regions of inflammation.

Keywords: PI3K; RasGEF; SOS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Enzyme Activation / drug effects
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Inflammation / pathology*
  • Mice
  • N-Formylmethionine Leucyl-Phenylalanine / pharmacology
  • Neutrophils / drug effects
  • Neutrophils / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Phosphatidylinositol Phosphates / metabolism
  • Phospholipase C beta / metabolism
  • Reactive Oxygen Species / metabolism
  • SOS1 Protein / metabolism*
  • Signal Transduction / drug effects
  • Son of Sevenless Proteins / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism*
  • ras Guanine Nucleotide Exchange Factors / metabolism
  • ras Proteins / metabolism*

Substances

  • Phosphatidylinositol Phosphates
  • Rasgrp4 protein, mouse
  • Reactive Oxygen Species
  • SOS1 Protein
  • Son of Sevenless Proteins
  • Sos2 protein, mouse
  • Tumor Necrosis Factor-alpha
  • phosphatidylinositol 3-phosphate
  • ras Guanine Nucleotide Exchange Factors
  • N-Formylmethionine Leucyl-Phenylalanine
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Extracellular Signal-Regulated MAP Kinases
  • Phospholipase C beta
  • ras Proteins