Phospholipase activity of phospholipase C-gamma1 is required for nerve growth factor-regulated MAP kinase signaling cascade in PC12 cells

J Biol Chem. 2003 Dec 26;278(52):52497-503. doi: 10.1074/jbc.M306744200. Epub 2003 Oct 21.

Abstract

Phospholipase C-gamma1 (PLC-gamma1) hydrolyzes phosphatidylinositol 4,5-bisphosphate to the second messengers inositol 1,4,5-trisphosphate and diacylglycerol (DAG). PLC-gamma1 is implicated in a variety of cellular signalings and processes including mitogenesis and calcium entry. However, numerous studies demonstrate that the lipase activity is not required for PLC-gamma1 to mediate these events. Here, we report that the phospholipase activity of PLC-gamma1 plays an essential role in nerve growth factor (NGF)-triggered Raf/MEK/MAPK pathway activation in PC12 cells. Employing PC12 cells stably transfected with an inducible form of wild-type PLC-gamma1 or lipase inactive PLC-gamma1 with histidine 335 mutated into glutamine in the catalytic domain, we show that NGF provokes robust activation of MAP kinase in wild-type but not in lipase inactive cells. Both Ras/C-Raf/MEK1 and Rap1/B-Raf/MEK1 pathways are intact in the wild-type cells. By contrast, these signaling cascades are diminished in the mutant cells. Pretreatment with cell permeable DAG analog 1-oleyl-2-acetylglycerol rescues the MAP kinase pathway activation in the mutant cells. These observations indicate that the lipase activity of PLC-gamma1 mediates NGF-regulated MAPK signaling upstream of Ras/Rap1 activation probably through second messenger DAG-activated Ras and Rap-GEFs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Catalytic Domain
  • Enzyme Activation
  • Genetic Vectors
  • Histidine / chemistry
  • MAP Kinase Signaling System*
  • Mitogen-Activated Protein Kinases / metabolism
  • Mutation
  • Nerve Growth Factor / metabolism*
  • PC12 Cells
  • Phospholipase C gamma
  • Plasmids / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins c-raf / metabolism
  • Rats
  • Recombinant Fusion Proteins / metabolism
  • Signal Transduction
  • Time Factors
  • Transfection
  • Type C Phospholipases / metabolism*
  • rap1 GTP-Binding Proteins / metabolism

Substances

  • Recombinant Fusion Proteins
  • Histidine
  • Nerve Growth Factor
  • Proto-Oncogene Proteins c-raf
  • Mitogen-Activated Protein Kinases
  • Type C Phospholipases
  • Phospholipase C gamma
  • rap1 GTP-Binding Proteins