Recruitment and activation of Raf-1 kinase by nitric oxide-activated Ras

Biochemistry. 2000 Aug 15;39(32):9901-8. doi: 10.1021/bi992954b.

Abstract

Nitric oxide (NO) and related species serve as cellular messengers in various physiological and pathological processes. The monomeric G protein, Ras, transduces multiple signaling pathways with varying biological responses. We have previously reported that NO triggers Ras activation and recruitment of an effector, phosphatidylinositol 3'-kinase (PI3K) and Ras-dependent activation of mitogen-activated protein (MAP) kinases which include extracellular signal regulated kinases (ERKs), c-Jun NH(2)-terminal kinase (JNK), and p38 MAP kinase. In this study, we further defined NO-activated Ras signaling pathways. We have identified Raf-1 as another effector recruited by NO-activated Ras in T lymphocytes. NO activation results in association of Ras and Raf-1 and is biologically significant, as we observe an NO-induced increase in Raf-1 kinase activity. Downstream to Raf-1 kinase lie MAP kinases and their subsequent downstream targets, transcription factors. We found that treatment of T lymphocytes with NO yielded phosphorylation of the transcription factor, Elk-1. This phoshorylation is dependent on NO binding to the cysteine 118 residue of Ras. By further delineating the pathway with pharmacological inhibitors, Elk-1 phosphorylation was also found to be dependent on PI3K and ERK. Moreover, NO triggered an increase in mRNA levels of the proinflammatory cytokine, tumor necrosis factor-alpha (TNF-alpha), which was ERK dependent. Thus, we have defined an NO-induced signaling pathway in T lymphocytes arising at the membrane where NO-activated Ras recruits Raf-1 and culminating in the nucleus where Elk-1 is phosphorylated and TNF-alpha messenger RNA is induced. This NO-activated Ras-mediated signaling pathway may play a critical role in Elk-1-induced transcriptional activation of T lymphocytes, host defense and inflammation.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Androstadienes / pharmacology
  • Cell Membrane / metabolism
  • Cell Nucleus / metabolism
  • Chromones / pharmacology
  • DNA-Binding Proteins*
  • Enzyme Activation
  • Humans
  • Jurkat Cells
  • Morpholines / pharmacology
  • Nitric Oxide / metabolism*
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation
  • Precipitin Tests
  • Protein Binding
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-raf / metabolism*
  • Signal Transduction
  • T-Lymphocytes / metabolism*
  • Transcription Factors*
  • Tumor Necrosis Factor-alpha / metabolism
  • Wortmannin
  • ets-Domain Protein Elk-1
  • ras Proteins / metabolism*

Substances

  • Androstadienes
  • Chromones
  • DNA-Binding Proteins
  • ELK1 protein, human
  • Morpholines
  • Phosphoinositide-3 Kinase Inhibitors
  • Proto-Oncogene Proteins
  • Transcription Factors
  • Tumor Necrosis Factor-alpha
  • ets-Domain Protein Elk-1
  • Nitric Oxide
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Proto-Oncogene Proteins c-raf
  • ras Proteins
  • Wortmannin