Rosmarinic acid inhibits Ca2+-dependent pathways of T-cell antigen receptor-mediated signaling by inhibiting the PLC-gamma 1 and Itk activity

Blood. 2003 May 1;101(9):3534-42. doi: 10.1182/blood-2002-07-1992. Epub 2003 Jan 2.

Abstract

Rosmarinic acid (RosA) is a hydroxylated compound frequently found in herbal plants and is mostly responsible for anti-inflammatory and antioxidative activity. Previously, we observed that RosA inhibited T-cell antigen receptor (TCR)- induced interleukin 2 (IL-2) expression and subsequent T-cell proliferation in vitro. In this study, we investigated in detail inhibitory mechanism of RosA on TCR signaling, which ultimately activates IL-2 promoter by activating transcription factors, such as nuclear factor of activated T cells (NF-AT) and activating protein-1 (AP-1). Interestingly, RosA inhibited NF-AT activation but not AP-1, suggesting that RosA inhibits Ca(2+)-dependent signaling pathways only. Signaling events upstream of NF-AT activation, such as the generation of inositol 1,4,5-triphosphate and Ca(2+) mobilization, and tyrosine phosphorylation of phospholipase C-gamma 1 (PLC-gamma 1) were strongly inhibited by RosA. Tyrosine phosphorylation of PLC-gamma 1 is largely dependent on 3 kinds of protein tyrosine kinases (PTKs), ie, Lck, ZAP-70, and Itk. We found that RosA efficiently inhibited TCR-induced tyrosine phosphorylation and subsequent activation of Itk but did not inhibit Lck or ZAP-70. ZAP-70-dependent signaling pathways such as the tyrosine phosphorylation of LAT and SLP-76 and serine/threonine phosphorylation of mitogen-activated protein kinases (MAPKs) were intact in the presence of RosA, confirming that RosA suppresses TCR signaling in a ZAP-70-independent manner. Therefore, we conclude that RosA inhibits TCR signaling leading to Ca(2+) mobilization and NF-AT activation by blocking membrane-proximal events, specifically, the tyrosine phosphorylation of inducible T cells kinase (Itk) and PLC-gamma 1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing*
  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology*
  • Calcium Signaling / drug effects*
  • Carrier Proteins / metabolism
  • Cinnamates / pharmacology*
  • DNA-Binding Proteins / metabolism
  • Depsides
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology*
  • GRB2 Adaptor Protein
  • Humans
  • Jurkat Cells / drug effects*
  • Jurkat Cells / enzymology
  • Jurkat Cells / immunology
  • Lymphocyte Specific Protein Tyrosine Kinase p56(lck) / physiology
  • Membrane Proteins*
  • Mice
  • Mice, Inbred BALB C
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / metabolism
  • Muromonab-CD3 / pharmacology
  • NFATC Transcription Factors
  • Nuclear Proteins*
  • Phospholipase C gamma
  • Phosphoproteins / metabolism
  • Phosphorylation / drug effects
  • Protein Processing, Post-Translational / drug effects
  • Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Protein-Tyrosine Kinases / physiology
  • Proteins / metabolism
  • Receptors, Antigen, T-Cell / drug effects*
  • Receptors, Antigen, T-Cell / immunology
  • Rosmarinic Acid
  • Transcription Factors / metabolism
  • Type C Phospholipases / antagonists & inhibitors*
  • ZAP-70 Protein-Tyrosine Kinase

Substances

  • Adaptor Proteins, Signal Transducing
  • Anti-Inflammatory Agents, Non-Steroidal
  • Carrier Proteins
  • Cinnamates
  • DNA-Binding Proteins
  • Depsides
  • Enzyme Inhibitors
  • GRB2 Adaptor Protein
  • GRB2 protein, human
  • Grb2 protein, mouse
  • LAT protein, human
  • Lat protein, mouse
  • Membrane Proteins
  • Muromonab-CD3
  • NFATC Transcription Factors
  • Nuclear Proteins
  • Phosphoproteins
  • Proteins
  • Receptors, Antigen, T-Cell
  • SLP-76 signal Transducing adaptor proteins
  • Transcription Factors
  • Protein-Tyrosine Kinases
  • Lymphocyte Specific Protein Tyrosine Kinase p56(lck)
  • ZAP-70 Protein-Tyrosine Kinase
  • ZAP70 protein, human
  • Zap70 protein, mouse
  • emt protein-tyrosine kinase
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • Type C Phospholipases
  • Phospholipase C gamma