Inhibition of activator protein 1 by barbiturates is mediated by differential effects on mitogen-activated protein kinases and the small G proteins ras and rac-1

J Pharmacol Exp Ther. 2004 Dec;311(3):1232-40. doi: 10.1124/jpet.104.071332. Epub 2004 Jul 19.

Abstract

Barbiturates are known to suppress protective immunity, and their therapeutic use is associated with nosocomial infections. Although barbiturates inhibit T cell proliferation, differentiation, and cytokine synthesis, only thiobarbiturates markedly reduce the activation of immune regulatory transcription factors such as nuclear factor-kappaB and nuclear factor of activated T cells. In this study, we investigated barbiturate-mediated effects on the regulation of the transcription factor activator protein 1 (AP-1) in primary T lymphocytes. We show that both thiobarbiturates and their oxy-analogs inhibit AP-1-dependent gene expression and AP-1 complex formation at clinically relevant doses. Furthermore, mitogen-activated protein (MAP) kinase activity, which transcriptionally and posttranslationally regulates AP-1 complex formation, is suppressed by most barbiturates. CD3/CD28- or phorbol 12-myristate 13-acetate (PMA)/ionomycin-induced p38 and extracellular signal-regulated kinase 1/2 phosphorylation or c-jun NH2-terminal kinase (JNK) 1/2 kinase activity was significantly diminished by pentobarbital, thiamylal, secobarbital, or methohexital treatment. These barbiturates also inhibited the initiators of the MAP kinase cascade, the small G proteins ras and rac-1, and prevented binding to their partners raf-1 and PAK, respectively. Thiopental, unlike the other barbiturates, only reduced ras and JNK activity upon direct CD3/CD28 receptor engagement. Contrarily, upon PMA/ionomycin stimulation, thiopental blocked AP-1-dependent gene expression independently of the small G protein ras and MAP kinases, thus suggesting an additional, unknown mechanism of AP-1 regulation. In conclusion, our results contribute to the explanation of a clinically manifested immune suppression in barbiturate-treated patients and support the idea of a MAP kinase-independent regulation of AP-1 by PKC and calcium in human T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Barbiturates / pharmacology*
  • CD3 Complex / metabolism
  • Electrophoretic Mobility Shift Assay
  • Genes, Reporter
  • Humans
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Luciferases / biosynthesis
  • Luciferases / genetics
  • MAP Kinase Kinase 4
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Mitogen-Activated Protein Kinase Kinases / metabolism
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors*
  • Neuropeptides / drug effects*
  • Nuclear Proteins / metabolism
  • Proto-Oncogene Proteins c-jun / biosynthesis
  • Proto-Oncogene Proteins c-jun / genetics
  • Proto-Oncogene Proteins p21(ras) / genetics
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / metabolism
  • Transcription Factor AP-1 / antagonists & inhibitors*
  • p38 Mitogen-Activated Protein Kinases / metabolism
  • rac GTP-Binding Proteins / drug effects*
  • rac1 GTP-Binding Protein
  • ras Proteins / drug effects*

Substances

  • Barbiturates
  • CD3 Complex
  • Neuropeptides
  • Nuclear Proteins
  • Proto-Oncogene Proteins c-jun
  • RAC1 protein, human
  • Transcription Factor AP-1
  • Luciferases
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4
  • Mitogen-Activated Protein Kinase Kinases
  • HRAS protein, human
  • Proto-Oncogene Proteins p21(ras)
  • rac GTP-Binding Proteins
  • rac1 GTP-Binding Protein
  • ras Proteins