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Hydrogen Peroxide Induces Murine Macrophage Chemokine Gene Transcription Via Extracellular Signal-Regulated Kinase- and Cyclic Adenosine 5'-Monophosphate (cAMP)-Dependent Pathways: Involvement of NF-B, Activator Protein 1, and cAMP Response Element Binding Protein¹

Centre de Recherche en Infectiologie, Centre Hospitalier Universitaire de Québec, Pavillon du Centre Hospitalier de l’Université Laval, and Département de Biologie Médicale, Faculté de Médecine, Université Laval, Ste-Foy, Québec, Canada

Hydrogen peroxide (H₂O₂) has been shown to act as a second messenger that activates chemokine expression. In the present study, we investigated the mechanisms underlying this cellular regulation in the murine macrophage cell line B10R. We report that H₂O₂ increases mRNA expression of various chemokines, macrophage-inflammatory protein (MIP)-1/CC chemokine ligand (CCL)3, MIP-1/CCL4, MIP-2/CXC chemokine ligand 2, and monocyte chemoattractant protein-1/CCL2, by activating the extracellular signal-regulated kinase (ERK) pathway and the nuclear translocation of the transcription factors NF-B, AP-1, and CREB. Blockage of the ERK pathway with specific inhibitors against mitogen-activated protein kinase kinase 1/2 and ERK1/ERK2 completely abolished both the H₂O₂-mediated chemokine up-regulation and the activation of all NF studied. Similarly, selective inhibition of cAMP and NF-B strongly down-regulated the induction of all chemokine transcripts as well as CREB and NF-B activation, respectively. Of interest, we detected a significant decrease of NF-B, AP-1, and CREB DNA binding activities by reciprocal competition for these binding sites when either specific cold oligonucleotides (NF-B, AP-1, and CREB) or Abs against various transcription factor subunits (p50, p65, c-Fos, Jun B, c-Jun, and CREB-1) were added. These findings indicate that cooperation between ERK- and cAMP-dependent pathways seems to be required to achieve the formation of an essential transcriptional factor complex for maximal H₂O₂-dependent chemokine modulation. Finally, experiments performed with actinomycin D suggest that H₂O₂-mediated MIP-1 mRNA up-regulation results from transcriptional control, whereas that of MIP-1, MIP-2, and monocyte chemoattractant protein-1 is due to both gene transcription activation and mRNA posttranscriptional stabilization.

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