Activation of the Mitogen Activated Protein Kinase Extracellular Signal-Regulated Kinase 1 and 2 by the Nitric Oxide-cGMP-cGMP-Dependent Protein Kinase Axis Regulates the Expression of Matrix Metalloproteinase 13 in Vascular Endothelial Cells

doi:10.1124/mol.62.4.927

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Vol. 62, Issue 4, 927-935, October 2002

Activation of the Mitogen Activated Protein Kinase Extracellular Signal-Regulated Kinase 1 and 2 by the Nitric Oxide-cGMP-cGMP-Dependent Protein Kinase Axis Regulates the Expression of Matrix Metalloproteinase 13 in Vascular Endothelial Cells

Carlos Zaragoza, Estrella Soria, Esther López, Darren Browning, Milagros Balbín, Carlos López-Otín, and Santiago Lamas

Centro de Investigaciones Biológicas, Instituto "Reina Sofía" de Investigaciones Nefrológicas, Consejo Superior de Investigaciones Científicas, and Fundación Centro Nacional de Investigaciones Cardiovasculares Carlos III, Madrid, Spain (C.Z., E.S., E.L., S.L.); Departamento de Bioquímica y Biología Molecular, Facultad de Medicina, Instituto Universitario de Oncología, Universidad de Oviedo, Oviedo, Spain (M.B., C.L.-O.); and Department of Biochemistry and Molecular Biology, Medical College of Georgia, Augusta, Georgia (D.B.)

Matrix metalloproteinases (MMPs) are synthesized in response to diverse stimuli, including cytokines, growth factors, hormones,and oxidative stress. Here we show that the nitric oxide (NO)donor 2-(N,N-diethylamino)-diazenolate-2-oxide (DEA-NO) and NOfrom murine macrophages transcriptionally regulate MMP-13 expressionin vascular endothelial cells (BAEC). The cGMP analog, 8-bromo-cGMP(8-Br-cGMP) mimicked the effect of NO, whereas incubation withthe guanylate cyclase inhibitor 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one,or the cGMP-dependent protein kinase (PKG) inhibitor phenyl-1,N²- etheno-8-bromoguanosine-3',5'-cyclic monophosphorothioate, Rp-isomer(PET) reduced the stimulatory effect of DEA-NO on the activationof the MMP-13 promoter. Overexpression of the catalytic subunitof PKG1- $alpha$ resulted in a 5- to 6-fold increase of the MMP-13 regulatoryregion over control cells. On the other hand, incubation withthe mitogen-activated protein/extracellular signal-regulated kinaseinhibitor 2'-amino-3'-methoxyflavone (PD98059) significantly reducedDEA-NO and 8-Br-cGMP promoter activation and mRNA expression ofMMP-13 in transfected BAEC. Moreover, a complex between PKG1- $alpha$ and the G-protein Raf-1, an upstream activator of the extracellularsignal-regulated kinase signaling pathway, was detected in cellsoverexpressing PKG1- $alpha$ or treated either with DEA-NO or 8-Br-cGMP.Thus, we propose that the NO-cGMP-PKG pathway enhances MMP-13expression by the activation of ERK 1,2. This effect of NO maybe the result of pathophysiological importance in the contextof inflammation oratherogenesis.

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