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Science 16 August 2002:
Vol. 297. no. 5584, pp. 1186 - 1190
DOI: 10.1126/science.1073634
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Reports

S-Nitrosylation of Matrix Metalloproteinases: Signaling Pathway to Neuronal Cell Death

Zezong Gu,1 Marcus Kaul,1 Boxu Yan,2* Steven J. Kridel,2* Jiankun Cui,1 Alex Strongin,2 Jeffrey W. Smith,2 Robert C. Liddington,2 Stuart A. Lipton1dagger

Matrix metalloproteinases (MMPs) are implicated in the pathogenesis of neurodegenerative diseases and stroke. However, the mechanism of MMP activation remains unclear. We report that MMP activation involves S-nitrosylation. During cerebral ischemia in vivo, MMP-9 colocalized with neuronal nitric oxide synthase. S-Nitrosylation activated MMP-9 in vitro and induced neuronal apoptosis. Mass spectrometry identified the active derivative of MMP-9, both in vitro and in vivo, as a stable sulfinic or sulfonic acid, whose formation was triggered by S-nitrosylation. These findings suggest a potential extracellular proteolysis pathway to neuronal cell death in which S-nitrosylation activates MMPs, and further oxidation results in a stable posttranslational modification with pathological activity.

1 Center for Neuroscience and Aging,
2 Program in Cell Adhesion and Extracellular Matrix Biology, The Burnham Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037, USA.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: slipton{at}burnham.org

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Nitric Oxide and Mechanisms of Redox Signaling.
J. Pfeilschifter, W. Eberhardt, and A. Huwiler (2003)
J. Am. Soc. Nephrol. 14, S237-240
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Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry.
R. Visse and H. Nagase (2003)
Circ. Res. 92, 827-839
   Abstract »    Full Text »    PDF »
Modulation of baroreceptor activity by gene transfer of nitric oxide synthase to carotid sinus adventitia.
S. S. Meyrelles, R. V. Sharma, H. Z. Mao, F. M. Abboud, and M. W. Chapleau (2003)
Am J Physiol Regulatory Integrative Comp Physiol 284, R1190-R1198
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Abnormal Expression of Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases in Brain Arteriovenous Malformations * Growth and Bleeding in BAVM: Another Role for MMPs.
T. Hashimoto, G. Wen, M. T. Lawton, N. J. Boudreau, A. W. Bollen, G.-Y. Yang, N. M. Barbaro, R. T. Higashida, C. F. Dowd, V. V. Halbach, et al. (2003)
Stroke 34, 925-931
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Proteomic Analysis of S-Nitrosylated Proteins in Mesangial Cells.
T. Kuncewicz, E. A. Sheta, I. L. Goldknopf, and B. C. Kone (2003)
Mol. Cell. Proteomics 2, 156-163
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Plasma Metalloproteinase-9 Concentration Predicts Hemorrhagic Transformation in Acute Ischemic Stroke * Editorial Comment.
M. Castellanos, R. Leira, J. Serena, J. M. Pumar, I. Lizasoain, J. Castillo, A. Davalos, and G. F. Hamann (2003)
Stroke 34, 40-46
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