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S-Nitrosylation of Matrix Metalloproteinases: Signaling Pathway to Neuronal Cell Death
Zezong Gu,1Marcus Kaul,1Boxu Yan,2*Steven J. Kridel,2*Jiankun Cui,1Alex Strongin,2Jeffrey W. Smith,2Robert C. Liddington,2Stuart A. Lipton1
Matrix metalloproteinases (MMPs) are implicated in the
pathogenesis of neurodegenerative diseases and stroke. However, themechanism of MMP activation remains unclear. We report that MMPactivation involves S-nitrosylation. During cerebral ischemiain vivo,
MMP-9 colocalized with neuronal nitric oxide synthase.S-Nitrosylation
activated MMP-9 in vitro and induced neuronalapoptosis. Mass
spectrometry identified the active derivativeof MMP-9, both in vitro
and in vivo, as a stable sulfinic or sulfonicacid, whose formation was
triggered by S-nitrosylation. Thesefindings suggest a potential
extracellular proteolysis pathwayto neuronal cell death in which
S-nitrosylation activates MMPs,and further oxidation results in a
stable posttranslational modificationwith 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.
To whom correspondence should be addressed. E-mail:
slipton{at}burnham.org
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|Abstract »|Full Text »|PDF »
A tautomeric zinc sensor for ratiometric fluorescence imaging: Application to nitric oxide-induced release of intracellular zinc.
C. J. Chang, J. Jaworski, E. M. Nolan, M. Sheng, and S. J. Lippard (2004)
PNAS
101, 1129-1134
|Abstract »|Full Text »|PDF »
Role of Matrix Metalloproteinases in Delayed Neuronal Damage after Transient Global Cerebral Ischemia.
S.-R. Lee, K. Tsuji, S.-R. Lee, and E. H. Lo (2004)
J. Neurosci.
24, 671-678
|Abstract »|Full Text »|PDF »
Matrix Metalloproteinase-9 Facilitates Remyelination in Part by Processing the Inhibitory NG2 Proteoglycan.
P. H. Larsen, J. E. Wells, W. B. Stallcup, G. Opdenakker, and V. W. Yong (2003)
J. Neurosci.
23, 11127-11135
|Abstract »|Full Text »|PDF »
Analyses of all matrix metalloproteinase members in leukocytes emphasize monocytes as major inflammatory mediators in multiple sclerosis.
A. Bar-Or, R. K. Nuttall, M. Duddy, A. Alter, H. J. Kim, I. Ifergan, C. J. Pennington, P. Bourgoin, D. R. Edwards, and V. W. Yong (2003)
Brain
126, 2738-2749
|Abstract »|Full Text »|PDF »
IL-8/CXCL8 and Growth-Related Oncogene {alpha}/CXCL1 Induce Chondrocyte Hypertrophic Differentiation.
D. Merz, R. Liu, K. Johnson, and R. Terkeltaub (2003)
J. Immunol.
171, 4406-4415
|Abstract »|Full Text »|PDF »
Nitric Oxide and Cyclic GMP Increase the Expression of Matrix Metalloproteinase-9 in Vascular Smooth Muscle.
M. Marcet-Palacios, K. Graham, C. Cass, A. D. Befus, I. Mayers, and M. W. Radomski (2003)
J. Pharmacol. Exp. Ther.
307, 429-436
|Abstract »|Full Text »|PDF »
Neurodegeneration in Striatum Induced by the Mitochondrial Toxin 3-Nitropropionic Acid: Role of Matrix Metalloproteinase-9 in Early Blood-Brain Barrier Disruption?.
G. W. Kim, Y. Gasche, S. Grzeschik, J.-C. Copin, C. M. Maier, and P. H. Chan (2003)
J. Neurosci.
23, 8733-8742
|Abstract »|Full Text »|PDF »
Mammalian Osmolytes and S-Nitrosoglutathione Promote {Delta}F508 Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) Protein Maturation and Function.
M. Howard, H. Fischer, J. Roux, B. C. Santos, S. R. Gullans, P. H. Yancey, and W. J. Welch (2003)
J. Biol. Chem.
278, 35159-35167
|Abstract »|Full Text »|PDF »
Nitric Oxide and Mechanisms of Redox Signaling.
J. Pfeilschifter, W. Eberhardt, and A. Huwiler (2003)
J. Am. Soc. Nephrol.
14, S237-240
|Abstract »|Full Text »|PDF »
Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry.
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
|Abstract »|Full Text »|PDF »
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
|Abstract »|Full Text »|PDF »
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
|Abstract »|Full Text »|PDF »
