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

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]  P. Gottschall,et al.  Zymographic measurement of gelatinase activity in brain tissue after detergent extraction and affinity-support purification , 1997, Journal of Neuroscience Methods.

[2]  Dongya Huang,et al.  In situ detection of AP sites and DNA strand breaks bearing 3'‐phosphate termini in ischemic mouse brain , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[3]  A. Hausladen,et al.  Oxidative modifications in nitrosative stress , 1998, Nature Structural Biology.

[4]  J W Smith,et al.  Substrate Hydrolysis by Matrix Metalloproteinase-9* , 2001, The Journal of Biological Chemistry.

[5]  T. Yoshimine,et al.  Elevation of Plasma Nitric Oxide End Products during Focal Cerebral Ischemia and Reperfusion in the Rat , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[6]  Joseph Loscalzo,et al.  A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds , 1993, Nature.

[7]  F. Barone,et al.  Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. , 1998, Stroke.

[8]  S. Lipton,et al.  Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation , 2000, Nature Neuroscience.

[9]  V. Wee Yong,et al.  Metalloproteinases in biology and pathology of the nervous system , 2001, Nature Reviews Neuroscience.

[10]  J. Stamler,et al.  Redox signaling: Nitrosylation and related target interactions of nitric oxide , 1994, Cell.

[11]  R. Knight,et al.  S-nitrosylation regulates apoptosis , 1997, Nature.

[12]  Eric J. Toone,et al.  (S)NO Signals: Translocation, Regulation, and a Consensus Motif , 1997, Neuron.

[13]  I. Campbell,et al.  Matrix metalloproteinases and their inhibitors in the nervous system: the good, the bad and the enigmatic , 1999, Trends in Neurosciences.

[14]  M. Moskowitz,et al.  Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. , 1994, Science.

[15]  S. Lipton,et al.  Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex , 1992, Neuron.

[16]  G. Schneider,et al.  Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. , 1999, Science.

[17]  G. Salvesen,et al.  The Regulation of Anoikis: MEKK-1 Activation Requires Cleavage by Caspases , 1997, Cell.

[18]  J. Arenillas,et al.  Matrix Metalloproteinase Expression After Human Cardioembolic Stroke: Temporal Profile and Relation to Neurological Impairment , 2001, Stroke.

[19]  H. Birkedal‐Hansen,et al.  The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Paul Tempst,et al.  Protein S-nitrosylation: a physiological signal for neuronal nitric oxide , 2001, Nature Cell Biology.

[21]  S. Ohnishi,et al.  Electron paramagnetic resonance study on nitric oxide production during brain focal ischemia and reperfusion in the rat , 1994, Brain Research.

[22]  S. Lipton,et al.  Tissue plasminogen activator (tPA) increase neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice , 1998, Nature Medicine.

[23]  J. Stamler,et al.  S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control , 1996, Nature.

[24]  M. Fujimura,et al.  Early Appearance of Activated Matrix Metalloproteinase-9 after Focal Cerebral Ischemia in Mice: A Possible Role in Blood—Brain Barrier Dysfunction , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[25]  Maria Panico,et al.  Inhibition of NF-κB DNA Binding by Nitric Oxide , 1996 .

[26]  T. Dawson,et al.  Gases as biological messengers: nitric oxide and carbon monoxide in the brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  D. Begley,et al.  Carrier-Mediated Delivery of Metabotropic Glutamate Receptor Ligands to the Central Nervous System: Structural Tolerance and Potential of the l-system Amino Acid Transporter at the Blood-Brain Barrier , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.