Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Open Life Sciences

formerly Central European Journal of Biology

Editor-in-Chief: Ratajczak, Mariusz

IMPACT FACTOR 2018: 0.504
5-year IMPACT FACTOR: 0.583

CiteScore 2018: 0.63

SCImago Journal Rank (SJR) 2018: 0.266
Source Normalized Impact per Paper (SNIP) 2018: 0.311

ICV 2017: 154.48

Open Access
See all formats and pricing
More options …
Volume 6, Issue 4


Volume 10 (2015)

Matrix metalloproteinases at key junctions in the pathomechanism of stroke

Zsolt Rottenberger / Krasimir Kolev
Published Online: 2011-05-21 | DOI: https://doi.org/10.2478/s11535-011-0030-z


Matrix metalloproteinases play a crucial role in the remodelling of the extracellular matrix through direct degradation of its structural proteins and control of extracellular signalling. The most common cause of ischemic brain damage is an atherothrombotic lesion in the supplying arteries. The progress of the atherosclerotic plaque development and the related thrombotic complications are mediated in part by matrix metalloproteinases. In addition to their role in the underlying disease, various members of this protease family are upregulated in the acute phase of ischemic brain damage as well as in the post-ischemic brain recovery following stroke. This review summarizes the current understanding of the matrix metalloproteinase-related molecular events at three stages of the ischemic cerebrovascular disease (in the atherosclerotic plaque, in the neurovascular unit of the brain and in the regenerating brain tissue).

Keywords: Extracellular matrix; Atherosclerosis; Blood-brain barrier; Ischemic damage; Brain regeneration

  • [1] Nagy Z., Blood-brain barrier and the cerebral endothelium, In: Johanson B.B., Owman C., Widner H., (Eds.), Pathophysiology of the bloodbrain barrier, Elsevier Science, Amsterdam — New York, 1990, 11–29 Google Scholar

  • [2] Rolfe D.F., Brown G.C., Cellular energy utilization and molecular origin of standard metabolic rate in mammals, Physiol. Rev., 1997, 77, 731–758 Google Scholar

  • [3] Webersinke G., Bauer H., Amberger A., Zach O., Bauer H.C., Comparison of gene expression of extracellular matrix molecules in brain microvascular endothelial cells and astrocytes, Biochem. Biophys. Res. Commun., 1992, 189, 877–884 http://dx.doi.org/10.1016/0006-291X(92)92285-6CrossrefGoogle Scholar

  • [4] Hornig C.R., Dorndorf W., Agnoli A.L., Haemorrhagic cerebral infarction — a prospective study, Stroke, 1986, 17, 179–185 CrossrefGoogle Scholar

  • [5] Gross J., Lapière C.M., Collagenolytic activity in amphibian tissues: a tissue culture assay, Proc. Natl. Acad. Sci. USA, 1962, 48, 1014–1022 http://dx.doi.org/10.1073/pnas.48.6.1014CrossrefGoogle Scholar

  • [6] Sternlicht M.D., Werb Z., How matrix metalloproteinases regulate cell behavior, Annu. Rev. Cell Dev. Biol., 2001, 17, 463–516 http://dx.doi.org/10.1146/annurev.cellbio.17.1.463CrossrefGoogle Scholar

  • [7] Fisher G.J., Talwar H.S., Lin J., Lin P., McPhillips F., Wang Z., et al., Retinoic acid inhibits induction of c-Jun protein by ultraviolet radiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo, J. Clin. Invest., 1998, 101, 1432–1440 http://dx.doi.org/10.1172/JCI2153CrossrefGoogle Scholar

  • [8] Sato H., Seiki M., Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells, Oncogene, 1993, 8, 395–405 Google Scholar

  • [9] Dong X., Song Y.N., Liu W.G., Guo X.L., MMP-9, a potential target for cerebral ischemic treatment, Curr. Neuropharmacol., 2009, 4, 269–275 http://dx.doi.org/10.2174/157015909790031157Google Scholar

  • [10] Vogel W., Gish G.D., Alves F., Pawson T., The discoidin domain receptor tyrosine kinases are activated by collagen, Mol. Cell, 1997, 1, 13–23 http://dx.doi.org/10.1016/S1097-2765(00)80003-9CrossrefGoogle Scholar

  • [11] Shrivastava A., Radziejewski C., Campbell E., Kovac L., McGlynn M., Ryan T.E., et al., An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors, Mol. Cell, 1997, 1, 25–34 http://dx.doi.org/10.1016/S1097-2765(00)80004-0CrossrefGoogle Scholar

  • [12] Gu Z., Kaul M., Yan B., Kridel S.J., Cui J., Strongin A.Y., et al., S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death, Science, 2002, 297, 1186–1190 http://dx.doi.org/10.1126/science.1073634CrossrefGoogle Scholar

  • [13] Wang X., Hou M., Tan L., Sun X., Zhang Y., Li P., et al., A hybrid protein of the amino-terminal fragment of urokinase and mutant plasminogen activator inhibitor-2 efficiently inhibits tumor cell invasion and metastasis, J. Cancer Res. Clin. Oncol., 2005, 131, 129–136 http://dx.doi.org/10.1007/s00432-004-0623-2CrossrefGoogle Scholar

  • [14] Nagase H., Woessner J.F., Matrix metalloproteinases, J. Biol. Chem., 1999, 274, 21491–21494 http://dx.doi.org/10.1074/jbc.274.31.21491CrossrefGoogle Scholar

  • [15] Sottrup-Jensen L., Birkedal-Hansen H., Human fibroblast collagenase-a-macroglobulin interactions. Localization of cleavage sites in the bait regions of five mammalian a-macroglobulins, J. Biol. Chem., 1989, 264, 393–401 Google Scholar

  • [16] Strongin A.Y., Collier I., Bannikov G., Marmer B.L., Grant G.A., Goldberg G.I., Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease, J. Biol. Chem., 1995, 270, 5331–5338 http://dx.doi.org/10.1074/jbc.270.10.5331CrossrefGoogle Scholar

  • [17] Langton K.P., Barker M.D., McKie N., Localization of the functional domains of human tissue inhibitor of metalloproteinases-3 and the effects of a Sorsby’s fundus dystrophy mutation, J. Biol. Chem., 1998, 273, 16778–16781 http://dx.doi.org/10.1074/jbc.273.27.16778CrossrefGoogle Scholar

  • [18] Loftus I.M., Naylor A.R., Goodall S., Crowther M., Jones L., Bell P.R.F., et al., Increased matrix metalloproteinase-9 activity in unstable carotid plaques. A potential role in acute plaque disruption, Stroke, 2000, 31, 40–47 CrossrefGoogle Scholar

  • [19] Nikkari S.T., O’Brien K.D., Ferguson M., Hatsukami T., Welgus H.G., Alpers C.E., et al., Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis, Circulation, 1995, 92, 1393–1398 CrossrefGoogle Scholar

  • [20] Sukhova G.K., Schönbeck U., Rabkin E., Schoen F.J., Poole A.R., Billinghurst R.C., et al., Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques, Circulation, 1999, 99, 2503–2509 CrossrefGoogle Scholar

  • [21] Herman M.P., Sukhova G.K., Libby P., Gerdes N., Tang N., Horton D.B., et al., Expression of neutrophil collagenase (matrix metalloproteinase-8) in human atheroma: a novel collagenolytic pathway suggested by transcriptional profiling, Circulation, 2001, 104, 1878–1880 http://dx.doi.org/10.1161/hc4101.097419CrossrefGoogle Scholar

  • [22] Galis Z.S., Muszynski M., Sukhova G.K., Simon-Morrissey E., Unemori E.N., Lark M.W., et al., Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion, Circ. Res., 1994, 75, 181–189 CrossrefGoogle Scholar

  • [23] Galis Z.S., Sukhova G.K., Kranzhöfer R., Clark S., Libby P., Macrophage foam cells from experimental atheroma constitutively produce matrix-degrading proteinases, Proc. Natl. Acad. Sci. USA, 1995, 92, 402–406 http://dx.doi.org/10.1073/pnas.92.2.402CrossrefGoogle Scholar

  • [24] Sarén P., Welgus H.G., Kovanen P.T., TNF-a and IL-1b selectively induce expression of 92-kDa gelatinase by human macrophages, J. Immunol., 1996, 157, 4159–4165 Google Scholar

  • [25] Rajagopalan S., Meng X.P., Ramasamy S., Harrison D.G., Galis Z.S., Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability, J. Clin. Invest., 1996, 98, 2572–2579 http://dx.doi.org/10.1172/JCI119076CrossrefGoogle Scholar

  • [26] Amento E.P., Ehsani N., Palmer H., Libby P., Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells, Arterioscler. Thromb., 1991, 11, 1223–1230 CrossrefGoogle Scholar

  • [27] Rekhter M.D., Zhang K., Narayanan A.S., Phan S., Schork M.A., Gordon D., Type I collagen gene expression in human atherosclerosis. Localization to specific plaque regions, Am. J. Pathol., 1993, 143, 1634–1648 Google Scholar

  • [28] Ang A.H., Tachas G., Campbell J.H., Bateman J.F., Campbell G.R., Collagen synthesis by cultured rabbit aortic smooth-muscle cells. Alteration with phenotype, Biochem. J., 1990, 265, 461–469 CrossrefGoogle Scholar

  • [29] Luttun A., Lutgens E., Manderveld A., Maris K., Collen D., Carmeliet P., et al., Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth, Circulation, 2004, 109, 1408–1414 http://dx.doi.org/10.1161/01.CIR.0000121728.14930.DECrossrefGoogle Scholar

  • [30] Godin D., Ivan E., Johnson C., Magid R., Galis Z.S., Remodeling of carotid artery is associated with increased expression of matrix metalloproteinases in mouse blood flow cessation model, Circulation, 2000, 102, 2861–2866 CrossrefGoogle Scholar

  • [31] Galis Z.S., Johnson C., Godin D., Magid R., Shipley J.M., Senior R.M., et al., Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling, Circ. Res., 2002, 91, 852–859 http://dx.doi.org/10.1161/01.RES.0000041036.86977.14CrossrefGoogle Scholar

  • [32] Galis Z.S., Sukhova G.K., Lark M.W., Libby P., Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques, J. Clin. Invest., 1994, 94, 2493–2503 http://dx.doi.org/10.1172/JCI117619CrossrefGoogle Scholar

  • [33] Fabunmi R.P., Sukhova G.K., Sugiyama S., Libby P., Expression of tissue inhibitor of metalloproteinases-3 in human atheroma and regulation in lesion-associated cells: a potential protective mechanism in plaque stability, Circ. Res., 1998, 83, 270–278 Google Scholar

  • [34] Mun-Bryce S., Rosenberg G.A., Matrix metalloproteinases in cerebrovascular disease, J. Cerebr. Blood Flow Metab., 1998, 18, 1163–1172 Google Scholar

  • [35] Rosenberg G.A., Mun-Bryce S., Wesley M., Kornfeld M., Collagenase-induced intracerebral hemorrhage in rats, Stroke, 1990, 21, 801–807 CrossrefGoogle Scholar

  • [36] Rosenberg G.A., Navratil M., Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat, Neurology, 1997, 48, 921–926. CrossrefGoogle Scholar

  • [37] Rosenberg G.A., Estrada E.Y., Dencoff J.E., Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain, Stroke, 1998, 29, 2189–2195 CrossrefGoogle Scholar

  • [38] Gasche Y., Fujimura M., Morita-Fujimura Y., Copin J.C., Kawase M., Massengale J., et al., Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction, J. Cerebr. Blood Flow Metab., 1999, 19, 1020–1028 Google Scholar

  • [39] Romanic A.M., White R.F., Arleth A.J., Ohlstein E.H., Barone F.C., Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size, Stroke, 1998, 29, 1020–1030 CrossrefGoogle Scholar

  • [40] Lapchak P.A., Chapman D.F., Zivin J.A., Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke, Stroke, 2000, 31, 3034–3040 CrossrefGoogle Scholar

  • [41] Heo J.H., Lucero J., Abumiya T., Koziol J.A., Copeland B.R., del Zoppo G.J., Matrix metalloproteinases increase very early during experimental focal cerebral ischemia, J. Cerebr. Blood Flow Metab., 1999, 19, 624–633 Google Scholar

  • [42] Ramos-Fernandez M., Bellolio M.F., Stead L.G., Matrix metalloproteinase-9 as a marker for acute ischemic stroke: a systematic review, J. Stroke Cerebrovasc. Dis., 2011, 20, 47–54 http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2009.10.008CrossrefGoogle Scholar

  • [43] Rosell A., Alvarez-Sabín J., Arenillas J.F., Rovira A., Delgado P., Fernández-Cadenas I., et al., A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke, Stroke, 2005, 36, 1415–1420 http://dx.doi.org/10.1161/01.STR.0000170641.01047.ccCrossrefGoogle Scholar

  • [44] Montaner J., Alvarez-Sabín J., Molina C.A., Anglés A., Abilleira S., Arenillas J., et al., Matrix metalloproteinase expression is related to hemorrhagic transformation after cardioembolic stroke, Stroke, 2001, 32, 2762–2767 http://dx.doi.org/10.1161/hs1201.99512CrossrefGoogle Scholar

  • [45] Montaner J., Molina C.A., Monasterio J., Abilleira S., Arenillas J.F., Ribó M., et al., Matrix metalloproteinase-9 pretreatment level predicts intracranial hemorrhagic complications after thrombolysis in human stroke, Circulation, 2003, 107, 598–603 http://dx.doi.org/10.1161/01.CIR.0000046451.38849.90CrossrefGoogle Scholar

  • [46] Asahi M., Wang X., Mori T., Sumii T., Jung J.C., Moskowitz M.A., et al., Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia, J. Neurosci., 2001, 21, 7724–7732 Google Scholar

  • [47] Svedin P., Hagberg H., Savman K., Zhu C., Mallard C., Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxiaischemia, J. Neurosci., 2007, 27, 1511–1518 http://dx.doi.org/10.1523/JNEUROSCI.4391-06.2007CrossrefGoogle Scholar

  • [48] Asahi M., Sumii T., Fini M.E., Itohara S., Lo E.H., Matrix metalloproteinase 2 gene knock-out has no effect on acute brain injury after focal ischemia, Neuroreport, 2001, 12, 3003–3007 http://dx.doi.org/10.1097/00001756-200109170-00050CrossrefGoogle Scholar

  • [49] Lucivero V., Prontera M., Mezzapesa D.M., Petruzellis M., Sancilio M., Tinelli A., et al., Different roles of matrix metalloproteinases-2 and -9 after human ischaemic stroke, Neurol. Sci., 2007, 28, 165–170 http://dx.doi.org/10.1007/s10072-007-0814-0CrossrefGoogle Scholar

  • [50] Yang Y., Estrada E.Y., Thompson J.F., Liu W., Rosenberg G.A., Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat, J. Cereb. Blood Flow Metab., 2007, 27, 697–709 http://dx.doi.org/10.1038/sj.jcbfm.9600440CrossrefGoogle Scholar

  • [51] Rosenberg G.A., Cunningham L.A., Wallace J., Alexander S., Estrada E.Y., Grossetete M., et al., Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures, Brain Res., 2001, 893, 104–112 http://dx.doi.org/10.1016/S0006-8993(00)03294-7CrossrefGoogle Scholar

  • [52] Kolev K., Skopál J., Simon L., Csonka É., Machovich R., Nagy Z., Matrix metalloproteinase-9 expression in post-hypoxic human brain capillary endothelial cells: H2O2 as a trigger and NF-κB as a signal transducer, Thromb. Haemost., 2003, 90, 528–537 Google Scholar

  • [53] Harkness K.A., Adamson P., Sussman J.D., Davies-Jones G.A., Greenwood J., Woodroofe M.N., Dexamethasone regulation of matrix metalloproteinase expression in CNS vascular endothelium, Brain, 2000, 123, 698–709 http://dx.doi.org/10.1093/brain/123.4.698CrossrefGoogle Scholar

  • [54] Gidday J.M., Gasche Y.G., Copin J.C., Shah A.R., Perez R.S., Shapiro S.D., et al., Leukocyte-derived matrix metalloproteinase-9 mediates blood-brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia, Am. J. Physiol. Heart Circ. Physiol., 2005, 289, 558–568 http://dx.doi.org/10.1152/ajpheart.01275.2004CrossrefGoogle Scholar

  • [55] Wang G., Guo Q., Hossain M., Fazio V., Zeynalov E., Janigro D., et al., Bone marrow-derived cells are the major source of MMP-9 contributing to blood-brain barrier dysfunction and infarct formation after ischemic stroke in mice, Brain Res., 2009, 1294, 183–192 http://dx.doi.org/10.1016/j.brainres.2009.07.070CrossrefGoogle Scholar

  • [56] Haas T.L., Davis S.J., Madri J.A., Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells, J. Biol. Chem., 1998, 273, 3604–3610 http://dx.doi.org/10.1074/jbc.273.6.3604CrossrefGoogle Scholar

  • [57] Cao W., Carney J.M., Duchon A., Floyd R.A., Chevion M., Oxygen free radical involvement in ischemia and reperfusion injury to brain, Neurosci. Lett., 1988, 88, 233–238 http://dx.doi.org/10.1016/0304-3940(88)90132-2CrossrefGoogle Scholar

  • [58] Halliwell B., Reactive oxygen species and the central nervous system, J. Neurochem., 1992, 59, 1609–1623 http://dx.doi.org/10.1111/j.1471-4159.1992.tb10990.xCrossrefGoogle Scholar

  • [59] Chinopoulos C., Tretter L., Rozsa A., Adam-Vizi V., Exacerbated responses to oxidative stress by an Na+ load in isolated nerve terminals: the role of ATP depletion and rise of [Ca2+]i, J. Neurosci., 2000, 20, 2094–2103 Google Scholar

  • [60] Hyslop P.A., Zhang Z., Pearson D.V., Phebus L.A., Measurement of striatal H2O2 by microdialysis following global forebrain ischemia and reperfusion in the rat: correlation with the cytotoxic potential of H2O2 in vitro, Brain Res., 1995, 671, 181–186 http://dx.doi.org/10.1016/0006-8993(94)01291-OCrossrefGoogle Scholar

  • [61] Ying W., Han S.H., Miller J.W., Swanson R.A., Acidosis potentiates oxidative neuronal death by multiple mechanisms, J. Neurochem., 1999, 73, 1549–1556. http://dx.doi.org/10.1046/j.1471-4159.1999.0731549.xCrossrefGoogle Scholar

  • [62] Zhang Z.G., Zhang L., Tsang W., Goussev A., Powers C., Ho K.L., et al., Dynamic platelet accumulation at the site of the occluded middle cerebral artery and in downstream microvessels is associated with loss of microvascular integrity after embolic middle cerebral artery occlusion, Brain Res., 2001, 912, 181–194 http://dx.doi.org/10.1016/S0006-8993(01)02735-4CrossrefGoogle Scholar

  • [63] Pagenstecher A., Stalder A.K., Kincaid C.L., Shapiro S.D., Campbell I.L., Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states, Am. J. Pathol., 1998, 152, 729–741 Google Scholar

  • [64] Itoh Y., Nagase H., Preferential inactivation of tissue inhibitor of metalloproteinases-1 that is bound to the precursor of matrix metalloproteinase 9 (progelatinase B) by human neutrophil elastase, J. Biol. Chem., 1995, 270, 16518–16521 http://dx.doi.org/10.1074/jbc.270.28.16518CrossrefGoogle Scholar

  • [65] Haddad J.J., Olver R.E., Land S.C., Antioxidant/pro-oxidant equilibrium regulates HIF-1a and NF-kB redox sensitivity. Evidence for inhibition by glutathione oxidation in alveolar epithelial cells, J. Biol. Chem., 2000, 275, 21130–21139 http://dx.doi.org/10.1074/jbc.M000737200CrossrefGoogle Scholar

  • [66] Nagy Z., Kolev K., Csonka É., Pék M., Machovich R., Contraction of human brain endothelial cells induced by thrombogenic and fibrinolytic factors. An in vitro cell culture model, Stroke, 1995, 26, 265–270 CrossrefGoogle Scholar

  • [67] Nagy Z., Kolev K., Csonka É., Vastag M., Machovich R., Perturbation of the integrity of the blood-brain barrier by fibrinolytic enzymes, Blood Coagul. Fibrinolysis, 1998, 9, 471–478 http://dx.doi.org/10.1097/00001721-199809000-00003CrossrefGoogle Scholar

  • [68] Turner J.S., Redpath G.T., Humphries J.E., Gonias S.L., Vandenberg S.R. Plasmin modulates the thrombin-evoked calcium response in C6 glioma cells, Biochem. J., 1994, 297, 175–179 Google Scholar

  • [69] Siao C.J., Fernandez S.R., Tsirka S.E., Cell typespecific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury, J. Neurosci., 2003, 23, 3234–3242 Google Scholar

  • [70] Tsuji K., Aoki T., Tejima E., Arai K., Lee S.R., Atochin D.N., et al., Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia, Stroke, 2005, 36, 1954–1959 http://dx.doi.org/10.1161/01.STR.0000177517.01203.ebGoogle Scholar

  • [71] Zhang C., An J., Haile W.B., Echeverry R., Strickland D.K., Yepes, M., Microglial low-density lipoprotein receptor-related protein 1 mediates the effect of tissue-type plasminogen activator on matrix metalloproteinase-9 activity in the ischemic brain, J. Cereb. Blood Flow Metab., 2009, 12, 1946–1954 http://dx.doi.org/10.1038/jcbfm.2009.174CrossrefGoogle Scholar

  • [72] Suzuki Y., Nagai N., Umemura K., Collen D., Lijnen H.R., Stromelysin-1 (MMP-3) is critical for intracranial bleeding after t-PA treatment of stroke in mice, J. Thromb. Haemost., 2007, 5, 1732–1739 http://dx.doi.org/10.1111/j.1538-7836.2007.02628.xCrossrefGoogle Scholar

  • [73] Suzuki Y., Nagai N., Yamakawa K, Kawakami J., Lijnen H.R., Umemura K., Tissue-type plasminogen activator (t-PA) induces stromelysin-1 (MMP-3) in endothelial cells through activation of lipoprotein receptor-related protein, Blood, 2009, 114, 3352–3358 http://dx.doi.org/10.1182/blood-2009-02-203919CrossrefGoogle Scholar

  • [74] Yepes M., Sandkvist M., Moore E.G., Bugge T.H., Strickland D.K., Lawrence D.A., Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein, J. Clin. Invest., 2003, 112, 1533–1540 CrossrefGoogle Scholar

  • [75] Bini A., Wu D., Schnuer J., Kudryk B.J., Characterization of stromelysin 1 (MMP-3), matrilysin (MMP-7), and membrane type 1 matrix metalloproteinase (MT1-MMP) derived fibrin(ogen) fragments D-dimer and D-like monomer: NH2-terminal sequences of late-stage digest fragments, Biochemistry, 1999, 38, 13928–13936 http://dx.doi.org/10.1021/bi991096gCrossrefGoogle Scholar

  • [76] Lelongt B., Bengatta S., Delauche M., Lund L.R., Werb Z., Ronco P.M., Matrix metalloproteinase 9 protects mice from anti-glomerular basement membrane nephritis through its fibrinolytic activity, J. Exp. Med., 2001, 193, 793–802 http://dx.doi.org/10.1084/jem.193.7.793CrossrefGoogle Scholar

  • [77] Kumura E., Yoshimine T., Iwatsuki K.I., Yamanaka K., Tanaka S., Hayakawa T., et al., Generation of nitric oxide and superoxide during reperfusion after focal cerebral ischemia in rats, Am. J. Physiol., 1996, 270, C748–C752 Google Scholar

  • [78] Cardone M.H., Salvesen G.S., Widmann C., Johnson G., Frisch S.M., The regulation of anoikis: MEKK-1 activation requires cleavage by caspases, Cell, 1997, 90, 315–323 http://dx.doi.org/10.1016/S0092-8674(00)80339-6Google Scholar

  • [79] Cunningham L.A., Wetzel M., Rosenberg G.A., Multiple roles for MMPs and TIMPs in cerebral ischemia, Glia, 2005, 50, 329–339 http://dx.doi.org/10.1002/glia.20169CrossrefGoogle Scholar

  • [80] Denker B.M., Nigam S.K., Molecular structure and assembly of the tight junction, Am. J. Physiol., 1998, 274, F1–F9 Google Scholar

  • [81] Hamann G.F., Okada Y., Fitridge R., del Zoppo G.J., Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion, Stroke, 1995, 26, 2120–2126 CrossrefGoogle Scholar

  • [82] Sole S., Petegnief V., Gorina R., Chamorro A., Planas A.M., Activation of matrix metalloproteinase-3 and agrin cleavage in cerebral ischemia/reperfusion, J. Neuropathol. Exp. Neurol., 2004, 63, 338–349 Google Scholar

  • [83] Gurney K.J., Estrada E.Y., Rosenberg G.A., Bloodbrain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation, Neurobiol. Dis., 2006, 23, 87–96 http://dx.doi.org/10.1016/j.nbd.2006.02.006Google Scholar

  • [84] Gu Z., Cui J., Brown S., Fridman R., Mobashery S., Strongin A.Y., et al., A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia, J. Neurosci., 2005, 25, 6401–6408 http://dx.doi.org/10.1523/JNEUROSCI.1563-05.2005CrossrefGoogle Scholar

  • [85] Frisch S.M., Francis H., Disruption of epithelial cell-matrix interactions induces apoptosis, J. Cell Biol., 1994, 124, 619–626 http://dx.doi.org/10.1083/jcb.124.4.619CrossrefGoogle Scholar

  • [86] Meredith J.E., Fazeli, B., Schwartz, M.A., The extracellular matrix as a cell survival factor, Mol. Biol. Cell, 1993, 4, 953–961 CrossrefGoogle Scholar

  • [87] Van den Steen P.E., Proost P., Wuyts A., Van Damme J., Opdenakker G., Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-a and leaves RANTES and MCP-2 intact, Blood, 2000, 96, 2673–2681 Google Scholar

  • [88] McQuibban G.A., Butler G.S., Gong J.H., Bendall L., Power C., Clark-Lewis I., et al., Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1, J. Biol. Chem., 2001, 276, 43503–43508 http://dx.doi.org/10.1074/jbc.M107736200CrossrefGoogle Scholar

  • [89] Zhang K., McQuibban G.A., Silva C., Butler G.S., Johnston J.B., Holden J., et al., HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration, Nature Neurosci., 2003, 6, 1064–1071 http://dx.doi.org/10.1038/nn1127Google Scholar

  • [90] Lee S.R., Kim H.Y., Rogowska J., Zhao B.Q., Bhide P., Parent J.M., et al., Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke, J. Neurosci., 2006, 26, 3491–3495 http://dx.doi.org/10.1523/JNEUROSCI.4085-05.2006CrossrefGoogle Scholar

  • [91] Barkho B.Z., Munoz A.E., Li X., Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines, Stem Cells, 2008, 26, 3139–3149 http://dx.doi.org/10.1634/stemcells.2008-0519CrossrefGoogle Scholar

  • [92] Nagel S., Sandy J.D., Meyding-Lamade U., Schwark C., Bartsch J.W., Wagner S., Focal cerebral ischemia induces changes in both MMP-13 and aggrecan around individual neurons, Brain Res., 2005, 1056, 43–50 http://dx.doi.org/10.1016/j.brainres.2005.07.036CrossrefGoogle Scholar

  • [93] Zhao B.Q., Wang S., Kim H.Y., Storrie H., Rosen B.R., Mooney D.J., et al., Role of matrix metalloproteinases in delayed cortical responses after stroke, Nature Med., 2006, 12, 441–445 http://dx.doi.org/10.1038/nm1387CrossrefGoogle Scholar

  • [94] Oh L.Y., Larsen P.H., Krekoski C.A., Edwards D.R., Donovan F., Werb Z., et al., Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes, J. Neurosci., 1999, 19, 8464–8475 Google Scholar

  • [95] Larsen P.H., Wells J.E., Stallcup W.B., Opdenakker G., Yong V.W., Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan, J. Neurosci., 2003, 23, 11127–11135 Google Scholar

  • [96] Shubayev V.I., Myers R.R., Matrix metalloproteinase-9 promotes nerve growth factor-induced neurite elongation but not new sprout formation in vitro, J. Neurosci. Res., 2004, 77, 229–239 http://dx.doi.org/10.1002/jnr.20160CrossrefGoogle Scholar

  • [97] Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., et al., Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis, Nature Cell Biol., 2000, 2, 737–744 http://dx.doi.org/10.1038/35036374CrossrefGoogle Scholar

  • [98] Zhang Z.G., Zhang L., Jiang Q., Zhang R., Davies K., Powers C., et al., VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain, J. Clin. Invest., 2000, 106, 829–838 http://dx.doi.org/10.1172/JCI9369CrossrefGoogle Scholar

  • [99] Seo D.W., Li H., Guedez L., Wingfield P.T., Diaz T., Salloum R., et al., TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism, Cell, 2003, 114, 171–180 http://dx.doi.org/10.1016/S0092-8674(03)00551-8CrossrefGoogle Scholar

  • [100] Qi J. H., Ebrahem Q., Moore N., Murphy G., Claesson-Welsh L., Bond M., et al., A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2, Nat. Med., 2003, 9, 407–415 http://dx.doi.org/10.1038/nm846CrossrefGoogle Scholar

About the article

Published Online: 2011-05-21

Published in Print: 2011-08-01

Citation Information: Open Life Sciences, Volume 6, Issue 4, Pages 471–485, ISSN (Online) 2391-5412, DOI: https://doi.org/10.2478/s11535-011-0030-z.

Export Citation

© 2011 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Churriyyatul Anam, Retnaningsih ., and Nyoman Suci
Pakistan Journal of Nutrition, 2018, Volume 17, Number 11, Page 535

Comments (0)

Please log in or register to comment.
Log in