Matrix metalloproteinases at key junctions in the pathomechanism of stroke

Review Article

Abstract

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 

References

  1. [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, 11–29Google Scholar
  2. [2]
    Rolfe D.F., Brown G.C., Cellular energy utilization and molecular origin of standard metabolic rate in mammals, Physiol. Rev., 1997, 77, 731–758PubMedGoogle Scholar
  3. [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, 877–884PubMedCrossRefGoogle Scholar
  4. [4]
    Hornig C.R., Dorndorf W., Agnoli A.L., Haemorrhagic cerebral infarction — a prospective study, Stroke, 1986, 17, 179–185PubMedGoogle Scholar
  5. [5]
    Gross J., Lapière C.M., Collagenolytic activity in amphibian tissues: a tissue culture assay, Proc. Natl. Acad. Sci. USA, 1962, 48, 1014–1022PubMedCrossRefGoogle Scholar
  6. [6]
    Sternlicht M.D., Werb Z., How matrix metalloproteinases regulate cell behavior, Annu. Rev. Cell Dev. Biol., 2001, 17, 463–516PubMedCrossRefGoogle Scholar
  7. [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, 1432–1440PubMedCrossRefGoogle Scholar
  8. [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, 395–405PubMedGoogle Scholar
  9. [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, 269–275CrossRefGoogle Scholar
  10. [10]
    Vogel W., Gish G.D., Alves F., Pawson T., The discoidin domain receptor tyrosine kinases are activated by collagen, Mol. Cell, 1997, 1, 13–23PubMedCrossRefGoogle Scholar
  11. [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, 25–34PubMedCrossRefGoogle Scholar
  12. [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, 1186–1190PubMedCrossRefGoogle Scholar
  13. [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, 129–136PubMedCrossRefGoogle Scholar
  14. [14]
    Nagase H., Woessner J.F., Matrix metalloproteinases, J. Biol. Chem., 1999, 274, 21491–21494PubMedCrossRefGoogle Scholar
  15. [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, 393–401PubMedGoogle Scholar
  16. [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, 5331–5338PubMedCrossRefGoogle Scholar
  17. [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, 16778–16781PubMedCrossRefGoogle Scholar
  18. [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, 40–47PubMedGoogle Scholar
  19. [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, 1393–1398PubMedGoogle Scholar
  20. [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, 2503–2509PubMedGoogle Scholar
  21. [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, 1878–1880CrossRefGoogle Scholar
  22. [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, 181–189PubMedGoogle Scholar
  23. [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, 402–406PubMedCrossRefGoogle Scholar
  24. [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, 4159–4165PubMedGoogle Scholar
  25. [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, 2572–2579PubMedCrossRefGoogle Scholar
  26. [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, 1223–1230PubMedGoogle Scholar
  27. [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, 1634–1648PubMedGoogle Scholar
  28. [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, 461–469PubMedGoogle Scholar
  29. [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, 1408–1414PubMedCrossRefGoogle Scholar
  30. [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, 2861–2866PubMedGoogle Scholar
  31. [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, 852–859PubMedCrossRefGoogle Scholar
  32. [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, 2493–2503PubMedCrossRefGoogle Scholar
  33. [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, 270–278PubMedGoogle Scholar
  34. [34]
    Mun-Bryce S., Rosenberg G.A., Matrix metalloproteinases in cerebrovascular disease, J. Cerebr. Blood Flow Metab., 1998, 18, 1163–1172Google Scholar
  35. [35]
    Rosenberg G.A., Mun-Bryce S., Wesley M., Kornfeld M., Collagenase-induced intracerebral hemorrhage in rats, Stroke, 1990, 21, 801–807PubMedGoogle Scholar
  36. [36]
    Rosenberg G.A., Navratil M., Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat, Neurology, 1997, 48, 921–926.PubMedGoogle Scholar
  37. [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, 2189–2195PubMedGoogle Scholar
  38. [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, 1020–1028Google Scholar
  39. [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, 1020–1030PubMedGoogle Scholar
  40. [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, 3034–3040PubMedGoogle Scholar
  41. [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, 624–633Google Scholar
  42. [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, 47–54PubMedCrossRefGoogle Scholar
  43. [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, 1415–1420PubMedCrossRefGoogle Scholar
  44. [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, 2762–2767PubMedCrossRefGoogle Scholar
  45. [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, 598–603PubMedCrossRefGoogle Scholar
  46. [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, 7724–7732PubMedGoogle Scholar
  47. [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, 1511–1518PubMedCrossRefGoogle Scholar
  48. [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, 3003–3007PubMedCrossRefGoogle Scholar
  49. [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, 165–170PubMedCrossRefGoogle Scholar
  50. [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, 697–709PubMedCrossRefGoogle Scholar
  51. [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, 104–112PubMedCrossRefGoogle Scholar
  52. [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, 528–537PubMedGoogle Scholar
  53. [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, 698–709PubMedCrossRefGoogle Scholar
  54. [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, 558–568CrossRefGoogle Scholar
  55. [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, 183–192PubMedCrossRefGoogle Scholar
  56. [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, 3604–3610PubMedCrossRefGoogle Scholar
  57. [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, 233–238PubMedCrossRefGoogle Scholar
  58. [58]
    Halliwell B., Reactive oxygen species and the central nervous system, J. Neurochem., 1992, 59, 1609–1623PubMedCrossRefGoogle Scholar
  59. [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, 2094–2103PubMedGoogle Scholar
  60. [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, 181–186PubMedCrossRefGoogle Scholar
  61. [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.PubMedCrossRefGoogle Scholar
  62. [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, 181–194PubMedCrossRefGoogle Scholar
  63. [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, 729–741PubMedGoogle Scholar
  64. [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, 16518–16521PubMedCrossRefGoogle Scholar
  65. [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, 21130–21139PubMedCrossRefGoogle Scholar
  66. [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, 265–270PubMedGoogle Scholar
  67. [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, 471–478PubMedCrossRefGoogle Scholar
  68. [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, 175–179PubMedGoogle Scholar
  69. [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, 3234–3242PubMedGoogle Scholar
  70. [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, 1954–1959PubMedCrossRefGoogle Scholar
  71. [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, 1946–1954CrossRefGoogle Scholar
  72. [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, 1732–1739PubMedCrossRefGoogle Scholar
  73. [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, 3352–3358PubMedCrossRefGoogle Scholar
  74. [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, 1533–1540PubMedGoogle Scholar
  75. [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, 13928–13936PubMedCrossRefGoogle Scholar
  76. [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, 793–802PubMedCrossRefGoogle Scholar
  77. [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–C752PubMedGoogle Scholar
  78. [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, 315–323PubMedCrossRefGoogle Scholar
  79. [79]
    Cunningham L.A., Wetzel M., Rosenberg G.A., Multiple roles for MMPs and TIMPs in cerebral ischemia, Glia, 2005, 50, 329–339PubMedCrossRefGoogle Scholar
  80. [80]
    Denker B.M., Nigam S.K., Molecular structure and assembly of the tight junction, Am. J. Physiol., 1998, 274, F1–F9PubMedGoogle Scholar
  81. [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, 2120–2126PubMedGoogle Scholar
  82. [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, 338–349PubMedGoogle Scholar
  83. [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, 87–96PubMedCrossRefGoogle Scholar
  84. [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, 6401–6408PubMedCrossRefGoogle Scholar
  85. [85]
    Frisch S.M., Francis H., Disruption of epithelial cell-matrix interactions induces apoptosis, J. Cell Biol., 1994, 124, 619–626PubMedCrossRefGoogle Scholar
  86. [86]
    Meredith J.E., Fazeli, B., Schwartz, M.A., The extracellular matrix as a cell survival factor, Mol. Biol. Cell, 1993, 4, 953–961PubMedGoogle Scholar
  87. [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, 2673–2681PubMedGoogle Scholar
  88. [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, 43503–43508PubMedCrossRefGoogle Scholar
  89. [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, 1064–1071PubMedCrossRefGoogle Scholar
  90. [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, 3491–3495PubMedCrossRefGoogle Scholar
  91. [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, 3139–3149PubMedCrossRefGoogle Scholar
  92. [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, 43–50PubMedCrossRefGoogle Scholar
  93. [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, 441–445PubMedCrossRefGoogle Scholar
  94. [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, 8464–8475PubMedGoogle Scholar
  95. [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, 11127–11135PubMedGoogle Scholar
  96. [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, 229–239PubMedCrossRefGoogle Scholar
  97. [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, 737–744PubMedCrossRefGoogle Scholar
  98. [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, 829–838PubMedCrossRefGoogle Scholar
  99. [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, 171–180PubMedCrossRefGoogle Scholar
  100. [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, 407–415PubMedCrossRefGoogle Scholar

Copyright information

© © Versita Warsaw and Springer-Verlag Wien 2011

Authors and Affiliations

  1. 1.Department of Medical BiochemistrySemmelweis UniversityBudapestHungary

Personalised recommendations