Brain extracellular matrix in neurodegeneration

Brain Pathology

Volumn 19, Issue 4, 2009, Pages 573-585

  Bonneh Barkay, Dafna ^b   Wiley, Clayton A ^a,b  

^a PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

CNS; ECM; Neurodegeneration

Indexed keywords

FIBROBLAST GROWTH FACTOR; GELATINASE A; GELATINASE B; HYALURONIC ACID BINDING PROTEIN; KAINIC ACID; LAMININ; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE 19; MICROTUBULE ASSOCIATED PROTEIN 2; PLATELET DERIVED GROWTH FACTOR; PROTEOCHONDROITIN SULFATE; STROMELYSIN; TENASCIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ALZHEIMER DISEASE; CELL DIFFERENTIATION; CEREBROVASCULAR ACCIDENT; DEMENTIA; ENZYME ACTIVATION; ENZYME ACTIVITY; EXCITOTOXICITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; BRAIN DISEASES; EXTRACELLULAR MATRIX; HUMANS; MACACA; MATRIX METALLOPROTEINASES; NERVE DEGENERATION; TISSUE PLASMINOGEN ACTIVATOR;

EID: 69949183657     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2008.00195.x     Document Type: Review

References (99)

1. Achim CL, Wiley CA (1996) Inflammation in AIDS and the role of the macrophage in brain pathology. Curr Opin Neurol 9 : 221 225.
2. Al'Qteishat A, Gaffney J, Krupinski J, Rubio F, West D, Kumar S et al (2006) Changes in hyaluronan production and metabolism following ischaemic stroke in man. Brain 129 : 2158 2176.
3. Angelov DN, Walther M, Streppel M, Guntinas-Lichius O, Neiss WF, Probstmeier R et al (1998) Tenascin-R is antiadhesive for activated microglia that induce downregulation of the protein after peripheral nerve injury: a new role in neuronal protection. J Neurosci 18 : 6218 6229.
4. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE et al (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20 : 2427 2438.
5. Avolio C, Ruggieri M, Giuliani F, Liuzzi GM, Leante R, Riccio P et al (2003) Serum MMP-2 and MMP-9 are elevated in different multiple sclerosis subtypes. J Neuroimmunol 136 : 46 53.
6. Back SA, Tuohy TM, Chen H, Wallingford N, Craig A, Struve J et al (2005) Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med 11 : 966 972.
7. Baig S, Wilcock GK, Love S (2005) Loss of perineuronal net N-acetylgalactosamine in Alzheimer's disease. Acta Neuropathol (Berl) 110 : 393 401.
8. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80 : 1267 1290.
9. Belichenko PV, Miklossy J, Celio MR (1997) HIV-I induced destruction of neocortical extracellular matrix components in AIDS victims. Neurobiol Dis 4 : 301 310.
10. Belichenko PV, Miklossy J, Belser B, Budka H, Celio MR (1999) Early destruction of the extracellular matrix around parvalbumin-immunoreactive interneurons in Creutzfeldt-Jakob disease. Neurobiol Dis 6 : 269 279.
11. Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14 : 375 403.
12. Bilousova TV, Rusakov DA, Ethell DW, Ethell IM (2006) Matrix metalloproteinase-7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation. J Neurochem 97 : 44 56.
13. Bo L, Geurts JJ, Mork SJ, van der Valk P (2006) Grey matter pathology in multiple sclerosis. Acta Neurol Scand Suppl 183 : 48 50.
14. Bowie ML, Troch MM, Delrow J, Dietze EC, Bean GR, Ibarra C et al (2007) Interferon regulatory factor-1 regulates reconstituted extracellular matrix (rECM)-mediated apoptosis in human mammary epithelial cells. Oncogene 26 : 2017 2026.
15. Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, Meyer H et al (2002) Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 22 : 7417 7427.
16. Bridges LC, Bowditch RD (2005) ADAM-integrin interactions: potential integrin regulated ectodomain shedding activity. Curr Pharm Des 11 : 837 847.
17. Bruckner G, Hausen D, Hartig W, Drlicek M, Arendt T, Brauer K (1999) Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease. Neuroscience 92 : 791 805.
18. Budka H, Costanzi G, Cristina S, Lechi A, Parravicini C, Trabattoni R et al (1987) Brain pathology induced by infection with the human immunodeficiency virus (HIV). A histological, immunocytochemical, and electron microscopical study of 100 autopsy cases. Acta Neuropathol 75 : 185 198.
19. Bukalo O, Schachner M, Dityatev A (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104 : 359 369.
20. Canning DR, McKeon RJ, DeWitt DA, Perry G, Wujek JR, Frederickson RC et al (1993) Beta-amyloid of Alzheimer's disease induces reactive gliosis that inhibits axonal outgrowth. Exp Neurol 124 : 289 298.
21. Carmichael ST (2006) Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 59 : 735 742.
22. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ (2000) Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci 20 : RC87.
23. Chen ZL, Strickland S (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91 : 917 925.
24. Conant K, McArthur JC, Griffin DE, Sjulson L, Wahl LM, Irani DN (1999) Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann Neurol 46 : 391 398.
25. Crocker SJ, Pagenstecher A, Campbell IL (2004) The TIMPs tango with MMPs and more in the central nervous system. J Neurosci Res 75 : 1 11.
26. Crocker SJ, Whitmire JK, Frausto RF, Chertboonmuang P, Soloway PD, Whitton JL et al (2006) Persistent macrophage/microglial activation and myelin disruption after experimental autoimmune encephalomyelitis in tissue inhibitor of metalloproteinase-1-deficient mice. Am J Pathol 169 : 2104 2116.
27. Cuzner ML, Opdenakker G (1999) Plasminogen activators and matrix metalloproteases, mediators of extracellular proteolysis in inflammatory demyelination of the central nervous system. J Neuroimmunol 94 : 1 14.
28. Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277 : 43707 43716.
29. DeWitt DA, Silver J, Canning DR, Perry G (1993) Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer's disease. Exp Neurol 121 : 149 152.
30. Dietze EC, Bowie ML, Mrozek K, Caldwell LE, Neal C, Marjoram RJ et al (2005) CREB-binding protein regulates apoptosis and growth of HMECs grown in reconstituted ECM via laminin-5. J Cell Sci 118 : 5005 5022.
31. Dityatev A, Schachner M (2003) Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 4 : 456 468.
32. Dityatev A, Schachner M (2006) The extracellular matrix and synapses. Cell Tissue Res 326 : 647 654.
33. Ellison JA, Velier JJ, Spera P, Jonak ZL, Wang X, Barone FC et al (1998) Osteopontin and its integrin receptor alpha(v)beta3 are upregulated during formation of the glial scar after focal stroke. Stroke 29 : 1698 1706 discussion IM, Ethell DW (2007) Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 85 : 2813 2823.
34. 2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci 22 : 7177 7194.
35. Franklin SL, Love S, Greene JR, Betmouni S (2008) Loss of perineuronal net in ME7 prion disease. J Neuropathol Exp Neurol 67 : 189 199.
36. Gary DS, Mattson MP (2001) Integrin signaling via the PI3-kinase-Akt pathway increases neuronal resistance to glutamate-induced apoptosis. J Neurochem 76 : 1485 1496.
37. Giraudon P, Szymocha R, Buart S, Bernard A, Cartier L, Belin MF et al (2000) T lymphocytes activated by persistent viral infection differentially modify the expression of metalloproteinases and their endogenous inhibitors, TIMPs, in human astrocytes: relevance to HTLV-I-induced neurological disease. J Immunol 164 : 2718 2727.
38. Gualandris A, Jones TE, Strickland S, Tsirka SE (1996) Membrane depolarization induces calcium-dependent secretion of tissue plasminogen activator. J Neurosci 16 : 2220 2225.
39. Gutowski NJ, Newcombe J, Cuzner ML. (1999) Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol Appl Neurobiol 25 : 207 214.
40. Hobohm C, Gunther A, Grosche J, Rossner S, Schneider D, Bruckner G (2005) Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats. J Neurosci Res 80 : 539 548.
41. van Horssen J, Otte-Holler I, David G, Maat-Schieman ML, van den Heuvel LP, Wesseling P et al (2001) Heparan sulfate proteoglycan expression in cerebrovascular amyloid beta deposits in Alzheimer's disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains. Acta Neuropathol (Berl) 102 : 604 614.
42. van Horssen J, Bo L, Dijkstra CD, de Vries HE (2006) Extensive extracellular matrix depositions in active multiple sclerosis lesions. Neurobiol Dis 24 : 484 491. (Pubitemid 44716678)
43. van Horssen J, Vos CM, Admiraal L, van Haastert ES, Montagne L, van der Valk P et al (2006) Matrix metalloproteinase-19 is highly expressed in active multiple sclerosis lesions. Neuropathol Appl Neurobiol 32 : 585 593.
44. van Horssen J, Dijkstra CD, de Vries HE (2007) The extracellular matrix in multiple sclerosis pathology. J Neurochem 103 : 1293 1301.
45. Jourquin J, Tremblay E, Bernard A, Charton G, Chaillan FA, Marchetti E et al (2005) Tissue inhibitor of metalloproteinases-1 (TIMP-1) modulates neuronal death, axonal plasticity, and learning and memory. Eur J Neurosci 22 : 2569 2578.
46. Kaminska B, Filipkowski RK, Biedermann IW, Konopka D, Nowicka D, Hetman M et al (1997) Kainate-evoked modulation of gene expression in rat brain. Acta Biochim Pol 44 : 781 789.
47. Kim YS, Kim SS, Cho JJ, Choi DH, Hwang O, Shin DH et al (2005) Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J Neurosci 25 : 3701 3711.
48. Laurent UB, Laurent TC, Hellsing LK, Persson L, Hartman M, Lilja K (1996) Hyaluronan in human cerebrospinal fluid. Acta Neurol Scand 94 : 194 206.
49. Le SS, Loucks FA, Udo H, Richardson-Burns S, Phelps RA, Bouchard RJ et al (2005) Inhibition of Rac GTPase triggers a c-Jun- and Bim-dependent mitochondrial apoptotic cascade in cerebellar granule neurons. J Neurochem 94 : 1025 1039.
50. Liu IH, Uversky VN, Munishkina LA, Fink AL, Halfter W, Cole GJ (2005) Agrin binds alpha-synuclein and modulates alpha-synuclein fibrillation. Glycobiology 15 : 1320 1331.
51. Lo EH, Wang X, Cuzner ML (2002) Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J Neurosci Res 69 : 1 9.
52. Lorenzl S, Albers DS, LeWitt PA, Chirichigno JW, Hilgenberg SL, Cudkowicz ME et al (2003) Tissue inhibitors of matrix metalloproteinases are elevated in cerebrospinal fluid of neurodegenerative diseases. J Neurol Sci 207 : 71 76.
53. Lorenzl S, Albers DS, Chirichigno JW, Augood SJ, Beal MF (2004) Elevated levels of matrix metalloproteinases-9 and -1 and of tissue inhibitors of MMPs, TIMP-1 and TIMP-2 in postmortem brain tissue of progressive supranuclear palsy. J Neurol Sci 218 : 39 45.
54. Madani R, Nef S, Vassalli JD (2003) Emotions are building up in the field of extracellular proteolysis. Trends Mol Med 9 : 183 185.
55. Matias-Roman S, Galvez BG, Genis L, Yanez-Mo M, de la Rosa G, Sanchez-Mateos P et al (2005) Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood 105 : 3956 3964.
56. Medina-Flores R, Wang G, Bissel SJ, Murphey-Corb M, Wiley CA (2004) Destruction of extracellular matrix proteoglycans is pervasive in simian retroviral neuroinfection. Neurobiol Dis 16 : 604 616.
57. Melchor JP, Strickland S (2005) Tissue plasminogen activator in central nervous system physiology and pathology. Thromb Haemost 93 : 655 660.
58. Milev P, Monnerie H, Popp S, Margolis RK, Margolis RU (1998) The core protein of the chondroitin sulfate proteoglycan phosphacan is a high-affinity ligand of fibroblast growth factor-2 and potentiates its mitogenic activity. J Biol Chem 273 : 21439 21442.
59. Miyata S, Nishimura Y, Nakashima T (2007) Perineuronal nets protect against amyloid beta-protein neurotoxicity in cultured cortical neurons. Brain Res 30 : 200 206.
60. Morawski M, Bruckner MK, Riederer P, Bruckner G, Arendt T (2004) Perineuronal nets potentially protect against oxidative stress. Exp Neurol 188 : 309 315.
61. Muir EM, Adcock KH, Morgenstern DA, Clayton R, von Stillfried N, Rhodes K et al (2002) Matrix metalloproteases and their inhibitors are produced by overlapping populations of activated astrocytes. Brain Res Mol Brain Res 100 : 103 117.
62. Nagase H, Woessner JF Jr. (1999) Matrix metalloproteinases. J Biol Chem 274 : 21491 21494.
63. Navia BA, Jordan BD, Price RW (1986) The AIDS dementia complex: I. Clinical features. Ann Neurol 19 : 517 524.
64. Nelson CM, Bissell MJ (2006) Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22 : 287 309.
65. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13 : 9 22.
66. Ogier C, Bernard A, Chollet AM, Led T, Hanessian S, Charton G et al (2006) Matrix metalloproteinase-2 (MMP-2) regulates astrocyte motility in connection with the actin cytoskeleton and integrins. Glia 54 : 272 284.
67. Okamoto M, Sakiyama J, Mori S, Kurazono S, Usui S, Hasegawa M et al (2003) Kainic acid-induced convulsions cause prolonged changes in the chondroitin sulfate proteoglycans neurocan and phosphacan in the limbic structures. Exp Neurol 184 : 179 195.
68. Osman M, Tortorella M, Londei M, Quaratino S (2002) Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases define the migratory characteristics of human monocyte-derived dendritic cells. Immunology 105 : 73 82.
69. Pagenstecher A, Wussler EM, Opdenakker G, Volk B, Campbell IL (2001) Distinct expression patterns and levels of enzymatic activity of matrix metalloproteinases and their inhibitors in primary brain tumors. J Neuropathol Exp Neurol 60 : 598 612.
70. Porter S, Clark IM, Kevorkian L, Edwards DR (2005) The ADAMTS metalloproteinases. Biochem J 386 : 15 27.
71. Raines EW, Ross R (1992) Compartmentalization of PDGF on extracellular binding sites dependent on exon-6-encoded sequences. J Cell Biol 116 : 533 543.
72. Rauvala H, Peng HB (1997) HB-GAM heparin-binding growth-associated molecule and heparin-type glycans in the development and plasticity of neuron-target contacts. Prog Neurobiol 52 : 127 144.
73. Reijerkerk A, Kooij G, van der Pol SM, Khazen S, Dijkstra CD, de Vries HE (2006) Diapedesis of monocytes is associated with MMP-mediated occludin disappearance in brain endothelial cells. FASEB J 20 : 2550 2552.
74. Rivera S, Tremblay E, Timsit S, Canals O, Ben-Ari Y, Khrestchatisky M (1997) Tissue inhibitor of metalloproteinases-1 (TIMP-1) is differentially induced in neurons and astrocytes after seizures: evidence for developmental, immediate early gene, and lesion response. J Neurosci 17 : 4223 4235.
75. Saghatelyan AK, Dityatev A, Schmidt S, Schuster T, Bartsch U, Schachner M (2001) Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol Cell Neurosci 17 : 226 240.
76. Saksela O, Rifkin DB (1990) Release of basic fibroblast growth factor-heparan sulfate complexes from endothelial cells by plasminogen activator-mediated proteolytic activity. J Cell Biol 110 : 767 775.
77. Sasaki A, Yamaguchi H, Ogawa A, Sugihara S, Nakazato Y (1997) Microglial activation in early stages of amyloid beta protein deposition. Acta Neuropathol 94 : 316 322.
78. Satoh K, Suzuki N, Yokota H (2000) ADAMTS-4 (a disintegrin and metalloproteinase with thrombospondin motifs) is transcriptionally induced in beta-amyloid treated rat astrocytes. Neurosci Lett 289 : 177 180.
79. Schuppel K, Brauer K, Hartig W, Grosche J, Earley B, Leonard BE et al (2002) Perineuronal nets of extracellular matrix around hippocampal interneurons resist destruction by activated microglia in trimethyltin-treated rats. Brain Res 958 : 448 453.
80. Sheehan JJ, Zhou C, Gravanis I, Rogove AD, Wu YP, Bogenhagen DF et al (2007) Proteolytic activation of monocyte chemoattractant protein-1 by plasmin underlies excitotoxic neurodegeneration in mice. J Neurosci 27 : 1738 1745.
81. Sithu SD, English WR, Olson P, Krubasik D, Baker AH, Murphy G et al (2007) Membrane-type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J Biol Chem 282 : 25010 25019.
82. Snow AD, Mar H, Nochlin D, Kimata K, Kato M, Suzuki S et al (1988) The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease. Am J Pathol 133 : 456 463.
83. Snow AD, Mar H, Nochlin D, Sekiguchi RT, Kimata K, Koike Y et al (1990) Early accumulation of heparan sulfate in neurons and in the beta-amyloid protein-containing lesions of Alzheimer's disease and Down's syndrome. Am J Pathol 137 : 1253 1270.
84. Snow AD, Mar H, Nochlin D, Kresse H, Wight TN (1992) Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease. J Histochem Cytochem 40 : 105 113.
85. Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J Neurosci 22 : 920 930.
86. Tsirka SE, Gualandris A, Amaral DG, Strickland S (1995) Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377 : 340 344.
87. Umehara Y, Yamada S, Nishimura S, Shioi J, Robakis NK, Sugahara K (2004) Chondroitin sulfate of appican, the proteoglycan form of amyloid precursor protein, produced by C6 glioma cells interacts with heparin-binding neuroregulatory factors. FEBS Lett 557 : 233 238.
88. Van Lint P, Libert C (2007) Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J Leukoc Biol 82 : 1375 1381.
89. Verbeek MM, Otte-Holler I, van den Born J, van den Heuvel LP, David G, Wesseling P et al (1999) Agrin is a major heparan sulfate proteoglycan accumulating in Alzheimer's disease brain. Am J Pathol 155 : 2115 2125.
90. Vlodavsky I, Miao HQ, Medalion B, Danagher P, Ron D (1996) Involvement of heparan sulfate and related molecules in sequestration and growth promoting activity of fibroblast growth factor. Cancer Metastasis Rev 15 : 177 186.
91. Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H et al (1999) Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 19 : 4245 4262.
92. Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57 : 276 289.
93. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64 : 841 848.
94. Yong VW (2005) Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 6 : 931 944.
95. Yong VW, Krekoski CA, Forsyth PA, Bell R, Edwards DR (1998) Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 21 : 75 80.
96. Yoshihara Y, Nakamura H, Obata K, Yamada H, Hayakawa T, Fujikawa K et al (2000) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis. Ann Rheum Dis 59 : 455 461.
97. Yuan W, Matthews RT, Sandy JD, Gottschall PE (2002) Association between protease-specific proteolytic cleavage of brevican and synaptic loss in the dentate gyrus of kainate-treated rats. Neuroscience 114 : 1091 1101.
98. Zhang K, McQuibban GA, Silva C, Butler GS, Johnston JB, Holden J et al (2003) HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration. Nat Neurosci 6 : 1064 1071.
99. Zhou J, Marten NW, Bergmann CC, Macklin WB, Hinton DR, Stohlman SA (2005) Expression of matrix metalloproteinases and their tissue inhibitor during viral encephalitis. J Virol 79 : 4764 4773.