Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke

Developmental Neurobiology

Volumn 71, Issue 11, 2011, Pages 1018-1039

  Baeten, Kim M ^a   Akassoglou, Katerina ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Basal lamina; Fibrinogen; Integrins; Ischemia; Laminin

Indexed keywords

AGRIN; COLLAGEN TYPE 4; ENTACTIN; FIBRINOGEN; FIBRONECTIN; INTEGRIN RECEPTOR; LAMININ; OSTEONECTIN; OSTEOPONTIN; PERLECAN; SCLEROPROTEIN;

ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; DYNAMICS; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; PATHOLOGY; PERICYTE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROKE;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MICROCIRCULATION; RECEPTORS, CELL SURFACE; STROKE;

EID: 80053924042     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20954     Document Type: Article

References (230)

1. Abbott NJ, Ronnback L, Hansson E. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53.
2. Abumiya T, Lucero J, Heo JH, Tagaya M, Koziol JA, Copeland BR, del Zoppo GJ. 1999. Activated microvessels express vascular endothelial growth factor and integrin alpha(v)beta3 during focal cerebral ischemia. J Cereb Blood Flow Metab 19: 1038-1050.
3. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, Degen JL, et al. 2007a. The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 204: 571-582.
4. Adams RA, Passino M, Sachs BD, Nuriel T, Akassoglou K. 2004. Fibrin mechanisms and functions in nervous system pathology. Mol Interv 4: 163-176.
5. Adams RA, Schachtrup C, Davalos D, Tsigelny I, Akassoglou K. 2007b. Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis. Curr Med Chem 14: 2925-2936.
6. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, et al. 2006. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 169: 566-583.
7. Adibhatla RM, Hatcher JF. 2008. Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies. CNS Neurol Disord Drug Targets 7: 243-253.
8. Agrawal S, Anderson P, Durbeej M, van Rooijen N, Ivars F, Opdenakker G, Sorokin LM. 2006. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 203: 1007-1019.
9. Akassoglou K, Yu WM, Akpinar P, Strickland S. 2002. Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33: 861-875.
10. Akiyama H, McGeer PL. 1990. Brain microglia constitutively express beta-2 integrins. J Neuroimmunol 30: 81-93.
11. Al Ahmad A, Taboada CB, Gassmann M, Ogunshola OO. 2011. Astrocytes and pericytes differentially modulate blood-brain barrier characteristics during development and hypoxic insult. J Cereb Blood Flow Metab 31:693-705.
12. Alamowitch S, Plaisier E, Favrole P, Prost C, Chen Z, Van Agtmael T, Marro B, et al. 2009. Cerebrovascular disease related to COL4A1 mutations in HANAC syndrome. Neurology 73: 1873-1882.
13. Alghisi GC, Ponsonnet L, Ruegg C. 2009. The integrin antagonist cilengitide activates alphaVbeta3, disrupts VE-cadherin localization at cell junctions and enhances permeability in endothelial cells. PLo S One 4: e4449.
14. Allaman I, Belanger M, Magistretti PJ. 2011. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34: 76-87.
15. Allt G, Lawrenson JG. 2001. Pericytes: cell biology and pathology. Cells Tissues Organs 169: 1-11.
16. Annes JP, Munger JS, Rifkin DB. 2003. Making sense of latent TGFbeta activation. J Cell Sci 116: 217-224.
17. Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y. 1999. Perlecan is essential for cartilage and cephalic development. Nat Genet 23: 354-358.
18. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, et al. 2010. Pericytes regulate the blood-brain barrier. Nature 468: 557-561.
19. Arnold SA, Rivera LB, Miller AF, Carbon JG, Dineen SP, Xie Y, Castrillon DH, et al. 2010. Lack of host SPARC enhances vascular function and tumor spread in an orthotopic murine model of pancreatic carcinoma. Dis Model Mech 3: 57-72.
20. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, et al. 2000. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20: 2427-2438.
21. Baeten KM, Richard MC, Kanse SM, Mutch NJ, Degen JL, Booth NA. 2010. Activation of single-chain urokinase-type plasminogen activator by platelet-associated plasminogen: A mechanism for stimulation of fibrinolysis by platelets. J Thromb Haemost 8: 1313-1322.
22. Bagley RG, Weber W, Rouleau C, Teicher BA. 2005. Pericytes and endothelial precursor cells: cellular interactions and contributions to malignancy. Cancer Res 65: 9741-9750.
23. Balabanov R, Washington R, Wagnerova J, Dore-Duffy P. 1996. CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc Res 52: 127-142.
24. Bandopadhyay R, Orte C, Lawrenson JG, Reid AR, De Silva S, Allt G. 2001. Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. J Neurocytol 30: 35-44.
25. Banerjee S, Bhat MA. 2007. Neuron-glial interactions in blood-brain barrier formation. Annu Rev Neurosci 30: 235-258.
26. Barber AJ, Lieth E. 1997. Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier. Dev Dyn 208: 62-74.
27. Baumann E, Preston E, Slinn J, Stanimirovic D. 2009. Post-ischemic hypothermia attenuates loss of the vascular basement membrane proteins, agrin and SPARC, and the blood-brain barrier disruption after global cerebral ischemia. Brain Res 1269: 185-197.
28. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV. 2010. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68: 409-427.
29. Berzin TM, Zipser BD, Rafii MS, Kuo-Leblanc V, Yancopoulos GD, Glass DJ, Fallon JR, Stopa EG. 2000. Agrin and microvascular damage in Alzheimer's disease. Neurobiol Aging 21: 349-355.
30. Booth NA. 1999. Fibrinolysis and thrombosis. Baillieres Best Pract Res Clin Haematol 12: 423-433.
31. Booth NA, Anderson JA, Bennett B. 1985. Platelet release protein which inhibits plasminogen activators. J Clin Pathol 38: 825-830.
32. Brachvogel B, Pausch F, Farlie P, Gaipl U, Etich J, Zhou Z, Cameron T, et al. 2007. Isolated Anxa5+/Sca-1+ perivascular cells from mouse meningeal vasculature retain their perivascular phenotype in vitro and in vivo. Exp Cell Res 313: 2730-2743.
33. Brekken RA, Sage EH. 2000. SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biol 19: 569-580.
34. Burgess RW, Skarnes WC, Sanes JR. 2000. Agrin isoforms with distinct amino termini: differential expression, localization, and function. J Cell Biol 151: 41-52.
35. Cambier S, Gline S, Mu D, Collins R, Araya J, Dolganov G, Einheber S, et al. 2005. Integrin alpha(v)beta8-mediated activation of transforming growth factor-beta by perivascular astrocytes: an angiogenic control switch. Am J Pathol 166: 1883-1894.
36. Candelario-Jalil E, Yang Y, Rosenberg GA. 2009. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158: 983-994.
37. Cardoso FL, Brites D, Brito MA. 2010. Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev 64: 328-363.
38. Caruso RA, Fedele F, Finocchiaro G, Pizzi G, Nunnari M, Gitto G, Fabiano V, et al. 2009. Ultrastructural descriptions of pericyte/endothelium peg-socket interdigitations in the microvasculature of human gastric carcinomas. Anticancer Res 29: 449-453.
39. Carvey PM, Hendey B, Monahan AJ. 2009. The blood-brain barrier in neurodegenerative disease: a rhetorical perspective. J Neurochem 111: 291-314.
40. Chang DI, Hosomi N, Lucero J, Heo JH, Abumiya T, Mazar AP, del Zoppo GJ. 2003. Activation systems for latent matrix metalloproteinase-2 are upregulated immediately after focal cerebral ischemia. J Cereb Blood Flow Metab 23: 1408-1419.
41. Chen W, Ma Q, Suzuki H, Hartman R, Tang J, Zhang JH. 2011. Osteopontin reduced hypoxia-ischemia neonatal brain injury by suppression of apoptosis in a rat pup model. Stroke 42: 764-769.
42. Clark AW, Krekoski CA, Bou SS, Chapman KR, Edwards DR. 1997. Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci Lett 238: 53-56.
43. Claudio L, Raine CS, Brosnan CF. 1995. Evidence of persistent blood-brain barrier abnormalities in chronic-progressive multiple sclerosis. Acta Neuropathol 90: 228-238.
44. Colgan OC, Collins NT, Ferguson G, Murphy RP, Birney YA, Cahill PA, Cummins PM. 2008. Influence of basolateral condition on the regulation of brain microvascular endothelial tight junction properties and barrier function. Brain Res 1193: 84-92.
45. Cortes-Canteli M, Paul J, Norris EH, Bronstein R, Ahn HJ, Zamolodchikov D, Bhuvanendran S, et al. 2010. Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer's disease. Neuron 66: 695-709.
46. Costell M, Gustafsson E, Aszodi A, Morgelin M, Bloch W, Hunziker E, Addicks K, et al. 1999. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 147: 1109-1122.
47. Daneman R, Zhou L, Kebede AA, Barres BA. 2010. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468: 562-566.
48. Dejana E, Tournier-Lasserve E, Weinstein BM. 2009. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell 16: 209-221.
49. del Zoppo GJ, Milner R. 2006. Integrin-matrix interactions in the cerebral microvasculature. Arterioscler Thromb Vasc Biol 26: 1966-1975.
50. del Zoppo GJ, Milner R, Mabuchi T, Hung S, Wang X, Koziol JA. 2006. Vascular matrix adhesion and the blood-brain barrier. Biochem Soc Trans 34: 1261-1266.
51. Ding Y, Clark JC. 2006. Cerebrovascular injury in stroke. Neurol Res 28: 3-10.
52. Dohgu S, Takata F, Yamauchi A, Nakagawa S, Egawa T, Naito M, Tsuruo T, et al. 2005. Brain pericytes contribute to the induction and up-regulation of blood-brain barrier functions through transforming growth factor-beta production. Brain Res 1038: 208-215.
53. Dong L, Chen Y, Lewis M, Hsieh JC, Reing J, Chaillet JR, Howell CY, et al. 2002. Neurologic defects and selective disruption of basement membranes in mice lacking entactin-1/nidogen-1. Lab Invest 82: 1617-1630.
54. Dore-Duffy P, Katychev A, Wang X, Van Buren E. 2006. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 26: 613-624.
55. Dore-Duffy P, Owen C, Balabanov R, Murphy S, Beaumont T, Rafols JA. 2000. Pericyte migration from the vascular wall in response to traumatic brain injury. Microvasc Res 60: 55-69.
56. Ek CJ, Dziegielewska KM, Stolp H, Saunders NR. 2006. Functional effectiveness of the blood-brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 496: 13-26.
57. Ellis V, Behrendt N, Dano K. 1991. Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J Biol Chem 266: 12752-12758.
58. Ellison JA, Barone FC, Feuerstein GZ. 1999. Matrix remodeling after stroke. De novo expression of matrix proteins and integrin receptors. Ann N Y Acad Sci 890: 204-222.
59. Ellison JA, Velier JJ, Spera P, Jonak ZL, Wang X, Barone FC, Feuerstein GZ. 1998. Osteopontin and its integrin receptor alpha(v)beta3 are upregulated during formation of the glial scar after focal stroke. Stroke 29: 1698-1706; discussion1707.
60. Engelhardt B. 2003. Development of the blood-brain barrier. Cell Tissue Res 314: 119-129.
61. Engelhardt B, Sorokin L. 2009. The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction. Semin Immunopathol 31: 497-511.
62. ffrench-Constant C, Colognato H. 2004. Integrins: versatile integrators of extracellular signals. Trends Cell Biol 14: 678-686.
63. Fisher M. 2009. Pericyte signaling in the neurovascular unit. Stroke 40: S13-15.
64. Flick MJ, Du X, Witte DP, Jirouskova M, Soloviev DA, Busuttil SJ, Plow EF, et al. 2004. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 113: 1596-1606.
65. Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M. 1994. The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125: 669-680.
66. Fukuda S, Fini CA, Mabuchi T, Koziol JA, Eggleston LL, Jr., del Zoppo GJ. 2004. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 35: 998-1004.
67. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR. 1996. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85: 525-535.
68. George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079-1091.
69. Gesemann M, Brancaccio A, Schumacher B, Ruegg MA. 1998. Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J Biol Chem 273: 600-605.
70. Giancotti FG, Ruoslahti E. 1999. Integrin signaling. Science 285: 1028-1032.
71. Goldblum SE, Ding X, Funk SE, Sage EH. 1994. SPARC (secreted protein acidic and rich in cysteine) regulates endothelial cell shape and barrier function. Proc Natl Acad Sci U S A 91: 3448-3452.
72. Gong Y, Kim SO, Felez J, Grella DK, Castellino FJ, Miles LA. 2001. Conversion of Glu-plasminogen to Lys-plasminogen is necessary for optimal stimulation of plasminogen activation on the endothelial cell surface. J Biol Chem 276: 19078-19083.
73. Gorlatov S, Medved L. 2002. Interaction of fibrin(ogen) with the endothelial cell receptor VE-cadherin: mapping of the receptor-binding site in the NH2-terminal portions of the fibrin beta chains. Biochemistry 41: 4107-4116.
74. Gould DB, Phalan FC, van Mil SE, Sundberg JP, Vahedi K, Massin P, Bousser MG, et al. 2006. Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med 354: 1489-1496.
75. Gravanis I, Tsirka SE. 2008. Tissue-type plasminogen activator as a therapeutic target in stroke. Expert Opin Ther Targets 12: 159-170.
76. Grazioli A, Alves CS, Konstantopoulos K, Yang JT. 2006.. Defective blood vessel development and pericyte/pvSMC distribution in alpha 4 integrin-deficient mouse embryos. Dev Biol 293: 165-177.
77. Grimpe B, Probst JC, Hager G. 1999. Suppression of nidogen-1 translation by antisense targeting affects the adhesive properties of cultured astrocytes. Glia 28: 138-149.
78. Halfter W, Dong S, Yip YP, Willem M, Mayer U. 2002. A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 22: 6029-6040.
79. Hallmann R, Horn N, Selg M, Wendler O, Pausch F, Sorokin LM. 2005. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev 85: 979-1000.
80. Hamann GF, Liebetrau M, Martens H, Burggraf D, Kloss CU, Bultemeier G, Wunderlich N, et al. 2002. Microvascular basal lamina injury after experimental focal cerebral ischemia and reperfusion in the rat. J Cereb Blood Flow Metab 22: 526-533.
81. Hamann GF, Okada Y, Fitridge R, del Zoppo GJ. 1995. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 26: 2120-2126.
82. Harhaj NS, Antonetti DA. 2004. Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 36: 1206-1237.
83. Haring HP, Berg EL, Tsurushita N, Tagaya M, del Zoppo GJ. 1996. E-selectin appears in nonischemic tissue during experimental focal cerebral ischemia. Stroke 27: 1386-1391; discussion 1391-1382.
84. Haseloff RF, Blasig IE, Bauer HC, Bauer H. 2005. In search of the astrocytic factor(s) modulating blood-brain barrier functions in brain capillary endothelial cells in vitro. Cell Mol Neurobiol 25: 25-39.
85. Heye N, Cervos-Navarro J. 1996. Microthromboemboli in acute infarcts: analysis of 40 autopsy cases. Stroke 27: 431-434.
86. Hoylaerts M, Rijken DC, Lijnen HR, Collen D. 1982. Kinetics of the activation of plasminogen by human tissue plasminogen activator. Role of fibrin. J Biol Chem 257: 2912-2919.
87. Huber JD, Egleton RD, Davis TP. 2001. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24: 719-725.
88. Hynes RO. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
89. Hynes RO. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
90. Iozzo RV, Cohen IR, Grassel S, Murdoch AD. 1994. The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem J 302 (Pt 3): 625-639.
91. Israeli D, Tanne D, Daniels D, Last D, Shneor R, Guez D, Landau E, et al. 2010. The application of MRI for depiction of subtle blood brain barrier disruption in stroke. Int J Biol Sci 7: 1-8.
92. Janzer RC, Raff MC. 1987. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325: 253-257.
93. Johansson PA, Dziegielewska KM, Liddelow SA, Saunders NR. 2008. The blood-CSF barrier explained: when development is not immaturity. Bioessays 30: 237-248.
94. Kang SH, Kramer JM. 2000. Nidogen is nonessential and not required for normal type IV collagen localization in Caenorhabditis elegans. Mol Biol Cell 11: 3911-3923.
95. Kastrup A, Groschel K, Ringer TM, Redecker C, Cordesmeyer R, Witte OW, Terborg C. 2008. Early disruption of the blood-brain barrier after thrombolytic therapy predicts hemorrhage in patients with acute stroke. Stroke 39: 2385-2387.
96. Kermode AG, Thompson AJ, Tofts P, MacManus DG, Kendall BE, Kingsley DP, Moseley IF, et al. 1990. Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenetic and clinical implications. Brain 113: 1477-1489.
97. Kniesel U, Wolburg H. 2000. Tight junctions of the blood-brain barrier. Cell Mol Neurobiol 20: 57-76.
98. Knoll R, Postel R, Wang J, Kratzner R, Hennecke G, Vacaru AM, Vakeel P, et al. 2007. Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116: 515-525.
99. Knox SM, Whitelock JM. 2006. Perlecan: how does one molecule do so many things? Cell Mol Life Sci 63: 2435-2445.
100. Kondo T, Kinouchi H, Kawase M, Yoshimoto T. 1996. Astroglial cells inhibit the increasing permeability of brain endothelial cell monolayer following hypoxia/reoxygenation. Neurosci Lett 208: 101-104.
101. Kose N, Asashima T, Muta M, Iizasa H, Sai Y, Terasaki T, Nakashima E. 2007. Altered expression of basement membrane-related molecules in rat brain pericyte, endothelial, and astrocyte cell lines after transforming growth factor-beta1 treatment. Drug Metab Pharmacokinet 22: 255-266.
102. Koto T, Takubo K, Ishida S, Shinoda H, Inoue M, Tsubota K, Okada Y, et al. 2007. Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells. Am J Pathol 170: 1389-1397.
103. Kwok JCF, Dick G, Wang D, Fawcett JW. 2011. Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol 71: 1073-1089.
104. Kwon I, Kim EH, del Zoppo GJ, Heo JH. 2009. Ultrastructural and temporal changes of the microvascular basement membrane and astrocyte interface following focal cerebral ischemia. J Neurosci Res 87: 668-676.
105. Lai CH, Kuo KH. 2005. The critical component to establish in vitro BBB model: Pericyte. Brain Res Brain Res Rev 50: 258-265.
106. Lam CK, Yoo T, Hiner B, Liu Z, Grutzendler J. 2010. Embolus extravasation is an alternative mechanism for cerebral microvascular recanalization. Nature 465: 478-482.
107. Languino LR, Duperray A, Joganic KJ, Fornaro M, Thornton GB, Altieri DC. 1995. Regulation of leukocyte-endothelium interaction and leukocyte transendothelial migration by intercellular adhesion molecule 1- fibrinogen recognition. Proc Natl Acad Sci U S A 92: 1505-1509.
108. Languino LR, Plescia J, Duperray A, Brian AA, Plow EF, Geltosky JE, Altieri DC. 1993. Fibrinogen mediates leukocyte adhesion to vascular endothelium through an ICAM-1-dependent pathway. Cell 73: 1423-1434.
109. Lassmann H, Zimprich F, Vass K, Hickey WF. 1991. Microglial cells are a component of the perivascular glia limitans. J Neurosci Res 28: 236-243.
110. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
111. Liesi P, Risteli L. 1989. Glial cells of mammalian brain produce a variant form of laminin. Exp Neurol 105: 86-92.
112. Lijnen HR. 2001. Elements of the fibrinolytic system. Ann N Y Acad Sci 936: 226-236.
113. Liotta LA, Goldfarb RH, Brundage R, Siegal GP, Terranova V, Garbisa S. 1981. Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res 41: 4629-4636.
114. Lukes A, Mun-Bryce S, Lukes M, Rosenberg GA. 1999. Extracellular matrix degradation by metalloproteinases and central nervous system diseases. Mol Neurobiol 19: 267-284.
115. Mark KS, Davis TP. 2002. Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 282: H1485-1494.
116. Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP. 2010. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58: 1094-1103.
117. McCarty JH. 2009. Integrin-mediated regulation of neurovascular development, physiology and disease. Cell Adh Migr 3: 211-215.
118. McCarty JH, Lacy-Hulbert A, Charest A, Bronson RT, Crowley D, Housman D, Savill J, et al. 2005. Selective ablation of alphav integrins in the central nervous system leads to cerebral hemorrhage, seizures, axonal degeneration and premature death. Development 132: 165-176.
119. McCarty JH, Monahan-Earley RA, Brown LF, Keller M, Gerhardt H, Rubin K, Shani M, et al. 2002. Defective associations between blood vessels and brain parenchyma lead to cerebral hemorrhage in mice lacking alphav integrins. Mol Cell Biol 22: 7667-7677.
120. McGeer PL, Zhu SG, Dedhar S. 1990. Immunostaining of human brain capillaries by antibodies to very late antigens. J Neuroimmunol 26: 213-218.
121. Melgar MA, Rafols J, Gloss D, Diaz FG. 2005. Postischemic reperfusion: ultrastructural blood-brain barrier and hemodynamic correlative changes in an awake model of transient forebrain ischemia. Neurosurgery 56: 571-581.
122. Meller R, Stevens SL, Minami M, Cameron JA, King S, Rosenzweig H, Doyle K, et al. 2005. Neuroprotection by osteopontin in stroke. J Cereb Blood Flow Metab 25: 217-225.
123. Mettouchi A, Klein S, Guo W, Lopez-Lago M, Lemichez E, Westwick JK, Giancotti FG. 2001. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell 8: 115-127.
124. Mi H, Haeberle H, Barres BA. 2001. Induction of astrocyte differentiation by endothelial cells. J Neurosci 21: 1538-1547.
125. Miles LA, Plow EF. 1985. Binding and activation of plasminogen on the platelet surface. J Biol Chem 260: 4303-4311.
126. Milner R. 2009. Microglial expression of alphavbeta3 and alphavbeta5 integrins is regulated by cytokines and the extracellular matrix: beta5 integrin null microglia show no defects in adhesion or MMP-9 expression on vitronectin. Glia 57: 714-723.
127. Milner R, Campbell IL. 2002. Developmental regulation of beta1 integrins during angiogenesis in the central nervous system. Mol Cell Neurosci 20: 616-626.
128. Milner R, Huang X, Wu J, Nishimura S, Pytela R, Sheppard D, ffrench-Constant C. 1999. Distinct roles for astrocyte alphavbeta5 and alphavbeta8 integrins in adhesion and migration. J Cell Sci 112 (Pt 23): 4271-4279.
129. Milner R, Hung S, Wang X, Berg GI, Spatz M, del Zoppo GJ. 2008a. Responses of endothelial cell and astrocyte matrix-integrin receptors to ischemia mimic those observed in the neurovascular unit. Stroke 39: 191-197.
130. Milner R, Hung S, Wang X, Spatz M, del Zoppo GJ. 2008b. The rapid decrease in astrocyte-associated dystroglycan expression by focal cerebral ischemia is protease-dependent. J Cereb Blood Flow Metab 28: 812-823.
131. Milner R, Relvas JB, Fawcett J, ffrench-Constant C. 2001. Developmental regulation of alphav integrins produces functional changes in astrocyte behavior. Mol Cell Neurosci 18: 108-118.
132. Miner JH, Cunningham J, Sanes JR. 1998. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol 143: 1713-1723.
133. Miner JH, Li C, Mudd JL, Go G, Sutherland AE. 2004. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131: 2247-2256.
134. Miranti CK, Brugge JS. 2002. Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol 4: E83-90.
135. Miyagoe Y, Hanaoka K, Nonaka I, Hayasaka M, Nabeshima Y, Arahata K, Takeda S. 1997. Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett 415: 33-39.
136. Miyamoto S, Teramoto H, Gutkind JS, Yamada KM. 1996. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J Cell Biol 135: 1633-1642.
137. Moore CJ, Winder SJ. 2010. Dystroglycan versatility in cell adhesion: a tale of multiple motifs. Cell Commun Signal 8: 3.
138. Morancho A, Rosell A, Garcia-Bonilla L, Montaner J. 2010. Metalloproteinase and stroke infarct size: role for anti-inflammatory treatment? Ann N Y Acad Sci 1207: 123-133.
139. Moro L, Venturino M, Bozzo C, Silengo L, Altruda F, Beguinot L, Tarone G, et al. 1998. Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. Embo J 17: 6622-6632.
140. Mosesson MW. 2005. Fibrinogen and fibrin structure and functions. J Thromb Haemost 3: 1894-1904.
141. Motamed K, Sage EH. 1998. SPARC inhibits endothelial cell adhesion but not proliferation through a tyrosine phosphorylation-dependent pathway. J Cell Biochem 70: 543-552.
142. Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, Sheppard D, et al. 2002. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol 157: 493-507.
143. Mu Z, Yang Z, Yu D, Zhao Z, Munger JS. 2008. TGFbeta1 and TGFbeta3 are partially redundant effectors in brain vascular morphogenesis. Mech Dev 125: 508-516.
144. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, et al. 1999. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96: 319-328.
145. Murray V, Norrving B, Sandercock PA, Terent A, Wardlaw JM, Wester P. 2010. The molecular basis of thrombolysis and its clinical application in stroke. J Intern Med 267: 191-208.
146. Murshed M, Smyth N, Miosge N, Karolat J, Krieg T, Paulsson M, Nischt R. 2000. The absence of nidogen 1 does not affect murine basement membrane formation. Mol Cell Biol 20: 7007-7012.
147. Nakagawa S, Deli MA, Nakao S, Honda M, Hayashi K, Nakaoke R, Kataoka Y, et al. 2007. Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol Neurobiol 27: 687-694.
148. Neuwelt EA, Bauer B, Fahlke C, Fricker G, Iadecola C, Janigro D, Leybaert L, et al. 2011. Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 12: 169-182.
149. Nguyen JV, Soto I, Kim KY, Bushong EA, Oglesby E, Valiente-Soriano FJ, Yang Z, et al. 2011. Myelination transition zone astrocytes are constitutively phagocytic and have synuclein dependent reactivity in glaucoma. Proc Natl Acad Sci U S A 108: 1176-1181.
150. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
151. Ninomia T, Wang L, Kumar SR, Kim A, Zlokovic BV. 2000. Brain injury and cerebrovascular fibrin deposition correlate with reduced antithrombotic brain capillary functions in a hypertensive stroke model. J Cereb Blood Flow Metab 20: 998-1009.
152. Nishimura SL. 2009. Integrin-mediated transforming growth factor-beta activation, a potential therapeutic target in fibrogenic disorders. Am J Pathol 175: 1362-1370.
153. Nishioku T, Dohgu S, Takata F, Eto T, Ishikawa N, Kodama KB, Nakagawa S, et al. 2009. Detachment of brain pericytes from the basal lamina is involved in disruption of the blood-brain barrier caused by lipopolysaccharide-induced sepsis in mice. Cell Mol Neurobiol 29: 309-316.
154. Noell S, Fallier-Becker P, Deutsch U, Mack AF, Wolburg H. 2009. Agrin defines polarized distribution of orthogonal arrays of particles in astrocytes. Cell Tissue Res 337: 185-195.
155. Okada Y, Copeland BR, Fitridge R, Koziol JA, del Zoppo GJ. 1994. Fibrin contributes to microvascular obstructions and parenchymal changes during early focal cerebral ischemia and reperfusion. Stroke 25: 1847-1853; discussion1853-1844.
156. Okada Y, Copeland BR, Hamann GF, Koziol JA, Cheresh DA, del Zoppo GJ. 1996. Integrin alphavbeta3 is expressed in selected microvessels after focal cerebral ischemia. Am J Pathol 149: 37-44.
157. Oki T, Takahashi S, Kuwabara S, Yoshiyama Y, Mori M, Hattori T, Suzuki N. 2004. Increased ability of peripheral blood lymphocytes to degrade laminin in multiple sclerosis. J Neurol Sci 222: 97-11.
158. Owens T, Bechmann I, Engelhardt B. 2008. Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol 67: 1113-1121.
159. Paul J, Strickland S, Melchor JP. 2007. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease. J Exp Med 204: 1999-2008.
160. Paulus W, Baur I, Schuppan D, Roggendorf W. 1993. Characterization of integrin receptors in normal and neoplastic human brain. Am J Pathol 143: 154-163.
161. Peppiatt CM, Howarth C, Mobbs P, Attwell D. 2006. Bidirectional control of CNS capillary diameter by pericytes. Nature 443: 700-704.
162. Petzelbauer P, Zacharowski PA, Miyazaki Y, Friedl P, Wickenhauser G, Castellino FJ, Groger M, et al. 2005. The fibrin-derived peptide Bbeta15-42 protects the myocardium against ischemia-reperfusion injury. Nat Med 11: 298-304.
163. Pinkstaff JK, Detterich J, Lynch G, Gall C. 1999. Integrin subunit gene expression is regionally differentiated in adult brain. J Neurosci 19: 1541-1556.
164. Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. 2004. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131: 1619-1628.
165. Proctor JM, Zang K, Wang D, Wang R, Reichardt LF. 2005. Vascular development of the brain requires beta8 integrin expression in the neuroepithelium. J Neurosci 25: 9940-9948.
166. Quaegebeur A, Segura I, Carmeliet P. 2010. Pericytes: blood-brain barrier safeguards against neurodegeneration?. Neuron 68: 321-323.
167. Ranby M. 1982. Studies on the kinetics of plasminogen activation by tissue plasminogen activator. Biochim Biophys Acta 704: 461-469.
168. Rascher G, Fischmann A, Kroger S, Duffner F, Grote EH, Wolburg H. 2002. Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: spatial segregation of tenascin and agrin. Acta Neuropathol 104: 85-91.
169. Redzic Z. 2011. Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: similarities and differences. Fluids Barriers CNS 8: 3.
170. Risau W, Lemmon V. 1988. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol 125: 441-450.
171. Rouach N, Giaume C. 2001. Connexins and gap junctional communication in astrocytes are targets for neuroglial interaction. Prog Brain Res 132: 203-214.
172. Ryu JK, Davalos D, Akassoglou K. 2009. Fibrinogen signal transduction in the nervous system. J Thromb Haemost 7 Suppl 1: 151-154.
173. Ryu JK, McLarnon JG. 2009. A leaky blood-brain barrier, fibrinogen infiltration and microglial reactivity in inflamed Alzheimer's disease brain. J Cell Mol Med 13: 2911-2925.
174. Sachs BD, Baillie GS, McCall JR, Passino MA, Schachtrup C, Wallace DA, Dunlop AJ, et al. 2007. p75 neurotrophin receptor regulates tissue fibrosis through inhibition of plasminogen activation via a PDE4/cAMP/PKA pathway. J Cell Biol 177: 1119-1132.
175. Sahni A, Arevalo MT, Sahni SK, Simpson-Haidaris PJ. 2009. The VE-cadherin binding domain of fibrinogen induces endothelial barrier permeability and enhances transendothelial migration of malignant breast epithelial cells. Int J Cancer 125: 577-584.
176. Sandoval KE, Witt KA. 2008. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32: 200-219.
177. Saunders NR, Ek CJ, Habgood MD, Dziegielewska KM. 2008. Barriers in the brain: a renaissance? Trends Neurosci 31: 279-286.
178. Schachtrup C, Lu P, Jones LL, Lee JK, Lu J, Sachs BD, Zheng B, Akassoglou K. 2007. Fibrinogen inhibits neurite outgrowth via beta3 integrin-mediated phosphorylation of the EGF receptor. Proc Natl Acad Sci U S A 104: 11814-11819.
179. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, Margolis RU, et al. 2010. Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J Neurosci 30: 5843-5854.
180. Schneller M, Vuori K, Ruoslahti E. 1997. Alphavbeta3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. Embo J 16: 5600-5607.
181. Scholler K, Trinkl A, Klopotowski M, Thal SC, Plesnila N, Trabold R, Hamann GF, et al. 2007. Characterization of microvascular basal lamina damage and blood-brain barrier dysfunction following subarachnoid hemorrhage in rats. Brain Res 1142: 237-246.
182. Schultz DR, Arnold PI. 1990. Properties of four acute phase proteins: C-reactive protein, serum amyloid A protein, alpha 1-acid glycoprotein, and fibrinogen. Semin Arthritis Rheum 20: 129-147.
183. Schwartz MA. 1997. Integrins, oncogenes, and anchorage independence. J Cell Biol 139: 575-578.
184. Schwartz MA, Ginsberg MH. 2002. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol 4: E65-68.
185. Shattil SJ, Hoxie JA, Cunningham M, Brass LF. 1985. Changes in the platelet membrane glycoprotein IIb. IIIa complex during platelet activation. J Biol Chem 260: 11107-11114.
186. Sheehan JJ, Tsirka SE. 2005. Fibrin-modifying serine proteases thrombin, tPA, and plasmin in ischemic stroke: a review. Glia 50: 340-350.
187. Shen W, Li S, Chung SH, Zhu L, Stayt J, Su T, Couraud PO, et al. 2011. Tyrosine phosphorylation of VE-cadherin and claudin-5 is associated with TGF-beta1-induced permeability of centrally derived vascular endothelium. Eur J Cell Biol 90: 323-332.
188. Siddharthan V, Kim YV, Liu S, Kim KS. 2007. Human astrocytes/astrocyte-conditioned medium and shear stress enhance the barrier properties of human brain microvascular endothelial cells. Brain Res 1147: 39-50.
189. Sidelmann JJ, Gram J, Jespersen J, Kluft C. 2000. Fibrin clot formation and lysis: basic mechanisms. Semin Thromb Hemost 26: 605-618.
190. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5: 146-156.
191. Sixt M, Engelhardt B, Pausch F, Hallmann R, Wendler O, Sorokin LM. 2001. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J Cell Biol 153: 933-946.
192. Smith MA, Hilgenberg LG. 2002. Agrin in the CNS: a protein in search of a function?. Neuroreport 13: 1485-1495.
193. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulsson M, Edgar D. 1999. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144: 151-160.
194. Sofroniew MV, Vinters HV. 2010. Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35.
195. Sorokin L, Girg W, Gopfert T, Hallmann R, Deutzmann R. 1994. Expression of novel 400-kDa laminin chains by mouse and bovine endothelial cells. Eur J Biochem 223: 603-610.
196. Stewart PA, Wiley MJ. 1981. Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev Biol 84: 183-192.
197. Stone DM, Nikolics K. 1995. Tissue- and age-specific expression patterns of alternatively spliced agrin mRNA transcripts in embryonic rat suggest novel developmental roles. J Neurosci 15: 6767-6778.
198. Stratman AN, Malotte KM, Mahan RD, Davis MJ, Davis GE. 2009. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 114: 5091-5101.
199. Sundberg C, Rubin K. 1996. Stimulation of beta1 integrins on fibroblasts induces PDGF independent tyrosine phosphorylation of PDGF beta-receptors. J Cell Biol 132: 741-752.
200. Tabrizi P, Wang L, Seeds N, McComb JG, Yamada S, Griffin JH, Carmeliet P, et al. 1999. Tissue plasminogen activator (tPA) deficiency exacerbates cerebrovascular fibrin deposition and brain injury in a murine stroke model: studies in tPA-deficient mice and wild-type mice on a matched genetic background. Arterioscler Thromb Vasc Biol 19: 2801-2806.
201. Tagaya M, Haring HP, Stuiver I, Wagner S, Abumiya T, Lucero J, Lee P, et al. 2001. Rapid loss of microvascular integrin expression during focal brain ischemia reflects neuron injury. J Cereb Blood Flow Metab 21: 835-846.
202. Tao-Cheng JH, Nagy Z, Brightman MW. 1987. Tight junctions of brain endothelium in vitro are enhanced by astroglia. J Neurosci 7: 3293-3299.
203. Tilling T, Engelbertz C, Decker S, Korte D, Huwel S, Galla HJ. 2002. Expression and adhesive properties of basement membrane proteins in cerebral capillary endothelial cell cultures. Cell Tissue Res 310: 19-29.
204. Tilling T, Korte D, Hoheisel D, Galla HJ. 1998. Basement membrane proteins influence brain capillary endothelial barrier function in vitro. J Neurochem 71: 1151-1157.
205. Ugarova TP, Lishko VK, Podolnikova NP, Okumura N, Merkulov SM, Yakubenko VP, Yee VC, et al. 2003. Sequence gamma 377-395(P2), but not gamma 190-202(P1), is the binding site for the alpha MI-domain of integrin alpha M beta 2 in the gamma C-domain of fibrinogen. Biochemistry 42: 9365-9373.
206. van Horssen J, Bo L, Vos CM, Virtanen I, de Vries HE. 2005. Basement membrane proteins in multiple sclerosis-associated inflammatory cuffs: potential role in influx and transport of leukocytes. J Neuropathol Exp Neurol 64: 722-729.
207. Vincent AJ, Lau PW, Roskams AJ. 2008. SPARC is expressed by macroglia and microglia in the developing and mature nervous system. Dev Dyn 237: 1449-1462.
208. Wagner S, Tagaya M, Koziol JA, Quaranta V, del Zoppo GJ. 1997. Rapid disruption of an astrocyte interaction with the extracellular matrix mediated by integrin alpha 6 beta 4 during focal cerebral ischemia/reperfusion. Stroke 28: 858-865.
209. Wang J, Milner R. 2006. Fibronectin promotes brain capillary endothelial cell survival and proliferation through alpha5beta1 and alphavbeta3 integrins via MAP kinase signalling. J Neurochem 96: 148-159.
210. Wang JF, Zhang XF, Groopman JE. 2001. Stimulation of beta 1 integrin induces tyrosine phosphorylation of vascular endothelial growth factor receptor-3 and modulates cell migration. J Biol Chem 276: 41950-41957.
211. Wang Q, Tang XN, Yenari MA. 2007. The inflammatory response in stroke. J Neuroimmunol 184: 53-68.
212. Wang S, Voisin MB, Larbi KY, Dangerfield J, Scheiermann C, Tran M, Maxwell PH, et al. 2006a. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med 203: 1519-1532.
213. Wang X, Lo EH. 2003. Triggers and mediators of hemorrhagic transformation in cerebral ischemia. Mol Neurobiol 28: 229-244.
214. Wang X, Louden C, Yue TL, Ellison JA, Barone FC, Solleveld HA, Feuerstein GZ. 1998a. Delayed expression of osteopontin after focal stroke in the rat. J Neurosci 18: 2075-2083.
215. Wang Y, Jin G, Miao H, Li JY, Usami S, Chien S. 2006b. Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras. Proc Natl Acad Sci U S A 103: 1774-1779.
216. Wang YF, Tsirka SE, Strickland S, Stieg PE, Soriano SG, Lipton SA. 1998b. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 4: 228-231.
217. Webersinke G, Bauer H, Amberger A, Zach O, Bauer HC. 1992. Comparison of gene expression of extracellular matrix molecules in brain microvascular endothelial cells and astrocytes. Biochem Biophys Res Commun 189: 877-884.
218. Wolburg H, Lippoldt A. 2002. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 38: 323-337.
219. Wolburg H, Noell S, Wolburg-Buchholz K, Mack A, Fallier-Becker P. 2009. Agrin, aquaporin-4, and astrocyte polarity as an important feature of the blood-brain barrier. Neuroscientist 15: 180-193.
220. Yamada KM, Even-Ram S. 2002. Integrin regulation of growth factor receptors. Nat Cell Biol 4: E75-76.
221. Yamagata K, Tagami M, Nara Y, Mitani M, Kubota A, Fujino H, Numano F, et al. 1997. Astrocyte-conditioned medium induces blood-brain barrier properties in endothelial cells. Clin Exp Pharmacol Physiol 24: 710-713.
222. Yamagata K, Tagami M, Takenaga F, Yamori Y, Itoh S. 2004. Hypoxia-induced changes in tight junction permeability of brain capillary endothelial cells are associated with IL-1beta and nitric oxide. Neurobiol Dis 17: 491-499.
223. Yang Z, Mochalkin I, Doolittle RF. 2000. A model of fibrin formation based on crystal structures of fibrinogen and fibrin fragments complexed with synthetic peptides. Proc Natl Acad Sci U S A 97: 14156-14161.
224. Yurchenco PD, Amenta PS, Patton BL. 2004. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol 22: 521-538.
225. Yurchenco PD, Patton BL. 2009. Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 15: 1277-1294.
226. Zaccaria ML, Di Tommaso F, Brancaccio A, Paggi P, Petrucci TC. 2001. Dystroglycan distribution in adult mouse brain: a light and electron microscopy study. Neuroscience 104: 311-324.
227. Zhang Y, Barres BA. 2010. Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 20: 588-594.
228. Zhang ZG, Chopp M, Goussev A, Lu D, Morris D, Tsang W, Powers C, et al. 1999. Cerebral microvascular obstruction by fibrin is associated with upregulation of PAI-1 acutely after onset of focal embolic ischemia in rats. J Neurosci 19: 10898-10907.
229. Zhu J, Motejlek K, Wang D, Zang K, Schmidt A, Reichardt LF. 2002. Beta8 integrins are required for vascular morphogenesis in mouse embryos. Development 129: 2891-2903.
230. Zlokovic BV. 2008. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201.