Sentries at the gate: Chemokines and the blood-brain barrier

Journal of NeuroVirology

Volumn 5, Issue 6, 1999, Pages 623-634

  Glabinski, Andrzej R ^a   Ransohoff, Richard M ^b  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

BBB; Chemotactic factors; Inflammation; Wounds and injuries

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE; CHEMOKINE RECEPTOR;

BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; NERVOUS SYSTEM INFLAMMATION; NERVOUS SYSTEM INJURY; PRIORITY JOURNAL; REVIEW;

EID: 0033378329     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.3109/13550289909021291     Document Type: Review

References (104)

1. Ahuja S, Gao J-L, Murphy P (1994). Chemokine receptors and molecular mimickry. Immunol Today 15: 281 - 287.
2. Ahuja S, Murphy P (1993). Molecular piracy of mammalian interleukin-8 receptor type B by herpesvirus saimiri. J Biol Chem 268: 20691 - 20694.
3. Andersson P-B, Perry VH, Gordon S (1992). Intracerebral injection of proinflammatory cytokines or leukocyte chemotaxins induces minimal myelomonocytic cell recruitment to the parenchyma of the central nervous system. J Exp Med 176: 255 - 259.
4. Andjelkovic AV, Spencer DD and Pachter JS (1999). Visualization of chemokine binding sites on human brain microvessels. J Cell Biol 145, 403 - 412.
5. Asensio VC, Campbell IL (1997). Chemokine gene expression in the brains of mice with lymphocytic choriomeningitis. J Virol 71: 7832 - 7840.
6. Asensio V, Kincaid C, Campbell I (1999). Chemokines and the inflammatory response to viral infection in the central nervous system with a focus on lymphocytic choriomeningitis virus. J Neurovirol 5: 65 - 75.
7. Balashov KE, Rottman JB, Weiner HL, Hancock WW (1999). CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-lalpha and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci USA 96, 6873 - 6878.
8. Barnes D, Huston M, Holmes R, Benveniste E, Yong V, Scholz P, Perez H (1996). Induction of RANTES expression by astrocytes and astrocytoma cell lines. J Neuroimmunol 71: 207 - 214.
9. Baron JL, Madri JA, Ruddle NH, Hashim G, Janeway CA (1993). Surface expression of alpha4 integrin by CD4 T cells is required for their entry into brain parenchyma. J Exp Med 177: 57 - 68.
10. Bartholdi D, Schwab ME (1997). Expression of proinflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci, 9: 1422 - 1438.
11. Bell MD, Taub DD, Perry VH (1996). Overriding the brain's intrinsic resistance to leukocyte recruitment with intraparenchymal injections of recombinant chemokines. Neuroscience 74: 283 - 292.
12. Berman J, Guida M, Warren J, Amat J, Brosnan C (1996). Localization of monocyte chemoattractant peptide-1 expression on the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat. J Immunol 156: 3017 - 3023.
13. Bolton SJ, Anthony DC, Perry VH (1998). Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience 86: 1245 - 1257.
14. Bourdoulous S, Bensaid A, Martinez D, Sheikboudou C, Trap I, Strosberg A, Couraud P (1995). Infection of bovine brain microvessel endothelial cells with Cowdria ruminantium elicits IL-1 beta, -6 and -8 mRNA production and expression of an unusual MHC class II DQ alpha transcript. J Immunol 154: 4032 - 4038.
15. Brosnan C, Bornstein M, Bloom B (1981). The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J Immunol 126: 614 - 620.
16. Charles P, Chen X, Horwitz M, Brosnan C (1999). Differential chemokine induction by the mouse adenovirus type-1 in the central nervous system of susceptible and resistant strains of mice. J Neurovirol 5: 55 - 64.
17. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO (1998). Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation n AIDS dementia. Proc Natl Acad Sci USA, 95, 3117 - 3121.
18. Cross AH, Cannella B, Brosnan CF, Raine CS (1990). Homing to central nervous system vascula ure by antigen-specific lymphocytes. I. Localization of 14C-labeled cells during acute, chronic, and relapsing experimental allergic encophalomyelitis. Lat Invest 63: 162 - 170.
19. Diamond M, Parkos C, Quinn M, Springer T. (1995). Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD18). J Cell Biol 130: 1473 - 1482.
20. Ehrlich L, Hu S, Sheng W, Sutton R, Rockswold G, Peterson P, Chao C. (1998). Cytokine regulation of human microglial cell IL-8 production. J Immunol 160: 1944 - 1948.
21. Fuentes M, Durham S, Swerdel M, Lewin A, Barton D, Megill J, Bravo R, Lira S (1995). Controlled recruitment of monocytes/macrophages to specific organs via transgenic expression of MCPÒ1. J Immunol 155: 5769 - 5776.
22. Gaetani P, Tartara F, Pignatti P, Tancioni F, Rodriquez Y, Baena R, De Benedetti F (1998). Cisternal CSF levels of cytokines after subarachnoid hemorrhage. Neurol Res 20: 337 - 342.
23. Ghirnikar R, Lee Y, He T, Eng L (1996). Chemokine expression in rat stab wound brain injury. J Neurosci Res 46: 727 - 733.
24. Ghirnikar R, Lee Y, Li J, Eng L (1998). Chemokine inhibition in rat stab wound brain injury using antisense oligodeoxynucleotides. Neurosci Lett 247: 21 - 24.
25. Gilat D, Hershkoviz R, Mekori Y, Vlodavsky I, Lider O (1994). Regulation of adhesion of CD4+ T lymphocytes to intact or heparinase-treated subendothelial extracellular matrix by diffusible or anchored RANTES and MIP-1 beta. J Immunol 153: 4899 - 4906.
26. Glabinski A, Krakowski M, Han Y, Owens T, Ransohoff R (1999). Chemokine expression in GKO mice (lacking interferon-gamma) with experimental autoimmune encephalomyelitis. J Neurovirol 5: 95 - 101.
27. Glabinski A, Tani M, Aras S, Stoler M, Tuohy V, Ransohoff R (1995a). Regulation and function of central nervous system chemokines. International J Dev Neurosci 13: 153 - 165.
28. Glabinski A, Tani M, Balasingam V, Yong VW, Ransohoff RM (1996). Chemokine monocyte chemoattractant protein-1 (MCP-1) is expressed by astrocytes after mechanical injury to the brain. J Immunol 156: 4363 - 4368.
29. Glabinski A, Tani M, Strieter R, Tuohy V, Ransohoff R (1997). Synchronous synthesis of a- and b-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of experimental autoimmune encephalomyelitis. Am J Pathol 150: 617 - 630.
30. Glabinski A, Tani M, Tuohy VK, Tuthill R, Ransohoff RM (1995b). Central nervous system chemokine gene expression follows leukocyte entry in acute murine experimental autoimmune encephalomyelitis. Brain Behav Immun 9, 315 - 330.
31. Glabinski A, Tuohy V, Ransohoff R (1998). Expression of chemokines RANTES, MIP-1 alpha and GRO-alpha correlates with inflammation in acute experimental autoimmune encephalomyelitis. Neuroimmunomodulation 5: 166 - 171.
32. Godiska R, Chantry D, Dietsch G, Gray P (1995). Chemokine expression in murine experimental autoimmune encephalomyelitis. J Neuroimmunol 58: 167 - 176.
33. Gourmala NG, Buttini M, Limonta S, Sauter A, Boddeke HW (1997). Differential and time-dependent expression of monocyte chemoattractant protein-1 mRNA by astrocytes and macrophages in rat brain: effects of ischemia and peripheral lipopolysaccharide administration. J Neuroimmunol 74: 35 - 44.
34. Grzybicki D, Moore S, Schelper R, Glabinski A, Ransohoff R, Murphy S (1998). Expression of monocyte chemoattractant protein (MCP-1) and nitric oxide synthase-2 following cerebral trauma. Acta Neuropathol 95: 98 - 103.
35. Guo H, Jin Y, Ishikawa M, Huang Y, van der Meide P, Link H, Xiao B (1998). Regulation of beta-chemokine mRNA expression in adult rat astrocytes by lipopolysaccharide, proinflammatory and immunoregulatory cytokines. Scand J Immunol 48: 502 - 508.
36. Halford W, Gebhardt B, Carr D (1996). Persistent cytokine expression in trigeminal ganglion latently infected with herpes simplex virus type 1. J Immunol 157: 3542 - 3549.
37. Hausmann E, Berman N, Wang Y-Y, Meara J, Wood G, Klein R (1998). Selective chemokine mRNA expression following brain injury. Brain Res 788, 49 - 59.
38. Hayashi M, Luo Y, Laning J, Strieter RM, Dorf ME (1995). Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J Neuroimmunol 60: 143 - 150.
39. Hickey WF, Hsu BL, Kimura H (1991). T-lymphocyte entry into the central nervous system. J Neurosci Res 28: 254 - 260.
40. Huffnagle G, McNeil L (1999). Dissemination of C. neoformans to the central nervous system: role of chemokines, Th1 immunity and leukocyte recruitment. J Neurovirol 5: 76 - 81.
41. Hulkower K, Brosnan CF, Aquino DA, Gammer W, Kulshcrestha S, Guida MP, Rapoport DA, Berman JW (1993). Expression of CSF-1, c-fms and MCP-1 in the central nervous system of rats with experimental allergic encephalomyelitis. J Immunol 150: 2525 - 2533.
42. Hvas J, McLean C, Justesen J, Kannourakis G, Steinman L, Oksenberg J, Bernard C (1997). Perivascular T cells express the proinflammatory chemokine RANTES mRNA in multiple sclerosis lesions. Scand J Immunol 46: 195 - 203.
43. Ivacko J, Szaflarski J, Malinak C, Flory C, Warren J, Silverstein F (1997). Hypoxic-ischemic injury induces monocyte chemoattractant protein-1 expression in neonatal rat brain. J Cereb Blood Flow Metab 17: 759 - 770.
44. Jiang Y, Salafranca M, Adhikari S, Xia Y, Feng L, Sonntag M, deFiebre C, Pennell N, Streit W, Harrison J (1998). Chemokine receptor expression in cultured glia and rat experimental allergic encephalomyelitis. J Neuroimmunol 86: 1 - 12.
45. Johansson BB (1990). The physiology of the blood-brain barrier. In: Circulating regulatory factors and neuroendocrine function. Porter JC, Jezova D (eds). Plenum Press: New York. pp. 25 - 39.
46. Karin N, Szafer F, Mitchell D, Gold D, Steinman L (1993). Selective and nonselective stages in homing of T lymphocytes to the central nervous system during experimental allergic encephalomyelitis. J Immunol 150: 4116 - 4124.
47. Karpus W, Ransohoff R (1998). Commentary: Chemokine regulation of experimental autoimmune encephalomyelitis: temporal and spatial expression patterns govern disease pathogenesis. J Immunol 161: 2667 - 2671.
48. Karpus WJ, Kennedy KJ (1997). MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J Leukoc Biol 62: 681 - 687.
49. Karpus WJ, Lukacs NW, McRae BL, Strieter RM, Kunkel SL, Miller SD (1995). An important role for the chemokine macrophage inflammatory protein-1α in the pathogenesis of the T cell -mediated autoimmune disease, experimental autoimmune encephalomyelitis. J Immunol 155: 5003 - 5010.
50. Kennedy K, Stieter R, Kunkel S, Lukacs N, Karpus W (1998). Acute and relapsing experimental autoimmune encephalomyelitis are regulated by differential expression of the CC chemokines macrophage inflammatory protein-1 and monocyte chemotactic protein 1. J Neuroimmunol 92: 98 - 108.
51. Kim JS, Gautam SC, Chopp M, Zaloga C, Jones ML, Ward PA, Wellch KMA (1995). Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J Neuroimmunol 56: 127 - 134.
52. Kossmann T, Stahel PF, Lenzlinger PM, Redl H, Dubs RW, Trentz O, Schlag G, Morganti-Kossmann MC (1997). Interleukin-8 released into the cerebrospinal fluid after brain injury is associated with blood-brain barrier dysfunction and nerve growth factor production. J Cereb Blood Flow Metab 17: 280 - 289.
53. Kuchroo VK, Martin CA, Greer JM, Ju S-T, Sobel RA, Dorf ME (1993). Cytokines and adhesion molecules contribute to the ability of myelin proteolipid protein-specific T cell clones to mediate experimental allergic encephalomyelitis. J Immunol 151: 4371 - 4382.
54. Lane T, Asensio V, Yu N, Paoletti A, Campbell I, Buchmeier M (1998). Dynamic regulation of alpha-and beta-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J Immunol 160: 970 - 978.
55. Lipovsky M, Gekker G, Hu S, Erhrlich L, Hoepelman A, Peterson P (1998). Cryptococcal glucuronoxylomannan induces interleukin (IL)-8 production by human microglia but inhibits neutrophil migration toward IL-8. J Infect Dis 177: 260 - 263.
56. Lin T, Young PR, McDonnell PC, White RF, Barone FC, Feuerstein GZ (1993). Cytokine-induced neutrophil chemoattractant mRNA expressed in cerebral ischemia. Neurosci Lett 164: 125 - 128.
57. Lopez-Cortes LF, Cruz-Ruiz M, Gomez-Mateos J, Viciana-Fernandez P, Martinez-Marcos FJ, Pachon J (1995). Interleukin-8 in cerebrospinal fluid from patients with meningitis of different etiologies: Its possible role as neutrophil chemotactic factor. J Infect Dis 172: 581 - 584.
58. Luster F (1998). Chemokines-chemotactic cytokines that mediate inflammation. New Engl J Med 338: 436 - 445.
59. Male D, Pryce G, Hughes C, Lantos P (1990). Lymphocyte migration into brain modelled in vitro: Controlled by lymphocyte activation, cytokines, and antigen. Cell Immunol 127: 1 - 11.
60. Matsumoto T, Ikeda K, Mukaida N, Harada A, Matsumoto Y, Yamashita J, Matsushima K (1997). Prevention of cerebral edema and infarct in cerebral reperfusion injury by an antibody to interleukin-8. Lab Invest 77: 119 - 125.
61. McManus C, Berman J, Brett F, Staunton H, Farrell M, Brosnan C (1998a). MCP-1, MCP-2 and MCP-3 expression in multiple sclerosis lesions: an immunohistochemical and in situ hybridization study. J Neuroimmunol 86: 20 - 29.
62. McManus C, Brosnan C, Berman J (1998b). Cytokine induction of MIP-1 alpha and MIP-1 beta in human fetal microglia. J Immunol 160: 1449 - 1455.
63. Mehta P, Bruccoleri A, Brown H, Harry G (1998). Increase in brain stem cytokine mRNA levels as an early response to chemical-induced myelin edema. J Neuroimmunol 88: 154 - 164.
64. Middleton J, Neil S, Wintle J, Clark-Lewis I, Moore H, Lam C, Auer M, Hub E, Rot A (1997). Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91: 385 - 395.
65. Miyagishi R, Kikuchi S, Fukazawa T, Tashiro K (1995). Macrophage inflammatory protein-la in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological diseases. J Neurol Sci 129: 223 - 227.
66. Miyagishi R, Kikuchi S, Takayama C, Inoue Y, Tashiro K. (1997). Identification of cell types producing RANTES, MIP-1α and MIP-1β in rat experimental autoimmune encephalomyelitis by in situ hybridization. J Neuroimmunol. 77: 17 - 26.
67. Miyamoto Y, Kim S (1999). Cytokine-induced production of macrophage inflammatory protein-1 alpha (MIP-1 alpha) in cultured human astrocytes. J Neurosci Res 55: 245 - 251.
68. Morita M, Kasahara T, Mukaida N, Matsushima K, Nagashima T, Nishizawa M, Yoshida M (1993). Induction and regulation of IL-8 and MCAF production in human brain tumor cell lines and brain tumor tissues. Eur Cytokine Netw 4: 351 - 358.
69. Nitta T, Allegretta M, Okumura K, Sato K, Steinman L (1992). Neoplastic and reactive human astrocytes express interleukin-8 gene. Neurosurgical Review 15, 203 - 207.
70. Norgard-Sumnicht K, Varki N, Varki A (1993). Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science 261: 480 - 483.
71. Oh J, Schwiebert L, Benveniste E (1999). Cytokine regulation of CC and CXC chemokine expression by human astrocytes. J Neurovirol 5: 82 - 94.
72. Pan Y, Lloyd C, Zhou H, Dolich S, Deeds J, Gonzalo JA, Vath J, Gosselin M, Ma J, Dussault B, Woolf E, Alperin G, Culpepper J, Gutierrez-Ramos JC, Gearing D (1997). Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature 387: 611 - 617.
73. Peterson PK, Hu S, Salak-Johnson J, Molitor TW, Chao CC (1997). Differential production of and migratory response to beta chemokines by human microglia and astrocytes. J Infect Dis 175: 478 - 481.
74. Randolph G, Furie M (1995). A soluble gradient of endogenous monocyte chemoattractant protein-1 promotes the transendothelial migration of monocytes in vitro. J Immunol 155: 3610 - 3618.
75. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, Estes ML, Thomas DM, Tuohy VK (1993). Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 7: 592 - 602.
76. Rollins BJ (1997). Chemokines. Blood 90: 909 - 928.
77. Romson J, Hook B, Kunkel S, Abrams G, Schork M, Lucchesi B (1983). Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 67: 1016 - 1023.
78. Rot A (1992). Binding of neutrophil attractant/activation protein-1 (interleukin-8) to resident dermal cells. Cytokine 4: 347 - 352.
79. Sanders V, Pittman C, White M, Wang G, Wiley C, Achim C (1998). Chemokines and receptors in HIV encephalitis. AIDS 12: 1021 - 1026.
80. Sasseville VG, Smith MM, Mackay CR, Pauley DR, Mansfield KG, Ringler DJ, Lackner AA (1996). Chemokine expression in simian immunodeficiency virus-induced AIDS encephalitis. Am J Pathol 149: 1459 - 1467.
81. Saukkonen K, Sande S, Cioffe C, Wolpe S, Sherry B, Cerami A, Tuomanen E (1990). The role of cytokines in the generation of inflammation and tissue damage in experimental gram-positive meningitis. J Exp Med 171: 439 - 448.
82. Seebach J, Bartholdi D, Frei K, Spanaus KS, Ferrero E, Widmer U, Isenmann S, Strieter RM, Schwab M, Pfister H, Fontana A (1995). Experimental Listeria meningoencephalitis. Macrophage inflammatory protein-1 alpha and -2 are produced intrathecally and mediate chemotactic activity in cerebrospinal fluid of infected mice. J Immunol 155: 4367 - 4375.
83. Selmaj K (1996). Pathophysiology of the blood-brain barrier. Springer Semin Immunopathol 18: 57 - 73.
84. Sharief MK, Ciardi M, Thompson EJ (1992). Blood-brain barrier damage in patients with bacterial meningitis: Association with tumor necrosis factor-alpha but not interleukin-1 beta. J Infect Dis 166: 350 - 358.
85. Simpson J, Newcombe J, Cuzner M, Woodroofe M (1998). Expression of monocyte chemoattractant protein-1 and other beta-chemokines by resident glia and inflammatory cells in multiple sclerosis lesions. J Neurorimmunol 84: 238 - 249.
86. Sørensen T, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik V, Qin S, Rottman J, Sellebjerg F, Strieter R, Frederiksen J, Ransohoff R (1999). Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 106, 807 - 815.
87. Spanaus KS, Nadal D, Pfister HW, Seebach J, Widmer U, Frei K, Gloor S, Fontana A (1997). C-X-C and C-C chemokines are expressed in the cerebrospinal fluid in bacterial meningitis and mediate chemotactic activity on peripheral blood-derived polymorphonuclear and mononuclear cells in vitro. J Immunol 158: 1956 - 1964.
88. Sprenger H, Rosler A, Tonn P, Braune JH, Huffmann G, Gemsa D (1996). Chemokines in the cerebrospinal fluid of patients with meningitis. Clin Immunol Immunopathol 80: 155 - 161.
89. Springer TA (1994). Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76: 301 - 314.
90. Sun D, Hu X, Liu X, Whitaker JN, Walker WS (1997). Expression of chemokine genes in rat glial cells: the effect of myelin basic protein-reactive encephalitogenic T cells. J Neurosci Res 48: 192 - 200.
91. Takami S, Nishikawa H, Minami M, Nishiyori A, Sato M, Akaike A, Satoh M (1997). Induction of macrophage inflammatory protein MIP-1 alpha mRNA on glial cells after focal cerebral ischemia in the rat. Neurosci Lett 227: 173 - 176.
92. Tanaka Y, Adams D, Shaw S (1993). Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes. Immunol Today 14: 111 - 115.
93. Tani M, Fuentes ME, Peterson JW, Trapp BD, Durham SK, Loy JK, Bravo R, Ransohoff RM, Lira SA (1996b). Neutrophil infiltration, glial reaction and neurological disease in transgenic mice expressing the chemokine N51/KC in oligodendrocytes. J Clin Invest 98: 529 - 539.
94. Tani M, Glabinski AR, Tuohy VK, Stoler MH, Estes ML, Ransohoff RM (1996a) In situ hybridization analysis of glial fibrillary acidic protein mRNA reveals evidence of biphasic astrocyte activation during acute experimental autoimmune encephalomyelitis. Am J Pathol 148: 889 - 896.
95. Tani M, Ransohoff RM. (1994). Do cytokines mediate inflammatory cell invasion of the central nervous system parenchyma? Brain Pathol, 4: 135 - 143.
96. Tipold A, Moore P, Zurbriggen A, Burgener I, Barben G, Vandevelde M (1999). Early T cell response in the central nervous system in canine distemper virus infection. Acta Neuropathol 97: 45 - 56.
97. Wang X, Yue T-L, Barone FC, Feuerstein GZ (1995). Monocyte chemoattractant protein-1 messenger RNA expression in rat ischemic cortex. Stroke 26: 661 - 666.
98. Weiss J, Downie S, Lyman W, Berman J (1998). Astrocyte-derived monocyte-chemoattractant protein-1 directs the transmigration of leukocytes across a model of the human blood-brain barrier. J Immunol 161: 6896 - 6903.
99. Wekerle H, Linnington C, Lassmann H, Meyermann R (1986). Cellular immune reactivity within the CNS. Trends Neurosci 9: 271 - 277.
100. Yamasaki Y, Matsuo Y, Matsuura N, Onodera H, Itoyama Y, Kogure K (1995). Transient increase of cytokineinduced neutrophil chemoattractant, a member of the interleukin-8 family, in ischemic brain areas after focal ischemia in rats. Stroke 26: 318 - 323.
101. Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, Karin N (1992). Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha4beta1 integrin. Nature 356: 63 - 66.
102. Yoshimoto T, Houkin K, Tada M, Abe H (1997). Induction of cytokines, chemokines and adhesion molecule mRNA in a rat forebrain reperfusion model. Acta Neuropathol 93: 154 - 158.
103. Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ (1989). Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med 169: 1449 - 1459.
104. Zach O, Bauer HC, Richter K, Webersinke G, Tontsch S, Bauer H (1997). Expression of a chemotactic cytokine (MCP-1) in cerebral capillary endothelial cells in vitro. Endothelium 5: 143 - 153.