Inflammation in the CNS: Balance between immunological privilege and immune responses

Progress in Neurobiology

Volumn 56, Issue 1, 1998, Pages 19-35

  Matyszak, M K ^a  

^a CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD BRAIN BARRIER; CELLULAR IMMUNITY; ENCEPHALITIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

EID: 0031874792     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(98)00014-8     Document Type: Article

References (131)

1. Adams, C. W. (1989) A Colour Atlas of Multiple Sclerosis and Other Myelin Disorders. Wolfe Medical Publications Ltd.
2. Adams R. D., Kubik C. S. The morbid anatomy of the demyelinative diseases. Am. J. Med. 12:1952;510-546.
3. Akbar A. N., Salmon M. Cellular environment and apoptosis: tissue microenvironment control activated T-cell death. Immunol. Today. 18:1997;72-76.
4. Amor S., Baker D., Layward L., McCormack K., van Noort J. M. Multiple sclerosis: variations on a theme. Immunol. Today. 18:1997;368-371.
5. Andersson P-B., Perry V. H., Gordon S. The acute inflammatory response to lipopolysaccharide in CNS parenchyma differs from that in other body tissues. Neuroscience. 48:1992;169-186.
6. Anthony D. C., Bolton S. J., Fearn S., Perry V. H. Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain. 120:1997;435-444.
7. Arvin B., Neville L. F., Barone F. C., Feuerstein G. Z. The role of inflammation and cytokines in brain injury. Neurosci. Biobehav. Rev. 20:1996;445-452.
8. Austyn J. M. New insights into the mobilization and phagocytic activity of dendritic cells. J. Exp. Med. 183:1996;1287-1292.
9. Barns D., Munro P. M., Youl B. D., Prineas J. W., McDonald W. I. The long standing multiple sclerosis lesion. A quantitative MRI and electron microscopy study. Brain. 114:1991;1271-1280.
10. Baron J. L., Madri J. A., Ruddle N. H., Hashim G. H., Janeway J. C. A. Surface expression of α4 integrin by CD4 T cells is required for their entry into brain parenchyma. J. Exp. Med. 177:1993;57-68.
11. Bauer J., Sminia T., Wouterlood F. G., Dijkstra C. D. Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neurosci. Res. 38:1994;365-375.
12. Baggiolini M., Dewald B., Moser B. Human chemokines: an update. A. Rev. Immunol. 15:1997;675-705.
13. Bell M. D., Lopez G-R., Lawson L., Hughes D., Fraser I., Gordon S., Perry V. H. Upregulation of the macrophage scavenger receptor in response to different forms of injury in the CNS. J. Neurocytol. 23:1994;605-613.
14. Bell M. D., Perry V. H. Adhesion molecule expression on murine cerebral endothelium following the injection of a proinflammogen or during acute neuronal degeneration. J. Neurocytol. 24:1995;695-710.
15. Bell M. D., Taub D. D., Kunkel S. J., Strieter R. M., Foley R., Gauldie J., Perry V. H. Recombinant human adenovirus with rat MIP-2 gene insertion causes prolonged PMN recruitment to the murine brain. Eur. J. Neurosci. 8:1996;1803-1811.
16. Bell M. D., Taub D. D., Perry V. H. Overriding the brain's intrinsic resistance to leukocyte recruitment with intraparenchymal injections of recombinant chemokines. Neuroscience. 74:1996;283-292.
17. Ben-Baruch A., Michiel D. F., Oppenheim J. J. Signals and receptors involved in recruitment of inflammatory cells. J. Biol. Chem. 270:1995;11703-11706.
18. Betmouni S., Perry V. H., Gordon J. L. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience. 74:1996;1-5.
19. Bianchi E., Bender J. R., Blasi F., Pardi R. Through and beyond the wall: late steps in leukocyte transendothelial migration. Immunol. Today. 18:1997;586-591.
20. van oud Alblas Blusse A., van der Linden-Schrever B., van Furth R. Origin and kinetics of pulmonary macrophages during an inflammatory reaction induced by intra-alveolar administration of aerosolized heat-killed BCG. Am. Rev. Respir. Dis. 128:1983;276-281.
21. Brenan M., Puklavec M. The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an Integrin. J. Exp. Med. 175:1992;1457-1465.
22. Bruck W., Bitsch A., Kolenda H., Bruck Y., Stiefel M., Lassmann H. Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann. Neurol. 42:1997;783-793.
23. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 67:1991;1033-1036.
24. Butcher E. C., Picker L. J. Lymphocyte homing and homeostasis. Science. 272:1996;60-66.
25. Byrnes A. P., Rusby J. E., Wood M. J., Charlton H. M. Adenovirus gene transfer causes inflammation in the brain. Neuroscience. 66:1995;1015-1024.
26. Byrnes A. P., Wood M. J., Charlton H. M. Role of T cells in inflammation caused by adenovirus vectors in the brain. Gene Therapy. 3:1996;644-651.
27. Cash E., Zhang Y., Rott O. Microglia present myelin antigens to T cells after phagocytosis of oligodendrocytes. Cell. Immunol. 147:1993;129-138.
28. Cella M., Engering A., Pinet V., Pieters J., Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells [see comments]. Nature. 388:1997;782-787.
29. Chopp M., Zhang R. L., Chen H., Li Y., Jing N., Rusche J. R. Postischaemic administration of anti-Mac-1 antibody reduces ischaemic cell-damage after transient middle cerebral-artery occlusion in rats. Stroke. 25:1994;869-875.
30. Clark R. S. B., Schiding J. K., Kaczorowski S. L., Marion D. W., Kochanek P. M. Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J. Neurotrauma. 5:1994;499-506.
31. Cserr H. F., Knopf P. M. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunol. Today. 13:1992;507-512.
32. Cumberbatch M., Fielding I., Kimber I. Modulation of epidermal Langerhans cell frequency by tumour necrosis factor-α Immunology. 81:1994;395-401.
33. D'Souza S. D., Bonetti B., Balasingam V., Cashman N. R., Barker P. A., Troutt A. B., Raine C. S., Antel J. P. Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J. Exp. Med. 184:1996;2361-2370.
34. De Simone R., Giampaolo A., Giometto B., Gallo P., Levi G., Peschle C., Aloisi F. The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J. Neuropathol. Exp. Neurol. 54:1995;175-187.
35. Deckert-Schluter M., Schluter D., Hof H., Wiestler O. D., Lassmann H. Differential expression of ICAM-1, VCAM-1 and their ligands LFA-1, Mac-1, CD43, VLA-4, and MHC class II antigens in murine Toxoplasma encephalitis: a light microscopic and ultrastructural immunohistochemical study. J. Neuropathol. Exp. Neurol. 53:1994;457-468.
36. Deli M. A., Descamps L., Dehouck M. P., Ceccnelli R., Joo F., Abraham C., Torpier G. Exposure to tumour necrosis factor-α to luminal membrane of bovine brain capillary endothelial cells cultured with astrocytes induces a delayed increase of permeability and cytoplasmic stress fiber formation of actin. J. Neurosci. Res. 41:1995;717-726.
37. Dopp J. M., Breneman S. M., Olschowka J. A. Expression of ICAM-1, VCAM-1, L-selectin, and leukosialin in the mouse central nervous system during the induction and remission stages of experimental allergic encephalomyelitis. J. Neuroimmunol. 54:1994;129-144.
38. Dusart I., Schwab M. E. Secondary cell death and inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6:1994;712-724.
39. Eralinna J. P., Soilu-Hanninen M., Roytta M., Hukkanen V., Salmi A. A., Salonen R. Blood-brain barrier breakdown and increased intercellular adhesion molecule (ICAM-1/CD54) expression after Semliki Forest (A7) virus infection facilitates the development of experimental allergic encephalomyelitis. J. Neuroimmunol. 66:1996;103-114.
40. Ferguson B., Matyszak M. K., Esiri M. M., Perry V. H. Axonal damage in acute multiple sclerosis lesions. Brain. 120:1997;393-399.
41. Filippi M., Barker G. J., Horsfield M. A., Sacares P. R., MacManus D. G., Thompson A. J., Tofts P. S., McDonald W. I., Miller D. H. Benign and secondary progressive multiple sclerosis: a preliminary quantitative MRI study. J. Neurol. 241:1994;246-251.
42. Fischer H. G., Nitzgen B., Germann T., Degitz K., Daubener W., Hadding U. Differentiation driven by granulocyte-macrophage colony stimulating factor endows microglia with interferon-γ independent antigen presenting function. J. Neuroimmunol. 42:1993;87-96.
43. Ford A. L., Foulcher E., Lemckert F. A., Sedgwick J. D. Microglia induce CD4 T lymphocyte final effector function and death. J. Exp. Med. 184:1996;1737-1745.
44. Ford A. L., Goodsall A. L., Hickey W. F., Sedgwick J. D. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J. Immunol. 154:1995;4309-4321.
45. Frei K., Siepl C., Groscurth P., Bodmer S., Schwerdel C., Fontana A. Antigen presentation and tumour cytotoxicity by interferon-γ-treated microglia cells. Eur. J. Immunol. 17:1987;1271-1278.
46. Gentleman S. M., Nash M. J., Sweeting C. J., Graham D. I., Roberts G. W. Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci. Lett. 160:1993;139-144.
47. Gijbels K., Masure S., Carton H., Opdenakker G. Gelatinase in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J. Neuroimmunol. 41:1992;29-34.
48. Gijbels K., Proost P., Masure S., Carton H., Billiau A., Opdenakker G. Gelatinase B is present in the cerebrospinal fluid during experimental autoimmune encephalomyelitis and cleaves myelin basic protein. J. Neurosci. Res. 36:1993;432-440.
49. Gondelman H. E., Lipton S. E., Tardieu M., Bukrinsky M. I., Nottet H. S. L. M. The neuropathogenesis of HIV-1 infection. J. Leukoc. Biol. 56:1994;389-398.
50. Gregson N. A., Koblar S., Hughes R. A. Antibodies to gangliosides in Guillain-Barré syndrome: specificity and relationship to clinical features. Q. J. Med. 86:1993;111-117.
51. Gregson N. A., Rees J. N., Hughes R. A. Reactivity of serum IgG-GM1 antibodies with the lipopolysaccharide fractions of Campylobacter jejuni isolates from patients with Guillain-Barré syndrome. J. Neuroimmunol. 73:1997;28-36.
52. Griffith T. S., Brunner T., Fletcher S. M., Green D. R., Ferguson T. A. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science. 270:1995;1189-1192.
53. Harling-Berg C., Knopf P. M., Merriam J., Cserr H. F. Role of cervical lymph nodes in the systemic humoral immune response to human serum albumin microinfused into rat cerebrospinal fluid. J. Neuroimmunol. 25:1989;185-193.
54. Hart D. J., Fabre J. W. Demonstration and characterization of Ia-positive dendritic cells in the interstitial connective tissues of rat heart and other tissues but not brain. J. Exp. Med. 153:1981;347-361.
55. Havenith C. E. G., Breedijk A. J., Hoefsmit E. C. M. Effect of bacillus Calmette-Guerin inoculation on numbers of dendritic cells in bronchoalveolar lavages of rats. Immunobiology. 184:1992;336-347.
56. Hayes G. M., Woodroofe M. N., Cuzner M. L. Microglia are the major cell type expressing MHC class II in human white matter. J. Neurol. Sci. 80:1987;25-37.
57. Head J. R., Griffin W. S. Functional capacity of solid tissue transplants in the brain: evidence for immunological privilege. Proc. R. Soc. Lond. B. Biol. Sci. 224:1985;375-387.
58. Hickey W. F., Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science. 239:1988;290-292.
59. Hickey W. F., Hsu B. L., Kimura H. T-lymphocyte entry into the central nervous system. J. Neurosci. Res. 28:1991;254-260.
60. Hickey W. F., Vass K., Lassmann H. Bone marrow-derived elements in the central nervous system: an immunohistochemical and ultrastructural survey of rat chimeras. J. Neuropathol. Exp. Neurol. 51:1992;246-256.
61. Ibrahim M. A. A., Chain B. M., Katz D. R. The injured cell: the role of the dendritic cell system as a sentinel receptor pathway. Immunol. Today. 16:1995;181-186.
62. Inaba K., Witmer P-M., Inaba M., Hathcock K. S., Sakuta H., Azuma M., Yagita H., Okumura K., Linsley P. S., Ikehara S., Steinman R. The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J. Exp. Med. 180:1994;1849-1860.
63. Jiang W., Swiggard W. J., Heufler C., Peng M., Mirza A., Steinman R. M., Nussenzwieg M. C. The receptor DEC-205 expressed by dendritic cells is involved in antigen processing. Nature. 375:1995;151-155.
64. Klyushnenkova E. N., Vanguri P. Ia expression and antigen presentation by glia: strain and cell type-specific differences among rat astrocytes and microglia. J. Neuroimmunol. 79:1997;190-201.
65. Kogure K., Yamasaki Y., Matsuo Y., Kato H., Onodera H. Inflammation of the brain after ischaemia. Acta Neurochirurgica. 66:(Suppl.):1996;40-43.
66. Lassmann H., Brunner C., Bradl M., Linington C. Experimental allergic encephalomyelitis: the balance between encephalitogenic T lymphocytes and demyelinating antibodies determines size and structure of demyelinated lesions. Acta Neuropathol. (Berl.). 75:1988;566-576.
67. Lassmann H., Schmied M., Vass K., Hickey W. F. Bone marrow derived elements and resident microglia in brain inflammation. Glia. 7:1993;19-24.
68. Lawson L. J., Matyszak M. K., Perry V. H. Lessons from microglia in special sites. Clin. Neuropathol. 12:1993;310-313.
69. Lawson L. J., Perry V. H., Dri P., Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 39:1990;151-170.
70. Lawson L. J., Perry V. H., Gordon S. Turnover of resident microglia in the normal adult mouse brain. Neuroscience. 48:1992;405-415.
71. Low W. C., Lewis P. R., Terri S. T. Embryonic neural transplants across a major histocompatibility barrier: survival and specificity of innervation. Brain Res. 262:1983;328-333.
72. Lucchinetti C. F., Bruck W., Rodriguez M., Lassmann H. Distinct patterns of multiple sclerosis pathology indicates heterogeneity on pathogenesis. Brain Pathol. 6:1996;259-274.
73. Lutz M. B., Rovere P., Kleijmeer M. J., Rescigno M., Abmann C. U., Oorschot V. M. J., Geuze H. J., Trucy J., Demandolx D., Davoust J., Ricciardi-Castagnoli P. Intracellular routes and selective retention of antigens in mildly acidic cathepsin D/lysosome-associated membrane protein-1/MHC II - positive vesicles in immature dendritic cells. J. Immunol. 159:1997;3707-3716.
74. MacPherson G. G., Jenkins C. D., Stein M. J., Edwards C. Endotoxin-mediated dendritic cell release from the intestine. Characterization of released dendritic cells and TNF dependence. J. Immunol. 154:1995;1317-1322.
75. Male D., Pryce G., Hughes C., Lantos P. Lymphocyte migration into brain modelled in vitro: control by lymphocyte activation, cytokines and antigen. Cell. Immunol. 127:1990;1-11.
76. Mason D. W., Charlton H. M., Jones A. J., Lavy C. B., Puklavec M., Simmonds S. J. The fate of allogeneic and xenogeneic neuronal tissue transplanted into the third ventricle of rodents. Neuroscience. 19:1986;685-694.
77. Matsumoto Y., Ohmori K., Fujiwara M. Immune regulation by brain cells in the central nervous system: microglia but not astrocytes present myelin basic protein to encephalitogenic T cells under in vivo-mimicking conditions. Immunology. 76:1992;209-216.
78. Matyszak M. K., Lawson L. J., Perry V. H., Gordon S. Stromal macrophages of the choroid plexus situated at an interface between the brain and peripheral immune system constitutively express major histocompatibility class II antigens. J. Neuroimmunol. 40:1992;173-181.
79. Matyszak M. K., Perry V. H. Demyelination in the central nervous system following a delayed-type hypersensitivity response to bacillus Calmette-Guérin. Neuroscience. 64:1995;967-977.
80. Matyszak M. K., Perry V. H. A comparison of leucocyte responses to heat-killed bacillus Calmette-Guérin in different CNS compartments. Neuropathol. Appl. Neurobiol. 22:1996;44-53.
81. Matyszak M. K., Perry V. H. The potential role of dendritic cells in immune mediated inflammatory responses in the central nervous system. Neuroscience. 74:1996;599-608.
82. Matyszak M. K., Townsend M. J., Perry V. H. Ultrastructural studies of an immune-mediated inflammatory response in the CNS parenchyma directed against a non-CNS antigen. Neuroscience. 78:1997;549-560.
83. McDonald W. I. Rachelle Fishman-Matthew Moore Lecture. The pathological and clinical dynamics of multiple sclerosis. J. Neuropathol. Exp. Neurol. 53:1994;338-343.
84. McGeer P. L., Kawamata T., Walker D. G., Akiyama H., Tooyama I., McGeer E. G. Microglia in degenerative neurological disease. Glia. 7:1993;84-92.
85. McGeer P. L., Rogers J. Anti-inflammatory agents as a therapeutic approach to Alzheimer's Disease. Neurology. 42:1992;447-449.
86. Megyeri P., Abraham C. S., Temesvari P., Kovacs J., Vas T., Speer C. P. Recombinant human tumour necrosis factor alpha constricts pial arterioles and increases blood-brain barrier permeability in newborn piglets. Neurosci. Lett. 148:1992;137-140.
87. Metlay J. P., Witmer P-M. D., Agger R., Crowley M. T., Lawless D., Steinman R. M. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med. 171:1990;1753-1771.
88. Miller M. D., Krangel M. S. Biology and biochemistry of the chemokines - a family of chemotactic and inflammatory cytokines. Crit. Rev. Immunol. 12:1992;17-46.
89. Montero-Menei C. N., Sindji L., Pouplard B-A., Jehan F., Denechaud L., Darcy F. Lipopolysaccharide intracerebral administration induces minimal inflammatory reaction in rat brain. Brain Res. 653:1994;101-111.
90. Narayanan S., Fu L., Pioro E., De Stefano N., Collins D. L., Francis G. S., Antel J. P., Matthews P. M., Arnold D. L. Imaging of axonal damage in multiple sclerosis: spatial distribution of magnetic resonance imaging lesions. Ann. Neurol. 41:1997;385-391.
91. Pan Y., Lloyd C., Zhou H., Dolich S., Deeds J., Gonzalo J. A., Vath J., Gosselin M., Ma J., Dussault B., Woolf E., Alperin G., Culpepper J., Gutierrez-Ramos J. C., Gearing D. Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature. 387:1997;611-617.
92. Pelletier M., Forget A., Bourassa D., Gros P., Skamene E. Immunopathology of BCG infection in genetically resistant and susceptible mouse strains. J. Immunol. 129:1982;2179-2185.
93. Perry V. H., Gordon S. Macrophages and the nervous system. Int. Rev. Cytol. 125:1991;203-244.
94. Perry V. H., Andersson P-B., Gordon S. Macrophages and inflammation in the central nervous system. Trends Neurosci. 16:1993;268-273.
95. Perry V. H., Matyszak M. K., Fearn S. Altered antigen expression of microglia in the aged rodent CNS. Glia. 7:1993;60-67.
96. Proost P., Van D-J, Opdenakker G. Leukocyte gelatinase B cleavage releases encephalitogens from human myelin basic protein. Biochem. Biophys. Res. Commun. 192:1993;1175-1181.
97. Raine C. S., Cross A. H. Axonal dystrophy as a consequence of long-term demyelination. Lab. Invest. 60:1989;714-725.
98. Raine C. S. The Norton Lecture: a review of the oligodendrocyte in the multiple sclerosis lesion. J. Neuroimmunol. 77:1997;135-152.
99. Rees J. H., Gregson N. A., Griffiths P. L., Hughes R. A. Campylobacter jejuni and Guillain-Barré syndrome. Q. J. Med. 86:1993;623-634.
100. Rees J. H., Soudain S. E., Gregson N. A., Hughes R. A. Campylobacter jejuni and Guillain-Barré syndrome. New Engl. J. Med. 333:1995;1374-1379.
101. Roake J. A., Rao A. S., Morris P. J., Larsen C. P., Hankins D. F., Austyn J. M. Dendritic cell loss from non-lymphoid tissues after systemic administration of lipopolysaccharide, tumour necrosis factor, and interleukin 1. J. Exp. Med. 181:1995;2237-2247.
102. Rogers J., Webster S., Lue L. F., Brachova L., Civin W. H., Emmerling M., Shivers B., Walker D., McGeer P. Inflammation and Alzheimer's disease pathogenesis. Neurobiol. Aging. 17:1996;681-686.
103. Sallusto F., Cella M., Danieli C., Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products [see comments]. J. Exp. Med. 182:1995;389-400.
104. Schlosshauer B. The blood-brain barrier: morphology, molecules, and neurothelin. BioEssays. 15:1993;341-346.
105. Schluger N. W., Rom W. N. Early responses to infection: chemokines as mediators of inflammation. Curr. Opin. Immunol. 9:1997;504-508.
106. Selmaj K. W., Raine C. S. Tumour necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23:1988;339-346.
107. Shaw J. A., Perry V. H., Mellanby J. Tetanus toxin-induced seizures cause microglial activation in rat hippocampus. Neurosci. Lett. 120:1990;66-69.
108. Sherriff F. E., Bridges L. R., Gentleman S. M., Sivaloganathan S., Wilson S. Markers of axonal injury in post mortem human brain. Acta Neuropathol. (Berl.). 88:1994;433-439.
109. Sminia T., De Groot C. J. A., Dijkstra C. D., Koetsier J. C., Polman C. H. Macrophages in the central nervous system of the rat. Immunobiology. 174:1987;43-50.
110. Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 76:1994;301-314.
111. Steinman R. M. The dendritic cell system and its role in immunogenicity. A. Rev. Immunol. 9:1991;271-296.
112. Stevenson P. G., Hawke S., Bangham C. R. Protection against lethal infuenza-virus encephalitis by intranasally primed CD8(+) memory T cells. J. Immunol. 157:1996;3065-3073.
113. Stevenson P. G., Hawke S., Sloan D. J., Bangham C. R. The immunogenicity of intracerebral virus-infection depends on anatomical site. J. Virol. 71:1997;145-151.
114. Strieter R. M., Standiford T. J., Guffnagle G. B., Colletti L. M., Lukacs N. W., Kunkel S. L. "The good, the bad and the ugly". The role of chemokines in models of human disease. J. Immunol. 156:1996;3583-3586.
115. Taub D. D., Oppenheim J. J. Chemokines, inflammation and immune system. Ther. Immun. 1:1994;229-235.
116. Van Vugt E., Verdaasdonk M. A., Beelen R. H., Kamperdijk E. W. Induction of an increased number of dendritic cells in the peritoneal cavity of rats by intraperitoneal administration of Bacillus Calmette-Guerin. Immunobiol. 186:1992;230-240.
117. Vass K., Lassmann H., Wekerle H., Wisniewski H. M. The distribution of Ia antigen in the lesions of rat acute experimental allergic encephalomyelitis. Acta Neuropathol. 70:1986;149-160.
118. Walker W. S., Gatewood J., Olivas E., Askew D., Havenith C. E. Mouse microglia cell lines differing in constitutive and interferon-γ-inducible antigen presenting activities for naive and memory CD4+ and CD8+ T cells. J. Neuroimmunol. 63:1995;163-174.
119. Wekerle H., Sun D., Oropeza W-R. L., Meyermann R. Immune reactivity in the nervous system: modulation of T-lymphocyte activation by glial cells. J. Exp. Biol. 132:1987;43-57.
120. Weller R. O., Engelhardt B., Phillips M. J. Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol. 6:1996;275-288.
121. Williams A. E., Lawson L. J., Perry V. H., Fraser H. Characterization of the microglial response in murine scrapie. Neuropathol. Appl. Neurobiol. 20:1994;47-55.
122. Williams K., Ulvestad E., Antel J. P. B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur. J. Immunol. 24:1994;3031-3037.
123. Williams K. C., Dooley N. P., Ulvestad E., Waage A., Blain M., Yong V. W., Antel J. P. Antigen presentation by human fetal astrocytes with the cooperative effect of microglia or the microglial-derived cytokine IL-1. Neuroscience. 15:1995;1869-1878.
124. Winzler C., Rovere P., Rescigno M., Granucci F., Penna G., Adorini L., Zimmermann V. S., Davoust J., Ricciardi-Castagnoli P. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J. Exp. Med. 185:1997;317-328.
125. Wisniewski H. M., Bloom B. R. Primary demyelination as a nonspecific consequence of a cell-mediated immune reaction. J. Exp. Med. 141:1975;346-359.
126. Wood M. J., Charlton H. M., Wood K. J., Kajiwara K., Byrnes A. P. Immune responses to adenovirus vectors in the nervous system. Trends Neurosci. 19:1996;497-501.
127. Yednock T. A., Cannon C., Fritz L. C., Sanchez-Madrid F., Steinman L., Karin N. Prevention of experimental autoimmune encephalomyelitis by antibodies against α4β1 integrin. Nature. 356:1992;63-66.
128. Zhang E. T., Richards H. K., Kida S., Weller R. O. Directional and compartemtalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol. 83:1992;233-239.
129. Zhang R. L., Chopp M., Jiang N., Tang W. X., Prostak J., Manning A. M., Anderson D. C. Anti-intercellular adhesion molecule-1 antibody reduces ischaemic cell damage after transient but not permanent middle cerebral artery occlusion in the Wistar rat. Stroke. 26:1995;1438-1442; discussion 1443.
130. Zierhut M., Bieber T., Brocker E. B., Forrester J. V., Foster C. S., Streilein J. W. Immunology of the skin and the eye. Immunol. Today. 17:1996;448-450.
131. Zinkernagel R. M., Hengartner H. Antiviral immunity. Immunol. Today. 18:1997;258-260.