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5 : Experimental Infection: Pathogenesis of Neurobehavioral Disease

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Abstract:

Even though findings obtained from experimental Borna disease virus (BDV) infection of other species gave many insights into species-specific pathogenic processes, BDV infection of the rat is the most common model for studying the pathogenesis of Borna disease (BD). In infections in which MHC class II-restricted cytotoxic T-cell activity was elicited in vitro, there has been no direct evidence for in vivo antiviral effector cell lysis. Thus, it was interesting that initial reports suggested that CD4 cells played the major role in the immunopathogenesis of BDV. Investigations of experimental adult BDV infection in other species replicated findings from the rat model and extended one's understanding of the pathogenesis of BD. Viral infections of the central nervous system (CNS) are a significant cause of congenital disease in newborns. Moreover, many neuropsychiatric disorders of children, such as autism, may result from early brain injury during critical periods of pre- or postnatal brain development. The hippocampal formation, especially neurons of the CA3 and CA4 areas, is one of the first targets of neonatal BDV infection. Damage to the cerebellum has also been observed in other perinatal virus infections, including lymphocytic choriomeningitis virus, rubella, mumps, rat parvovirus, or reovirus type III. The study of the pathogenesis of neurological diseases caused by BDV infection is a formidable challenge. Importantly, during the asymptomatic phase of the disease, the virus replication was predominantly detected in the cerebral cortex and hippocampus.

Citation: Pletnikov M, Gonzalez-Dunia D, Stitz L. 2002. Experimental Infection: Pathogenesis of Neurobehavioral Disease, p 125-178. In Carbone K (ed), Borna Disease Virus and Its Role in Neurobehavioral Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817909.ch5
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Figures

Image of Figure 1.
Figure 1.

Cortical brain atrophy as a consequence of BDV infection in rats. Note the profound atrophy of the brain parenchyma and hydrocephalus ex vacuo (*) in the BDV-infected rat (A) compared to the intact brain parenchyma in the sham-inoculated rat (B). Original magnification, ×30 (present magnification, ×20). Hematoxylin-and-eosin staining was used. Courtesy of Thomas Bilzer.

Citation: Pletnikov M, Gonzalez-Dunia D, Stitz L. 2002. Experimental Infection: Pathogenesis of Neurobehavioral Disease, p 125-178. In Carbone K (ed), Borna Disease Virus and Its Role in Neurobehavioral Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817909.ch5
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Image of Figure 2.
Figure 2.

Obese (left) and nonobese (right) rats infected with BDV as adults.

Citation: Pletnikov M, Gonzalez-Dunia D, Stitz L. 2002. Experimental Infection: Pathogenesis of Neurobehavioral Disease, p 125-178. In Carbone K (ed), Borna Disease Virus and Its Role in Neurobehavioral Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817909.ch5
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Image of Figure 3.
Figure 3.

BDV antigen expression in PCs of the cerebellum at day 10 p.i. immunostaining of BDV nucleoprotein in sham-inoculated (A) and neonatally BDV-infected (B) Lewis rats. Note the expression of BDV antigen in many PCs in a BDV-infected rat (arrow). Original magnification, ×100 (present magnification, ×70). Courtesy of Aymeric Hans, Unité des virus lents, Institut Pasteur, Paris, France.

Citation: Pletnikov M, Gonzalez-Dunia D, Stitz L. 2002. Experimental Infection: Pathogenesis of Neurobehavioral Disease, p 125-178. In Carbone K (ed), Borna Disease Virus and Its Role in Neurobehavioral Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817909.ch5
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Image of Figure 4.
Figure 4.

Degeneration of the DG of the hippocampus in neonatally BDV-infected rats at day 30 p.i. (A) Sham-inoculated rat; (B) BDV-infected rat. Note the disappearance of DG in the BDV-infected rat (arrowhead) compared to control DG. Hematoxylin and eosin staining was used. Original magnification, ×100 (present magnification, ×80).

Citation: Pletnikov M, Gonzalez-Dunia D, Stitz L. 2002. Experimental Infection: Pathogenesis of Neurobehavioral Disease, p 125-178. In Carbone K (ed), Borna Disease Virus and Its Role in Neurobehavioral Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817909.ch5
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Image of Figure 5.
Figure 5.

Hypoplasia of the cerebellum following neonatal BDV infection at day 30 p.i. Shown are representative sagittal sections of the cerebellum of a sham-inoculated rat (A) and a BDV-infected rat (B). Hematoxylin and eosin staining was used. Original magnification, ×12.5 (present magnification, ×8).

Citation: Pletnikov M, Gonzalez-Dunia D, Stitz L. 2002. Experimental Infection: Pathogenesis of Neurobehavioral Disease, p 125-178. In Carbone K (ed), Borna Disease Virus and Its Role in Neurobehavioral Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817909.ch5
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References

/content/book/10.1128/9781555817909.chap5
1. Allan, J. E.,, and P. C. Doherty. 1985. Immune T cells can protect or induce fatal neurological disease in murine lymphocytic choriomeningitis. Cell. Immunol. 90:401407.
2. Altman, J.,, and K. Sudarshan. 1975. Postnatal development of locomotion in the laboratory rat. Anim. Behav. 23:896920.
3. Ando, K.,, T. Moriyama,, L. G. Guidott,, S. Wirth,, R. D. Schreiber,, and H. J. Schlicht. 1993. Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J. Exp. Med. 178:15411554.
4. Anzil, A.,, K. Blinzinger,, K. and A. Mayr. 1973. Persistent Borna virus infection in adult hamsters. Arch. Gesamt. Virusforsch. 40:5257.
5. Asensio, V. C.,, and I. L. Campbell. 1999. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci. 22:504512.
6. Ashman, R. B.,, and A. A. Müllbacher. 1979. T helper cell for anti-viral cytotoxic T cell responses. J. Exp. Med. 150:12771282.
7. Autenrieth, C. F. 1823 . Ueber die hitzige Kopf-Krankheit der Pferde. Auf Verlangen des Münsinger Vereins zur Beförderung der Pferdezucht auf der Alb und zunächst fuer diese Gegend. Bey Heinrich Laupp, Tübingen, Germany.
8. Baenziger, J.,, H. Hengartner,, R. M. Zinkernagel,, and G. A. Cole. 1986. Induction or prevention of immunopathological disease by cloned cytotoxic T cell lines specific for lymphocytic choriomeningitis virus. Eur. J. Immunol. 16:387393.
9. Bautista, J. R.,, S. A. Rubin,, T. H. Moran,, G. J. Schwartz,, and K. M. Carbone. 1995. Developmental injury to the cerebellum following perinatal Borna disease virus infection. Dev. Brain Res. 90:4553.
10. Bautista, J. R.,, G. J. Schwartz,, J. C. de la torre,, T. H. Moran,, and K. M. Carbone. 1994. Early and persistent abnormalities in rats with neonatally acquired Borna disease virus infection. Brain Res. Bull. 34:3136.
11. Becher, B.,, A. Prat and J. P. Antel. 2000. Brain-immune connection: immuno-regulatory properties of CNS-resident Cells. Glia 29:293304.
12. Bennink, J. R.,, and P. C. Doherty. 1978. Different rules govern help for cytotoxic T cells and B cells. Nature 276:829831.
13. Billaud, J. N.,, C. Ly,, T. R. Phillips,, and J. C. de la torre. 2000. Borna disease virus persistence causes inhibition of glutamate uptake by feline primary cortical astrocytes. J. Virol. 74:1043810446.
14. Bilzer, T.,, O. Planz,, W. I. Lipkin,, L. Stitz. 1995. Presence of CD4+ and CD8+ T cells and expression of MHC class I and MHC class II antigen in horses with Borna disease virus-induced encephalitis. Brain Pathol. 5:223230.
15. Bilzer, T.,, and L. Stitz. 1993. Brain cell lesions in Borna disease are mediated by T cells. Arch. Virol. Suppl. 7:153158.
16. Bilzer, T.,, and L. Stitz. 1994. Immune-mediated brain atrophy. CD8+T cells contribute to tissue destruction during borna disease. J. Immunol. 153:818823.
17. Bray, G. A.,, and D. A. York. 1979. Hypothalamic and genetic obesity in experimental animals. Physiol. Rev. 59:719803.
18. Briese, T.,, M. Hornig,, and W. I. Lipkin. 1999. Bornavirus immunopathogenesis in rodents: models for human neurological diseases. J. Neurovirol. 5:604612.
19. Browning, M.,, C. S. Reiss,, and A. S. Huang. 1990a. The soluble viral glycoprotein of vesicular stomatitis virus efficiently sensitizes target cells for lysis by CD4+ T lymphocytes. J. Virol. 64:38103816.
20. Browning, M. J.,, A. S. Huang,, and C. S. Reiss. 1990b. Cytolytic T lymphocytes from the BALB/c-H-2dm2 mouse recognize the vesicular stomatitis virus glycoprotein and are restricted by class II MHC antigens. J. Immunol. 145:985994.
21. Bruce-Keller, A. 1999. Microglial-neuronal Interactions in synaptic damage and recovery. J. Neurosci. Res. 58:191201.
22. Byrne, J. A.,, and M. B. Oldstone. 1984. Biology of cloned cytotoxic T lymphocytes specific for lymphocytic choriomeningitis virus: clearance of virus in vivo. J. Virol. 51:682686.
23. Cambell, I. L. 1991. Cytokines in viral diseases. Curr. Opin. Immunol. 3:486491.
24. Caplazi, P.,, A. Waldvogel,, L. Stitz,, U. Braun,, and F. Ehrensperger. 1994. Borna disease in naturally infected cattle. J. Comp. Pathol. 111:6572.
25. Carbone, K.,, and M. Pletnikov. 2000. Borna again, starting from the beginning. Mol. Psychiatry 5:577.
26. Carbone, K. M.,, C. S. Duchala,, J. W. Griffin,, A. L. Kincaid,, and O. Narayan. 1987. Pathogenesis of Borna disease in rats: evidence that intra-axonal spread is the major route for virus dissemination and the determinant for disease incubation. J. Virol. 61:34313440.
27. Carbone, K. M.,, T. R. Moench,, and W. I. Lipkin. 1991a. Borna disease virus replicates in astrocytes, Schwann cells and ependymal cells in persistently infected rats: location of viral genomic and messenger RNAs by in situ hybridization. J. Neuropathol. Exp. Neurol. 50:205214.
28. Carbone, K. M.,, S. W. Park,, S. A. Rubin,, R. W. Waltrip II,, and G. B. Vogelsang. 1991b. Borna disease: association with a maturation defect in the cellular immune response. J. Virol. 65:61546164.
29. Carbone, K. M.,, S. A. Rubin,, Y. Nishino,, and M. Pletnikov. 2001. Borna disease: virus induced neurobehavioral disease pathogenesis. Curr. Opin. Microbiol. Rev. 4:467475.
30. Carbone, K. M.,, S. A. Rubin,, A. M. Sierra-Honigmann,, and H. M. Lederman. 1993. Characterization of a glial cell line persistently infected with Borna disease virus (BDV): influence of neurotrophic factors on BDV protein and RNA expression. J. Virol. 67:14531460.
31. Carbone, K. M.,, B. D. Trapp,, J. W. Griffin,, C. S. Duchala,, and O. Narayan. 1989. Astrocytes and Schwann cells are virus-host cells in the nervous system of rats with Borna disease. J. Neuropathol. Exp. Neurol. 48:631644.
32. Cash, E.,, A. Minty,, P. Ferrara,, D. Caput,, D. Fradelizi,, and O. Rott. 1994. Macrophage-inactivating IL-13 suppresses experimental autoimmune encephalomyelitis in rats. J. Immunol. 153:42584267.
33. Ciaranello, A. L.,, and R. D. Ciaranello. 1995. The neurobiology of infantile autism. Annu. Rev. Neurosci. 18:10128.
34. Clark, D. A. 1994. The whole truth about perforin. Nature 369:1618.
35. Cubitt, B.,, and J. C. de la torre. 1994. Borna disease virus (BDV), a nonsegmented RNA virus, replicates in the nuclei of infected cells where infectious BDV ribonucleoproteins are present. J. Virol. 68:13711381.
36. Danner, K.,, D. Heubeck,, and A. Mayr. 1978. In vitro studies on Borna disease. I. The use of cell cultures for the demonstration, titration and production of Borna virus. Arch. Virol. 57:6375.
37. Deschl, U.,, L. Stitz,, S. Herzog,, K. Frese,, and R. Rott. 1990. Determination of immune cells and expression of major histocompatibility complex class II antigen in encephalitic lesions of experimental Borna disease. Acta Neuropathol. (Berlin) 81:4150.
38. Ding, A. H.,, C. F. Nathan,, and D. J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141:24072412.
39. Dittrich, W.,, L. Bode,, H. Ludwig,, M. Kao,, and K. Scheider. 1989. Learning deficiencies in Borna disease virus-infected but clinically healthy rats. Biol. Psychiatry 20:818828.
40. Eddleston, M.,, and L. Mucke. 1993. Molecular profile of reactive astrocytes—implications for their role in neurologic disease. Neuroscience 54:1536.
41. Eichenbaum, H.,, C. Stewart,, and R. G. Morris. 1990. Hippocampal representation in place learning. J. Neurosci. 10:35313542.
42. Eisenman, L. M.,, R. Brothers,, M. H. Tran,, R. B. Kean,, G. M. Dickson,, B. Dietzschold,, and D. C. Hooper. 1999. Neonatal Borna disease virus infection in the rat causes a loss of Purkinje cells in the cerebellum. J. Neurovirol. 5:181189.
43. Fanselow, M. S. 2000. Contextual fear, gestalt memories, and the hippocampus. Behav. Brain Res. 110:7381.
44. Festing, M. F. 2001. Experimental approaches to the determination of genetic variability. Toxicol. Lett. 120:293300.
45. Fierz, W.,, B. Endler,, K. Reske,, H. Wekerle,, and A. Fontana. 1985. Astrocytes as antigen-presenting cells. I. Induction of la antigen expression on astrocytes by T cells via immune interferon and its effect on antigen presentation. J. Immunol. 134:37853793.
46. Fleischer, B. 1984. Acquisition of specific cytotoxic activity by human T4+ T lymphocytes in culture. Nature 308:365367.
47. Fontana, A.,, W. Fierz,, and H. Wekerle. 1984. Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature 307:273276.
48. Fontana, A.,, K. Frei,, S. Bodmer,, E. Hofer,, M. H. Schreier, , M. A. Palladino, Jr. 1989. Transforming growth factor-beta inhibits the generation of cytotoxic T cells in virus-infected mice. J. Immunol. 143:32303234.
49. Fowell, D.,, and D. Mason. 1993. Evidence that the T cell repertoire of normal rats contains cells with the potential to cause diabetes. Characterization of the CD4+ T cell subset that inhibits this autoimmune potential. J. Exp. Med. 177:627636.
50. Furrer, E.,, T. Bilzer,, L. Stitz,, and O. Planz. 2001. Neutralizing antibodies in persistent Borna disease virus infection: prophylactic effect of gp94-specific monoclonal antibodies in preventing encephalitis. J. Virol. 75:943951.
51. Galoyan, A. 2000. Neurochemistry of brain neuroendocrine immune system: signal molecules. Neurochem. Res. 25:13431355.
52. Gies, U.,, T. Bilzer,, L. Stitz,, and J. F. Staiger. 1998. Disturbance of the cortical cholinergic innervation in Borna disease prior to encephalitis. Brain Pathol. 8:3948.
53. Gies, U.,, T. J. Gorsc,, J. Mulder,, O. Planz,, L. Stitz,, T. Bilzer,, P. G. Luiten,, and T. Harkany. 2001. Cortical cholinergic decline parallels the progression of Borna disease virus encephalitis. Neuroreport 12:37673772.
54. Goldowitz, D.,, and K. Hamre. 1998. The cells and molecules that make a cerebellum. Trends Neurosci. 21:375382.
55. Gonzalez-Dunia, D.,, M. Eddleston,, N. Mackman,, K. M. Carbone,, and J. C. de la torre. 1996. Expression of tissue factor is increased in astrocytes within the central nervous system during persistent infection with Borna disease virus. J. Virol. 70:58125820.
56. Gonzalez-Dunia, D.,, C. Sauder,, and J. C. de la torre. 1997. Borna disease virus and the brain. Brain Res. Bull. 44:647664.
57. Gonzalez-Dunia, D.,, M. Watanabe,, S. Syan,, M. Mallory,, E. Masliah,, and J. C. de la torre. 2000. Synaptic pathology in Borna disease virus persistent infection. J. Virol. 74:34413448.
58. Gosztonyi, G.,, and H. Ludwig. 1984. Borna disease of horses. An immunohistological and virological study of naturally infected animals. Acta Neuropathol. (Berlin) 64:213221.
59. Gosztonyi, G.,, and H. Ludwig. 1995. Borna disease—neuropathology and pathogenesis. Curr. Top. Microbiol. Immunol. 190:3973.
60. Gosztonyi, G.,, B. Dietzschold,, M. Kao,, C. E. Rupprecht,, H. Ludwig,, and H. Koprowski. 1993. Rabies and Borna disease. A comparative pathogenetic study of two neurovirulent agents. Lab. Investig. 68:285295.
61. Gould, E.,, and B. S. McEwen. 1993. Neuronal birth and death. Curr. Opin. Neurobiol. 3:676682.
62. Haliensleben, W.,, M. Schwemmie,, J. Hausmann,, L. Stitz,, B. Volk,, A. Pagenstecher,, and P. Staeheli. 1998. Borna disease virus-induced neurological disorder in mice: infection of neonates results in immunopathology. J. Virol. 72:43794386.
63. Halloran, P. F.,, J. Urmson,, P. H. Van der Meide,, and P. Autenried P. 1989. Regulation of MHC expression in vivo. II. IFN-α/β inducers and recombinant IFN-α modulate MHC antigen expression in mouse tissues. J. Immunol. 142:42414247.
64. Hans, A.,, S. Syan,, C. Crosio,, P. Sassone-Corsi,, M. Brahic,, and D. Gonzalez-Dunia. 2001. Borna disease virus persistent infection activates mitogen-activated protein kinase and blocks neuronal differentiation of pc12 cells. J. Biol. Chem. 276:72587265.
65. Hatalski, C. G.,, S. Kliche,, L. Stitz,, and W. I. Lipkin. 1995. Neutralizing antibodies in Borna disease virus-infected rats. J. Virol. 69:741747.
66. Hatalski, C. G.,, W. F. Hickey,, and W. I. Lipkin. 1998. Evolution of the immune response in the central nervous system following infection with Borna disease virus. J. Neuroimmunol. 90:137142.
67. Hatalski, C. G.,, W. F. Hickey,, and W. I. Lipkin. 1998. Humoral immunity in the central nervous system of Lewis rats infected with Borna disease virus. J. Neuroimmunol. 90:128136.
68. Hausmann, J.,, W. Hallensleben,, J. C. de la torre,, A. Pagenstecher,, C. Zimmermann,, and H. Pircher. 1999. T cell ignorance in mice to Borna disease virus can be overcome by peripheral expression of the viral nucleoprotein. Proc. Natl. Acad. Sci. USA 96:97699774.
69. Henkart, P. A. 1985. Mechanism of lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 3:3158.
70. Herden, C. S., Herzog, J. A. Richt, A. Nesseler, M. Christ, K. Failing, and K. Frese. 2000. Distribution of Borna disease virus in the brain of rats infected with an obesity-inducing virus strain. Brain Pathol. 10:3948.
71. Herzog, S.,, K. Frese,, and R. Rott. 1991. Studies on the genetic control of resitsance of black hooded rats to Borna disease. J. Gen. Virol. 72:535540.
72. Herzog, S.,, C. Kompter,, K. Frese,, and R. Rott. 1984. Replication of Borna disease virus in rats: age-dependent differences in tissue distribution. Med. Microbiol. Immunol. (Berlin) 173:171177.
73. Herzog, S.,, and R. Rott. 1980. Replication of Borna disease virus in cell culture. Med. Microbiol. Immunol. 168:153158.
74. Herzog, S.,, K. Wonigeit,, K. Frese,, H. J. Hedrich,, and R. Rott. 1985. Effect of Borna disease virus infection on athymic rats. J. Gen. Virol. 66:503508.
75. Hickey, W. F.,, B. L. Hsu,, and H. Kimura. 1991. T-lymphocyte entry into the central nervous system. J. Neurosci. Res. 28:254260.
76. Hirano, N.,, M. Kao,, and H. Ludwig. 1983. Persistent, tolerant or subacute infection in Borna disease virus-infected rats. J. Gen. Virol. 64:15211530.
77. Hornig, M.,, M. Solbrig,, N. Horscroft,, H. Weissenbock,, and W. I. Lipkin. 2001. Borna disease virus infection of adult and neonatal rats: models for neuropsychiatric disease. Curr. Top. Microbiol. Immunol. 253:157177.
78. Hornig, M.,, H. Weissenbock,, N. Horscroft,, and W. I. Lipkin. 1999. An infection-based model of neurodevelopmental damage. Proc. Nat. Acad. Sci. USA 96:1210212107.
79. Irigoin, C.,, E. M., Rodriguez,, M. Heinrichs,, K. Frese,, S. Herzog,, and A. Oksche. 1990. Immunocytochemical study of the subcommissural organ of rats with induced postnatal hydrocephalus. Exp. Brain Res. 82:384392.
80. Jacobson, S.,, J. R. Richert,, W. E. Biddison,, A. Satinsky,, R. J. Hartzman,, and H. F. McFarland. 1984. Measles virus-specific T4+ human cytotoxic T cell clones are restricted by class II HLA antigens J. Immunol. 133:754757.
81. Johnson, R. T. 1982. Selective vulnerability of neural cells to viral infections. Adv. Neurol.
82. Johnson, R. T. 1998. Viral Infections of the Nervous System. Lippincott-Raven, Philadelphia, Pa. 36:331337.
83. Kägi, D.,, B. Ledermann,, and K. Bürki. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perform-deficient mice. Nature 369:3137.
84. Kaluza, G.,, G. Lell,, M. Reinacher,, L. Stitz,, and W. R. Willems. 1987. Neurogenic spread of Semliki Forest virus in mice. Arch. Virol. 93:97110.
85. Kao, M.,, H. Ludwig,, and G. Gosztonyi. 1984. Adaptation of Borna disease virus to the mouse. J. Gen. Virol. 65:18451849.
86. Kaplan, D. R.,, R. Griffith,, V. L. Braciale,, and T. J. Braciale. 1984. Influenza virus-specific human cytotoxic T cell clones: heterogeneity in antigen specificity and restriction by class II MHC products. Cell. Immunol. 88:193199.
87. Kast, W. M.,, A. M. Bronkhorst,, L. P. DeWaal,, and C. J. M. Melief. 1986. Cooperation between cytotoxic and helper T lymphocytes in protection against lethal Sendal virus infection: protection by T cells is MHC-restricted and MHC-regulated: a model for MHC-disease associations. J. Exp. Med. 164:723738.
88. Kliche, S.,, T. Briese,, A. H. Henschen,, L. Stitz,, and W. I. Lipkin. 1994. Characterization of a Borna disease virus glycoprotein, gp18. J. Virol. 68:69186923.
89. Koprowski, H.,, Y. M. Zheng,, E. Heber-Katz,, N. Fraser,, L. Rorke,, and Z. F. Fu. 1993. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc. Natl. Acad. Sci. USA 90:30243027. (Erratum, 90:5378.)
90. Krey, H.,, H. Ludwig,, and R. Rott. 1979. Spread of infectious virus along the optic nerve into the retina in Borna disease virus-infected rabbits. Arch. Virol. 61:283288.
91. Krey, H.,, L. Stitz,, and H. Ludwig. 1982. Virus-induced pigment epithelitis in rhesus monkeys. Clinical and histological findings. Ophthalmologica 185:205213.
92. Lalonde, R. 1997. Visuospatial abilities. Int. Rev. Neurobiol. 41:191215.
93. Leist, T. P.,, M. Kohler,, and R. M. Zinkernagel. 1989. Impaired generation of antiviral cytotoxicity against lymphocytic choriomeningitis and vaccinia virus in mice treated with CD4-specific monoclonal antibody. Scand. J. Immunol. 30:679686.
94. Levi-Montalcini, R.,, S. D. Skaper,, R. Dal Toso,, L. Petrelli,, and A. Leon. 1996. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci. 19:514520.
95. Lewis, A. J.,, J. L. Whitton,, C. G. Hatalski,, H. Weissenbock,, and W. I. Lipkin. 1999. Effect of immune priming on Borna disease. J. Virol. 73:25412546.
96. Lipkin, W. I.,, K. M. Carbone,, M. C. Wilson,, C. S. Duchala,, O. Narayan,, and M. B. Oldstone. 1988. Neurotransmitter abnormalities in Borna disease. Brain Res. 475:366370.
97. Luckacher, A. E.,, L. A. Morrison,, V. L. Braciale,, B. Malissen,, and T. J. Braciale. 1985. Expression of specific cytolytic activity by H-2 I region-restricted, influenza virus-specific T lymphocyte clones. J. Exp. Med. 162:171187.
98. Ludwig, H.,, H. Becht,, and L. Groh. 1973. Borna disease, a slow virus infection: biological properties of the virus. Med. Microbiol. Immunol. (Berlin) 158:275289.
99. Ludwig, H.,, and L. Bode. 2001. Borna disease virus: new aspects on infection, disease, diagnosis and epidemiology. Rev. Sci. Tech. 19:259288.
100. Ludwig, H.,, L. Bode,, and G. Gosztonyi. 1988. Borna disease: a persistent virus infection of the central nervous system. Prog. Med. Virol. 35:107151.
101. Ludwig, H.,, K. Furuya,, L. Bode,, N. Klein,, R. Durrwald,, and D. S. Lee. 1993. Biology and neurobiology of Borna disease viruses (BDV), defined by antibodies, neutralizability and their pathogenic potential. Arch. Virol. Suppl. 7:111133.
102. Ludwig, H.,, and P. Thein. 1977. Demonstration of specific antibodies in the central nervous system of horses naturally infected with Borna disease virus. Med. Microbiol. Immunol. 163:215226.
103. Massa, P. T.,, R. Dörries,, and V. Ter Meulen. 1986. Viral particles induce antigen expression on astrocytes. Nature 320:543546.
104. Mims, C. A. 1960. Intracerebral injections and the growth of viruses in the mouse brain. Br. J. Exp. Pathol. 41:5259.
105. Monjan, A. A.,, D. H. Gilden,, G. A. Cole,, and N. Nathanson. 1971. Cerebellar hypoplasia in neonatal rats caused by lymphocytic choriomeningitis virus. Science 171:194196.
106. Morales, J. A.,, S. Herzog,, C. Kompter,, K. Frese,, and R. Rott. 1988. Axonal transport of Borna disease virus along olfactory pathways in spontaneously and experimentally infected rats. Med. Microbiol. Immunol. (Berlin) 177:5168.
107. Müller, C.,, D. Kägi,, and T. Aebischer. 1989. Detection of perforin and granzyme A mRNAs in infiltrating cells during LCMV infection of mice. Eur. J. Immunol. 19:12531259.
108. Nakamura, Y.,, M. Kishi,, T. Nakaya,, S. Asahi,, H. Tanaka,, H. Sentsui,, K. Ikeda,, and K. Ikuta. 1995. Demonstration of Borna disease virus RNA in peripheral blood mononuclear cells from healthy horses in Japan. Vaccine 13:10761079.
109. Narayan, O.,, S. Herzog,, K. Frese,, H. Scheefers,, and R. Rott. 1983a. Behavioral disease in rats caused by immunopathological responses to persistent borna virus in the brain. Science 220:14011403.
110. Narayan, O.,, S. Herzog,, K. Frese,, H. Scheefers,, and R. Rott. 1983b. Pathogenesis of Borna disease in rats: immune-mediated viral ophthalmoencephalopathy causing blindness and behavioral abnormalities. J. Infect. Dis. 148:305315.
111. Nathan, C. 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:30513064.
112. Nicolau, S. 1928. Les modifictions histo-pathologiques des capsules surrénales et des glandes salivaires des lapins morts d’encéphalomeyélite enzootique expérimentale (maladie de Borna). C. R. Acad. Sci. 186:655657.
113. Nicolau, S.,, and I. A. Galloway. 1927. Preliminary note on the experimental study of enzootic encephalo-myelitis (Borna disease). Br. J. Exp. Pathol. 8:336341.
114. Nicolau, S.,, and I. A. Galloway. 1928. Étude sur les inclusions intranucléaires caractérisant la maladie de Borna. C. R. Soc. Biol. Fil. 99:14551457.
115. Nicolau, S.,, and N. Stroian. 1928. Altérations du système nerveux de l’estomac et de l’intestin des lapins morts d’encéphalo-myélite enzootique expérimentale (maladie de Borna). C. R. Soc. Biol. Fil. 99:11021106.
116. Nishino, Y.,, D. Kobasa,, S. A. Rubin,, M. V. Pletnikov,, and K. M. Carbone. 2002. Enhanced neurovirulence of Borna disease virus variants associated with nucleotide changes in the glycoprotein and L polymerase genes. J. Virol. 76:86508658.
117. Nitzschke, E. 1963. Untersuchungen ueber die experimentelle Bornavirus-Infektion bei der Ratte. Zentbl. Vetmed. Reihe B 10:470527.
118. Noske, K.,, T. Bilzer,, O. Planz,, and L. Stitz. 1998 . Virus-specific CD4+ T cells eliminate Borna disease virus from the brain via induction of cytotoxic CD8+ T cells. J. Virol. 72:43874395.
119. Oster-Granite, M. L.,, and R. M. Herndon. 1985. The pathogenesis of parvovirus-induced cerebellar hypoplasia in the Syrian hamster Mesocricetus auratus. Fluorescent antibody, foliation, cytoarchitectonic, golgi and electron microscopic studies. J. Comp. Neurol. 169:481522.
120. Paliard, X.,, R. W. Malefijt,, J. E. de Vries,, and H. Spits. 1988. Interleukin-4 mediates CD8 induction on human CD4+ T-cell clones. Nature 335:642644.
121. Palladino, M. A.,, R. E. Morris,, H. F. Starnes,, and A. D. Levinson. 1990. The transforming growth factor-β. A new family of immunoregulatory molecules. Ann. N. Y. Acad. Sci. 593:181187.
122. Pankseep, J., 1990. The psychoneurology of fear: evolutionary perspective and the role of animal models in understanding human anxiety, p. 358. In G. D. Burrows, , M. Roth, , and R. Noyes (ed.), Handbook of Anxiety, vol. 3. The Neurobiobiology of Anxiety. Elsevier, Amsterdam, The Netherlands.
123. Pankseep, J.,, S. Siviy,, and L. Normansell. 1984. The psychobiology of play: theoretical and methodological perspectives. Neurosci. Biobehav. Rev. 8:465492.
124. Petrosini, L.,, M. Leggio,, and M. Molinari. 1998. The cerebellum in the spatial problem solving: a co-star or a guest star? Prog. Neurobiol. 56:191210.
125. Pette, H.,, and S. Környey. 1935. Über die Pathogenese und die Histologie der Bornaschen Krankheit im Tierexperiment. Dtsch. Z. Nervenheilkd. 136:2065.
126. Planz, O.,, T. Bilzer,, M. Sobbe,, and L. Stitz. 1993. Lysis of major histocompatibility complex class I-bearing cells in Borna disease virus-induced degenerative encephalopathy. J. Exp. Med. 178:163174.
127. Planz, O.,, T. Bilzer,, and L. Stitz. 1995. Immunopathogenic role of T-cell subsets in Borna disease virus-induced progressive encephalitis. J. Virol. 69:896903.
128. Planz, O.,, T. Dumrese,, S. Hulpusch,, M. Schirle,, S. Stevanovic,, and L. Stitz. 2001. A naturally processed rat major histocompatibility complex class I-associated viral peptide as target structure of Borna disease virus-specific CD8+ T cells. J. Biol. Chem. 276:1368913694.
129. Planz, O.,, S. Pleschka,, and S. Ludwig. 2001. MEK-specific inhibitor U0126 blocks spread of Borna disease virus in cultured cells. J. Virol. 75:48714877.
130. Planz, O.,, and L. Stitz. 1999. Borna disease virus nucleoprotein (p40) is a major target for CD8+-T-cell-mediated immune response. J. Virol. 73:17151718.
131. Plata-Salaman, C. R.,, S. E. Ilyin,, D. Gayle,, A. Romanovitch,, and K. M. Carbone. 1999. Regional cytokine, cytokine receptor and neuropeptide mRNA changes associated with behavioral and neuroanatomical abnormalities in persistent, noninflammatory virus infection of neonatal rats. Ann. N. Y. Acad. Sci. 890:469.
132. Pletnikov, M.,, S. Rubin,, K. Carbone,, T. Moran,, and G. J. Schwartz. 2001. Neonatal Borna disease virus infection (BDV)-induced damage to the cerebellum is associated with sensorimotor deficits in developing Lewis rats. Dev. Brain Res. 126:112.
133. Pletnikov, M.,, S. Rubin,, G. Schwartz,, K. Carbone,, and T. H. Moran. 2000. Effects of neonatal rat Borna disease virus (BDV) infection on the postnatal development of brain monoaminergic systems. Dev. Brain Res. 119:179185.
134. Pletnikov, M.,, S. Rubin,, G. Schwartz,, T. Moran,, T. Sobotka,, and K. M. Carbone. 1999a. Persistent neonatal Borna disease virus (BDV) infection of the brain causes chronic emotional abnormalities in adult rats. Physiol. Behav. 66:823831.
135. Pletnikov, M.,, S. Rubin,, K. Vasudevan,, T. Moran,, and K. M. Carbone. 1999b. Developmental brain injury associated with abnormal play behavior in neonatally Borna disease virus-infected Lewis rats: a model of autism. Behav. Brain. Res. 100:4350.
136. Pletnikov, M. V.,, M. L. Jones,, S. A. Rubin,, T. H. Moran,, and K. M. Carbone. 2001. Rat model of autism spectrum disorders. Genetic background effects on Borna disease virus-induced developmental brain damage. Ann. N. Y. Acad. Sci. 939:318319.
137. Powell, M. B.,, D. Mitchell,, J. Lederman,, J. Buckmeier,, S. S. Zamvil,, and M. Graham. 1990. Lymphotoxin and tumor necrosis factor-alpha production by myelin basic protein-specific T cell clones correlates with encephalitogenicity. Int. Immunol. 2:539544.
138. Quagliarello, V. J.,, B. Wispelwey, , W. J. Long, Jr.,, and W. M. Scheld. 1991. Recombinant human interleukin-1 induces meningitis and blood-brain barrier injury in the rat. Characterization and comparison with tumor necrosis factor. J. Clin. Investig. 87:13601366.
139. Raine, C. S.,, and B. N. Fields. 1973. Reovirus type III encephalitis: a virologic and ultrastructural study. J. Neuropathol. Exp. Neurol. 32:1933.
140. Reinacher, M.,, J. Bonin,, O. Narayan,, and C. Scholtissek. 1983. Pathogenesis of neurovirulent influenza A virus infection in mice. Route of entry of virus into brain determines infection of different populations of cells. Lab. Investig. 49:686692.
141. Richt, J.,, L. Stitz,, U. Deschi,, K. Frese,, and R. Rott. 1990. Borna disease virus-induced meningo-encephalomyelitis caused by a virus-specific CD4+ T cell-mediated immune reaction. J. Gen. Virol. 71:25652573.
142. Richt, J. A.,, S. Herzog,, K. Haberzettl,, and R. Rott. 1993. Demonstration of Borna disease virus-specific RNA in secretions of naturally infected horses by the polymerase chain reaction. Med. Microbiol. Immunol. (Berlin) 182:293304.
143. Richt, J. A.,, and L. Stitz. 1992. Borna disease virus-infected astrocytes function in vitro as antigen-presenting and target cells for virus-specific CD4-bearing lymphocytes. Arch. Virol. 124:95109.
144. Richt, J. A.,, L. Stitz,, H. Wekerle,, and R. Rott. 1989. Borna disease, a progressive meningoencephalo-myelitis as a model for CD4+ T cell-mediated immunopathology in the brain. J. Exp. Med. 170:10451050.
145. Rohrenbeck, A. M.,, M. Bette,, D. C. Hooper,, F. Nyberg,, L. E. Eiden,, and B. Dietzschold. 1999. Upregulation of COX-2 and CGRP expression in resident cells of the Borna disease virus-infected brain is dependent upon inflammation. Neurobiol. Dis. 6:1534.
146. Rolls, E. 2000. Memory systems in the brain. Annu. Rev. Psychol. 51:599630.
147. Rothwell, N. J., , and S. J. Hopkins. 1995. Cytokines and the nervous system. II. Actions and mechanisms of action. Trends Neurosci. 18:130136.
148. Rubin, S. A.,, J. R. Bautista,, T. H. Moran,, G. J. Schwartz,, and K. M. Carbone. 1999a. Viral terato-genesis: brain developmental damage associated with maturation state at time of infection. Dev. Brain Res. 112:237244.
149. Rubin, S. A.,, A. M. Sierra-Honigmann,, H. M. Lederman,, R. W. Waltrip II,, J. J. Eiden,, and K. M. Carbone. 1995. Hematologic consequences of Borna disease virus infection of rat bone marrow and thymus stromal cells. Blood 85:27622769.
150. Rubin, S. A.,, P. Sylves,, M. W. Vogel,, M., Pletnikov,, T. H. Moran,, G. J. Schwartz,, and K. M. Carbone. 1999b. Borna disease virus-induced hippocampal dentate gyrus damage is associated with spatial learning and memory deficits. Brain Res. Bull. 48:2330.
151. Rubin, S. A.,, R. W. Waltrip II,, J. R. Bautista,, and K. M. Carbone. 1993. Borna disease virus in mice: host-specific differences in disease expression. J. Virol. 67:548552.
152. Rubin, S. A.,, T. A. Yednock,, and K. M. Carbone. 1998. In vivo treatment with anti-α4 integrin suppresses clinical and pathological evidence of Borna disease virus infection. J. Neuroimmunol. 84:158163.
153. Ruddle, N. H.,, C. M. Bergman,, K. M. McGrath,, E. G. Lingenheld,, M. L. Grunnet,, and S. J. Padula. 1990. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 172:11931200.
154. Ruddle, N. H.,, and D. S. Schmid. 1987. The role of lymphotoxin in T-cell-mediated cytotoxicity. Ann. Inst. Pasteur Immunol. 138:314320.
155. Saito, N.,, A. Itouji,, Y. Totani,, I. Osawa,, H. Koide,, N. Fujisawa,, K. Ogita,, and C. Tanaka. 1993. Cellular and intracellular localization of epsilon-subspecies of protein kinase C in the rat brain presynaptic localization of the epsilon-subspecies. Brain Res. 607:241248.
156. Sauder, C.,, and J. C. de la torre. 1999. Cytokine expression in the rat central nervous system following perinatal Borna disease virus infection. J. Neuroimmunol. 96:2945.
157. Sauder, C.,, W. Hallensleben,, A. Pagenstecher,, S. Schneckenburger,, L. Biro,, D. Pertlik,, J. Hausmann,, M. Suter,, and P. Staeheli. 2000. Chemokine gene expression in astrocytes of Borna disease virus-infected rats and mice in the absence of inflammation. J. Virol. 74:92679280.
158. Schwemmle, M.,, B. De,, L. C. Shi,, A. Banerjee,, and W. I. Lipkin. 1997. Borna disease virus P-protein is phosphorylated by protein kinase c-epsilon and casein kinase II. J. Biol. Chem. 272:2181821823.
159. Seifried, O.,, and H. Spatz. 1930. Die Ausbreitung der enzephalitischen Reaktion bei der Bornaschen Krankheit der Pferde und deren Beziehung zu der Enzephalitis epidemica, der Heine-Medinschen Krankheit und der Lyssa des Menschen. Eine vergleichend-pathologische Studie. Z. Ges. Neurol. Psychiat. 124:317383.
160. Selmaj, K. W. 1992. The role of cytokines in inflammatory conditions of the central nervous system. Semin. Neurosci. 4:221229.
161. Sethi, K. K.,, H. Naher,, and I. Stroehmann. 1988. Phenotypic heterogeneity of cerebrospinal fluid-derived HIV-specific and HLA-restricted cytotoxic T-cell clones. Nature 335:178181.
162. Shankar, V.,, M. Kao,, A. N. Hamir,, H. Sheng,, H. Koprowski,, and B. Dietzschold. 1992. Kinetics of virus spread and changes in levels of several cytokine mRNAs in the brain after intranasal infection of rats with Borna disease virus. J. Virol. 66:992998.
163. Sierra-Honigmann, A. M.,, S. A. Rubin,, M. G. Estafanous,, R. H. Yolken,, and K. M. Carbone. 1993. Borna disease virus in peripheral blood mononuclear and bone marrow cells of neonatally and chronically infected rats. J. Neuroimmunol. 45:3136.
164. Simmons, R. D.,, and D. O. Willenborg. 1990. Direct injection of cytokines into the spinal cord causes autoimmune encephalomyelitis-like inflammation. J. Neurol. Sci. 100:3742.
165. Sloviter, R. S.,, G. Valiquette,, G. M. Abrams,, E. C. Ronk,, A. L. Sollas,, L. A. Paul,, and S. S. Neubort. 1989. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 243:535538.
166. Smeyne, R. J.,, T. Chu,, A. Lewin,, F. S. Bian,, S. Crisman,, C. Kunsch,, S. A. Lira,, and J. Oberdick. 1995. Local control of granule cell generation by cerebellar Purkinje cells. Mol. Cell. Neurosci. 6:230251.
167. Sobbe, M.,, T. Bilzer,, S. Gommel,, K. Noske,, O. Planz,, and L. Stitz. 1997. Induction of degenerative brain lesions after adoptive transfer of brain lymphocytes from Borna disease virus-infected rats: presence of CD8+ T cells and perforin mRNA. J. Virol. 71:24002407.
168. Solbrig, M. V.,, J. H. Fallon,, and W. I. Lipkin. 1995. Behavioral disturbances and pharmacology of Borna disease. Curr. Top. Microbiol. Immunol. 190:93101.
169. Solbrig, M. V.,, G. F. Koob,, J. H. Fallon,, and W. I. Lipkin. 1994. Tardive dyskinetic syndrome in rats infected with Borna disease virus. Neurobiol. Dis. 1:111119.
170. Solbrig, M. V.,, G. F. Koob,, J. H. Fallon,, S. Reid,, and W. I. Lipkin. 1996a. Prefrontal cortex dysfunction in Borna disease virus (BDV)-infected rats. Biol. Psychiatry 40:629636.
171. Solbrig, M. V., , G. F. Koob, , J. N. Joyce, , and W. I. Lipkin. 1996b. A neural substrate of hyperactivity in Borna disease: changes in brain dopamine receptors. Virology 222:332338.
172. Solbrig, M. V.,, G. F. Koob,, and W. I. Lipkin. 1998. Cocaine sensitivity in Borna disease virus-infected rats. Pharmacol. Biochem. Behav. 59:10471052.
173. Solbrig, M. V.,, G. F. Koob,, L. H. Parsons,, T. Kadota,, N. Horscroft,, T. Briese,, and W. I. Lipkin. 2000. Neurotrophic factor expression after CNS viral injury produces enhanced sensitivity to psychostimulants: potential mechanism for addiction vulnerability. J Neurosci. 20:RC104.
174. Sprankel, H.,, K. Richarz,, H. Ludwig,, and R. Rott. 1978. Behavior alterations in tree shrews (Tupaia glis) induced by Borna disease virus. Med. Microbiol. Immunol. (Berlin) 165:118.
175. Stitz, L.,, B. Dietzschold,, and K. M. Carbone,. 1995. Immunopathogenesis of Borna disease, p. 7592. In H. Koprowski, and I. Lipkin (ed.), Borna Disease. Springer-Verlag KG, Berlin, Germany.
176. Stitz, L.,, H. Krey,, and H. Ludwig. 1980. Borna disease in rhesus monkeys as a model for uveo-cerebral symptoms. J. Med. Virol. 6:333340.
177. Stitz, L.,, K. Noske,, O. Planz,, E. Furrer,, W. I. Lipkin,, and T. Bilzer. 1998. A functional role for neutralizing antibodies in Borna disease: influence on virus tropism outside the central nervous system. J. Virol. 72:88848892.
178. Stitz, L.,, O. Planz,, T. Bilzer,, K. Frei,, and A. Fontana. 1991a. Transforming growth factor-beta modulates T cell-mediated encephalitis caused by Borna disease virus. Pathogenic importance of CD8+ cells and suppression of antibody formation. J. Immunol. 147:35813586.
179. Stitz, L.,, D. Schilken,, and K. Frese. 1991b. Atypical dissemination of the highly neurotropic Borna disease virus during persistent infection in cyclosporine A-treated, immunosuppressed rats. J. Virol. 65:457460.
180. Stitz, L.,, M. Sobbe,, and T. Bilzer. 1992. Preventive effects of early anti-CD4 or anti-CD8 treatment on Borna disease in rats. J. Virol. 66:33163323.
181. Stitz, L.,, D. Soeder,, U. Deschl,, K. Frese,, and R. Roff. 1989. Inhibition of immune-mediated meningo-encephalitis in persistently Borna disease virus-infected rats by cyclosporine A. J. Immunol. 143:42504256.
182. Street, N. E.,, and T. R. Mosmann. 1991. Functional diversity of T lymphocytes due to secretion of different cytokine patterns. FASEB J. 5:171177.
183. Stuhler, G.,, and P. Walden. 1993. Collaboration of helper and cytotoxic T lymphocytes Eur. J. Immunol. 23:22792286.
184. Suzumura, A.,, E. Lavi,, S. R. Weiss,, and D. H. Silberberg. 1986. Coronavirus infection induces H-2 antigen expression on oligodendrocytes and astrocytes. Science 232:991993.
185. Takano, T.,, M. Uno,, T. Yamano,, and M. Shimada. 1994. Pathogenesis of cerebellar deformity in experimental Chiari type I malformation caused by mumps virus. Acta Neuropathol. 87:168173.
186. Tedeschi, B.,, J. N. Barrett,, and R. W. Keane. 1986. Astrocytes produce interferon that enhances the expression of H-2 antigens on a subpopulation of brain cells. J. Cell Biol. 102:22442253.
187. Thivolet, C.,, A. Bendelac,, P. Bedossa,, J. F. Bach,, and C. Carnaud. 1991. CD8+ T cell homing to the pancreas in the nonobese diabetic mouse is CD4+ T cell-dependent. J. Immunol. 146:8588.
188. Tomlinson, A. H.,, and M. M. Esiri. 1983. Herpes simplex encephalitis. Immunohistological demonstration of spread of virus via olfactory pathways in mice. J. Neurol. Sci. 60:473484.
189. Vaher, P. R.,, V. N. Luine,, E. Gould,, and B. S. McEwen. 1994. Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology. Brain Res. 656:7178.
190. Wahl, S. M.,, N. McCartney-Francis,, and S. E. Mergenhagen. 1989. Inflammatory and immunomodulatory roles of TGF-beta. Immunol. Today 10:258261.
191. Watanabe, M.,, L. Byeong-Jae,, W. Kamitani,, T. Kobayashi,, H. Taniyama,, K. Tomonaga,, and K. Ikuta. 2001. Neurological diseases and viral dynamics in the brains of neonatally Borna disease virus-infected gerbils. Virology 282:6576.
192. Waxham, M. N.,, and J. S. Wolinsky. 1984. Rubella virus and its effects on the central nervous system. Neurol. Clin. 2:367385.
193. Weissenbock, H.,, M. Hornig,, W. F. Hickey,, and W. I. Lipkin. 2000. Microglial activation and neuronal apoptosis in Bornavirus infected neonatal Lewis rats. Brain Pathol. 10:260272.
194. Wekerle, H.,, C. Linington,, H. Lassmann,, and R. Meyermann. 1986. Cellular immune reactivity within the CNS. Trends Neurosci. 271277.
195. Wong, G. H.,, P. F. Bartlett,, I. Clark-Lewis,, F. Battye,, and J. W. Schrader. 1984. Inducible expression of H-2 and Ia antigens on brain cells. Nature 310:688691.
196. Wong, G. H. W.,, I. Clark-Lewis,, A. W. Harris,, and J. W. Schrader. 1984. Effect of cloned interferon-γ on expression of H-2 and Ia antigens on cell lines of hemopoietic, lymphoid, epithelial, fibroblastic and neuronal origin. Eur. J. Immunol. 14:5256.
197. Yasukawa, M.,, and J. M. Zarling. 1984. Human cytotoxic T cell clones directed against herpes simplex infected cells. I. Lysis restricted by HLA class II MB and DR antigens. J. Immunol. 133:422427.
198. Zinkernagel, R. M.,, G. N. Callahan,, A. Althage,, S. Cooper,, J. W. Streilein,, and J. J. Klein. 1978. The lymphoreticular system in triggering virus-plus-self-specific cytotoxic T cells: evidence for T help. J. Exp. Med. 147:897911.
199. Zinkernagel, R. M.,, and P. C. Doherty. 1979. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function, and responsiveness. Adv. Immunol. 27:51177.
200. Zinkernagel, R. M.,, M. Eppler,, and H. P. Pircher,. 1989. Immune-protection versus immunopathology by antiviral T cell responses, p. 906913. In F. Melchers (ed.), Progress in Immunology, 7th ed. Springer-Verlag, Berlin, Germany.
201. Zocher, M.,, S. Czub,, J. Schulte-Monting,, J. C. de la torre,, and C. Sauder. 2000. Alterations in neurotrophin and neurotrophin receptor gene expression patterns in the rat central nervous system following perinatal Borna disease virus infection. J. Neurovirol. 6:462477.
202. Zwick, W. 1929. Neuere Untersuchungen über die seuchenhafte Gehirn- und Rückenmarksentzündung (Bornasche Krankheit) der Pferde. Dtsch. Z. Nervenheilkd. 110:316322.
203. Zwick, W., 1939. Bornasche Krankheit und Enzephalomyelitis der Tiere, p. 254354. In E. Gildenmeister, , E. Haagen, , and O. Waldmann (ed.), Handbuch der Viruskrankheiten, vol. 2. Fischer, Jena, Germany.
204. Zwick, W.,, and O. Seifried. 1924. Untersuchungen ueber die in Hessen gehaeuft auftretende seuchenhafte Gehirn- und Rueckenmarksentzuendung (Bornasche Krankheit) bei Pferden. Berl. Tieraerztl. Wochenschr. 40:465471.
205. Zwick, W.,, O. Seifried,, and J. Witte. 1927. Experimentelle Untersuchungen uber die seuchenhafte Gehirn- und Rückenmarksentzündung der Pferde (Bornasche Krankheit). Z. Infektkrankh. Haustiere 30:42136.
206. Zwick, W.,, O. Seifried,, and J. Witte. 1929. Weitere Beitrage zur Erforschung der Bornaschen Krankheit des Pferdes. Arch. Tierheilkd. 59:511545.

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