Spatiotemporal analysis of Purkinje cell degeneration relative to parasagittal expression domains in a model of neonatal viral infection

Journal of Virology

Volumn 81, Issue 6, 2007, Pages 2675-2687

  Williams, Brent L ^a   Yaddanapudi, Kavitha ^a   Hornig, Mady ^a   Lipkin, W Ian ^a  

^a Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE ISOENZYME P; ALDOLASE C; EXCITATORY AMINO ACID TRANSPORTER 4; FRUCTOSE BISPHOSPHATE ALDOLASE; HERMES ANTIGEN; HYALURONIC ACID; MESSENGER RNA; METALLOTHIONEIN I; METALLOTHIONEIN II; UNCLASSIFIED DRUG; ZEBRIN II;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BORNA DISEASE; BORNA DISEASE VIRUS; CELL LOSS; CELL SURVIVAL; CEREBELLUM; CEREBELLUM INJURY; CEREBELLUM VERMIS; CONTROLLED STUDY; IMMUNOFLUORESCENCE; INFLAMMATION; MICROGLIA; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PURKINJE CELL; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANIMALS, NEWBORN; BORNA DISEASE; BORNA DISEASE VIRUS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DEATH; CEREBELLUM; EXCITATORY AMINO ACID TRANSPORTER 4; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; KINETICS; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOFRUCTOKINASE-1, TYPE C; POLYMERASE CHAIN REACTION; PURKINJE CELLS; RATS; RATS, INBRED LEW; RNA, MESSENGER;

BORNA DISEASE VIRUS; EPICOCCUM; RATTUS;

EID: 33947400648     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02245-06     Document Type: Article

References (80)

1. Ahn, A. H., S. Dziennis, R. Hawkes, and K. Herrup. 1994. The cloning of zebrin II reveals its identity with aldolase C. Development 120:2081-2090.
2. Altman, J., and S. A. Bayer. 1985. Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration, and settling of Purkinje cells. J. Comp. Neurol. 231:42-65.
3. Andersen, C. M., and R. A. Swanson. 2000. Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1-14.
4. Balaban, C. D., R. J. Schuerger, and J. D. Porter. 2000. Zonal organization of flocculo-vestibular connections in rats. Neuroscience 99:669-682.
5. Bardeletti, G. 1977. Respiration and ATP level in BHK21/13S cells during the earliest stages of rubella virus replication. Intervirology 8:100-109.
6. Bardell, D., and M. Essex. 1974. Glycolysis during early infection with feline and human cells with feline leukemia virus. Infect. Immun. 9:824-827.
7. 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. 34:31-40.
8. 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. Brain Res. Dev. Brain Res. 90:45-53.
9. 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. 74:10438-10446.
10. Bonthius, D. J., J. Mahoney, M. J. Buchmeier, B. Karacay, and D. Taggard. 2002. Critical role for glial cells in the propagation and spread of lymphocytic choriomeningitis virus in the developing rat brain. J. Virol. 76:6618-6635.
11. Briese, T., C. G. Hatalski, S. Kliche, Y. S. Park, and W. I. Lipkin. 1995. Enzyme-linked immunosorbent assay for detecting antibodies to Borna disease virus-specific proteins. J. Clin. Microbiol. 33:348-351.
12. 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) 81:41-50.
13. Dittrich, W., L. Bode, M. Kao, and K. Schneider. 1989. Learning deficiencies in Borna disease virus-infected but clinically healthy rats. Biol. Psych. 26: 818-828.
14. Duchala, C. S., H. E. Shick, J. Garcia, D. M. Deweese, X. Sun, V. J. Stewart, and W. B. Macklin. 2004. The toppler mouse: a novel mutant exhibiting loss of Purkinje cells. J. Comp. Neurol. 476:113-129.
15. Dusart, I., M. P. Morel, and C. Sotelo. 1994. Parasagittal compartmentation of adult rat Purkinje cells expressing the low-affinity nerve growth factor receptor: changes of pattern expression after a traumatic lesion. Neuroscience 63:351-356.
16. Edwards, M. A., J. E. Crandall, N. Leclerc, and M. Yamamoto. 1994. Effects of nervous mutation on Purkinje cell compartments defined by zebrin II and 9-O-acetylated gangliosides expression. Neurosci. Res. 19:167-174.
17. 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. 5:181-189.
18. Ekdahl, C. T., J. H. Claasen, S. Bonde, Z. Kokaia, and O. Lindvall. 2003. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 100:13632-13637.
19. El-Bacha, T., M. M. Menezes, M. C. Azevedo e Silva, M. Sola-Penna, and A. T. Da Poian. 2004. Mayaro virus infection alters glucose metabolism in cultured cells through activation of the enzyme 6-phosphofructo 1-kinase. Mol. Cell. Biochem. 266:191-198.
20. Ferguson, S. A. 1996. Neuroanatomical and functional alterations resulting from early postnatal cerebellar insults in rodents. Pharmacol. Biochem. Behav. 55:663-671.
21. Fukuda, K., N. Aihara, S. M. Sagar, F. R. Sharp, L. H. Pitts, J. Honkaniemi, and L. J. Noble. 1996. Purkinje cell vulnerability to mild traumatic brain injury. J. Neurotrauma 13:255-266.
22. Gaut, J. R., and L. M. Hendershot. 1993. The modification and assembly of proteins in the endoplasmic reticulum. Curr. Opin. Cell Biol. 5:589-595.
23. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
24. Gravel, C., L. M. Eisenman, R. Sasseville, and R. Hawkes. 1987. Parasagittal organization of the rat cerebellar cortex: direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivo-cerebellar projection. J. Comp. Neurol. 265:294-310.
25. Hallensleben, W., M. Schwemmle, 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. 72:4379-4386.
26. Hatanaka, M., R. J. Huebner, and R. V. Gilden. 1969. Alterations in the characteristics of sugar uptake by mouse cells transformed by murine sar-coma viruses. J. Natl. Cancer Inst. 43:1091-1096.
27. Hernandez-Fonseca, K., and L. Massieu. 2005. Disruption of endoplasmic reticulum calcium stores is involved in neuronal death induced by glycolysis inhibition in cultured hippocampal neurons. J. Neurosci. Res. 82:196-205.
28. Hirano, N., M. Kao, and H. Ludwig. 1983. Persistent, tolerant or subacute infection in Borna disease virus-infected rats. J. Gen. Virol. 64:1521-1530.
29. Hornig, M., H. Weissenbock, N. Horscroft, and W. I. Lipkin. 1999. An infection-based model of neurodevelopmental damage. Proc. Natl. Acad. Sci. USA 96:12102-12107.
30. Hu, W. H., W. M. Walters, X. M. Xia, S. A. Karmally, and J. R. Bethea. 2003. Neuronal glutamate transporter EAAT4 is expressed in astrocytes. Glia 44:13-25.
31. Iwata, M., A. Hirano, and J. H. French. 1979. Degeneration of the cerebellar system in X-chromosome-linked copper malabsorption. Ann. Neurol. 5:542-549.
32. Jana, M., X. Liu, S. Koka, S. Ghosh, T. M. Petro, and K. Pahan. 2001. Ligation of CD40 stimulates the induction of nitric-oxide synthase in microglial cells. J. Biol. Chem. 276:44527-44533.
33. Jeong, Y. G., B. H. Hyun, and R. Hawkes. 2000. Abnormalities in cerebellar Purkinje cells in the novel ataxic mutant mouse, pogo. Brain Res. Dev. Brain Res. 125:61-67.
34. Kume, A., A. Takahashi, Y. Hashizume, and J. Asai. 1991. A histometrical and comparative study on Purkinje cell loss and olivary nucleus cell loss in multiple system atrophy. J. Neurol. Sci. 101:178-186.
35. Leclerc, N., C. Gravel, and R. Hawkes. 1988. Development of parasagittal zonation in the rat cerebellar cortex: MabQ113 antigenic bands are created postnatally by the suppression of antigen expression in a subset of Purkinje cells. J. Comp. Neurol. 273:399-420.
36. Levisohn, L., A. Cronin-Golomb, and J. D. Schmahmann. 2000. Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain 123:1041-1050.
37. Lohof, A. M., N. Delhaye-Bouchaud, and J. Mariani. 1996. Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev. Neurosci. 7:85-101.
38. Marin-Teva, J. L., I. Dusart, C. Colin, A. Gervais, N. van Rooijen, and M. Mallat. 2004. Microglia promote the death of developing Purkinje cells. Neuron 41:535-547.
39. Monje, M. L., H. Toda, and T. D. Palmer, 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-1765.
40. Nagao, S., S. Kwak, and I. Kanazawa, 1997. EAAT4, a glutamate transporter with properties of a chloride channel, is predominantly localized in Purkinje cell dendrites, and forms parasagittal compartments in rat cerebellum. Neuroscience 78:929-933.
41. Nakki, R., J. Koistinaho, F. R. Sharp, and S. M. Sagar. 1995. Cerebellar toxicity of phencyclidine. J. Neurosci. 15:2097-2108.
42. O'Hearn, E., and M. E. Molliver. 1993. Degeneration of Purkinje cells in parasagittal zones of the cerebellar vermis after treatment with ibogaine or harmaline. Neuroscience 55:303-310.
43. Ohmori, H., H. Ogura, M. Yasuda, S. Nakamura, T. Hatta, K. Kawano, T. Michikawa, K. Yamashita, and K. Mikoshiba. 1999. Developmental neurotoxicity of phenytoin on granule cells and Purkinje cells in mouse cerebellum. J. Neurochem. 72:1497-1506.
44. 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. 169:481-522.
45. Parpura, V., T. A. Basarsky, F. Liu, K. Jeftinija, S. Jeftinija, and P. G. Haydon. 1994. Glutamate-mediated astrocyte-neuron signalling. Nature 369: 744-747.
46. Pletnikov, M. V., S. A. Rubin, K. Vasudevan, T. H. Moran, and K. M. Carbone. 1999. Developmental brain injury associated with abnormal play behavior in neonatally Borna disease virus-infected Lewis rats: a model of autism. Behav. Brain Res. 100:43-50.
47. Pletnikov, M. V., S. A. Rubin, G. J. Schwarte, T. H. Moran, T. J. Sobotka, and K. M. Carbone. 1999. Persistent neonatal Borna disease virus (BDV) infection of the brain causes chronic emotional abnormalities in adult rats. Physiol. Behav. 66:823-831.
48. Pletnikov, M. V., S. A. Rubin, K. M. Carbone, T. H. 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. Brain Res. Dev. Brain Res. 126:1-12.
49. Raine, C. S., and B. N. Fields. 1973. Reovirus type III encephalitis-a virologic and ultrastructural study. J. Neuropathol. Exp. Neurol. 32:19-33.
50. Reyes, M. G., and A. Gordon. 1981. Cerebellar vermis in schizophrenia. Lancet ii:700-701.
51. Rock, R. B., G. Gekker, S. Hu, W. S. Sheng, M. Cheeran, J. R. Lokensgard, and P. K. Peterson. 2004. Role of microglia in central nervous system infections. Clin. Microbiol. Rev. 17:942-964.
52. Rossi, F., A. Jankovski, and C. Sotelo. 1995. Target neuron controls the integrity of afferent axon phenotype: a study on the Purkinje cell-climbing fiber system in cerebellar mutant mice. J. Neurosci. 15:2040-2056.
53. Rubin, S. A., J. R. Bautista, T. H. Moran, G. J. Schwartz, and K. M. Carbone. 1999. Viral teratogenesis: brain developmental damage associated with maturation state at time of infection. Brain Res. Dev. Brain Res. 112:237-244.
54. Rubin, S. A., P. Sylves, M. Vogel, M. Pletnikov, T. H. Moran, G. J. Schwartz, and K. M. Carbone. 1999. Borna disease virus-induced hippocampal dentate gyrus damage is associated with spatial learning and memory deficits. Brain Res. Bull. 48:23-30.
55. Rubin, S. A., M. Pletnikov, R. Taffs, K. E. Wright, E. G. Brown, and K. M. Carbone. 2000. Evaluation of a neonatal rat model for prediction of mumps virus neurovirulence in humans. J. Virol. 74:5382-5384.
56. Ruigrok, T. J., R. J. Osse, and J. Voogd. 1992. Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum. J. Comp. Neurol. 316:129-150.
57. Sarna, J., S. R. Miranda, E. H. Schuchman, and R. Hawkes. 2001. Patterned cerebellar Purkinje cell death in a transgenic mouse model of Niemann Pick type A/B disease. Eur. J. Neurosci. 13:1873-1880.
58. Sarna, J. R., and R. Hawkes. 2003. Patterned Purkinje cell death in the cerebellum. Prog. Neurobiol. 70:473-507.
59. Sarna, J. R., M. Larouche, H. Marzban, R. V. Sillitoe, D. E. Rancourt, and R. Hawkes. 2003. Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neural. 456:279-291.
60. Sauder, C., D. P. Wolfer, H. P. Lipp, P. Staeheli, and J. Hausmann. 2001. Learning deficits in mice with persistent Borna disease virus infection of the CNS associated with elevated chemokine expression. Behav. Brain Res. 120:189-201.
61. Schell, M. J., M. E. Molliver, and S. H. Snyder. 1995. D-Serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc. Natl. Acad. Sci. USA 92:3948-3952.
62. Schmahmann, J. D. 1991. An emerging concept. The cerebellar contribution to higher function. Arch. Neurol. 48:1178-1187.
63. Singh, V. N, M. Singh, J. T. August, and B. L. Horecker. 1974. Alterations in glucose metabolism in chick-embryo cells transformed by Rous sarcoma virus: intracellular levels of glycolytic intermediates. Proc. Natl. Acad. Sci. USA 71:4129-4132.
64. Smeyne, R. J., T. Chu, A. Lewin, F. 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. 6:230-251.
65. 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. 87:168-173.
66. Takayasu, Y., M. Iino, W. Kakegawa, H. Maeno, K. Watase, K. Wada, D. Yanagihara, T. Miyazaki, O. Komine, M. Watanabe, K. Tanaka, and S. Ozawa. 2005. Differential roles of glial and neuronal glutamate transporters in Purkinje cell synapses. J. Neurosci. 25:8788-8793.
67. Terekhina, N. A., I. Petrovich, and T. G. Parkhomenko. 1998. Glycolytic metabolites and adenosine triphosphoric acid in the herpes-infected eye. Zh. Mikrobiol. Epidemiol. Immunobiol. 2:92-94.
68. Tolbert, D. L., M. W. Bradley, E. G. Tolod, I. Torres-Aleman, and B. R. Clark. 2001. Chronic intraventricular infusion of glial cell line-derived neurotrophic factor (GDNF) rescues some cerebellar Purkinje cells from heredodegeneration. Exp. Neurol. 170:375-379.
69. Voogd, J., and T. J. Ruigrok. 1997. Transverse and longitudinal patterns in the mammalian cerebellum. Prog. Brain Res. 114:21-37.
70. Voogd, J., J. Pardoe, T. J. Ruigrok, and R. Apps. 2003. The distribution of climbing and mossy fiber collateral branches from the copula pyramidis and the paramedian lobule: congruence of climbing fiber cortical zones and the pattern of zebrin banding within the rat cerebellum. J. Neurosci. 23:4645-4656.
71. Wadiche, J. I., and C. E. Jahr. 2005. Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat. Neurosci. 8:1329-1334.
72. Wassef, M., C. Sotelo, B. Cholley, A. Brehier, and M. Thomasset. 1987. Cerebellar mutations affecting the postnatal survival of Purkinje cells in the mouse disclose a longitudinal pattern of differentially sensitive cells. Dev. Biol. 124:379-389.
73. 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. 10:260-272.
74. Welsh, J. P., G. Yuen, D. G. Placantonakis, T. Q. Vu, F. Haiss, E. O'Hearn, M. E. Molliver, and S. A. Aicher. 2002. Why do Purkinje cells die so easily after global brain ischemia? Aldolase C, EAAT4, and the cerebellar contribution to posthypoxic myoclonus. Adv. Neurol. 89:331-359.
75. Wenning, G. K., F. Tison, L. Elliott, N. P. Quinn, and S. E. Daniel. 1996. Olivopontocerebellar pathology in multiple system atrophy. Mov. Disord. 11:157-162.
76. Wiesmann, C., and A. M. de Vos. 2001. Nerve growth factor: structure and function. Cell. Mol. Life Sci. 58:748-759.
77. Williams, B. L., and W. I. Lipkin. 2006. Endoplasmic reticulum stress and neurodegeneration in rats neonatally infected with Borna disease virus. J. Virol. 80:8613-8626.
78. Williams, B. L., K. Yaddanapudi, C. M. Kirk, A. Soman, M. Hornig, and W. I. Lipkin. 2006. Metallothioneins and zinc dysregulation contribute to neurodevelopmental damage in a model of perinatal viral infection. Brain Pathol. 16:1-14.
79. Yang, Q., Y. Hashizume, M. Yoshida, Y. Wang, Y. Goto, N. Mitsuma, K. Ishikawa, and H. Mizusawa. 2000. Morphological Purkinje cell changes in spinocerebellar ataxia type 6. Acta Neuropathol. (Berlin) 100:371-376.
80. 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 Borna disease virus infection. J. Neurovirol. 6:462-477.