Cited by 173Multiple Sclerosis Research StudiesViral Infections and Immunology ResearchVirology and Viral Diseases

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Experimental models of virus-induced demyelination of the central nervous system

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Dal Canto, Mauro C., Rabinowitz, Stanley G.·1982·Annals of Neurology

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Abstract

One of the arguments in favor of a viral pathogenesis for multiple sclerosis is the existence of several experimental and natural animal models of virus‐induced primary demyelination. This review deals comprehensively with such models. Well‐known examples of demyelinating viral infections in their natural host are JHM, Theiler, visna, and canine distemper encephalomyelitides. Recent reports of experimental murine infections with pathogens such as vesicular stomatitis, Chandipura, herpes simplex, Venezuelan equine encephalomyelitis, and Semliki Forest viruses are also discussed. The thrust of the review is to include viral models suspected of producing primary demyelination on an immunopathological basis.

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Zimprich, F., Winter, J., Wege, H., & Lassmann, H. (1991) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1991.tb00750.x · Cited by 32
“models to study the pathogenesis of such diseases (Dal Canto & Rabinowitz, 1981; Kyuwa & Stohlman, 1990) .”
In vitro characterization and preferential infection by canine distemper virus of glial precursors with Schwann cell characteristics from adult canine brain
Orlando, E., Imbschweiler, I., Gerhauser, I., Baumgärtner, W., & Wewetzer, K. (2008) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2008.00958.x · Cited by 30
Olfactory neural pathway in mouse hepatitis virus nasoencephalitis
Barthold, S. (2004) · Acta Neuropathologica · doi:10.1007/bf00686390 · Cited by 30
“The murine coronavirus, mouse hepatitis virus (MHV), has served prominently as a model of viral encephalitis and demyelinating disease in mice and rats [7, 18-20].”
Background
Bilateral neuroretinitis associated with mumps.
Khubchandani, R., Rane, T., Agarwal, P., Nabi, F., Patel, P., & Shetty, A. (2002) · Archives of Neurology · doi:10.1001/archneur.59.10.1633 · Cited by 29
“Additionally, the temporal framework and immunopathologic features of postinfectious encephalitis closely resemble those of experimental models of virus-induced demyelination of the central nervous system.(19) The role of corticosteroids is controversial.”
Background
Dengue virus infects mouse cultured neurons but not astrocytes
Imbert, J., Guevara, P., Ramos-Castañeda, J., Ramos, C., & Sotelo, J. (1994) · Journal of Medical Virology · doi:10.1002/jmv.1890420304 · Cited by 29
Restricted infection with canine distemper virus leads to down-regulation of myelin gene transcription in cultured oligodendrocytes
Graber, H., Müller, C., Vandevelde, M., & Zurbriggen, A. (2004) · Acta Neuropathologica · doi:10.1007/bf00296516 · Cited by 29
“Like other reproducible demyelinating diseases in animals, canine distemper is considered a model for studying human demyelinating diseases such as multiple sclerosis [ 5 ].”
Background
Neuroimmune interactions in a model of multiple sclerosis
Welsh, C., Steelman, A., Mi, W., Young, C., Storts, R., Welsh, T. H., & Meagher, M. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03984.x · Cited by 27
Spontaneous and induced remyelination in multiple sclerosis and the theiler's virus model of central nervous system demyelination
Miller, D. J., & Rodriguez, M. (1995) · Microscopy Research and Technique · doi:10.1002/jemt.1070320306 · Cited by 28
Magnetic resonance imaging findings in acute canine distemper virus infection.
Bathen-Noethen, A., Stein, V. M., Puff, C., Baumgaertner, W., & Tipold, A. (2008) · Journal of Small Animal Practice · doi:10.1111/j.1748-5827.2008.00552.x · Cited by 26
Neurotoxic potential of reactive astrocytes in canine distemper demyelinating leukoencephalitis
Klemens, J., Ciurkiewicz, M., Chludzinski, E., Iseringhausen, M., Klotz, D., Pfankuche, V., Ulrich, R., Herder, V., Puff, C., Baumgärtner, W., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-48146-9 · Cited by 24
Experimental strategies to promote central nervous system remyelination in multiple sclerosis: Insights gained from the Theiler's virus model system
Miller, D. J., Asakura, K., & Rodriguez, M. (1995) · Journal of Neuroscience Research · doi:10.1002/jnr.490410302 · Cited by 24
Chronic relapsing demyelinating encephalomyelitis associated with persistent spontaneous canine distemper virus infection
Higgins, R. J., Child, G., & Vandevelde, M. (2004) · Acta Neuropathologica · doi:10.1007/bf00687381 · Cited by 24
“It would be of great comparative interest to other viral models of demyelinating disease [ 5 ] and multiple sclerosis [20] to define the immunological mechanisms resulting in clearance of antigen from the chronic demyelinating lesions and for the progressive multiphasic nature of this disease.”
Background
Recovery of Myelin after Induction of Oligodendrocyte Cell Death in Postnatal Brain
Jalabi, W., Boehm, N., Grucker, D., & Ghandour, M. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2748-04.2005 · Cited by 23
“Ethidium bromide (Yajima and Suzuki, 1979), lysolecithin (Hall, 1972), cuprizone (Blakemore, 1973; Hiremath et al., 1998), and viral infection in animal (Martin and Nathanson, 1979; Dal Canto and Rabinowitz, 1982; Stohlman and Hinton, 2001; Fazakerley and Walker, 2003) were extensively used.”
Immunity and the nervous system: Basic tenets
Waksman, B. (1983) · Annals of Neurology · doi:10.1002/ana.410130602 · Cited by 22
Ultrastructural and biochemical findings in brain cell cultures infected with canine distemper virus
Glaus, T., Griot, C., Richard, A., Althaus, U., Herschkowitz, N., & Vandevelde, M. (2004) · Acta Neuropathologica · doi:10.1007/bf00294222 · Cited by 21
“The mechanism of primary demyelination in canine distemper (CD), an animal model for demyelinating disease in man [9] is still unclear.”
Background
Transgenic mouse models of multiple sclerosis
Scheikl, T., Pignolet, B., Mars, L. T., & Liblau, R. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0481-9 · Cited by 18
“In rodents, various viruses, including murine hepatitis virus (strain JHM) and Semliki Forest virus, can induce inflammatory demyelination [20].”
Background
The Pathogenesis of Canine Distemper Virus Induced Demyelination
Baumgärtner, W., & Alldinger, S. (2005) · doi:10.1007/0-387-25518-4_51 · Cited by 19
Polyomavirus Models of Brain Infection and the Pathogenesis of Multiple Sclerosis
Stoner, G. (1993) · Brain Pathology · doi:10.1111/j.1750-3639.1993.tb00748.x · Cited by 18
Impact of Theiler's virus infection on hippocampal neuronal progenitor cells: differential effects in two mouse strains
Jafari, M., Haist, V., Baumgärtner, W., Wagner, S., Stein, V. M., Tipold, A., Wendt, H., & Potschka, H. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01256.x · Cited by 16
Theiler's virus-associated antigens on the surfaces of cultured glial cells.
Rodriguez, M., Siegel, L. M., Hovanec-Burns, D., Bologa, L., & Graves, M. (1988) · Virology · doi:10.1016/0042-6822(88)90517-x · Cited by 16
The Possible Role of Viral Infections in Multiple Sclerosis
ter Meulen, V. (1986) · doi:10.1007/978-94-009-4143-4_40 · Cited by 16
STAT4‐ and STAT6‐signaling molecules in a murine model of multiple sclerosis
Rodriguez, M., Zoecklein, L. J., Gamez, J. D., Pavelko, K. D., Papke, L. M., Nakane, S., Howe, C. L., Radhakrishnan, S., Hansen, M. J., David, C. S., et al. (2005) · The FASEB Journal · doi:10.1096/fj.05-4650fje · Cited by 16
“, picornaviruses, corona viruses, toga viruses, and herpes viruses) (2) and viruses that cause human disease characterized by demyelination (i.”
Background
Cerebral Involvement in Children with Acute and Relapsing Inflammatory Polyneuropathy
Willis, J., & den Bergh, P. V. (1988) · Journal of Child Neurology · doi:10.1177/088307388800300310 · Cited by 15
The involvement of the cerebral cortex in human immunodeficiency virus encephalopathy: a morphological and immunohistochemical study
Ciardi, A., Sinclair, E., Scaravilli, F., Harcourt-Webster, N., & Lucas, S. (2004) · Acta Neuropathologica · doi:10.1007/bf00662637 · Cited by 15
“According to this theory [ 9 ] myelin is destroyed by soluble immune factors liberated by activated monocytes and lymphocytes with a mechanism similar to the demyelination in Theiler's virus infection [7].”
Method
Canine distemper virus-immune complexes induce bystander degeneration of oligodendrocytes
Botteron, C., Zurbriggen, A., Griot, C., & Vandevelde, M. (2004) · Acta Neuropathologica · doi:10.1007/bf00713532 · Cited by 15
“Canine distemper virus (CDV) infection in the dog is an animal model for human demyelinating disorders, such as multiple sclerosis [4].”
Background
Deep spatial profiling of Venezuelan equine encephalitis virus reveals increased genetic diversity amidst neuroinflammation and cell death during brain infection
Williams, E. P., Xue, Y., Lee, J., Fitzpatrick, E. A., Kong, Y., Reichard, W., Writt, H., & Jonsson, C. B. (2023) · Journal of Virology · doi:10.1128/jvi.00827-23 · Cited by 15
A Mechanism of Virus-Induced Demyelination
Sarma, J. D. (2010) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2010/109239 · Cited by 14
“There are other but not many CNS disorders in which increased amounts of IgG and OGBs are found.”
Background
Canine distemper virus-induced glial cell changes in vitro
Zurbriggen, A., & Vandevelde, M. (2004) · Acta Neuropathologica · doi:10.1007/bf00684920 · Cited by 14
“Lytic infection of oligodendrocytes as, e.g., in mouse corona virus infection ( Dal Canto and Rabinowitz 1982 ) is not apparent in distemper.”
Background
Comparison of Reported Spinal Cord Lesions in Progressive Multiple Sclerosis with Theiler’s Murine Encephalomyelitis Virus Induced Demyelinating Disease
Leitzen, E., Jin, W., Herder, V., Beineke, A., Elmarabet, S., Baumgärtner, W., & Hansmann, F. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040989 · Cited by 13
Distribution of 3β-Hydroxysteroid Dehydrogenase in the Cerebellum in Canine Distemper Virus Infection
Yarım, M., & Kabakci, N. (2002) · Journal of Comparative Pathology · doi:10.1053/jcpa.2002.0594 · Cited by 8
Immunocytochemical localization of MAG, MBP and P0 protein in acute and relapsing demyelinating lesions of Theiler's virus infection.
Canto, M. C. D., & Barbano, R. (1985) · Journal of Neuroimmunology · doi:10.1016/0165-5728(85)90003-7 · Cited by 13
Glial proteins in canine distemper virus-induced demyelination
Vandevelde, M., Bichsel, P., Cerruti-Sola, S., Steck, A., Kristensen, F., & Higgins, R. J. (1983) · Acta Neuropathologica · doi:10.1007/bf00691492 · Cited by 13
“However, Higgins et al. (1982) clearly demonstrated segmental demyelination in early distemper lesions similar to the one in experimental corona virus infection in mice, a disease in which oligodendrocytes are known to be the primary target (Lampert 1978; Dal Canto and Rabinowitz 1982 ).”
Background
Reactive Oxygen Species Are Key Mediators of Demyelination in Canine Distemper Leukoencephalitis but not in Theiler’s Murine Encephalomyelitis
Attig, F., Spitzbarth, I., Kalkuhl, A., Deschl, U., Puff, C., Baumgärtner, W., & Ulrich, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133217 · Cited by 15
“Similarly, TMEV-induced demyelinating lesions in mice share pathological similarities with MS lesions, and the immune response of infected mice appears to play an important role in the pathogenesis of demyelination [46].”
Background
Phenotypic and functional characterization of CD8+ T lymphocytes from the central nervous system of rats with coronavirus JHM induced demyelinating encephalomyelitis.
Hein, A., Schwender, S., Imrich, H., Sopper, S., Czub, M., & Dörries, R. (1995) · Journal of Neurovirology · doi:10.3109/13550289509111023 · Cited by 12
Pathogenesis of Demyelinating Encephalopathy in Dogs with Spontaneous Acute Canine Distemper
Pan, Y., Liu, X.-Y., Meng, L.-P., Zhu, G., Xia, Y., Chen, J.-S., & Yoshikawa, T. (2013) · doi:10.1016/s2095-3119(13)60233-6 · Cited by 11
Oligodendrocyte infection and demyelination produced in mice by the M9 mutant of Semliki Forest virus
Sheahan, B., Gates, M., Caffrey, J., & Atkins, G. (2004) · Acta Neuropathologica · doi:10.1007/bf00691874 · Cited by 11
“The relative importance of these factors in different models has been the subject of intensive investigation (Wisniewski 1977; Dal Canto and Rabinowitz 1982) .”
Background
In vitro cytotoxicity and demyelination induced by theiler viruses in cultures of spinal cord slices
Shahar, A., Frankel, G., David, Y., & Friedmann, A. (1986) · Journal of Neuroscience Research · doi:10.1002/jnr.490160408 · Cited by 11
Facilitation of experimental allergic encephalomyelitis by irradiation and virus infection: role of inflammatory cells
Erälinna, J., Soilu-Hänninen, M., Röyttä, M., Ilonen, J., Mäkelä, M., Salmi, A., & Salonen, R. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90149-x · Cited by 10
Distribution of Theiler's virus in the CNS of athymic nude mice: effect of varying the route of inoculation.
Love, S. (1987) · Journal of Neurological Sciences · doi:10.1016/0022-510x(87)90183-3 · Cited by 10

Authors: Dal Canto, M. C., & Rabinowitz, S. G.
Affiliations: Northwestern University (US)
Venue: Annals of Neurology
Publisher: Wiley
Published: 1982-02
Volume: 11
Issue: 2
Pages: 109-127
ISSN: 0364-5134 (ISSN-L)
1531-8249
DOI: 10.1002/ana.410110202
PMC: PMC7159566
OpenAlex: W2025146338
Cited by: 173
References: 92
Citations by year: 2024: 3 · 2023: 2 · 2022: 1 · 2019: 4 · 2017: 1 · 2016: 4 · 2014: 2 · 2013: 2 · 2012: 3
FWCI: 2.52
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 8284 d)
Locations: Annals of Neurology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Health Sciences › Medicine › Infectious Diseases › Viral Infections and Immunology Research
Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
Keywords: demyelination, multiple sclerosis, viral pathogenesis, animal models, JHM virus, Theiler's virus, visna virus, canine distemper virus, vesicular stomatitis virus, Chandipura virus, herpes simplex virus, Venezuelan equine encephalitis virus, Semliki Forest virus, central nervous system demyelination, immunopathology
MeSH terms: Animals, Antibodies, Viral, Central Nervous System Diseases, Coronaviridae Infections, Demyelinating Diseases, Disease Models, Animal, Distemper, Distemper Virus, Canine, Dogs, Encephalitis Virus, Venezuelan Equine, Maus Elberfeld virus, Enterovirus Infections, Herpes Simplex, Multiple Sclerosis, Pneumonia, Progressive Interstitial, of Sheep, Rhabdoviridae, Sheep, Virus Diseases, Visna-maedi virus

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Experimental models of virus-induced demyelination of the central nervous system

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