Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system

Phares, Timothy W; Kean, Rhonda B; Mikheeva, Tatiana; Hooper, D Craig

doi:10.4049/jimmunol.176.12.7666

Cited by 193Barrier Structure and Function StudiesRabies epidemiology and controlNeuroinflammation and Neurodegeneration Mechanisms

Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system

Phares, Timothy W, Kean, Rhonda B, Mikheeva, Tatiana, Hooper, D Craig·2006·The Journal of Immunology

DOI 10.4049/jimmunol.176.12.7666

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Abstract

The loss of blood-brain barrier (BBB) integrity in CNS inflammatory responses triggered by infection and autoimmunity has generally been associated with the development of neurological signs. In the present study, we demonstrate that the clearance of the attenuated rabies virus CVS-F3 from the CNS is an exception; increased BBB permeability and CNS inflammation occurs in the absence of neurological sequelae. We speculate that regionalization of the CNS inflammatory response contributes to its lack of pathogenicity. Despite virus replication and the expression of several chemokines and IL-6 in both regions being similar, the up-regulation of MIP-1beta, TNF-alpha, IFN-gamma, and ICAM-1 and the loss of BBB integrity was more extensive in the cerebellum than in the cerebral cortex. The accumulation of CD4- and CD19-positive cells was higher in the cerebellum than the cerebral cortex. Elevated CD19 levels were paralleled by kappa-L chain expression levels. The timing of BBB permeability changes, kappa-L chain expression in CNS tissues, and Ab production in the periphery suggest that the in situ production of virus-neutralizing Ab may be more important in virus clearance than the infiltration of circulating Ab. The data indicate that, with the possible exception of CD8 T cells, the effectors of rabies virus clearance are more commonly targeted to the cerebellum. This is likely the result of differences in the capacity of the tissues of the cerebellum and cerebral cortex to mediate the events required for BBB permeability changes and cell invasion during virus infection.

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Rabies virus-induced encephalitis results in elevation of pro-inflammatory cytokines, and increased TNFα and IFN-γ have been causally linked to increased BBB permeability allowing strong influx of immune factors.
“It has been reported that rabies virus-induced encephalitis results in an elevation of different pro-inflammatory cytokines. Increased levels of TNFα and IFN-γ have been causally linked to increased BBB permeability which also allows the strong influx of immune factors [42,43].”
From An mRNA Vaccine Encoding Rabies Virus Glycoprotein Induces Protection against Lethal Infection in Mice and Correlates of Protection in Adult and Newborn Pigs (2016) · cites this paper as [42]

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Authors: Phares, T. W., Kean, R. B., Mikheeva, T., & Hooper, D. C.
Affiliations: Thomas Jefferson University (US)
ORCID: Hooper, D Craig
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2006-06
Volume: 176
Issue: 12
Pages: 7666-7675
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.176.12.7666
OpenAlex: W1929661393
Cited by: 193
References: 52
Citations by year: 2026: 3 · 2025: 5 · 2024: 5 · 2023: 3 · 2022: 10 · 2021: 7 · 2020: 9 · 2019: 6 · 2018: 6 · 2017: 14 · 2016: 15 · 2015: 18 · 2014: 15 · 2013: 15 · 2012: 8
FWCI: 7.90
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Allergy and Infectious Diseases (AI-09706)
Topics: Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Life Sciences › Immunology and Microbiology › Virology › Rabies epidemiology and control
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: rabies virus, blood-brain barrier permeability, neuroinflammation, cerebellum, cerebral cortex, viral clearance, kappa light chain, virus-neutralizing antibodies, CD19, CD4+ T cells, CD8+ T cells, chemokines, MIP-1β, TNF-α, interferon-gamma, ICAM-1
MeSH terms: Administration, Intranasal, Animals, Antibodies, Viral, Blood-Brain Barrier, Cell Membrane Permeability, Cerebellum, Cerebral Cortex, Female, Inflammation, Interferon-gamma, Male, Mice, Inbred Strains, Rabies, Rabies virus, Tumor Necrosis Factor-alpha, Interleukin-6, Intercellular Adhesion Molecule-1, Chemokines, Mice

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Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system

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