Mouse Adenovirus Type 1-Induced Breakdown of the Blood-Brain Barrier

Gralinski, Lisa E.; Ashley, Shanna L.; Dixon, Shandee D.; Spindler, Katherine R.

doi:10.1128/jvi.00954-09

Cited by 70Barrier Structure and Function StudiesVirus-based gene therapy researchInfectious Encephalopathies and Encephalitis

Mouse Adenovirus Type 1-Induced Breakdown of the Blood-Brain Barrier

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Gralinski, Lisa E., Ashley, Shanna L., Dixon, Shandee D., Spindler, Katherine R.·2009·Journal of Virology

DOI 10.1128/jvi.00954-09PMC PMC2738240

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Abstract

Infection with mouse adenovirus type 1 (MAV-1) results in fatal acute encephalomyelitis in susceptible mouse strains via infection of brain endothelial cells. Wild-type (wt) MAV-1 causes less brain inflammation than an early region 3 (E3) null virus in C57BL/6 mice. A mouse brain microvascular endothelial cell line infected with wt MAV-1 had higher expression of mRNAs for the proinflammatory chemokines CCL2 and CCL5 than mock- and E3 null virus-infected cells. Primary mouse brain endothelial cells infected with wt virus had elevated levels of CCL2 compared to mock- or E3 null virus-infected cells. Infection of C57BL/6 mice with wt MAV-1 or the E3 null virus caused a dose-dependent breakdown of the blood-brain barrier, primarily due to direct effects of virus infection rather than inflammation. The tight junction proteins claudin-5 and occludin showed reduced surface expression on primary mouse brain endothelial cells following infection with either wt MAV-1 or the E3 null virus. mRNAs and protein for claudin-5, occludin, and zona occludens 2 were also reduced in infected cells. MAV-1 infection caused a loss of transendothelial electrical resistance in primary mouse brain endothelial cells that was not dependent on E3 or on MAV-1-induced CCL2 expression. Taken together, these results demonstrate that MAV-1 infection caused breakdown of the blood-brain barrier accompanied by decreased surface expression of tight junction proteins. Furthermore, while the MAV-1-induced pathogenesis and inflammation were dependent on E3, MAV-1-induced breakdown of the blood-brain barrier and alteration of endothelial cell function were not dependent on E3 or CCL2.

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Viral infections in general downregulate TJ proteins and promote chemokine production and vascular cell adhesion molecule 1 (VCAM-1) expression in brain endothelial cells, thereby weakening the BBB and facilitating entry into the brain.
“Viral infections in general downregulate TJ proteins and promote chemokine production and vascular cell adhesion molecule 1 (VCAM-1) expression in brain endothelial cells, thereby weakening the BBB and facilitating entry into the brain (5, 212, 399, 613).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [212]
The Results report that mouse adenovirus infection increased chemokine expression in brain endothelial cells; the Discussion reports reduced tight-junction proteins and blood–brain barrier breakdown (pages unavailable). The Results identify VCAM as a marker already expressed by the endothelial cells, not as an infection-induced increase. The paper discusses several viruses, but does not establish this entire sequence as a general mechanism for viral entry into the brain. (LLM, conf=0.88)
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Authors: Gralinski, L. E., Ashley, S. L., Dixon, S. D., & Spindler, K. R.
Affiliations: University of North Carolina at Chapel Hill (US)
ORCID: Gralinski, Lisa E.
Ashley, Shanna L.
Dixon, Shandee D.
Spindler, Katherine R.
Venue: Journal of Virology
Publisher: American Society for Microbiology
Published: 2009-09-15
Volume: 83
Issue: 18
Pages: 9398-9410
ISSN: 0022-538X (ISSN-L)
1098-5514
DOI: 10.1128/jvi.00954-09
PMC: PMC2738240
OpenAlex: W2171534618
Cited by: 70
References: 87
Citations by year: 2026: 1 · 2025: 2 · 2024: 6 · 2023: 3 · 2022: 3 · 2021: 7 · 2020: 1 · 2019: 5 · 2018: 2 · 2017: 5 · 2016: 6 · 2015: 7 · 2014: 2 · 2013: 4 · 2012: 8
FWCI: 3.20
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Virology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (AI007528)
National Institute of Allergy and Infectious Diseases (T32AI007528, R01AI023762)
Topics: Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Health Sciences › Medicine › Infectious Diseases › Infectious Encephalopathies and Encephalitis
Keywords: mouse adenovirus type 1, blood-brain barrier disruption, brain endothelial cells, MCP-1, RANTES, chemokines, tight junction proteins, claudin-5, occludin, ZO-2, transendothelial electrical resistance, encephalomyelitis, viral pathogenesis, C57BL/6 mice
MeSH terms: Adenoviridae, Adenoviridae Infections, Animals, Blood-Brain Barrier, Brain, Inflammation, Membrane Proteins, Mice, Inbred C57BL, Down-Regulation, Connexins, Immediate-Early Proteins, Chemokine CCL2, Tight Junctions, Endothelial Cells, Mice

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Mouse Adenovirus Type 1-Induced Breakdown of the Blood-Brain Barrier

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