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Cited by 14Infectious Encephalopathies and EncephalitisInfluenza Virus Research StudiesVirology and Viral Diseases

Viral entry and translation in brain endothelia provoke influenza-associated encephalopathy

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Kimura-Ohba, Shihoko, Kitamura, Mieko, Tsukamoto, Yusuke, Kogaki, Shigetoyo, Sakai, Shinsuke, Fushimi, Hiroaki, Matsuoka, Keiko, Takeuchi, Makoto +3 more·2024·Acta Neuropathologica
DOI 10.1007/s00401-024-02723-zPMC PMC11061015
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Abstract

Influenza-associated encephalopathy (IAE) is extremely acute in onset, with high lethality and morbidity within a few days, while the direct pathogenesis by influenza virus in this acute phase in the brain is largely unknown. Here we show that influenza virus enters into the cerebral endothelium and thereby induces IAE. Three-weeks-old young mice were inoculated with influenza A virus (IAV). Physical and neurological scores were recorded and temporal-spatial analyses of histopathology and viral studies were performed up to 72 h post inoculation. Histopathological examinations were also performed using IAE human autopsy brains. Viral infection, proliferation and pathogenesis were analyzed in cell lines of endothelium and astrocyte. The effects of anti-influenza viral drugs were tested in the cell lines and animal models. Upon intravenous inoculation of IAV in mice, the mice developed encephalopathy with brain edema and pathological lesions represented by micro bleeding and injured astrocytic process (clasmatodendrosis) within 72 h. Histologically, massive deposits of viral nucleoprotein were observed as early as 24 h post infection in the brain endothelial cells of mouse models and the IAE patients. IAV inoculated endothelial cell lines showed deposition of viral proteins and provoked cell death, while IAV scarcely amplified. Inhibition of viral transcription and translation suppressed the endothelial cell death and the lethality of mouse models. These data suggest that the onset of encephalopathy should be induced by cerebral endothelial infection with IAV. Thus, IAV entry into the endothelium, and transcription and/or translation of viral RNA, but not viral proliferation, should be the key pathogenesis of IAE.

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  • Influenza infection may enter the brain through several routes or send deleterious signals to the brain via sensory neurons and trigger neuroinflammation or associated chronic alterations in the CNS.

    “Influenza infection may enter the brain through several routes [122,123] or send deleterious signals to the brain via sensory neurons [124] and trigger neuroinflammation or associated chronic alterations in the CNS [125].”

    From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [122]

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Cited by

Sorted by citations

Authors
Kimura-Ohba, S., Kitamura, M., Tsukamoto, Y., Kogaki, S., Sakai, S., Fushimi, H., Matsuoka, K., Takeuchi, M., Itoh, K., Ueda, K., & Kimura, T.
Affiliations
  • National Institute of Biomedical Innovation, Health and Nutrition (JP)
  • Osaka Prefectural Medical Center (JP)
  • Osaka Women's and Children's Hospital (JP)
  • Kyoto Prefectural University of Medicine (JP)
  • The University of Osaka (JP)
ORCID
Venue
Acta Neuropathologica
Publisher
Springer Science and Business Media LLC
Published
2024-04-30
Volume
147
Issue
1
Pages
77-77
ISSN
  • 0001-6322 (ISSN-L)
  • 1432-0533
DOI
10.1007/s00401-024-02723-z
PMC
PMC11061015
OpenAlex
W4396518392
Cited by
14
References
0
Citations by year
2026: 7 · 2025: 6 · 2024: 1
FWCI
4.84
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Neuropathologica (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • OUKA (Osaka University Knowledge Archive) (Osaka University) (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by)
Funders
  • Japan Agency for Medical Research and Development (20he08220 08j0001, JP21gm5010001)
  • Japan Society for the Promotion of Science (21K15638, 18J40004)
  • Osaka University
Topics
  • Health Sciences › Medicine › Infectious Diseases › Infectious Encephalopathies and Encephalitis
  • Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
  • Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
Keywords
influenza-associated encephalopathy, influenza A virus, brain endothelium, viral entry, viral RNA translation, viral transcription, endothelial cell death, cerebral edema, viral nucleoprotein, astrocytes, pathogenesis, antiviral agents
MeSH terms
Animals, Brain, Brain Diseases, Disease Models, Animal, Endothelium, Female, Humans, Influenza, Human, Male, Mice, Inbred C57BL, Orthomyxoviridae Infections, Influenza A virus, Endothelial Cells, Mice, Virus Internalization

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