Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection

Yusuke Matsumoto, Yohei Hayashi, Hiroko Omori, Tomoyuki Honda, Takuji Daito, Masayuki Horie, Kazuyoshi Ikuta, Kan Fujino, Shoko Nakamura, Urs Schneider, Geoffrey Chase, Tamotsu Yoshimori, Martin Schwemmle, Keizo Tomonaga

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Bornaviruses are nonsegmented negative-strand RNA viruses that establish a persistent infection in the nucleus and occasionally integrate a DNA genome copy into the host chromosomal DNA. However, how these viruses achieve intranuclear infection remains unclear. We show that Borna disease virus (BDV), a mammalian bornavirus, closely associates with the cellular chromosome to ensure intranuclear infection. BDV generates viral factories within the nucleus using host chromatin as a scaffold. In addition, the viral ribonucleoprotein (RNP) interacts directly with the host chromosome throughout the cell cycle, using core histones as a docking platform. HMGB1, a host chromatin-remodeling DNA architectural protein, is required to stabilize RNP on chromosomes and for efficient BDV RNA transcription in the nucleus. During metaphase, the association of RNP with mitotic chromosomes allows the viral RNA to segregate into daughter cells and ensure persistent infection. Thus, bornaviruses likely evolved a chromosome-dependent life cycle to achieve stable intranuclear infection.

Original languageEnglish (US)
Pages (from-to)492-503
Number of pages12
JournalCell Host and Microbe
Volume11
Issue number5
DOIs
StatePublished - May 17 2012
Externally publishedYes

Fingerprint

Bornaviridae
Borna disease virus
Chromosomes
Ribonucleoproteins
Infection
DNA
HMGB1 Protein
Chromatin Assembly and Disassembly
RNA Viruses
Viral RNA
Metaphase
Life Cycle Stages
Histones
Chromatin
Cell Cycle
Genome
RNA
Viruses

ASJC Scopus subject areas

  • Immunology and Microbiology(all)
  • Cancer Research
  • Molecular Biology

Cite this

Matsumoto, Y., Hayashi, Y., Omori, H., Honda, T., Daito, T., Horie, M., ... Tomonaga, K. (2012). Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. Cell Host and Microbe, 11(5), 492-503. https://doi.org/10.1016/j.chom.2012.04.009

Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. / Matsumoto, Yusuke; Hayashi, Yohei; Omori, Hiroko; Honda, Tomoyuki; Daito, Takuji; Horie, Masayuki; Ikuta, Kazuyoshi; Fujino, Kan; Nakamura, Shoko; Schneider, Urs; Chase, Geoffrey; Yoshimori, Tamotsu; Schwemmle, Martin; Tomonaga, Keizo.

In: Cell Host and Microbe, Vol. 11, No. 5, 17.05.2012, p. 492-503.

Research output: Contribution to journalArticle

Matsumoto, Y, Hayashi, Y, Omori, H, Honda, T, Daito, T, Horie, M, Ikuta, K, Fujino, K, Nakamura, S, Schneider, U, Chase, G, Yoshimori, T, Schwemmle, M & Tomonaga, K 2012, 'Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection', Cell Host and Microbe, vol. 11, no. 5, pp. 492-503. https://doi.org/10.1016/j.chom.2012.04.009
Matsumoto, Yusuke ; Hayashi, Yohei ; Omori, Hiroko ; Honda, Tomoyuki ; Daito, Takuji ; Horie, Masayuki ; Ikuta, Kazuyoshi ; Fujino, Kan ; Nakamura, Shoko ; Schneider, Urs ; Chase, Geoffrey ; Yoshimori, Tamotsu ; Schwemmle, Martin ; Tomonaga, Keizo. / Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. In: Cell Host and Microbe. 2012 ; Vol. 11, No. 5. pp. 492-503.
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