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

Cell Host and Microbe

Volumn 11, Issue 5, 2012, Pages 492-503

  Matsumoto, Yusuke ^a,b   Hayashi, Yohei ^b,f   Omori, Hiroko ^b   Honda, Tomoyuki ^a   Daito, Takuji ^a,g   Horie, Masayuki ^a,c   Ikuta, Kazuyoshi ^b   Fujino, Kan ^a,b   Nakamura, Shoko ^a   Schneider, Urs ^c   Chase, Geoffrey ^c   Yoshimori, Tamotsu ^d   Schwemmle, Martin ^c   Tomonaga, Keizo ^a,e  

^a KYOTO UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF FREIBURG   (Germany)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^g NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; HISTONE; RIBONUCLEOPROTEIN; SCAFFOLD PROTEIN; VIRUS RNA;

ARTICLE; BORNA DISEASE VIRUS; CELL CYCLE; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; HOST CELL; HOST CHROMOSOME; INFECTION; INTRANUCLEAR INFECTION; METAPHASE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; RNA TRANSCRIPTION;

BORNA DISEASE VIRUS; CELL CYCLE; CELL LINE; CELL NUCLEUS; CHROMOSOME SEGREGATION; HISTONES; HMGB1 PROTEIN; HOST-PATHOGEN INTERACTIONS; HUMANS; NUCLEOPROTEINS; PROTEIN BINDING; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRAL PROTEINS; VIRUS REPLICATION;

BORNA DISEASE VIRUS; BORNAVIRUS; MAMMALIA; RNA VIRUSES;

EID: 84861166952     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.04.009     Document Type: Article

References (39)

1. A. Agresti, P. Scaffidi, A. Riva, V.R. Caiolfa, and M.E. Bianchi GR and HMGB1 interact only within chromatin and influence each other's residence time Mol. Cell 18 2005 109 121
2. M.E. Ballestas, P.A. Chatis, and K.M. Kaye Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen Science 284 1999 641 644
3. A.J. Barbera, J.V. Chodaparambil, B. Kelley-Clarke, V. Joukov, J.C. Walter, K. Luger, and K.M. Kaye The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA Science 311 2006 856 861
4. V.A. Belyi, A.J. Levine, and A.M. Skalka Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes PLoS Pathog. 6 2010 e1001030 10.1371/journal.ppat.1001030
5. M.E. Bianchi, and A. Agresti HMG proteins: dynamic players in gene regulation and differentiation Curr. Opin. Genet. Dev. 15 2005 496 506
6. T. Bonaldi, G. Langst, R. Strohner, P.B. Becker, and M.E. Bianchi The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding EMBO J. 21 2002 6865 6873
7. D. Brnic, V. Stevanovic, M. Cochet, C. Agier, J. Richardson, C.N. Montero-Menei, O. Milhavet, M. Eloit, and M. Coulpier Borna disease virus infects human neural progenitor cells and impairs neurogenesis J. Virol. 86 2012 2512 2522
8. A. Calado, and M. Carmo-Fonseca Localization of poly(A)-binding protein 2 (PABP2) in nuclear speckles is independent of import into the nucleus and requires binding to poly(A) RNA J. Cell Sci. 113 2000 2309 2318
9. K.M. Carbone, T.R. Moench, and W.I. Lipkin Borna disease virus replicates in astrocytes, Schwann cells and ependymal cells in persistently infected rats: location of viral genomic and messenger RNAs by in situ hybridization J. Neuropathol. Exp. Neurol. 50 1991 205 214
10. F. Catez, and R. Hock Binding and interplay of HMG proteins on chromatin: lessons from live cell imaging Biochim. Biophys. Acta 1799 2009 15 27
11. G. Chase, D. Mayer, A. Hildebrand, R. Frank, Y. Hayashi, K. Tomonaga, and M. Schwemmle Borna disease virus matrix protein is an integral component of the viral ribonucleoprotein complex that does not interfere with polymerase activity J. Virol. 81 2007 743 749
12. K.M. Feeney, and J.L. Parish Targeting mitotic chromosomes: a conserved mechanism to ensure viral genome persistence Proc. Biol. Sci. 276 2009 1535 1544
13. L.R. Friend, S.P. Han, J.A. Rothnagel, and R. Smith Differential subnuclear localisation of hnRNPs A/B is dependent on transcription and cell cycle stage Biochim. Biophys. Acta 1783 2008 1972 1980
14. D. Gonzalez-Dunia, B. Cubitt, F.A. Grasser, and J.C. de la Torre Characterization of Borna disease virus p56 protein, a surface glycoprotein involved in virus entry J. Virol. 71 1997 3208 3218
15. K. Hagiwara, W. Kamitani, S. Takamura, H. Taniyama, T. Nakaya, H. Tanaka, R. Kirisawa, H. Iwai, and K. Ikuta Detection of Borna disease virus in a pregnant mare and her fetus Vet. Microbiol. 72 2000 207 216
16. M. Hock, I. Kraus, G. Schoehn, M. Jamin, C. Andrei-Selmer, W. Garten, and W. Weissenhorn RNA induced polymerization of the Borna disease virus nucleoprotein Virology 397 2010 64 72
17. M. Horie, T. Honda, Y. Suzuki, Y. Kobayashi, T. Daito, T. Oshida, K. Ikuta, P. Jern, T. Gojobori, and J.M. Coffin Endogenous non-retroviral RNA virus elements in mammalian genomes Nature 463 2010 84 87
18. W. Kamitani, Y. Shoya, T. Kobayashi, M. Watanabe, B.J. Lee, G. Zhang, K. Tomonaga, and K. Ikuta Borna disease virus phosphoprotein binds a neurite outgrowth factor, amphoterin/HMG-1 J. Virol. 75 2001 8742 8751
19. A. Krithivas, M. Fujimuro, M. Weidner, D.B. Young, and S.D. Hayward Protein interactions targeting the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus to cell chromosomes J. Virol. 76 2002 11596 11604
20. X. Lahaye, A. Vidy, C. Pomier, L. Obiang, F. Harper, Y. Gaudin, and D. Blondel Functional characterization of Negri bodies (NBs) in rabies virus-infected cells: evidence that NBs are sites of viral transcription and replication J. Virol. 83 2009 7948 7958
21. C.W. Lehman, and M.R. Botchan Segregation of viral plasmids depends on tethering to chromosomes and is regulated by phosphorylation Proc. Natl. Acad. Sci. USA 95 1998 4338 4343
22. P. Menager, P. Roux, F. Megret, J.P. Bourgeois, A.M. Le Sourd, A. Danckaert, M. Lafage, C. Prehaud, and M. Lafon Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies PLoS Pathog. 5 2009 e1000315 10.1371/journal.ppat.1000315
23. S. Muller, L. Ronfani, and M.E. Bianchi Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function J. Intern. Med. 255 2004 332 343
24. Y. Nakamura, H. Takahashi, Y. Shoya, T. Nakaya, M. Watanabe, K. Tomonaga, K. Iwahashi, K. Ameno, N. Momiyama, and H. Taniyama Isolation of Borna disease virus from human brain tissue J. Virol. 74 2000 4601 4611
25. M. Okamoto, K. Hagiwara, W. Kamitani, T. Sako, K. Hirayama, R. Kirisawa, M. Tsuji, C. Ishihara, H. Iwai, and T. Kobayashi Experimental vertical transmission of Borna disease virus in the mouse Arch. Virol. 148 2003 1557 1568
26. R.D. Phair, P. Scaffidi, C. Elbi, J. Vecerova, A. Dey, K. Ozato, D.T. Brown, G. Hager, M. Bustin, and T. Misteli Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins Mol. Cell. Biol. 24 2004 6393 6402
27. T. Piolot, M. Tramier, M. Coppey, J.C. Nicolas, and V. Marechal Close but distinct regions of human herpesvirus 8 latency-associated nuclear antigen 1 are responsible for nuclear targeting and binding to human mitotic chromosomes J. Virol. 75 2001 3948 3959
28. K.V. Prasanth, P.A. Sacco-Bubulya, S.G. Prasanth, and D.L. Spector Sequential entry of components of the gene expression machinery into daughter nuclei Mol. Biol. Cell 14 2003 1043 1057
29. U. Schneider Novel insights into the regulation of the viral polymerase complex of neurotropic Borna disease virus Virus Res. 111 2005 148 160
30. U. Schneider, M. Naegele, P. Staeheli, and M. Schwemmle Active borna disease virus polymerase complex requires a distinct nucleoprotein-to- phosphoprotein ratio but no viral X protein J. Virol. 77 2003 11781 11789
31. U. Schneider, A. Martin, M. Schwemmle, and P. Staeheli Genome trimming by Borna disease viruses: viral replication control or escape from cellular surveillance? Cell. Mol. Life Sci. 64 2007 1038 1042
32. M. Schwemmle, M. Salvatore, L. Shi, J. Richt, C.H. Lee, and W.I. Lipkin Interactions of the borna disease virus P, N, and X proteins and their functional implications J. Biol. Chem. 273 1998 9007 9012
33. P. Staeheli, C. Sauder, J. Hausmann, F. Ehrensperger, and M. Schwemmle Epidemiology of Borna disease virus J. Gen. Virol. 81 2000 2123 2135
34. M. Stros HMGB proteins: interactions with DNA and chromatin Biochim. Biophys. Acta 1799 2010 101 113
35. E. Suberbielle, A. Stella, F. Pont, C. Monnet, E. Mouton, L. Lamouroux, B. Monsarrat, and D. Gonzalez-Dunia Proteomic analysis reveals selective impediment of neuronal remodeling upon Borna disease virus infection J. Virol. 82 2008 12265 12279
36. K. Tomonaga Mechanism of nuclear transport and persistent infection of Borna disease virus Tanpakushitsu Kakusan Koso 52 Suppl 10 2007 1168 1174
37. K. Tomonaga, T. Kobayashi, and K. Ikuta Molecular and cellular biology of Borna disease virus infection Microbes Infect. 4 2002 491 500
38. J. You, J.L. Croyle, A. Nishimura, K. Ozato, and P.M. Howley Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes Cell 117 2004 349 360
39. G. Zhang, T. Kobayashi, W. Kamitani, S. Komoto, M. Yamashita, S. Baba, H. Yanai, K. Ikuta, and K. Tomonaga Borna disease virus phosphoprotein represses p53-mediated transcriptional activity by interference with HMGB1 J. Virol. 77 2003 12243 12251