CoChat
Sign Up
Cited by 85Chromosomal and Genetic VariationsVirology and Viral DiseasesEvolution and Genetic Dynamics

Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes

Open access
Horie, Masayuki, Kobayashi, Yuki, Suzuki, Yoshiyuki, Tomonaga, Keizo·2013·Philosophical Transactions of the Royal Society B: Biological Sciences
DOI 10.1098/rstb.2012.0499PMC PMC3758186
Open this paper in CoChat — free account

Abstract

Bornaviruses are the only animal RNA viruses that establish a persistent infection in their host cell nucleus. Studies of bornaviruses have provided unique information about viral replication strategies and virus–host interactions. Although bornaviruses do not integrate into the host genome during their replication cycle, we and others have recently reported that there are DNA sequences derived from the mRNAs of ancient bornaviruses in the genomes of vertebrates, including humans, and these have been designated endogenous borna-like (EBL) elements. Therefore, bornaviruses have been interacting with their hosts as driving forces in the evolution of host genomes in a previously unexpected way. Studies of EBL elements have provided new models for virology, evolutionary biology and general cell biology. In this review, we summarize the data on EBL elements including what we have newly identified in eukaryotes genomes, and discuss the biological significance of EBL elements, with a focus on EBL nucleoprotein elements in mammalian genomes. Surprisingly, EBL elements were detected in the genomes of invertebrates, suggesting that the host range of bornaviruses may be much wider than previously thought. We also review our new data on non-retroviral integration of Borna disease virus.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1098/rstb.2012.0499

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Borna disease viruses may have integrated into mammalian genomes over 65 Ma.

    “Borna disease viruses may have integrated into mammalian genomes over 65 Ma (Horie et al. 2013).”

    From RELAX: Detecting Relaxed Selection in a Phylogenetic Framework (2015) · cites this paper as Horie et al. 2013

    The ‘Paleovirology of bornaviruses’ section says that bornavirus-like elements in several mammalian genomes appear to have been established approximately 65 Ma, and that bornavirus infection in mammals may go back to 65 Ma. It does not establish integration over 65 Ma ago. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 78

  1. [1]1. Tomonaga K, Kobayashi T, Ikuta K. 2002 Molecular and cellular biology of Borna disease virus infection. Microbes Infect. 4 , 491-500. (doi:10.1016/S12864579(02)01564-2) · DOI
  2. [3]3. Cros JF, Palese P. 2003 Trafficking of viral genomic RNA into and out of the nucleus: influenza, Thogoto and Borna disease viruses. Virus Res. 95 , 3-12. (doi:10.1016/S0168-1702(03)00159-X) · DOI
  3. [5]5. Matsumoto Y et al . 2012 Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. Cell Host Microbe 11 , 492-503. (doi:10.1016/j.chom.2012. 04.009) · DOI
  4. [6]6. Honda T, Fujino K, Okuzaki D, Ohtaki N, Matsumoto Y, Horie M, Daito T, Itoh M, Tomonaga K. 2011 Upregulation of insulin-like growth factor binding protein 3 in astrocytes of transgenic mice that express Borna disease virus phosphoprotein. J. Virol. 85 , 4567-4571. (doi:10.1128/jvi.01817-10) · DOI
  5. [7]7. Kamitani W et al . 2003 Glial expression of Borna disease virus phosphoprotein induces behavioral and neurological abnormalities in transgenic mice. Proc. Natl Acad. Sci. USA 100 , 8969-8974. (doi:10. 1073/pnas.1531155100)
  6. [8]8. Prat CM, Schmid S, Farrugia F, Cenac N, Le Masson G, Schwemmle M, Gonzalez-Dunia D. 2009 Mutation of the protein kinase C site in Borna disease virus phosphoprotein abrogates viral interference with neuronal signaling and restores normal synaptic activity. PLoS Pathog. 5 , e1000425. (doi:10.1371/journal.ppat.1000425) · DOI
  7. [9]9. Schmid S, Mayer D, Schneider U, Schwemmle M. 2007 Functional characterization of the major and minor phosphorylation sites of the P protein of Borna disease virus. J. Virol. 81 , 5497-5507. (doi:10.1128/jvi.02233-06) · DOI
  8. [10]10. Watanabe Y, Ohtaki N, Hayashi Y, Ikuta K, Tomonaga K. 2009 Autogenous translational regulation of the Borna disease virus negative elements will be helpful in understanding the evolutionary relationships between bornaviruses and their hosts. Acknowledgements. We are grateful to Peter Reuther for giving useful information. M.H. was supported in part by JSPS Postdoctoral Fellowships for Research Abroad. Funding statement. This study was supported in part by the Funding Programme for Next-Generation World-Leading Researchers (NEXT programme) from the Japan Society for the Promotion of Science (JSPS) (K.T). - control factor X from polycistronic mRNA using host RNA helicases. PLoS Pathog. 5 , e1000654. (doi:10. 1371/journal.ppat.1000654)
  9. [12]12. Peng G, Zhang F, Zhang Q, Wu K, Zhu F, Wu J. 2007 Borna disease virus P protein inhibits nitric oxide synthase gene expression in astrocytes. Virology 366 , 446-452. (doi:10.1016/j.virol.2007. 04.031) · DOI
  10. [13]13. Volmer R, Monnet C, Gonzalez-Dunia D. 2006 Borna disease virus blocks potentiation of presynaptic activity through inhibition of protein kinase C signaling. PLoS Pathog. 2 , e19. (doi:10.1371/journal. ppat.0020019) · DOI
  11. [14]14. Schneider U. 2005 Novel insights into the regulation of the viral polymerase complex of neurotropic Borna disease virus. Virus Res. 111 , 148-160. (doi:10.1016/j.virusres.2005.04.006) · DOI
  12. [15]15. Chase G, Mayer D, Hildebrand A, Frank R, Hayashi Y, Tomonaga K, Schwemmle M. 2007 Borna disease virus matrix protein is an integral component of the viral ribonucleoprotein complex that does not interfere with polymerase activity. J. Virol. 81 , 743-749. (doi:10.1128/jvi.01351-06) · DOI
  13. [17]17. Clemente R, Sisman E, Aza-Blanc P, de la Torre JC. 2010 Identification of host factors involved in Borna disease virus cell entry through a small interfering RNA functional genetic screen. J. Virol. 84 , 3562-3575. (doi:10.1128/jvi.02274-09) · DOI
  14. [20]20. Honda T, Horie M, Daito T, Ikuta K, Tomonaga K. 2009 Molecular chaperone BiP interacts with Borna disease virus glycoprotein at the cell surface. - J. Virol. 83 , 12 622-12 625. (doi:10.1128/jvi. 01201-09) · DOI
  15. [21]21. Perez M, Watanabe M, Whitt MA, de la Torre JC. 2001 N-terminal domain of Borna disease virus G ( p56) protein is sufficient for virus receptor recognition and cell entry. J. Virol. 75 , 7078-7085. (doi:10.1128/jvi.75.15.7078-7085.2001) · DOI
  16. [22]22. Poenisch M, Wille S, Ackermann A, Staeheli P, Schneider U. 2007 The X protein of Borna disease virus serves essential functions in the viral multiplication cycle. J. Virol. 81 , 7297-7299. (doi:10.1128/jvi.02468-06) · DOI
  17. [23]23. Poenisch M, Staeheli P, Schneider U. 2008 Viral accessory protein X stimulates the assembly of functional Borna disease virus polymerase complexes. J. Gen. Virol. 89 , 1442-1445. (doi:10.1099/vir.0.2008/000638-0) · DOI
  18. [24]24. Poenisch M, Burger N, Staeheli P, Bauer G, Schneider U. 2009 Protein X of Borna disease virus inhibits apoptosis and promotes viral persistence in the central nervous systems of newborn-infected rats. J. Virol. 83 , 4297-4307. (doi:10.1128/jvi. 02321-08) · DOI
  19. [25]25. Hayashi Y, Horie M, Daito T, Honda T, Ikuta K, Tomonaga K. 2009 Heat shock cognate protein 70 controls Borna disease virus replication via interaction with the viral non-structural protein X. Microbes Infect. 11 , 394-402. (doi:10.1016/j.micinf. 2009.01.006) · DOI
  20. [26]26. Berg M, Johansson M, Montell H, Berg AL. 2001 Wild birds as a possible natural reservoir of Borna disease virus. Epidemiol. Infect. 127 , 173-178. (doi:10.1017/S0950268801005702) · DOI
  21. [27]27. Gosztonyi G. 2008 Natural and experimental Borna disease virus infections: neuropathology and pathogenetic considerations. APMIS Suppl. 116 , 53-57. (doi:10.1111/j.1600-0463.2008. 000m8.x) · DOI
  22. [28]28. Malkinson M, Weisman Y, Ashash E, Bode L, Ludwig H. 1993 Borna disease in ostriches. Vet. Rec. 133 , 304. (doi:10.1136/vr.133.12.304-b) · DOI
  23. [30]30. Rott R, Herzog S, Fleischer B, Winokur A, Amsterdam J, Dyson W, Koprowski H. 1985 Detection of serum antibodies to Borna disease virus in patients with psychiatric disorders. Science 228 , 755-756. (doi:10.1126/science.3922055) · DOI
  24. [31]31. Hornig M et al . 2012 Absence of evidence for bornavirus infection in schizophrenia, bipolar disorder and major depressive disorder. Mol. Psychiatry 17 , 486-493. (doi:10.1038/mp. 2011.179) · DOI
  25. [32]32. Hilbe M, Herrsche R, Kolodziejek J, Nowotny N, Zlinszky K, Ehrensperger F. 2006 Shrews as reservoir hosts of Borna disease virus. Emerg. Infect. Dis. 12 , 675-677. (doi:10.3201/eid1204.051418) · DOI
  26. [33]33. Puorger ME, Hilbe M, Muller JP, Kolodziejek J, Nowotny N, Zlinszky K, Ehrensperger F. 2010 Distribution of Borna disease virus antigen and RNA in tissues of naturally infected bicolored white-toothed shrews, Crocidura leucodon , supporting their role as reservoir host species. Vet. Pathol. 47 , 236-244. (doi:10.1177/03009 85809351849) · DOI
  27. [35]35. Nowotny N, Kolodziejek J, Jehle CO, Suchy A, Staeheli P, Schwemmle M. 2000 Isolation and characterization of a new subtype of Borna disease virus. J. Virol. 74 , 5655-5658. (doi:10.1128/JVI.74. 12.5655-5658.2000) · DOI
  28. [37]37. Kistler AL et al . 2008 Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virol. J. 5 , 88. (doi:10.1186/1743-422x-5-88) · DOI
  29. [38]38. Gregory CR, Latimer KS, Niagro FD, Ritchie BW, Campagnoil RP, Norton TM, McManamon R, Greenacre CB. 1994 A review of proventricular dilatation syndrome. J. Assoc. Avian Veterinarians 8 , 69-75. (doi:10.2307/27671120) · DOI
  30. [39]39. Gancz AY et al . 2009 Experimental induction of proventricular dilatation disease in cockatiels ( Nymphicus hollandicus ) inoculated with brain homogenates containing avian bornavirus 4. Virol. J. 6 , 100. (doi:10.1186/1743-422x-6-100) · DOI
  31. [41]41. De Kloet SR, Dorrestein GM. 2009 Presence of avian bornavirus RNA and anti-avian bornavirus antibodies in apparently healthy macaws. Avian Dis. 53 , 568-573. (doi:10.1637/8828-040209-reg.1) · DOI
  32. [42]42. Horie M, Ueda K, Ueda A, Honda T, Tomonaga K. 2012 Detection of avian bornavirus 5 RNA in Eclectus roratus with feather picking disorder. Microbiol. Immunol. 56 , 346-349. (doi:10.1111/j. 1348-0421.2012.00436.x) · DOI
  33. [43]43. Kistler AL, Smith JM, Greninger AL, Derisi JL, Ganem D. 2010 Analysis of naturally occurring avian bornavirus infection and transmission during an outbreak of proventricular dilatation disease among captive psittacine birds. J. Virol. 84 , 2176-2179. (doi:10.1128/jvi.02191-09) · DOI
  34. [44]44. Weissenbock H, Sekulin K, Bakonyi T, Hogler S, Nowotny N. 2009 Novel avian bornavirus in a nonpsittacine species (canary; Serinus canaria ) with enteric ganglioneuritis and encephalitis. J. Virol. 83 , 11 367-11 371. (doi:10.1128/jvi.01343-09) · DOI
  35. [45]45. Payne S, Covaleda L, Jianhua G, Swafford S, Baroch J, Ferro PJ, Lupiani B, Heatley J, Tizard I. 2011 Detection and characterization of a distinct bornavirus lineage from healthy Canada geese ( Branta canadensis ). J. Virol. 85 , 12 053-12 056. (doi:10.1128/jvi.05700-11) · DOI
  36. [46]46. Delnatte P, Berkvens C, Kummrow M, Smith DA, Campbell D, Crawshaw G, Ojkic D, DeLay J. 2011 New genotype of avian bornavirus in wild geese and trumpeter swans in Canada. Vet. Rec. 169 , 108. (doi:10.1136/vr.d4620) · DOI
  37. [47]47. Guo J, Covaleda L, Heatley JJ, Baroch JA, Tizard I, Payne SL. 2012 Widespread avian bornavirus infection in mute swans in the northeast United States. Vet. Med. 3 , 49-52. (doi:10.2147/VMRR. S33353) · DOI
  38. [48]48. Weissenbock H et al . 2009 Avian bornaviruses in psittacine birds from Europe and Australia with proventricular dilatation disease. Emerg. Infect. Dis. 15 , 1453-1459. (doi:10.3201/eid1509.090353) · DOI
  39. [49]49. Rubbenstroth D, Rinder M, Kaspers B, Staeheli P. 2012 Efficient isolation of avian bornaviruses (ABV) from naturally infected psittacine birds and identification of a new ABV genotype from a salmon-crested cockatoo ( Cacatua moluccensis ). Vet. Microbiol. 161 , 36-42. (doi:10.1016/j.vetmic. 2012.07.004) · DOI
  40. [50]50. Rubbenstroth D et al . 2013 Avian bornaviruses are widely distributed in canary birds ( Serinus canaria f. domestica). Vet. Microbiol. 165 , 287-295. (doi:10.1016/j.vetmic.2013.03.024) · DOI
  41. [51]51. Horie M et al . 2010 Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463 , 84-87. (doi:10.1038/nature08695) · DOI
  42. [52]52. Fujino K, Horie M, Honda T, Nakamura S, Matsumoto Y, Francischetti IM, Tomonaga K. 2012 Evolutionarily conserved interaction between the phosphoproteins and X proteins of bornaviruses from different vertebrate species. PLoS ONE 7 , e51161. (doi:10.1371/journal.pone.0051161) · DOI
  43. [53]53. Jern P, Coffin JM. 2008 Effects of retroviruses on host genome function. Annu. Rev. Genet. 42 , 709732. (doi:10.1146/annurev.genet.42.110807.091501) · DOI · Paper page
  44. [54]54. Lander ES et al . 2001 Initial sequencing and analysis of the human genome. Nature 409 , 860-921. (doi:10.1038/35057062) · DOI · Paper page
  45. [55]55. Waterston RH et al . 2002 Initial sequencing and comparative analysis of the mouse genome. Nature 420 , 520-562. (doi:10.1038/nature01262) · DOI · Paper page
  46. [56]56. Weiss RA. 2006 The discovery of endogenous retroviruses. Retrovirology 3 , 67. (doi:10.1186/17424690-3-67) · DOI
  47. [57]57. Geuking MB, Weber J, Dewannieux M, Gorelik E, Heidmann T, Hengartner H, Zinkernagel RM, Hangartner L. 2009 Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 323 , 393-396. (doi:10.1126/science.1167375) · DOI
  48. [58]58. Klenerman P, Hengartner H, Zinkernagel RM. 1997 A non-retroviral RNA virus persists in DNA form. Nature 390 , 298-301. (doi:10.1038/36876) · DOI
  49. [59]59. Zhdanov VM. 1975 Integration of viral genomes. Nature 256 , 471-473. (doi:10.1038/256471a0) · DOI
  50. [60]60. Crochu S, Cook S, Attoui H, Charrel RN, De Chesse R, Belhouchet M, Lemasson JJ, de Micco P, de Lamballerie X. 2004 Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J. Gen. Virol. 85 , 1971-1980. (doi:10.1099/vir.0.79850-0) · DOI
  51. [61]61. Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I. 2007 Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intraand inter-species recombination. J. Gen. Virol. 88 , 3428-3438. (doi:10.1099/vir.0.83284-0) · DOI
  52. [62]62. Tanne E, Sela I. 2005 Occurrence of a DNA sequence of a non-retro RNA virus in a host plant genome and its expression: evidence for recombination between viral and host RNAs. Virology 332 , 614-622. (doi:10.1016/j.virol.2004.11.007) · DOI
  53. [63]63. Belyi VA, Levine AJ, Skalka AM. 2010 Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog. 6 , e1001030. (doi:10.1371/journal.ppat.1001030) · DOI
  54. [64]64. Katzourakis A, Gifford RJ. 2010 Endogenous viral elements in animal genomes. PLoS Genet. 6 , e1001191. (doi:10.1371/journal.pgen.1001191) · DOI
  55. [65]65. Kinnunen PM et al . 2011 Intracerebral Borna disease virus infection of bank voles leading to peripheral spread and reverse transcription of viral RNA. PLoS ONE 6 , e23622. (doi:10.1371/journal.pone.0023622) · DOI
  56. [66]66. Rauer M, Gotz J, Schuppli D, Staeheli P, Hausmann J. 2004 Transgenic mice expressing the nucleoprotein of Borna disease virus in either neurons or astrocytes: decreased susceptibility to homotypic infection and disease. J. Virol. 78 , 3621-3632. (doi:10.1128/JVI.78.7.3621-3632.2004) · DOI
  57. [67]67. Whelan SP, Barr JN, Wertz GW. 2004 Transcription and replication of nonsegmented negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283 , 61-119. (doi:10.1007/978-3-662-06099-5\_3) · DOI
  58. [68]68. Zhang Z, Carriero N, Gerstein M. 2004 Comparative analysis of processed pseudogenes in the mouse and human genomes. Trends Genet. 20 , 62-67. (doi:10.1016/j.tig.2003.12.005) · DOI
  59. [69]69. O'Leary MA et al . 2013 The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339 , 662-667. (doi:10.1126/science. 1229237) · DOI · Paper page
  60. [74]74. Gilbert N, Lutz-Prigge S, Moran JV. 2002 Genomic deletions created upon LINE-1 retrotransposition. Cell 110 , 315-325. (doi:10.1016/S00928674(02)00828-0) · DOI
  61. [75]75. Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, Taccioli GE, Batzer MA, Moran JV. 2002 DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat. Genet. 31 , 159-165. (doi:10.1038/ng898) · DOI
  62. [77]77. Ohshima K, Hattori M, Yada T, Gojobori T, Sakaki Y, Okada N. 2003 Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates. Genome Biol. 4 , R74. (doi:10.1186/gb-2003-4-11-r74) · DOI
  63. [78]78. Aswad A, Katzourakis A. 2012 Paleovirology and virally derived immunity. Trends Ecol. Evol. 27 , 627-636. (doi:10.1016/j.tree.2012.07.007) · DOI
  64. [79]79. Blaise S, de Parseval N, Benit L, Heidmann T. 2003 Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2 , a gene conserved on primate evolution. Proc. Natl Acad. Sci. USA 100 , 13 013-13 018. (doi:10.1073/ pnas.2132646100)
  65. [80]80. Dupressoir A, Marceau G, Vernochet C, Benit L, Kanellopoulos C, Sapin V, Heidmann T. 2005 Syncytin-A and syncytin-B , two fusogenic placentaspecific murine envelope genes of retroviral origin conserved in Muridae. Proc. Natl Acad. Sci. USA 102 , 725-730. (doi:10.1073/pnas.0406509102) · DOI
  66. [81]81. Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, Opolon P, Heidmann T. 2009 Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirusderived, envelope gene. Proc. Natl Acad. Sci. USA
  67. [10]10. 106 , 12 127-12 132. (doi:10.1073/pnas. 0902925106) · DOI
  68. [84]84. Kobayashi Y, Horie M, Tomonaga K, Suzuki Y. 2011 No evidence for natural selection on endogenous borna-like nucleoprotein elements after the divergence of Old World and New World monkeys. PLoS ONE 6 , e24403. (doi:10.1371/journal.pone. 0024403) · DOI
  69. [85]85. Goic B et al . 2013 RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila . Nat. Immunol. 14 , 396-403. (doi:10.1038/ni.2542) · DOI
  70. [88]88. Schneider U, Naegele M, Staeheli P, Schwemmle M. 2003 Active Borna disease virus polymerase complex requires a distinct nucleoprotein-tophosphoprotein ratio but no viral X protein. J. Virol. 77 , 11 781-11 789. (doi:10.1128/JVI.77.21.1178111789.2003) · DOI
  71. [91]91. Obolenskaya EV, Lee MY, Dokuchaev NE, Oshida T, Lee MS, Lee H, Lissovsky AA. 2009 Diversity of Palaearctic chipmunks ( Tamias , Sciuridae). Mammalia 73 , 281-298. (doi:10.1515/MAMM. 2009.047) · DOI
  72. [92]92. Platt II RN, Ray DA. 2012 A non-LTR retroelement extinction in Spermophilus tridecemlineatus . 500 , 47-53. (doi:10.1016/j.gene.2012.03.051) · DOI
  73. [93]93. Arnaud F et al . 2007 A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog. 3 , e170. (doi:10.1371/journal.ppat. 0030170) · DOI
  74. [96]96. Brnic D, Stevanovic V, Cochet M, Agier C, Richardson J, Montero-Menei CN, Milhavet O, Eloit M, Coulpier M. 2012 Borna disease virus infects human neural progenitor cells and impairs neurogenesis. J. Virol. 86 , 2512-2522. (doi:10.1128/jvi.05663-11) · DOI
  75. [97]97. Coufal NG et al . 2009 L1 retrotransposition in human neural progenitor cells. Nature 460 , 1127-1131. (doi:10.1038/nature08248) · DOI · Paper page
  76. [98]98. Daito T, Fujino K, Honda T, Matsumoto Y, Watanabe Y, Tomonaga K. 2011 A novel Borna disease virus vector system that stably expresses foreign proteins from an intercistronic noncoding region. J. Virol. 85 , 12 170-12 178. (doi:10.1128/jvi.05554-11) · DOI
  77. [99]99. Jordan A, Bisgrove D, Verdin E. 2003 HIV reproducibly establishes a latent infection after acute infection of T cells in vitro . EMBO J. 22 , 1868-1877. (doi:10.1093/emboj/cdg188) · DOI · Paper page
  78. [100]100. Coffin JM, Hughes SH, Varmus HE. (eds) 1997 Retroviruses . Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. Experimental Applications. Available at http://www.ncbi.nlm.nih.gov/books/ NBK19399/.

Cited by

Sorted by citations

Authors
Horie, M., Kobayashi, Y., Suzuki, Y., & Tomonaga, K.
Affiliations
  • University of Freiburg (DE)
  • Nihon University (JP)
  • Nagoya City University (JP)
  • Department of Viral Oncology, Institute for Virus Research, Kyoto University, Kyoto 606-8507, Japan
Corresponding author
Horie, Masayuki
ORCID
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2013-09-19
Volume
368
Issue
1626
Pages
20120499
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
DOI
10.1098/rstb.2012.0499
PMC
PMC3758186
OpenAlex
W2138559742
Cited by
85
References
0
Citations by year
2026: 3 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 13 · 2019: 8 · 2018: 9 · 2017: 6 · 2016: 13 · 2015: 6 · 2014: 5 · 2013: 1
FWCI
0.87
Type
journal article
Language
en
Open access
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
bornavirus, Borna disease virus, host-virus interaction, host genome evolution, mammalian genomes, invertebrate genomes, host range
MeSH terms
Animals, Biological Evolution, Humans, Nucleoproteins, Virus Replication, Genome, Mononegavirales Infections, Bornaviridae, Eukaryota

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review