The biological significance of bornavirus-derived genes in mammals

Current Opinion in Virology

Volumn 25, Issue , 2017, Pages 1-6

  Horie, Masayuki ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

BORNAVIRUS; BORNAVIRUS LIKE ELEMENT; CELL FUNCTION; EUKARYOTE; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; VIRUS GENE; ANIMAL; BORNAVIRIDAE; ENDOGENOUS RETROVIRUS; GENETICS; GENOME; HUMAN; HUMAN GENOME; MOLECULAR EVOLUTION; PHYSIOLOGY; RNA VIRUS; VIROLOGY; VIRUS DNA CELL DNA INTERACTION; VIRUS REPLICATION;

ANIMALS; BORNAVIRIDAE; ENDOGENOUS RETROVIRUSES; EUKARYOTA; EVOLUTION, MOLECULAR; GENOME; GENOME, HUMAN; HUMANS; MAMMALS; RNA VIRUSES; VIRUS INTEGRATION; VIRUS REPLICATION;

EID: 85021295212     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2017.06.004     Document Type: Review

References (55)

1. Katzourakis, A., Gifford, R.J., Endogenous viral elements in animal genomes. PLoS Genet, 6, 2010, e1001191.
2. Weiss, R.A., The discovery of endogenous retroviruses. Retrovirology, 3, 2006, 67.
3. Jern, P., Coffin, J.M., Effects of retroviruses on host genome function. Annu Rev Genet 42 (2008), 709–732.
4. Mi, S., Lee, X., Li, X., Veldman, G.M., Finnerty, H., Racie, L., LaVallie, E., Tang, X.Y., Edouard, P., Howes, S., et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403 (2000), 785–789.
5. Blaise, S., de Parseval, N., Benit, L., Heidmann, T., Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci U S A 100 (2003), 13013–13018.
6. Dupressoir, A., Marceau, G., Vernochet, C., Benit, L., Kanellopoulos, C., Sapin, V., Heidmann, T., Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci U S A 102 (2005), 725–730.
7. Dupressoir, A., Vernochet, C., Bawa, O., Harper, F., Pierron, G., Opolon, P., Heidmann, T., Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc Natl Acad Sci U S A 106 (2009), 12127–12132.
8. Horie, M., Honda, T., Suzuki, Y., Kobayashi, Y., Daito, T., Oshida, T., Ikuta, K., Jern, P., Gojobori, T., Coffin, J.M., et al. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463 (2010), 84–87.
9. Horie, M., Kobayashi, Y., Suzuki, Y., Tomonaga, K., Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes. Philos Trans R Soc Lond B Biol Sci, 368, 2013, 20120499.
10. Belyi, V.A., Levine, A.J., Skalka, A.M., Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog, 6, 2010, e1001030.
11. Taylor, D.J., Leach, R.W., Bruenn, J., Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol, 10, 2010, 193.
12. Arriagada, G., Gifford, R.J., Parvovirus-derived endogenous viral elements in two South American rodent genomes. J Virol 88 (2014), 12158–12162.
13. Aswad, A., Katzourakis, A., The first endogenous herpesvirus, identified in the tarsier genome, and novel sequences from primate rhadinoviruses and lymphocryptoviruses. PLoS Genet, 10, 2014, e1004332.
14. Gilbert, C., Meik, J.M., Dashevsky, D., Card, D.C., Castoe, T.A., Schaack, S., Endogenous hepadnaviruses, bornaviruses and circoviruses in snakes. Proc Biol Sci, 281, 2014, 20141122.
15. Cui, J., Wang, L.F., Genomic mining reveals deep evolutionary relationships between bornaviruses and bats. Viruses 7 (2015), 5792–5800.
16. Geisler, C., Jarvis, D.L., Rhabdovirus-like endogenous viral elements in the genome of Spodoptera frugiperda insect cells are actively transcribed: implications for adventitious virus detection. Biologicals 44 (2016), 219–225.
17. Ballinger, M.J., Bruenn, J.A., Taylor, D.J., Phylogeny, integration and expression of sigma virus-like genes in Drosophila. Mol Phylogenet Evol 65 (2012), 251–258.
18. Liu, H., Fu, Y., Jiang, D., Li, G., Xie, J., Cheng, J., Peng, Y., Ghabrial, S.A., Yi, X., Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol 84 (2010), 11876–11887.
19. Belyi, V.A., Levine, A.J., Skalka, A.M., Sequences from ancestral single-stranded DNA viruses in vertebrate genomes: the parvoviridae and circoviridae are more than 40 to 50 million years old. J Virol 84 (2010), 12458–12462.
20. Gilbert, C., Feschotte, C., Genomic fossils calibrate the long-term evolution of hepadnaviruses. PLoS Biol, 2010, 8.
21. Kapoor, A., Simmonds, P., Lipkin, W.I., Discovery and characterization of mammalian endogenous parvoviruses. J Virol 84 (2010), 12628–12635.
22. Lequime, S., Lambrechts, L., Discovery of flavivirus-derived endogenous viral elements in Anopheles mosquito genomes supports the existence of Anopheles-associated insect-specific flaviviruses. Virus Evol, 3, 2017, vew035.
23. Chiba, S., Kondo, H., Tani, A., Saisho, D., Sakamoto, W., Kanematsu, S., Suzuki, N., Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog, 7, 2011, e1002146.
24. Fort, P., Albertini, A., Van-Hua, A., Berthomieu, A., Roche, S., Delsuc, F., Pasteur, N., Capy, P., Gaudin, Y., Weill, M., Fossil rhabdoviral sequences integrated into arthropod genomes: ontogeny, evolution, and potential functionality. Mol Biol Evol 29 (2012), 381–390.
25. Smith, R.H., Hallwirth, C.V., Westerman, M., Hetherington, N.A., Tseng, Y.S., Cecchini, S., Virag, T., Ziegler, M.L., Rogozin, I.B., Koonin, E.V., et al. Germline viral “fossils” guide in silico reconstruction of a mid-Cenozoic era marsupial adeno-associated virus. Sci Rep, 6, 2016, 28965.
26. Liu, H., Fu, Y., Xie, J., Cheng, J., Ghabrial, S.A., Li, G., Peng, Y., Yi, X., Jiang, D., Widespread endogenization of densoviruses and parvoviruses in animal and human genomes. J Virol 85 (2011), 9863–9876.
27. Kuhn, J.H., Durrwald, R., Bao, Y., Briese, T., Carbone, K., Clawson, A.N., deRisi, J.L., Garten, W., Jahrling, P.B., Kolodziejek, J., et al. Taxonomic reorganization of the family Bornaviridae. Arch Virol 160 (2015), 621–632.
28. Stenglein, M.D., Leavitt, E.B., Abramovitch, M.A., McGuire, J.A., DeRisi, J.L., Genome sequence of a bornavirus recovered from an African Garter Snake (Elapsoidea loveridgei). Genome Announc, 2014, 2.
29. Kistler, A.L., Gancz, A., Clubb, S., Skewes-Cox, P., Fischer, K., Sorber, K., Chiu, C.Y., Lublin, A., Mechani, S., Farnoushi, Y., et al. Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virol J, 5, 2008, 88.
30. Honkavuori, K.S., Shivaprasad, H.L., Williams, B.L., Quan, P.L., Hornig, M., Street, C., Palacios, G., Hutchison, S.K., Franca, M., Egholm, M., et al. Novel borna virus in psittacine birds with proventricular dilatation disease. Emerg Infect Dis 14 (2008), 1883–1886.
31. Kinnunen, P.M., Palva, A., Vaheri, A., Vapalahti, O., Epidemiology and host spectrum of Borna disease virus infections. J Gen Virol 94 (2013), 247–262.
32. Hoffmann, B., Tappe, D., Hoper, D., Herden, C., Boldt, A., Mawrin, C., Niederstrasser, O., Muller, T., Jenckel, M., van der Grinten, E., et al. A variegated squirrel bornavirus associated with fatal human encephalitis. N Engl J Med 373 (2015), 154–162.
33. Gray, P., Hoppes, S., Suchodolski, P., Mirhosseini, N., Payne, S., Villanueva, I., Shivaprasad, H.L., Honkavuori, K.S., Lipkin, W.I., Briese, T., et al. Use of avian bornavirus isolates to induce proventricular dilatation disease in conures. Emerg Infect Dis 16 (2010), 473–479.
34. Staeheli, P., Sauder, C., Hausmann, J., Ehrensperger, F., Schwemmle, M., Epidemiology of Borna disease virus. J Gen Virol 81 (2000), 2123–2135.
35. Cui, J., Zhao, W., Huang, Z., Jarvis, E.D., Gilbert, M., Walker, P.J., Holmes, E.C., Zhang, G., Low frequency of paleoviral infiltration across the avian phylogeny. Genome Biol, 15, 2014, 539.
36. Tomonaga, K., Kobayashi, T., Ikuta, K., Molecular and cellular biology of Borna disease virus infection. Microbes Infect 4 (2002), 491–500.
37. 37•• Kobayashi, Y., Horie, M., Nakano, A., Murata, K., Itou, T., Suzuki, Y., Exaptation of bornavirus-like nucleoprotein elements in Afrotherians. PLoS Pathog, 12, 2016, e1005785 This paper analyzed 2 EBLNs in afrotherians that were estimated to be endogenized more than 83.3 MYA, showing the evidences that the EBLNs encodes functional proteins in the hosts.
38. 38• Horie, M., Kobayashi, Y., Honda, T., Fujino, K., Akasaka, T., Kohl, C., Wibbelt, G., Muhldorfer, K., Kurth, A., Muller, M.A., et al. An RNA-dependent RNA polymerase gene in bat genomes derived from an ancient negative-strand RNA virus. Sci Rep, 6, 2016, 25873 This manuscript showed that an EBLL in bats of the genus Eptesicus has maintained a large and intact ORF and functional motifs essential for RdRp activity for more than 11.8 million years.
39. Ikeda, H., Sugimura, H., Fv-4 resistance gene: a truncated endogenous murine leukemia virus with ecotropic interference properties. J Virol 63 (1989), 5405–5412.
40. Taylor, G.M., Gao, Y., Sanders, D.A., Fv-4: identification of the defect in Env and the mechanism of resistance to ecotropic murine leukemia virus. J Virol 75 (2001), 11244–11248.
41. Mura, M., Murcia, P., Caporale, M., Spencer, T.E., Nagashima, K., Rein, A., Palmarini, M., Late viral interference induced by transdominant Gag of an endogenous retrovirus. Proc Natl Acad Sci U S A 101 (2004), 11117–11122.
42. Aswad, A., Katzourakis, A., Paleovirology and virally derived immunity. Trends Ecol Evol 27 (2012), 627–636.
43. Honda, T., Tomonaga, K., Endogenous non-retroviral RNA virus elements evidence a novel type of antiviral immunity. Mob Genet Elements, 6, 2016, e1165785.
44. Suzuki, Y., Kobayashi, Y., Horie, M., Tomonaga, K., Origin of an endogenous bornavirus-like nucleoprotein element in thirteen-lined ground squirrels. Genes Genet Syst 89 (2014), 143–148.
45. 45•• Fujino, K., Horie, M., Honda, T., Merriman, D.K., Tomonaga, K., Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome. Proc Natl Acad Sci U S A 111 (2014), 13175–13180 This study showed that exogenous expression of an EBLN in the thirteen-lined ground squirrel inhibits bornavirus replication. This is the first report showing that non-retroviral EVEs may act as antiviral genes in the host cells.
46. Tarlinton, R.E., Meers, J., Young, P.R., Retroviral invasion of the koala genome. Nature 442 (2006), 79–81.
47. 47•• Parrish, N.F., Fujino, K., Shiromoto, Y., Iwasaki, Y.W., Ha, H., Xing, J., Makino, A., Kuramochi-Miyagawa, S., Nakano, T., Siomi, H., et al. piRNAs derived from ancient viral processed pseudogenes as transgenerational sequence-specific immune memory in mammals. RNA 21 (2015), 1691–1703 This study reported that EBLNs are enriched in piRNA-generating loci in two lineages of mammals, and proposed the hypothesis that EBLN-derived piRNAs might have been involved in antiviral defense.
48. Zhang, P., Kang, J.Y., Gou, L.T., Wang, J., Xue, Y., Skogerboe, G., Dai, P., Huang, D.W., Chen, R., Fu, X.D., et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res 25 (2015), 193–207.
49. Parrish, N.F., Tomonaga, K., Endogenized viral sequences in mammals. Curr Opin Microbiol 31 (2016), 176–183.
50. 50• Sofuku, K., Parrish, N.F., Honda, T., Tomonaga, K., Transcription profiling demonstrates epigenetic control of non-retroviral RNA virus-derived elements in the human genome. Cell Rep 12 (2015), 1548–1554 This paper showed that all 7 hsEBLNs are expressed as RNAs in at least one tissue, and proposed that hsEBLN-1 might function as a DNA element or non-coding RNA.
51. Kobayashi, Y., Horie, M., Tomonaga, K., Suzuki, Y., No evidence for natural selection on endogenous borna-like nucleoprotein elements after the divergence of Old World and New World monkeys. PLoS One, 6, 2011, e24403.
52. 52•• Myers, K.N., Barone, G., Ganesh, A., Staples, C.J., Howard, A.E., Beveridge, R.D., Maslen, S., Skehel, J.M., Collis, S.J., The bornavirus-derived human protein EBLN1 promotes efficient cell cycle transit, microtubule organisation and genome stability. Sci Rep, 6, 2016, 35548 This study revealed that hsEBLN-1 is expressed as a protein in several cell lines, which is involved in cellular functions, such as genome stability and cell cycle.
53. He, P., Sun, L., Zhu, D., Zhang, H., Zhang, L., Guo, Y., Liu, S., Zhou, J., Xu, X., Xie, P., Knock-down of endogenous bornavirus-like nucleoprotein 1 inhibits cell growth and induces apoptosis in human oligodendroglia cells. Int J Mol Sci, 17, 2016, 435.
54. Horie, M., Akasaka, T., Matsuda, S., Ogawa, H., Imai, K., Establishment and characterization of a cell line derived from Eptesicus nilssonii. J Vet Med Sci 78 (2016), 1727–1729.
55. Zong, J., Yao, X., Yin, J., Zhang, D., Ma, H., Evolution of the RNA-dependent RNA polymerase (RdRP) genes: duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447 (2009), 29–39.