The First Endogenous Herpesvirus, Identified in the Tarsier Genome, and Novel Sequences from Primate Rhadinoviruses and Lymphocryptoviruses

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Herpesviridae is a family of DNA viruses that have characteristically large and complex genomes. This defining feature is also responsible for bioinformatic challenges that complicate herpesvirus genomics, and why an endogenous herpesvirus remains elusive. Given that several species of herpesvirus are clinically relevant to humans, there is a pressing demand for techniques capable of generating and managing large quantities of herpesvirus genome data. This is coupled with a need to explore herpesvirus diversity in order to understand pathogenesis within an evolutionary context. Lessons from the study of ancient viral integrations have also highlighted the need to include information offered by paleoviruses. Using perspectives from paleovirology and metagenomics, we identify three herpesviruses within the genome data of their primate hosts, including the first endogenous herpesvirus. All three viruses are closely related to important human pathogens and two of them are entirely new species. Both comparative molecular biology and evolutionary analysis were applied to examine our results for their clinical relevance. Furthermore, we demonstrate how this analytical approach was also used for the data collection itself, by treating nucleotide databases in their entirety as a single metagenomic resource.

Vyšlo v časopise: The First Endogenous Herpesvirus, Identified in the Tarsier Genome, and Novel Sequences from Primate Rhadinoviruses and Lymphocryptoviruses. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004332
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004332

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Zdroje

1. LavergneA, de ThoisyB, PouliquenJ-F, Ruiz-GarcíaM, LacosteV (2011) Partial molecular characterisation of New World non-human primate lymphocryptoviruses. Infect Genet Evol 11: 1782–1789 doi:10.1016/j.meegid.2011.07.017

2. McGeochDJ, GathererD, DolanA (2005) On phylogenetic relationships among major lineages of the Gammaherpesvirinae. J Gen Virol 86: 307–316 doi:10.1099/vir.0.80588-0

3. McGeochDJ, RixonFJ, DavisonAJ (2006) Topics in herpesvirus genomics and evolution. Virus Res 117: 90–104 doi:10.1016/j.virusres.2006.01.002

4. McGeoch DJ, Davison AJ, Dolan A, Gatherer D, Sevilla-Reyes EE (2010) Molecular Evolution of the Herpesvirales. In: Domingo E, Holland JJ, editors. The Origin and Evolution of Viruses. Academic Press. 447–475 p. doi:10.1002/9780470688618.taw0208.

5. Fields BN, Knipe DM, Howley PM (2007) Fields Virology. 5th ed. Philadelphia: Lippincott Williams and Wilkins.

6. TischerBK, OsterriederN (2010) Herpesviruses–a zoonotic threat? Vet Microbiol 140: 266–270 doi:10.1016/j.vetmic.2009.06.020

7. KatzourakisA, GiffordRJ (2010) Endogenous viral elements in animal genomes. PLoS Genet 6: e1001191.

8. FeschotteC, GilbertC (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13: 283–296 doi:10.1038/nrg3199

9. HurleyEA, AggerS, McNeilJA, LawrenceJB, CalendarA, et al. (1991) When Epstein-Barr virus persistently infects B-cell lines, it frequently integrates. J Virol 65: 1245–1254.

10. MorissetteG, FlamandL (2010) Herpesviruses and chromosomal integration. J Virol 84: 12100–12109 doi:10.1128/JVI.01169-10

11. KauferBB, JarosinskiKW, OsterriederN (2011) Herpesvirus telomeric repeats facilitate genomic integration into host telomeres and mobilization of viral DNA during reactivation. J Exp Med 208: 605–615 doi:10.1084/jem.20101402

12. DelecluseHJ, HammerschmidtW (1993) Status of Marek's disease virus in established lymphoma cell lines: herpesvirus integration is common. J Virol 67: 82–92.

13. DelecluseHJ, SchüllerS, HammerschmidtW (1993) Latent Marek's disease virus can be activated from its chromosomally integrated state in herpesvirus-transformed lymphoma cells. EMBO J 12: 3277–3286.

14. ArbuckleJH, PantrySN, MedveczkyMM, PrichettJ, LoomisKS, et al. (2013) Mapping the telomere integrated genome of human herpesvirus 6A and 6B. Virology doi:10.1016/j.virol.2013.03.030

15. ArbuckleJH, MedveczkyMM, LukaJ, HadleySH, LuegmayrA, et al. (2010) The latent human herpesvirus-6A genome specifically integrates in telomeres of human chromosomes in vivo and in vitro. PNAS 107: 5563–5568 doi:10.1073/pnas.0913586107

16. PellettPE, AblashiDV, AmbrosPF, AgutH, CasertaMT, et al. (2012) Chromosomally integrated human herpesvirus 6: questions and answers. Rev Med Virol 22: 144–155 doi:10.1002/rmv.715

17. DelwartE (2013) A Roadmap to the Human Virome. PLoS Pathog 9: e1003146 doi:10.1371/journal.ppat.1003146

18. WilkieGS, DavisonAJ, WatsonM, KerrK, SandersonS, et al. (2013) Complete Genome Sequences of Elephant Endotheliotropic Herpesviruses 1A and 1B Determined Directly from Fatal Cases. J Virol 87: 6700–6712 doi:10.1128/JVI.00655-13

19. EhlersB, OchsA, LeendertzF, GoltzM, BoeschC, et al. (2003) Novel simian homologues of Epstein-Barr virus. J Virol 77: 10695–10699.

20. KumarS, SubramanianS (2002) Mutation rates in mammalian genomes. PNAS 99: 803–808 doi:10.1073/pnas.022629899

21. PaceJK, GilbertC, ClarkMS, FeschotteC (2008) Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. PNAS 105: 17023–17028 doi:10.1073/pnas.0806548105

22. PerelmanP, JohnsonWE, RoosC, SeuánezHN, HorvathJE, et al. (2011) A molecular phylogeny of living primates. PLoS Genet 7: e1001342 doi:10.1371/journal.pgen.1001342

23. HolmesEC (2011) The Evolution of Endogenous Viral Elements. Cell Host Microbe 10: 368–377 doi:10.1016/j.chom.2011.09.002

24. AswadA, KatzourakisA (2012) Paleovirology and virally derived immunity. Trends Ecol Evol 27: 627–636 doi:10.1016/j.tree.2012.07.007

25. TadagakiK, NakanoK, YamanishiK (2005) Human herpesvirus 7 open reading frames U12 and U51 encode functional beta-chemokine receptors. J Virol 79: 7068–7076 doi:10.1128/JVI.79.11.7068-7076.2005

26. ThomsonBJ, EfstathiouS, HonessRW (1991) Acquisition of the human adeno-associated virus type-2 rep gene by human herpesvirus type-6. Nature 351: 78–80 doi:10.1038/351078a0

27. McGeochDJ, DolanA, RalphAC (2000) Toward a Comprehensive Phylogeny for Mammalian and Avian Herpesviruses. J Virol 74: 10401–10406 doi:10.1128/JVI.74.22.10401-10406.2000

28. EhlersB, DuralG, YasmumN, LemboT, de ThoisyB, et al. (2008) Novel mammalian herpesviruses and lineages within the Gammaherpesvirinae: cospeciation and interspecies transfer. J Virol 82: 3509–3516 doi:10.1128/JVI.02646-07

29. McGeochDJ (2001) Molecular evolution of the gamma-Herpesvirinae. Philos Trans R Soc Lond B Biol Sci 356: 421–435 doi:10.1098/rstb.2000.0775

30. GernerCS, DolanA, McGeochDJ (2004) Phylogenetic relationships in the Lymphocryptovirus genus of the Gammaherpesvirinae. Virus Res 99: 187–192 doi:10.1016/j.virusres.2003.10.011

31. DavisonAJ, EberleR, EhlersB, HaywardGS, McGeochDJ, et al. (2009) The order Herpesvirales. Arch Virol 154: 171–177 doi:10.1007/s00705-008-0278-4

32. EhlersB, SpiessK, LeendertzF, PeetersM, BoeschC, et al. (2010) Lymphocryptovirus phylogeny and the origins of Epstein-Barr virus. J Gen Virol 91: 630–642 doi:10.1099/vir.0.017251-0

33. EhlersB, SpiessK, LeendertzF, PeetersM, BoeschC, et al. (2010) Lymphocryptovirus phylogeny and the origins of Epstein-Barr virus. J Gen Virol 91: 630–642 doi:10.1099/vir.0.017251-0

34. CrawfordDH (2001) Biology and disease associations of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 356: 461–473 doi:10.1098/rstb.2000.0783

35. RamasubramanyanS, KanhereA, OsbornK, FlowerK, JennerRG, et al. (2012) Genome-wide analyses of Zta binding to the Epstein-Barr virus genome reveals interactions in both early and late lytic cycles and an epigenetic switch leading to an altered binding profile. J Virol 86: 12494–12502 doi:10.1128/JVI.01705-12

36. FujiiK, YokoyamaN, KiyonoT, KuzushimaK, HommaM, et al. (2000) The Epstein-Barr Virus Pol Catalytic Subunit Physically Interacts with the BBLF4-BSLF1-BBLF2/3 Complex. J Virol 74: 2550–2557 doi:10.1128/JVI.74.6.2550-2557.2000

37. El-GuindyA, Ghiassi-NejadM, GoldenS, DelecluseH-J, MillerG (2013) Essential role of Rta in lytic DNA replication of Epstein-Barr virus. J Virol 87: 208–223 doi:10.1128/JVI.01995-12

38. ChiuY-F, SugdenB, ChangP-J, ChenL-W, LinY-J, et al. (2012) Characterization and intracellular trafficking of Epstein-Barr virus BBLF1, a protein involved in virion maturation. J Virol 86: 9647–9655 doi:10.1128/JVI.01126-12

39. RessingME, HorstD, GriffinBD, TellamJ, ZuoJ, et al. (2008) Epstein-Barr virus evasion of CD8(+) and CD4(+) T cell immunity via concerted actions of multiple gene products. Semin Cancer Biol 18: 397–408 doi:10.1016/j.semcancer.2008.10.008

40. CohenJI, LekstromK (1999) Epstein-Barr virus BARF1 protein is dispensable for B-cell transformation and inhibits alpha interferon secretion from mononuclear cells. J Virol 73: 7627–7632.

41. HislopAD, RessingME, van LeeuwenD, PudneyVA, HorstD, et al. (2007) A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J Exp Med 204: 1863–1873 doi:10.1084/jem.20070256

42. KvansakulM, WeiAH, FletcherJI, WillisSN, ChenL, et al. (2010) Structural basis for apoptosis inhibition by Epstein-Barr virus BHRF1. PLoS Pathog 6: e1001236 doi:10.1371/journal.ppat.1001236

43. LakeCM, Hutt-FletcherLM (2004) The Epstein-Barr virus BFRF1 and BFLF2 proteins interact and coexpression alters their cellular localization. Virology 320: 99–106 doi:10.1016/j.virol.2003.11.018

44. GonnellaR, FarinaA, SantarelliR, RaffaS, FeederleR, et al. (2005) Characterization and intracellular localization of the Epstein-Barr virus protein BFLF2: interactions with BFRF1 and with the nuclear lamina. J Virol 79: 3713–3727 doi:10.1128/JVI.79.6.3713-3727.2005

45. PavlovaS, FeederleR, GärtnerK, FuchsW, GranzowH, et al. (2013) An Epstein-Barr virus mutant produces immunogenic defective particles devoid of viral DNA. J Virol 87: 2011–2022 doi:10.1128/JVI.02533-12

46. WhitehurstCB, VaziriC, ShackelfordJ, PaganoJS (2012) Epstein-Barr virus BPLF1 deubiquitinates PCNA and attenuates polymerase η recruitment to DNA damage sites. J Virol 86: 8097–8106 doi:10.1128/JVI.00588-12

47. MassaM, MazzoliF, PignattiP, De BenedettiF, PassaliaM, et al. (2002) Proinflammatory responses to self HLA epitopes are triggered by molecular mimicry to Epstein-Barr virus proteins in oligoarticular juvenile idiopathic arthritis. Arthritis Rheum 46: 2721–2729 doi:10.1002/art.10564

48. RezaeeSAR, CunninghamC, DavisonAJ, BlackbournDJ (2006) Kaposi's sarcoma-associated herpesvirus immune modulation: an overview. J Gen Virol 87: 1781–1804 doi:10.1099/vir.0.81919-0

49. KellyGL, StrasserA (2011) The essential role of evasion from cell death in cancer. Adv Cancer Res 111: 39–96 doi:10.1016/B978-0-12-385524-4.00002-7

50. DavisonAJ, StowND (2005) New genes from old: redeployment of dUTPase by herpesviruses. J Virol 79: 12880–12892 doi:10.1128/JVI.79.20.12880-12892.2005

51. HartJ, AckermannM, JayawardaneG, RussellG, HaigDM, et al. (2007) Complete sequence and analysis of the ovine herpesvirus 2 genome. J Gen Virol 88: 28–39 doi:10.1099/vir.0.82284-0

52. AhujaSK, MurphyPM (1993) Molecular piracy of mammalian interleukin-8 receptor type B by herpesvirus saimiri. J Biol Chem 268: 20691–20694.

53. GlaunsingerB, GanemD (2004) Lytic KSHV Infection Inhibits Host Gene Expression by Accelerating Global mRNA Turnover. Mol Cell 13: 713–723 doi:10.1016/S1097-2765(04)00091-7

54. GlaunsingerB, ChavezL, GanemD (2005) The Exonuclease and Host Shutoff Functions of the SOX Protein of Kaposi's Sarcoma-Associated Herpesvirus Are Genetically Separable. J Virol 79: 7396–7401.

55. ZhuFX, KingSM, SmithEJ, LevyDE, YuanY (2002) A Kaposi's sarcoma-associated herpesviral protein inhibits virus-mediated induction of type I interferon by blocking IRF-7 phosphorylation and nuclear accumulation. PNAS 99: 5573–5578 doi:10.1073/pnas.082420599

56. DamaniaB, JeongJH, BowserBS, DeWireSM, StaudtMR, et al. (2004) Comparison of the Rta/Orf50 Transactivator Proteins of Gamma-2-Herpesviruses. J Virol 78: 5491–5499 doi:10.1128/JVI.78.10.5491-5499.2004

57. De León VázquezE, KayeKM (2011) The internal Kaposi's sarcoma-associated herpesvirus LANA regions exert a critical role on episome persistence. J Virol 85: 7622–7633 doi:10.1128/JVI.00304-11

58. KaulR, VermaSC, RobertsonES (2007) Protein complexes associated with the Kaposi's sarcoma-associated herpesvirus-encoded LANA. Virology 364: 317–329 doi:10.1016/j.virol.2007.03.010

59. WatanabeT, SugayaM, AtkinsAM, AquilinoEA, YangA, et al. (2003) Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen prolongs the life span of primary human umbilical vein endothelial cells. J Virol 77: 6188–6196.

60. FujimuroM, HaywardSD (2003) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus manipulates the activity of glycogen synthase kinase-3beta. J Virol 77: 8019–8030.

61. CaiQ, XiaoB, SiH, CerviniA, GaoJ, et al. (2012) Kaposi's sarcoma herpesvirus upregulates Aurora A expression to promote p53 phosphorylation and ubiquitylation. PLoS Pathog 8: e1002566 doi:10.1371/journal.ppat.1002566

62. LacosteV, VerschoorEJ, NerrienetE, GessainA (2005) A novel homologue of Human herpesvirus 6 in chimpanzees. J Gen Virol 86: 2135–2140 doi:10.1099/vir.0.81034-0

63. ArbuckleJH, MedveczkyPG (2011) The molecular biology of human herpesvirus-6 latency and telomere integration. Microbes Infect 13: 731–741.

64. RiethmanH (2008) Human telomere structure and biology. Annu Rev Genomics Hum Genet 9: 1–19 doi:10.1146/annurev.genom.8.021506.172017

65. HuangY, Hidalgo-BravoA, ZhangE, CottonVE, Mendez-BermudezA, et al. (2013) Human telomeres that carry an integrated copy of human herpesvirus 6 are often short and unstable, facilitating release of the viral genome from the chromosome. Nucleic Acids Res gkt840 doi:10.1093/nar/gkt840

66. ThomsonBJ, WeindlerFW, GrayD, SchwaabV, HeilbronnR (1994) Human Herpesvirus 6 (HHV-6) Is a Helper Virus for Adeno-Associated Virus Type 2 (AAV-2) and the AAV-2 rep Gene Homologue in HHV-6 Can Mediate AAV-2 DNA Replication and Regulate Gene Expression. Virology 204: 304–311.

67. PerryGH, LouisEE, RatanA, Bedoya-ReinaOC, BurhansRC, et al. (2013) Aye-aye population genomic analyses highlight an important center of endemism in northern Madagascar. PNAS 110: 5823–5828 doi:10.1073/pnas.1211990110

68. RenzetteN, BhattacharjeeB, JensenJD, GibsonL, KowalikTF (2011) Extensive genome-wide variability of human cytomegalovirus in congenitally infected infants. PLoS Pathog 7: e1001344 doi:10.1371/journal.ppat.1001344

69. ChristouL (2011) The global burden of bacterial and viral zoonotic infections. Clin Microbiol Infect 17: 326–330 doi:10.1111/j.1469-0691.2010.03441.x

70. ChangH, WachtmanLM, PearsonCB, LeeJ-S, LeeH-R, et al. (2009) Non-human primate model of Kaposi's sarcoma-associated herpesvirus infection. PLoS Pathog 5: e1000606 doi:10.1371/journal.ppat.1000606

71. HuffJL, BarryPA (2003) B-virus (Cercopithecine herpesvirus 1) infection in humans and macaques: potential for zoonotic disease. Emerg Infect Dis 9: 246–250 doi:10.3201/eid0902.020272

72. WilkieGS, DavisonAJ, WatsonM, KerrK, SandersonS, et al. (2013) Complete genome sequences of elephant endotheliotropic herpesviruses 1A and 1B determined directly from fatal cases. J Virol 87: 6700–6712 doi:10.1128/JVI.00655-13

73. HorieM, HondaT, SuzukiY, KobayashiY, DaitoT, et al. (2010) Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463: 84–87 doi:10.1038/nature08695

74. BelyiVA, LevineAJ, SkalkaAM (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

75. CornelisG, HeidmannO, Bernard-StoecklinS, ReynaudK, VéronG, et al. (2012) Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. PNAS 109: E432–41 doi:10.1073/pnas.1115346109

76. PrüferK, MunchK, HellmannI, AkagiK, MillerJR, et al. (2012) The bonobo genome compared with the chimpanzee and human genomes. Nature 486: 527–531 doi:10.1038/nature11128

77. PerryGH, ReevesD, MelstedP, RatanA, MillerW, et al. (2012) A genome sequence resource for the aye-aye (Daubentonia madagascariensis), a nocturnal lemur from Madagascar. Genome Biol Evol 4: 126–135 doi:10.1093/gbe/evr132