Novel Polyomaviruses of Nonhuman Primates: Genetic and Serological Predictors for the Existence of Multiple Unknown Polyomaviruses within the Human Population

English version České info

Polyomaviruses are a family of small non-enveloped DNA viruses that encode oncogenes and have been associated, to greater or lesser extent, with human disease and cancer. Currently, twelve polyomaviruses are known to circulate within the human population. To further examine the diversity of human polyomaviruses, we have utilized a combinatorial approach comprised of initial degenerate primer-based PCR identification and phylogenetic analysis of nonhuman primate (NHP) polyomavirus species, followed by polyomavirus-specific serological analysis of human sera. Using this approach we identified twenty novel NHP polyomaviruses: nine in great apes (six in chimpanzees, two in gorillas and one in orangutan), five in Old World monkeys and six in New World monkeys. Phylogenetic analysis indicated that only four of the nine chimpanzee polyomaviruses (six novel and three previously identified) had known close human counterparts. To determine whether the remaining chimpanzee polyomaviruses had potential human counterparts, the major viral capsid proteins (VP1) of four chimpanzee polyomaviruses were expressed in E. coli for use as antigens in enzyme-linked immunoassay (ELISA). Human serum/plasma samples from both Côte d'Ivoire and Germany showed frequent seropositivity for the four viruses. Antibody pre-adsorption-based ELISA excluded the possibility that reactivities resulted from binding to known human polyomaviruses. Together, these results support the existence of additional polyomaviruses circulating within the human population that are genetically and serologically related to existing chimpanzee polyomaviruses.

Vyšlo v časopise: Novel Polyomaviruses of Nonhuman Primates: Genetic and Serological Predictors for the Existence of Multiple Unknown Polyomaviruses within the Human Population. PLoS Pathog 9(6): e32767. doi:10.1371/journal.ppat.1003429
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003429

Souhrn

Zdroje

1. Eddy BE (1969) Polyoma virus. In: Gard CHSM, K.F., editor. Virology Monographs. New York: Springer-Verlag. pp 1–114.

2. Gross L (1983) Oncogenic viruses. Oxford: Pergamon Press.

3. Major EO (1996) Human polyomaviruses. In: Fields BNH, P.M.; Griffin, D.E., editors. fields Virology: Lippincott Williams & Wilkins.

4. PipasJM (2009) SV40: Cell transformation and tumorigenesis. Virology 384: 294–303.

5. DamaniaB (2007) DNA tumor viruses and human cancer. Trends Microbiol 15: 38–44.

6. McLaughlin-DrubinME, MungerK (2008) Viruses associated with human cancer. Biochim Biophys Acta 1782: 127–150.

7. AbendJR, JiangM, ImperialeMJ (2009) BK virus and human cancer: innocent until proven guilty. Semin Cancer Biol 19: 252–260.

8. JiangM, AbendJR, JohnsonSF, ImperialeMJ (2009) The role of polyomaviruses in human disease. Virology 384: 266–273.

9. PadgettBL, WalkerDL, ZuRheinGM, EckroadeRJ, DesselBH (1971) Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1: 1257–1260.

10. GardnerSD, FieldAM, ColemanDV, HulmeB (1971) New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1: 1253–1257.

11. BrewBJ, DaviesNW, CinqueP, CliffordDB, NathA (2010) Progressive multifocal leukoencephalopathy and other forms of JC virus disease. Nat Rev Neurol 6: 667–679.

12. FengH, ShudaM, ChangY, MoorePS (2008) Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319: 1096–1100.

13. van der MeijdenE, JanssensRW, LauberC, Bouwes BavinckJN, GorbalenyaAE, et al. (2010) Discovery of a new human polyomavirus associated with trichodysplasia spinulosa in an immunocompromized patient. PLoS Pathog 6: e1001024.

14. AllanderT, AndreassonK, GuptaS, BjerknerA, BogdanovicG, et al. (2007) Identification of a third human polyomavirus. J Virol 81: 4130–4136.

15. GaynorAM, NissenMD, WhileyDM, MackayIM, LambertSB, et al. (2007) Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog 3: e64.

16. SchowalterRM, PastranaDV, PumphreyKA, MoyerAL, BuckCB (2010) Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7: 509–515.

17. ScudaN, HofmannJ, Calvignac-SpencerS, RuprechtK, LimanP, et al. (2011) A novel human polyomavirus closely related to the african green monkey-derived lymphotropic polyomavirus. J Virol 85: 4586–4590.

18. SiebrasseEA, ReyesA, LimES, ZhaoG, MkakosyaRS, et al. (2012) Identification of MW polyomavirus, a novel polyomavirus in human stool. J Virol 86(19): 10321–6.

19. LimES, ReyesA, AntonioM, SahaD, IkumapayiUN, et al. (2012) Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology 436(2): 295–303.

20. KorupS, RietscherJ, Calvignac-SpencerS, TruschF, HofmannJ, et al. (2013) Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS One 8: e58021.

21. KeanJM, RaoS, WangM, GarceaRL (2009) Seroepidemiology of human polyomaviruses. PLoS Pathog 5: e1000363.

22. KnowlesWA, PipkinP, AndrewsN, VyseA, MinorP, et al. (2003) Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. J Med Virol 71: 115–123.

23. StoltA, SasnauskasK, KoskelaP, LehtinenM, DillnerJ (2003) Seroepidemiology of the human polyomaviruses. J Gen Virol 84: 1499–1504.

24. ViscidiRP, RollisonDE, SondakVK, SilverB, MessinaJL, et al. (2011) Age-specific seroprevalence of Merkel cell polyomavirus, BK virus, and JC virus. Clin Vaccine Immunol 18: 1737–1743.

25. TruschF, KleinM, FinsterbuschT, KuhnJ, HofmannJ, et al. (2012) Seroprevalence of human polyomavirus 9 and cross-reactivity to African green monkey-derived lymphotropic polyomavirus. J Gen Virol 93: 698–705.

26. BrownP, TsaiT, GajdusekDC (1975) Seroepidemiology of human papovaviruses. Discovery of virgin populations and some unusual patterns of antibody prevalence among remote peoples of the world. Am J Epidemiol 102: 331–340.

27. ViscidiRP, ClaymanB (2006) Serological cross reactivity between polyomavirus capsids. Adv Exp Med Biol 577: 73–84.

28. Calvignac-SpencerS, LeendertzSA, GillespieTR, LeendertzFH (2012) Wild great apes as sentinels and sources of infectious disease. Clin Microbiol Infect 18: 521–527.

29. JohneR, EnderleinD, NieperH, MullerH (2005) Novel polyomavirus detected in the feces of a chimpanzee by nested broad-spectrum PCR. J Virol 79: 3883–3887.

30. LeendertzFH, ScudaN, CameronKN, KidegaT, ZuberbuhlerK, et al. (2011) African great apes are naturally infected with polyomaviruses closely related to Merkel cell polyomavirus. J Virol 85: 916–924.

31. TaoY, MangS, ConrardyC, KuzminIV, RecuencoS, et al. (2012) Discovery of Diverse Polyomaviruses in Bats and the Evolutionary History of the Polyomaviridae. J Gen Virol 94: 738–48.

32. JohneR, BuckCB, AllanderT, AtwoodWJ, GarceaRL, et al. (2011) Taxonomical developments in the family Polyomaviridae. Arch Virol 156: 1627–1634.

33. SalunkeDM, CasparDL, GarceaRL (1989) Polymorphism in the assembly of polyomavirus capsid protein VP1. Biophys J 56: 887–900.

34. LiuM, ZhangT, ZhangY, MengF, LiX, et al. (2010) Development and evaluation of a VP1-ELISA for detection of antibodies to duck hepatitis type 1 virus. J Virol Methods 169: 66–69.

35. van der MeijdenE, KazemS, BurgersMM, JanssensR, Bouwes BavinckJN, et al. (2011) Seroprevalence of trichodysplasia spinulosa-associated polyomavirus. Emerg Infect Dis 17: 1355–1363.

36. BradeL, Muller-LantzschN, zur HausenH (1981) B-lymphotropic papovavirus and possibility of infections in humans. J Med Virol 6: 301–308.

37. TakemotoKK, SegawaK (1983) A new monkey lymphotropic papovavirus: characterization of the virus and evidence of a related virus in humans. Prog Clin Biol Res 105: 87–96.

38. WilfingA, WinklerS, SchrattbauerK, WillheimM, BaierK, et al. (2001) African-European differences in the capacity of T-cell cytokine production. Am J Trop Med Hyg 65: 504–509.

39. SagniaB, Ateba NdongoF, Ndiang Moyo TetangS, Ndongo TorimiroJ, CairoC, et al. (2011) Reference values of lymphocyte subsets in healthy, HIV-negative children in Cameroon. Clin Vaccine Immunol 18: 790–795.

40. CarterJJ, PaulsonKG, WipfGC, MirandaD, MadeleineMM, et al. (2009) Association of Merkel cell polyomavirus-specific antibodies with Merkel cell carcinoma. J Natl Cancer Inst 101: 1510–1522.

41. PastranaDV, TolstovYL, BeckerJC, MoorePS, ChangY, et al. (2009) Quantitation of human seroresponsiveness to Merkel cell polyomavirus. PLoS Pathog 5: e1000578.

42. ChenT, MattilaPS, JarttiT, RuuskanenO, Soderlund-VenermoM, et al. (2011) Seroepidemiology of the newly found trichodysplasia spinulosa-associated polyomavirus. J Infect Dis 204: 1523–1526.

43. TouzeA, GaitanJ, ArnoldF, CazalR, FleuryMJ, et al. (2010) Generation of Merkel cell polyomavirus (MCV)-like particles and their application to detection of MCV antibodies. J Clin Microbiol 48: 1767–1770.

44. TolstovYL, PastranaDV, FengH, BeckerJC, JenkinsFJ, et al. (2009) Human Merkel cell polyomavirus infection II. MCV is a common human infection that can be detected by conformational capsid epitope immunoassays. Int J Cancer 125: 1250–1256.

45. KoendgenS, KuhlH, N'GoranPK, WalshPD, SchenkS, et al. (2008) Pandemic human viruses cause decline of endangered great apes. Curr Biol 18: 260–264.

46. LeendertzFH, EllerbrokH, BoeschC, Couacy-HymannE, Matz-RensingK, et al. (2004) Anthrax kills wild chimpanzees in a tropical rainforest. Nature 430: 451–452.

47. Fowler ME, Miller RE (2008) Zoo and Wildlife Medicine. St. Louis: Saunders.

48. WeversD, MetzgerS, BabweteeraF, BieberbachM, BoeschC, et al. (2011) Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol 85: 10774–10784.

49. GouyM, GuindonS, GascuelO (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221–224.

50. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

51. NotredameC, HigginsDG, HeringaJ (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205–217.

52. Di TommasoP, MorettiS, XenariosI, OrobitgM, MontanyolaA, et al. (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39: W13–17.

53. TalaveraG, CastresanaJ (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564–577.

54. AbascalF, ZardoyaR, PosadaD (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.

55. DrummondAJ, SuchardMA, XieD, RambautA (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969–1973.

56. GuindonS, DufayardJF, LefortV, AnisimovaM, HordijkW, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.

57. GuindonS, LethiecF, DurouxP, GascuelO (2005) PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33: W557–559.