1887

Journal of General Virology header logo

Volume 102, Issue 9

The host range restriction of bat-associated no-known-vector flaviviruses occurs post-entry Open Access

Abstract

Most flaviviruses are transmitted horizontally between vertebrate hosts by haematophagous arthropods. Others exhibit host ranges restricted to vertebrates or arthropods. Vertebrate-specific flaviviruses are commonly referred to as no-known-vector (NKV) flaviviruses and can be separated into bat- and rodent-associated NKV flaviviruses. Rio Bravo virus (RBV) is one of eight recognized bat-associated NKV (B-NKV) flaviviruses. Studies designed to identify the genetic determinants that condition the host range restriction of B-NKV flaviviruses have never been performed. To investigate whether the host range restriction occurs at the level of attachment or entry, chimeric flaviviruses were created by inserting the pre-membrane and envelope protein genes of RBV into the genetic backbones of yellow fever virus (YFV) and Zika virus (ZIKV), two mosquito-borne flaviviruses associated with human disease. The chimeric viruses infected both vertebrate and mosquito cells. In vertebrate cells, all viruses produced similar mean peak titres, but the chimeric viruses grew more slowly than their parental viruses during early infection. In mosquito cells, the chimeric virus of YFV and RBV grew more slowly than YFV at early post-inoculation time points, but reached a similar mean peak titre. In contrast, the chimeric virus of ZIKV and RBV produced a mean peak titre that was approximately 10-fold lower than ZIKV. The chimeric virus of YFV and RBV produced an intermediate plaque phenotype, while the chimeric virus of ZIKV and RBV produced smaller plaques than both parental viruses. To conclude, we provide evidence that the structural glycoproteins of RBV permit entry into both mosquito and vertebrate cells, indicating that the host range restriction of B-NKV flaviviruses is mediated by a post-attachment/entry event.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): chimeric , entry , flavivirus , host range , no-known-vector flavivirus and Rio Bravo virus
Funding
This study was supported by the:
  • Consejo Nacional de Ciencia y Tecnología (Award 406531)
    • Principle Award Recipient: JermiliaCharles
  • National Institutes of Health (Award R01AI114720)
    • Principle Award Recipient: BradJ Blitvich
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001647
2021-09-06
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/9/jgv001647.html?itemId=/content/journal/jgv/10.1099/jgv.0.001647&mimeType=html&fmt=ahah

References

  1. Simmonds P, Becher P, Bukh J, Gould EA, Meyers G et al. ICTV virus taxonomy profile: Flaviviridae . J Gen Virol 2017; 98 :2–3 [View Article] [PubMed]
     [Google Scholar]
  2. Lindenbach BD, Thiel H-J, Rice CM. Flaviviridae: The viruses and the replication. Knipe D, Howley P. eds In Fields Virology, 6th. edn 2013 pp 1101–1152
     [Google Scholar]
  3. Zhang X, Jia R, Shen H, Wang M, Yin Z et al. Structures and functions of the envelope glycoprotein in flavivirus infections. Viruses 2017; 9 :11
     [Google Scholar]
  4. Li L, Lok S-M, Yu I-M, Zhang Y, Kuhn RJ et al. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 2008; 319:1830–1834 [View Article] [PubMed]
     [Google Scholar]
  5. Roby JA, Setoh YX, Hall RA, Khromykh AA. Post-translational regulation and modifications of flavivirus structural proteins. J Gen Virol 2015; 96 :1551–1569 [View Article] [PubMed]
     [Google Scholar]
  6. Blitvich BJ, Firth AE. Insect-specific flaviviruses: a systematic review of their discovery, host range, mode of transmission, superinfection exclusion potential and genomic organization. Viruses 2015; 7 :1927–1959 [View Article] [PubMed]
     [Google Scholar]
  7. Blitvich BJ. Firth AE: A review of flaviviruses that have no known arthropod vector. Viruses 2017; 9 : [View Article] [PubMed]
     [Google Scholar]
  8. Barrett AD, Higgs S. Yellow fever: a disease that has yet to be conquered. Annu Rev Entomol 2007; 52 :209–229 [View Article] [PubMed]
     [Google Scholar]
  9. Gutierrez-Bugallo G, Piedra LA, Rodriguez M, Bisset JA, Lourenco-de-Oliveira R et al. Vector-borne transmission and evolution of Zika virus. Nat Ecol Evol 2019; 3 :561–569 [View Article] [PubMed]
     [Google Scholar]
  10. Bolling BG, Weaver SC, Tesh RB, Vasilakis N. Insect-specific virus discovery: significance for the arbovirus community. Viruses 2015; 7:4911–4928 [View Article] [PubMed]
     [Google Scholar]
  11. Carvalho VL, Long MT. Insect-specific viruses: an overview and their relationship to arboviruses of concern to humans and animals. Virology 2021; 557:34–43 [View Article] [PubMed]
     [Google Scholar]
  12. Tajima S, Takasaki T, Matsuno S, Nakayama M, Kurane I. Genetic characterization of Yokose virus, a flavivirus isolated from the bat in Japan. Virology 2005; 332:38–44 [View Article] [PubMed]
     [Google Scholar]
  13. L’Vov DK, Al’khovskii SV, Shchelkanov M, Shchetinin AM, Deriabin PG et al. [Taxonomy of the Sokuluk virus (SOKV) (Flaviviridae, Flavivirus, Entebbe bat virus group) isolated from bats (Vespertilio pipistrellus Schreber, 1774), ticks (Argasidae Koch, 1844), and birds in Kyrgyzstan]. Vopr Virusol 2014; 59:30–34 [PubMed]
     [Google Scholar]
  14. Varelas-Wesley I, Calisher CH. Antigenic relationships of flaviviruses with undetermined arthropod-borne status. Am J Trop Med Hyg 1982; 31:1273–1284 [View Article] [PubMed]
     [Google Scholar]
  15. Burns KF, Farinacci CJ. Virus of bats antigenically related to St. Louis encephalitis. Science 1956; 123:227 [View Article]
     [Google Scholar]
  16. Burns KF, Farinacci CJ, Shelton DF. Virus of bats antigenically related to group B arthropod-borne encephalitis viruses. Am J Clin Pathol 1957; 27:257–264 [View Article] [PubMed]
     [Google Scholar]
  17. Constantine DG, Woodall DF. Latent infection of Rio Bravo virus in salivary glands of bats. Public Health Rep 1964; 79:1033–1039 [PubMed]
     [Google Scholar]
  18. Price JL. Isolation of Rio Bravo and a hitherto undescribed agent, Tamana bat virus, from insectivorous bats in Trinidad, with serological evidence of infection in bats and man. Am J Trop Med Hyg 1978; 27:153–161 [View Article] [PubMed]
     [Google Scholar]
  19. Sulkin SE, Sims RA, Allen R. Isolation of St. Louis encephalitis virus from bats (Tadarida b. mexicana) in Texas. Science 1966; 152:223–225 [View Article] [PubMed]
     [Google Scholar]
  20. Wilhelm AR, Gerone PJ. Growth of Rio Bravo virus in cell cultures. Appl Microbiol 1970; 20:612–615 [View Article] [PubMed]
     [Google Scholar]
  21. Hendricks DA, Hardy JL, Reeves WC. Comparison of biological properties of St. Louis encephalitis and Rio Bravo viruses. Am J Trop Med Hyg 1983; 32:602–609 [View Article] [PubMed]
     [Google Scholar]
  22. Main OM, Hardy JL, Reeves WC. Growth of arboviruses and other viruses in a continuous line of Culex tarsalis cells. J Med Entomol 1977; 14:107–112 [View Article] [PubMed]
     [Google Scholar]
  23. Cahoon BE, Hardy JL, Reeves WC. Growth of California encephalitis and other viruses in Aedes dorsalis (Diptera: Culicidae) cell cultures. J Med Entomol 1979; 16:104–111 [View Article] [PubMed]
     [Google Scholar]
  24. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 2008; 9:857–865 [View Article] [PubMed]
     [Google Scholar]
  25. Aubry F, Nougairede A, de Fabritus L, Querat G, Gould EA et al. Single-stranded positive-sense RNA viruses generated in days using infectious subgenomic amplicons. J Gen Virol 2014; 95:2462–2467 [View Article] [PubMed]
     [Google Scholar]
  26. Anon The International Catalog of Arboviruses including certain other viruses of vertebrates. In Centers for Disease Control and Prevention Colorado, USA : Fort Collins;
     [Google Scholar]
  27. Davis JW, Hardy JL. In vitro studies with Modoc virus in Vero cells: plaque assay and kinetics of growth, neutralization, and thermal inactivation. Appl Microbiol 1973; 26:344–348 [View Article] [PubMed]
     [Google Scholar]
  28. Gould EA, Solomon T. Pathogenic flaviviruses. Lancet 2008; 371:500–509 [View Article] [PubMed]
     [Google Scholar]
  29. Gubler DJ, Kuno G, Markoff L. Flaviviruses. Knipe D, Howley P. eds In Fields Virology Philadelphia, Pennsylvania, USA: Lippincott Williams and Wilkins; 2007 pp 1153–1252
     [Google Scholar]
  30. Sulkin SE, Burns KF, Shelton DF, Wallis C. Bat salivary gland virus: infections of man and monkey. Tex Rep Biol Med 1962; 20:113–127 [PubMed]
     [Google Scholar]
  31. Cook EB. Safety in the public health laboratory. Public Health Rep 1961; 76:51–56 [PubMed]
     [Google Scholar]
  32. Charlier N, Molenkamp R, Leyssen P, Paeshuyse J, Drosten C et al. Exchanging the yellow fever virus envelope proteins with Modoc virus prM and E proteins results in a chimeric virus that is neuroinvasive in SCID mice. J Virol 2004; 78:7418–7426 [View Article] [PubMed]
     [Google Scholar]
  33. Saiyasombat R, Carrillo-Tripp J, Miller WA, Bredenbeek PJ, Blitvich BJ. Substitution of the premembrane and envelope protein genes of Modoc virus with the homologous sequences of West Nile virus generates a chimeric virus that replicates in vertebrate but not mosquito cells. Virol J 2014; 11:150 [View Article] [PubMed]
     [Google Scholar]
  34. Tumban E, Maes NE, Schirtzinger EE, Young KI, Hanson CT et al. Replacement of conserved or variable sequences of the mosquito-borne dengue virus 3’ UTR with homologous sequences from Modoc virus does not change infectivity for mosquitoes. J Gen Virol 2013; 94:783–788 [View Article] [PubMed]
     [Google Scholar]
  35. Charlier N, Davidson A, Dallmeier K, Molenkamp R, De Clercq E et al. Replication of not-known-vector flaviviruses in mosquito cells is restricted by intracellular host factors rather than by the viral envelope proteins. J Gen Virol 2010; 91:1693–1697 [View Article] [PubMed]
     [Google Scholar]
  36. Johnson HN. Ecological implications of antigenically related mammalian viruses for which arthropod vectors are unknown and avian associated soft tick viruses. Jpn J Med Sci Biol 1967; 20 Suppl:160–166 [PubMed]
     [Google Scholar]
  37. Zarnke RL, Yuill TM. Modoc-like virus isolated from wild deer mice (Peromyscus maniculatus) in Alberta. J Wildl Dis 1985; 21:94–99 [View Article] [PubMed]
     [Google Scholar]
  38. Roundy CM, Azar SR, Rossi SL, Weaver SC, Vasilakis N. Insect-specific viruses: a historical overview and recent developments. Adv Virus Res 2017; 98:119–146 [View Article] [PubMed]
     [Google Scholar]
  39. Harrison JJ, Hobson-Peters J, Colmant AMG, Koh J, Newton ND et al. Antigenic characterization of new lineage II insect-specific flaviviruses in Australian mosquitoes and identification of host restriction factors. mSphere 2020; 5:
     [Google Scholar]
  40. Junglen S, Korries M, Grasse W, Wieseler J, Kopp A et al. Host range restriction of insect-specific flaviviruses occurs at several levels of the viral life cycle. mSphere 2017; 2:
     [Google Scholar]
  41. Piyasena TBH, Newton ND, Hobson-Peters J, Vet LJ, Setoh YX et al. Chimeric viruses of the insect-specific flavivirus Palm Creek with structural proteins of vertebrate-infecting flaviviruses identify barriers to replication of insect-specific flaviviruses in vertebrate cells. J Gen Virol 2019; 100:1580–1586 [View Article] [PubMed]
     [Google Scholar]
  42. Piyasena TBH, Setoh YX, Hobson-Peters J, Newton ND, Bielefeldt-Ohmann H et al. Infectious dnas derived from insect-specific flavivirus genomes enable identification of pre- and post-entry host restrictions in vertebrate cells. Sci Rep 2017; 7:2940 [View Article] [PubMed]
     [Google Scholar]
  43. Tangudu CS, Charles J, Nunez-Avellaneda D, Hargett AM, Brault AC et al. Chimeric Zika viruses containing structural protein genes of insect-specific flaviviruses cannot replicate in vertebrate cells due to entry and post-translational restrictions. Virology 2021; 559:30–39 [View Article] [PubMed]
     [Google Scholar]
  44. Hazlewood JE, Rawle DJ, Tang B, Yan K, Vet LJ et al. A zika vaccine generated using the chimeric insect-specific binjari virus platform protects against fetal brain infection in pregnant mice. Vaccines (Basel) 2020; 8: [View Article] [PubMed]
     [Google Scholar]
  45. Hobson-Peters J, Harrison JJ, Watterson D, Hazlewood JE, Vet LJ et al. A recombinant platform for flavivirus vaccines and diagnostics using chimeras of a new insect-specific virus. Sci Transl Med 2019; 11:522
     [Google Scholar]
  46. Colmant AMG, Hobson-Peters J, Slijkerman TAP, Harrison JJ, Pijlman GP et al. Insect-specific flavivirus replication in mammalian cells is inhibited by physiological temperature and the zinc-finger antiviral protein. Viruses 2021; 13: [View Article] [PubMed]
     [Google Scholar]
  47. Luo X, Wang X, Gao Y, Zhu J, Liu S et al. Molecular mechanism of RNA recognition by zinc-finger antiviral protein. Cell Rep 2020; 30:52
     [Google Scholar]
  48. Maharaj PD, Anishchenko M, Langevin SA, Fang Y, Reisen WK et al. Structural gene (prME) chimeras of St Louis encephalitis virus and West Nile virus exhibit altered in vitro cytopathic and growth phenotypes. J Gen Virol 2012; 93:39–49 [View Article] [PubMed]
     [Google Scholar]
  49. Huang CY, Silengo SJ, Whiteman MC, Kinney RM. Chimeric dengue 2 PDK-53/West Nile NY99 viruses retain the phenotypic attenuation markers of the candidate PDK-53 vaccine virus and protect mice against lethal challenge with West Nile virus. J Virol 2005; 79:7300–7310 [View Article] [PubMed]
     [Google Scholar]
  50. Giel-Moloney M, Goncalvez AP, Catalan J, Lecouturier V, Girerd-Chambaz Y et al. Chimeric yellow fever 17D-Zika virus (ChimeriVax-Zika) as a live-attenuated Zika virus vaccine. Sci Rep 2018; 8:13206 [View Article] [PubMed]
     [Google Scholar]
  51. Kenney JL, Anishchenko M, Hermance M, Romo H, Chen CI et al. Generation of a lineage II Powassan virus (deer tick virus) cDNA clone: assessment of flaviviral genetic determinants of tick and mosquito vector competence. Vector Borne Zoonotic Dis 2018; 18:371–381 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001647
Loading
The host range restriction of bat-associated no-known-vector flaviviruses occurs post-entry
J. Gen. Virol. 102, 001647 (2021); https://doi.org/10.1099/jgv.0.001647
/content/journal/jgv/10.1099/jgv.0.001647
/content/journal/jgv/10.1099/jgv.0.001647
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error