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Clinical profile of Asian and African strains of Zika virus in immunocompetent mice

  • Shin, Minna (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University) ;
  • Kim, Jini (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University) ;
  • Park, Jeongho (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University) ;
  • Hahn, Tae-Wook (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
  • Received : 2021.03.05
  • Accepted : 2021.05.20
  • Published : 2021.06.30

Abstract

The mosquito-borne pathogen Zika virus may result in neurological disorders such as Guillain-Barré syndrome and microcephaly. The virus is classified as a member of the Flaviviridae family and its wide spread in multiple continents is a significant threat to public health. So, there is a need to develop animal models to examine the pathogenesis of the disease and to develop vaccines. To examine the clinical profile during Zika virus infection, we infected neonatal and adult wild-type mice (C57BL/6 and Balb/c) and compared the clinical signs of African-lineage strain (MR766) and Asian-lineage strain (PRVABC59, MEX2-81) of Zika virus. Consistent with previous reports, eight-week-old female Balb/c mice infected with these viral strains showed no changes in body weight, survival rate, and neurologic signs, but demonstrated increases in the weights of spleens and hearts. However, one-day-old neonates showed significantly lower survival rate and body weight with the African-lineage strain than the Asian-lineage strain. These results confirmed the pathogenic differences between Zika virus strains. We also evaluated the clinical responses in neonatal and adult mice of different strains. Our findings suggest that these are useful mouse models for characterization of Zika virus for vaccine development.

Keywords

Acknowledgement

This research was supported by funding from the Korea Centers for Disease Control and Prevention (2016-ER4203-02). We also would like to thank Eunjin Hong for providing technical assistance.

References

  1. Dick GW, Kitchen SF, Haddow AJ. Zika virus. I. Isolations and serological specificity. Trans R Soc Trop Med Hyg 1952;46:509-520. https://doi.org/10.1016/0035-9203(52)90042-4
  2. Fields BN, Knipe DM, Howley PM. Fields Virology. 6th ed. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, 2013.
  3. Lindenbach BD, Rice CM. Molecular biology of flaviviruses. Adv Virus Res 2003;59:23-61. https://doi.org/10.1016/S0065-3527(03)59002-9
  4. Musso D, Gubler DJ. Zika virus. Clin Microbiol Rev 2016;29:487-524. https://doi.org/10.1128/CMR.00072-15
  5. Cao-Lormeau VM, Blake A, Mons S, Lastere S, Roche C, Vanhomwegen J, Dub T, Baudouin L, Teissier A, Larre P, Vial AL, Decam C, Choumet V, Halstead SK, Willison HJ, Musset L, Manuguerra JC, Despres P, Fournier E, Mallet HP, Musso D, Fontanet A, Neil J, Ghawche F. Guillain-Barre Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 2016;387:1531-1539. https://doi.org/10.1016/S0140-6736(16)00562-6
  6. Cao-Lormeau VM, Roche C, Teissier A, Robin E, Berry AL, Mallet HP, Sall AA, Musso D. Zika virus, French polynesia, South pacific, 2013. Emerg Infect Dis 2014;20:1085-1086. https://doi.org/10.3201/eid2006.140138
  7. Paploski IA, Prates AP, Cardoso CW, Kikuti M, Silva MM, Waller LA, Reis MG, Kitron U, Ribeiro GS. Time lags between exanthematous illness attributed to Zika virus, Guillain-Barre syndrome, and microcephaly, Salvador, Brazil. Emerg Infect Dis 2016;22:1438-1444. https://doi.org/10.3201/eid2208.160496
  8. Sejvar JJ, Baughman AL, Wise M, Morgan OW. Population incidence of Guillain-Barre syndrome: a systematic review and meta-analysis. Neuroepidemiology 2011;36:123-133. https://doi.org/10.1159/000324710
  9. World Health Organization (WHO). Zika situation reports [Internet]. WHO, Geneva, 2016 [cited 2020 Feb 26]. Available from: https://apps.who.int/iris/handle/10665/246155.
  10. World Health Organization (WHO). WHO Director-General summarizes the outcome of the emergency committee regarding clusters of microencephaly and Gullain Barre Syndrome [Internet]. WHO, Geneva, 2016 [cited 2020 Feb 26]. Available from: https://www.who.int/news/item/01-02-2016-who-director-general-summarizes-the-outcome-of-the-emergency-committee-regarding-clusters-of-microcephaly-and-guillain-barr%C3%A9-syndrome.
  11. Likos A, Griffin I, Bingham AM, Stanek D, Fischer M, White S, Hamilton J, Eisenstein L, Atrubin D, Mulay P, Scott B, Jenkins P, Fernandez D, Rico E, Gillis L, Jean R, Cone M, Blackmore C, McAllister J, Vasquez C, Rivera L, Philip C. Local mosquito-borne transmission of Zika virus - Miami-Dade and Broward Counties, Florida, June-August 2016. MMWR Morb Mortal Wkly Rep 2016;65:1032-1038. https://doi.org/10.15585/mmwr.mm6538e1
  12. Metsky HC, Matranga CB, Wohl S, Schaffner SF, Freije CA, Winnicki SM, West K, Qu J, Baniecki ML, Gladden-Young A, Lin AE, Tomkins-Tinch CH, Ye SH, Park DJ, Luo CY, Barnes KG, Shah RR, Chak B, Barbosa-Lima G, Delatorre E, Vieira YR, Paul LM, Tan AL, Barcellona CM, Porcelli MC, Vasquez C, Cannons AC, Cone MR, Hogan KN, Kopp EW, Anzinger JJ, Garcia KF, Parham LA, Ramirez RMG, Montoya MCM, Rojas DP, Brown CM, Hennigan S, Sabina B, Scotland S, Gangavarapu K, Grubaugh ND, Oliveira G, Robles-Sikisaka R, Rambaut A, Gehrke L, Smole S, Halloran ME, Villar L, Mattar S, Lorenzana I, Cerbino-Neto J, Valim C, Degrave W, Bozza PT, Gnirke A, Andersen KG, Isern S, Michael SF, Bozza FA, Souza TML, Bosch I, Yozwiak NL, MacInnis BL, Sabeti PC. Zika virus evolution and spread in the Americas. Nature 2017;546:411-415. https://doi.org/10.1038/nature22402
  13. World Health Organization (WHO). Countries and territories with current or previous Zika virus transmission [internet]. WHO, Geneva, 2019 [cited 2020 Jul 22]. Available from: https://www.who.int/emergencies/diseases/zika/countries-with-zika-and-vectors-table.pdf.
  14. Faye O, Freire CC, Iamarino A, Faye O, de Oliveira JV, Diallo M, Zanotto PM, Sall AA. Molecular evolution of Zika virus during its emergence in the 20(th) century. PLoS Negl Trop Dis 2014;8:e2636. https://doi.org/10.1371/journal.pntd.0002636
  15. Haddow AD, Schuh AJ, Yasuda CY, Kasper MR, Heang V, Huy R, Guzman H, Tesh RB, Weaver SC. Genetic characterization of Zika virus strains: geographic expansion of the Asian lineage. PLoS Negl Trop Dis 2012;6:e1477. https://doi.org/10.1371/journal.pntd.0001477
  16. Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 2008;14:1232-1239. https://doi.org/10.3201/eid1408.080287
  17. Pettersson JH, Bohlin J, Dupont-Rouzeyrol M, Brynildsrud OB, Alfsnes K, Cao-Lormeau VM, Gaunt MW, Falconar AK, de Lamballerie X, Eldholm V, Musso D, Gould EA. Re-visiting the evolution, dispersal and epidemiology of Zika virus in Asia. Emerg Microbes Infect 2018;7:79. https://doi.org/10.1038/s41426-018-0082-5
  18. Liu ZY, Shi WF, Qin CF. The evolution of Zika virus from Asia to the Americas. Nat Rev Microbiol 2019;17:131-139. https://doi.org/10.1038/s41579-018-0134-9
  19. Hu T, Li J, Carr MJ, Duchene S, Shi W. The Asian lineage of Zika virus: transmission and evolution in Asia and the Americas. Virol Sin 2019;34:1-8. https://doi.org/10.1007/s12250-018-0078-2
  20. Sheridan MA, Balaraman V, Schust DJ, Ezashi T, Roberts RM, Franz AWE. African and Asian strains of Zika virus differ in their ability to infect and lyse primitive human placental trophoblast. PLoS One 2018;13:e0200086. https://doi.org/10.1371/journal.pone.0200086
  21. Duggal NK, Ritter JM, McDonald EM, Romo H, Guirakhoo F, Davis BS, Chang GJ, Brault AC. Differential neurovirulence of African and Asian genotype Zika virus isolates in outbred immunocompetent mice. Am J Trop Med Hyg 2017;97:1410-1417. https://doi.org/10.4269/ajtmh.17-0263
  22. Smith DR, Sprague TR, Hollidge BS, Valdez SM, Padilla SL, Bellanca SA, Golden JW, Coyne SR, Kulesh DA, Miller LJ, Haddow AD, Koehler JW, Gromowski GD, Jarman RG, Alera MTP, Yoon IK, Buathong R, Lowen RG, Kane CD, Minogue TD, Bavari S, Tesh RB, Weaver SC, Linthicum KJ, Pitt ML, Nasar F. African and Asian Zika Virus Isolates display phenotypic differences both in vitro and in vivo. Am J Trop Med Hyg 2018;98:432-444. https://doi.org/10.4269/ajtmh.17-0685
  23. Roundy CM, Azar SR, Rossi SL, Huang JH, Leal G, Yun R et al. Variation in Aedes aegypti mosquito competence for Zika virus transmission. Emerg Infect Dis 2017;23:625-632. https://doi.org/10.3201/eid2304.161484
  24. Simonin Y, van Riel D, Van de Perre P, Rockx B, Salinas S. Differential virulence between Asian and African lineages of Zika virus. PLoS Negl Trop Dis 2017;11:e0005821. https://doi.org/10.1371/journal.pntd.0005821
  25. Manangeeswaran M, Ireland DD, Verthelyi D. Zika (PRVABC59) infection is associated with T cell infiltration and neurodegeneration in CNS of immunocompetent neonatal C57Bl/6 Mice. PLoS Pathog 2016;12:e1006004. https://doi.org/10.1371/journal.ppat.1006004
  26. Yu J, Liu X, Ke C, Wu Q, Lu W, Qin Z, He X, Liu Y, Deng J, Xu S, Li Y, Zhu L, Wan C, Zhang Q, Xiao W, Xie Q, Zhang B, Zhao W. Effective suckling C57BL/6, Kunming, and BALB/c mouse models with remarkable neurological manifestation for Zika virus infection. Viruses 2017;9:165. https://doi.org/10.3390/v9070165
  27. Faizan MI, Abdullah M, Ali S, Naqvi IH, Ahmed A, Parveen S. Zika virus-induced microcephaly and its possible molecular mechanism. Intervirology 2016;59:152-158. https://doi.org/10.1159/000452950
  28. Gorman MJ, Caine EA, Zaitsev K, Begley MC, Weger-Lucarelli J, Uccellini MB, Tripathi S, Morrison J, Yount BL, Dinnon KH 3rd, Ruckert C, Young MC, Zhu Z, Robertson SJ, McNally KL, Ye J, Cao B, Mysorekar IU, Ebel GD, Baric RS, Best SM, Artyomov MN, Garcia-Sastre A, Diamond MS. An immunocompetent mouse model of Zika virus infection. Cell Host Microbe 2018 23:672-685. e6. https://doi.org/10.1016/j.chom.2018.04.003
  29. Semple BD, Blomgren K, Gimlin K, Ferriero DM, Noble-Haeusslein LJ. Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol 2013;106-107:1-16. https://doi.org/10.1016/j.pneurobio.2013.04.001
  30. Pletnikov MV, Rubin SA, Moran TH, Carbone KM. Exploring the cerebellum with a new tool: neonatal Borna disease virus (BDV) infection of the rat's brain. Cerebellum 2003;2:62-70. https://doi.org/10.1080/14734220309425
  31. Amstey MS, Kobos K. An experimental model for disseminated herpesvirus infection of the neonate. Am J Obstet Gynecol 1976;125:40-44. https://doi.org/10.1016/0002-9378(76)90888-7
  32. Pedras-Vasconcelos JA, Puig M, Sauder C, Wolbert C, Ovanesov M, Goucher D, Verthelyi D. Immunotherapy with CpG oligonucleotides and antibodies to TNF-alpha rescues neonatal mice from lethal arenavirus-induced meningoencephalitis. J Immunol 2008;180:8231-8240. https://doi.org/10.4049/jimmunol.180.12.8231
  33. Couderc T, Chretien F, Schilte C, Disson O, Brigitte M, Guivel-Benhassine F, Touret Y, Barau G, Cayet N, Schuffenecker I, Despres P, Arenzana-Seisdedos F, Michault A, Albert ML, Lecuit M. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog 2008;4:e29. https://doi.org/10.1371/journal.ppat.0040029
  34. Reiner SL, Locksley RM. The regulation of immunity to Leishmania major. Annu Rev Immunol 1995;13:151-177. https://doi.org/10.1146/annurev.iy.13.040195.001055
  35. Obeyesekere I, Hermon Y. Arbovirus heart disease: myocarditis and cardiomyopathy following dengue and chikungunya fever--a follow-up study. Am Heart J 1973;85:186-194. https://doi.org/10.1016/0002-8703(73)90459-6
  36. Kato F, Tajima S, Nakayama E, Kawai Y, Taniguchi S, Shibasaki K, Taira M, Maeki T, Lim CK, Takasaki T, Saijo M. Characterization of large and small-plaque variants in the Zika virus clinical isolate ZIKV/Hu/S36/Chiba/2016. Sci Rep 2017;7:16160. https://doi.org/10.1038/s41598-017-16475-2