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African and Asian Zika Virus Isolates Display Phenotypic Differences Both In Vitro and In Vivo
Zika virus (ZIKV) is a mosquito-borne member of the genus Flavivirus that has emerged since 2007 to cause outbreaks in Africa, Asia, Oceania, and most recently, in the Americas. Here, we used an isolate history as well as genetic and phylogenetic analyses to characterize three low-passage isolates representing African (ArD 41525) and Asian (CPC-0740, SV0127-14) lineages to investigate the potential phenotypic differences in vitro and in vivo. The African isolate displayed a large plaque phenotype (∼3–4 mm) on Vero and HEK-293 cells, whereas the Asian isolates either exhibited a small plaque phenotype (∼1–2 mm) or did not produce any plaques. In multistep replication kinetics in nine different vertebrate and insect cell lines, the African isolate consistently displayed faster replication kinetics and yielded ∼10- to 10,000-fold higher peak virus titers (infectious or RNA copies) compared with the Asian isolates. Oral exposure of Aedes aegypti mosquitoes with the African isolate yielded higher infection and dissemination rates compared with the Asian isolates. Infection of Ifnar1−/− mice with the African isolate produced a uniformly fatal disease, whereas infection with the Asian isolates produced either a delay in time-to-death or a significantly lower mortality rate. Last, the African isolate was > 10,000-fold more virulent than the Asian isolates in an interferon type I antibody blockade mouse model. These data demonstrate substantial phenotypic differences between low-passage African and Asian isolates both in vitro and in vivo and warrant further investigation. They also highlight the need for basic characterization of ZIKV isolates, as the utilization of the uncharacterized isolates could have consequences for animal model and therapeutic/vaccine development.
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Author Notes
Financial support: This study was supported by a grant from the Defense Advanced Research Projects Agency. Dr. B. S. H. is supported by National Research Council Research Associateship.
Authors’ addresses: Darci R. Smith, Thomas R. Sprague, Bradley S. Hollidge, Stephanie M. Valdez, Joseph W. Golden, Lynn Jean Miller, and Farooq Nasar, Virology Division, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD, E-mails: darci.r.smith.ctr@mail.mil, thomas.r.sprague7.ctr@mail.mil, bradley.s.hollidge.ctr@mail.mil, stephanie.m.valdez5.ctr@mail.mil, joseph.w.golden.ctr@mail.mil, lynn.j.miller.mil@mail.mil, and farooq.nasar.ctr@mail.mil. Susana L. Padilla, Stephanie A. Bellanca, Andrew D. Haddow, and Robert G. Lowen, Department of Entomology, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD, E-mails: susana.l.padilla.mil@mail.mil, stephanie.a.bellanca.ctr@mail.mil, andrew.d.haddow.ctr@mail.mil, and robert.g.lowen.mil@mail.mil. Susan R. Coyne, David A. Kulesh, Jeff W. Koehler, and Timothy D. Minogue, Diagnostics Systems Division, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD, E-mails: susan.r.coyne.civ@mail.mil, david.a.kulesh.civ@mail.mil, jeff.w.koehler.ctr@mail.mil, and timothy.d.minogue.civ@mail.mil. Gregory D. Gromowski and Richard G. Jarman, Viral Disease Branch, Walter Reed Army Institute of Research, Silver Spring, MD, E-mails: gregory.d.gromowski.civ@mail.mil and richard.g.jarman.mil@mail.mil. Maria Theresa P. Alera, Virology Research Unit, Philippines-Armed Forces Research Institute of Medical Sciences, Cebu City, Philippines, E-mail: mariatheresa.alera.ca@afrims.org. In-Kyu Yoon, Department of Dengue, International Vaccine Institute, Seoul, Republic of Korea, E-mail: inkyu.yoon@ivi.int. Rome Buathong, Department of Disease Control, Bureau of Epidemiology, Ministry of Public Health, Nonthaburi, Thailand, E-mail: romebua@health2.moph.go.th. Christopher D. Kane, Molecular and Translational Sciences Division, Therapeutic Development Center, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD, E-mail: christopher.d.kane.ctr@mail.mil. Sina Bavari and Margaret L. Pitt, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD, E-mails: sina.bavari.civ@mail.mil and margaret.l.pitt.civ@mail.mil. Robert B. Tesh and Scott C. Weaver, Department of Pathology, University of Texas, Medical Branch, Galveston, TX, E-mails: rtesh@utmb.edu and sweaver@utmb.edu. Kenneth J. Linthicum, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, FL, E-mail: kenneth.linthicum@ars.usda.gov.
The views expressed in this article are those of the authors and do not reflect the official policy or position of the U.S. Department of Defense, or the Department of the Army.