Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice

ABSTRACT Preexisting immunity against dengue virus or West Nile virus was previously reported to mediate antibody-dependent enhancement (ADE) of Zika virus (ZIKV) infection in a mouse model. We show here that ZIKV-immune plasma samples from both symptomatic and asymptomatic individuals mediated ZIKV...

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Autores principales:	Byoung-Shik Shim, Young-Chan Kwon, Michael J. Ricciardi, Mars Stone, Yuka Otsuka, Fatma Berri, Jaclyn M. Kwal, Diogo M. Magnani, Cody B. Jackson, Audrey S. Richard, Philip Norris, Michael Busch, Christine L. Curry, Michael Farzan, David Watkins, Hyeryun Choe
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Zika virus antibody-dependent enhancement congenital disease homotypic microcephaly pregnancy Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a6218489bb8a42a58651197c773f907b
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spelling	oai:doaj.org-article:a6218489bb8a42a58651197c773f907b2021-11-15T16:22:10ZZika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice10.1128/mBio.00758-192150-7511https://doaj.org/article/a6218489bb8a42a58651197c773f907b2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00758-19https://doaj.org/toc/2150-7511ABSTRACT Preexisting immunity against dengue virus or West Nile virus was previously reported to mediate antibody-dependent enhancement (ADE) of Zika virus (ZIKV) infection in a mouse model. We show here that ZIKV-immune plasma samples from both symptomatic and asymptomatic individuals mediated ZIKV ADE of infection in vitro and in mice. In a lethal infection model with a viral inoculum 10 times higher, both ADE and protection were observed, depending on the amount of infused immune plasma. In a vertical-transmission model, ZIKV-immune plasma infused to timed pregnant mice increased fetal demise and decreased the body weight of surviving fetuses. Depletion of IgG from an immune plasma abolished ADE of infection, and the presence of purified IgG alone mediated ADE of infection. Higher viral loads and proinflammatory cytokines were detected in mice treated with ZIKV-immune plasma samples compared to those receiving control plasma. Together, these data show that passive immunization with homotypic ZIKV antibodies, depending on the concentration, could either worsen or limit a subsequent ZIKV infection. IMPORTANCE Antibody-dependent enhancement (ADE) of virus infection is common to many viruses and is problematic when plasma antibody levels decline to subneutralizing concentrations. ADE of infection is especially important among flaviviruses, many of which are the cause of global health problems. Recently, human plasma samples immune to heterologous flaviviruses were shown to promote Zika virus (ZIKV) infection. Here we showed in immunocompromised mouse models that homologous immune plasma samples protect mice from subsequent infection at high antibody concentrations but that they mediate ADE of infection and increase ZIKV pathogenesis in adult mice and fetal demise during pregnancy at low concentrations.Byoung-Shik ShimYoung-Chan KwonMichael J. RicciardiMars StoneYuka OtsukaFatma BerriJaclyn M. KwalDiogo M. MagnaniCody B. JacksonAudrey S. RichardPhilip NorrisMichael BuschChristine L. CurryMichael FarzanDavid WatkinsHyeryun ChoeAmerican Society for MicrobiologyarticleZika virusantibody-dependent enhancementcongenital diseasehomotypicmicrocephalypregnancyMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Zika virus antibody-dependent enhancement congenital disease homotypic microcephaly pregnancy Microbiology QR1-502
spellingShingle	Zika virus antibody-dependent enhancement congenital disease homotypic microcephaly pregnancy Microbiology QR1-502 Byoung-Shik Shim Young-Chan Kwon Michael J. Ricciardi Mars Stone Yuka Otsuka Fatma Berri Jaclyn M. Kwal Diogo M. Magnani Cody B. Jackson Audrey S. Richard Philip Norris Michael Busch Christine L. Curry Michael Farzan David Watkins Hyeryun Choe Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice
description	ABSTRACT Preexisting immunity against dengue virus or West Nile virus was previously reported to mediate antibody-dependent enhancement (ADE) of Zika virus (ZIKV) infection in a mouse model. We show here that ZIKV-immune plasma samples from both symptomatic and asymptomatic individuals mediated ZIKV ADE of infection in vitro and in mice. In a lethal infection model with a viral inoculum 10 times higher, both ADE and protection were observed, depending on the amount of infused immune plasma. In a vertical-transmission model, ZIKV-immune plasma infused to timed pregnant mice increased fetal demise and decreased the body weight of surviving fetuses. Depletion of IgG from an immune plasma abolished ADE of infection, and the presence of purified IgG alone mediated ADE of infection. Higher viral loads and proinflammatory cytokines were detected in mice treated with ZIKV-immune plasma samples compared to those receiving control plasma. Together, these data show that passive immunization with homotypic ZIKV antibodies, depending on the concentration, could either worsen or limit a subsequent ZIKV infection. IMPORTANCE Antibody-dependent enhancement (ADE) of virus infection is common to many viruses and is problematic when plasma antibody levels decline to subneutralizing concentrations. ADE of infection is especially important among flaviviruses, many of which are the cause of global health problems. Recently, human plasma samples immune to heterologous flaviviruses were shown to promote Zika virus (ZIKV) infection. Here we showed in immunocompromised mouse models that homologous immune plasma samples protect mice from subsequent infection at high antibody concentrations but that they mediate ADE of infection and increase ZIKV pathogenesis in adult mice and fetal demise during pregnancy at low concentrations.
format	article
author	Byoung-Shik Shim Young-Chan Kwon Michael J. Ricciardi Mars Stone Yuka Otsuka Fatma Berri Jaclyn M. Kwal Diogo M. Magnani Cody B. Jackson Audrey S. Richard Philip Norris Michael Busch Christine L. Curry Michael Farzan David Watkins Hyeryun Choe
author_facet	Byoung-Shik Shim Young-Chan Kwon Michael J. Ricciardi Mars Stone Yuka Otsuka Fatma Berri Jaclyn M. Kwal Diogo M. Magnani Cody B. Jackson Audrey S. Richard Philip Norris Michael Busch Christine L. Curry Michael Farzan David Watkins Hyeryun Choe
author_sort	Byoung-Shik Shim
title	Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice
title_short	Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice
title_full	Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice
title_fullStr	Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice
title_full_unstemmed	Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice
title_sort	zika virus-immune plasmas from symptomatic and asymptomatic individuals enhance zika pathogenesis in adult and pregnant mice
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/a6218489bb8a42a58651197c773f907b
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Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice

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