Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques

Michael K. McCracken; Gregory D. Gromowski; Heather L. Friberg; Xiaoxu Lin; Peter Abbink; Rafael De La Barrera; Kenneth H. Eckles; Lindsey S. Garver; Michael Boyd; David Jetton; Dan H. Barouch; Matthew C. Wise; Bridget S. Lewis; Jeffrey R. Currier; Kayvon Modjarrad; Mark Milazzo; Michelle Liu; Anna B. Mullins; J. Robert Putnak; Nelson L. Michael; Richard G. Jarman; Stephen J. Thomas

doi:10.1371/journal.ppat.1006487

Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques

Michael K. McCracken, Gregory D. Gromowski, Heather L. Friberg, Xiaoxu Lin, Peter Abbink, Rafael De La Barrera, Kenneth H. Eckles, Lindsey S. Garver, Michael Boyd, David Jetton, Dan H. Barouch, Matthew C. Wise, Bridget S. Lewis, Jeffrey R. Currier, Kayvon Modjarrad, Mark Milazzo, Michelle Liu, Anna B. Mullins, J. Robert Putnak, Nelson L. MichaelRichard G. Jarman^*, Stephen J. Thomas

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

116 Scopus citations

Abstract

Studies have demonstrated cross-reactivity of anti-dengue virus (DENV) antibodies in human sera against Zika virus (ZIKV), promoting increased ZIKV infection in vitro. However, the correlation between in vitro and in vivo findings is not well characterized. Thus, we evaluated the impact of heterotypic flavivirus immunity on ZIKV titers in biofluids of rhesus macaques. Animals previously infected (≥420 days) with DENV2, DENV4, or yellow fever virus were compared to flavivirus-naïve animals following infection with a Brazilian ZIKV strain. Sera from DENV-immune macaques demonstrated cross-reactivity with ZIKV by antibody-binding and neutralization assays prior to ZIKV infection, and promoted increased ZIKV infection in cell culture assays. Despite these findings, no significant differences between flavivirus-naïve and immune animals were observed in viral titers, neutralizing antibody levels, or immune cell kinetics following ZIKV infection. These results indicate that prior infection with heterologous flaviviruses neither conferred protection nor increased observed ZIKV titers in this non-human primate ZIKV infection model.

Original language	English
Article number	e1006487
Journal	PLoS Pathogens
Volume	13
Issue number	8
DOIs	https://doi.org/10.1371/journal.ppat.1006487
State	Published - Aug 2017
Externally published	Yes

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McCracken, M. K., Gromowski, G. D., Friberg, H. L., Lin, X., Abbink, P., De La Barrera, R., Eckles, K. H., Garver, L. S., Boyd, M., Jetton, D., Barouch, D. H., Wise, M. C., Lewis, B. S., Currier, J. R., Modjarrad, K., Milazzo, M., Liu, M., Mullins, A. B., Putnak, J. R., ... Thomas, S. J. (2017). Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques. PLoS Pathogens, 13(8), Article e1006487. https://doi.org/10.1371/journal.ppat.1006487

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title = "Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques",

abstract = "Studies have demonstrated cross-reactivity of anti-dengue virus (DENV) antibodies in human sera against Zika virus (ZIKV), promoting increased ZIKV infection in vitro. However, the correlation between in vitro and in vivo findings is not well characterized. Thus, we evaluated the impact of heterotypic flavivirus immunity on ZIKV titers in biofluids of rhesus macaques. Animals previously infected (≥420 days) with DENV2, DENV4, or yellow fever virus were compared to flavivirus-na{\"i}ve animals following infection with a Brazilian ZIKV strain. Sera from DENV-immune macaques demonstrated cross-reactivity with ZIKV by antibody-binding and neutralization assays prior to ZIKV infection, and promoted increased ZIKV infection in cell culture assays. Despite these findings, no significant differences between flavivirus-na{\"i}ve and immune animals were observed in viral titers, neutralizing antibody levels, or immune cell kinetics following ZIKV infection. These results indicate that prior infection with heterologous flaviviruses neither conferred protection nor increased observed ZIKV titers in this non-human primate ZIKV infection model.",

author = "McCracken, {Michael K.} and Gromowski, {Gregory D.} and Friberg, {Heather L.} and Xiaoxu Lin and Peter Abbink and {De La Barrera}, Rafael and Eckles, {Kenneth H.} and Garver, {Lindsey S.} and Michael Boyd and David Jetton and Barouch, {Dan H.} and Wise, {Matthew C.} and Lewis, {Bridget S.} and Currier, {Jeffrey R.} and Kayvon Modjarrad and Mark Milazzo and Michelle Liu and Mullins, {Anna B.} and Putnak, {J. Robert} and Michael, {Nelson L.} and Jarman, {Richard G.} and Thomas, {Stephen J.}",

year = "2017",

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McCracken, MK, Gromowski, GD, Friberg, HL, Lin, X, Abbink, P, De La Barrera, R, Eckles, KH, Garver, LS, Boyd, M, Jetton, D, Barouch, DH, Wise, MC, Lewis, BS, Currier, JR, Modjarrad, K, Milazzo, M, Liu, M, Mullins, AB, Putnak, JR, Michael, NL, Jarman, RG & Thomas, SJ 2017, 'Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques', PLoS Pathogens, vol. 13, no. 8, e1006487. https://doi.org/10.1371/journal.ppat.1006487

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AU - McCracken, Michael K.

AU - Gromowski, Gregory D.

AU - Friberg, Heather L.

AU - Lin, Xiaoxu

AU - Abbink, Peter

AU - De La Barrera, Rafael

AU - Eckles, Kenneth H.

AU - Garver, Lindsey S.

AU - Boyd, Michael

AU - Jetton, David

AU - Barouch, Dan H.

AU - Wise, Matthew C.

AU - Lewis, Bridget S.

AU - Currier, Jeffrey R.

AU - Modjarrad, Kayvon

AU - Milazzo, Mark

AU - Liu, Michelle

AU - Mullins, Anna B.

AU - Putnak, J. Robert

AU - Michael, Nelson L.

AU - Jarman, Richard G.

AU - Thomas, Stephen J.

PY - 2017/8

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N2 - Studies have demonstrated cross-reactivity of anti-dengue virus (DENV) antibodies in human sera against Zika virus (ZIKV), promoting increased ZIKV infection in vitro. However, the correlation between in vitro and in vivo findings is not well characterized. Thus, we evaluated the impact of heterotypic flavivirus immunity on ZIKV titers in biofluids of rhesus macaques. Animals previously infected (≥420 days) with DENV2, DENV4, or yellow fever virus were compared to flavivirus-naïve animals following infection with a Brazilian ZIKV strain. Sera from DENV-immune macaques demonstrated cross-reactivity with ZIKV by antibody-binding and neutralization assays prior to ZIKV infection, and promoted increased ZIKV infection in cell culture assays. Despite these findings, no significant differences between flavivirus-naïve and immune animals were observed in viral titers, neutralizing antibody levels, or immune cell kinetics following ZIKV infection. These results indicate that prior infection with heterologous flaviviruses neither conferred protection nor increased observed ZIKV titers in this non-human primate ZIKV infection model.

AB - Studies have demonstrated cross-reactivity of anti-dengue virus (DENV) antibodies in human sera against Zika virus (ZIKV), promoting increased ZIKV infection in vitro. However, the correlation between in vitro and in vivo findings is not well characterized. Thus, we evaluated the impact of heterotypic flavivirus immunity on ZIKV titers in biofluids of rhesus macaques. Animals previously infected (≥420 days) with DENV2, DENV4, or yellow fever virus were compared to flavivirus-naïve animals following infection with a Brazilian ZIKV strain. Sera from DENV-immune macaques demonstrated cross-reactivity with ZIKV by antibody-binding and neutralization assays prior to ZIKV infection, and promoted increased ZIKV infection in cell culture assays. Despite these findings, no significant differences between flavivirus-naïve and immune animals were observed in viral titers, neutralizing antibody levels, or immune cell kinetics following ZIKV infection. These results indicate that prior infection with heterologous flaviviruses neither conferred protection nor increased observed ZIKV titers in this non-human primate ZIKV infection model.

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SN - 1553-7366

VL - 13

JO - PLoS Pathogens

JF - PLoS Pathogens

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ER -

Impact of prior flavivirus immunity on Zika virus infection in rhesus macaques

Abstract

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