Previous exposure to dengue virus is associated with increased zika virus burden at the maternal-fetal interface in rhesus macaques

Chelsea M. Crooks; Andrea M. Weiler; Sierra L. Rybarczyk; Mason I. Bliss; Anna S. Jaeger; Megan E. Murphy; Heather A. Simmons; Andres Mejia; Michael K. Fritsch; Jennifer M. Hayes; Jens C. Eickhoff; Ann M. Mitzey; Elaina Razo; Katarina M. Braun; Elizabeth A. Brown; Keisuke Yamamoto; Phoenix M. Shepherd; Amber Possell; Kara Weaver; Kathleen M. Antony; Terry K. Morgan; Christina M. Newman; Dawn M. Dudley; Nancy Schultz-Darken; Eric Peterson; Leah C. Katzelnick; Angel Balmaseda; Eva Harris; David H. O’Connor; Emma L. Mohr; Thaddeus G. Golos; Thomas C. Friedrich; Matthew T. Aliota

doi:10.1371/journal.pntd.0009641

Previous exposure to dengue virus is associated with increased zika virus burden at the maternal-fetal interface in rhesus macaques

Chelsea M. Crooks, Andrea M. Weiler, Sierra L. Rybarczyk, Mason I. Bliss, Anna S. Jaeger, Megan E. Murphy, Heather A. Simmons, Andres Mejia, Michael K. Fritsch, Jennifer M. Hayes, Jens C. Eickhoff, Ann M. Mitzey, Elaina Razo, Katarina M. Braun, Elizabeth A. Brown, Keisuke Yamamoto, Phoenix M. Shepherd, Amber Possell, Kara Weaver, Kathleen M. AntonyTerry K. Morgan, Christina M. Newman, Dawn M. Dudley, Nancy Schultz-Darken, Eric Peterson, Leah C. Katzelnick, Angel Balmaseda, Eva Harris, David H. O’Connor, Emma L. Mohr, Thaddeus G. Golos, Thomas C. Friedrich, Matthew T. Aliota

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Abstract

Concerns have arisen that pre-existing immunity to dengue virus (DENV) could enhance Zika virus (ZIKV) disease, due to the homology between ZIKV and DENV and the observation of antibody-dependent enhancement (ADE) among DENV serotypes. To date, no study has examined the impact of pre-existing DENV immunity on ZIKV pathogenesis during pregnancy in a translational non-human primate model. Here we show that macaques with a prior DENV-2 exposure had a higher burden of ZIKV vRNA in maternal-fetal interface tissues as compared to DENV-naive macaques. However, pre-existing DENV immunity had no detectable impact on ZIKV replication kinetics in maternal plasma, and all pregnancies progressed to term without adverse outcomes or gross fetal abnormalities detectable at delivery. Understanding the risks of ADE to pregnant women worldwide is critical as vaccines against DENV and ZIKV are developed and licensed and as DENV and ZIKV continue to circulate.

Original language	English (US)
Article number	e0009641
Journal	PLoS neglected tropical diseases
Volume	15
Issue number	7
DOIs	https://doi.org/10.1371/journal.pntd.0009641
State	Published - Jul 2021

ASJC Scopus subject areas

Public Health, Environmental and Occupational Health
Infectious Diseases

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Crooks, C. M., Weiler, A. M., Rybarczyk, S. L., Bliss, M. I., Jaeger, A. S., Murphy, M. E., Simmons, H. A., Mejia, A., Fritsch, M. K., Hayes, J. M., Eickhoff, J. C., Mitzey, A. M., Razo, E., Braun, K. M., Brown, E. A., Yamamoto, K., Shepherd, P. M., Possell, A., Weaver, K., ... Aliota, M. T. (2021). Previous exposure to dengue virus is associated with increased zika virus burden at the maternal-fetal interface in rhesus macaques. PLoS neglected tropical diseases, 15(7), Article e0009641. https://doi.org/10.1371/journal.pntd.0009641

Crooks, CM, Weiler, AM, Rybarczyk, SL, Bliss, MI, Jaeger, AS, Murphy, ME, Simmons, HA, Mejia, A, Fritsch, MK, Hayes, JM, Eickhoff, JC, Mitzey, AM, Razo, E, Braun, KM, Brown, EA, Yamamoto, K, Shepherd, PM, Possell, A, Weaver, K, Antony, KM, Morgan, TK, Newman, CM, Dudley, DM, Schultz-Darken, N, Peterson, E, Katzelnick, LC, Balmaseda, A, Harris, E, O’Connor, DH, Mohr, EL, Golos, TG, Friedrich, TC & Aliota, MT 2021, 'Previous exposure to dengue virus is associated with increased zika virus burden at the maternal-fetal interface in rhesus macaques', PLoS neglected tropical diseases, vol. 15, no. 7, e0009641. https://doi.org/10.1371/journal.pntd.0009641

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title = "Previous exposure to dengue virus is associated with increased zika virus burden at the maternal-fetal interface in rhesus macaques",

abstract = "Concerns have arisen that pre-existing immunity to dengue virus (DENV) could enhance Zika virus (ZIKV) disease, due to the homology between ZIKV and DENV and the observation of antibody-dependent enhancement (ADE) among DENV serotypes. To date, no study has examined the impact of pre-existing DENV immunity on ZIKV pathogenesis during pregnancy in a translational non-human primate model. Here we show that macaques with a prior DENV-2 exposure had a higher burden of ZIKV vRNA in maternal-fetal interface tissues as compared to DENV-naive macaques. However, pre-existing DENV immunity had no detectable impact on ZIKV replication kinetics in maternal plasma, and all pregnancies progressed to term without adverse outcomes or gross fetal abnormalities detectable at delivery. Understanding the risks of ADE to pregnant women worldwide is critical as vaccines against DENV and ZIKV are developed and licensed and as DENV and ZIKV continue to circulate.",

author = "Crooks, {Chelsea M.} and Weiler, {Andrea M.} and Rybarczyk, {Sierra L.} and Bliss, {Mason I.} and Jaeger, {Anna S.} and Murphy, {Megan E.} and Simmons, {Heather A.} and Andres Mejia and Fritsch, {Michael K.} and Hayes, {Jennifer M.} and Eickhoff, {Jens C.} and Mitzey, {Ann M.} and Elaina Razo and Braun, {Katarina M.} and Brown, {Elizabeth A.} and Keisuke Yamamoto and Shepherd, {Phoenix M.} and Amber Possell and Kara Weaver and Antony, {Kathleen M.} and Morgan, {Terry K.} and Newman, {Christina M.} and Dudley, {Dawn M.} and Nancy Schultz-Darken and Eric Peterson and Katzelnick, {Leah C.} and Angel Balmaseda and Eva Harris and O{\textquoteright}Connor, {David H.} and Mohr, {Emma L.} and Golos, {Thaddeus G.} and Friedrich, {Thomas C.} and Aliota, {Matthew T.}",

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year = "2021",

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AU - Crooks, Chelsea M.

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AU - Bliss, Mason I.

AU - Jaeger, Anna S.

AU - Murphy, Megan E.

AU - Simmons, Heather A.

AU - Mejia, Andres

AU - Fritsch, Michael K.

AU - Hayes, Jennifer M.

AU - Eickhoff, Jens C.

AU - Mitzey, Ann M.

AU - Razo, Elaina

AU - Braun, Katarina M.

AU - Brown, Elizabeth A.

AU - Yamamoto, Keisuke

AU - Shepherd, Phoenix M.

AU - Possell, Amber

AU - Weaver, Kara

AU - Antony, Kathleen M.

AU - Morgan, Terry K.

AU - Newman, Christina M.

AU - Dudley, Dawn M.

AU - Schultz-Darken, Nancy

AU - Peterson, Eric

AU - Katzelnick, Leah C.

AU - Balmaseda, Angel

AU - Harris, Eva

AU - O’Connor, David H.

AU - Mohr, Emma L.

AU - Golos, Thaddeus G.

AU - Friedrich, Thomas C.

AU - Aliota, Matthew T.

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Previous exposure to dengue virus is associated with increased zika virus burden at the maternal-fetal interface in rhesus macaques

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