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Prior dengue immunity enhances Zika virus infection of the maternal-fetal interface in rhesus macaques

View ORCID ProfileC. M. Crooks, A. M. Weiler, S. L. Rybarczyk, M. I. Bliss, A. S. Jaeger, M. E. Murphy, H. A. Simmons, A. Mejia, M. K. Fritsch, J. M. Hayes, J. C. Eickhoff, A. M. Mitzey, E. Razo, K. M. Braun, E. A. Brown, K. Yamamoto, P. M. Shepherd, A. Possell, K. Weaver, K. M. Antony, T. K. Morgan, C. M. Newman, D. M. Dudley, N. Schultz-Darken, E. Peterson, L. C. Katzelnick, A. Balmaseda, E. Harris, D. H. O’Connor, E. L. Mohr, T. G. Golos, View ORCID ProfileT. C. Friedrich, View ORCID ProfileM. T. Aliota
doi: https://doi.org/10.1101/2021.01.25.428184
C. M. Crooks
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA
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A. M. Weiler
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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S. L. Rybarczyk
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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M. I. Bliss
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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A. S. Jaeger
3Department of Veterinary and Biomedical Sciences, University of Minnesota, Twin Cities, St. Paul, MN, USA
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M. E. Murphy
4Department of Comparative Biosciences, University of Wisconsin-Madison, Madison, WI, USA
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H. A. Simmons
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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A. Mejia
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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M. K. Fritsch
5Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, USA
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J. M. Hayes
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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J. C. Eickhoff
6Department of Biostatistics and Medical Informatics, University of Wisconsin-Madison, Madison, WI, USA
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A. M. Mitzey
4Department of Comparative Biosciences, University of Wisconsin-Madison, Madison, WI, USA
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E. Razo
7Department of Pediatrics, University of Wisconsin-Madison, Madison, WI, USA
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K. M. Braun
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA
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E. A. Brown
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA
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K. Yamamoto
5Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, USA
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P. M. Shepherd
5Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, USA
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A. Possell
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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K. Weaver
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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K. M. Antony
8Department of Obstetrics and Gynecology, University of Wisconsin-Madison, Madison, WI, USA
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T. K. Morgan
9Department of Pathology, Oregon Health and Science University, Portland, OR, USA
10Department of Obstetrics and Gynecology, Oregon Health and Science University, Portland, OR, USA
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C. M. Newman
5Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, USA
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D. M. Dudley
5Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, USA
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N. Schultz-Darken
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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E. Peterson
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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L. C. Katzelnick
11Division of Infectious Diseases and Vaccinology, University of California Berkeley, Berkeley, CA, USA
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A. Balmaseda
12Sustainable Sciences Institute, Managua, Nicaragua
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E. Harris
11Division of Infectious Diseases and Vaccinology, University of California Berkeley, Berkeley, CA, USA
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D. H. O’Connor
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
5Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, USA
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E. L. Mohr
7Department of Pediatrics, University of Wisconsin-Madison, Madison, WI, USA
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T. G. Golos
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
4Department of Comparative Biosciences, University of Wisconsin-Madison, Madison, WI, USA
8Department of Obstetrics and Gynecology, University of Wisconsin-Madison, Madison, WI, USA
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T. C. Friedrich
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA
2Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA
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  • For correspondence: tfriedri@wisc.edu mtaliota@umn.edu
M. T. Aliota
3Department of Veterinary and Biomedical Sciences, University of Minnesota, Twin Cities, St. Paul, MN, USA
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  • For correspondence: tfriedri@wisc.edu mtaliota@umn.edu
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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 prior DENV-2 exposure enhanced ZIKV infection of maternal-fetal interface tissues in 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.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 26, 2021.
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Prior dengue immunity enhances Zika virus infection of the maternal-fetal interface in rhesus macaques
C. M. Crooks, A. M. Weiler, S. L. Rybarczyk, M. I. Bliss, A. S. Jaeger, M. E. Murphy, H. A. Simmons, A. Mejia, M. K. Fritsch, J. M. Hayes, J. C. Eickhoff, A. M. Mitzey, E. Razo, K. M. Braun, E. A. Brown, K. Yamamoto, P. M. Shepherd, A. Possell, K. Weaver, K. M. Antony, T. K. Morgan, C. M. Newman, D. M. Dudley, N. Schultz-Darken, E. Peterson, L. C. Katzelnick, A. Balmaseda, E. Harris, D. H. O’Connor, E. L. Mohr, T. G. Golos, T. C. Friedrich, M. T. Aliota
bioRxiv 2021.01.25.428184; doi: https://doi.org/10.1101/2021.01.25.428184
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Prior dengue immunity enhances Zika virus infection of the maternal-fetal interface in rhesus macaques
C. M. Crooks, A. M. Weiler, S. L. Rybarczyk, M. I. Bliss, A. S. Jaeger, M. E. Murphy, H. A. Simmons, A. Mejia, M. K. Fritsch, J. M. Hayes, J. C. Eickhoff, A. M. Mitzey, E. Razo, K. M. Braun, E. A. Brown, K. Yamamoto, P. M. Shepherd, A. Possell, K. Weaver, K. M. Antony, T. K. Morgan, C. M. Newman, D. M. Dudley, N. Schultz-Darken, E. Peterson, L. C. Katzelnick, A. Balmaseda, E. Harris, D. H. O’Connor, E. L. Mohr, T. G. Golos, T. C. Friedrich, M. T. Aliota
bioRxiv 2021.01.25.428184; doi: https://doi.org/10.1101/2021.01.25.428184

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