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A rhesus macaque model of Asia lineage Zika virus infection

Dawn M. Dudley, Matthew T. Aliota, Emma Mohr, Andrea M. Weiler, Gabrielle Lehrer-Brey, Kim L. Weisgrau, Mariel S. Mohns, Meghan E. Breitbach, Mustafa N. Rasheed, Christina M. Newman, Dane D. Gellerup, Louise H. Moncla, Jennifer Post, Nancy Schultz-Darken, Michele L. Schotkzo, Jennifer M. Hayes, Josh A. Eudailey, M. Anthony Moody, Sallie R. Permar, Shelby L. O’Connor, Eva G. Rakasz, Heather A. Simmons, Saverio Capuano III, Thaddeus G. Golos, Jorge E. Osorio, Thomas C. Friedrich, David H. O’Connor
doi: https://doi.org/10.1101/046334
Dawn M. Dudley
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
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Matthew T. Aliota
2Department of Pathobiological Sciences, University of Wisconsin-Madison
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Emma Mohr
3Department of Pediatrics, School of Medicine and Public Health, University of Wisconsin-Madison
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Andrea M. Weiler
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Gabrielle Lehrer-Brey
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Kim L. Weisgrau
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Mariel S. Mohns
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
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Meghan E. Breitbach
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
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Mustafa N. Rasheed
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
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Christina M. Newman
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
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Dane D. Gellerup
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Louise H. Moncla
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
2Department of Pathobiological Sciences, University of Wisconsin-Madison
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Jennifer Post
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Nancy Schultz-Darken
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Michele L. Schotkzo
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Jennifer M. Hayes
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Josh A. Eudailey
5Department of Pediatrics and Human Vaccine Institute, Duke University Medical Center
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M. Anthony Moody
5Department of Pediatrics and Human Vaccine Institute, Duke University Medical Center
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Sallie R. Permar
5Department of Pediatrics and Human Vaccine Institute, Duke University Medical Center
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Shelby L. O’Connor
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
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Eva G. Rakasz
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Heather A. Simmons
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Saverio Capuano III
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Thaddeus G. Golos
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
6Department of Comparative Biosciences and Obstetrics and Gynecology, University of Wisconsin-Madison.
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Jorge E. Osorio
2Department of Pathobiological Sciences, University of Wisconsin-Madison
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Thomas C. Friedrich
2Department of Pathobiological Sciences, University of Wisconsin-Madison
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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David H. O’Connor
1Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison
4Wisconsin National Primate Research Center, University of Wisconsin-Madison
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Abstract

Infection with Asian lineage Zika virus has been associated with Guillain-Barré syndrome and fetal abnormalities 1–4, but the mechanisms and risk factors for these outcomes remain unknown. Here we show that rhesus macaques are susceptible to infection by an Asian-lineage virus closely related to strains currently circulating in the Americas. Following subcutaneous inoculation, Zika virus RNA was detected in plasma one day post-infection (dpi) in all animals (N = 8, including 2 animals infected during the first trimester of pregnancy). Plasma viral loads peaked above 1 × 105 viral RNA copies/mL in seven of eight animals. Viral RNA was also present in saliva, urine, and cerebrospinal fluid (CSF), consistent with case reports from infected humans. Viral RNA was cleared from plasma and urine by 21 dpi in non-pregnant animals. In contrast, both pregnant animals remained viremic longer, up to 57 days. In all animals, infection was associated with transient increases in proliferating natural killer cells, CD8+ T cells, CD4+ T cells, and plasmablasts. Neutralizing antibodies were detected in all animals by 21 dpi. Rechallenge of three non-pregnant animals with the Asian-lineage Zika virus 10 weeks after the initial challenge resulted in no detectable virus replication, suggesting that primary Zika virus infection elicits protective immunity against homologous virus strains. These data establish that Asian-lineage Zika virus infection of rhesus macaques provides a relevant animal model for studying pathogenesis in pregnant and non-pregnant individuals and evaluating potential interventions against human infection, including during pregnancy.

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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-ND 4.0 International license.
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Posted May 10, 2016.
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A rhesus macaque model of Asia lineage Zika virus infection
Dawn M. Dudley, Matthew T. Aliota, Emma Mohr, Andrea M. Weiler, Gabrielle Lehrer-Brey, Kim L. Weisgrau, Mariel S. Mohns, Meghan E. Breitbach, Mustafa N. Rasheed, Christina M. Newman, Dane D. Gellerup, Louise H. Moncla, Jennifer Post, Nancy Schultz-Darken, Michele L. Schotkzo, Jennifer M. Hayes, Josh A. Eudailey, M. Anthony Moody, Sallie R. Permar, Shelby L. O’Connor, Eva G. Rakasz, Heather A. Simmons, Saverio Capuano III, Thaddeus G. Golos, Jorge E. Osorio, Thomas C. Friedrich, David H. O’Connor
bioRxiv 046334; doi: https://doi.org/10.1101/046334
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A rhesus macaque model of Asia lineage Zika virus infection
Dawn M. Dudley, Matthew T. Aliota, Emma Mohr, Andrea M. Weiler, Gabrielle Lehrer-Brey, Kim L. Weisgrau, Mariel S. Mohns, Meghan E. Breitbach, Mustafa N. Rasheed, Christina M. Newman, Dane D. Gellerup, Louise H. Moncla, Jennifer Post, Nancy Schultz-Darken, Michele L. Schotkzo, Jennifer M. Hayes, Josh A. Eudailey, M. Anthony Moody, Sallie R. Permar, Shelby L. O’Connor, Eva G. Rakasz, Heather A. Simmons, Saverio Capuano III, Thaddeus G. Golos, Jorge E. Osorio, Thomas C. Friedrich, David H. O’Connor
bioRxiv 046334; doi: https://doi.org/10.1101/046334

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