Zika viral dynamics and shedding in rhesus and cynomolgus macaques

Osuna, Christa E.; Lim, So -Yon; Deleage, Claire; Griffin, Bryan D.; Stein, Derek; Schroeder, Lukas T.; Omange, Robert; Best, Katharine; Luo, Ma; Hraber, Peter Thomas; Andersen-Elyard, Hanne; Ojeda, Erwing Fabian Cardozo; Huang, Scott; Vanlandingham, Dana L.; Higgs, Stephen; Perelson, Alan S.; Estes, Jacob D.; Safronetz, David; Lewis, Mark G.; Whitney, James B.

doi:10.1038/nm.4206

Title: Zika viral dynamics and shedding in rhesus and cynomolgus macaques

Journal Article · Mon Oct 03 00:00:00 EDT 2016 · Nature Medicine

DOI:https://doi.org/10.1038/nm.4206· OSTI ID:1334153

^[1]; Lim, So -Yon ^[1]; Deleage, Claire ^[2]; Griffin, Bryan D. ^[3]; Stein, Derek ^[3]; Schroeder, Lukas T. ^[3];

^[3]; Best, Katharine ^[4]; Luo, Ma ^[3];

^[4]; Andersen-Elyard, Hanne ^[5]; Ojeda, Erwing Fabian Cardozo ^[4]; Huang, Scott ^[6]; Vanlandingham, Dana L. ^[6]; Higgs, Stephen ^[6]; Perelson, Alan S. ^[4]; Estes, Jacob D. ^[2]; Safronetz, David ^[3]; Lewis, Mark G. ^[5]; Whitney, James B. ^[7]

Harvard Medical School, Boston, MA (United States)
Frederick National Lab. for Cancer Research, Frederick, MD (United States)
National Microbiology Lab., Winnipeg, MB (Canada)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Bioqual, Rockville, MD (United States)
Kansas State Univ., Manhattan, KS (United States)
Harvard Medical School, Boston, MA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Infection with Zika virus has been associated with serious neurological complications and fetal abnormalities. However, the dynamics of viral infection, replication and shedding are poorly understood. Here we show that both rhesus and cynomolgus macaques are highly susceptible to infection by lineages of Zika virus that are closely related to, or are currently circulating in, the Americas. After subcutaneous viral inoculation, viral RNA was detected in blood plasma as early as 1 d after infection. Viral RNA was also detected in saliva, urine, cerebrospinal fluid (CSF) and semen, but transiently in vaginal secretions. Although viral RNA during primary infection was cleared from blood plasma and urine within 10 d, viral RNA was detectable in saliva and seminal fluids until the end of the study, 3 weeks after the resolution of viremia in the blood. The control of primary Zika virus infection in the blood was correlated with rapid innate and adaptive immune responses. We also identified Zika RNA in tissues, including the brain and male and female reproductive tissues, during early and late stages of infection. Re-infection of six animals 45 d after primary infection with a heterologous strain resulted in complete protection, which suggests that primary Zika virus infection elicits protective immunity. Finally, early invasion of Zika virus into the nervous system of healthy animals and the extent and duration of shedding in saliva and semen underscore possible concern for additional neurologic complications and nonarthropod-mediated transmission in humans.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1334153

Report Number(s):: LA-UR-16-25423

Journal Information:: Nature Medicine, Journal Name: Nature Medicine; ISSN 1078-8956

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 3 works

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Zika Virus Tissue and Blood Compartmentalization in Acute Infection of Rhesus Macaques Coffey, Lark L.; Pesavento, Patricia A.; Keesler, Rebekah I. PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0171148	journal	January 2017
Recombinant Zika virus envelope protein elicited protective immunity against Zika virus in immunocompetent mice Liang, Huabin; Yang, Ruoheng; Liu, Zhihua PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0194860	journal	March 2018
Dengue immune sera enhance Zika virus infection in human peripheral blood monocytes through Fc gamma receptors Li, Min; Zhao, Lingzhai; Zhang, Chao PLOS ONE, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pone.0200478	journal	July 2018
Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques Nguyen, Sydney M.; Antony, Kathleen M.; Dudley, Dawn M. PLOS Pathogens, Vol. 13, Issue 5 https://doi.org/10.1371/journal.ppat.1006378	journal	May 2017
Zika virus infection at mid-gestation results in fetal cerebral cortical injury and fetal death in the olive baboon Gurung, Sunam; Reuter, Nicole; Preno, Alisha PLOS Pathogens, Vol. 15, Issue 1 https://doi.org/10.1371/journal.ppat.1007507	journal	January 2019
Primary infection with dengue or Zika virus does not affect the severity of heterologous secondary infection in macaques Breitbach, Meghan E.; Newman, Christina M.; Dudley, Dawn M. PLOS Pathogens, Vol. 15, Issue 8 https://doi.org/10.1371/journal.ppat.1007766	journal	August 2019
High Infection Rates for Adult Macaques after Intravaginal or Intrarectal Inoculation with Zika Virus Haddow, Andrew D.; Nalca, Aysegul; Rossi, Franco D. Emerging Infectious Diseases, Vol. 23, Issue 8 https://doi.org/10.3201/eid2308.170036	journal	August 2017
Route of Infection Influences Zika Virus Shedding in a Guinea Pig Model Saver, Ashley E.; Crawford, Stephanie A.; Joyce, Jonathan D. Cells, Vol. 8, Issue 11 https://doi.org/10.3390/cells8111437	journal	November 2019
Zika Virus Persistently and Productively Infects Primary Adult Sensory Neurons In Vitro Swartwout, Brianna; Zlotnick, Marta; Saver, Ashley Pathogens, Vol. 6, Issue 4 https://doi.org/10.3390/pathogens6040049	journal	October 2017
Zika Virus Trafficking and Interactions in the Human Male Reproductive Tract Da Silva, Lucia Pathogens, Vol. 7, Issue 2 https://doi.org/10.3390/pathogens7020051	journal	May 2018
Preliminary Studies on Immune Response and Viral Pathogenesis of Zika Virus in Rhesus Macaques Woollard, Shawna; Olwenyi, Omalla; Dutta, Debashis Pathogens, Vol. 7, Issue 3 https://doi.org/10.3390/pathogens7030070	journal	August 2018
Late Neurological Consequences of Zika Virus Infection: Risk Factors and Pharmaceutical Approaches Souza, Isis N. O.; Barros-Aragão, Fernanda G. Q.; Frost, Paula S. Pharmaceuticals, Vol. 12, Issue 2 https://doi.org/10.3390/ph12020060	journal	April 2019
Comparative Pathogenesis of Asian and African-Lineage Zika Virus in Indian Rhesus Macaque’s and Development of a Non-Human Primate Model Suitable for the Evaluation of New Drugs and Vaccines Rayner, Jonathan; Kalkeri, Raj; Goebel, Scott Viruses, Vol. 10, Issue 5 https://doi.org/10.3390/v10050229	journal	May 2018
A ‘Furry-Tale’ of Zika Virus Infection: What Have We Learned from Animal Models? Nazerai, Loulieta; Pravsgaard Christensen, Jan; Randrup Thomsen, Allan Viruses, Vol. 11, Issue 1 https://doi.org/10.3390/v11010029	journal	January 2019
Zika Virus: Recent Advances towards the Development of Vaccines and Therapeutics McArthur, Monica Viruses, Vol. 9, Issue 6 https://doi.org/10.3390/v9060143	journal	June 2017
A Novel Neutralizing Antibody Specific to the DE Loop of VP1 Can Inhibit EV-D68 Infection in Mice Zheng, Huiwen; Wang, Jingjing; Li, Bingxiang The Journal of Immunology, Vol. 201, Issue 9 https://doi.org/10.4049/jimmunol.1800655	journal	October 2018
Zika seroprevalence declines and neutralizing antibodies wane in adults following outbreaks in French Polynesia and Fiji Henderson, Alasdair D.; Aubry, Maite; Kama, Mike eLife, Vol. 9 https://doi.org/10.7554/elife.48460	journal	January 2020
Structural and Practical Identifiability Analysis of Zika Epidemiological Models Tuncer, Necibe; Marctheva, Maia; LaBarre, Brian Bulletin of Mathematical Biology, Vol. 80, Issue 8 https://doi.org/10.1007/s11538-018-0453-z	journal	June 2018
Zika virus pathogenesis in rhesus macaques is unaffected by pre-existing immunity to dengue virus Pantoja, Petraleigh; Pérez-Guzmán, Erick X.; Rodríguez, Idia V. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15674	journal	June 2017
Early cellular innate immune responses drive Zika viral persistence and tissue tropism in pigtail macaques O’Connor, Megan A.; Tisoncik-Go, Jennifer; Lewis, Thomas B. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05826-w	journal	August 2018
Routes of Zika virus dissemination in the testis and epididymis of immunodeficient mice Tsetsarkin, Konstantin A.; Maximova, Olga A.; Liu, Guangping Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07782-x	journal	December 2018
Time elapsed between Zika and dengue virus infections affects antibody and T cell responses Pérez-Guzmán, Erick X.; Pantoja, Petraleigh; Serrano-Collazo, Crisanta Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12295-2	journal	September 2019
Experimental Zika Virus Inoculation in a New World Monkey Model Reproduces Key Features of the Human Infection Chiu, Charles Y.; Sánchez-San Martín, Claudia; Bouquet, Jerome Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-17067-w	journal	December 2017
Multimodal assessments of Zika virus immune pathophysiological responses in marmosets Lum, Fok-Moon; Zhang, Wei; Lim, Kheng-Choon Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35481-6	journal	November 2018
High susceptibility, viral dynamics and persistence of South American Zika virus in New World monkey species Berry, Neil; Ferguson, Deborah; Ham, Claire Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-50918-2	journal	October 2019
Zika virus infection at mid-gestation results in fetal cerebral cortical injury and fetal death in the olive baboon Gurung, Sunam; Reuter, Nicole; Preno, Alisha https://doi.org/10.1101/331108	posted_content	May 2018
Antibody responses to Zika virus proteins in pregnant and non-pregnant macaques Hefron, Anna S.; Mohr, Emma L.; Baker, David PLOS Neglected Tropical Diseases https://doi.org/10.1101/352880	journal	August 2018
Ocular and uteroplacental pathology in a macaque pregnancy with congenital Zika virus infection Mohr, Emma L.; Block, Lindsey N.; Newman, Christina M. PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0190617	journal	January 2018
Human stem cell-derived hepatocyte-like cells support Zika virus replication and provide a relevant model to assess the efficacy of potential antivirals Tricot, Tine; Helsen, Nicky; Kaptein, Suzanne J. F. PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0209097	journal	December 2018
Zika virus preferentially replicates in the female reproductive tract after vaginal inoculation of rhesus macaques Carroll, Timothy; Lo, Ming; Lanteri, Marion PLOS Pathogens, Vol. 13, Issue 7 https://doi.org/10.1371/journal.ppat.1006537	journal	July 2017
Development of a Zika Virus Infection Model in Cynomolgus Macaques Koide, Fusataka; Goebel, Scott; Snyder, Beth Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.02028	journal	December 2016
Modeling the 2013 Zika Outbreak in French Polynesia: Intervention Strategies Gwalani, Harsha; Hawamdeh, Faris; Mikler, Armin Applied System Innovation, Vol. 1, Issue 3 https://doi.org/10.3390/asi1030031	journal	August 2018
ZIKV Demonstrates Minimal Pathologic Effects and Mosquito Infectivity in Viremic Cynomolgus Macaques Azar, Sasha; Rossi, Shannan; Haller, Sherry Viruses, Vol. 10, Issue 11 https://doi.org/10.3390/v10110661	journal	November 2018
Sexual transmission of Zika virus and other flaviviruses: A living systematic review. Counotte, Michel Jacques; Kim, Caron Rahn; Wang, Jingying Public Library of Science https://doi.org/10.7892/boris.118965	text	January 2018
Aedes aegypti AgBR1 antibodies modulate early Zika virus infection of mice Uraki, Ryuta; Hastings, Andrew K.; Marin-Lopez, Alejandro Nature Microbiology, Vol. 4, Issue 6 https://doi.org/10.1038/s41564-019-0385-x	journal	March 2019
Zika plasma viral dynamics in nonhuman primates provides insights into early infection and antiviral strategies Best, Katharine; Guedj, Jeremie; Madelain, Vincent Proceedings of the National Academy of Sciences, Vol. 114, Issue 33 https://doi.org/10.1073/pnas.1704011114	journal	August 2017
Time elapsed between Zika and dengue virus infections affects antibody and T cell responses L. J., White,; L., Cruz,; T., Arana, Nature Publishing Group https://doi.org/10.17615/1x5g-ec51	text	January 2019
Zika virus pathogenesis in rhesus macaques is unaffected by pre-existing immunity to dengue virus Olga, González,; V., Rodríguez, Idia; Petraleigh, Pantoja, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/7pma-1j24	text	January 2017
Postnatal Zika virus infection is associated with persistent abnormalities in brain structure, function, and behavior in infant macaques V., Avanzato,; J., Habib,; Z., Kovacs-Balint, American Association for the Advancement of Science https://doi.org/10.17615/zqxj-nt15	text	January 2018
Immune Cell Dynamics in Rhesus Macaques Infected with a Brazilian Strain of Zika Virus Silveira, Eduardo L. V.; Rogers, Kenneth A.; Gumber, Sanjeev The Journal of Immunology, Vol. 199, Issue 3 https://doi.org/10.4049/jimmunol.1700256	journal	June 2017
Infection via mosquito bite alters Zika virus tissue tropism and replication kinetics in rhesus macaques Dudley, Dawn M.; Newman, Christina M.; Lalli, Joseph Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02222-8	journal	December 2017
An optimized purified inactivated Zika vaccine provides sustained immunogenicity and protection in cynomolgus macaques Lecouturier, Valérie; Pavot, Vincent; Berry, Catherine npj Vaccines, Vol. 5, Issue 1 https://doi.org/10.1038/s41541-020-0167-8	journal	March 2020
Complete Protection in Macaques Conferred by Purified Inactivated Zika Vaccine: Defining a Correlate of Protection Young, Ginger; Bohning, Kelly J.; Zahralban-Steele, Melissa Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-60415-6	journal	February 2020
Simian Immunodeficiency Virus Infection of Rhesus Macaques Results in Delayed Zika Virus Clearance Vinton, Carol L.; Magaziner, Samuel J.; Dowd, Kimberly A. mBio, Vol. 10, Issue 6 https://doi.org/10.1128/mbio.02790-19	journal	December 2019
Zika virus reservoirs: Implications for transmission, future outbreaks, drug and vaccine development Kalkeri, Raj; Murthy, Krishna K. F1000Research, Vol. 6 https://doi.org/10.12688/f1000research.12695.1	journal	October 2017
Zika Virus: What Have We Learnt Since the Start of the Recent Epidemic? Saiz, Juan-Carlos; Martín-Acebes, Miguel A.; Bueno-Marí, Rubén Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01554	journal	August 2017
Mathematical Analysis of Viral Replication Dynamics and Antiviral Treatment Strategies: From Basic Models to Age-Based Multi-Scale Modeling Zitzmann, Carolin; Kaderali, Lars Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01546	journal	July 2018
Susceptibility of Chicken Embryos, Sheep, Cattle, Pigs, and Chickens to Zika Virus Infection Ambagala, Aruna; Truong, Thang; Cottam-Birt, Colleen Frontiers in Veterinary Science, Vol. 7 https://doi.org/10.3389/fvets.2020.00023	journal	February 2020
Zika Virus in the Male Reproductive Tract Stassen, Liesel; Armitage, Charles; van der Heide, David Viruses, Vol. 10, Issue 4 https://doi.org/10.3390/v10040198	journal	April 2018
Research Models and Tools for the Identification of Antivirals and Therapeutics against Zika Virus Infection Alves, Marco P.; Vielle, Nathalie J.; Thiel, Volker Viruses, Vol. 10, Issue 11 https://doi.org/10.3390/v10110593	journal	October 2018

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