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Genetic Diversity and Evolution

Arteriviruses, Pegiviruses, and Lentiviruses Are Common among Wild African Monkeys

Adam L. Bailey, Michael Lauck, Ria R. Ghai, Chase W. Nelson, Katelyn Heimbruch, Austin L. Hughes, Tony L. Goldberg, Jens H. Kuhn, Anna J. Jasinska, Nelson B. Freimer, Cristian Apetrei, David H. O'Connor
G. Silvestri, Editor
Adam L. Bailey
aDepartment of Pathology and Laboratory Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
bWisconsin National Primate Research Center, Madison, Wisconsin, USA
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Michael Lauck
aDepartment of Pathology and Laboratory Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
bWisconsin National Primate Research Center, Madison, Wisconsin, USA
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Ria R. Ghai
cOdum School of Ecology, University of Georgia, Athens, Georgia, USA
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Chase W. Nelson
dDepartment of Biological Sciences, University of South Carolina, Columbia, South Carolina, USA
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Katelyn Heimbruch
aDepartment of Pathology and Laboratory Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
bWisconsin National Primate Research Center, Madison, Wisconsin, USA
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Austin L. Hughes
dDepartment of Biological Sciences, University of South Carolina, Columbia, South Carolina, USA
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Tony L. Goldberg
bWisconsin National Primate Research Center, Madison, Wisconsin, USA
eDepartment of Pathobiological Sciences, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Jens H. Kuhn
fIntegrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, Maryland, USA
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  • ORCID record for Jens H. Kuhn
Anna J. Jasinska
gCenter for Neurobehavioral Genetics, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, California, USA
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Nelson B. Freimer
gCenter for Neurobehavioral Genetics, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, California, USA
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Cristian Apetrei
hCenter for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
iDepartment of Microbiology and Molecular Genetics, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
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David H. O'Connor
aDepartment of Pathology and Laboratory Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
bWisconsin National Primate Research Center, Madison, Wisconsin, USA
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G. Silvestri
Emory University
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DOI: 10.1128/JVI.00573-16
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ABSTRACT

Nonhuman primates (NHPs) are a historically important source of zoonotic viruses and are a gold-standard model for research on many human pathogens. However, with the exception of simian immunodeficiency virus (SIV) (family Retroviridae), the blood-borne viruses harbored by these animals in the wild remain incompletely characterized. Here, we report the discovery and characterization of two novel simian pegiviruses (family Flaviviridae) and two novel simian arteriviruses (family Arteriviridae) in wild African green monkeys from Zambia (malbroucks [Chlorocebus cynosuros]) and South Africa (vervet monkeys [Chlorocebus pygerythrus]). We examine several aspects of infection, including viral load, genetic diversity, evolution, and geographic distribution, as well as host factors such as age, sex, and plasma cytokines. In combination with previous efforts to characterize blood-borne RNA viruses in wild primates across sub-Saharan Africa, these discoveries demonstrate that in addition to SIV, simian pegiviruses and simian arteriviruses are widespread and prevalent among many African cercopithecoid (i.e., Old World) monkeys.

IMPORTANCE Primates are an important source of viruses that infect humans and serve as an important laboratory model of human virus infection. Here, we discover two new viruses in African green monkeys from Zambia and South Africa. In combination with previous virus discovery efforts, this finding suggests that these virus types are widespread among African monkeys. Our analysis suggests that one of these virus types, the simian arteriviruses, may have the potential to jump between different primate species and cause disease. In contrast, the other virus type, the pegiviruses, are thought to reduce the disease caused by human immunodeficiency virus (HIV) in humans. However, we did not observe a similar protective effect in SIV-infected African monkeys coinfected with pegiviruses, possibly because SIV causes little to no disease in these hosts.

This work is dedicated to the memory of Austin L. Hughes, who died unexpectedly during the preparation of the manuscript. He was our collaborator, mentor, and friend, and we are deeply indebted to him for the great contributions he made, both to our lives and to this work.

FOOTNOTES

    • Received 30 March 2016.
    • Accepted 6 May 2016.
    • Accepted manuscript posted online 11 May 2016.
  • Address correspondence to David H. O'Connor, doconnor{at}primate.wisc.edu.
  • Citation Bailey AL, Lauck M, Ghai RR, Nelson CW, Heimbruch K, Hughes AL, Goldberg TL, Kuhn JH, Jasinska AJ, Freimer NB, Apetrei C, O'Connor DH, International Vervet Research Consortium. 2016. Arteriviruses, pegiviruses, and lentiviruses are common among wild African monkeys. J Virol 90:6724–6737. doi:10.1128/JVI.00573-16.

  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/JVI.00573-16.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Arteriviruses, Pegiviruses, and Lentiviruses Are Common among Wild African Monkeys
Adam L. Bailey, Michael Lauck, Ria R. Ghai, Chase W. Nelson, Katelyn Heimbruch, Austin L. Hughes, Tony L. Goldberg, Jens H. Kuhn, Anna J. Jasinska, Nelson B. Freimer, Cristian Apetrei, David H. O'Connor for the International Vervet Research Consortium
Journal of Virology Jul 2016, 90 (15) 6724-6737; DOI: 10.1128/JVI.00573-16

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Arteriviruses, Pegiviruses, and Lentiviruses Are Common among Wild African Monkeys
Adam L. Bailey, Michael Lauck, Ria R. Ghai, Chase W. Nelson, Katelyn Heimbruch, Austin L. Hughes, Tony L. Goldberg, Jens H. Kuhn, Anna J. Jasinska, Nelson B. Freimer, Cristian Apetrei, David H. O'Connor for the International Vervet Research Consortium
Journal of Virology Jul 2016, 90 (15) 6724-6737; DOI: 10.1128/JVI.00573-16
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