Non-Human Primate Models of Enteric Viral Infections
Abstract
:1. Introduction
2. Conventional and Specific Pathogen-Free (SPF) Research Colonies of Captive NHPs
3. Enteric Virus Infections in Captive NHPs
4. The Common Enteric Virus Infections in Humans
5. Simian Rotaviruses
6. Rhesus Enteric Caliciviruses (ReCV)
7. Advantages of Studies that Utilize NHP Models
8. Other Enteric Viruses
9. Enteric Virome and Gut Dysbiosis
Funding
Conflicts of Interest
References
- Landsteiner, K. Zur kenntnis der antifermentativen, lytischen and agglutinieren wirkungen des blutserums und der lymphe. Zentralblatt Bakteriol. 1900, 27, 357–362. (In German) [Google Scholar]
- Garcia-Tellez, T.; Huot, N.; Ploquin, M.J.; Rascle, P.; Jacquelin, B.; Muller-Trutwin, M. Non-human primates in HIV research: Achievements, limits and alternatives. Infect. Genet. Evol. 2016, 46, 324–332. [Google Scholar] [CrossRef] [PubMed]
- Malherbe, H.; Harvin, R. The cytopathic effects of vervet monkey viruses. S. Afr. Med. J. 1963, 37, 407–411. [Google Scholar] [PubMed]
- Stuker, G.; Oshiro, L.S.; Schmidt, N.J. Antigenic comparisons of two new rotaviruses from rhesus monkeys. J. Clin. Microbiol. 1980, 11, 202–203. [Google Scholar] [PubMed]
- McNeal, M.M.; Sestak, K.; Choi, A.H.C.; Basu, M.; Cole, M.J.; Aye, P.P.; Bohm, R.P.; Ward, R.L. Development of a rotavirus-shedding model in rhesus macaques, using a homologous wild-type rotavirus of a new P genotype. J. Virol. 2005, 79, 944–954. [Google Scholar] [CrossRef] [PubMed]
- Hoshino, Y.; Honma, S.; Jones, R.W.; Santos, N.; Nakagomi, O.; Nakagomi, T.; Kapikian, A.Z.; Thoules, M.E. A rotavirus strain isolated from pig-tailed macaque (Macaca nemestrina) with diarrhea bears a P6 [1]: G8 specificity. Virology 2006, 345, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Farkas, T.; Sestak, K.; Wei, C.; Jiang, X. Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J. Virol. 2008, 82, 5408–5416. [Google Scholar] [CrossRef] [PubMed]
- Farkas, T.; Dufour, J.; Jiang, X.; Sestak, K. Detection of norovirus-, sapovirus- and rhesus enteric calicivirus-specific antibodies in captive juvenile macaques. J. Gen. Virol. 2010, 91, 734–738. [Google Scholar] [CrossRef] [PubMed]
- Farkas, T.; Cross, R.W.; Hargitt, E.; Lerche, N.W.; Morrow, A.L.; Sestak, K. Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J. Virol. 2010, 84, 8617–8625. [Google Scholar] [CrossRef] [PubMed]
- Wei, C.; Farkas, T.; Sestak, K.; Jiang, X. Recovery of infectious virus by transfection of in vitro-generated RNA from Tulane calicivirus cDNA. J. Virol. 2008, 82, 11429–11436. [Google Scholar] [CrossRef] [PubMed]
- Matthijnssens, J.; Taraporewala, Z.F.; Yang, H.; Rao, S.; Yuan, L.; Cao, D.; Hoshino, Y.; Mertens, P.P.; Carner, G.R.; McNeal, M.; et al. Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J. Virol. 2010, 84, 2013–2026. [Google Scholar] [CrossRef] [PubMed]
- Otsyula, M.; Yee, J.; Suleman, M.; Tarara, R.; Martins, J.; Woods, P.; Glass, R.; Jennings, M. Rotavirus infection in African non-human primates. Ann. Trop. Med. Parasitol. 1996, 90, 659–661. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Tu, X.; Humphrey, C.; McClure, H.; Jiang, X.; Qin, C.; Glass, R.I.; Jiang, B. Detection of viral agents in fecal specimens of monkeys with diarrhea. J. Med. Primatol. 2007, 36, 101–107. [Google Scholar] [CrossRef] [PubMed]
- O’Ryan, M. Rotarix (RIX4414): An oral human rotavirus vaccine. Expert Rev. Vaccines 2007, 6, 11–19. [Google Scholar] [CrossRef] [PubMed]
- Matson, D.O. The pentavalent rotavirus vaccine, RotaTeq. Semin. Pediatr. Infect. Dis. 2006, 17, 195–199. [Google Scholar] [CrossRef] [PubMed]
- Sestak, K.; McNeal, M.M.; Choi, A.; Cole, M.J.; Ramesh, G.; Alvarez, X.; Aye, P.P.; Bohm, R.P.; Mohamadzadeh, M.; Ward, R.L. Defining T-cell-mediated immune responses in rotavirus-infected juvenile rhesus macaques. J. Virol. 2004, 78, 10258–10264. [Google Scholar] [CrossRef] [PubMed]
- Soike, K.F.; Gary, G.W.; Gibson, S. Susceptibility of non-human primate species to infection by simian rotavirus SA-11. Am. J. Vet. Res. 1980, 41, 1098–1103. [Google Scholar] [PubMed]
- Coots, A.; Donnelly, B.; Mohanty, S.K.; McNeal, M.; Sestak, K.; Tiao, G. Rotavirus infection of human cholangiocytes parallels the murine model of biliary atresia. J. Surg. Res. 2012, 177, 275–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walther, A.; Mohanty, S.K.; Donelly, B.; Coots, A.; Lages, C.S.; Lobeck, I.; Dupree, P.; Meller, J.; McNeal, M.; Sestak, K.; et al. Rhesus rotavirus VP4 sequence-specific activation of mononuclear cells is associated with cholangiopathy in murine biliary atresia. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 309, G466–G474. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohanty, S.K.; Donelly, B.; Lobeck, I.; Walther, A.; Dupree, P.; Coots, A.; Meller, J.; McNeal, M.; Sestak, K.; Tiao, G. The SRL peptide of rotavirus VP4 protein governs cholangiocyte infection and the murine model of biliary atresia. Hepatology 2017, 65, 1278–1292. [Google Scholar] [CrossRef] [PubMed]
- Lindesmith, L.C.; Ferris, M.T.; Mullan, C.W.; Ferreira, J.; Debbink, K.; Swanstrom, J.; Richardson, C.; Goodwin, R.R.; Baehner, F.; Mendelman, P.M.; et al. Broad blockade antibody responses in human volunteers after immunization with a multivalent norovirus VLP candidate vaccine: Immunological analyses from a phase I clinical trial. PLoS Med. 2015, 12, e1001807. [Google Scholar] [CrossRef] [PubMed]
- Karst, S.M.; Wobus, C.E. A working model of how noroviruses infect the intestine. PLoS Pathog. 2015, 11, e1004626. [Google Scholar] [CrossRef] [PubMed]
- Kolawole, A.O.; Rocha-Pereira, J.; Elftman, M.D.; Neyts, J.; Wobus, C.E. Inhibition of human norovirus by a viral polymerase inhibitor in the B cell culture system and in the mouse model. Antivir. Res. 2016, 132, 46–49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baldridge, M.T.; Lee, S.; Brown, J.J.; McAllister, N.; Urbanek, K.; Dermody, T.S.; Nice, T.J.; Virgin, H.W. Expression of IfnIr1 on intestinal epithelial cells is critical to the antiviral effects of interferon lambda against Norovirus and Reovirus. J. Virol. 2017, 91, e02079-16. [Google Scholar] [CrossRef] [PubMed]
- Atmar, R.L.; Ramani, S.; Estes, M.K. Human noroviruses: Recent advances in a 50-year history. Curr. Opin. Infect. Dis. 2018. [CrossRef] [PubMed]
- Rocha-Pereira, J.; Jacobs, S.; Noppen, S.; Verbeken, E.; Michiels, T.; Neyts, J. Interferon lambda (IFN-λ) efficiently blocks norovirus transmission in a mouse model. Antivir. Res. 2018, 149. [Google Scholar] [CrossRef] [PubMed]
- Thorne, L.; Lu, J.; Chaudhry, Y.; Bailey, D.; Goodfellow, I. Targetting macrophage- and intestinal epithelial cell-specific microRNAs against norovirus restricts replication in vivo. J. Gen. Virol. 2018. [Google Scholar] [CrossRef]
- Ettayebi, K.; Crawford, S.E.; Murakami, K.; Broughman, J.R.; Karandikar, U.; Tenge, V.R.; Neill, F.H.; Blutt, S.E.; Zeng, X.L.; Qu, L.; et al. Replication of human noroviruses in stem cell-derived human enteroids. Science 2016, 353, 1387–1393. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramani, S.; Crawford, S.E.; Blutt, S.E.; Estes, M.K. Human organoidcultures: Transformative new tools for human virus studies. Curr. Opin. Virol. 2018, 29, 79–86. [Google Scholar] [CrossRef] [PubMed]
- Smits, S.L.; Rahman, M.; Schapendonk, C.M.; van Leeuwen, M.; Faruque, A.S.; Haagmans, B.L.; Endtz, H.P.; Osterhaus, A.D. Calicivirus from novel Recovirus genogroup in human diarrhea, Bangladesh. Emerg. Infect. Dis. 2012, 18, 1192–1195. [Google Scholar] [CrossRef] [PubMed]
- Jones, M.K.; Watanabe, M.; Zhu, S.; Graves, C.L.; Keyes, L.R.; Grau, K.R.; Gonzalez-Hernandez, M.B.; Iovine, N.M.; Wobus, C.E.; Vinje, J.; et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 2014, 346, 755–759. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karst, S.M. Identification of a novel cellular target and a co-factor for norovirus infection—B cells & commensal bacteria. Gut Microbes 2015, 6, 266–271. [Google Scholar] [PubMed]
- Bok, K.; Parra, G.I.; Mitra, T.; Abente, E.; Shaver, C.K.; Boon, D.; Engle, R.; Yu, C.; Kapikian, A.Z.; Sosnovtsev, S.V.; et al. Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc. Natl. Acad. Sci. USA 2011, 108, 325–330. [Google Scholar] [CrossRef] [PubMed]
- Sestak, K.; Feely, S.; Fey, B.; Dufour, J.; Hargitt, E.; Alvarez, X. Pahar, rhesus macaques with primate enteric caliciviruses. PLoS ONE 2012, 7, e37973. [Google Scholar] [CrossRef] [PubMed]
- Mohan, M.; Chow, C.T.; Ryan, C.N.; Chan, L.S.; Dufour, J.; Aye, P.P.; Blanchard, J.; Moehs, C.P.; Sestak, K. Dietary gluten-induced gut dysbiosis is accompanied by selective upregulation of microRNAs with intestinal tight junction and bacteria-binding motifs in rhesus macaque model of celiac disease. Nutrients 2016, 8. [Google Scholar] [CrossRef] [PubMed]
- Farkas, T. Natural Norovirus infections in rhesus macaques. Emerg. Infect. Dis. 2016, 22, 1272–1274. [Google Scholar] [CrossRef] [PubMed]
- Adams, N.; Boice, R. A longitudinal-study of dominance in an outdoor colony of domestic rats. J. Comp. Psychol. 1983, 97, 24–33. [Google Scholar] [CrossRef]
- Sengupta, P. The laboratory rat: Relating its age with human’s. Int. J. Prev. Med. 2013, 4, 624–630. [Google Scholar] [PubMed]
- Mwenda, J.M.; Nyachieo, A.; Langat, D.K.; Steele, D.A. Serological detection of adenoviruses in non-human primates maintained in a colony in Kenya. East Afr. Med. J. 2005, 82, 371–375. [Google Scholar] [PubMed]
- Ng, T.F.; Zhang, W.; Sachsenroder, J.; Kondov, N.O.; da Costa, A.C.; Vega, E.; Holtz, L.R.; Wu, G.; Wang, D.; Stine, C.O.; et al. A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evol. 2015, 1, 17. [Google Scholar] [CrossRef] [PubMed]
- He, Z.; Liu, B.; Tao, Y.; Li, C.; Xia, M.; Zhong, W.; Jiang, X.; Liu, H.; Tan, M. Norovirus GII.17 natural infections in rhesus monkeys, China. Emerg. Infect. Dis. 2017, 23, 316–319. [Google Scholar] [CrossRef] [PubMed]
- Kapusinszky, B.; Ardeshir, A.; Mulvaney, U.; Deng, X.; Delwart, E. Case-control comparison of enteric viromes in captive rhesus macaques with acute or idiopathic chronic diarrhea. J. Virol. 2017, 91, e00952-17. [Google Scholar] [CrossRef] [PubMed]
- Brooks, J.; Watson, A.J. The enteric virome in inflammatory bowel disease. Gastroenterology 2015, 149, 1120–1121. [Google Scholar] [CrossRef] [PubMed]
- Handley, S.A.; Desai, C.; Zhao, G.; Droit, L.; Monaco, C.L.; Schroeder, A.C.; Nkolola, J.P.; Norman, M.E.; Miller, A.D.; Wang, D.; et al. SIV infection-mediated changes in gastrointestinal bacterial microbiome and virome are associated with immunodeficiency and prevented by vaccination. Cell Host Microbe 2016, 19, 323–335. [Google Scholar] [CrossRef] [PubMed]
- D’arc, M.; Furtado, C.; Siqueira, J.D.; Seuanez, H.N.; Ayouba, A.; Peeters, M.; Soares, M.A. Assessment of the gorilla gut virome in association with natural simian immunodeficiency virus infection. Retrovirology 2018, 15, 19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barbian, H.J.; Li, Y.; Ramirez, M.; Klase, Z.; Lipende, I.; Mjungu, D.; Moeller, A.H.; Wilson, M.L.; Pusey, A.E.; Lonsdorf, E.V.; et al. Destabilization of the gut microbiome marks the end-stage of simian immunodeficiency virus infection in wild chimpanzees. Am. J. Primatol. 2018, 80. [Google Scholar] [CrossRef] [PubMed]
© 2018 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Sestak, K. Non-Human Primate Models of Enteric Viral Infections. Viruses 2018, 10, 544. https://doi.org/10.3390/v10100544
Sestak K. Non-Human Primate Models of Enteric Viral Infections. Viruses. 2018; 10(10):544. https://doi.org/10.3390/v10100544
Chicago/Turabian StyleSestak, Karol. 2018. "Non-Human Primate Models of Enteric Viral Infections" Viruses 10, no. 10: 544. https://doi.org/10.3390/v10100544
APA StyleSestak, K. (2018). Non-Human Primate Models of Enteric Viral Infections. Viruses, 10(10), 544. https://doi.org/10.3390/v10100544