Phyloepidemiological analysis reveals that viral divergence led to the paucity of simian immunodeficiency virus SIVmus/gsn/ mon infections in wild populations

Journal of Virology

Volumn 91, Issue 6, 2017, Pages

  Schmidt, Fabian ^a   Liegeois, Florian ^b   Greenwood, Edward J D ^a   LeBreton, Matthew ^c   Lester, James ^a   Deleplancque, Luc ^d   Peeters, Martine ^b   Aghokeng, Avelin ^e   Tamoufe, Ubald ^f,g   Diffo, Joseph L D ^f,g   Takuo, Jean M ^f,g   Wolfe, Nathan D ^f,g   Leroy, Eric ^d   Rouet, François ^d   Heeney, Jonathan L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c Mosaic   (Cameroon)

^d CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

^e Institute of Medical Research and Medicinal Plant Studies Yaounde   (Cameroon)

^f METABIOTA INC   (United States)

^g Centre International de Recherches Médicales de Franceville ^*  (Cameroon)

Author keywords

Bushmeat; Cameroon; Gabon; Guenon; Lentivirus; Nonhuman primate; Simian immunodeficiency virus; SIV prevalence

Indexed keywords

ANIMAL CELL; ARTICLE; BLOOD SAMPLING; CERCOPITHECINAE; CLADISTICS; GEOGRAPHIC DISTRIBUTION; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION DISTRIBUTION; POPULATION RESEARCH; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS CELL INTERACTION; ANIMAL; CAMEROON; CLASSIFICATION; GABON; GENETIC VARIATION; GENETICS; HAPLORHINI; ISOLATION AND PURIFICATION; PHYLOGEOGRAPHY; PREVALENCE; TOPOGRAPHY; VIROLOGY;

ANIMALS; CAMEROON; GABON; GENETIC VARIATION; HAPLORHINI; PHYLOGEOGRAPHY; PREVALENCE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TOPOGRAPHY, MEDICAL;

EID: 85014094914     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01884-16     Document Type: Article

References (32)

1. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, Marx PA, Hahn BH, Sharp PM. 2003. Hybrid origin of SIV in chimpanzees. Science 300:1713. https://doi.org/10.1126/science.1080657.
2. Schindler M, Münch J, Kutsch O, Li H, Santiago ML, Bibollet-Ruche F, Müller-Trutwin MC, Novembre FJ, Peeters M, Courgnaud V, Bailes E, Roques P, Sodora DL, Silvestri G, Sharp PM, Hahn BH, Kirchhoff F. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125:1055-1067. https://doi.org/10.1016/j.cell.2006.04.033.
3. Barlow KL, Ajao AO, Clewley JP. 2003. Characterization of a novel simian immunodeficiency virus (SIVmonNG1) genome sequence from a mona monkey (Cercopithecus mona). J Virol 77:6879-6888. https://doi.org/10.1128/JVI.77.12.6879-6888.2003.
4. Courgnaud V, Abela B, Pourrut X, Mpoudi-Ngole E, Loul S, Delaporte E, Peeters M. 2003. Identification of a new simian immunodeficiency virus lineage with a vpu gene present among different Cercopithecus monkeys (C. mona, C. cephus, and C. nictitans) from Cameroon. J Virol 77: 12523-12534.
5. Aghokeng AF, Ayouba A, Mpoudi-Ngole E, Loul S, Liegeois F, Delaporte E, Peeters M. 2010. Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat provides insights into risks for potential new cross-species transmissions. Infect Genet Evol 10:386-396. https://doi.org/10.1016/j.meegid.2009.04.014.
6. Liegeois F, Boue V, Mouacha F, Butel C, Mve-Ondo B, Pourrut X, Leroy E, Peeters M, Rouet F. 2012. New STLV-3 strains and a divergent SIVmus strain identified in non-human primate bushmeat in Gabon. Retrovirology 9:28. https://doi.org/10.1186/1742-4690-9-28.
7. Ma D, Jasinska A, Kristoff J, Grobler JP, Turner T, Jung Y, Schmitt C, Raehtz K, Feyertag F, Martinez Sosa N, Wijewardana V, Burke DS, Robertson DL, Tracy R, Pandrea I, Freimer N, Apetrei C, International Vervet Research Consortium. 2013. SIVagm infection in wild African green monkeys from South Africa: epidemiology, natural history, and evolutionary considerations. PLoS Pathog 9:e1003011. https://doi.org/10.1371/journal.ppat.1003011.
8. Otsyula M, Yee J, Jennings M, Suleman M, Gettie A, Tarara R, Isahakia M, Marx P, Lerche N. 1996. Prevalence of antibodies against simian immunodeficiency virus (SIV) and simian T-lymphotropic virus (STLV) in a colony of non-human primates in Kenya, East Africa. Ann Trop Med Parasitol 90:65-70. https://doi.org/10.1080/00034983.1996.11813027.
9. Souquière S, Bibollet-Ruche F, Robertson DL, Makuwa M, Apetrei C, Onanga R, Kornfeld C, Plantier J-C, Gao F, Abernethy K, White LJT, Karesh W, Telfer P, Wickings EJ, Mauclere P, Marx PA, Barre-Sinoussi F, Hahn BH, Müller-Trutwin MC, Simon F. 2001. Wild Mandrillus sphinx are carriers of two types of lentivirus. J Virol 75:7086-7096. https://doi.org/10.1128/JVI.75.15.7086-7096.2001.
10. Aghokeng AF, Liu W, Bibollet-Ruche F, Loul S, Mpoudi-Ngole E, Laurent C, Mwenda JM, Langat DK, Chege GK, McClure HM, Delaporte E, Shaw GM, Hahn BH, Peeters M. 2006. Widely varying SIV prevalence rates in naturally infected primate species from Cameroon. Virology 345: 174-189. https://doi.org/10.1016/j.virol.2005.09.046.
11. Ndembi N, Kaptué L, Ido E. 2009. Exposure to SIVmnd-2 in southern Cameroon: public health implications. AIDS Rev 11:135-139.
12. Lauck M, Switzer WM, Sibley SD, Hyeroba D, Tumukunde A, Weny G, Taylor B, Shankar A, Ting N, Chapman CA, Friedrich TC, Goldberg TL, O'Connor DH. 2013. Discovery and full genome characterization of two highly divergent simian immunodeficiency viruses infecting black-andwhite colobus monkeys (Colobus guereza) in Kibale National Park, Uganda. Retrovirology 10:1. https://doi.org/10.1186/1742-4690-10-1.
13. Courgnaud V, Pourrut X, Bibollet-Ruche F, Mpoudi-Ngole E, Bourgeois A, Delaporte E, Peeters M. 2001. Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family. J Virol 75:857-866. https://doi.org/10.1128/JVI.75.2.857-866.2001.
14. Ahuka-Mundeke S, Ayouba A, Mbala-Kingebeni P, Liegeois F, Esteban A, Lunguya-Metila O, Demba D, Bilulu G, Mbenzo-Abokome V, Inogwabini B-I, Muyembe-Tamfum J-J, Delaporte E, Peeters M. 2011. Novel multiplexed HIV/simian immunodeficiency virus antibody detection assay. Emerg Infect Dis 17:2277-2286. https://doi.org/10.3201/eid1712.110783.
15. Keele BF, van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, Bibollet-Ruche F, Chen Y, Wain LV, Liegeois F, Loul S, Ngole EM, Bienvenue Y, Delaporte E, Brookfield JFY, Sharp PM, Shaw GM, Peeters M, Hahn BH. 2006. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523-526. https://doi.org/10.1126/science.1126531.
16. Santiago ML, Rodenburg CM, Kamenya S, Bibollet-Ruche F, Gao F, Bailes E, Meleth S, Soong S-J, Kilby JM, Moldoveanu Z, Fahey B, Muller MN, Ayouba A, Nerrienet E, McClure HM, Heeney JL, Pusey AE, Collins DA, Boesch C, Wrangham RW, Goodall J, Sharp PM, Shaw GM, Hahn BH. 2002. SIVcpz in wild chimpanzees. Science 295:465. https://doi.org/10.1126/science.295.5554.465.
17. Li Y, Ndjango J-B, Learn GH, Ramirez MA, Keele BF, Bibollet-Ruche F, Liu W, Easlick JL, Decker JM, Rudicell RS, Inogwabini B-I, Ahuka-Mundeke S, Leendertz FH, Reynolds V, Muller MN, Chancellor RL, Rundus AS, Simmons N, Worobey M, Shaw GM, Peeters M, Sharp PM, Hahn BH. 2012. Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J Virol 86:10776-10791. https://doi.org/10.1128/JVI.01498-12.
18. Santiago ML, Lukasik M, Kamenya S, Li Y, Bibollet-Ruche F, Bailes E, Muller MN, Emery M, Goldenberg DA, Lwanga JS, Ayouba A, Nerrienet E, McClure HM, Heeney JL, Watts DP, Pusey AE, Collins DA, Wrangham RW, Goodall J, Brookfield JFY, Sharp PM, Shaw GM, Hahn BH. 2003. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J Virol 77:7545-7562. https://doi.org/10.1128/JVI.77.13.7545-7562.2003.
19. Boue V, Locatelli S, Boucher F, Ayouba A, Butel C, Esteban A, Okouga A-P, Ndoungouet A, Motsch P, Le Flohic G, Ngari P, Prugnolle F, Ollomo B, Rouet F, Liegeois F. 2015. High rate of simian immunodeficiency virus (SIV) infections in wild chimpanzees in northeastern Gabon. Viruses 7:4997-5015. https://doi.org/10.3390/v7092855.
20. Rudicell RS, Holland Jones J, Wroblewski EE, Learn GH, Li Y, Robertson JD, Greengrass E, Grossmann F, Kamenya S, Pintea L, Mjungu DC, Lonsdorf EV, Mosser A, Lehman C, Collins DA, Keele BF, Goodall J, Hahn BH, Pusey AE, Wilson ML. 2010. Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog 6:e1001116. https://doi.org/10.1371/journal.ppat.1001116.
21. Liegeois F, Schmidt F, Boue V, Butel C, Mouacha F, Ngari P, Ondo BM, Leroy E, Heeney JL, Delaporte E, Peeters M, Rouet F. 2014. Full-length genome analyses of two new simian immunodeficiency virus (SIV) strains from mustached monkeys (C. cephus) in Gabon illustrate a complex evolutionary history among the SIVmus/mon/gsn lineage. Viruses 6:2880-2898. https://doi.org/10.3390/v6072880.
22. Aghokeng AF, Bailes E, Loul S, Courgnaud V, Mpoudi-Ngolle E, Sharp PM, Delaporte E, Peeters M. 2007. Full-length sequence analysis of SIVmus in wild populations of mustached monkeys (Cercopithecus cephus) from Cameroon provides evidence for two co-circulating SIVmus lineages. Virology 360:407-418. https://doi.org/10.1016/j.virol.2006.10.048.
23. Worobey M, Telfer P, Souquière S, Hunter M, Coleman CA, Metzger MJ, Reed P, Makuwa M, Hearn G, Honarvar S, Roques P, Apetrei C, Kazanji M, Marx PA. 2010. Island biogeography reveals the deep history of SIV. Science 329:1487. https://doi.org/10.1126/science.1193550.
24. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86:6196-6200. https://doi.org/10.1073/pnas.86.16.6196.
25. van der Kuyl AC, Dekker JT, Goudsmit J. 2000. Primate genus Miopithecus: evidence for the existence of species and subspecies of dwarf guenons based on cellular and endogenous viral sequences. Mol Phylogenet Evol 14:403-413. https://doi.org/10.1006/mpev.1999.0721.
26. Lebreton M, Switzer WM, Djoko CF, Gillis A, Jia H, Sturgeon MM, Shankar A, Zheng H, Nkeunen G, Tamoufe U, Nana A, Le Doux-Diffo J, Tafon B, Kiyang J, Schneider BS, Burke DS, Wolfe ND. 2014. A gorilla reservoir for human T-lymphotropic virus type 4. Emerg Microbes Infect 3:e7. https://doi.org/10.1038/emi.2014.7.
27. Sintasath DM, Wolfe ND, Lebreton M, Jia H, Garcia AD, Le Doux-Diffo J, Tamoufe U, Carr JK, Folks TM, Mpoudi-Ngole E, Burke DS, Heneine W, Switzer WM. 2009. Simian T-lymphotropic virus diversity among nonhu-man primates, Cameroon. Emerg Infect Dis 15:175-184. https://doi.org/10.3201/eid1502.080584.
28. Simon F, Souquière S, Damond F, Kfutwah A, Makuwa M, Leroy E, Rouquet P, Berthier JL, Rigoulet J, Lecu A, Telfer PT, Pandrea I, Plantier JC, Barré-Sinoussi F, Roques P, Müller-Trutwin MC, Apetrei C. 2001. Synthetic peptide strategy for the detection of and discrimination among highly divergent primate lentiviruses. AIDS Res Hum Retroviruses 17:937-952. https://doi.org/10.1089/088922201750290050.
29. Kahle D, Wickham H. 2013. ggmap: spatial visualization with ggplot2. R J 5:144-161.
30. Ellis BR, Munene E, Elliott D, Robinson J, Otsyula MG, Michael SF. 2004. Seroprevalence of simian immunodeficiency virus in wild and captive born Sykes' monkeys (Cercopithecus mitis) in Kenya. Retrovirology 1:34. https://doi.org/10.1186/1742-4690-1-34.
31. Arnold C, Matthews LJ, Nunn CL. 2010. The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol Issues News Rev 19:114-118. https://doi.org/10.1002/evan.20251.
32. Jovani R, Tella JL. 2006. Parasite prevalence and sample size: misconceptions and solutions. Trends Parasitol 22:214-218. https://doi.org/10.1016/j.pt.2006.02.011.