High rate of simian immunodeficiency virus (SIV) infections in wild chimpanzees in northeastern Gabon

Viruses

Volumn 7, Issue 9, 2015, Pages 4997-5015

  Boué, Vanina ^a,b   Locatelli, Sabrina ^a   Boucher, Floriane ^a,b   Ayouba, Ahidjo ^a   Butel, Christelle ^a   Esteban, Amandine ^a   Okouga, Alain Prince ^b   Ndoungouet, Alphonse ^b   Motsch, Peggy ^b   Le Flohic, Guillaume ^b   Ngari, Paul ^b   Prugnolle, Franck ^b,c   Ollomo, Benjamin ^b   Rouet, François ^b,d   Liégeois, Florian ^a,b,c  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

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

^c CNRS   (France)

^d INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

Author keywords

Africa; AIDS; Antibody; Chimpanzee; Microsatellite; Prevalence; Primate; Retrovirus; SIV; Transmission

Indexed keywords

ARTICLE; CHIMPANZEE; CONTROLLED STUDY; ENVELOPE GENE; FECES ANALYSIS; GENE AMPLIFICATION; GEOGRAPHIC DISTRIBUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEROLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; STRUCTURAL GENE; VIRUS DETECTION; VIRUS PREVALENCE; VIRUS TRANSMISSION; ANIMAL; BLOOD; DISEASE TRANSMISSION; DNA SEQUENCE; FECES; GABON; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR EPIDEMIOLOGY; MOLECULAR GENETICS; PAN TROGLODYTES; PREVALENCE; TRANSMISSION; VIROLOGY;

MICROSATELLITE DNA; POL PROTEIN; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ANIMALS; ANTIBODIES, VIRAL; DISEASE TRANSMISSION, INFECTIOUS; FECES; GABON; GENE PRODUCTS, ENV; GENE PRODUCTS, POL; MICROSATELLITE REPEATS; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; PAN TROGLODYTES; PREVALENCE; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84941631087     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7092855     Document Type: Article

References (56)

1. Keele, B.F.; Van Heuverswyn, F.; Li, Y.; Bailes, E.; Takehisa, J.; Santiago, M.L.; Bibollet-Ruche, F.; Chen, Y.; Wain, L.V.; Liegeois, F.; et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 2006, 313, 523–526.
2. Van Heuverswyn, F.; Li, Y.; Neel, C.; Bailes, E.; Keele, B.F.; Liu, W.; Loul, S.; Butel, C.; Liegeois, F.; Bienvenue, Y.; et al. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 2006, 444, 164–164.
3. D’Arc, M.; Ayouba, A.; Esteban, A.; Learn, G.H.; Boue, V.; Liegeois, F.; Etienne, L.; Tagg, N.; Leendertz, F.H.; Boesch, C.; et al. Origin of the HIV-1 group O epidemic in western lowland gorillas. Proc. Natl. Acad. Sci. USA 2015, 112, E1343–E1352.
4. Etienne, L.; Locatelli, S.; Ayouba, A.; Esteban, A.; Butel, C.; Liegeois, F.; Aghokeng, A.; Delaporte, E.; Mpoudi Ngole, E.; Peeters, M. Noninvasive follow-up of Simian Immunodeficiency Virus infection in wild-living nonhabituated western lowland gorillas in Cameroon. J. Virol. 2012, 86, 9760–9772.
5. Van Heuverswyn, F.; Li, Y.; Bailes, E.; Neel, C.; Lafay, B.; Keele, B.F.; Shaw, K.S.; Takehisa, J.; Kraus, M.H.; Loul, S.; et al. Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 2007, 368, 155–171.
6. Rudicell, R.S.; Piel, A.K.; Stewart, F.; Moore, D.L.; Learn, G.H.; Li, Y.; Takehisa, J.; Pintea, L.; Shaw, G.M.; Moore, J.; et al. High prevalence of Simian Immunodeficiency Virus infection in a community of savanna chimpanzees. J. Virol. 2011, 85, 9918–9928.
7. Neel, C.; Etienne, L.; Li, Y.; Takehisa, J.; Rudicell, R.S.; Bass, I.N.; Moudindo, J.; Mebenga, A.; Esteban, A.; Van Heuverswyn, F.; et al. Molecular epidemiology of Simian Immunodeficiency Virus infection in wild-living gorillas. J. Virol. 2010, 84, 1464–1476.
8. Rudicell, R.S.; Holland Jones, J.; Wroblewski, E.E.; Learn, G.H.; Li, Y.; Robertson, J.D.; Greengrass, E.; Grossmann, F.; Kamenya, S.; Pintea, L.; et al. Impact of Simian Immunodeficiency Virus infection on chimpanzee population dynamics. PLoS Pathog. 2010, 6, e1001116.
9. Locatelli, S.; McKean, K.A.; Sesink Clee, P.R.; Gonder, M.K. The evolution of resistance to Simian Immunodeficiency Virus (SIV): A review. Int. J. Primatol. 2014, 35, 349–375.
10. Locatelli, S.; Peeters, M. Cross-species transmission of Simian Retroviruses: How and why they could lead to the emergence of new diseases in the human population. AIDS 2012, 26, 659–673.
11. Pandrea, I.; Apetrei, C. Where the wild things are: Pathogenesis of SIV infection in African nonhuman primate hosts. Curr. HIV/AIDS Rep. 2010, 7, 28–36.
12. Keele, B.F.; Jones, J.H.; Terio, K.A.; Estes, J.D.; Rudicell, R.S.; Wilson, M.L.; Li, Y.; Learn, G.H.; Beasley, T.M.; Schumacher-Stankey, J.; et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 2009, 460, 515–519.
13. Etienne, L.; Nerrienet, E.; LeBreton, M.; Bibila, G.T.; Foupouapouognigni, Y.; Rousset, D.; Nana, A.; Djoko, C.F.; Tamoufe, U.; Aghokeng, A.F.; et al. Characterization of a new Simian Immunodeficiency Virus strain in a naturally infected Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology 2011, 8.
14. Schmidt, F.; Greenwood, E.J.D.; Nagel, M.; Herbert, A.; Liégeois, F.; Mouinga-Ondémé, A.; Peeters, M.; Sica, J.; Oloussou, D.; Heeney, J.L.; et al. ARV treatment of a naturally SIVcpz infected and disease progressing Pan troglodytes troglodytes Chimpanzee shows clinical and immunovirological efficiency. In 38th Annual Meeting on Retroviruses, Cold Spring Harbor Laboratory, NY, USA, 20-25 May 2013.
15. Joint United Nations Programme on HIV/AIDS (UNAIDS). Unaids report on the global aids epidemic 2013, 2013.
16. Simon, F.; Mauclere, P.; Roques, P.; Loussert-Ajaka, I.; Muller-Trutwin, M.C.; Saragosti, S.; Georges-Courbot, M.C.; Barre-Sinoussi, F.; Brun-Vezinet, F. Identification of a new Human Immunodeficiency Virus type 1 distinct from group M and group O. Nat. Med. 1998, 4, 1032–1037.
17. Plantier, J.C.; Leoz, M.; Dickerson, J.E.; De Oliveira, F.; Cordonnier, F.; Lemee, V.; Damond, F.; Robertson, D.L.; Simon, F. A new Human Immunodeficiency Virus derived from gorillas. Nat. Med. 2009, 15, 871–872.
18. Liegeois, F.; Boue, V.; Butel, C.; Mouinga-Ondeme, A.; Sica, J.; Zamba, C.; Peeters, M.; Delaporte, E.; Rouet, F. HIV type-1 group O infection in gabon: Low prevalence rate but circulation of genetically diverse and drug-resistant HIV type-1 group O strains. AIDS Res. Hum. Retroviruses 2013, 29, 1085–1090.
19. Vessiere, A.; Rousset, D.; Kfutwah, A.; Leoz, M.; Depatureaux, A.; Simon, F.; Plantier, J.C. Diagnosis and monitoring of HIV-1 group O-infected patients in cameroun. J. Acquir. Immune Defic. Syndr. 2010, 53, 107–110.
20. Hemelaar, J. The origin and diversity of the HIV-1 pandemic. Trends Mol. Med. 2012, 18, 182–192.
21. Groves, C. Smithsonian series in comparative evolutionary biology. In Primate taxonomy; Smithsonian Institution Press: Washington D.C., WA, USA, 2001.
22. Sharp, P.M.; Shaw, G.M.; Hahn, B.H. Simian Immunodeficiency Virus infection of chimpanzees. J. Virol. 2005, 79, 3891–3902.
23. Leendertz, S.A.; Locatelli, S.; Boesch, C.; Kucherer, C.; Formenty, P.; Liegeois, F.; Ayouba, A.; Peeters, M.; Leendertz, F.H. No evidence for transmission of SIVwrc from western red colobus monkeys (Piliocolobus badius badius) to wild west african chimpanzees (Pan troglodytes verus) despite high exposure through hunting. BMC Microbiol. 2011, 11.
24. Prince, A.M.; Brotman, B.; Lee, D.H.; Andrus, L.; Valinsky, J.; Marx, P. Lack of evidence for HIV type 1-related SIVcpz infection in captive and wild chimpanzees (Pan troglodytes verus) in West Africa. AIDS Res. Hum. Retroviruses 2002, 18, 657–660.
25. Oates, J.F.; Groves, C.P.; Jenkins, P.D. The type locality of Pan troglodytes vellerosus (gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates 2009, 50, 78–80.
26. Li, Y.; Ndjango, J.B.; Learn, G.H.; Ramirez, M.A.; Keele, B.F.; Bibollet-Ruche, F.; Liu, W.; Easlick, J.L.; Decker, J.M.; Rudicell, R.S.; et al. Eastern Chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J. Virol. 2012, 86, 10776–10791.
27. Peeters, M.; Honore, C.; Huet, T.; Bedjabaga, L.; Ossari, S.; Bussi, P.; Cooper, R.W.; Delaporte, E. Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS 1989, 3, 625–630.
28. Huet, T.; Cheynier, R.; Meyerhans, A.; Roelants, G.; Wain-Hobson, S. Genetic organization of a chimpanzee lentivirus related to HIV. Nature 1990, 345, 356–359.
29. Souquiere, S.; Makuwa, M.; Salle, B.; Kazanji, M. New strain of Simian Immunodeficiency Virus identified in wild-born chimpanzees from Central Africa. PLoS ONE 2012, 7, e44298.
30. Liegeois, F.; Boue, V.; Mouacha, F.; Butel, C.; Ondo, B.M.; Pourrut, X.; Leroy, E.; Peeters, M.; Rouet, F. New STLV-3 strains and a divergent SIVmus strain identified in non-human primate bushmeat in Gabon. Retrovirology 2012, 9, 28.
31. Liegeois, F.; Schmidt, F.; Boue, V.; Butel, C.; Mouacha, F.; Ngari, P.; Ondo, B.M.; Leroy, E.; Heeney, J.L.; Delaporte, E.; et al. 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 2014, 6, 2880–2898.
32. Fouchet, D.; Verrier, D.; Ngoubangoye, B.; Souquiere, S.; Makuwa, M.; Kazanji, M.; Gonzalez, J.P.; Pontier, D. Natural Simian Immunodeficiency Virus transmission in mandrills: A family affair? Proc. Biol. Sci. 2012, 279, 3426–3435.
33. Souquiere, S.; Bibollet-Ruche, F.; Robertson, D.L.; Makuwa, M.; Apetrei, C.; Onanga, R.; Kornfeld, C.; Plantier, J.C.; Gao, F.; Abernethy, K.; et al. Wild Mandrillus sphinx are carriers of two types of lentivirus. J. Virol. 2001, 75, 7086–7096.
34. Peeters, M.; Courgnaud, V.; Abela, B.; Auzel, P.; Pourrut, X.; Bibollet-Ruche, F.; Loul, S.; Liegeois, F.; Butel, C.; Koulagna, D.; et al. Risk to human health from a plethora of Simian Immunodeficiency Viruses in primate bushmeat. Emerg. Infect. Dis. 2002, 8, 451–457.
35. Boom, R.; Sol, C.J.; Salimans, M.M.; Jansen, C.L.; Wertheim-van Dillen, P.M.; van der Noordaa, J. Rapid and simple method for purification of nucleic acids. J. Clin. Microbiol. 1990, 28, 495–503.
36. Van der Kuyl, A.C.; Dekker, J.T.; Goudsmit, J. Primate genus Miopithecus: Evidence for the existence of species and subspecies of dwarf guenons based on cellular and endogenous viral sequences. Mol. Phylogenet. Evol. 2000, 14, 403–413.
37. Kocher, T.D.; Thomas, W.K.; Meyer, A.; Edwards, S.V.; Paabo, S.; Villablanca, F.X.; Wilson, A.C. Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 1989, 86, 6196–6200.
38. National Librairy of Medicine Basic local alignment search tools. Available online: http://blast.ncbi.nlm.nih. gov/Blast.cgi (accessed on 15 November 2014).
39. Sullivan, K.M.; Mannucci, A.; Kimpton, C.P.; Gill, P. A rapid and quantitative DNA sex test: Fluorescence-based PCR analysis of X-Y homologous gene amelogenin. Biotechniques 1993, 15, 636–638.
40. Bonin, A.; Bellemain, E.; Bronken Eidesen, P.; Pompanon, F.; Brochmann, C.; Taberlet, P. How to track and assess genotyping errors in population genetics studies. Mol. Ecol. 2004, 13, 3261–3273.
41. Kalinowski, S.T.; Taper, M.L.; Marshall, T.C. Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 2007, 16, 1099–1106.
42. Vigilant, L.; Guschanski, K. Using genetics to understand the dynamics of wild primate populations. Primates 2009, 50, 105–120.
43. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. Mega5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731–2739.
44. Guindon, S.; Dufayard, J.F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of phyml 3.0. Syst. Biol. 2010, 59, 307–321.
45. Milne, I.; Lindner, D.; Bayer, M.; Husmeier, D.; McGuire, G.; Marshall, D.F.; Wright, F. Topali v2: A rich graphical interface for evolutionary analyses of multiple alignments on hpc clusters and multi-core desktops. Bioinformatics 2009, 25, 126–127.
46. Mitchell, M.W.; Locatelli, S.; Sesink Clee, P.R.; Thomassen, H.A.; Gonder, M.K. Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot. BMC Evol. Biol. 2015, 15.
47. Telfer, P.T.; Souquiere, S.; Clifford, S.L.; Abernethy, K.A.; Bruford, M.W.; Disotell, T.R.; Sterner, K.N.; Roques, P.; Marx, P.A.; Wickings, E.J. Molecular evidence for deep phylogenetic divergence in Mandrillus sphinx. Mol. Ecol. 2003, 12, 2019–2024.
48. Anthony, N.M.; Johnson-Bawe, M.; Jeffery, K.; Clifford, S.L.; Abernethy, K.A.; Tutin, C.E.; Lahm, S.A.; White, L.J.; Utley, J.F.; Wickings, E.J.; et al. The role of pleistocene refugia and rivers in shaping gorilla genetic diversity in Central Africa. Proc. Natl. Acad. Sci. USA 2007, 104, 20432–20436.
49. Locatelli, S.; Liegeois, F.; Lafay, B.; Roeder, A.D.; Bruford, M.W.; Formenty, P.; Noe, R.; Delaporte, E.; Peeters, M. Prevalence and genetic diversity of Simian Immunodeficiency Virus infection in wild-living red colobus monkeys (Piliocolobus badius badius) from the Taï forest, Côte d’Ivoire: SIVwrc in wild-living western red colobus monkeys. Infect. Genet. Evol. 2008, 8, 1–14.
50. Tutin, C.; Fernandez, M. Nationwide census of gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes troglodytes) populations in Gabon. Am. J. Primatol. 1984, 6, 313–336.
51. IUCN. Red list of threatened species. Available online: http://www.iucnredlist.org (accessed on 30 March 2015).
52. Bibollet-Ruche, F.; Gao, F.; Bailes, E.; Saragosti, S.; Delaporte, E.; Peeters, M.; Shaw, G.M.; Hahn, B.H.; Sharp, P.M. Complete genome analysis of one of the earliest SIVcpzPtt strains from Gabon (SIVcpzGab-2). AIDS Res. Hum. Retroviruses 2004, 20, 1377–1381.
53. Bermejo, M.; Rodriguez-Teijeiro, J.D.; Illera, G.; Barroso, A.; Vila, C.; Walsh, P.D. Ebola outbreak killed 5000 gorillas. Science 2006, 314, 1564.
54. Walsh, P.D.; Abernethy, K.A.; Bermejo, M.; Beyers, R.; De Wachter, P.; Akou, M.E.; Huijbregts, B.; Mambounga, D.I.; Toham, A.K.; Kilbourn, A.M.; et al. Catastrophic ape decline in Western Equatorial Africa. Nature 2003, 422, 611–614.
55. Leroy, E.M.; Rouquet, P.; Formenty, P.; Souquiere, S.; Kilbourne, A.; Froment, J.M.; Bermejo, M.; Smit, S.; Karesh, W.; Swanepoel, R.; et al. Multiple ebola virus transmission events and rapid decline of Central African wildlife. Science 2004, 303, 387–390.
56. Fa, J.E.; Ryan, S.F.; Bell, D.J. Hunting vulnerability, ecological charasteristics and harvest rates of buschmeat species in afrotropical forest. Biol. Conserv. 2005, 121, 167–176.