Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir

Journal of Virology

Volumn 86, Issue 19, 2012, Pages 10776-10791

  Li, Yingying ^a   Ndjango, Jean Bosco ^b   Learn, Gerald H ^a   Ramirez, Miguel A ^a   Keele, Brandon F ^c   Bibollet Ruche, Frederic ^a   Liu, Weimin ^a   Easlick, Juliet L ^d   Decker, Julie M ^d   Rudicell, Rebecca S ^d,r   Inogwabini, Bila Isia ^e,f   Ahuka Mundeke, Steve ^g,h   Leendertz, Fabian H ⁱ   Reynolds, Vernon ^j,k   Muller, Martin N ^l   Chancellor, Rebecca L ^m,n   Rundus, Aaron S ^m,n   Simmons, Nicole ^o   Worobey, Michael ^p   Shaw, George M ^a   Peeters, Martine ^h   Sharp, Paul M ^q   Hahna, Beatrice H ^a   more..

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF KISANGANI   (Congo)

^c SAIC FREDERICK INC   (United States)

^d University of Alabama at Birmingham   (United States)

^e Lac Tumba Project   (Congo)

^f SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^g Institut National de Recherche Biomedicale   (Congo)

^h INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

ⁱ ROBERT KOCH INSTITUTE   (Germany)

^j UNIVERSITY OF OXFORD   (United Kingdom)

^k BUDONGO CONSERVATION FIELD STATION   (Uganda)

^l UNIVERSITY OF NEW MEXICO   (United States)

^m WEST CHESTER UNIVERSITY   (United States)

ⁿ Great Ape Trust   (Rwanda)

^o MAKERERE UNIVERSITY   (Uganda)

^p The University of Arizona   (United States)

^q UNIVERSITY OF EDINBURGH   (United Kingdom)

^r NATIONAL INSTITUTES OF HEALTH   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ANTIBODY DETECTION; ARTICLE; CHIMPANZEE; CONTROLLED STUDY; GENE AMPLIFICATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HABITUATION; HAPLOTYPE; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; PAN PANISCUS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; RESERVOIR; SEQUENCE ALIGNMENT; SEX DETERMINATION; SIMIAN IMMUNODEFICIENCY VIRUS; UNINDEXED SEQUENCE; VIRUS INFECTIVITY;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; CD4-POSITIVE T-LYMPHOCYTES; DEMOCRATIC REPUBLIC OF THE CONGO; FEMALE; GENETIC VARIATION; GENOME; GEOGRAPHY; HUMANS; LIKELIHOOD FUNCTIONS; MALE; MOLECULAR SEQUENCE DATA; PAN PANISCUS; PAN TROGLODYTES; PHYLOGENY; RWANDA; SEQUENCE HOMOLOGY, AMINO ACID; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; UGANDA; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1; PAN; PAN PANISCUS; PAN TROGLODYTES SCHWEINFURTHII; PAN TROGLODYTES TROGLODYTES; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84869015088     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01498-12     Document Type: Article

References (87)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104-2105.
2. Ahuka-Mundeke S, et al. 2011. Novel multiplexed HIV/simian immunodeficiency virus antibody detection assay. Emerg. Infect. Dis. 17:2277-2286.
3. Bailes E, et al. 2003. Hybrid origin of SIV in chimpanzees. Science 300: 1713.
4. Balazs AB, et al. 2012. Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature. 481:81-84.
5. Bennett EL, et al. 2007. Hunting for consensus: reconciling bushmeat harvest, conservation, and development policy in West and Central Africa. Conserv. Biol. 21:884-887.
6. Betsem E, Rua R, Tortevoye P, Froment A, Gessain A. 2011. Frequent and recent human acquisition of simian foamy viruses through apes' bites in central Africa. PLoS Pathog. 7:e1002306. doi:10.1371/journal.ppat.1002306.
7. Bibollet-Ruche F, et al. 2012. Efficient SIVcpz replication in human lymphoid tissue requires viral matrix protein adaptation. J. Clin. Invest. 122:1644-1652.
8. Bonifacino JS, Traub LM. 2003. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72:395-447.
9. Bowden R, et al. 2012. Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population. PLoS Genet. 8:e1002504. doi:10.1371/journal.pgen.1002504.
10. Butynski TM. 2001. Africa's great apes, p 3-56. In Beck B, et al (ed), Great apes and humans-the ethics of coexistence. Smithsonian Institution Press, Washington, DC.
11. Calvignac-Spencer S, Leendertz SAJ, Gillespie TR, Leendertz FH. 2012. Wild great apes as sentinels and sources of infectious disease. Clin. Microbiol. Infect. 18:521-527.
12. Chancellor RL, Langergraber K, Ramirez S, Rundus AS, Vigilant L. 2012. Genetic sampling of unhabituated chimpanzees (Pan troglodytes schweinfurthii) in Gishwati forest reserve, an isolated forest fragment in
13. Chen BK, Gandhi RT, Baltimore D. 1996. CD4 down-modulation during infection of human T cells with human immunodeficiency virus type 1 involves independent activities of vpu, env, and nef. J. Virol. 70:6044-6053.
14. Decker JM, et al. 2009. Effective activation alleviates the replication block of CCR5-tropic HIV-1 in chimpanzee CD4+lymphocytes. Virology 394: 109-118.
15. Dube M, et al. 2010. Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog. 6:e1000856. doi:10.1371/ journal.ppat.1000856.
16. Eng B, Ainsworth P, Waye JS. 1994. Anomalous migration of PCR products using nondenaturing polyacrylamide gel electrophoresis: the amelogenin sex-typing system. J. Forensic Sci. 39:1356-1359.
17. Etienne L, et al. 2011. Characterization of a new simian immunodeficiency virus strain in a naturally infected Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology 8:4.
18. Evans DT, Serra-Moreno R, Singh RK, Guatelli JC. 2010. BST-2/ tetherin: a new component of the innate immune response to enveloped viruses. Trends Microbiol. 18:388-396.
19. Fruth B, et al. 2008. Pan paniscus. The IUCN Red List of Threatened Species, IUCN, Cambridge, United Kingdom. http://www.iucnredlist.org /details/15932/0.
20. Gao F, et al. 1999. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436-441.
21. Gough NR, et al. 1999. Utilization of the indirect lysosome targeting pathway by lysosome-associated membrane proteins (LAMPs) is influenced largely by the C-terminal residue of their GYXXφ targeting signals. J. Cell Sci. 112(Part 23):4257-4269.
22. Guindon S, et al. 2010. New algorithms and methods to estimate maximum- likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321.
23. Gupta RK, Towers GJ. 2009. A tail of tetherin: how pandemic HIV-1 conquered the world. Cell Host Microbe 6:393-395.
24. Hahn BH, Shaw GM, De Cock KM, Sharp PM. 2000. AIDS as a zoonosis: scientific and public health implications. Science 287:607-614.
25. Hicks TC. 2010. A chimpanzee mega-culture? Exploring behavioral continuity in Pan troglodytes schweinfurthii across northern DR Congo. Ph.D. thesis. University of Amsterdam, Amsterdam, The Netherlands.
26. Hicks TC, et al. 2010. Trade in orphans and bushmeat threatens one of the Democratic Republic of the Congo's most important populations of eastern chimpanzees (Pan troglodytes schweinfurthii). Afr. Primates 7:1-18.
27. Johnson PR, et al. 2009. Vector-mediated gene transfer engenders longlived neutralizing activity and protection against SIV infection in monkeys. Nat. Med. 15:901-906.
28. Kanemori Y, Uto K, Sagata N. 2005. Beta-TrCP recognizes a previously undescribed nonphosphorylated destruction motif in Cdc25A and Cdc25B phosphatases. Proc. Natl. Acad. Sci. U. S. A. 102:6279-6284.
29. Keele BF, et al. 2009. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460:515-519.
30. Keele BF, et al. 2006. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523-526.
31. Kobayashi T, et al. 2011. Identification of amino acids in the human tetherin transmembrane domain responsible for HIV-1 Vpu interaction and susceptibility. J. Virol. 85:932-945.
32. Krüger O, Affeldt E, Brackmann M, Milhahn K. 1998. Group size and composition of Colobus guereza in Kyambura Gorge, southwest Uganda, in relation to chimpanzee activity. Int. J. Primatol. 19:287-297.
33. Kueck T, Neil SJ. 2012. A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PLoS Pathog. 8:e1002609. doi:10.1371/ journal.ppat.1002609.
34. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
35. Leendertz SA, et al. 2011. 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. 11:24.
36. Liegeois F, et al. 2012. Identification of new divergent SIVcpzPtt strains in wild living chimpanzees in Gabon, poster 528. The Conference on Retroviruses and Opportunistic Infections, Seattle, WA. http://www .retroconference.org/2012b/PDFs/528.pdf.
37. Lim ES, Malik HS, Emerman M. 2010. Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J. Virol. 84:7124-7134.
38. Ling B, et al. 2003. Noninvasive detection of new simian immunodeficiency virus lineages in captive sooty mangabeys: ability to amplify virion RNA from fecal samples correlates with viral load in plasma. J. Virol. 77:2214-2226.
39. Liu W, et al. 2008. Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. PLoS Pathog. 4:e1000097. doi: 10.1371/journal.ppat.1000097.
40. Margottin F, et al. 1998. A novel human WD protein, h-βTrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1:565-574.
41. Moll M, Andersson SK, Smed-Sorensen A, Sandberg JK. 2010. Inhibition of lipid antigen presentation in dendritic cells by HIV-1 Vpu interference with CD1d recycling from endosomal compartments. Blood 116: 1876-1884.
42. Neel C, et al. 2010. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J. Virol. 84:1464-1476.
43. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
44. Peeters M, et al. 2002. Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg. Infect. Dis. 8:451-457.
45. Peeters M, et al. 1992. Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wildcaptured chimpanzee. AIDS 6:447-451.
46. Pepin J. 2011. The origins of AIDS. Cambridge University Press, New York, NY.
47. Perez-Caballero D, et al. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499-511.
48. Plantier JC, et al. 2009. A new human immunodeficiency virus derived from gorillas. Nat. Med. 15:871-872.
49. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 72: 2855-2864.
50. Plumptre AJ, Masozera M, Vedder A. 2001. The impact of civil war on the conservation of protected areas in Rwanda. Biodiversity Support Program, Washington, DC. http://www.worldwildlife.org/bsp/publications /africa/145/pdf/Rwanda.pdf.
51. Plumptre AJ, et al. 2010. Eastern chimpanzee (Pan troglodytes schweinfurthii): status survey and conservation action plan 2010-2020. IUCN/ SSC Primate Specialist Group, Arlington, VA. http://data.iucn.org/dbtw -wpd/edocs/2010-023.pdf.
52. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
53. Reynolds V. 2005. The chimpanzees of the Budongo forest: ecology, behaviour, and conservation. Oxford University Press, New York, NY.
54. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. 54. Rudicell RS, et al. 2010. Impact of simian immunodeficiency virus infection
55. Rudicell RS, et al. 2010. Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog. 6:e1001116. doi: 10.1371/journal.ppat.1001116.
56. Rudicell RS, et al. 2011. High prevalence of simian immunodeficiency virus infection in a community of savanna chimpanzees. J. Virol. 85: 9918-9928.
57. Ruiz A, Hill MS, Schmitt K, Guatelli J, Stephens EB. 2008. Requirements of the membrane proximal tyrosine and dileucine-based sorting signals for efficient transport of the subtype C Vpu protein to the plasma membrane and in virus release. Virology 378:58-68.
58. Ryan SJ, Walsh PD. 2011. Consequences of non-intervention for infectious disease in African great apes. PLoS One 6:e29030. doi:10.1371/ journal.pone.0029030.
59. Santiago ML, et al. 2003. Amplification of a complete simian immunodeficiency virus genome from fecal RNA of a wild chimpanzee. J. Virol. 77:2233-2242.
60. Santiago ML, et al. 2003. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J. Virol. 77:7545-7562.
61. Santiago ML, et al. 2002. SIVcpz in wild chimpanzees. Science 295:465.
62. Sauter D, et al. 2009. Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6:409-421.
63. Sauter D, Specht A, Kirchhoff F. 2010. Tetherin: holding on and letting go. Cell 141:392-398.
64. Shah AH, et al. 2010. Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 8:397-409.
65. Sharp PM, Hahn BH. 2010. The evolution of HIV-1 and the origin of AIDS. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:2487-2494.
66. Sharp PM, Hahn BH. 2011. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1:a006841. doi:10.1101/cshperspect/ a006841.
67. Sharp PM, Shaw GM, Hahn BH. 2005. Simian immunodeficiency virus infection of chimpanzees. J. Virol. 79:3891-3902.
68. Simon F, et al. 1998. Identification of a new human immunodeficiency virus type 1 distinct from groupMand group O. Nat. Med. 4:1032-1037.
69. Skasko M, et al. 2012. HIV-1 Vpu protein antagonizes innate restriction factor BST-2 via lipid-embedded helix-helix interactions. J. Biol. Chem. 287:58-67.
70. Sullivan KM, Mannucci A, Kimpton CP, Gill P. 1993. A rapid and quantitative DNA sex test: fluorescence-based PCR analysis of X-Y homologous gene amelogenin. Biotechniques 15:636-638, 640-641.
71. Surbeck M, Fowler A, Deimel C, Hohmann G. 2009. Evidence for the consumption of arboreal, diurnal primates by bonobos (Pan paniscus). Am. J. Primatol. 71:171-174.
72. Surbeck M, Hohmann G. 2008. Primate hunting by bonobos at Lui- Kotale, Salonga National Park. Curr. Biol. 18:R906 -R907.
73. Takehisa J, et al. 2009. Origin and biology of simian immunodeficiency virus in wild-living western gorillas. J. Virol. 83:1635-1648.
74. Takehisa J, et al. 2007. Generation of infectious molecular clones of simian immunodeficiency virus from fecal consensus sequences of wild chimpanzees. J. Virol. 81:7463-7475.
75. Terio KA, et al. 2011. Pathologic lesions in chimpanzees (Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004-2010. J. Zoo Wildl. Med. 42:597-607.
76. Van Damme N, et al. 2008. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3:245-252.
77. Vanden Haesevelde MM, et al. 1996. Sequence analysis of a highly divergent HIV-1-related lentivirus isolated from a wild captured chimpanzee. Virology 221:346-350.
78. Van Dooren S, et al. 2002. Lack of evidence for infection with simian immunodeficiency virus in bonobos. AIDS Res. Hum. Retroviruses 18: 213-216.
79. Van Heuverswyn F, et al. 2007. Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 368: 155-171.
80. Van Heuverswyn F, et al. 2006. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444:164.
81. Vigan R, Neil SJ. 2010. Determinants of tetherin antagonism in the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein. J. Virol. 84:12958-12970.
82. Vigan R, Neil SJ. 2011. Separable determinants of subcellular localization and interaction account for the inability of group O HIV-1 Vpu to counteract tetherin. J. Virol. 85:9737-9748.
83. Wain LV, et al. 2007. Adaptation of HIV-1 to its human host. Mol. Biol. Evol. 24:1853-1860.
84. Wei X, et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
85. Worobey M, et al. 2004. Origin of AIDS: contaminated polio vaccine theory refuted. Nature 428:820.
86. Yang SJ, Lopez LA, Exline CM, Haworth KG, Cannon PM. 2011. Lack of adaptation to human tetherin in HIV-1 group O and P. Retrovirology 8:78.
87. Yang SJ, et al. 2010. Anti-tetherin activities in Vpu-expressing primate lentiviruses. Retrovirology 7:13