Coinfection of Ugandan red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with novel, divergent delta-, lenti-, and spumaretroviruses

Journal of Virology

Volumn 83, Issue 21, 2009, Pages 11318-11329

  Goldberg, Tony L ^a,g   Sintasath, David M ^b   Chapman, Colin A ^c,d,g   Cameron, Kenneth M ^d   Karesh, William B ^d   Tang, Shaohua ^e   Wolfe, Nathan D ^f,i   Rwego, Innocent B ^g   Ting, Nelson ^h   Switzer, William M ^e  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d WILDLIFE CONSERVATION SOCIETY   (United States)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^f Global Viral Forecasting Initiative   (United States)

^g MAKERERE UNIVERSITY   (Uganda)

^h E11 SSH   (United States)

ⁱ STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ARTICLE; COEVOLUTION; CONTROLLED STUDY; FEMALE; GEOGRAPHIC DISTRIBUTION; LONG TERMINAL REPEAT; MALE; MIXED INFECTION; MONKEY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RETROVIRUS; SIMIAN FOAMY VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS; UGANDA; VIRUS CELL INTERACTION;

ANIMALS; BIOLOGICAL EVOLUTION; COLOBUS; DELTARETROVIRUS INFECTIONS; DNA, MITOCHONDRIAL; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; MALE; PHYLOGENY; RETROVIRIDAE INFECTIONS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN FOAMY VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN T-LYMPHOTROPIC VIRUS 1; UGANDA;

COLOBUS; COLOBUS GUEREZA; COLOBUS SP.; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 2; PILIOCOLOBUS; PRIMATES; PROCOLOBUS; PROCOLOBUS BADIUS; RABBIT FIBROMA VIRUS; RETROVIRIDAE; SIMIAE; SIMIAN FOAMY VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN T-LYMPHOTROPIC VIRUS 3;

EID: 70350322310     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02616-08     Document Type: Article

References (70)

1. Apetrei, C., D. L. Robertson, and P. A. Marx. 2004. The history of SIVS and AIDS: epidemiology, phylogeny and biology of isolates from naturally SIV-infected non-human primates (NHP) in Africa. Front. Biosci. 9:225-254.
2. Biek, R., A. J. Drummond, and M. Poss. 2006. A virus reveals population structure and recent demographic history of its carnivore host. Science 311:538-541. (Pubitemid 43157734)
3. Calattini, S., E. B. A. Betsem, A. Froment, P. Mauclère, P. Tortevoye, C. Schmitt, R. Njouom, A. Saib, and A. Gessain. 2007. Simian foamy virus transmission from apes to humans, rural Cameroon. Emerg. Infect. Dis. 13:1314-1320.
4. Chapman, C. A., and L. J. Chapman. 2002. Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133:861-875.
5. Chapman, C. A., and J. E. Lambert. 2000. Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda. Am. J. Primatol. 50:169-185.
6. Chapman, C. A., T. T. Struhsaker, and J. E. Lambert. 2005. Thirty years of research in Kibale National Park, Uganda, reveals a complex picture for conservation. Int. J. Primatol. 26:539-555.
7. Charleston, M. A., and D. L. Robertson. 2002. Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst. Biol. 51:528-535.
8. Chen, Z., A. Luckay, D. L. Sodora, P. Telfer, P. Reed, A. Gettie, J. M. Kanu, R. F. Sadek, J. Yee, D. D. Ho, L. Zhang, and P. A. Marx. 1997. Human immunodeficiency virus type 2 (HIV-2) seroprevalence and characterization of a distinct HIV-2 genetic subtype from the natural range of simian immunodeficiency virus-infected sooty mangabeys. J. Virol. 71:3953-3960. (Pubitemid 27172410)
9. Courgnaud, V., P. Formenty, C. Akoua-Koffi, R. Noe, C. Boesch, E. Delaporte, and M. Peeters. 2003. Partial molecular characterization of two simian immunodeficiency viruses (SIV) from African colobids: SIVwrc from Western red colobus (Piliocolobus badius) and SIVolc from olive colobus (Procolobus verus). J. Virol. 77:744-748.
10. Courgnaud, V., X. Pourrut, F. Bibollet-Ruche, E. Mpoudi-Ngole, A. Bourgeois, E. Delaporte, and M. Peeters. 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.
11. Crandall, K. A. 1996. Multiple interspecies transmissions of human and simian T-cell leukemia/lymphoma virus type I sequences. Mol. Biol. Evol. 13:115-131.
12. Delson, E., I. Tattersall, J. A. Van Couvering, and A. S. Brooks (ed.). 2000. Encyclopedia of human evolution and prehistory, 2nd ed. Garland, New York, NY.
13. Disotell, T. R. 2006. Primate phylogenetics. In Encyclopedia of life sciences. John Wiley & Sons, Ltd., Chichester, United Kingdom. doi:10.1038/npg.els.0006101.
14. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
15. Endicott, P., and S. Y. Ho. 2008. A Bayesian evaluation of human mitochondrial substitution rates. Am. J. Hum. Genet. 82:895-902.
16. Gao, F., E. Bailes, D. L. Robertson, Y. Chen, C. M. Rodenburg, S. F. Michael, L. B. Cummins, L. O. Arthur, M. Peeters, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 1999. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436-441.
17. Gebo, D. L., L. MacLatchy, R. Kityo, A. Deino, J. Kingston, and D. Pilbeam. 1997. A hominoid genus from the early Miocene of Uganda. Science 276:401-404. (Pubitemid 27180698)
18. Georges-Courbot, M. C., C. Y. Lu, M. Makuwa, P. Telfer, R. Onanga, G. Dubreuil, Z. Chen, S. M. Smith, A. Georges, F. Gao, B. H. Hahn, and P. A. Marx. 1998. Natural infection of a household pet red-capped mangabey (Cercocebus torquatus torquatus) with a new simian immunodeficiency virus. J. Virol. 72:600-608.
19. Goldberg, T. L., T. R. Gillespie, and I. B. Rwego. 2008. Health and disease in the people, primates, and domestic animals of Kibale National Park: implications for conservation, p. 75-87. In R. Wrangham and E. Ross (ed.), Science and conservation in African forests: the benefits of long-term research. Cambridge University Press, Cambridge, United Kingdom.
20. Goldberg, T. L., T. R. Gillespie, I. B. Rwego, and C. Kaganzi. 2006. Killing of a pearl-spotted owlet (Glaucidium perlatum) by male red colobus monkeys (Procolobus tephrosceles) in a forest fragment near Kibale National Park, Uganda. Am. J. Primatol. 68:1007-1011.
21. Groves, C. P. 2001. Primate taxonomy. Smithsonian Institution Press, Washington, DC.
22. Grubb, P., T. M. Butynski, J. F. Oates, S. K. Bearder, T. R. Disotell, C. P. Groves, and T. T. Struhsaker. 2003. Assessment of the diversity of African primates. Int. J. Primatol. 24:1301-1357.
23. Hahn, B. H., G. M. Shaw, K. M. De Cock, and P. M. Sharp. 2000. AIDS as a zoonosis: scientific and public health implications. Science 287:607-614. (Pubitemid 30070900)
24. Hirsch, V. M., B. J. Campbell, E. Bailes, R. Goeken, C. Brown, W. R. Elkins, M. Axthelm, M. Murphey-Corb, and P. M. Sharp. 1999. Characterization of a novel simian immunodeficiency virus (SIV) from L'Hoest monkeys (Cercopithecus l'hoesti): implications for the origins of SIVmnd and other primate lentiviruses. J. Virol. 73:1036-1045.
25. Hirsch, V. M., R. A. Olmsted, M. Murphey-Corb, R. H. Purcell, and P. R. Johnson. 1989. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339:389-392.
26. Hu, J., W. M. Switzer, B. T. Foley, D. L. Robertson, R. M. Goeken, B. T. Korber, V. M. Hirsch, and B. E. Beer. 2003. Characterization and comparison of recombinant simian immunodeficiency virus from drill (Mandrillus leucophaeus) and mandrill (Mandrillus sphinx) isolates. J. Virol. 77:4867-4880.
27. Hussain, A. I., V. Shanmugam, V. B. Bhullar, B. E. Beer, D. Vallet, A. Gautier-Hion, N. D. Wolfe, W. B. Karesh, A. M. Kilbourn, Z. Tooze, W. Heneine, and W. M. Switzer. 2003. Screening for simian foamy virus infection by using a combined antigen Western blot assay: evidence for a wide distribution among Old World primates and identification of four new divergent viruses. Virology 309:248-257.
28. Jin, M. J., H. Hui, D. L. Robertson, M. C. Muller, F. Barre-Sinoussi, V. M. Hirsch, J. S. Allan, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 1994. Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO J. 13:2935-2947. (Pubitemid 24191704)
29. Jin, M. J., J. Rogers, J. E. Phillips-Conroy, J. S. Allan, R. C. Desrosiers, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 1994. Infection of a yellow baboon with simian immunodeficiency virus from African green monkeys: evidence for cross-species transmission in the wild. J. Virol. 68:8454-8460.
30. Leakey, M. G. 1993. Evolution of Theropithecus in the Turkana Basin, p. 85-124. In N. G. Jablonski (ed.), Theropithecus: the rise and fall of a primate genus. Cambridge University Press, Cambridge, United Kingdom.
31. Leakey, M. G., C. S. Feibel, I. McDougall, C. Ward, and A. Walker. 1998. New specimens and confirmation of an early age for Australopithecus anamensis. Nature 393:62-66.
32. Leendertz, F. H., S. Junglen, C. Boesch, P. Formenty, E. Couacy-Hymann, V. Courgnaud, G. Pauli, and H. Ellerbrok. 2004. High variety of different simian T-cell leukemia virus type 1 strains in chimpanzees (Pan troglodytes verus) of the Tai National Park, Cote d'Ivoire. J. Virol. 78:4352-4356.
33. Leendertz, F. H., F. Zirkel, E. Couacy-Hymann, H. Ellerbrok, V. A. Morozov, G. Pauli, C. Hedemann, P. Formenty, S. A. Jensen, C. Boesch, and S. Junglen. 2008. Interspecies transmission of simian foamy virus in a natural predator-prey system. J. Virol. 82:7741-7744.
34. Liegeois, F., V. Courgnaud, W. M. Switzer, H. W. Murphy, S. Loul, A. Aghokeng, X. Pourrut, E. Mpoudi-Ngole, E. Delaporte, and M. Peeters. 2006. Molecular characterization of a novel simian immunodeficiency virus lineage (SIVtal) from northern talapoins (Miopithecus ogouensis). Virology 349:55-65. (Pubitemid 43732481)
35. Liegeois, F., B. Lafay, P. Formenty, S. Locatelli, V. Courgnaud, E. Delaporte, and M. Peeters. 2009. Full-length genome characterization of a novel simian immunodeficiency virus lineage (SIVolc) from olive colobus (Procolobus verus) and new SIVwrcPbb strains from western red colobus (Piliocolobus badius badius) from the Tai forest in Ivory Coast. J. Virol. 83:428-439.
36. Liegeois, F., B. Lafay, W. M. Switzer, S. Locatelli, E. Mpoudi-Ngole, S. Loul, W. Heneine, E. Delaporte, and M. Peeters. 2007. Identification and molecular characterization of new STLV-1 and STLV-3 strains in wild-caught nonhuman primates in Cameroon. Virology 371:405-417. (Pubitemid 351181324)
37. Liu, W., M. Worobey, Y. Li, B. F. Keele, F. Bibollet-Ruche, Y. Guo, P. A. Goepfert, M. L. Santiago, J. B. Ndjango, C. Neel, S. L. Clifford, C. Sanz, S. Kamenya, M. L. Wilson, A. E. Pusey, N. Gross-Camp, C. Boesch, V. Smith, K. Zamma, M. A. Huffman, J. C. Mitani, D. P. Watts, M. Peeters, G. M. Shaw, W. M. Switzer, P. M. Sharp, and B. H. Hahn. 2008. Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. PLoS Pathog. 4:e1000097.
38. Locatelli, S., B. Lafay, F. Liegeois, N. Ting, E. Delaporte, and M. Peeters. 2008. Full molecular characterization of a simian immunodeficiency virus, SIVwrcpbt from Temminck's red colobus (Piliocolobus badius temminckii) from Abuko Nature Reserve, The Gambia. Virology 376:90-100.
39. Locatelli, S., F. Liegeois, B. Lafay, A. D. Roeder, M. W. Bruford, P. Formenty, R. Noe, E. Delaporte, and M. Peeters. 2008. Prevalence and genetic diversity of simian immunodeficiency virus infection in wild-living red colobus monkeys (Piliocolobus badius badius) from the Tai forest, Côte d'Ivoire. Infect. Genet. Evol. 8:1-14.
40. Martin, D. P., C. Williamson, and D. Posada. 2005. RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260-262. (Pubitemid 40202028)
41. Meertens, L., J. Rigoulet, P. Mauclere, M. Van Beveren, G. M. Chen, O. Diop, G. Dubreuil, M. C. Georges-Goubot, J. L. Berthier, J. Lewis, and A. Gessain. 2001. Molecular and phylogenetic analyses of 16 novel simian T-cell leukemia virus type 1 from Africa: close relationship of STLV-1 from Allenopithecus nigroviridis to HTLV-1 subtype B strains. Virology 287:275-285.
42. Ndongmo, C. B., W. M. Switzer, C. P. Pau, C. Zeh, A. Schaefer, D. Pieniazek, T. M. Folks, and M. L. Kalish. 2004. New multiple antigenic peptide-based enzyme immunoassay for detection of simian immunodeficiency virus infection in nonhuman primates and humans. J. Clin. Microbiol. 42:5161-5169.
43. Nerrienet, E., X. Amouretti, M. C. Muller-Trutwin, V. Poaty-Mavoungou, I. Bedjebaga, H. T. Nguyen, G. Dubreuil, S. Corbet, E. J. Wickings, F. Barre-Sinoussi, A. J. Georges, and M. C. Georges-Courbot. 1998. Phylogenetic analysis of SIV and STLV type I in mandrills (Mandrillus sphinx): indications that intracolony transmissions are predominantly the result of male-to-male aggressive contacts. AIDS Res. Hum. Retrovir. 14:785-796.
44. Posada, D., and T. R. Buckley. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53:793-808.
45. Qiao, B., T. L. Goldberg, G. J. Olsen, and R. M. Weigel. 2006. A computer simulation analysis of the accuracy of partial genome sequencing and restriction fragment analysis in the reconstruction of phylogenetic relationships. Infect. Genet. Evol. 6:323-330.
46. Raaum, R. L., K. N. Sterner, C. M. Noviello, C. B. Stewart, and T. R. Disotell. 2005. Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. J. Hum. Evol. 48:237-257.
47. Sanderson, M. J. 2003. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301-302.
48. Santiago, M. L., M. Lukasik, S. Kamenya, Y. Li, F. Bibollet-Ruche, E. Bailes, M. N. Muller, M. Emery, D. A. Goldenberg, J. S. Lwanga, A. Ayouba, E. Nerrienet, H. M. McClure, J. L. Heeney, D. P. Watts, A. E. Pusey, D. A. Collins, R. W. Wrangham, J. Goodall, J. F. Brookfield, P. M. Sharp, G. M. Shaw, and B. H. Hahn. 2003. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J. Virol. 77:7545-7562.
49. Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502-504. (Pubitemid 34284960)
50. Schweizer, M., and D. Neumann-Haefelin. 1995. Phylogenetic analysis of primate foamy viruses by comparison of pol sequences. Virology 207:577-582.
51. Sharp, P. M., D. L. Robertson, and B. H. Hahn. 1995. Cross-species transmission and recombination of 'AIDS' viruses. Philos. Trans. R. Soc. London 349:41-47.
52. Steiper, M. E., and N. M. Young. 2006. Primate molecular divergence dates. Mol. Phylogenet. Evol. 41:384-394.
53. Steiper, M. E., N. M. Young, and T. Y. Sukarna. 2004. Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence. Proc. Natl. Acad. Sci. USA 101:17021-17026.
54. Sterner, K. N., R. L. Raaum, Y. P. Zhang, C. B. Stewart, and T. R. Disotell. 2006. Mitochondrial data support an odd-nosed colobine clade. Mol. Phylogenet. Evol. 40:1-7.
55. Struhsaker, T. T. 1997. Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. University Press of Florida, Gainesville.
56. Struhsaker, T. T. 1975. The red colobus monkey. University of Chicago Press, Chicago, IL.
57. Switzer, W. M., V. Bhullar, V. Shanmugam, M. E. Cong, B. Parekh, N. W. Lerche, J. L. Yee, J. J. Ely, R. Boneva, L. E. Chapman, T. M. Folks, and W. Heneine. 2004. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. J. Virol. 78:2780-2789.
58. Switzer, W. M., B. Parekh, V. Shanmugam, V. Bhullar, S. Phillips, J. J. Ely, and W. Heneine. 2005. The epidemiology of simian immunodeficiency virus infection in a large number of wild- and captive-born chimpanzees: evidence for a recent introduction following chimpanzee divergence. AIDS Res. Hum. Retrovir. 21:335-342.
59. Switzer, W. M., M. Salemi, S. H. Qari, H. Jia, R. R. Gray, A. Katzourakis, S. J. Marriott, K. N. Pryor, N. D. Wolfe, D. S. Burke, T. M. Folks, and W. Heneine. 2009. Ancient, independent evolution and distinct molecular features of the novel human T-lymphotropic virus type 4. Retrovirology 6:9.
60. Switzer, W. M., M. Salemi, V. Shanmugam, F. Gao, M. E. Cong, C. Kuiken, V. Bhullar, B. E. Beer, D. Vallet, A. Gautier-Hion, Z. Tooze, F. Villinger, E. C. Holmes, and W. Heneine. 2005. Ancient co-speciation of simian foamy viruses and primates. Nature 434:376-380.
61. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
62. Ting, N. 2008. Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys. J. Hum. Evol. 55:312-325.
63. Van Dooren, S., V. Shanmugam, V. Bhullar, B. Parekh, A. M. Vandamme, W. Heneine, and W. M. Switzer. 2004. Identification in gelada baboons (Theropithecus gelada) of a distinct simian T-cell lymphotropic virus type 3 with a broad range of Western blot reactivity. J. Gen. Virol. 85:507-519.
64. van Rensburg, E. J., S. Engelbrecht, J. Mwenda, J. D. Laten, B. A. Robson, T. Stander, and G. K. Chege. 1998. Simian immunodeficiency viruses (SIVs) from eastern and southern Africa: detection of a SIVagm variant from a chacma baboon. J. Gen. Virol. 79:1809-1814.
65. Watts, D. P., and J. C. Mitani. 2002. Hunting behavior of chimpanzees at Ngogo, Kibale National Park, Uganda. Int. J. Primatol. 23:1-28.
66. Wertheim, J. O., and M. Worobey. 2007. A Challenge to the ancient origin of SIVagm based on African green monkey mitochondrial genomes. PLoS Pathog. 3:e95.
67. Wolfe, N. D., W. Heneine, J. K. Carr, A. D. Garcia, V. Shanmugam, U. Tamoufe, J. N. Torimiro, A. T. Prosser, M. Lebreton, E. Mpoudi-Ngole, F. E. McCutchan, D. L. Birx, T. M. Folks, D. S. Burke, and W. M. Switzer. 2005. Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proc. Natl. Acad. Sci. USA 102:7994-7999.
68. Wolfe, N. D., W. M. Switzer, J. K. Carr, V. B. Bhullar, V. Shanmugam, U. Tamoufe, A. T. Prosser, J. N. Torimiro, A. Wright, E. Mpoudi-Ngole, F. E. McCutchan, D. L. Birx, T. M. Folks, D. S. Burke, and W. Heneine. 2004. Naturally acquired simian retrovirus infections in central African hunters. Lancet 363:932-937.
69. Womble, D. D. 2000. Web-based interfaces for the GCG sequence analysis programs. Methods Mol. Biol. 132:23-30.
70. Xia, X., and Z. Xie. 2001. DAMBE: software package for data analysis in molecular biology and evolution. J. Hered. 92:371-373. (Pubitemid 32848767)