SIVagm Infection in Wild African Green Monkeys from South Africa: Epidemiology, Natural History, and Evolutionary Considerations

PLoS Pathogens

Volumn 9, Issue 1, 2013, Pages

  Ma, Dongzhu ^a   Jasinska, Anna ^b   Kristoff, Jan ^a   Grobler, J Paul ^c   Turner, Trudy ^c,d   Jung, Yoon ^b   Schmitt, Christopher ^b   Raehtz, Kevin ^a   Feyertag, Felix ^e   Martinez Sosa, Natalie ^a   Wijewardana, Viskam ^a   Burke, Donald S ^a   Robertson, David L ^e   Tracy, Russell ^f   Pandrea, Ivona ^a,g   Freimer, Nelson ^b   Apetrei, Cristian ^a,g  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF THE FREE STATE   (South Africa)

^d UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f UNIVERSITY OF VERMONT   (United States)

^g UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD4 ANTIGEN; CHEMOKINE; CYTOKINE; INTERLEUKIN 6;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL TRANSLOCATION; CHLOROCEBUS; CONTROLLED STUDY; DNA SEQUENCE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETIC ANALYSIS; GENETIC VARIABILITY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHYLOGENY; PLEISTOCENE; POLYMERASE CHAIN REACTION; PREVALENCE; REAL TIME POLYMERASE CHAIN REACTION; RETROVIRUS INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SEROLOGY; SEXUAL MATURITY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SOUTH AFRICA; UIRED IMMUNE DEFICIENCY SYNDROME; UNINDEXED SEQUENCE; VIRUS LOAD;

ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; MALE; MOLECULAR SEQUENCE DATA; MUTATION RATE; RECOMBINATION, GENETIC; REPETITIVE SEQUENCES, NUCLEIC ACID; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SOUTH AFRICA;

EID: 84875079117     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003011     Document Type: Article

References (133)

1. VandeWoude S, Apetrei C, (2006) Going wild: Lessons from T-lymphotropic naturally occurring lentiviruses. Clin Microbiol Rev 19: 728-762.
2. Worobey M, Telfer P, Souquière S, Hunter M, Coleman CA, et al. (2010) Island biogeography reveals the deep history of SIV. Science 330: 1487.
3. Ahuka-Mundeke S, Ayouba A, Mbala-Kingebeni P, Liegeois F, Esteban A, et al. (2011) Novel multiplexed HIV/simian immunodeficiency virus antibody detection assay. Emerg Infect Dis 17: 2277-2286.
4. Groves C (2001) Primate taxonomy. Washington, DC: Smithsonian Institution Press.
5. Groves CP (2005) Order Primates. In: Wilson DE, Reeder DM, editors. Mammal Species of the World. Baltimore, MD: The Johns Hopkins University Press. pp. 111-184.
6. Grubb P, Butinsky TM, Oates JF, Bearder SK, Disotell TD, et al. (2003) Assessment of the diversity of African primates. Int J Primatol 24: 1301-1357.
7. Fomsgaard A, Allan J, Gravell M, London WT, Hirsch VM, et al. (1990) Molecular characterization of simian lentiviruses from east African green monkeys. J Med Primatol 19: 295-303.
8. Hirsch VM, McGann C, Dapolito G, Goldstein S, Ogen-Odoi A, et al. (1993) Identification of a new subgroup of SIVagm in tantalus monkeys. Virology 197: 426-430.
9. Fukasawa M, Miura T, Hasegawa A, Morikawa S, Tsujimoto H, et al. (1988) Sequence of simian immunodeficiency virus from African green monkey, a new member of the HIV/SIV group. Nature 333: 457-461.
10. Jin MJ, Hui H, Robertson DL, Muller MC, Barre-Sinoussi F, et al. (1994) Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO J 13: 2935-2947.
11. Allan JS, Short M, Taylor ME, Su S, Hirsch VM, et al. (1991) Species-specific diversity among simian immunodeficiency viruses from African green monkeys. J Virol 65: 2816-2828.
12. Hendry RM, Wells MA, Phelan MA, Schneider AL, Epstein JS, et al. (1986) Antibodies to simian immunodeficiency virus in African green monkeys in Africa in 1957-62. Lancet 2: 455.
13. Lowenstine LJ, Pedersen NC, Higgins J, Pallis KC, Uyeda A, et al. (1986) Seroepidemiologic survey of captive Old-World primates for antibodies to human and simian retroviruses, and isolation of a lentivirus from sooty mangabeys (Cercocebus atys). Int J Cancer 38: 563-574.
14. Ohta Y, Masuda T, Tsujimoto H, Ishikawa K, Kodama T, et al. (1988) Isolation of simian immunodeficiency virus from African green monkeys and seroepidemiologic survey of the virus in various non-human primates. Int J Cancer 41: 115-122.
15. Phillips-Conroy JE, Jolly CJ, Petros B, Allan JS, Desrosiers RC, (1994) Sexual transmission of SIVagm in wild grivet monkeys. J Med Primatol 23: 1-7.
16. Jolly C, Phillips-Conroy JE, Turner TR, Broussard S, Allan JS, (1996) SIVagm incidence over two decades in a natural population of Ethiopian grivet monkeys (Cercopithecus aethiops aethiops). J Med Primatol 25: 78-83.
17. Goldstein S, Brown CR, Ourmanov I, Pandrea I, Buckler-White A, et al. (2006) Comparison of simian immunodeficiency virus SIVagmVer replication and CD4+ T-cell dynamics in vervet and sabaeus African green monkeys. J Virol 80: 4868-4877.
18. Muller MC, Saksena NK, Nerrienet E, Chappey C, Herve VM, et al. (1993) Simian immunodeficiency viruses from central and western Africa: evidence for a new species-specific lentivirus in tantalus monkeys. J Virol 67: 1227-1235.
19. Johnson PR, Fomsgaard A, Allan J, Gravell M, London WT, et al. (1990) Simian immunodeficiency viruses from African green monkeys display unusual genetic diversity. J Virol 64: 1086-1092.
20. Baier M, Garber C, Muller C, Cichutek K, Kurth R, (1990) Complete nucleotide sequence of a simian immunodeficiency virus from African green monkeys: a novel type of intragroup divergence. Virology 176: 216-221.
21. Li Y, Naidu Y, Fultz P, Daniel MD, Desrosiers RC, (1989) Genetic diversity of simian immunodeficiency virus. J Med Primatol 18: 261-269.
22. Xing J, Wang H, Zhang Y, Ray DA, Tosi AJ, et al. (2007) A mobile element-based evolutionary history of guenons (tribe Cercopithecini). BMC Biol 5: 5.
23. Pandrea I, Apetrei C, (2010) Where the wild things are: Pathogenesis of SIV infection in African nonhuman primate hosts. Curr HIV/AIDS Reports 7: 28-36.
24. Pandrea I, Silvestri G, Apetrei C, (2009) AIDS in African nonhuman primate hosts of SIVs: A new paradigm of SIV infection. Curr HIV Res 6: 57-72.
25. Pandrea I, Apetrei C, Dufour J, Dillon N, Barbercheck J, et al. (2006) Simian immunodeficiency virus (SIV) SIVagm.sab infection of Caribbean African green monkeys: New model of the study of SIV pathogenesis in natural hosts. J Virol 80: 4858-4867.
26. Pandrea I, Kornfeld C, Ploquin MJ-I, Apetrei C, Faye A, et al. (2005) Impact of viral factors on very early in vivo replication profiles in SIVagm-infected African green monkeys. J Virol 79: 6249-6259.
27. Pandrea I, Silvestri G, Onanga R, Veazey RS, Marx PA, et al. (2006) Simian immunodeficiency viruses replication dynamics in African non-human primate hosts: common patterns and species-specific differences. J Med Primatol 35: 194-201.
28. Broussard SR, Staprans SI, White R, Whitehead EM, Feinberg MB, et al. (2001) Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. J Virol 75: 2262-2275.
29. Goldstein S, Ourmanov I, Brown CR, Beer BE, Elkins WR, et al. (2000) Wide range of viral load in healthy african green monkeys naturally infected with simian immunodeficiency virus. J Virol 74: 11744-11753.
30. Pandrea I, Gautam R, Ribeiro R, Brenchley JM, Butler IF, et al. (2007) Acute loss of intestinal CD4+ T cells is not predictive of SIV virulence. J Immunol 179: 3035-3046.
31. Pandrea I, Ribeiro RM, Gautam R, Gaufin T, Pattison M, et al. (2008) Simian immunodeficiency virus SIVagm dynamics in African green monkeys. J Virol 82: 3713-3724.
32. Favre D, Lederer S, Kanwar B, Ma ZM, Proll S, et al. (2009) Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathogens 5: e1000295.
33. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, et al. (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119: 3544-3555.
34. Kornfeld C, Ploquin MJ, Pandrea I, Faye A, Onanga R, et al. (2005) Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 115: 1082-1091.
35. Gaufin T, Pattison M, Gautam R, Stoulig C, Dufour J, et al. (2009) Effect of B cell depletion on viral replication and clinical outcome of SIV infection in a natural host. J Virol 83: 10347-10357.
36. Gaufin T, Ribeiro RM, Gautam R, Dufour J, Mandell D, et al. (2010) Experimental depletion of CD8+ cells in acutely SIVagm-infected African green monkeys results in increased viral replication. Retrovirology 7: 42.
37. Zahn RC, Rett MD, Korioth-Schmitz B, Sun Y, Buzby AP, et al. (2008) Simian Immunodeficiency Virus (SIV)-specific CD8+ T cell responses in chronically SIVagm-infected vervet African green monkeys. J Virol 82: 11577-11588.
38. Zahn RC, Rett MD, Li M, Tang H, Korioth-Schmitz B, et al. (2010) Suppression of adaptive immune responses during primary SIV infection of sabaeus African green monkeys delays partial containment of viremia but does not induce disease. Blood 115: 3070-3078.
39. Schmitz JE, Zahn RC, Brown CR, Rett MD, Li M, et al. (2009) Inhibition of adaptive immune responses leads to a fatal clinical outcome in SIV-infected pigtailed macaques but not vervet African green monkeys. PLoS Pathog 5: e1000691.
40. Hirsch VM, (2004) What can natural infection of African monkeys with simian immunodeficiency virus tell us about the pathogenesis of AIDS? AIDS Rev 6: 40-53.
41. Gicheru MM, Otsyula M, Spearman P, Graham BS, Miller CJ, et al. (1999) Neutralizing antibody responses in Africa green monkeys naturally infected with simian immunodeficiency virus (SIVagm). J Med Primatol 28: 97-104.
42. Estaquier J, Idziorek T, de Bels F, Barre-Sinoussi F, Hurtrel B, et al. (1994) Programmed cell death and AIDS: significance of T-cell apoptosis in pathogenic and nonpathogenic primate lentiviral infections. Proc Natl Acad Sci U S A 91: 9431-9435.
43. Cumont MC, Diop O, Vaslin B, Elbim C, Viollet L, et al. (2008) Early divergence in lymphoid tissue apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J Virol 82: 1175-1184.
44. Pandrea I, Sodora DL, Silvestri G, Apetrei C, (2008) Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol 29: 419-428.
45. Paiardini M, Cervasi B, Reyes-Aviles E, Micci L, Ortiz AM, et al. (2011) Reduced CCR5 up-regulation upon activation limits virus replication in central-memory CD4+ T cells of SIV-infected sooty mangabeys. Nature Medicine 17: 830-836.
46. Pandrea I, Apetrei C, Gordon S, Barbercheck J, Dufour J, et al. (2007) Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 109: 1069-1076.
47. Pandrea I, Onanga R, Souquiere S, Mouinga-Ondéme A, Bourry O, et al. (2008) Paucity of CD4+CCR5+ T-cells may prevent breastfeeding transmission of SIV in natural non-human primate hosts. J Virol 82: 5501-5509.
48. Beaumier CM, Harris LD, Goldstein S, Klatt NR, Whitted S, et al. (2009) CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat Med 15: 879-885.
49. Vinton C, Klatt NR, Harris LD, Briant JA, Sanders-Beer BE, et al. (2011) CD4-like immunological function by CD4- T cells in multiple natural hosts of simian immunodeficiency virus. J Virol 85: 8702-8708.
50. Apetrei C, Gaufin T, Gautam R, Vinton C, Hirsch VM, et al. (2010) Pattern of SIVagm infection in patas monkeys suggests that host adaptation to SIV infection may result in resistance to infection and virus extinction. J Infect Dis 202 (Suppl 3):: S371-376.
51. Silvestri G, Paiardini M, Pandrea I, Lederman MM, Sodora DL, (2007) Understanding the benign nature of SIV infection in natural hosts. J Clin Invest 117: 3148-3154.
52. Charleston MA, Robertson DL, (2002) Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol 51: 528-535.
53. Wertheim JO, Worobey M, (2007) A challenge to the ancient origin of SIVagm based on African green monkey mitochondrial genomes. PLoS Pathog 3: e95.
54. Hahn BH, Shaw GM, De Cock KM, Sharp PM, (2000) AIDS as a zoonosis: scientific and public health implications. Science 287: 607-614.
55. Peeters M, Courgnaud V, Abela B, Auzel P, Pourrut X, et al. (2002) Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg Infect Dis 8: 451-457.
56. Apetrei C, Robertson DL, Marx PA, (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.
57. Courgnaud V, Abela B, Pourrut X, Mpoudi-Ngole E, Loul S, et al. (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.
58. Courgnaud V, Formenty P, Akoua-Koffi C, Noe R, Boesch C, et al. (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.
59. Courgnaud V, Pourrut X, Bibollet-Ruche F, Mpoudi-Ngole E, Bourgeois A, et al. (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.
60. Courgnaud V, Salemi M, Pourrut X, Mpoudi-Ngole E, Abela B, et al. (2002) Characterization of a novel simian immunodeficiency virus with a vpu gene from greater spot-nosed monkeys (Cercopithecus nictitans) provides new insights into simian/human immunodeficiency virus phylogeny. J Virol 76: 8298-8309.
61. Apetrei C, Metzger MJ, Robinson D, Ling B, Telfer PT, et al. (2005) Detection and partial characterization of new simian immunodeficiency virus (SIVsm) strains from bush meat samples from rural Sierra Leone. J Virol 79: 2631-2636.
62. Liegeois F, Courgnaud V, Switzer WM, Murphy HW, Loul S, et al. (2006) Molecular characterization of a novel simian immunodeficiency virus lineage (SIVtal) from northern talapoins (Miopithecus ogouensis). Virology 349: 55-65.
63. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, et al. (2006) Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313: 523-526.
64. Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, et al. (2006) Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444: 164.
65. Santiago ML, Lukasik M, Kamenya S, Li Y, Bibollet-Ruche F, et al. (2003) Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J Virol 77: 7545-7562.
66. Santiago ML, Range F, Keele BF, Li Y, Bailes E, et al. (2005) Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 79: 12515-12527.
67. Santiago ML, Rodenburg CM, Kamenya S, Bibollet-Ruche F, Gao F, et al. (2002) SIVcpz in wild chimpanzees. Science 295: 465.
68. Keele BF, Holland Jones J, Terio K, Estes JD, Rudicell RS, et al. (2009) Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460: 515-519.
69. Rudicell RS, Holland Jones J, Wroblewski EE, Learn GH, Li Y, et al. (2010) Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog 6: e1001116 doi: 10.1371/journal.ppat.1001116.
70. Terio KA, Kinsel MJ, Raphael J, Mlengeya T, Lipende I, et al. (2011) Pathologic lesions in chimpanzees (Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004-2010. J Zoo Wildl Med 42: 597-607.
71. Kirchhoff F, Morrison HG, Desrosiers RC, (1995) Identification of V3 mutations that can compensate for inactivating mutations in C4 of simian immunodeficiency virus. Virology 213: 179-189.
72. Konig RR, Flory E, Steidl S, Neumann J, Coulibaly C, et al. (2002) Engineered CD4- and CXCR4-using simian immunodeficiency virus from African green monkeys is neutralization sensitive and replicates in nonstimulated lymphocytes. J Virol 76: 10627-10636.
73. Steidl S, Stitz J, Schmitt I, Konig R, Flory E, et al. (2002) Coreceptor Switch of [MLV(SIVagm)] pseudotype vectors by V3-loop exchange. Virology 300: 205-216.
74. Recordon-Pinson P, Soulie C, Flandre P, Descamps D, Lazrek M, et al. (2010) Evaluation of the genotypic prediction of HIV-1 coreceptor use versus a phenotypic assay and correlation with the virological response to maraviroc: the ANRS GenoTropism study. Antimicrob Agents Chemother 54: 3335-3340.
75. Lengauer T, Sander O, Sierra S, Thielen A, Kaiser R, (2007) Bioinformatics prediction of HIV coreceptor usage. Nat Biotechnol 25: 1407-1410.
76. Gautam R, Carter AC, Katz N, Butler IF, Barnes M, et al. (2007) In vitro characterization of primary SIVsmm isolates belonging to different lineages. In vitro growth on rhesus macaque cells is not predictive for in vivo replication in rhesus macaques. Virology 362: 257-270.
77. Mellors JW, Munoz A, Giorgi JV, Margolick JB, Tassoni CJ, et al. (1997) Plasma viral load and CD4+ lymphocytes as prognostic markers of HIV-1 infection. Ann Intern Med 126: 946-954.
78. Mellors JW, Rinaldo CR Jr, Gupta P, White RM, Todd JA, et al. (1996) Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272: 1167-1170.
79. Apetrei C, Gautam R, Sumpter B, Carter AC, Gaufin T, et al. (2007) Virus-subtype specific features of natural SIVsmm infection in sooty mangabeys. J Virol 81: 7913-7923.
80. Diop OM, Gueye A, Dias-Tavares M, Kornfeld C, Faye A, et al. (2000) High levels of viral replication during primary simian immunodeficiency virus SIVagm infection are rapidly and strongly controlled in African green monkeys. J Virol 74: 7538-7547.
81. Onanga R, Kornfeld C, Pandrea I, Estaquier J, Souquiere S, et al. (2002) High levels of viral replication contrast with only transient changes in CD4+ and CD8+ cell numbers during the early phase of experimental infection with simian immunodeficiency virus SIVmnd-1 in Mandrillus sphinx. J Virol 76: 10256-10263.
82. Onanga R, Souquiere S, Makuwa M, Mouinga-Ondeme A, Simon F, et al. (2006) Primary simian immunodeficiency virus SIVmnd-2 infection in mandrills (Mandrillus sphinx). J Virol 80: 3303-3309.
83. Silvestri G, Fedanov A, Germon S, Kozyr N, Kaiser WJ, et al. (2005) Divergent host responses during primary simian immunodeficiency virus SIVsm infection of natural sooty mangabey and nonnatural rhesus macaque hosts. J Virol 79: 4043-4054.
84. Gordon S, Klatt NR, Milush JM, Engram J, Dunham RM, et al. (2007) Severe depletion of mucosal CD4+ T cells in AIDS-free SIV-infected sooty mangabeys. J Immunol 179: 3026-3034.
85. Pandrea I, Onanga R, Kornfeld C, Rouquet P, Bourry O, et al. (2003) High levels of SIVmnd-1 replication in chronically infected Mandrillus sphinx. Virology 317: 119-127.
86. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, et al. (2003) Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18: 441-452.
87. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, et al. (2003) Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 17: 1871-1879.
88. Brenchley JM, Price DA, Douek DC, (2006) HIV disease: fallout from a mucosal catastrophe? Nat Immunol 7: 235-239.
89. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nature Medicine 12: 1365-1371.
90. Pandrea I, Gaufin T, Brenchley JM, Gautam R, Monjure C, et al. (2008) Experimentally-induced immune activation in natural hosts of SIV induces significant increases in viral replication and CD4+ T cell depletion. J Immunol 181: 6687-6691.
91. Bosinger SE, Li Q, Gordon SN, Klatt NR, Duan L, et al. (2009) Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 119: 3556-3572.
92. Muller MC, Barre-Sinoussi F, (2003) SIVagm: genetic and biological features associated with replication. Front Biosci 8: D1170-1185.
93. Johnson PR, Gravell M, Allan J, Goldstein S, Olmsted RA, et al. (1989) Genetic diversity among simian immunodeficiency virus isolates from African green monkeys. J Med Primatol 18: 271-277.
94. Apetrei C, Kaur A, Lerche NW, Metzger M, Pandrea I, et al. (2005) Molecular epidemiology of SIVsm in US Primate Centers unravels the origin of SIVmac and SIVstm. J Virol 79: 8991-9005.
95. Chen Z, Telfier P, Gettie A, Reed P, Zhang L, et al. (1996) Genetic characterization of new West African simian immunodeficiency virus SIVsm: geographic clustering of household-derived SIV strains with human immunodeficiency virus type 2 subtypes and genetically diverse viruses from a single feral sooty mangabey troop. J Virol 70: 3617-3627.
96. Souquiere S, Bibollet-Ruche F, Robertson DL, Makuwa M, Apetrei C, et al. (2001) Wild Mandrillus sphinx are carriers of two types of lentivirus. J Virol 75: 7086-7096.
97. Pandrea I, Parrish NF, Raehtz K, Gaufin T, Barbian HJ, et al. (2012) Mucosal SIV transmission in African green monkeys: Susceptibility to infection is proportional to target cell availability at mucosal sites. J Virol 86: 4158-4168.
98. Ma ZM, Keele BF, Qureshi H, Stone M, Desilva V, et al. (2011) SIVmac251 is inefficiently transmitted to rhesus macaques by penile inoculation with a single SIVenv variant found in ramp-up phase plasma. AIDS Res Hum Retroviruses 27: 1259-1269.
99. Andelman SJ (1986) Ecological and social determinants of cercopithecine mating patterns. In: Rubenstein DI, Wrangham RW, editors. Ecological Aspects of Social Evolution. Princeton: Princeton University Press. pp. 201-216.
100. Cords M (2000) The number of males in guenon groups. In: Kappeler P, editor. Primate Males: Causes and Consequences of Variation in Group Composition. Cambridge, UK: Cambridge University Press. pp. 84-96.
101. Keddy AC, (1986) Female mate choice in vervet monkeys (Cercopithecus aethiops sabaeus). American Journal of Primatology 10: 125-134.
102. Weingrill T, Willems EP, Krutzen M, Noe R, (2011) Determinants of Paternity Success in a Group of Captive Vervet Monkeys (Chlorocebus aethiops sabaeus). International Journal of Primatology 32: 415-429.
103. Cowlishaw G, Dunbar RIM, (1991) Dominance rank and mating success in male primates. Animal Behaviour 41: 1045-1056.
104. Andelman SJ, (1987) Evolution of concealed ovulation in vervet monkeys (Cercopithecus aethiops). Am Naturalist 129: 785-799.
105. Nerrienet E, Amouretti X, Muller-Trutwin MC, Poaty-Mavoungou V, Bedjebaga I, et al. (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 Retroviruses 14: 785-796.
106. Cheney D, Seyfarth R, (1983) Nonrandom dispersal in free-ranging vervet monkeys: Social and genetic consequences. Am Naturalist 122: 392-412.
107. Amedee AM, Rychert J, Lacour N, Fresh L, Ratterree M, (2004) Viral and immunological factors associated with breast milk transmission of SIV in rhesus macaques. Retrovirology 1: 17.
108. Chahroudi A, Meeker T, Lawson B, Ratcliffe S, Else J, et al. (2011) Mother-to-infant transmission of simian immunodeficiency virus is rare in sooty mangabeys and is associated with low viremia. J Virol 85: 5757-5763.
109. Beer B, Denner J, Brown CR, Norley S, zur Megede J, et al. (1998) Simian immunodeficiency virus of African green monkeys is apathogenic in the newborn natural host. J Acquir Immune Defic Syndr Hum Retrovirol 18: 210-220.
110. Ruprecht RM, Baba TW, Liska V, Ray NB, Martin LN, et al. (1999) Oral transmission of primate lentiviruses. J Infect Dis 179 (Suppl 3):: S408-412.
111. Chenine AL, Siddappa NB, Kramer VG, Sciaranghella G, Rasmussen RA, et al. (2010) Relative transmissibility of an R5 clade C simian-human immunodeficiency virus across different mucosae in macaques parallels the relative risks of sexual HIV-1 transmission in humans via different routes. J Infect Dis 201: 1155-1163.
112. Cheney D, Seyfarth R, Smuts B, (1986) Social relationships and social cognition in nonhuman primates. Science 234: 1361-1366.
113. Schwab P, Debes PV, Witt T, Hartl GB, Hmwe SS, et al. (2012) Genetic structure of the common impala (Aepyceros melampus melampus) in South Africa: pylogeography and implications for conservation. J Zool Syst Evol Res 50: 76-84.
114. Sithaldeen R, Bishop JM, Ackermann RR, (2009) Mitochondrial DNA analysis reveals Plio-Pleistocene diversification within the chacma baboon. Mol Phylogenet Evol 53: 1042-1048.
115. Drummond AJ, Suchard MA, Xie D, Rambaut A, (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969-1973.
116. Pandrea I, Onanga R, Rouquet P, Bourry O, Ngari P, et al. (2001) Chronic SIV infection ultimately causes immunodeficiency in African non-human primates. AIDS 15: 2461-2462.
117. Traina-Dorge V, Blanchard J, Martin L, Murphey-Corb M, (1992) Immunodeficiency and lymphoproliferative disease in an African green monkey dually infected with SIV and STLV-I. AIDS Res Hum Retroviruses 8: 97-100.
118. Ling B, Apetrei C, Pandrea I, Veazey RS, Lackner AA, et al. (2004) Classic AIDS in a sooty mangabey after an 18-year natural infection. J Virol 78: 8902-8908.
119. Apetrei C, Gormus B, Pandrea I, Metzger M, ten Haaft P, et al. (2004) Direct inoculation of simian immunodeficiency virus from sooty mangabeys in black mangabeys (Lophocebus aterrimus): first evidence of AIDS in a heterologous African species and different pathologic outcomes of experimental infection. J Virol 78: 11506-11518.
120. Etienne L, Nerrienet E, LeBreton M, Bibila GT, Foupouapouognigni Y, 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.
121. Pandrea I, Cornell E, Wilson C, Ribeiro RM, Ma D, et al. (2012) Coagulation biomarkers predict disease progression in SIV-infected nonhuman primates. Blood 120: 1357-1366.
122. Lederer S, Favre D, Walters KA, Proll S, Kanwar B, et al. (2009) Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog 5: e1000296.
123. Lederman MM, Alter G, Daskalakis DC, Rodriguez B, Sieg SF, et al. (2010) Determinants of protection among HIV-exposed seronegative persons: an overview. J Infect Dis 202 (Suppl 3):: S333-338.
124. Watkins DI, Burton DR, Kallas EG, Moore JP, Koff WC, (2008) Nonhuman primate models and the failure of the Merck HIV-1 vaccine in humans. Nat Med 14: 617-621.
125. Grobler P, Turner T, (2010) A novel trap design for the capture and sedation of vervet monkeys (Chlorocebus aethiops). South Afr J Wildlife Res 40: 163-168.
126. Bibollet-Ruche F, Bailes E, Gao F, Pourrut X, Barlow KL, et al. (2004) A new simian immunodeficiency virus lineage (SIVdeb) infecting de Brazza's monkeys (Cercopithecus neglectus): Evidence for a Cercopithecus monkey virus clade. J Virol 78: 7748-7762.
127. Gao F, Yue L, Robertson DL, Hill SC, Hui H, et al. (1994) Genetic diversity of human immunodeficiency virus type 2: evidence for distinct sequence subtypes with differences in virus biology. J Virol 68: 7433-7447.
128. Jin MJ, Rogers J, Phillips-Conroy JE, Allan JS, Desrosiers RC, et al. (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.
129. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
130. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
131. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
132. Simon F, Souquiere S, Damond F, Kfutwah A, Makuwa M, et al. (2001) Synthetic peptide strategy for the detection of and discrimination among highly divergent primate lentiviruses. AIDS Res Hum Retroviruses 17: 937-952.
133. Kuiken C, Foley B, Leitner T, Apetrei C, Hahn B, et al. (2010) HIV Sequence Compendium. Los Alamos National Laboratory, New Mexico, LA-UR 10-03684: Theoretical Biology and Biophysics Group.