Skip to main content

Advertisement

SpringerLink
Log in

The Evolution of Resistance to Simian Immunodeficiency Virus (SIV): A Review

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Examining how pathogens cross species boundaries, spread within species, and persist within their hosts is an essential part of understanding the factors that underpin the evolution of virulence and host resistance. Here, we review current knowledge about the genetic diversity, molecular epidemiology, prevalence, and pathogenicity of simian immunodeficiency viruses (SIVs). SIVs have crossed species boundaries from simian hosts to humans on at least 12 separate occasions, one of which led to the global HIV–AIDS crisis. Though SIVs infect a wide range of primates, scientists have only recently begun to describe the natural history of SIV infection in their natural hosts. Several new studies reveal how both viral and host factors are responsible for the transmission to, and adaptation in, new hosts. These studies also suggest that the spread of the virus may be affected by host-specific traits, including social structure, mating system and demographic history. These studies challenge the traditional view that SIV is relatively benign in its natural host, and instead suggest that a highly dynamic relationship exists between SIV and its simian hosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aghokeng, A. F., Ayouba, A., Mpoudi-Ngole, E., Loul, S., Liegeois, F., Delaporte, E., et al. (2010). Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat provides insights into risks for potential new cross-species transmissions. Infection, Genetics and Evolution, 10(3), 386–396.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ahuka-Mundeke, S., Ayouba, A., Mbala-Kingebeni, P., Liegeois, F., Esteban, A., Lunguya-Metila, O., et al. (2011). A novel multiplexed HIV/SIV antibody detection assay identified new simian immunodeficiency viruses in primate bushmeat in the Democratic Republic of Congo. Emerging Infectious Diseases, 17(12), 2277–2286.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Alcantara, S., Reece, J., Amarasena, T., Rose, R. D., Manitta, J., Amin, J., et al. (2009). Thrombocytopenia is strongly associated with simian AIDS in pigtail macaques. Journal of Acquired Immune Deficiency Syndromes, 51(4), 374–379.

    PubMed  Google Scholar 

  • Amedee, A. M., 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.

    PubMed Central  PubMed  Google Scholar 

  • Andersson, S., Norrgren, H., da Silva, Z., Biague, A., Bamba, S., Kwok, S., et al. (2000). Plasma viral load in HIV-1 and HIV-2 singly and dually infected individuals in Guinea-Bissau, West Africa: Significantly lower plasma virus set point in HIV-2 infection than in HIV-1 infection. Archives of Internal Medicine, 160(21), 3286–3293.

    PubMed  CAS  Google Scholar 

  • Apetrei, C., Gaufin, T., Gautam, R., Vinton, C., Hirsch, V., Lewis, M., et al. (2010). Pattern of SIVagm infection in patas monkeys suggests that host adaptation to simian immunodeficiency virus infection may result in resistance to infection and virus extinction. Journal of Infectious Diseases, 202(Suppl 3), S371–376.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Apetrei, C., Gormus, B., Pandrea, I., Metzger, M., ten Haaft, P., Martin, L. N., et al. (2004a). 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. Journal of Virology, 78(21), 11506–11518.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Apetrei, C., Metzger, M. J., Richardson, D., Ling, B., Telfer, P. T., Reed, P., et al. (2005). Detection and partial characterization of simian immunodeficiency virus SIVsm strains from bush meat samples from rural Sierra Leone. Journal of Virology, 79(4), 2631–2636.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Apetrei, C., Pandrea, I., & Mellors, J. W. (2012). Nonhuman primate models for HIV cure research. PLoS Pathogens, 8(8), e1002892.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Apetrei, C., Robertson, D. L., & Marx, P. A. (2004b). The history of SIVS and AIDS: Epidemiology, phylogeny and biology of isolates from naturally SIV infected non-human primates (NHP) in Africa. Frontiers in Bioscience, 9, 225–254.

    PubMed  CAS  Google Scholar 

  • Arandjelovic, M., Head, J., Rabanal, L. I., Schubert, G., Mettke, E., Boesch, C., et al. (2011). Non-invasive genetic monitoring of wild central chimpanzees. PLoS ONE, 6(3), e14761.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ayouba, A., Akoua-Koffi, C., Calvignac-Spencer, S., Esteban, A., Locatelli, S., Li, H., et al. (2013). Evidence for continuing cross-species transmission of SIVsmm to humans: Characterization of a new HIV-2 lineage in rural Cote d'Ivoire. AIDS. doi:10.1097/01.aids.0000432443.22684.50.

    PubMed Central  PubMed  Google Scholar 

  • Bailes, E., Gao, F., Bibollet-Ruche, F., Courgnaud, V., Peeters, M., Marx, P. A., et al. (2003). Hybrid origin of SIV in chimpanzees. Science, 300(5626), 1713.

    PubMed  CAS  Google Scholar 

  • Barnett, S. W., Murthy, K. K., Herndier, B. G., & Levy, J. A. (1994). An AIDS-like condition induced in baboons by HIV-2. Science, 266(5185), 642–646.

    PubMed  CAS  Google Scholar 

  • Beaumier, C. M., Harris, L. D., Goldstein, S., Klatt, N. R., Whitted, S., McGinty, J., et al. (2009). CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nature Medicine, 15(8), 879–885.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Beer, B. E., Bailes, E., Sharp, P. M., & Hirsch, V. M. (1999). Diversity and evolution of primate lentiviruses. In C. L. Kuiken, B. Foley, B. Hahn, B. Korber, F. McCutchan, P. A. Marx, et al. (Eds.), Human retroviruses and AIDS (pp. 460–474). Los Alamos, NM: Los Alamos National Laboratory.

    Google Scholar 

  • Beer, B. E., Foley, B. T., Kuiken, C. L., Tooze, Z., Goeken, R. M., Brown, C. R., et al. (2001). Characterization of novel simian immunodeficiency viruses from red-capped mangabeys from Nigeria (SIVrcmNG409 and -NG411). Journal of Virology, 75(24), 12014–12027.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Berry, N., Jaffar, S., Schim van der Loeff, M., Ariyoshi, K., Harding, E., N'Gom, P. T., et al. (2002). Low level viremia and high CD4% predict normal survival in a cohort of HIV type-2-infected villagers. AIDS Research and Human Retroviruses, 18(16), 1167–1173.

    PubMed  Google Scholar 

  • Blaak, H., van't Wout, A. B., Brouwer, M., Hooibrink, B., Hovenkamp, E., & Schuitemaker, H. (2000). In vivo HIV-1 infection of CD45RA(+)CD4(+) T cells is established primarily by syncytium-inducing variants and correlates with the rate of CD4(+) T cell decline. Proceedings of the National Academy of Sciences of the USA, 97(3), 1269–1274.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taï Forest: Behavioural ecology and evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Brenchley, J. M., Silvestri, G., & Douek, D. C. (2010). Nonprogressive and progressive primate immunodeficiency lentivirus infections. Immunity, 32(6), 737–742.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Broussard, S. R., Staprans, S. I., White, R., Whitehead, E. M., Feinberg, M. B., & Allan, J. S. (2001). Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. Journal of Virology, 75(5), 2262–2275.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chahroudi, A., Meeker, T., Lawson, B., Ratcliffe, S., Else, J., & Silvestri, G. (2011). Mother-to-infant transmission of simian immunodeficiency virus is rare in sooty mangabeys and is associated with low viremia. Journal of Virology, 85(12), 5757–5763.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Charleston, M. A., & Robertson, D. L. (2002). Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Systematic Biology, 51(3), 528–535.

    PubMed  CAS  Google Scholar 

  • Chen, Z., Kwon, D., Jin, Z., Monard, S., Telfer, P., Jones, M. S., et al. (1998). Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. Journal of Experimental Medicine, 188(11), 2057–2065.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chen, Z., Telfer, P., Gettie, A., Reed, P., Zhang, L., Ho, D. D., 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. Journal of Virology, 70(6), 3617–3627.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chiu, Y. L., & Greene, W. C. (2009). APOBEC3G: An intracellular centurion. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1517), 689–703.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Compton, A. A., & Emerman, M. (2013). Convergence and divergence in the evolution of the APOBEC3G-Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLoS Pathogens, 9(1), e1003135.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Corbet, S., Muller-Trutwin, M. C., Versmisse, P., Delarue, S., Ayouba, A., Lewis, J., et al. (2000). env sequences of simian immunodeficiency viruses from chimpanzees in Cameroon are strongly related to those of human immunodeficiency virus group N from the same geographic area. Journal of Virology, 74(1), 529–534.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Curlin, M. E., Zioni, R., Hawes, S. E., Liu, Y., Deng, W., Gottlieb, G. S., et al. (2010). HIV-1 envelope subregion length variation during disease progression. PLoS Pathogens, 6(12), e1001228.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Damond, F., Worobey, M., Campa, P., Farfara, I., Colin, G., Matheron, S., et al. (2004). Identification of a highly divergent HIV type 2 and proposal for a change in HIV type 2 classification. AIDS Research and Human Retroviruses, 20(6), 666–672.

    PubMed  CAS  Google Scholar 

  • D’arc, M., Ayouba, A., Esteban, A., Etienne, L., Locatelli, S., Aghokeng, A., et al. (2013). Gorillas in southwest Cameroon are the reservoir of HIV-1 group P ancestors. Paper presented at the Conference on Retroviruses and Opportunistic Infections (CROI), Atlanta, GA.

  • de Groot, N. G., Heijmans, C. M., de Groot, N., Otting, N., de Vos-Rouweller, A. J., Remarque, E. J., et al. (2008). Pinpointing a selective sweep to the chimpanzee MHC class I region by comparative genomics. Molecular Ecology, 17(8), 2074–2088.

    PubMed  Google Scholar 

  • de Silva, T. I., Cotten, M., & Rowland-Jones, S. L. (2008). HIV-2: The forgotten AIDS virus. Trends in Microbiology, 16(12), 588–595.

    PubMed  Google Scholar 

  • Diop, O. M., Gueye, A., Ayouba, A., Nerrienet, E., Corbet, S., Mauclere, P., et al. (2002). Simian immunodeficiency viruses and the origin of HIVs (2nd ed.). Dordrecht, The Netherlands: Kluwer Academic/Plenum Press.

    Google Scholar 

  • Diop, O. M., Gueye, A., Dias-Tavares, M., Kornfeld, C., Faye, A., Ave, P., et al. (2000). High levels of viral replication during primary simian immunodeficiency virus SIVagm infection are rapidly and strongly controlled in African green monkeys. Journal of Virology, 74(16), 7538–7547.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Djoko, C. F., Wolfe, N. D., Aghokeng, A. F., Lebreton, M., Liegeois, F., Tamoufe, U., et al. (2012). Failure to detect simian immunodeficiency virus infection in a large Cameroonian cohort with high non-human primate exposure. Ecohealth, 9(1), 17–23.

    PubMed  Google Scholar 

  • Etienne, L., Hahn, B. H., Sharp, P. M., Matsen, F. A., & Emerman, M. (2013). Gene loss and adaptation to hominids underlie the ancient origin of HIV-1. Cell Host & Microbe, 14(1), 85–92.

    CAS  Google Scholar 

  • Etienne, L., Locatelli, S., Ayouba, A., Esteban, A., Butel, C., Liegeois, F., et al. (2012). Noninvasive follow-up of simian immunodeficiency virus infection in wild-living nonhabituated western lowland gorillas in Cameroon. Journal of Virology, 86(18), 9760–9772.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Etienne, L., Nerrienet, E., LeBreton, M., Bibila, G. T., Foupouapouognigni, Y., Rousset, D., 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.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fouchet, D., Verrier, D., Ngoubangoye, B., Souquiere, S., Makuwa, M., Kazanji, M., et al. (2012). Natural simian immunodeficiency virus transmission in mandrills: A family affair? Proceedings of the Royal Society of London B: Biological Sciences, 279(1742), 3426–3435.

    Google Scholar 

  • Gaddis, N. C., Sheehy, A. M., Ahmad, K. M., Swanson, C. M., Bishop, K. N., Beer, B. E., et al. (2004). Further investigation of simian immunodeficiency virus Vif function in human cells. Journal of Virology, 78(21), 12041–12046.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., et al. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature, 397(6718), 436–441.

    PubMed  CAS  Google Scholar 

  • Georges-Courbot, M. C., Lu, C. Y., Makuwa, M., Telfer, P., Onanga, R., Dubreuil, G., et al. (1998). Natural infection of a household pet red-capped mangabey (Cercocebus torquatus torquatus) with a new simian immunodeficiency virus. Journal of Virology, 72(1), 600–608.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Gifford, R. J. (2012). Viral evolution in deep time: Lentiviruses and mammals. Trends in Genetics, 28(2), 89–100.

    PubMed  CAS  Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Groves, C. (2001). Primate taxonomy. Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Gurtler, L. G., Hauser, P. H., Eberle, J., von Brunn, A., Knapp, S., Zekeng, L., et al. (1994). A new subtype of human immunodeficiency virus type 1 (MVP-5180) from Cameroon. Journal of Virology, 68(3), 1581–1585.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hahn, B. H., Shaw, G. M., De Cock, K. M., & Sharp, P. M. (2000). AIDS as a zoonosis: Scientific and public health implications. Science, 287(5453), 607–614.

    PubMed  CAS  Google Scholar 

  • Hamel, D. J., Sankale, J. L., Eisen, G., Meloni, S. T., Mullins, C., Gueye-Ndiaye, A., et al. (2007). Twenty years of prospective molecular epidemiology in Senegal: Changes in HIV diversity. AIDS Research and Human Retroviruses, 23(10), 1189–1196.

    PubMed  CAS  Google Scholar 

  • Harris, R. S., Bishop, K. N., Sheehy, A. M., Craig, H. M., Petersen-Mahrt, S. K., Watt, I. N., et al. (2003). DNA deamination mediates innate immunity to retroviral infection. Cell, 113(6), 803–809.

    PubMed  CAS  Google Scholar 

  • Heeney, J. L., Rutjens, E., Verschoor, E. J., Niphuis, H., ten Haaft, P., Rouse, S., et al. (2006). Transmission of simian immunodeficiency virus SIVcpz and the evolution of infection in the presence and absence of concurrent human immunodeficiency virus type 1 infection in chimpanzees. Journal of Virology, 80(14), 7208–7218.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hirsch, V. M., Dapolito, G., McGann, C., Olmsted, R. A., Purcell, R. H., & Johnson, P. R. (1989a). Molecular cloning of SIV from sooty mangabey monkeys. Journal of Medical Primatology, 18(3–4), 279–285.

    PubMed  CAS  Google Scholar 

  • Hirsch, V. M., Olmsted, R. A., Murphey-Corb, M., Purcell, R. H., & Johnson, P. R. (1989b). An African primate lentivirus (SIVsm) closely related to HIV-2. Nature, 339(6223), 389–392.

    PubMed  CAS  Google Scholar 

  • Hrecka, K., Hao, C., Gierszewska, M., Swanson, S. K., Kesik-Brodacka, M., Srivastava, S., et al. (2011). Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature, 474(7353), 658–661.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hu, J., Switzer, W. M., Foley, B. T., Robertson, D. L., Goeken, R. M., Korber, B. T., et al. (2003). Characterization and comparison of recombinant simian immunodeficiency virus from drill (Mandrillus leucophaeus) and mandrill (Mandrillus sphinx) isolates. Journal of Virology, 77(8), 4867–4880.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hvilsom, C., Carlsen, F., Siegismund, H. R., Corbet, S., Nerrienet, E., & Fomsgaard, A. (2008). Genetic subspecies diversity of the chimpanzee CD4 virus-receptor gene. Genomics, 92(5), 322–328.

    PubMed  CAS  Google Scholar 

  • Jia, B., Serra-Moreno, R., Neidermyer, W., Rahmberg, A., Mackey, J., Fofana, I. B., et al. (2009). Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathogens, 5(5), e1000429.

    PubMed Central  PubMed  Google Scholar 

  • Jin, M. J., Hui, H., Robertson, D. L., Muller, M. C., Barre-Sinoussi, F., Hirsch, V. M., et al. (1994). Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO Journal, 13(12), 2935–2947.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Jouvenet, N., Neil, S. J., Zhadina, M., Zang, T., Kratovac, Z., Lee, Y., et al. (2009). Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. Journal of Virology, 83(4), 1837–1844.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Katzourakis, A., Gifford, R. J., Tristem, M., Gilbert, M. T., & Pybus, O. G. (2009). Macroevolution of complex retroviruses. Science, 325(5947), 1512.

    PubMed  CAS  Google Scholar 

  • Keele, B. F., Jones, J. H., Terio, K. A., Estes, J. D., Rudicell, R. S., Wilson, M. L., et al. (2009). Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature, 460(7254), 515–519.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Keele, B. F., Van Heuverswyn, F., Li, Y., Bailes, E., Takehisa, J., Santiago, M. L., et al. (2006). Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science, 313(5786), 523–526.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kestens, L., Vingerhoets, J., Peeters, M., Vanham, G., Vereecken, C., Penne, G., et al. (1995). Phenotypic and functional parameters of cellular immunity in a chimpanzee with a naturally acquired simian immunodeficiency virus infection. Journal of Infectious Diseases, 172(4), 957–963.

    PubMed  CAS  Google Scholar 

  • King, A. M. Q., Adams, M. J., Carstens, E. B., & Lefkowitz, E. J. (2012). Virus taxonomy: Classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses (1st ed.). San Diego: Elsevier Academic Press.

    Google Scholar 

  • Kingdon, J. (1997). The Kingdon field guide to African mammals. London: Academic Press.

    Google Scholar 

  • Kirchhoff, F. (2009). Is the high virulence of HIV-1 an unfortunate coincidence of primate lentiviral evolution? Nature Reviews Microbiology, 7(6), 467–476.

    PubMed  CAS  Google Scholar 

  • Kirchhoff, F. (2010). Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host & Microbe, 8(1), 55–67.

    CAS  Google Scholar 

  • Kirchhoff, F., Schindler, M., Specht, A., Arhel, N., & Munch, J. (2008). Role of Nef in primate lentiviral immunopathogenesis. Cellular and Molecular Life Sciences, 65(17), 2621–2636.

    PubMed  CAS  Google Scholar 

  • Korber, B., Muldoon, M., Theiler, J., Gao, F., Gupta, R., Lapedes, A., et al. (2000). Timing the ancestor of the HIV-1 pandemic strains. Science, 288(5472), 1789–1796.

    PubMed  CAS  Google Scholar 

  • Kornfeld, C., Ploquin, M. J., Pandrea, I., Faye, A., Onanga, R., Apetrei, C., et al. (2005). Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. Journal of Clinical Investigation, 115(4), 1082–1091.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kratovac, Z., Virgen, C. A., Bibollet-Ruche, F., Hahn, B. H., Bieniasz, P. D., & Hatziioannou, T. (2008). Primate lentivirus capsid sensitivity to TRIM5 proteins. Journal of Virology, 82(13), 6772–6777.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Krupp, A., McCarthy, K. R., Ooms, M., Letko, M., Morgan, J. S., Simon, V., et al. (2013). APOBEC3G polymorphism as a selective barrier to cross-species transmission and emergence of pathogenic SIV and AIDS in a primate host. PLoS Pathogens, 9(10), e1003641.

    PubMed Central  PubMed  Google Scholar 

  • Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Segeral, E., et al. (2011). SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature, 474(7353), 654–657.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lasky, L. A., Nakamura, G., Smith, D. H., Fennie, C., Shimasaki, C., Patzer, E., et al. (1987). Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell, 50(6), 975–985.

    PubMed  CAS  Google Scholar 

  • Leendertz, F. H., Zirkel, F., Couacy-Hymann, E., Ellerbrok, H., Morozov, V. A., Pauli, G., et al. (2008). Interspecies transmission of simian foamy virus in a natural predator-prey system. Journal of Virology, 82(15), 7741–7744.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Leendertz, S. A., Junglen, S., Hedemann, C., Goffe, A., Calvignac, S., Boesch, C., et al. (2010). High prevalence, coinfection rate, and genetic diversity of retroviruses in wild red colobus monkeys (Piliocolobus badius badius) in Tai National Park, Cote d'Ivoire. Journal of Virology, 84(15), 7427–7436.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Leendertz, S. A., Locatelli, S., Boesch, C., Kucherer, C., Formenty, P., Liegeois, F., 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 Microbiology, 11(1), 24.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lemey, P., Pybus, O. G., Wang, B., Saksena, N. K., Salemi, M., & Vandamme, A. M. (2003). Tracing the origin and history of the HIV-2 epidemic. Proceedings of the National Academy of Sciences of the USA, 100(11), 6588–6592.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Le Tortorec, A., & Neil, S. J. (2009). Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. Journal of Virology, 83(22), 11966–11978.

    PubMed Central  PubMed  Google Scholar 

  • Levy, J. A. (2007). HIV and the pathogenesis of AIDS (3rd ed.). Washington, DC: ASM Press.

    Google Scholar 

  • Li, Y., Ndjango, J. B., Learn, G. H., Ramirez, M. A., Keele, B. F., Bibollet-Ruche, F., et al. (2012). Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. Journal of Virology, 86(19), 10776–10791.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lin, Y. L., Mettling, C., Portales, P., Reynes, J., Clot, J., & Corbeau, P. (2002). Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proceedings of the National Academy of Scienes of the USA, 99(24), 15590–15595.

    CAS  Google Scholar 

  • Locatelli, S., Liegeois, F., Lafay, B., Roeder, A. D., Bruford, M. W., Formenty, P., et al. (2008). Prevalence and genetic diversity of simian immunodeficiency virus infection in wild-living red colobus monkeys (Piliocolobus badius badius) from the Tai forest, Cote d'Ivoire SIVwrc in wild-living western red colobus monkeys. Infection, Genetics and Evolution, 8(1), 1–14.

    PubMed  CAS  Google Scholar 

  • Locatelli, S., & Peeters, M. (2012). Cross-species transmission of simian retroviruses: How and why they could lead to the emergence of new diseases in the human population. AIDS, 26(6), 659–673.

    PubMed  Google Scholar 

  • Loehle, C. (1995). Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326–335.

    Google Scholar 

  • Lowenstine, L. J., Lerche, N. W., Yee, J. L., Uyeda, A., Jennings, M. B., Munn, R. J., et al. (1992). Evidence for a lentiviral etiology in an epizootic of immune deficiency and lymphoma in stump-tailed macaques (Macaca arctoides). Journal of Medical Primatology, 21(1), 1–14.

    PubMed  CAS  Google Scholar 

  • Ma, D., Jasinska, A., Kristoff, J., Grobler, J. P., Turner, T., Jung, Y., et al. (2013). SIVagm infection in wild African green monkeys from South Africa: Epidemiology, natural history, and evolutionary considerations. PLoS Pathogens, 9(1), e1003011.

    PubMed Central  PubMed  CAS  Google Scholar 

  • MacFie, T. S., Nerrienet, E., de Groot, N. G., Bontrop, R. E., & Mundy, N. I. (2009). Patterns of diversity in HIV-related loci among subspecies of chimpanzee: Concordance at CCR5 and differences at CXCR4 and CX3CR1. Molecular Biology and Evolution, 26(4), 719–727.

    PubMed  CAS  Google Scholar 

  • MacNeil, A., Sarr, A. D., Sankale, J. L., Meloni, S. T., Mboup, S., & Kanki, P. (2007). Direct evidence of lower viral replication rates in vivo in human immunodeficiency virus type 2 (HIV-2) infection than in HIV-1 infection. Journal of Virology, 81(10), 5325–5330.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Malim, M. H. (2009). APOBEC proteins and intrinsic resistance to HIV-1 infection. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1517), 675–687.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Malim, M. H., & Emerman, M. (2008). HIV-1 accessory proteins—ensuring viral survival in a hostile environment. Cell Host & Microbe, 3(6), 388–398.

    CAS  Google Scholar 

  • Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L., & Trono, D. (2003). Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature, 424(6944), 99–103.

    PubMed  CAS  Google Scholar 

  • Marx, P. A., Li, Y., Lerche, N. W., Sutjipto, S., Gettie, A., Yee, J. A., et al. (1991). Isolation of a simian immunodeficiency virus related to human immunodeficiency virus type 2 from a west African pet sooty mangabey. Journal of Virology, 65(8), 4480–4485.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Mauclere, P., Loussert-Ajaka, I., Damond, F., Fagot, P., Souquieres, S., Monny Lobe, M., et al. (1997). Serological and virological characterization of HIV-1 group O infection in Cameroon. AIDS, 11(4), 445–453.

    PubMed  CAS  Google Scholar 

  • McGraw, W. S., Zuberbühler, K., & Noë, R. (2007). Monkeys of the Taï Forest: An African primate community. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • McGrew, W. C., Marchant, L. F., & Nishida, T. (1996). Great ape societies. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Milush, J. M., Mir, K. D., Sundaravaradan, V., Gordon, S. N., Engram, J., Cano, C. A., et al. (2011). Lack of clinical AIDS in SIV-infected sooty mangabeys with significant CD4+ T cell loss is associated with double-negative T cells. Journal of Clinical Investigation, 121(3), 1102–1110.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Moore, J. P., Kitchen, S. G., Pugach, P., & Zack, J. A. (2004). The CCR5 and CXCR4 coreceptors—central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Research and Human Retroviruses, 20(1), 111–126.

    PubMed  CAS  Google Scholar 

  • Morse, S. S., Mazet, J. A., Woolhouse, M., Parrish, C. R., Carroll, D., Karesh, W. B., et al. (2012). Prediction and prevention of the next pandemic zoonosis. Lancet, 380(9857), 1956–1965.

    PubMed Central  PubMed  Google Scholar 

  • Muller-Trutwin, M. C., Corbet, S., Tavares, M. D., Herve, V. M., Nerrienet, E., Georges-Courbot, M. C., et al. (1996). The evolutionary rate of nonpathogenic simian immunodeficiency virus (SIVagm) is in agreement with a rapid and continuous replication in vivo. Virology, 223(1), 89–102.

    PubMed  CAS  Google Scholar 

  • Mwaengo, D. M., & Novembre, F. J. (1998). Molecular cloning and characterization of viruses isolated from chimpanzees with pathogenic human immunodeficiency virus type 1 infections. Journal of Virology, 72(11), 8976–8987.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Neel, C., Etienne, L., Li, Y., Takehisa, J., Rudicell, R. S., Bass, I. N., et al. (2010). Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. Journal of Virology, 84(3), 1464–1476.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Neil, S., & Bieniasz, P. (2009). Human immunodeficiency virus, restriction factors, and interferon. Journal of Interferon and Cytokine Research, 29(9), 569–580.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Neil, S., Zang, T., & Bieniasz, P. (2008). Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature, 451(7177), 425–430.

    PubMed  CAS  Google Scholar 

  • Nerrienet, E., Amouretti, X., Muller-Trutwin, M. C., Poaty-Mavoungou, V., Bedjebaga, I., Nguyen, H. T., 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 Research and Human Retroviruses, 14(9), 785–796.

    PubMed  CAS  Google Scholar 

  • Nishida, T., Zamma, K., Matsusaka, T., Inaba, A., & McGrew, W. C. (2010). Chimpanzee behavior in the wild: An audio-visual encyclopedia. Tokyo: Springer Science+Business Media.

    Google Scholar 

  • Novembre, F. J., de Rosayro, J., Nidtha, S., O'Neil, S. P., Gibson, T. R., Evans-Strickfaden, T., et al. (2001). Rapid CD4(+) T-cell loss induced by human immunodeficiency virus type 1(NC) in uninfected and previously infected chimpanzees. Journal of Virology, 75(3), 1533–1539.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Nunn, C. L., Gittleman, J. L., & Antonovics, J. (2000). Promiscuity and the primate immune system. Science, 290(5494), 1168–1170.

    PubMed  CAS  Google Scholar 

  • Nyambi, P. N., Lewi, P., Peeters, M., Janssens, W., Heyndrickx, L., Fransen, K., et al. (1997). Study of the dynamics of neutralization escape mutants in a chimpanzee naturally infected with the simian immunodeficiency virus SIVcpz-ant. Journal of Virology, 71(3), 2320–2330.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Nygren, A., Bergman, T., Matthews, T., Jornvall, H., & Wigzell, H. (1988). 95- and 25-kDa fragments of the human immunodeficiency virus envelope glycoprotein gp120 bind to the CD4 receptor. Proceedings of the National Academy of Sciences of the USA, 85(17), 6543–6546.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Oates, J. F., Groves, C. P., & Jenkins, P. D. (2009). The type locality of Pan troglodytes vellerosus (Gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates, 50(1), 78–80.

    PubMed  Google Scholar 

  • O'Donovan, D., Ariyoshi, K., Milligan, P., Ota, M., Yamuah, L., Sarge-Njie, R., et al. (2000). Maternal plasma viral RNA levels determine marked differences in mother-to-child transmission rates of HIV-1 and HIV-2 in The Gambia. MRC/Gambia Government/University College London Medical School working group on mother-child transmission of HIV. AIDS, 14(4), 441–448.

    PubMed  Google Scholar 

  • Onanga, R., Kornfeld, C., Pandrea, I., Estaquier, J., Souquiere, S., Rouquet, P., 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. Journal of Virology, 76(20), 10256–10263.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Onanga, R., Souquiere, S., Makuwa, M., Mouinga-Ondeme, A., Simon, F., Apetrei, C., et al. (2006). Primary simian immunodeficiency virus SIVmnd-2 infection in mandrills (Mandrillus sphinx). Journal of Virology, 80(7), 3301–3309.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ondoa, P., Davis, D., Kestens, L., Vereecken, C., Garcia Ribas, S., Fransen, K., et al. (2002). In vitro susceptibility to infection with SIVcpz and HIV-1 is lower in chimpanzee than in human peripheral blood mononuclear cells. Journal of Medical Virology, 67(3), 301–311.

    PubMed  CAS  Google Scholar 

  • Ondoa, P., Davis, D., Willems, B., Heyndrickx, L., Kestens, L., van der Berg, I., et al. (2001). Genetic variability of the V1 and V2 env domains of SIVcpz-ant and neutralization pattern of plasma viruses in a chimpanzee infected naturally. Journal of Medical Virology, 65(4), 765–776.

    PubMed  CAS  Google Scholar 

  • O'Neil, S. P., Novembre, F. J., Hill, A. B., Suwyn, C., Hart, C. E., Evans-Strickfaden, T., et al. (2000). Progressive infection in a subset of HIV-1-positive chimpanzees. Journal of Infectious Diseases, 182(4), 1051–1062.

    PubMed  Google Scholar 

  • Paiardini, M., Cervasi, B., Reyes-Aviles, E., Micci, L., Ortiz, A. M., Chahroudi, A., et al. (2011). Low levels of SIV infection in sooty mangabey central memory CD T cells are associated with limited CCR5 expression. Nature Medicine, 17(7), 830–836.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Paiardini, M., Pandrea, I., Apetrei, C., & Silvestri, G. (2009). Lessons learned from the natural hosts of HIV-related viruses. Annual Review of Medicine, 60, 485–495.

    PubMed  CAS  Google Scholar 

  • Pandrea, I., & Apetrei, C. (2010). Where the wild things are: Pathogenesis of SIV infection in African nonhuman primate hosts. Current HIV/AIDS Reports, 7(1), 28–36.

    PubMed Central  PubMed  Google Scholar 

  • Pandrea, I., Apetrei, C., Gordon, S., Barbercheck, J., Dufour, J., Bohm, R., et al. (2007). Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood, 109(3), 1069–1076.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pandrea, I., Kornfeld, C., Ploquin, M. J., Apetrei, C., Faye, A., Rouquet, P., et al. (2005). Impact of viral factors on very early in vivo replication profiles in simian immunodeficiency virus SIVagm-infected African green monkeys. Journal of Virology, 79(10), 6249–6259.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pandrea, I., Onanga, R., Rouquet, P., Bourry, O., Ngari, P., Wickings, E. J., et al. (2001). Chronic SIV infection ultimately causes immunodeficiency in African non-human primates. AIDS, 15(18), 2461–2462.

    PubMed  CAS  Google Scholar 

  • Pandrea, I., Onanga, R., Souquiere, S., Mouinga-Ondeme, A., Bourry, O., Makuwa, M., et al. (2008a). Paucity of CD4+ CCR5+ T cells may prevent transmission of simian immunodeficiency virus in natural nonhuman primate hosts by breast-feeding. Journal of Virology, 82(11), 5501–5509.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pandrea, I., Parrish, N. F., Raehtz, K., Gaufin, T., Barbian, H. J., Ma, D., et al. (2012). Mucosal simian immunodeficiency virus transmission in African green monkeys: Susceptibility to infection is proportional to target cell availability at mucosal sites. Journal of Virology, 86(8), 4158–4168.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pandrea, I., Ribeiro, R. M., Gautam, R., Gaufin, T., Pattison, M., Barnes, M., et al. (2008b). SIVagm dynamics in African green monkeys. Journal of Virology, 82(7), 3713–24.

  • Pandrea, I., Sodora, D. L., Silvestri, G., & Apetrei, C. (2008c). Into the wild: Simian immunodeficiency virus (SIV) infection in natural hosts. Trends in Immunology, 29(9), 419–428.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Peeters, M., Courgnaud, V., Abela, B., Auzel, P., Pourrut, X., Bibollet-Ruche, F., et al. (2002). Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerging Infectious Diseases, 8(5), 451–457.

    PubMed Central  PubMed  Google Scholar 

  • Peeters, M., Fransen, K., Delaporte, E., Van den Haesevelde, M., Gershy-Damet, G. M., Kestens, L., et al. (1992). Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. AIDS, 6(5), 447–451.

    PubMed  CAS  Google Scholar 

  • Peeters, M., Gueye, A., Mboup, S., Bibollet-Ruche, F., Ekaza, E., Mulanga, C., et al. (1997). Geographical distribution of HIV-1 group O viruses in Africa. AIDS, 11(4), 493–498.

    PubMed  CAS  Google Scholar 

  • Peeters, M., Janssens, W., Fransen, K., Brandful, J., Heyndrickx, L., Koffi, K., et al. (1994). Isolation of simian immunodeficiency viruses from two sooty mangabeys in Cote d'Ivoire: Virological and genetic characterization and relationship to other HIV type 2 and SIVsm/mac strains. AIDS Research and Human Retroviruses, 10(10), 1289–1294.

    PubMed  CAS  Google Scholar 

  • Phillips-Conroy, J. E., Jolly, C. J., Petros, B., Allan, J. S., & Desrosiers, R. C. (1994). Sexual transmission of SIVagm in wild grivet monkeys. Journal of Medical Primatology, 23(1), 1–7.

    PubMed  CAS  Google Scholar 

  • Planelles, V., & Benichou, S. (2009). Vpr and its interactions with cellular proteins. Current Topics in Microbiology and Immunology, 339, 177–200.

    PubMed  CAS  Google Scholar 

  • Plantier, J. C., Leoz, M., Dickerson, J. E., De Oliveira, F., Cordonnier, F., Lemée, V., et al. (2009). A new human immunodeficiency virus derived from gorillas. Nature Medicine, 15(8), 871–872.

    PubMed  CAS  Google Scholar 

  • Popper, S. J., Sarr, A. D., Gueye-Ndiaye, A., Mboup, S., Essex, M. E., & Kanki, P. J. (2000). Low plasma human immunodeficiency virus type 2 viral load is independent of proviral load: Low virus production in vivo. Journal of Virology, 74(3), 1554–1557.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Prince, A. M., Brotman, B., Lee, D. H., Andrus, L., Valinsky, J., & Marx, P. (2002). Lack of evidence for HIV type 1–related SIVcpz infection in captive and wild chimpanzees (Pan troglodytes verus) in West Africa. AIDS Research and Human Retroviruses, 18(9), 657–660.

    PubMed  Google Scholar 

  • Raugi, D. N., Gottlieb, G. S., Sow, P. S., Toure, M., Sall, F., Gaye, A., et al. (2013). HIV-1 outcompetes HIV-2 in dually infected Senegalese individuals with low CD4(+) cell counts. AIDS, 27(15), 2441–2450.

    PubMed  Google Scholar 

  • Rey-Cuille, M. A., Berthier, J. L., Bomsel-Demontoy, M. C., Chaduc, Y., Montagnier, L., Hovanessian, A. G., et al. (1998). Simian immunodeficiency virus replicates to high levels in sooty mangabeys without inducing disease. Journal of Virology, 72(5), 3872–3886.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Reynolds, V. (2005). The chimpanzees of the Budongo Forest: Ecology, behaviour, and conservation. Oxford: Oxford University Press.

    Google Scholar 

  • Rieg, G., Yeaman, M., Lail, A. E., Donfield, S. M., Gomperts, E. D., & Daar, E. S. (2007). Platelet count is associated with plasma HIV type 1 RNA and disease progression. AIDS Research and Human Retroviruses, 23(10), 1257–1261.

    PubMed  CAS  Google Scholar 

  • Robbins, M. M., Sicotte, P., & Stewart, K. J. (2005). Mountain gorillas: Three decades of research at Karisoke. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Rudicell, R. S., Holland Jones, J., Wroblewski, E. E., Learn, G. H., Li, Y., Robertson, J. D., et al. (2010). Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathogens, 6(9), e1001116.

    PubMed Central  PubMed  Google Scholar 

  • Rudicell, R. S., Piel, A. K., Stewart, F., Moore, D. L., Learn, G. H., Li, Y., et al. (2011). High prevalence of simian immunodeficiency virus infection in a community of savanna chimpanzees. Journal of Virology, 85(19), 9918–9928.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Rushmore, J., Caillaud, D., Matamba, L., Stumpf, R. M., Borgatti, S. P., & Altizer, S. (2013). Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. Journal of Animal Ecology. doi:10.1111/1365-2656.12088.

    PubMed  Google Scholar 

  • Samson, M., Libert, F., Doranz, B. J., Rucker, J., Liesnard, C., Farber, C. M., et al. (1996). Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature, 382(6593), 722–725.

    PubMed  CAS  Google Scholar 

  • Santiago, M. L., Range, F., Keele, B. F., Li, Y., Bailes, E., Bibollet-Ruche, F., 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. Journal of Virology, 79(19), 12515–12527.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Santiago, M. L., Rodenburg, C. M., Kamenya, S., Bibollet-Ruche, F., Gao, F., Bailes, E., et al. (2002). SIVcpz in wild chimpanzees. Science, 295(5554), 465.

    PubMed  CAS  Google Scholar 

  • Sauter, D., Schindler, M., Specht, A., Landford, W. N., Munch, J., Kim, K. A., 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(5), 409–421.

    CAS  Google Scholar 

  • Sauter, D., Specht, A., & Kirchhoff, F. (2010). Tetherin: Holding on and letting go. Cell, 141(3), 392–398.

    PubMed  CAS  Google Scholar 

  • Sauter, D., Vogl, M., & Kirchhoff, F. (2011). Ancient origin of a deletion in human BST2/Tetherin that confers protection against viral zoonoses. Human Mutation, 32(11), 1243–1245.

    PubMed  CAS  Google Scholar 

  • Sawyer, S. L., Wu, L. I., Emerman, M., & Malik, H. S. (2005). Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proceedigs of the National Academy of Sciences of the USA, 102(8), 2832–2837.

    CAS  Google Scholar 

  • Scaradavou, A. (2002). HIV-related thrombocytopenia. Blood Reviews, 16(1), 73–76.

    PubMed  CAS  Google Scholar 

  • Schindler, M., Munch, J., Kutsch, O., Li, H., Santiago, M. L., Bibollet-Ruche, F., et al. (2006). Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell, 125(6), 1055–1067.

    PubMed  CAS  Google Scholar 

  • Shankarappa, R., Margolick, J. B., Gange, S. J., Rodrigo, A. G., Upchurch, D., Farzadegan, H., et al. (1999). Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. Journal of Virology, 73(12), 10489–10502.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sharp, P. M., Bailes, E., Gao, F., Beer, B. E., Hirsch, V. M., & Hahn, B. H. (2000). Origins and evolution of AIDS viruses: Estimating the time-scale. Biochemical Society Transactions, 28(2), 275–282.

    PubMed  CAS  Google Scholar 

  • Sheehy, A. M., Gaddis, N. C., Choi, J. D., & Malim, M. H. (2002). Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature, 418(6898), 646–650.

    PubMed  CAS  Google Scholar 

  • Silvestri, G. (2005). Naturally SIV-infected sooty mangabeys: Are we closer to understanding why they do not develop AIDS? Journal of Medical Primatology, 34(5–6), 243–252.

    PubMed  CAS  Google Scholar 

  • Silvestri, G., Fedanov, A., Germon, S., Kozyr, N., Kaiser, W. J., Garber, D. A., et al. (2005). Divergent host responses during primary simian immunodeficiency virus SIVsm infection of natural sooty mangabey and nonnatural rhesus macaque hosts. Journal of Virology, 79(7), 4043–4054.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Silvestri, G., Paiardini, M., Pandrea, I., Lederman, M. M., & Sodora, D. L. (2007). Understanding the benign nature of SIV infection in natural hosts. Journal of Clinical Investigation, 117(11), 3148–3154.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Silvestri, G., Sodora, D. L., Koup, R. A., Paiardini, M., O'Neil, S. P., McClure, H. M., et al. (2003). Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity, 18(3), 441–452.

    PubMed  CAS  Google Scholar 

  • Simon, F., Mauclere, P., Roques, P., Loussert-Ajaka, I., Muller-Trutwin, M. C., Saragosti, S., et al. (1998). Identification of a new human immunodeficiency virus type 1 distinct from group M and group O. Nature Medicine, 4(9), 1032–1037.

    PubMed  CAS  Google Scholar 

  • Sodora, D. L., & Ross, T. M. (2009). Simian immunodeficiency virus pathogenesis. Current HIV Research, 7(1), 1.

    PubMed  CAS  Google Scholar 

  • Souquiere, S., Bibollet-Ruche, F., Robertson, D. L., Makuwa, M., Apetrei, C., Onanga, R., et al. (2001). Wild Mandrillus sphinx are carriers of two types of lentivirus. Journal of Virology, 75(15), 7086–7096.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Stremlau, M., Owens, C. M., Perron, M. J., Kiessling, M., Autissier, P., & Sodroski, J. (2004). The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature, 427(6977), 848–853.

    PubMed  CAS  Google Scholar 

  • Sundaravaradan, V., Saleem, R., Micci, L., Gasper, M. A., Ortiz, A. M., Else, J., et al. (2013). Multifunctional double-negative T cells in sooty mangabeys mediate T-helper functions irrespective of SIV infection. PLoS Pathogens, 9(6), e1003441.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Takehisa, J., Kraus, M. H., Ayouba, A., Bailes, E., Van Heuverswyn, F., Decker, J. M., et al. (2009). Origin and biology of simian immunodeficiency virus in wild-living western gorillas. Journal of Virology, 83(4), 1635–1648.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Takehisa, J., Kraus, M. H., Decker, J. M., Li, Y., Keele, B. F., Bibollet-Ruche, F., et al. (2007). Generation of infectious molecular clones of simian immunodeficiency virus from fecal consensus sequences of wild chimpanzees. Journal of Virology, 81(14), 7463–7475.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Taylor, A. B., & Goldsmith, M. L. (2003). Gorilla biology: A multidisciplinary perspective. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Thrall, P. H., Antonovics, J., & Dobson, A. P. (2000). Sexually transmitted diseases in polygynous mating systems: Prevalence and impact on reproductive success. Proceedings of the Royal Society of London B: Biological Sciences, 267(1452), 1555–1563.

    CAS  Google Scholar 

  • 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 Research and Human Retroviruses, 8(1), 97–100.

    PubMed  CAS  Google Scholar 

  • UNAIDS (2010). UNAIDS report on the global AIDS epidemic 2010. Available at: www.unaids.org/globalreport/global_report.htm (Accessed February 20, 2013).

  • Vallari, A., Holzmayer, V., Harris, B., Yamaguchi, J., Ngansop, C., Makamche, F., et al. (2011). Confirmation of putative HIV-1 group P in Cameroon. Journal of Virology, 85(3), 1403–1407.

    PubMed Central  PubMed  CAS  Google Scholar 

  • van der Loeff, M. F., Awasana, A. A., Sarge-Njie, R., van der Sande, M., Jaye, A., Sabally, S., et al. (2006). Sixteen years of HIV surveillance in a West African research clinic reveals divergent epidemic trends of HIV-1 and HIV-2. International Journal of Epidemiology, 35(5), 1322–1328.

    PubMed  Google Scholar 

  • van de Woude, S., & Apetrei, C. (2006). Going wild: Lessons from naturally occurring T-lymphotropic lentiviruses. Clinical Microbiology Reviews, 19(4), 728–762.

    Google Scholar 

  • Van Heuverswyn, F., Li, Y., Bailes, E., Neel, C., Lafay, B., Keele, B. F., et al. (2007). Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology, 368(1), 155–171.

    PubMed  Google Scholar 

  • Van Heuverswyn, F., Li, Y., Neel, C., Bailes, E., Keele, B. F., Liu, W., et al. (2006). Human immunodeficiency viruses: SIV infection in wild gorillas. Nature, 444(7116), 164.

    PubMed  Google Scholar 

  • Veazey, R. S., & Lackner, A. A. (2004). Getting to the guts of HIV pathogenesis. Journal of Experimental Medicine, 200(6), 697–700.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Villinger, F., Folks, T. M., Lauro, S., Powell, J. D., Sundstrom, J. B., Mayne, A., et al. (1996). Immunological and virological studies of natural SIV infection of disease-resistant nonhuman primates. Immunology Letters, 51(1–2), 59–68.

    PubMed  CAS  Google Scholar 

  • Vinton, C., Klatt, N. R., Harris, L. D., Briant, J. A., Sanders-Beer, B. E., Herbert, R., et al. (2011). CD4-like immunological function by CD4-T cells in multiple natural hosts of simian immunodeficiency virus. Journal of Virology, 85(17), 8702–8708.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wain, L. V., Bailes, E., Bibollet-Ruche, F., Decker, J. M., Keele, B. F., Van Heuverswyn, F., et al. (2007). Adaptation of HIV-1 to its human host. Molecular Biology and Evolution, 24(8), 1853–1860.

    PubMed  CAS  Google Scholar 

  • Watts, D. P., Mitani, J. C., & Sherrow, H. M. (2002). New cases of inter-community infanticide by male chimpanzees at Ngogo, Kibale National Park, Uganda. Primates, 43(4), 263–270.

    PubMed  Google Scholar 

  • Weiss, R. A., & Heeney, J. L. (2009). Infectious diseases: An ill wind for wild chimps? Nature, 460(7254), 470–471.

    PubMed  CAS  Google Scholar 

  • Wertheim, J. O., & Kosakovsky Pond, S. L. (2011). Purifying selection can obscure the ancient age of viral lineages. Molecular Biology and Evolution, 28(12), 3355–3365.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wertheim, J. O., & Worobey, M. (2007). A challenge to the ancient origin of SIVagm based on African green monkey mitochondrial genomes. PLoS Pathogens, 3(7), 866–873.

    CAS  Google Scholar 

  • Wertheim, J. O., & Worobey, M. (2009). Dating the age of the SIV lineages that gave rise to HIV-1 and HIV-2. PLoS Computational Biology, 5(5), e1000377.

    PubMed Central  PubMed  Google Scholar 

  • Wolfe, N. D., Dunavan, C. P., & Diamond, J. (2007). Origins of major human infectious diseases. Nature, 447(7142), 279–283.

    PubMed  CAS  Google Scholar 

  • Wooding, S., Stone, A. C., Dunn, D. M., Mummidi, S., Jorde, L. B., Weiss, R. K., et al. (2005). Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5. American Journal of Human Genetics, 76(2), 291–301.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Worobey, M., Gemmel, M., Teuwen, D. E., Haselkorn, T., Kunstman, K., Bunce, M., et al. (2008). Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature, 455(7213), 661–664.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Worobey, M., Santiago, M. L., Keele, B. F., Ndjango, J. B., Joy, J. B., Labama, B. L., et al. (2004). Origin of AIDS: Contaminated polio vaccine theory refuted. Nature, 428(6985), 820.

    PubMed  CAS  Google Scholar 

  • Worobey, M., Telfer, P., Souquiere, S., Hunter, M., Coleman, C. A., Metzger, M. J., et al. (2010). Island biogeography reveals the deep history of SIV. Science, 329(5998), 1487.

    PubMed  CAS  Google Scholar 

  • Wrangham, R., McGrew, W. C., de Waal, F. B. M., & Heltne, P. G. (1996). Chimpanzee cultures. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Yant, L. J., Friedrich, T. C., Johnson, R. C., May, G. E., Maness, N. J., Enz, A. M., et al. (2006). The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. Journal of Virology, 80(10), 5074–5077.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang, F., Wilson, S. J., Landford, W. C., Virgen, B., Gregory, D., Johnson, M. C., et al. (2009). Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host & Microbe, 6(1), 54–67.

    CAS  Google Scholar 

  • Zhang, Y., Lou, B., Lal, R. B., Gettie, A., Marx, P. A., & Moore, J. P. (2000). Use of inhibitors to evaluate coreceptor usage by simian and simian/human immunodeficiency viruses and human immunodeficiency virus type 2 in primary cells. Journal of Virology, 74(15), 6893–6910.

    PubMed Central  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the journal editor Joanna M. Setchell and two anonymous reviewers for their useful comments on earlier versions of the manuscript. The authors declare to have no conflicts of interest.

Author information

Authors and Affiliations

  1. UMI 233, TransVIHMI, Institut de Recherche pour le Développement and University of Montpellier 1, 34394, Montpellier, Cedex 5, France

    Sabrina Locatelli

  2. Department of Biological Sciences, University at Albany-State University of New York, Albany, New York, 12222, USA

    Kurt A. McKean, Paul R. Sesink Clee & Mary Katherine Gonder

  3. Department of Biology, Drexel University, Philadelphia, Pennsylvania, 19104, USA

    Paul R. Sesink Clee & Mary Katherine Gonder

Authors
  1. Sabrina Locatelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kurt A. McKean
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul R. Sesink Clee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mary Katherine Gonder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sabrina Locatelli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Locatelli, S., McKean, K.A., Sesink Clee, P.R. et al. The Evolution of Resistance to Simian Immunodeficiency Virus (SIV): A Review. Int J Primatol 35, 349–375 (2014). https://doi.org/10.1007/s10764-014-9763-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-014-9763-7

Keywords

Search

Navigation