1887

Abstract

The mandrill () is naturally infected by two types of simian immunodeficiency virus (SIV): SIVmnd types 1 and 2. Both of these viruses cause long-term, non-progressive infections in their natural host despite high plasma viral loads. This study assessed the susceptibility of rhesus macaques to infection by these two types of SIVmnd and compared the virological and basic immunological characteristics of the resulting infections with those observed in natural infection in mandrills. Whilst both SIVmnd types induced similar levels of virus replication during acute infection in both mandrills and macaques, they produced a more pronounced CD4 T-cell depletion in rhesus macaques that persisted longer during the initial stage of infection. Pro-inflammatory cytokine responses were also induced at higher levels in rhesus macaques early in the infection. During the chronic phase of infection in mandrills, which in this case was followed for up to 2 years after infection, high levels of chronic virus replication did not induce significant changes in CD4 or CD8 T-cell counts. In rhesus macaques, the overall chronic virus replication level was lower than in mandrills. At the end of the follow-up period, although the viral loads of SIVmnd-1 and SIVmnd-2 were relatively similar in rhesus macaques, only SIVmnd-1-infected rhesus macaques showed significant CD4 T-cell depletion, in the context of higher levels of CD4 and CD8 T-cell activation, compared with SIVmnd-infected mandrills. The demonstration of the ability of both SIVmnd types to induce persistent infections in rhesus macaques calls for a careful assessment of the potential of these two viruses to emerge as new human pathogens.

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2009-02-01
2019-11-23
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References

  1. Apetrei, C., Robertson, D. L. & Marx, P. A. ( 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.[CrossRef]
    [Google Scholar]
  2. Apetrei, C., Kaur, A., Lerche, N. W., Metzger, M., Pandrea, I., Hardcastle, J., Falkenstein, S., Bohm, R., Koehler, J. & other authors ( 2005; ). Molecular epidemiology of simian immunodeficiency virus SIVsm in U.S. primate centers unravels the origin of SIVmac and SIVstm. J Virol 79, 8991–9005.[CrossRef]
    [Google Scholar]
  3. Apetrei, C., Lerche, N. W., Pandrea, I., Gormus, B., Silvestri, G., Kaur, A., Robertson, D. L., Hardcastle, J., Lackner, A. A. & Marx, P. A. ( 2006; ). Kuru experiments triggered the emergence of pathogenic SIVmac. AIDS 20, 317–321.[CrossRef]
    [Google Scholar]
  4. Bailes, E., Gao, F., Bibollet-Ruche, F., Courgnaud, V., Peeters, M., Marx, P. A., Hahn, B. H. & Sharp, P. M. ( 2003; ). Hybrid origin of SIV in chimpanzees. Science 300, 1713 [CrossRef]
    [Google Scholar]
  5. Beer, B. E., Bailes, E., Goeken, R., Dapolito, G., Coulibaly, C., Norley, S. G., Kurth, R., Gautier, J. P., Gautier-Hion, A. & other authors ( 1999; ). Simian immunodeficiency virus (SIV) from sun-tailed monkeys (Cercopithecus solatus): evidence for host-dependent evolution of SIV within the C. lhoesti superspecies. J Virol 73, 7734–7744.
    [Google Scholar]
  6. Beer, B. E., Brown, C. R., Whitted, S., Goldstein, S., Goeken, R., Plishka, R., Buckler-White, A. & Hirsch, V. M. ( 2005; ). Immunodeficiency in the absence of high viral load in pig-tailed macaques infected with simian immunodeficiency virus SIVsun or SIVlhoest. J Virol 79, 14044–14056.[CrossRef]
    [Google Scholar]
  7. Brown, C. R., Czapiga, M., Kabat, J., Dang, Q., Ourmanov, I., Nishimura, Y., Martin, M. A. & Hirsch, V. M. ( 2007; ). Unique pathology in simian immunodeficiency virus-infected rapid progressor macaques is consistent with a pathogenesis distinct from that of classical AIDS. J Virol 81, 5594–5606.[CrossRef]
    [Google Scholar]
  8. Chakrabarti, L. A. ( 2004; ). The paradox of simian immunodeficiency virus infection in sooty mangabeys: active viral replication without disease progression. Front Biosci 9, 521–539.[CrossRef]
    [Google Scholar]
  9. Chen, Z., Gettie, A., Ho, D. D. & Marx, P. A. ( 1998; ). Primary SIVsm isolates use the CCR5 coreceptor from sooty mangabeys naturally infected in West Africa: a comparison of coreceptor usage of primary SIVsm, HIV-2, and SIVmac. Virology 246, 113–124.[CrossRef]
    [Google Scholar]
  10. Clewley, J. P., Lewis, J. C., Brown, D. W. & Gadsby, E. L. ( 1998; ). A novel simian immunodeficiency virus (SIVdrl) pol sequence from the drill monkey, Mandrillus leucophaeus. J Virol 72, 10305–10309.
    [Google Scholar]
  11. Dunham, R., Pagliardini, P., Gordon, S., Sumpter, B., Engram, J., Moanna, A., Paiardini, M., Mandl, J. N., Lawson, B. & other authors ( 2006; ). The AIDS resistance of naturally SIV-infected sooty mangabeys is independent of cellular immunity to the virus. Blood 108, 209–217.[CrossRef]
    [Google Scholar]
  12. Estaquier, J., Idziorek, T., de Bels, F., Barré-Sinoussi, F., Hurtrel, B., Aubertin, A. M., Venet, A., Mehtali, M., Muchmore, E. & other authors ( 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.[CrossRef]
    [Google Scholar]
  13. Fultz, P. N. ( 1991; ). Replication of an acutely lethal simian immunodeficiency virus activates and induces proliferation of lymphocytes. J Virol 65, 4902–4909.
    [Google Scholar]
  14. Gordon, S. N., Klatt, N. R., Bosinger, S. E., Brenchley, J. M.,, Milush, J. M., Engram, J. C., Dunham, R. M., Paiardini, M., Klucking, S. & other authors ( 2007; ). Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol 179, 3026–3034.[CrossRef]
    [Google Scholar]
  15. Gormus, B. J., Martin, L. N. & Baskin, G. B. ( 2004; ). A brief history of the discovery of natural simian immunodeficiency virus (SIV) infections in captive sooty mangabey monkeys. Front Biosci 9, 216–224.[CrossRef]
    [Google Scholar]
  16. 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, 607–614.[CrossRef]
    [Google Scholar]
  17. Harris, E. E. & Disotell, T. R. ( 1998; ). Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primates: Papionini). Mol Biol Evol 15, 892–900.[CrossRef]
    [Google Scholar]
  18. Hirsch, V. M. ( 2004; ). What can natural infection of African monkeys with simian immunodeficiency virus tell us about the pathogenesis of AIDS? AIDS Rev 6, 40–53.
    [Google Scholar]
  19. Hirsch, V. M. & Johnson, P. R. ( 1994; ). Pathogenic diversity of simian immunodeficiency viruses. Virus Res 32, 183–203.[CrossRef]
    [Google Scholar]
  20. Hirsch, V. M., Olmsted, R. A., Murphey-Corb, M., Purcell, R. H. & Johnson, P. R. ( 1989; ). An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339, 389–392.[CrossRef]
    [Google Scholar]
  21. Hirsch, V. M., Dapolito, G. A., Goldstein, S., McClure, H., Emau, P., Fultz, P. N., Isahakia, M., Lenroot, R., Myers, G. & Johnson, P. R. ( 1993; ). A distinct African lentivirus from Sykes' monkeys. J Virol 67, 1517–1528.
    [Google Scholar]
  22. Hirsch, V. M., Dapolito, G., Johnson, P. R., Elkins, W. R., London, W. T., Montali, R. J., Goldstein, S. & Brown, C. ( 1995; ). Induction of AIDS by simian immunodeficiency virus from an African green monkey: species-specific variation in pathogenicity correlates with the extent of in vivo replication. J Virol 69, 955–967.
    [Google Scholar]
  23. Hirsch, V. M., Campbell, B. J., Bailes, E., Goeken, R., Brown, C., Elkins, W. R., Axthelm, M., Murphey-Corb, M. & Sharp, P. M. ( 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.
    [Google Scholar]
  24. Hu, J., Switzer, W. M., Foley, B. T., Robertson, D. L., Goeken, R. M., Korber, B. T., Hirsch, V. M. & Beer, B. E. ( 2003; ). Characterization and comparison of recombinant simian immunodeficiency virus from drill (Mandrillus leucophaeus) and mandrill (Mandrillus sphinx) isolates. J Virol 77, 4867–4880.[CrossRef]
    [Google Scholar]
  25. Kaur, A., Grant, R. M., Means, R. E., McClure, H., Feinberg, M. & Johnson, R. P. ( 1998; ). Diverse host responses and outcomes following simian immunodeficiency virus SIVmac239 infection in sooty mangabeys and rhesus macaques. J Virol 72, 9597–9611.
    [Google Scholar]
  26. Keele, B. F., Van Heuverswyn, F., Li, Y., Bailes, E., Takehisa, J., Santiago, M. L., Bibollet-Ruche, F., Chen, Y., Wain, L. V. & other authors ( 2006; ). Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313, 523–526.[CrossRef]
    [Google Scholar]
  27. Kornfeld, C., Ploquin, M. J., Pandrea, I., Faye, A., Onanga, R., Apetrei,, C., Poaty-Mavoungou, V., Rouquet, P., Estaquier, J. & other authors ( 2005; ). Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 115, 1082–1091.[CrossRef]
    [Google Scholar]
  28. Ling, B., Apetrei, C., Pandrea, I., Veazey, R. S., Lackner, A. A., Gormus, B. & Marx, P. A. ( 2004; ). Classic AIDS in a sooty mangabey after an 18-year natural infection. J Virol 78, 8902–8908.[CrossRef]
    [Google Scholar]
  29. Mansfield, K. G., Lerch, N. W., Gardner, M. B. & Lackner, A. A. ( 1995; ). Origins of simian immunodeficiency virus infection in macaques at the New England Regional Primate Research Center. J Med Primatol 24, 116–122.[CrossRef]
    [Google Scholar]
  30. Marx, P. A., Li, Y., Lerche, N. W., Sutjipto, S., Gettie, A., Yee, J. A., Brotman, B. H., Prince, A. M., Hanson, A. & other authors ( 1991; ). Isolation of a simian immunodeficiency virus related to human immunodeficiency virus type 2 from a West African pet sooty mangabey. J Virol 65, 4480–4485.
    [Google Scholar]
  31. Marx, P. A., Alcabes, P. G. & Drucker, E. ( 2001; ). Serial human passage of simian immunodeficiency virus by unsterile injections and the emergence of epidemic human immunodeficiency virus in Africa. Philos Trans R Soc Lond B Biol Sci 356, 911–920.[CrossRef]
    [Google Scholar]
  32. McClure, H. M., Anderson, D. C., Fultz, P. N., Ansari, A. A., Lockwood, E. & Brodie, A. ( 1989; ). Spectrum of disease in macaque monkeys chronically infected with SIV/SMM. Vet Immunol Immunopathol 21, 13–24.[CrossRef]
    [Google Scholar]
  33. Muller, M. C. & Barré-Sinoussi, F. ( 2003; ). SIVagm: genetic and biological features associated with replication. Front Biosci 8, d1170–d1185.[CrossRef]
    [Google Scholar]
  34. Murphey-Corb, M., Martin, L. N., Rangan, S. R., Baskin, G. B., Gormus, B. J., Wolf, R. H., Andes, W. A., West, M. & Montelaro, R. C. ( 1986; ). Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature 321, 435–437.[CrossRef]
    [Google Scholar]
  35. Nishimura, Y., Igarashi, T., Buckler-White, A., Buckler, C., Imamichi, H., Goeken, R. M., Lee, W. R., Lafont, B. A., Byrum, R. & other authors ( 2007; ). Loss of naive cells accompanies memory CD4+ T-cell depletion during long-term progression to AIDS in simian immunodeficiency virus-infected macaques. J Virol 81, 893–902.[CrossRef]
    [Google Scholar]
  36. Norley, S., Beer, B., Holzammer, S., zur Megede, J. & Kurth, R. ( 1999; ). Why are the natural hosts of SIV resistant to AIDS? Immunol Lett 66, 47–52.[CrossRef]
    [Google Scholar]
  37. Onanga, R., Kornfeld, C., Pandrea, I., Estaquier, J., Souquière, S., Rouquet, P., Mavoungou, V. P., Bourry, O., M'Boup, S. & other authors ( 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.[CrossRef]
    [Google Scholar]
  38. Onanga, R., SouquiÉre, S., Makuwa, M., Mouinga-Ondeme, A., Simon, F., Apetrei, C. & Roques, P. ( 2006; ). Primary simian immunodeficiency virus SIVmnd-2 infection in mandrills (Mandrillus sphinx). J Virol 80, 3301–3309.[CrossRef]
    [Google Scholar]
  39. Osterhaus, A. D., Pedersen, N., van Amerongen, G., Frankenhuis, M. T., Marthas, M., Reay, E., Rose, T. M., Pamungkas, J. & Bosch, M. L. ( 1999; ). Isolation and partial characterization of a lentivirus from talapoin monkeys (Myopithecus talapoin). Virology 260, 116–124.[CrossRef]
    [Google Scholar]
  40. Pandrea, I., Onanga, R., Rouquet, P., Bourry, O., Ngari, P., Wickings, E. J., Roques, P. & Apetrei, C. ( 2001; ). Chronic SIV infection ultimately causes immunodeficiency in African non-human primates. AIDS 15, 2461–2462.[CrossRef]
    [Google Scholar]
  41. Pandrea, I., Kornfeld, C., Ploquin, M. J., Apetrei, C., Faye, A., Rouquet, P., Roques, P., Simon, F., Barré-Sinoussi, F. & other authors ( 2005; ). Impact of viral factors on very early in vivo replication profiles in simian immunodeficiency virus SIVagm-infected African green monkeys. J Virol 79, 6249–6259.[CrossRef]
    [Google Scholar]
  42. Pandrea, I., Silvestri, G., Onanga, R., Veazey, R. S., Marx, P. A., Hirsch, V. & Apetrei, C. ( 2006; ). Simian immunodeficiency viruses replication dynamics in African non-human primate hosts: common patterns and species-specific differences. J Med Primatol 35, 194–201.[CrossRef]
    [Google Scholar]
  43. Pandrea, I. V., Gautam, R., Ribeiro, R. M., Brenchley, J. M., Butler, I. F., Pattison, M., Rasmussen, T., Marx, P. A., Silvestri, G. & other authors ( 2007; ). Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 179, 3035–3046.[CrossRef]
    [Google Scholar]
  44. Pandrea, I., Onanga, R., SouquiÉre, S., Mouinga-Ondéme, A., Bourry, O., Makuwa, M., Rouquet, P., Silvestri, G., Simon, F. & other authors ( 2008a; ). Paucity of CD4+ CCR5+ T cells may prevent transmission of simian immunodeficiency virus in natural nonhuman primate hosts by breast-feeding. J Virol 82, 5501–5509.[CrossRef]
    [Google Scholar]
  45. Pandrea, I., Ribeiro, R. M., Gautam, R., Gaufin, T., Pattison, M., Barnes, M., Monjure, C., Stoulig, C., Dufour, J. & other authors ( 2008b; ). SIVagm dynamics in African green monkeys. J Virol 82, 3713–3724.[CrossRef]
    [Google Scholar]
  46. Peeters, M., Courgnaud, V., Abela, B., Auzel, P., Pourrut, X., Bibollet-Ruche, F., Loul, S., Liegeois, F., Butel, C. & other authors ( 2002; ). Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg Infect Dis 8, 451–457.[CrossRef]
    [Google Scholar]
  47. Schols, D. & De Clercq, E. ( 1998; ). The simian immunodeficiency virus mnd(GB-1) strain uses CXCR4, not CCR5, as coreceptor for entry in human cells. J Gen Virol 79, 2203–2205.
    [Google Scholar]
  48. Silvestri, G. ( 2005; ). Naturally SIV-infected sooty mangabeys: are we closer to understanding why they do not develop AIDS? J Med Primatol 34, 243–252.[CrossRef]
    [Google Scholar]
  49. Silvestri, G., Sodora, D. L., Koup, R. A., Paiardini, M., O'Neil, S. P., McClure, H. M., Staprans, S. I. & Feinberg, M. B. ( 2003; ). Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18, 441–452.[CrossRef]
    [Google Scholar]
  50. Silvestri, G., Fedanov, A., Germon, S., Kozyr, N., Kaiser, W. J., Garber, D. A., McClure, H., Feinberg, M. B. & Staprans, S. I. ( 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.[CrossRef]
    [Google Scholar]
  51. Simon, F., SouquiÉre, S., Damond, F., Kfutwah, A., Makuwa, M., Leroy, E., Rouquet, P., Berthier, J. L., Rigoulet, J. & other authors ( 2001; ). Synthetic peptide strategy for the detection of and discrimination among highly divergent primate lentiviruses. AIDS Res Hum Retroviruses 17, 937–952.[CrossRef]
    [Google Scholar]
  52. Smith, S. M., Makuwa, M., Lee, F., Gettie, A., Russo, C. & Marx, P. A. ( 1998; ). SIVrcm infection of macaques. J Med Primatol 27, 94–98.[CrossRef]
    [Google Scholar]
  53. SouquiÉre, S., Bibollet-Ruche, F., Robertson, D. L., Makuwa, M., Apetrei, C., Onanga, R., Kornfeld, C., Plantier, J. C., Gao, F. & other authors ( 2001; ). Wild Mandrillus sphinx are carriers of two types of lentivirus. J Virol 75, 7086–7096.[CrossRef]
    [Google Scholar]
  54. Takehisa, J., Harada, Y., Ndembi, N., Mboudjeka, I., Taniguchi, Y., Ngansop, C., Kuate, S., Zekeng, L., Ibuki, K. & other authors ( 2001; ). Natural infection of wild-born mandrills (Mandrillus sphinx) with two different types of simian immunodeficiency virus. AIDS Res Hum Retroviruses 17, 1143–1154.[CrossRef]
    [Google Scholar]
  55. Telfer, P. T., SouquiÉre, S., Clifford, S. L., Abernethy, K. A., Bruford, M. W., Disotell, T. R., Sterner, K. N., Roques, P., Marx, P. A. & Wickings, E. J. ( 2003; ). Molecular evidence for deep phylogenetic divergence in Mandrillus sphinx. Mol Ecol 12, 2019–2024.[CrossRef]
    [Google Scholar]
  56. 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.[CrossRef]
    [Google Scholar]
  57. Tsujimoto, H., Cooper, R. W., Kodama, T., Fukasawa, M., Miura, T., Ohta, Y., Ishikawa, K., Nakai, M., Frost, E. & other authors ( 1988; ). Isolation and characterization of simian immunodeficiency virus from mandrills in Africa and its relationship to other human and simian immunodeficiency viruses. J Virol 62, 4044–4050.
    [Google Scholar]
  58. Tsujimoto, H., Hasegawa, A., Maki, N., Fukasawa, M., Miura, T., Speidel, S., Cooper, R. W., Moriyama, E. N., Gojobori, T. & Hayami, M. ( 1989; ). Sequence of a novel simian immunodeficiency virus from a wild-caught African mandrill. Nature 341, 539–541.[CrossRef]
    [Google Scholar]
  59. VandeWoude, S. & Apetrei, C. ( 2006; ). Going wild: lessons from naturally occurring T-lymphotropic lentiviruses. Clin Microbiol Rev 19, 728–762.[CrossRef]
    [Google Scholar]
  60. Wang, Z., Metcalf, B., Ribeiro, R. M., McClure, H. & Kaur, A. ( 2006; ). Th-1-type cytotoxic CD8+ T-lymphocyte responses to simian immunodeficiency virus (SIV) are a consistent feature of natural SIV infection in sooty mangabeys. J Virol 80, 2771–2783.[CrossRef]
    [Google Scholar]
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