Species-specific diversity among simian immunodeficiency viruses from African green monkeys. (original) (raw)

J Virol. 1991 Jun; 65(6): 2816–2828.

Department of Virology and Immunology, Southwest Foundation for Biomedical Research, San Antonio, Texas 78228-0147.

Abstract

The prevalence, natural history, and genetic characteristics of simian immunodeficiency virus (SIV) infections in most feral African monkey species are presently unknown, yet this information is essential to elucidate their origin and relationship to other simian and human immunodeficiency viruses. In this study, a combination of classical and molecular approaches were used to identify and characterize SIV isolates from West African green monkeys (Cercopithecus sabaeus) (SIVagm isolates). Four SIVagm viruses from wild-caught West African green monkeys were isolated and analyzed biologically and molecularly. Amplification, cloning, and sequencing of a 279-bp polymerase fragment directly from uncultured peripheral blood mononuclear cells was facilitated by the use of nested polymerase chain reaction. The results indicated that West African green monkeys are naturally infected with SIVs which are closely related to East African SIVagm isolates. However, structural, antigenic, and genetic differences were observed which strongly suggest that the West African green monkey viruses comprise a phylogenetically distinct subgroup of SIVagm. These findings support our previous hypothesis that SIVagm viruses may have evolved and diverged coincident with the evolution and divergence of their African green monkey host. In addition, this study describes a polymerase chain reaction-based approach that allows the identification and molecular analysis of divergent SIV strains directly from primary monkey tissue. This approach, which does not depend on virus isolation methods, should facilitate future studies aimed at elucidating the origins and natural history of SIVs in feral African green monkey populations.

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Albert J, Fenyö EM. Simple, sensitive, and specific detection of human immunodeficiency virus type 1 in clinical specimens by polymerase chain reaction with nested primers. J Clin Microbiol. 1990 Jul;28(7):1560–1564. [PMC free article] [PubMed] [Google Scholar]
Allan JS, Coligan JE, Lee TH, Barin F, Kanki PJ, M'Boup S, McLane MF, Groopman JE, Essex M. Immunogenic nature of a Pol gene product of HTLV-III/LAV. Blood. 1987 Jan;69(1):331–333. [PubMed] [Google Scholar]
Allan JS, Kanda P, Kennedy RC, Cobb EK, Anthony M, Eichberg JW. Isolation and characterization of simian immunodeficiency viruses from two subspecies of African green monkeys. AIDS Res Hum Retroviruses. 1990 Mar;6(3):275–285. [PubMed] [Google Scholar]
Allan JS, Strauss J, Buck DW. Enhancement of SIV infection with soluble receptor molecules. Science. 1990 Mar 2;247(4946):1084–1088. [PubMed] [Google Scholar]
Baier M, Werner A, Cichutek K, Garber C, Müller C, Kraus G, Ferdinand FJ, Hartung S, Papas TS, Kurth R. Molecularly cloned simian immunodeficiency virus SIVagm3 is highly divergent from other SIVagm isolates and is biologically active in vitro and in vivo. J Virol. 1989 Dec;63(12):5119–5123. [PMC free article] [PubMed] [Google Scholar]
Chakrabarti L, Guyader M, Alizon M, Daniel MD, Desrosiers RC, Tiollais P, Sonigo P. Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature. 1987 Aug 6;328(6130):543–547. [PubMed] [Google Scholar]
Daniel MD, Letvin NL, King NW, Kannagi M, Sehgal PK, Hunt RD, Kanki PJ, Essex M, Desrosiers RC. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science. 1985 Jun 7;228(4704):1201–1204. [PubMed] [Google Scholar]
Daniel MD, Letvin NL, Sehgal PK, Hunsmann G, Schmidt DK, King NW, Desrosiers RC. Long-term persistent infection of macaque monkeys with the simian immunodeficiency virus. J Gen Virol. 1987 Dec;68(Pt 12):3183–3189. [PubMed] [Google Scholar]
Daniel MD, Li Y, Naidu YM, Durda PJ, Schmidt DK, Troup CD, Silva DP, MacKey JJ, Kestler HW, 3rd, Sehgal PK, et al. Simian immunodeficiency virus from African green monkeys. J Virol. 1988 Nov;62(11):4123–4128. [PMC free article] [PubMed] [Google Scholar]
Desrosiers RC. HIV-1 origins. A finger on the missing link. Nature. 1990 May 24;345(6273):288–289. [PubMed] [Google Scholar]
Dewhurst S, Embretson JE, Anderson DC, Mullins JI, Fultz PN. Sequence analysis and acute pathogenicity of molecularly cloned SIVSMM-PBj14. Nature. 1990 Jun 14;345(6276):636–640. [PubMed] [Google Scholar]
Doolittle RF. Immunodeficiency viruses: the simian-human connection. Nature. 1989 Jun 1;339(6223):338–339. [PubMed] [Google Scholar]
Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. [PubMed] [Google Scholar]
Fenyö EM, Morfeldt-Månson L, Chiodi F, Lind B, von Gegerfelt A, Albert J, Olausson E, Asjö B. Distinct replicative and cytopathic characteristics of human immunodeficiency virus isolates. J Virol. 1988 Nov;62(11):4414–4419. [PMC free article] [PubMed] [Google Scholar]
Fukasawa M, Miura T, Hasegawa A, Morikawa S, Tsujimoto H, Miki K, Kitamura T, Hayami M. Sequence of simian immunodeficiency virus from African green monkey, a new member of the HIV/SIV group. Nature. 1988 Jun 2;333(6172):457–461. [PubMed] [Google Scholar]
Fultz PN, McClure HM, Anderson DC, Swenson RB, Anand R, Srinivasan A. Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabey monkeys (Cercocebus atys). Proc Natl Acad Sci U S A. 1986 Jul;83(14):5286–5290. [PMC free article] [PubMed] [Google Scholar]
Gartner S, Markovits P, Markovitz DM, Kaplan MH, Gallo RC, Popovic M. The role of mononuclear phagocytes in HTLV-III/LAV infection. Science. 1986 Jul 11;233(4760):215–219. [PubMed] [Google Scholar]
Gazdar AF, Carney DN, Bunn PA, Russell EK, Jaffe ES, Schechter GP, Guccion JG. Mitogen requirements for the in vitro propagation of cutaneous T-cell lymphomas. Blood. 1980 Mar;55(3):409–417. [PubMed] [Google Scholar]
Gendelman HE, Baca LM, Husayni H, Turpin JA, Skillman D, Kalter DC, Orenstein JM, Hoover DL, Meltzer MS. Macrophage-HIV interaction: viral isolation and target cell tropism. AIDS. 1990 Mar;4(3):221–228. [PubMed] [Google Scholar]
Gurgo C, Guo HG, Franchini G, Aldovini A, Collalti E, Farrell K, Wong-Staal F, Gallo RC, Reitz MS., Jr Envelope sequences of two new United States HIV-1 isolates. Virology. 1988 Jun;164(2):531–536. [PubMed] [Google Scholar]
Guyader M, Emerman M, Sonigo P, Clavel F, Montagnier L, Alizon M. Genome organization and transactivation of the human immunodeficiency virus type 2. Nature. 1987 Apr 16;326(6114):662–669. [PubMed] [Google Scholar]
Hendry RM, Wells MA, Phelan MA, Schneider AL, Epstein JS, Quinnan GV. Antibodies to simian immunodeficiency virus in African green monkeys in Africa in 1957-62. Lancet. 1986 Aug 23;2(8504):455–455. [PubMed] [Google Scholar]
Hirsch VM, Edmondson P, Murphey-Corb M, Arbeille B, Johnson PR, Mullins JI. SIV adaptation to human cells. Nature. 1989 Oct 19;341(6243):573–574. [PubMed] [Google Scholar]
Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature. 1989 Jun 1;339(6223):389–392. [PubMed] [Google Scholar]
Hoxie JA, Haggarty BS, Bonser SE, Rackowski JL, Shan H, Kanki PJ. Biological characterization of a simian immunodeficiency virus-like retrovirus (HTLV-IV): evidence for CD4-associated molecules required for infection. J Virol. 1988 Aug;62(8):2557–2568. [PMC free article] [PubMed] [Google Scholar]
Huet T, Cheynier R, Meyerhans A, Roelants G, Wain-Hobson S. Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature. 1990 May 24;345(6273):356–359. [PubMed] [Google Scholar]
Johnson PR, Fomsgaard A, Allan J, Gravell M, London WT, Olmsted RA, Hirsch VM. Simian immunodeficiency viruses from African green monkeys display unusual genetic diversity. J Virol. 1990 Mar;64(3):1086–1092. [PMC free article] [PubMed] [Google Scholar]
Johnson PR, Gravell M, Allan J, Goldstein S, Olmsted RA, Dapolito G, McGann C, London WT, Purcell RH, Hirsch VM. Genetic diversity among simian immunodeficiency virus isolates from African green monkeys. J Med Primatol. 1989;18(3-4):271–277. [PubMed] [Google Scholar]
Kanki PJ, Kurth R, Becker W, Dreesman G, McLane MF, Essex M. Antibodies to simian T-lymphotropic retrovirus type III in African green monkeys and recognition of STLV-III viral proteins by AIDS and related sera. Lancet. 1985 Jun 8;1(8441):1330–1332. [PubMed] [Google Scholar]
Kikukawa R, Koyanagi Y, Harada S, Kobayashi N, Hatanaka M, Yamamoto N. Differential susceptibility to the acquired immunodeficiency syndrome retrovirus in cloned cells of human leukemic T-cell line Molt-4. J Virol. 1986 Mar;57(3):1159–1162. [PMC free article] [PubMed] [Google Scholar]
Koenig S, Hirsch VM, Olmsted RA, Powell D, Maury W, Rabson A, Fauci AS, Purcell RH, Johnson PR. Selective infection of human CD4+ cells by simian immunodeficiency virus: productive infection associated with envelope glycoprotein-induced fusion. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2443–2447. [PMC free article] [PubMed] [Google Scholar]
Kong LI, Lee SW, Kappes JC, Parkin JS, Decker D, Hoxie JA, Hahn BH, Shaw GM. West African HIV-2-related human retrovirus with attenuated cytopathicity. Science. 1988 Jun 10;240(4858):1525–1529. [PubMed] [Google Scholar]
Kornfeld H, Riedel N, Viglianti GA, Hirsch V, Mullins JI. Cloning of HTLV-4 and its relation to simian and human immunodeficiency viruses. Nature. 1987 Apr 9;326(6113):610–613. [PubMed] [Google Scholar]
Kraus G, Werner A, Baier M, Binniger D, Ferdinand FJ, Norley S, Kurth R. Isolation of human immunodeficiency virus-related simian immunodeficiency viruses from African green monkeys. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2892–2896. [PMC free article] [PubMed] [Google Scholar]
Kumar P, Hui HX, Kappes JC, Haggarty BS, Hoxie JA, Arya SK, Shaw GM, Hahn BH. Molecular characterization of an attenuated human immunodeficiency virus type 2 isolate. J Virol. 1990 Feb;64(2):890–901. [PMC free article] [PubMed] [Google Scholar]
Letvin NL, Daniel MD, Sehgal PK, Desrosiers RC, Hunt RD, Waldron LM, MacKey JJ, Schmidt DK, Chalifoux LV, King NW. Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science. 1985 Oct 4;230(4721):71–73. [PubMed] [Google Scholar]
Li Y, Naidu YM, Daniel MD, Desrosiers RC. Extensive genetic variability of simian immunodeficiency virus from African green monkeys. J Virol. 1989 Apr;63(4):1800–1802. [PMC free article] [PubMed] [Google Scholar]
Lowenstine LJ, Pedersen NC, Higgins J, Pallis KC, Uyeda A, Marx P, Lerche NW, Munn RJ, Gardner MB. 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. 1986 Oct 15;38(4):563–574. [PubMed] [Google Scholar]
Meyerhans A, Cheynier R, Albert J, Seth M, Kwok S, Sninsky J, Morfeldt-Månson L, Asjö B, Wain-Hobson S. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell. 1989 Sep 8;58(5):901–910. [PubMed] [Google Scholar]
Mullis KB, Faloona FA. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. [PubMed] [Google Scholar]
Murphey-Corb M, Martin LN, Rangan SR, Baskin GB, Gormus BJ, Wolf RH, Andes WA, West M, Montelaro RC. Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature. 1986 May 22;321(6068):435–437. [PubMed] [Google Scholar]
Ohta Y, Masuda T, Tsujimoto H, Ishikawa K, Kodama T, Morikawa S, Nakai M, Honjo S, Hayami M. Isolation of simian immunodeficiency virus from African green monkeys and seroepidemiologic survey of the virus in various non-human primates. Int J Cancer. 1988 Jan 15;41(1):115–122. [PubMed] [Google Scholar]
Peeters M, Honoré C, Huet T, Bedjabaga L, Ossari S, Bussi P, Cooper RW, Delaporte E. Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS. 1989 Oct;3(10):625–630. [PubMed] [Google Scholar]
Popovic M, Sarngadharan MG, Read E, Gallo RC. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science. 1984 May 4;224(4648):497–500. [PubMed] [Google Scholar]
Querat G, Audoly G, Sonigo P, Vigne R. Nucleotide sequence analysis of SA-OMVV, a visna-related ovine lentivirus: phylogenetic history of lentiviruses. Virology. 1990 Apr;175(2):434–447. [PubMed] [Google Scholar]
Ratner L, Fisher A, Jagodzinski LL, Mitsuya H, Liou RS, Gallo RC, Wong-Staal F. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res Hum Retroviruses. 1987 Spring;3(1):57–69. [PubMed] [Google Scholar]
Salter RD, Howell DN, Cresswell P. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics. 1985;21(3):235–246. [PubMed] [Google Scholar]
Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed] [Google Scholar]
Sharp PM, Li WH. Understanding the origins of AIDS viruses. Nature. 1988 Nov 24;336(6197):315–315. [PubMed] [Google Scholar]
Simmonds P, Balfe P, Peutherer JF, Ludlam CA, Bishop JO, Brown AJ. Human immunodeficiency virus-infected individuals contain provirus in small numbers of peripheral mononuclear cells and at low copy numbers. J Virol. 1990 Feb;64(2):864–872. [PMC free article] [PubMed] [Google Scholar]
Smith SD, Shatsky M, Cohen PS, Warnke R, Link MP, Glader BE. Monoclonal antibody and enzymatic profiles of human malignant T-lymphoid cells and derived cell lines. Cancer Res. 1984 Dec;44(12 Pt 1):5657–5660. [PubMed] [Google Scholar]
Smith TF, Srinivasan A, Schochetman G, Marcus M, Myers G. The phylogenetic history of immunodeficiency viruses. Nature. 1988 Jun 9;333(6173):573–575. [PubMed] [Google Scholar]
Tsujimoto H, Cooper RW, Kodama T, Fukasawa M, Miura T, Ohta Y, Ishikawa K, Nakai M, Frost E, Roelants GE, et al. Isolation and characterization of simian immunodeficiency virus from mandrills in Africa and its relationship to other human and simian immunodeficiency viruses. J Virol. 1988 Nov;62(11):4044–4050. [PMC free article] [PubMed] [Google Scholar]
Tsujimoto H, Hasegawa A, Maki N, Fukasawa M, Miura T, Speidel S, Cooper RW, Moriyama EN, Gojobori T, Hayami M. Sequence of a novel simian immunodeficiency virus from a wild-caught African mandrill. Nature. 1989 Oct 12;341(6242):539–541. [PubMed] [Google Scholar]

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