Isolation and characterization of a syncytium-inducing, macrophage/T-cell line-tropic human immunodeficiency virus type 1 isolate that readily infects chimpanzee cells in vitro and in vivo

Journal of Virology

Volumn 69, Issue 7, 1995, Pages 4453-4462

  Shibata, Riri ^a   Hoggan, M David ^a   Broscius, Christine ^a   Englund, George ^a   Theodore, Theodore S ^a   Buckler White, Alicia ^b   Arthur, Larry O ^c   Israel, Zimra ^d   Schultz, Alan ^a   Lane, H Clifford ^a   Martin, Malcolm A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUSION; CHIMPANZEE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTIVITY; VIRUS PATHOGENESIS; VIRUS STRAIN;

EID: 0029018332     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.69.7.4453-4462.1995     Document Type: Article

References (69)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Alizon, M., S. Wain-Hobson, L. Montagnier, and P. Sonigo. 1986. Genetic variability of the AIDS virus: nucleotide sequence analysis of two isolates from African patients. Cell 46:63-74.
3. Alter, H. J., J. W. Eichberg, H. Masur, W. C. Saxinger, R. Gallo, A. M. Macher, H. C. Lane, and A. S. Fauci. 1984. Transmission of HTLV-III infection from human plasma to chimpanzees: an animal model for AIDS. Science 226:549-552.
4. Arthur, L. O., J. W. Bess, Jr., D. J. Waters, S. W. Pyle, J. C. Kelliher, P. L. Nara, K. Krohn, W. G. Robey, A. J. Langlois, R. C. Gallo, and P. J. Fischinger. 1989. Challenge of chimpanzees (Pan troglodytes) immunized with human immunodeficiency virus envelope glycoprotein gp120. J. Virol. 63: 5046-5053.
5. Barre-Sinoussi, F., J. C. Chermann, F. Rey, M. T. Nugeyre, S. Chamaret, J. Gruest, C. Dauguet, C. Axler-Blin, F. Vezinet-Brun, F. Rouzioux, W. Rozenbaum, and L. Montagnier. 1983. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220:868-871.
6. Bear, S. E., P. N. Tsichlis, and R. S. Schwartz. 1980. H-2-mediated resistance to an ecotropic type C retrovirus: localization of controlling genes and ontogenic studies of resistance. Immunogenetics 11:451-465.
7. Broder, C. C., and E. A. Berger. 1993. CD4 molecules with a diversity of mutations encompassing the CDR3 region efficiently support human immunodeficiency virus type 1 envelope glycoprotein-mediated cell fusion. J. Virol. 67:913-926.
8. Buller, R. S., K. Wehrly, J. L. Portis, and B. Chesebro. 1990. Host genes conferring resistance to a central nervous system disease induced by a polytropic recombinant Friend murine retrovirus. J. Virol. 64:493-498.
9. Camerini, D., and B. Seed. 1990. A CD4 domain important for HIV-mediated syncytium formation lies outside the virus binding site. Cell 60:747-754.
10. Castro, B. A., M. Nepomuceno, N. W. Lerche, J. W. Eichberg, and J. A. Levy. 1991. Persistent infection of baboons and rhesus monkeys with different strains of HIV-2. Virology 184:219-226.
11. Castro, B. A., C. M. Walker, J. W. Eichberg, and J. A. Levy. 1991. Suppression of human immunodeficiency virus replication by CD8+ cells from infected and uninfected chimpanzees. Cell. Immunol. 132:246-255.
12. Castro, B. A., C. M. Walker, M. Tateno, C. Cheng-Mayer, R. Heberling, J. W. Eichberg, and J. A. Levy. 1989. Human immunodeficiency virus (HIV) from experimentally infected chimpanzees: isolation and characterization. J. Med. Primatol. 18:337-342.
13. Cheng-Mayer, C., D. Seto, M. Tateno, and J. A. Levy. 1988. Biologic features of HIV-1 that correlate with virulence in the host. Science 240:80-82.
14. Cichutek, K., and S. Norley. 1993. Lack of immune suppression in SIV-infected natural hosts. AIDS 7:S25-S35.
15. Clapham, P. R., R. A. Weiss, A. G. Dalgleish, M. Exley, D. Whitby, and N. Hogg. 1987. Human immunodeficiency virus infection of monocytic and T-lymphocytic cells: receptor modulation and differentiation induced by phorbol ester. Virology 158:44-51.
16. Clark, S. J., M. S. Saag, W. D. Decker, S. Campbell-Hill, J. L. Roberson, P. J. Veldkamp, J. C. Kappes, B. H. Hahn, and G. M. Shaw. 1991. High titers of cytopathic virus in plasma of patients with symptomatic primary HIV-1 infection. N. Engl. J. Med. 324:954-960.
17. Collman, R., J. W. Balliet, S. A. Gregory, H. Friedman, D. L. Kelson, N. Nathanson, and A. Srivivasan. 1992. An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. J. Virol. 66:7517-7521.
18. Conley, A. J. (Merck Research Laboratory). Personal communication.
19. + T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J. Virol. 67:1772-1777.
20. Corbin, A., and M. Sitbon. 1993. Protection against retroviral diseases after vaccination is conferred by interference to superinfection with attenuated murine leukemia viruses. J. Virol. 67:5146-5152.
21. Daar, E. S., T. Moudgil, R. D. Meyer, and D. D. Ho. 1991. Transient high levels of viremia in patients with primary human immunodeficiency virus type 1 infection. N. Engl. J. Med. 324:961-964.
22. Dewar, R. L., H. C. Highbarger, M. D. Sarmiento, J. A. Todd, M. B. Vasudevachari, R. T. Davey, Jr., J. A. Kovacs, N. P. Salzman, H. C. Lane, and M. S. Urdea. 1994. Application of branched DNA signal amplification to monitor human immunodeficiency virus type 1 burden in human plasma. J. Infect. Dis. 170:1172-1179.
23. Francis, D. P., P. M. Feorino, J. R. Broderson, H. M. McClore, J. P. Getchell, C. R. McGrath, B. Swenson, J. S. McDougal, E. L. Palmer, and A. Harrison. 1984. Infection of chimpanzees with lymphadenopathy-associated virus. Lancet ii:1276-1277.
24. Fultz, P. N. 1993. Nonhuman primate models for AIDS. Clin. Infect. Dis. 17:S230-S235.
25. Fultz, P. N., H. M. McClure, D. C. Anderson, and W. M. Switzer. 1989. Identification and biologic characterization of an acutely lethal variant of simian immunodeficiency virus from sooty mangabeys (SIV/SMM). AIDS Res. Hum. Retroviruses 5:397-409.
26. Fultz, P. N., H. M. McClure, R. B. Swenson, and D. C. Anderson. 1989. HIV infection of chimpanzees as a model for testing chemotherapeutics. Intervirology 30(Suppl. 1):51-58.
27. Fultz, P. N., H. M. McClure, R. B. Swenson, C. R. McGrath, A. Brodie, J. P. Getchell, F. C. Jensen, D. C. Anderson, J. R. Broderson, and D. P. Francis. 1986. Persistent infection of chimpanzees with human T-lymphotropic virus type III/lymphadenopathy-associated virus: a potential model for acquired immunodeficiency syndrome. J. Virol. 58:116-124.
28. Fultz, P. N., A. Srinivasan, C. R. Greene, D. Butler, R. B. Swenson, and H. M. McClure. 1987. Superinfection of a chimpanzee with a second strain of human immunodeficiency virus. J. Virol. 61:4026-4029.
29. Gajdusek, D. C., H. L. Amyx, C. J. Gibbs, Jr., D. M. Asher, P. Rodgers-Johnson, L. G. Epstein, P. S. Sarin, R. C. Gallo, A. Maluish, L. O. Arthur, L. Montagnier, and D. Mildvan. 1985. Infection of chimpanzees by human T-lymphotropic retroviruses in brain and other tissues from AIDS patients. Lancet i:55-56.
30. Gajdusek, D. C., H. L. Amyx, C. J. Gibbs, Jr., D. M. Asher, R. T. Yanagihara, P. Rodgers-Johnson, P. W. Brown, P. S. Sarin, R. C. Gallo, A. Maluish, L. O. Arthur, R. V. Gilden, L. Montagnier, J. C. Chermann, F. B. Barre-Sinoussi, D. Mildvan, U. Mathur, and R. Leavitt. 1984. Transmission experiments with human T-lymphotropic retroviruses and human AIDS tissue. Lancet i:1415-1416.
31. Gendelman, H. E., J. M. Orenstein, M. A. Martin, C. Ferrua, R. Mitra, T. Phipps, L. A. Wahl, H. C. Lane, A. S. Fauci, D. S. Burke, D. Skillman, and M. S. Meltzer. 1988. Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-related monocytes. J. Exp. Med. 167:1428-1441.
32. Ghosh, S. K., P. N. Fultz, E. Keddie, M. S. Saag, P. M. Sharp, B. H. Hahn, and G. M. Shaw. 1993. A molecular clone of HIV-1 tropic and cytopathic for human and chimpanzee lymphocytes. Virology 194:858-864.
33. Gibbs, C. J., Jr., R. Peters, M. Gravell, B. K. Johnson, F. C. Jensen, D. J. Carlo, and J. Salk. 1991. Observations after human immunodeficiency virus immunization and challenge of human immunodeficiency virus seropositive and seronegative chimpanzees. Proc. Natl. Acad. Sci. USA 88:3348-3352.
34. Harada, S., Y. Koyanagi, and N. Yamamoto. 1985. Infection of HTLV-III/ LAV in HTLV-1-carrying cells MT-2 and MT-4 and application in a plaque assay. Science 229:563-566.
35. Hirsch, V. M., and P. R. Johnson. 1994. Pathogenic diversity of simian immunodeficiency viruses. Virus Res. 32:183-203.
36. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
37. Johnson, B. K., G. A. Stone, M. S. Godec, D. M. Asher, D. C. Gajdusek, and C. J. Gibbs, Jr. 1993. Long-term observations of human immunodeficiency virus-infected chimpanzees. AIDS Res. Hum. Retroviruses 9:375-378.
38. Klimkait, T., K. Strebel, M. D. Hoggan, M. A. Martin, and J. M. Orenstein. 1990. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J. Virol. 64:621-629.
39. Lazdins, J. K., K. Woods-Cook, M. Walker, and E. Alteri. 1990. The lipophilic muramyl peptide MTP-PE is a potent inhibitor of HIV replication in macrophages. AIDS Res. Hum. Retroviruses 6:1157-1161.
40. Leder, P., D. Tiemeier, and L. Enquist. 1977. EK2 derivatives of bacteriophage lambda useful in the cloning of DNA from higher organisms: the Lambda gtWES system. Science 196:175-177.
41. Leonard, J., C. Parrott, A. J. Buckler-White, W. Turner, E. K. Ross, M. A. Martin, and A. B. Rabson. 1989. The NF-κB binding sites in the human immunodeficiency virus type 1 long terminal repeat are not required for virus infectivity. J. Virol. 63:4919-4924.
42. Li, Y., H. Hui, C. J. Burgess, R. W. Price, P. M. Sharp, B. H. Hahn, and G. M. Shaw. 1992. Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J. Virol. 66:6587-6600.
43. Matthews, T. Unpublished data.
44. McNearney, T., Z. Hornickova, R. Markham, A. Birdwell, M. Arens, A. Saah, and L. Ratner. 1992. Relationship of human immunodeficiency virus type 1 sequence heterogeneity to stage of disease. Proc. Natl. Acad. Sci. USA 89:10247-10251.
45. Morrow, W. J., J. Homsy, J. W. Eichberg, J. Krowka, L. Z. Pan, I. Gaston, H. Legg, N. Lerche, J. Thomas, and J. A. Levy. 1989. Long-term observation of baboons, rhesus monkeys, and chimpanzees inoculated with HIV and given periodic immunosuppressive treatment. AIDS Res. Hum. Retroviruses 5:233-245.
46. Murthy, K. (Southwest Foundation for Biomedical Research). Personal communication.
47. Myers, G. 1993. HIV-1 sequence subtypes and phylogenic trees, p. 2-3. In G. Myers, B. Korber, J. A. Berzofsky, and R. F. Smith (ed.), Human retroviruses and AIDS. Los Alamos National Laboratory, Los Alamos, N.Mex.
48. mac. J. Virol. 62:4691-4696.
49. Nara, P. L., W. Hatch, J. Kessler, J. Kelliher, and S. Carter. 1989. The biology of human immunodeficiency virus-1 IIIB infection in the chimpanzee: in vivo and in vitro correlations. J. Med. Primatol. 18:343-355.
50. Nara, P. L., W. G. Robey, L. O. Arthur, D. M. Asher, A. V. Wolff, C. J. Gibbs, Jr., D. C. Gajdusek, and P. J. Fischinger. 1987. Persistent infection of chimpanzees with human immunodeficiency virus: serological responses and properties of reisolated viruses. J. Virol. 61:3173-3180.
51. Niu, M. T., D. S. Stein, and S. M. Schnittman. 1993. Primary human immunodeficiency virus type 1 infection: review of pathogenesis and early treatment intervention in humans and animal retrovirus infections. J. Infect. Dis. 168:1490-1501.
52. Peden, K., M. Emerman, and L. Montagnier. 1991. Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI. Virology 185: 661-672.
53. Popovic, M., M. G. Sarngadharan, E. Read, and R. C. Gallo. 1984. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 224:497-500.
54. Potts, B. J., W. Maury, and M. A. Martin. 1990. Replication of HIV-1 in primary monocyte cultures. Virology 175:465-476.
55. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 27:493-497.
56. Ross, E. K., A. J. Buckler-White, A. B. Rabson, G. Englund, and M. A. Martin. 1991. Contribution of NF-κB and Sp1 binding motifs to the replicative capacity of human immunodeficiency virus type 1: distinct patterns of viral growth are determined by T-cell types. J. Virol. 65:4350-4358.
57. Saksela, K., E. Muchmore, M. Girald, P. Fultz, and D. Baltimore. 1993. High viral load in lymph nodes and latent human immunodeficiency virus (HIV) in peripheral blood cells of HIV-1-infected chimpanzees. J. Virol. 67:7423-7427.
58. Schuitemaker, H., L. Meyaard, N. A. Kootstra, R. Dubbes, S. A. Otto, M. Tersmette, J. L. Heeney, and F. Miedema. 1993. Lack of T cell dysfunction and programmed cell death in human immunodeficiency virus type 1-infected chimpanzees correlates with absence of monocytotropic variants. J. Infect. Dis. 168:1140-1147.
59. Simmonds, P., P. Balfe, J. F. Peutherer, C. A. Ludlam, J. O. Bishop, and A. J. Brown. 1990. Human immunodeficiency virus-infected individuals contain provirus in small numbers of peripheral mononuclear cells and at low copy numbers. J. Virol. 64:864-872.
60. Theodore, T. S., et al. Unpublished data.
61. van Griensven, G. J., E. M. de Vroome, F. de Wolf, J. Goudsmit, M. Roos, and R. A. Coutinho. 1990. Risk factors for progression of human immunodeficiency virus (HIV) infection among seroconverted and seropositive homosexual men. Am. J. Epidemiol. 132:203-210.
62. Wain-Hobson, S., P. Sonigo, O. Danos, S. Cole, and M. Alizon. 1985. Nucleotide sequence of the AIDS virus, LAV. Cell 40:9-17.
63. Walker, C. M., D. J. Moody, D. P. Stiles, and J. A. Levy. 1986. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234:1563-1566.
64. Ward, J. W., T. J. Bush, H. A. Perkins, L. E. Lieb, J. R. Allen, D. Goldfinger, S. M. Samson, S. H. Pepkowitz, L. P. Fernando, P. V. Holland, S. H. Kleinman, A. J. Grindon, J. L. Garner, G. W. Rutherford, and S. D. Holmberg. 1989. The natural history of transfusion-associated infection with human immunodeficiency virus. Factors influencing the rate of progression to disease. N. Engl. J. Med. 321:947-952.
65. Watanabe, M., D. J. Ringler, P. N. Fultz, J. J. MacKey, J. E. Boyson, C. G. Levine, and N. L. Letvin. 1991. A chimpanzee-passaged human immunodeficiency virus isolate is cytopathic for chimpanzee cells but does not induct disease. J. Virol. 65:3344-3348.
66. Willey, R. L., D. Smith, L. Lasky, T. S. Theodore, P. L. Earl, B. Moss, D. J. Capon, and M. A. Martin. 1988. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol. 62:139-147.
67. Zhang, L. Q., P. Mackenzie, A. Cleland, E. C. Holmes, A. J. Brown, and P. Simmonds. 1993. Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J. Virol. 67:3345-3356.
68. Zhu, T., H. Mo, N. Wang, D. S. Nam, Y. Cao, R. A. Koup, and D. D. Ho. 1996. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261:1179-1181.
69. Zunich, K. M., and H. C. Lane. 1991. Immunologic abnormalities in HIV infection. Hematol. Oncol. Clin. N. Am. 5:215-228.