Abstract
Several epidemiologic and clinical studies suggest that patients coinfected with human immunodeficiency virus (HIV), the primary etiologic agent in AIDS, and other viruses, such as cytomegalovirus or human T-cell leukemia virus (HTLV), have a more severe clinical course than those infected with HIV alone. Cells infected with two viruses can, in some cases, give rise to phenotypically mixed virions with altered or broadened cell tropism and could therefore account for some of these findings. Such pseudotypes could alter the course of disease by infecting more tissues than are normally infected by HIV. We show here that HIV type 1 (HIV-1) efficiently incorporates the HTLV type I (HTLV-I) envelope glycoprotein and that both HIV-1 and HTLV-II accept other widely divergent envelope glycoproteins to form infectious pseudotype viruses whose cellular tropisms and relative abilities to be transmitted by cell-free virions or by cell contact are determined by the heterologous envelope. We also show that the mechanism by which virions incorporate heterologous envelope glycoproteins is independent of the presence of the homologous glycoprotein or heterologous gag proteins. These results may have important implications for the mechanism of HIV pathogenesis.
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- Boettiger D. Animal virus pseudotypes. Prog Med Virol. 1979;25:37–68. [PubMed] [Google Scholar]
- Bonetti A., Weber R., Vogt M. W., Wunderli W., Siegenthaler W., Lüthy R. Co-infection with human immunodeficiency virus-type 1 (HIV-1) and cytomegalovirus in two intravenous drug users. Ann Intern Med. 1989 Aug 15;111(4):293–296. doi: 10.7326/0003-4819-111-4-293. [DOI] [PubMed] [Google Scholar]
- Calafat J., Janssen H., Démant P., Hilgers J., Závada J. Specific selection of host cell glycoproteins during assembly of murine leukaemia virus and vesicular stomatitis virus: presence of Thy-1 glycoprotein and absence of H-2, Pgp-1 and T-200 glycoproteins on the envelopes of these virus particles. J Gen Virol. 1983 Jun;64(Pt 6):1241–1253. doi: 10.1099/0022-1317-64-6-1241. [DOI] [PubMed] [Google Scholar]
- Chen I. S., McLaughlin J., Golde D. W. Long terminal repeats of human T-cell leukaemia virus II genome determine target cell specificity. Nature. 1984 May 17;309(5965):276–279. doi: 10.1038/309276a0. [DOI] [PubMed] [Google Scholar]
- Chen I. S., Quan S. G., Golde D. W. Human T-cell leukemia virus type II transforms normal human lymphocytes. Proc Natl Acad Sci U S A. 1983 Nov;80(22):7006–7009. doi: 10.1073/pnas.80.22.7006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chesebro B., Buller R., Portis J., Wehrly K. Failure of human immunodeficiency virus entry and infection in CD4-positive human brain and skin cells. J Virol. 1990 Jan;64(1):215–221. doi: 10.1128/jvi.64.1.215-221.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clapham P., Nagy K., Cheingsong-Popov R., Exley M., Weiss R. A. Productive infection and cell-free transmission of human T-cell leukemia virus in a nonlymphoid cell line. Science. 1983 Dec 9;222(4628):1125–1127. doi: 10.1126/science.6316502. [DOI] [PubMed] [Google Scholar]
- Fiala M., Cone L. A., Chang C. M., Mocarski E. S. Cytomegalovirus viremia increases with progressive immune deficiency in patients infected with HTLV-III. AIDS Res. 1986 Summer;2(3):175–181. doi: 10.1089/aid.1.1986.2.175. [DOI] [PubMed] [Google Scholar]
- Gabuzda D. H., Ho D. D., de la Monte S. M., Hirsch M. S., Rota T. R., Sobel R. A. Immunohistochemical identification of HTLV-III antigen in brains of patients with AIDS. Ann Neurol. 1986 Sep;20(3):289–295. doi: 10.1002/ana.410200304. [DOI] [PubMed] [Google Scholar]
- Gebhardt A., Bosch J. V., Ziemiecki A., Friis R. R. Rous sarcoma virus p19 and gp35 can be chemically crosslinked to high molecular weight complexes. An insight into virus assembly. J Mol Biol. 1984 Apr 5;174(2):297–317. doi: 10.1016/0022-2836(84)90340-1. [DOI] [PubMed] [Google Scholar]
- Gendelman H. E., Phelps W., Feigenbaum L., Ostrove J. M., Adachi A., Howley P. M., Khoury G., Ginsberg H. S., Martin M. A. Trans-activation of the human immunodeficiency virus long terminal repeat sequence by DNA viruses. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9759–9763. doi: 10.1073/pnas.83.24.9759. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harouse J. M., Kunsch C., Hartle H. T., Laughlin M. A., Hoxie J. A., Wigdahl B., Gonzalez-Scarano F. CD4-independent infection of human neural cells by human immunodeficiency virus type 1. J Virol. 1989 Jun;63(6):2527–2533. doi: 10.1128/jvi.63.6.2527-2533.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartley J. W., Rowe W. P. Naturally occurring murine leukemia viruses in wild mice: characterization of a new "amphotropic" class. J Virol. 1976 Jul;19(1):19–25. doi: 10.1128/jvi.19.1.19-25.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hattori T., Koito A., Takatsuki K., Ikematsu S., Matsuda J., Mori H., Fukui M., Akashi K., Matsumoto K. Frequent infection with human T-cell lymphotropic virus type I in patients with AIDS but not in carriers of human immunodeficiency virus type 1. J Acquir Immune Defic Syndr. 1989;2(3):272–276. [PubMed] [Google Scholar]
- Horvat R. T., Wood C., Balachandran N. Transactivation of human immunodeficiency virus promoter by human herpesvirus 6. J Virol. 1989 Feb;63(2):970–973. doi: 10.1128/jvi.63.2.970-973.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunsch C., Hartle H. T., Wigdahl B. Infection of human fetal dorsal root ganglion glial cells with human immunodeficiency virus type 1 involves an entry mechanism independent of the CD4 T4A epitope. J Virol. 1989 Dec;63(12):5054–5061. doi: 10.1128/jvi.63.12.5054-5061.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee H., Swanson P., Shorty V. S., Zack J. A., Rosenblatt J. D., Chen I. S. High rate of HTLV-II infection in seropositive i.v. drug abusers in New Orleans. Science. 1989 Apr 28;244(4903):471–475. doi: 10.1126/science.2655084. [DOI] [PubMed] [Google Scholar]
- Lodish H. F., Porter M. Specific incorporation of host cell surface proteins into budding vesicular stomatitis virus particles. Cell. 1980 Jan;19(1):161–169. doi: 10.1016/0092-8674(80)90397-9. [DOI] [PubMed] [Google Scholar]
- Lusso P., di Marzo Veronese F., Ensoli B., Franchini G., Jemma C., DeRocco S. E., Kalyanaraman V. S., Gallo R. C. Expanded HIV-1 cellular tropism by phenotypic mixing with murine endogenous retroviruses. Science. 1990 Feb 16;247(4944):848–852. doi: 10.1126/science.2305256. [DOI] [PubMed] [Google Scholar]
- Malim M. H., Hauber J., Fenrick R., Cullen B. R. Immunodeficiency virus rev trans-activator modulates the expression of the viral regulatory genes. Nature. 1988 Sep 8;335(6186):181–183. doi: 10.1038/335181a0. [DOI] [PubMed] [Google Scholar]
- Mann R., Mulligan R. C., Baltimore D. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell. 1983 May;33(1):153–159. doi: 10.1016/0092-8674(83)90344-6. [DOI] [PubMed] [Google Scholar]
- Metsikkö K., Garoff H. Role of heterologous and homologous glycoproteins in phenotypic mixing between Sendai virus and vesicular stomatitis virus. J Virol. 1989 Dec;63(12):5111–5118. doi: 10.1128/jvi.63.12.5111-5118.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mosca J. D., Bednarik D. P., Raj N. B., Rosen C. A., Sodroski J. G., Haseltine W. A., Pitha P. M. Herpes simplex virus type-1 can reactivate transcription of latent human immunodeficiency virus. Nature. 1987 Jan 1;325(6099):67–70. doi: 10.1038/325067a0. [DOI] [PubMed] [Google Scholar]
- Ostrove J. M., Leonard J., Weck K. E., Rabson A. B., Gendelman H. E. Activation of the human immunodeficiency virus by herpes simplex virus type 1. J Virol. 1987 Dec;61(12):3726–3732. doi: 10.1128/jvi.61.12.3726-3732.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Page K. A., Landau N. R., Littman D. R. Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity. J Virol. 1990 Nov;64(11):5270–5276. doi: 10.1128/jvi.64.11.5270-5276.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palker T. J., Tanner M. E., Scearce R. M., Streilein R. D., Clark M. E., Haynes B. F. Mapping of immunogenic regions of human T cell leukemia virus type I (HTLV-I) gp46 and gp21 envelope glycoproteins with env-encoded synthetic peptides and a monoclonal antibody to gp46. J Immunol. 1989 Feb 1;142(3):971–978. [PubMed] [Google Scholar]
- Pedersen N. C., Torten M., Rideout B., Sparger E., Tonachini T., Luciw P. A., Ackley C., Levy N., Yamamoto J. Feline leukemia virus infection as a potentiating cofactor for the primary and secondary stages of experimentally induced feline immunodeficiency virus infection. J Virol. 1990 Feb;64(2):598–606. doi: 10.1128/jvi.64.2.598-606.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perez L. G., Davis G. L., Hunter E. Mutants of the Rous sarcoma virus envelope glycoprotein that lack the transmembrane anchor and cytoplasmic domains: analysis of intracellular transport and assembly into virions. J Virol. 1987 Oct;61(10):2981–2988. doi: 10.1128/jvi.61.10.2981-2988.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pumarola-Sune T., Navia B. A., Cordon-Cardo C., Cho E. S., Price R. W. HIV antigen in the brains of patients with the AIDS dementia complex. Ann Neurol. 1987 May;21(5):490–496. doi: 10.1002/ana.410210513. [DOI] [PubMed] [Google Scholar]
- Raffi F., Boudart D., Billaudel S. Acute co-infection with human immunodeficiency virus (HIV) and cytomegalovirus. Ann Intern Med. 1990 Feb 1;112(3):234–235. doi: 10.7326/0003-4819-112-3-234. [DOI] [PubMed] [Google Scholar]
- RusS G., Poláková K., Závada J. Assembly of xenotropic murine leukaemia virus-related antigens from the surface of mouse L cells by vesicular stomatitis virus. Acta Virol. 1983 Mar;27(2):105–109. [PubMed] [Google Scholar]
- Salahuddin S. Z., Ablashi D. V., Markham P. D., Josephs S. F., Sturzenegger S., Kaplan M., Halligan G., Biberfeld P., Wong-Staal F., Kramarsky B. Isolation of a new virus, HBLV, in patients with lymphoproliferative disorders. Science. 1986 Oct 31;234(4776):596–601. doi: 10.1126/science.2876520. [DOI] [PubMed] [Google Scholar]
- Seto E., Yen T. S., Peterlin B. M., Ou J. H. Trans-activation of the human immunodeficiency virus long terminal repeat by the hepatitis B virus X protein. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8286–8290. doi: 10.1073/pnas.85.21.8286. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimotohno K., Wachsman W., Takahashi Y., Golde D. W., Miwa M., Sugimura T., Chen I. S. Nucleotide sequence of the 3' region of an infectious human T-cell leukemia virus type II genome. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6657–6661. doi: 10.1073/pnas.81.21.6657. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siekevitz M., Josephs S. F., Dukovich M., Peffer N., Wong-Staal F., Greene W. C. Activation of the HIV-1 LTR by T cell mitogens and the trans-activator protein of HTLV-I. Science. 1987 Dec 11;238(4833):1575–1578. doi: 10.1126/science.2825351. [DOI] [PubMed] [Google Scholar]
- Sommerfelt M. A., Williams B. P., Clapham P. R., Solomon E., Goodfellow P. N., Weiss R. A. Human T cell leukemia viruses use a receptor determined by human chromosome 17. Science. 1988 Dec 16;242(4885):1557–1559. doi: 10.1126/science.3201246. [DOI] [PubMed] [Google Scholar]
- Southern P. J., Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet. 1982;1(4):327–341. [PubMed] [Google Scholar]
- Spector D. H., Wade E., Wright D. A., Koval V., Clark C., Jaquish D., Spector S. A. Human immunodeficiency virus pseudotypes with expanded cellular and species tropism. J Virol. 1990 May;64(5):2298–2308. doi: 10.1128/jvi.64.5.2298-2308.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Starcich B., Ratner L., Josephs S. F., Okamoto T., Gallo R. C., Wong-Staal F. Characterization of long terminal repeat sequences of HTLV-III. Science. 1985 Feb 1;227(4686):538–540. doi: 10.1126/science.2981438. [DOI] [PubMed] [Google Scholar]
- Stuve L. L., Brown-Shimer S., Pachl C., Najarian R., Dina D., Burke R. L. Structure and expression of the herpes simplex virus type 2 glycoprotein gB gene. J Virol. 1987 Feb;61(2):326–335. doi: 10.1128/jvi.61.2.326-335.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas E. K., Weber J. N., McClure J., Clapham P. R., Singhal M. C., Shriver M. K., Weiss R. A. Neutralizing monoclonal antibodies to the AIDS virus. AIDS. 1988 Feb;2(1):25–29. doi: 10.1097/00002030-198802000-00004. [DOI] [PubMed] [Google Scholar]
- Turner J. M., Brodsky M. H., Irving B. A., Levin S. D., Perlmutter R. M., Littman D. R. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell. 1990 Mar 9;60(5):755–765. doi: 10.1016/0092-8674(90)90090-2. [DOI] [PubMed] [Google Scholar]
- Webster A., Lee C. A., Cook D. G., Grundy J. E., Emery V. C., Kernoff P. B., Griffiths P. D. Cytomegalovirus infection and progression towards AIDS in haemophiliacs with human immunodeficiency virus infection. Lancet. 1989 Jul 8;2(8654):63–66. doi: 10.1016/s0140-6736(89)90312-7. [DOI] [PubMed] [Google Scholar]
- Weiss R. A., Bennett P. L. Assembly of membrane glycoproteins studied by phenotypic mixing between mutants of vesicular stomatitis virus and retroviruses. Virology. 1980 Jan 30;100(2):252–274. doi: 10.1016/0042-6822(80)90518-8. [DOI] [PubMed] [Google Scholar]
- Weiss R. A., Payne L. N. The heritable nature of the factor in chicken cells which acts as a helper virus for Rous sarcoma virus. Virology. 1971 Aug;45(2):508–515. doi: 10.1016/0042-6822(71)90351-5. [DOI] [PubMed] [Google Scholar]
- Wiley C. A., Nelson J. A. Role of human immunodeficiency virus and cytomegalovirus in AIDS encephalitis. Am J Pathol. 1988 Oct;133(1):73–81. [PMC free article] [PubMed] [Google Scholar]
- Wiley C. A., Schrier R. D., Nelson J. A., Lampert P. W., Oldstone M. B. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci U S A. 1986 Sep;83(18):7089–7093. doi: 10.1073/pnas.83.18.7089. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willey R. L., Bonifacino J. S., Potts B. J., Martin M. A., Klausner R. D. Biosynthesis, cleavage, and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9580–9584. doi: 10.1073/pnas.85.24.9580. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Witte O. N., Baltimore D. Mechanism of formation of pseudotypes between vesicular stomatitis virus and murine leukemia virus. Cell. 1977 Jul;11(3):505–511. doi: 10.1016/0092-8674(77)90068-x. [DOI] [PubMed] [Google Scholar]
- Yamamoto N., Okada M., Koyanagi Y., Kannagi M., Hinuma Y. Transformation of human leukocytes by cocultivation with an adult T cell leukemia virus producer cell line. Science. 1982 Aug 20;217(4561):737–739. doi: 10.1126/science.6980467. [DOI] [PubMed] [Google Scholar]
- Zhu Z. H., Chen S. S., Huang A. S. Phenotypic mixing between human immunodeficiency virus and vesicular stomatitis virus or herpes simplex virus. J Acquir Immune Defic Syndr. 1990;3(3):215–219. [PubMed] [Google Scholar]