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J Virol. May 1997; 71(5): 3588–3596.
PMCID: PMC191506

Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity.

Abstract

Human immunodeficiency virus type 1 (HIV-1) acquires several host cell membrane proteins when it buds from infected cells. To study the effect of virally incorporated host-derived ICAM-1 glycoproteins on the biology of HIV-1, we have developed a transient expression system that has enabled us to produce virus particles differing only in the absence or the presence of virion-bound ICAM-1. By using a single-round infection assay based on an ICAM-1-negative target T-cell line stably transfected with an HIV-1 long terminal repeat driven luciferase gene construct, we have been able to demonstrate that the acquisition of host-derived ICAM-1 by HIV-1 has functional significance, since it leads to a pronounced increase in viral infectivity (4.6- to 9.8-fold) in an ICAM-1/LFA-1-dependent fashion, as shown by blocking with anti-ICAM-1 and -LFA-1 antibodies. The same potentiating effect on viral infectivity was also observed with monocytoid cells. Studies of the kinetics of infection revealed that the positive effect mediated by virally embedded host cell membrane ICAM-1 is due to an increase in the efficiency of early steps in the viral life cycle. These results provide new insights into how incorporation of host proteins can modulate the biological properties of HIV-1. Our findings have direct clinical relevance, considering that ICAM-1 is expressed on the surface of virus-infected cells and, more importantly, that host-derived ICAM-1 has been shown to be acquired by clinical HIV-1 isolates grown on primary mononuclear cells. These data justify a more complete analysis of the other putative role(s) that virally incorporated ICAM-1 may play in the life cycle of HIV-1, for example, at the level of neutralization sensitivity.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol. 1986 Aug;59(2):284–291. [PMC free article] [PubMed]
  • Aguilar-Cordova E, Chinen J, Donehower L, Lewis DE, Belmont JW. A sensitive reporter cell line for HIV-1 tat activity, HIV-1 inhibitors, and T cell activation effects. AIDS Res Hum Retroviruses. 1994 Mar;10(3):295–301. [PubMed]
  • Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science. 1996 Jun 28;272(5270):1955–1958. [PubMed]
  • Arthur LO, Bess JW, Jr, Sowder RC, 2nd, Benveniste RE, Mann DL, Chermann JC, Henderson LE. Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines. Science. 1992 Dec 18;258(5090):1935–1938. [PubMed]
  • Bazil V, Stefanová I, Hilgert I, Kristofová H, Vanek S, Horejsí V. Monoclonal antibodies against human leucocyte antigens. IV. Antibodies against subunits of the LFA-1 (CD11a/CD18) leucocyte-adhesion glycoprotein. Folia Biol (Praha) 1990;36(1):41–50. [PubMed]
  • Benkirane M, Blanc-Zouaoui D, Hirn M, Devaux C. Involvement of human leukocyte antigen class I molecules in human immunodeficiency virus infection of CD4-positive cells. J Virol. 1994 Oct;68(10):6332–6339. [PMC free article] [PubMed]
  • Berman PW, Nakamura GR. Adhesion mediated by intercellular adhesion molecule 1 attenuates the potency of antibodies that block HIV-1 gp160-dependent syncytium formation. AIDS Res Hum Retroviruses. 1994 May;10(5):585–593. [PubMed]
  • Bérubé P, Barbeau B, Cantin R, Sékaly RP, Tremblay M. Repression of human immunodeficiency virus type 1 long terminal repeat-driven gene expression by binding of the virus to its primary cellular receptor, the CD4 molecule. J Virol. 1996 Jun;70(6):4009–4016. [PMC free article] [PubMed]
  • Cantin R, Fortin JF, Tremblay M. The amount of host HLA-DR proteins acquired by HIV-1 is virus strain- and cell type-specific. Virology. 1996 Apr 15;218(2):372–381. [PubMed]
  • Capobianchi MR, Fais S, Castilletti C, Gentile M, Ameglio F, Dianzani F. A simple and reliable method to detect cell membrane proteins on infectious human immunodeficiency virus type 1 particles. J Infect Dis. 1994 Apr;169(4):886–889. [PubMed]
  • Castilletti C, Capobianchi MR, Fais S, Abbate I, Ficociello B, Ameglio F, Cordiali Fei P, Santini SM, Dianzani F. HIV type 1 grown on interferon gamma-treated U937 cells shows selective increase in virion-associated intercellular adhesion molecule 1 and HLA-DR and enhanced infectivity for CD4-negative cells. AIDS Res Hum Retroviruses. 1995 May;11(5):547–553. [PubMed]
  • Chen C, Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. [PMC free article] [PubMed]
  • Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, et al. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell. 1996 Jun 28;85(7):1135–1148. [PubMed]
  • Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature. 1984 Dec 20;312(5996):763–767. [PubMed]
  • Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 1996 Jun 20;381(6584):661–666. [PubMed]
  • Dimitrov DS. Fusin--a place for HIV-1 and T4 cells to meet. Nat Med. 1996 Jun;2(6):640–641. [PubMed]
  • Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell. 1996 Jun 28;85(7):1149–1158. [PubMed]
  • Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, et al. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature. 1996 Jun 20;381(6584):667–673. [PubMed]
  • Dustin ML, Rothlein R, Bhan AK, Dinarello CA, Springer TA. Induction by IL 1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J Immunol. 1986 Jul 1;137(1):245–254. [PubMed]
  • Eichmann K, Jönsson JI, Falk I, Emmrich F. Effective activation of resting mouse T lymphocytes by cross-linking submitogenic concentrations of the T cell antigen receptor with either Lyt-2 or L3T4. Eur J Immunol. 1987 May;17(5):643–650. [PubMed]
  • Emmrich F, Kanz L, Eichmann K. Cross-linking of the T cell receptor complex with the subset-specific differentiation antigen stimulates interleukin 2 receptor expression in human CD4 and CD8 T cells. Eur J Immunol. 1987 Apr;17(4):529–534. [PubMed]
  • Fais S, Capobianchi MR, Abbate I, Castilletti C, Gentile M, Cordiali Fei P, Ameglio F, Dianzani F. Unidirectional budding of HIV-1 at the site of cell-to-cell contact is associated with co-polarization of intercellular adhesion molecules and HIV-1 viral matrix protein. AIDS. 1995 Apr;9(4):329–335. [PubMed]
  • Fecondo JV, Pavuk NC, Silburn KA, Read DM, Mansell AS, Boyd AW, McPhee DA. Synthetic peptide analogs of intercellular adhesion molecule 1 (ICAM-1) inhibit HIV-1 replication in MT-2 cells. AIDS Res Hum Retroviruses. 1993 Aug;9(8):733–740. [PubMed]
  • Felber BK, Pavlakis GN. A quantitative bioassay for HIV-1 based on trans-activation. Science. 1988 Jan 8;239(4836):184–187. [PubMed]
  • Feng Y, Broder CC, Kennedy PE, Berger EA. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science. 1996 May 10;272(5263):872–877. [PubMed]
  • Gelderblom H, Reupke H, Winkel T, Kunze R, Pauli G. MHC-antigens: constituents of the envelopes of human and simian immunodeficiency viruses. Z Naturforsch C. 1987 Nov-Dec;42(11-12):1328–1334. [PubMed]
  • Gomez MB, Hildreth JE. Antibody to adhesion molecule LFA-1 enhances plasma neutralization of human immunodeficiency virus type 1. J Virol. 1995 Aug;69(8):4628–4632. [PMC free article] [PubMed]
  • Gruber MF, Webb DS, Gerrard TL, Mostowski HS, Vujcic L, Golding H. Re-evaluation of the involvement of the adhesion molecules ICAM-1/LFA-1 in syncytia formation of HIV-1-infected subclones of a CEM T-cell leukemic line. AIDS Res Hum Retroviruses. 1991 Jan;7(1):45–53. [PubMed]
  • Henderson LE, Sowder R, Copeland TD, Oroszlan S, Arthur LO, Robey WG, Fischinger PJ. Direct identification of class II histocompatibility DR proteins in preparations of human T-cell lymphotropic virus type III. J Virol. 1987 Feb;61(2):629–632. [PMC free article] [PubMed]
  • Hildreth JE, Orentas RJ. Involvement of a leukocyte adhesion receptor (LFA-1) in HIV-induced syncytium formation. Science. 1989 Jun 2;244(4908):1075–1078. [PubMed]
  • Hoxie JA, Fitzharris TP, Youngbar PR, Matthews DM, Rackowski JL, Radka SF. Nonrandom association of cellular antigens with HTLV-III virions. Hum Immunol. 1987 Jan;18(1):39–52. [PubMed]
  • Julius M, Newell K, Maroun C, Haughn L. Functional consequences of CD4-TCR/CD3 interactions. Semin Immunol. 1991 May;3(3):161–166. [PubMed]
  • Kalter DC, Gendelman HE, Meltzer MS. Inhibition of human immunodeficiency virus infection in monocytes by monoclonal antibodies against leukocyte adhesion molecules. Immunol Lett. 1991 Oct;30(2):219–227. [PubMed]
  • Keizer GD, Visser W, Vliem M, Figdor CG. A monoclonal antibody (NKI-L16) directed against a unique epitope on the alpha-chain of human leukocyte function-associated antigen 1 induces homotypic cell-cell interactions. J Immunol. 1988 Mar 1;140(5):1393–1400. [PubMed]
  • Klatzmann D, Champagne E, Chamaret S, Gruest J, Guetard D, Hercend T, Gluckman JC, Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature. 1984 Dec 20;312(5996):767–768. [PubMed]
  • Kupfer A, Singer SJ, Janeway CA, Jr, Swain SL. Coclustering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5888–5892. [PMC free article] [PubMed]
  • Lasky LA, Nakamura G, Smith DH, Fennie C, Shimasaki C, Patzer E, Berman P, Gregory T, Capon DJ. Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell. 1987 Sep 11;50(6):975–985. [PubMed]
  • Ledbetter JA, Gilliland LK, Schieven GL. The interaction of CD4 with CD3/Ti regulates tyrosine phosphorylation of substrates during T cell activation. Semin Immunol. 1990 Mar;2(2):99–106. [PubMed]
  • Ledbetter JA, June CH, Grosmaire LS, Rabinovitch PS. Crosslinking of surface antigens causes mobilization of intracellular ionized calcium in T lymphocytes. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1384–1388. [PMC free article] [PubMed]
  • Guo MM, Hildreth JE. HIV acquires functional adhesion receptors from host cells. AIDS Res Hum Retroviruses. 1995 Sep;11(9):1007–1013. [PubMed]
  • Lifson JD, Reyes GR, McGrath MS, Stein BS, Engleman EG. AIDS retrovirus induced cytopathology: giant cell formation and involvement of CD4 antigen. Science. 1986 May 30;232(4754):1123–1127. [PubMed]
  • Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986 Nov 7;47(3):333–348. [PubMed]
  • Marlin SD, Springer TA. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell. 1987 Dec 4;51(5):813–819. [PubMed]
  • McCallus DE, Ugen KE, Sato AI, Williams WV, Weiner DB. Construction of a recombinant bacterial human CD4 expression system producing a bioactive CD4 molecule. Viral Immunol. 1992 Summer;5(2):163–172. [PubMed]
  • Meerloo T, Sheikh MA, Bloem AC, de Ronde A, Schutten M, van Els CA, Roholl PJ, Joling P, Goudsmit J, Schuurman HJ. Host cell membrane proteins on human immunodeficiency virus type 1 after in vitro infection of H9 cells and blood mononuclear cells. An immuno-electron microscopic study. J Gen Virol. 1993 Jan;74(Pt 1):129–135. [PubMed]
  • Meerloo T, Parmentier HK, Osterhaus AD, Goudsmit J, Schuurman HJ. Modulation of cell surface molecules during HIV-1 infection of H9 cells. An immunoelectron microscopic study. AIDS. 1992 Oct;6(10):1105–1116. [PubMed]
  • Orentas RJ, Hildreth JE. Association of host cell surface adhesion receptors and other membrane proteins with HIV and SIV. AIDS Res Hum Retroviruses. 1993 Nov;9(11):1157–1165. [PubMed]
  • Pantaleo G, Butini L, Graziosi C, Poli G, Schnittman SM, Greenhouse JJ, Gallin JI, Fauci AS. Human immunodeficiency virus (HIV) infection in CD4+ T lymphocytes genetically deficient in LFA-1: LFA-1 is required for HIV-mediated cell fusion but not for viral transmission. J Exp Med. 1991 Feb 1;173(2):511–514. [PMC free article] [PubMed]
  • Rothlein R, Dustin ML, Marlin SD, Springer TA. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J Immunol. 1986 Aug 15;137(4):1270–1274. [PubMed]
  • Saifuddin M, Parker CJ, Peeples ME, Gorny MK, Zolla-Pazner S, Ghassemi M, Rooney IA, Atkinson JP, Spear GT. Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. J Exp Med. 1995 Aug 1;182(2):501–509. [PMC free article] [PubMed]
  • Schols D, Pauwels R, Desmyter J, De Clercq E. Presence of class II histocompatibility DR proteins on the envelope of human immunodeficiency virus demonstrated by FACS analysis. Virology. 1992 Jul;189(1):374–376. [PubMed]
  • Schwartz S, Felber BK, Fenyö EM, Pavlakis GN. Rapidly and slowly replicating human immunodeficiency virus type 1 isolates can be distinguished according to target-cell tropism in T-cell and monocyte cell lines. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7200–7203. [PMC free article] [PubMed]
  • Springer TA. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. [PubMed]
  • Staunton DE, Marlin SD, Stratowa C, Dustin ML, Springer TA. Primary structure of ICAM-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell. 1988 Mar 25;52(6):925–933. [PubMed]
  • Trowbridge IS, Thomas ML. CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. Annu Rev Immunol. 1994;12:85–116. [PubMed]
  • Woska JR, Jr, Morelock MM, Jeanfavre DD, Bormann BJ. Characterization of molecular interactions between intercellular adhesion molecule-1 and leukocyte function- associated antigen-1. J Immunol. 1996 Jun 15;156(12):4680–4685. [PubMed]

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