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    Paul R Clapham PhD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentProgram in Molecular Medicine
    AddressUniversity of Massachusetts Medical School
    373 Plantation Street
    Worcester MA 01605
    Phone508-856-6281
      Other Positions
      InstitutionUMMS - School of Medicine
      DepartmentMicrobiology and Physiological Systems

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentImmunology and Virology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentInterdisciplinary Graduate Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMolecular Genetics and Microbiology

      InstitutionUMMS - Programs, Centers and Institutes
      DepartmentCenter for AIDS Research

        Overview 
        Narrative

        The HIV envelope: Biology, Receptors and Cellular Tropisms

        HIV uses cell surface receptors to attach to and enter cells. Interactions with CD4 and a coreceptor are usually required for HIV to efficiently enter cells. Coreceptors are seven-transmembrane receptors that belong to the chemokine receptor family. Viruses transmitted and present in the asymptomatic stages of infection use the chemokine receptor CCR5 as a coreceptor, while variants that use CXCR4 emerge later in disease in up to 50% of AIDS patients. More than a dozen other coreceptors have been identified that confer infection in vitro for various HIV and SIV strains. However, these are not currently believed to be significant for HIV replication in vivo.Dr. Paul Clapham

        Our group is investigating how HIV-1 adapts for replication in different environments and cell types in vivo. We use PCR to amplify envelopes from patient tissue. This avoids viral culture that may introduce mutations into envelope genes. We have shown that CCR5-using envelopes vary substantially in tropism and capacity to exploit low levels of CD4 and/or CCR5 for infection. Thus, envelopes from brain tissue are predominantly highly macrophage-tropic and can exploit low levels of CD4 for infection. In contrast, the majority of envelopes from immune tissue required high levels of CD4 for infection and were non-macrophage-tropic. Current research aims to evaluate whether highly macrophage-tropic variants evolve at different sites in vivo. For example, if highly macrophage-tropic variants are present in semen, they may confer more efficient transmission. We are also investigating the selective pressures that confer macrophage-tropic and non-macrophage-tropic phenotypes for CCR5-using HIV-1. Do these phenotypes simply reflect adaptation for replication in T-cells in immune tissue and for macrophages in the brain? Or do the phenotypes result from different immune pressures conferred by neutralizing antibodies in immune tissue, contrasting with brain tissue where neutralizing antibodies are usually excluded by the blood brain barrier.

        Projects that examine other aspects of the biology of the HIV-1 envelope are also ongoing to investigate (1) the trafficking of newly synthesized envelope glycoproteins to the sites of virus budding and (2) vpu regulation of envelope expression and maturation in vitro and in vivo.

        Paul Clapham, PhD



        Rotation Projects

        Rotation Projects

        Rotation projects are available in support of our research. See the research description section of this page.



        Bibliographic 
        selected publications
        List All   |   Timeline
        1. Peters PJ, Richards K, Clapham P. Human immunodeficiency viruses: propagation, quantification, and storage. Curr Protoc Microbiol. 2013; Chapter 15:Unit 15J.1.
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        2. O'Connell O, Repik A, Reeves JD, Gonzalez-Perez MP, Quitadamo B, Anton ED, Duenas-Decamp M, Peters P, Lin R, Zolla-Pazner S, Corti D, Wallace A, Wang S, Kong XP, Lu S, Clapham PR. Efficiency of bridging-sheet recruitment explains HIV-1 R5 envelope glycoprotein sensitivity to soluble CD4 and macrophage tropism. J Virol. 2013 Jan; 87(1):187-98.
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        3. Gonzalez-Perez MP, O'Connell O, Lin R, Sullivan WM, Bell J, Simmonds P, Clapham PR. Independent evolution of macrophage-tropism and increased charge between HIV-1 R5 envelopes present in brain and immune tissue. Retrovirology. 2012; 9:20.
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        4. Dueñas-Decamp MJ, O'Connell OJ, Corti D, Zolla-Pazner S, Clapham PR. The W100 pocket on HIV-1 gp120 penetrated by b12 is not a target for other CD4bs monoclonal antibodies. Retrovirology. 2012; 9:9.
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        5. Clapham PR, Lu S. Vaccinology: precisely tuned antibodies nab HIV. Nature. 2011 Sep 22; 477(7365):416-7.
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        6. Kishko M, Somasundaran M, Brewster F, Sullivan JL, Clapham PR, Luzuriaga K. Genotypic and functional properties of early infant HIV-1 envelopes. Retrovirology. 2011; 8:67.
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        7. Shen R, Meng G, Ochsenbauer C, Clapham PR, Grams J, Novak L, Kappes JC, Smythies LE, Smith PD. Stromal down-regulation of macrophage CD4/CCR5 expression and NF-?B activation mediates HIV-1 non-permissiveness in intestinal macrophages. PLoS Pathog. 2011 May; 7(5):e1002060.
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        8. Brown RJ, Peters PJ, Caron C, Gonzalez-Perez MP, Stones L, Ankghuambom C, Pondei K, McClure CP, Alemnji G, Taylor S, Sharp PM, Clapham PR, Ball JK. Intercompartmental recombination of HIV-1 contributes to env intrahost diversity and modulates viral tropism and sensitivity to entry inhibitors. J Virol. 2011 Jun; 85(12):6024-37.
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        9. Vaine M, Duenas-Decamp M, Peters P, Liu Q, Arthos J, Wang S, Clapham P, Lu S. Two closely related Env antigens from the same patient elicited different spectra of neutralizing antibodies against heterologous HIV-1 isolates. J Virol. 2011 May; 85(10):4927-36.
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        10. Musich T, Peters PJ, Duenas-Decamp MJ, Gonzalez-Perez MP, Robinson J, Zolla-Pazner S, Ball JK, Luzuriaga K, Clapham PR. A conserved determinant in the V1 loop of HIV-1 modulates the V3 loop to prime low CD4 use and macrophage infection. J Virol. 2011 Mar; 85(5):2397-405.
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        11. Duenas-Decamp MJ, Clapham PR. HIV-1 gp120 determinants proximal to the CD4 binding site shift protective glycans that are targeted by monoclonal antibody 2G12. J Virol. 2010 Sep; 84(18):9608-12.
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        12. Richards KH, Aasa-Chapman MM, McKnight A, Clapham PR. Modulation of HIV-1 macrophage-tropism among R5 envelopes occurs before detection of neutralizing antibodies. Retrovirology. 2010; 7:48.
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        13. Zhang S, Alexander L, Wang T, Agler M, Zhou N, Fang H, Kadow J, Clapham P, Lin PF. Protection against HIV-envelope-induced neuronal cell destruction by HIV attachment inhibitors. Arch Virol. 2010 May; 155(5):777-81.
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        14. Agrawal L, Maxwell CR, Peters PJ, Clapham PR, Liu SM, Mackay CR, Strayer DS. Complexity in human immunodeficiency virus type 1 (HIV-1) co-receptor usage: roles of CCR3 and CCR5 in HIV-1 infection of monocyte-derived macrophages and brain microglia. J Gen Virol. 2009 Mar; 90(Pt 3):710-22.
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        15. Shen R, Richter HE, Clements RH, Novak L, Huff K, Bimczok D, Sankaran-Walters S, Dandekar S, Clapham PR, Smythies LE, Smith PD. Macrophages in vaginal but not intestinal mucosa are monocyte-like and permissive to human immunodeficiency virus type 1 infection. J Virol. 2009 Apr; 83(7):3258-67.
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        16. Duenas-Decamp MJ, Peters PJ, Burton D, Clapham PR. Determinants flanking the CD4 binding loop modulate macrophage tropism of human immunodeficiency virus type 1 R5 envelopes. J Virol. 2009 Mar; 83(6):2575-83.
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        17. Repik A, Clapham PR. Plugging gp120s cavity. Structure. 2008 Nov 12; 16(11):1603-4.
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        18. Duenas-Decamp MJ, Peters P, Burton D, Clapham PR. Natural resistance of human immunodeficiency virus type 1 to the CD4bs antibody b12 conferred by a glycan and an arginine residue close to the CD4 binding loop. J Virol. 2008 Jun; 82(12):5807-14.
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        19. Peters PJ, Duenas-Decamp MJ, Sullivan WM, Brown R, Ankghuambom C, Luzuriaga K, Robinson J, Burton DR, Bell J, Simmonds P, Ball J, Clapham PR. Variation in HIV-1 R5 macrophage-tropism correlates with sensitivity to reagents that block envelope: CD4 interactions but not with sensitivity to other entry inhibitors. Retrovirology. 2008; 5:5.
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        20. Sullivan WM, Dorr P, Perros M, Hudson R, Leif J, Luzuriaga K, Clapham PR. Lack of alternative coreceptor use by pediatric HIV-1 R5 isolates for infection of primary cord or adult peripheral blood mononuclear cells. Arch Virol. 2008; 153(2):363-6.
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        21. Richards KH, Clapham PR. Effects of vpu start-codon mutations on human immunodeficiency virus type 1 replication in macrophages. J Gen Virol. 2007 Oct; 88(Pt 10):2780-92.
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        22. Repik A, Richards KH, Clapham PR. The promise of CCR5 antagonists as new therapies for HIV-1. Curr Opin Investig Drugs. 2007 Feb; 8(2):130-9.
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        23. Gorry PR, Dunfee RL, Mefford ME, Kunstman K, Morgan T, Moore JP, Mascola JR, Agopian K, Holm GH, Mehle A, Taylor J, Farzan M, Wang H, Ellery P, Willey SJ, Clapham PR, Wolinsky SM, Crowe SM, Gabuzda D. Changes in the V3 region of gp120 contribute to unusually broad coreceptor usage of an HIV-1 isolate from a CCR5 Delta32 heterozygote. Virology. 2007 May 25; 362(1):163-78.
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        24. Peters PJ, Dueñas-Decamp MJ, Sullivan WM, Clapham PR. Variation of macrophage tropism among HIV-1 R5 envelopes in brain and other tissues. J Neuroimmune Pharmacol. 2007 Mar; 2(1):32-41.
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        25. Richards KH, Clapham PR. Human immunodeficiency viruses: propagation, quantification, and storage. Curr Protoc Microbiol. 2006 Sep; Chapter 15:Unit15J.1.
          View in: PubMed
        26. Peters PJ, Sullivan WM, Duenas-Decamp MJ, Bhattacharya J, Ankghuambom C, Brown R, Luzuriaga K, Bell J, Simmonds P, Ball J, Clapham PR. Non-macrophage-tropic human immunodeficiency virus type 1 R5 envelopes predominate in blood, lymph nodes, and semen: implications for transmission and pathogenesis. J Virol. 2006 Jul; 80(13):6324-32.
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        27. Bhattacharya J, Repik A, Clapham PR. Gag regulates association of human immunodeficiency virus type 1 envelope with detergent-resistant membranes. J Virol. 2006 Jun; 80(11):5292-300.
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        28. Ho HT, Fan L, Nowicka-Sans B, McAuliffe B, Li CB, Yamanaka G, Zhou N, Fang H, Dicker I, Dalterio R, Gong YF, Wang T, Yin Z, Ueda Y, Matiskella J, Kadow J, Clapham P, Robinson J, Colonno R, Lin PF. Envelope conformational changes induced by human immunodeficiency virus type 1 attachment inhibitors prevent CD4 binding and downstream entry events. J Virol. 2006 Apr; 80(8):4017-25.
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        29. Willey S, Peters PJ, Sullivan WM, Dorr P, Perros M, Clapham PR. Inhibition of CCR5-mediated infection by diverse R5 and R5X4 HIV and SIV isolates using novel small molecule inhibitors of CCR5: effects of viral diversity, target cell and receptor density. Antiviral Res. 2005 Nov; 68(2):96-108.
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        30. Cilliers T, Willey S, Sullivan WM, Patience T, Pugach P, Coetzer M, Papathanasopoulos M, Moore JP, Trkola A, Clapham P, Morris L. Use of alternate coreceptors on primary cells by two HIV-1 isolates. Virology. 2005 Aug 15; 339(1):136-44.
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        31. Neil SJ, Aasa-Chapman MM, Clapham PR, Nibbs RJ, McKnight A, Weiss RA. The promiscuous CC chemokine receptor D6 is a functional coreceptor for primary isolates of human immunodeficiency virus type 1 (HIV-1) and HIV-2 on astrocytes. J Virol. 2005 Aug; 79(15):9618-24.
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        32. Elvin SJ, Williamson ED, Scott JC, Smith JN, Pérez De Lema G, Chilla S, Clapham P, Pfeffer K, Schlöndorff D, Luckow B. Evolutionary genetics: Ambiguous role of CCR5 in Y. pestis infection. Nature. 2004 Jul 22; 430(6998):417.
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        33. Peters PJ, Bhattacharya J, Hibbitts S, Dittmar MT, Simmons G, Bell J, Simmonds P, Clapham PR. Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol. 2004 Jul; 78(13):6915-26.
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        34. Bhattacharya J, Peters PJ, Clapham PR. Human immunodeficiency virus type 1 envelope glycoproteins that lack cytoplasmic domain cysteines: impact on association with membrane lipid rafts and incorporation onto budding virus particles. J Virol. 2004 May; 78(10):5500-6.
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        35. Willey SJ, Reeves JD, Hudson R, Miyake K, Dejucq N, Schols D, De Clercq E, Bell J, McKnight A, Clapham PR. Identification of a subset of human immunodeficiency virus type 1 (HIV-1), HIV-2, and simian immunodeficiency virus strains able to exploit an alternative coreceptor on untransformed human brain and lymphoid cells. J Virol. 2003 Jun; 77(11):6138-52.
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        36. Thomas ER, Shotton C, Weiss RA, Clapham PR, McKnight A. CD4-dependent and CD4-independent HIV-2: consequences for neutralization. AIDS. 2003 Feb 14; 17(3):291-300.
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        37. Reynolds L, Ullman C, Moore M, Isalan M, West MJ, Clapham P, Klug A, Choo Y. Repression of the HIV-1 5' LTR promoter and inhibition of HIV-1 replication by using engineered zinc-finger transcription factors. Proc Natl Acad Sci U S A. 2003 Feb 18; 100(4):1615-20.
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        38. Bhattacharya J, Peters PJ, Clapham PR. CD4-independent infection of HIV and SIV: implications for envelope conformation and cell tropism in vivo. AIDS. 2003; 17 Suppl 4:S35-43.
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        39. Clapham PR, McKnight A. Cell surface receptors, virus entry and tropism of primate lentiviruses. J Gen Virol. 2002 Aug; 83(Pt 8):1809-29.
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        40. Vyakarnam A, Eyeson J, Teo I, Zuckerman M, Babaahmady K, Schuitemaker H, Shaunak S, Rostron T, Rowland-Jones S, Simmons G, Clapham P. Evidence for a post-entry barrier to R5 HIV-1 infection of CD4 memory T cells. AIDS. 2001 Sep 7; 15(13):1613-26.
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        41. Characterization of a late entry event in the replication cycle of human immunodeficiency virus type 2. J Virol. 2001 Aug; 75(15):6914-22.
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        42. Blanpain C, Buser R, Power CA, Edgerton M, Buchanan C, Mack M, Simmons G, Clapham PR, Parmentier M, Proudfoot AE. A chimeric MIP-1alpha/RANTES protein demonstrates the use of different regions of the RANTES protein to bind and activate its receptors. J Leukoc Biol. 2001 Jun; 69(6):977-85.
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        43. Clapham PR, McKnight A. HIV-1 receptors and cell tropism. Br Med Bull. 2001; 58:43-59.
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        44. Proudfoot AE, Fritchley S, Borlat F, Shaw JP, Vilbois F, Zwahlen C, Trkola A, Marchant D, Clapham PR, Wells TN. The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity. J Biol Chem. 2001 Apr 6; 276(14):10620-6.
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        45. Dejucq N, Simmons G, Clapham PR. T-cell line adaptation of human immunodeficiency virus type 1 strain SF162: effects on envelope, vpu and macrophage-tropism. J Gen Virol. 2000 Dec; 81(Pt 12):2899-904.
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        46. Simmons G, Reeves JD, Hibbitts S, Stine JT, Gray PW, Proudfoot AE, Clapham PR. Co-receptor use by HIV and inhibition of HIV infection by chemokine receptor ligands. Immunol Rev. 2000 Oct; 177:112-26.
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        47. Sabroe I, Peck MJ, Van Keulen BJ, Jorritsma A, Simmons G, Clapham PR, Williams TJ, Pease JE. A small molecule antagonist of chemokine receptors CCR1 and CCR3. Potent inhibition of eosinophil function and CCR3-mediated HIV-1 entry. J Biol Chem. 2000 Aug 25; 275(34):25985-92.
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        48. Elsner J, Mack M, Brühl H, Dulkys Y, Kimmig D, Simmons G, Clapham PR, Schlöndorff D, Kapp A, Wells TN, Proudfoot AE. Differential activation of CC chemokine receptors by AOP-RANTES. J Biol Chem. 2000 Mar 17; 275(11):7787-94.
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        49. Stine JT, Wood C, Hill M, Epp A, Raport CJ, Schweickart VL, Endo Y, Sasaki T, Simmons G, Boshoff C, Clapham P, Chang Y, Moore P, Gray PW, Chantry D. KSHV-encoded CC chemokine vMIP-III is a CCR4 agonist, stimulates angiogenesis, and selectively chemoattracts TH2 cells. Blood. 2000 Feb 15; 95(4):1151-7.
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        50. Reeves JD, Hibbitts S, Simmons G, McKnight A, Azevedo-Pereira JM, Moniz-Pereira J, Clapham PR. Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4-negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism in vivo. J Virol. 1999 Sep; 73(9):7795-804.
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        51. Dejucq N, Simmons G, Clapham PR. Expanded tropism of primary human immunodeficiency virus type 1 R5 strains to CD4(+) T-cell lines determined by the capacity to exploit low concentrations of CCR5. J Virol. 1999 Sep; 73(9):7842-7.
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        52. Hibbitts S, Reeves JD, Simmons G, Gray PW, Epstein LG, Schols D, de Clercq E, Wells TN, Proudfoot AE, Clapham PR. Coreceptor ligand inhibition of fetal brain cell infection by HIV type 1. AIDS Res Hum Retroviruses. 1999 Jul 20; 15(11):989-1000.
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        53. Proudfoot AE, Wells TN, Clapham PR. Chemokine receptors--future therapeutic targets for HIV? Biochem Pharmacol. 1999 Mar 1; 57(5):451-63.
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        54. Clapham PR, Reeves JD, Simmons G, Dejucq N, Hibbitts S, McKnight A. HIV coreceptors, cell tropism and inhibition by chemokine receptor ligands. Mol Membr Biol. 1999 Jan-Mar; 16(1):49-55.
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        55. Simmons G, Reeves JD, McKnight A, Dejucq N, Hibbitts S, Power CA, Aarons E, Schols D, De Clercq E, Proudfoot AE, Clapham PR. CXCR4 as a functional coreceptor for human immunodeficiency virus type 1 infection of primary macrophages. J Virol. 1998 Oct; 72(10):8453-7.
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        56. Reeves JD, Heveker N, Brelot A, Alizon M, Clapham PR, Picard L. The second extracellular loop of CXCR4 is involved in CD4-independent entry of human immunodeficiency virus type 2. J Gen Virol. 1998 Jul; 79 ( Pt 7):1793-9.
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        57. McKnight A, Dittmar MT, Moniz-Periera J, Ariyoshi K, Reeves JD, Hibbitts S, Whitby D, Aarons E, Proudfoot AE, Whittle H, Clapham PR. A broad range of chemokine receptors are used by primary isolates of human immunodeficiency virus type 2 as coreceptors with CD4. J Virol. 1998 May; 72(5):4065-71.
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        58. Mack M, Luckow B, Nelson PJ, Cihak J, Simmons G, Clapham PR, Signoret N, Marsh M, Stangassinger M, Borlat F, Wells TN, Schlöndorff D, Proudfoot AE. Aminooxypentane-RANTES induces CCR5 internalization but inhibits recycling: a novel inhibitory mechanism of HIV infectivity. J Exp Med. 1998 Apr 20; 187(8):1215-24.
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        59. Bron R, Klasse PJ, Wilkinson D, Clapham PR, Pelchen-Matthews A, Power C, Wells TN, Kim J, Peiper SC, Hoxie JA, Marsh M. Promiscuous use of CC and CXC chemokine receptors in cell-to-cell fusion mediated by a human immunodeficiency virus type 2 envelope protein. J Virol. 1997 Nov; 71(11):8405-15.
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        60. Dittmar MT, Simmons G, Hibbitts S, O'Hare M, Louisirirotchanakul S, Beddows S, Weber J, Clapham PR, Weiss RA. Langerhans cell tropism of human immunodeficiency virus type 1 subtype A through F isolates derived from different transmission groups. J Virol. 1997 Oct; 71(10):8008-13.
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        61. Kledal TN, Rosenkilde MM, Coulin F, Simmons G, Johnsen AH, Alouani S, Power CA, Lüttichau HR, Gerstoft J, Clapham PR, Clark-Lewis I, Wells TN, Schwartz TW. A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma-associated herpesvirus. Science. 1997 Sep 12; 277(5332):1656-9.
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        62. Willett BJ, Picard L, Hosie MJ, Turner JD, Adema K, Clapham PR. Shared usage of the chemokine receptor CXCR4 by the feline and human immunodeficiency viruses. J Virol. 1997 Sep; 71(9):6407-15.
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        63. Clapham PR, Weiss RA. Immunodeficiency viruses. Spoilt for choice of co-receptors. Nature. 1997 Jul 17; 388(6639):230-1.
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        64. Dittmar MT, Simmons G, Donaldson Y, Simmonds P, Clapham PR, Schulz TF, Weiss RA. Biological characterization of human immunodeficiency virus type 1 clones derived from different organs of an AIDS patient by long-range PCR. J Virol. 1997 Jul; 71(7):5140-7.
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        65. Picard L, Simmons G, Power CA, Meyer A, Weiss RA, Clapham PR. Multiple extracellular domains of CCR-5 contribute to human immunodeficiency virus type 1 entry and fusion. J Virol. 1997 Jul; 71(7):5003-11.
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        66. Picard L, Wilkinson DA, McKnight A, Gray PW, Hoxie JA, Clapham PR, Weiss RA. Role of the amino-terminal extracellular domain of CXCR-4 in human immunodeficiency virus type 1 entry. Virology. 1997 Apr 28; 231(1):105-11.
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        67. Simmons G, Clapham PR, Picard L, Offord RE, Rosenkilde MM, Schwartz TW, Buser R, Wells TN, Proudfoot AE. Potent inhibition of HIV-1 infectivity in macrophages and lymphocytes by a novel CCR5 antagonist. Science. 1997 Apr 11; 276(5310):276-9.
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        68. Dittmar MT, McKnight A, Simmons G, Clapham PR, Weiss RA, Simmonds P. HIV-1 tropism and co-receptor use. Nature. 1997 Feb 6; 385(6616):495-6.
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        69. McKnight A, Wilkinson D, Simmons G, Talbot S, Picard L, Ahuja M, Marsh M, Hoxie JA, Clapham PR. Inhibition of human immunodeficiency virus fusion by a monoclonal antibody to a coreceptor (CXCR4) is both cell type and virus strain dependent. J Virol. 1997 Feb; 71(2):1692-6.
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        70. Simmons G, Wilkinson D, Reeves JD, Dittmar MT, Beddows S, Weber J, Carnegie G, Desselberger U, Gray PW, Weiss RA, Clapham PR. Primary, syncytium-inducing human immunodeficiency virus type 1 isolates are dual-tropic and most can use either Lestr or CCR5 as coreceptors for virus entry. J Virol. 1996 Dec; 70(12):8355-60.
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        71. Endres MJ, Clapham PR, Marsh M, Ahuja M, Turner JD, McKnight A, Thomas JF, Stoebenau-Haggarty B, Choe S, Vance PJ, Wells TN, Power CA, Sutterwala SS, Doms RW, Landau NR, Hoxie JA. CD4-independent infection by HIV-2 is mediated by fusin/CXCR4. Cell. 1996 Nov 15; 87(4):745-56.
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        72. McKnight A, Shotton C, Cordell J, Jones I, Simmons G, Clapham PR. Location, exposure, and conservation of neutralizing and nonneutralizing epitopes on human immunodeficiency virus type 2 SU glycoprotein. J Virol. 1996 Jul; 70(7):4598-606.
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        73. Weiss RA, Clapham PR. Hot fusion of HIV. Nature. 1996 Jun 20; 381(6584):647-8.
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        74. Pelchen-Matthews A, Clapham P, Marsh M. Role of CD4 endocytosis in human immunodeficiency virus infection. J Virol. 1995 Dec; 69(12):8164-8.
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        75. McKnight A, Clapham PR. Immune escape and tropism of HIV. Trends Microbiol. 1995 Sep; 3(9):356-61.
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        76. Simmons G, McKnight A, Takeuchi Y, Hoshino H, Clapham PR. Cell-to-cell fusion, but not virus entry in macrophages by T-cell line tropic HIV-1 strains: a V3 loop-determined restriction. Virology. 1995 Jun 1; 209(2):696-700.
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        77. McKnight A, Weiss RA, Shotton C, Takeuchi Y, Hoshino H, Clapham PR. Change in tropism upon immune escape by human immunodeficiency virus. J Virol. 1995 May; 69(5):3167-70.
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        78. Patience C, McKnight A, Clapham PR, Boyd MT, Weiss RA, Schulz TF. CD26 antigen and HIV fusion? Science. 1994 May 20; 264(5162):1159-60; author reply 1162-5.
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        79. McKnight A, Clapham PR, Weiss RA. HIV-2 and SIV infection of nonprimate cell lines expressing human CD4: restrictions to replication at distinct stages. Virology. 1994 May 15; 201(1):8-18.
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        80. Clapham P, McKnight A, Simmons G, Weiss R. Is CD4 sufficient for HIV entry? Cell surface molecules involved in HIV infection. Philos Trans R Soc Lond B Biol Sci. 1993 Oct 29; 342(1299):67-73.
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        81. Palker TJ, Riggs ER, Spragion DE, Muir AJ, Scearce RM, Randall RR, McAdams MW, McKnight A, Clapham PR, Weiss RA, et al. Mapping of homologous, amino-terminal neutralizing regions of human T-cell lymphotropic virus type I and II gp46 envelope glycoproteins. J Virol. 1992 Oct; 66(10):5879-89.
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        82. McKnight A, Clapham PR, Goudsmit J, Cheingsong-Popov R, Weber JN, Weiss RA. Development of HIV-1 group-specific neutralizing antibodies after seroconversion. AIDS. 1992 Aug; 6(8):799-802.
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        83. Clapham PR, McKnight A, Weiss RA. Human immunodeficiency virus type 2 infection and fusion of CD4-negative human cell lines: induction and enhancement by soluble CD4. J Virol. 1992 Jun; 66(6):3531-7.
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        84. Broliden PA, von Gegerfelt A, Clapham P, Rosen J, Fenyö EM, Wahren B, Broliden K. Identification of human neutralization-inducing regions of the human immunodeficiency virus type 1 envelope glycoproteins. Proc Natl Acad Sci U S A. 1992 Jan 15; 89(2):461-5.
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        85. McKeating J, Balfe P, Clapham P, Weiss RA. Recombinant CD4-selected human immunodeficiency virus type 1 variants with reduced gp120 affinity for CD4 and increased cell fusion capacity. J Virol. 1991 Sep; 65(9):4777-85.
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        86. Clapham PR, Blanc D, Weiss RA. Specific cell surface requirements for the infection of CD4-positive cells by human immunodeficiency virus types 1 and 2 and by Simian immunodeficiency virus. Virology. 1991 Apr; 181(2):703-15.
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        87. McDougal JS, Maddon PJ, Orloff G, Clapham PR, Dalgleish AG, Jamal S, Weiss RA, Axel RA. Role of CD4 in the penetration of cells by HIV. Adv Exp Med Biol. 1991; 300:145-54; discussion 155-8.
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        88. Clements GJ, Price-Jones MJ, Stephens PE, Sutton C, Schulz TF, Clapham PR, McKeating JA, McClure MO, Thomson S, Marsh M, et al. The V3 loops of the HIV-1 and HIV-2 surface glycoproteins contain proteolytic cleavage sites: a possible function in viral fusion? AIDS Res Hum Retroviruses. 1991 Jan; 7(1):3-16.
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        89. Moore JP, Sattentau QJ, Clapham PR. Enhancement of soluble CD4-mediated HIV neutralization and gp 120 binding by CD4 autoantibodies and monoclonal antibodies. AIDS Res Hum Retroviruses. 1990 Nov; 6(11):1273-9.
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        90. Durda PJ, Bacheler L, Clapham P, Jenoski AM, Leece B, Matthews TJ, McKnight A, Pomerantz R, Rayner M, Weinhold KJ. HIV-1 neutralizing monoclonal antibodies induced by a synthetic peptide. AIDS Res Hum Retroviruses. 1990 Sep; 6(9):1115-23.
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        91. McKeating JA, McKnight A, McIntosh K, Clapham PR, Mulder C, Weiss RA. Evaluation of human and simian immunodeficiency virus plaque and neutralization assays. J Gen Virol. 1989 Dec; 70 ( Pt 12):3327-33.
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        92. Weber J, Clapham P, McKeating J, Stratton M, Robey E, Weiss R. Infection of brain cells by diverse human immunodeficiency virus isolates: role of CD4 as receptor. J Gen Virol. 1989 Oct; 70 ( Pt 10):2653-60.
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        93. Weiss RA, Clapham PR, McClure M, Marsh M. The CD4 receptor for the AIDS virus. Biochem Soc Trans. 1989 Aug; 17(4):644-7.
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        94. Arthos J, Deen KC, Chaikin MA, Fornwald JA, Sathe G, Sattentau QJ, Clapham PR, Weiss RA, McDougal JS, Pietropaolo C, et al. Identification of the residues in human CD4 critical for the binding of HIV. Cell. 1989 May 5; 57(3):469-81.
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        95. Tersmette M, van Dongen JJ, Clapham PR, de Goede RE, Wolvers-Tettero IL, Geurts van Kessel A, Huisman JG, Weiss RA, Miedema F. Human immunodeficiency virus infection studied in CD4-expressing human-murine T-cell hybrids. Virology. 1989 Feb; 168(2):267-73.
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        96. Clapham PR, Weber JN, Whitby D, McIntosh K, Dalgleish AG, Maddon PJ, Deen KC, Sweet RW, Weiss RA. Soluble CD4 blocks the infectivity of diverse strains of HIV and SIV for T cells and monocytes but not for brain and muscle cells. Nature. 1989 Jan 26; 337(6205):368-70.
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        97. Sommerfelt MA, Williams BP, Clapham PR, Solomon E, Goodfellow PN, Weiss RA. Human T cell leukemia viruses use a receptor determined by human chromosome 17. Science. 1988 Dec 16; 242(4885):1557-9.
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        98. Maddon PJ, McDougal JS, Clapham PR, Dalgleish AG, Jamal S, Weiss RA, Axel R. HIV infection does not require endocytosis of its receptor, CD4. Cell. 1988 Sep 9; 54(6):865-74.
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        99. Dalgleish AG, Chanh TC, Kennedy RC, Kanda P, Clapham PR, Weiss RA. Neutralization of diverse HIV-1 strains by monoclonal antibodies raised against a gp41 synthetic peptide. Virology. 1988 Jul; 165(1):209-15.
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        100. Berman PW, Groopman JE, Gregory T, Clapham PR, Weiss RA, Ferriani R, Riddle L, Shimasaki C, Lucas C, Lasky LA, et al. Human immunodeficiency virus type 1 challenge of chimpanzees immunized with recombinant envelope glycoprotein gp120. Proc Natl Acad Sci U S A. 1988 Jul; 85(14):5200-4.
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        101. Weiss RA, Clapham PR, Weber JN, Whitby D, Tedder RS, O'Connor T, Chamaret S, Montagnier L. HIV-2 antisera cross-neutralize HIV-1. AIDS. 1988 Apr; 2(2):95-100.
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        102. Sattentau QJ, Clapham PR, Weiss RA, Beverley PC, Montagnier L, Alhalabi MF, Gluckmann JC, Klatzmann D. The human and simian immunodeficiency viruses HIV-1, HIV-2 and SIV interact with similar epitopes on their cellular receptor, the CD4 molecule. AIDS. 1988 Apr; 2(2):101-5.
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        103. Thomas EK, Weber JN, McClure J, Clapham PR, Singhal MC, Shriver MK, Weiss RA. Neutralizing monoclonal antibodies to the AIDS virus. AIDS. 1988 Feb; 2(1):25-9.
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        104. Weiss RA, Clapham PR, McClure MO, McKeating JA, McKnight A, Dalgleish AG, Sattentau QJ, Weber JN. Human immunodeficiency viruses: neutralization and receptors. J Acquir Immune Defic Syndr. 1988; 1(6):536-41.
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        105. Clapham PR, Weiss RA, Dalgleish AG, Exley M, Whitby D, Hogg N. Human immunodeficiency virus infection of monocytic and T-lymphocytic cells: receptor modulation and differentiation induced by phorbol ester. Virology. 1987 May; 158(1):44-51.
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        106. Weller IV, Carne CA, Sattentau Q, Smith A, Tedder RS, Clapham P, Dalgleish A, Weber J, Adler MW. Human immunodeficiency virus (HIV) infection in the regular sexual partners of homosexual men with AIDS and persistent generalised lymphadenopathy. J Med Virol. 1987 May; 22(1):91-8.
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        107. Hausmann EH, Gelderblom HR, Clapham PR, Pauli G, Weiss RA. Detection of HIV envelope specific antibodies by immunoelectron microscopy and correlation with antibody titer and virus neutralizing activity. J Virol Methods. 1987 May; 16(1-2):125-37.
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        108. Timar J, Nagy K, Robertson D, Clapham P, Weiss RA. Ultrastructure and immunoelectron microscopy of human T-cell leukaemia virus type I-producing lymphoid and non-lymphoid human tumour cells. J Gen Virol. 1987 Apr; 68 ( Pt 4):1011-20.
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        109. Weber JN, Clapham PR, Weiss RA, Parker D, Roberts C, Duncan J, Weller I, Carne C, Tedder RS, Pinching AJ, et al. Human immunodeficiency virus infection in two cohorts of homosexual men: neutralising sera and association of anti-gag antibody with prognosis. Lancet. 1987 Jan 17; 1(8525):119-22.
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        110. Pauli G, Hausmann E, Weiss R, Clapham P, Schneider J, Hunsmann G, Gallo RC, Daniel MD, Koch MA, Gelderblom H. LAV/HTLV-III: fine-structure analysis, localization of structural proteins, and detection of envelope antigens by patient sera. Haematol Blood Transfus. 1987; 31:407-9.
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        111. Weiss RA, Clapham PR, Dalgleish AG, Weber JN. Neutralization and receptor recognition of human T-lymphotropic retroviruses. Haematol Blood Transfus. 1987; 31:387-91.
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        112. Weiss RA, Clapham PR, Weber JN, Dalgleish AG, Lasky LA, Berman PW. Variable and conserved neutralization antigens of human immunodeficiency virus. Nature. 1986 Dec 11-17; 324(6097):572-5.
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        113. 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):333-48.
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        114. McDougal JS, Maddon PJ, Dalgleish AG, Clapham PR, Littman DR, Godfrey M, Maddon DE, Chess L, Weiss RA, Axel R. The T4 glycoprotein is a cell-surface receptor for the AIDS virus. Cold Spring Harb Symp Quant Biol. 1986; 51 Pt 2:703-11.
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        115. Hoshino H, Clapham PR, Weiss RA, Miyoshi I, Yoshida M, Miwa M. Human T-cell leukemia virus type I: pseudotype neutralization of Japanese and American isolates with human and rabbit sera. Int J Cancer. 1985 Dec 15; 36(6):671-5.
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        116. Weiss RA, Clapham PR, Cheingsong-Popov R, Dalgleish AG, Carne CA, Weller IV, Tedder RS. Neutralization of human T-lymphotropic virus type III by sera of AIDS and AIDS-risk patients. Nature. 1985 Jul 4-10; 316(6023):69-72.
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        117. Weiss RA, Clapham P, Nagy K, Hoshino H. Envelope properties of human T-cell leukemia viruses. Curr Top Microbiol Immunol. 1985; 115:235-46.
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        118. 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 20-1985 Jan 2; 312(5996):763-7.
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        119. Tedder RS, Shanson DC, Jeffries DJ, Cheingsong-Popov R, Clapham P, Dalgleish A, Nagy K, Weiss RA. Low prevalence in the UK of HTLV-I and HTLV-II infection in subjects with AIDS, with extended lymphadenopathy, and at risk of AIDS. Lancet. 1984 Jul 21; 2(8395):125-8.
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        120. Nagy K, Clapham P, Weiss R, Földes I. [Specific antibodies against human T cell leukemia virus found in AIDS patients]. Orv Hetil. 1984 Jun 24; 125(26):1557-60.
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        121. Clapham P, Nagy K, Weiss RA. Pseudotypes of human T-cell leukemia virus types 1 and 2: neutralization by patients' sera. Proc Natl Acad Sci U S A. 1984 May; 81(9):2886-9.
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        122. Hoshino H, Weiss RA, Clapham P, Miwa M, Miyoshi I, Yoshida M, Sugimura T. Pseudotype viruses bearing envelope antigens of Japanese isolates of human T-cell leukemia viruses type I. Princess Takamatsu Symp. 1984; 15:159-64.
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        123. Clapham P, Nagy K, Cheingsong-Popov R, Exley M, Weiss RA. Productive infection and cell-free transmission of human T-cell leukemia virus in a nonlymphoid cell line. Science. 1983 Dec 9; 222(4628):1125-7.
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        124. Nagy K, Clapham P, Cheingsong-Popov R, Weiss RA. Human T-cell leukemia virus type I: induction of syncytia and inhibition by patients' sera. Int J Cancer. 1983 Sep 15; 32(3):321-8.
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