Neutralization sensitivity of HIV-1 Env-pseudotyped virus clones is determined by co-operativity between mutations which modulate the CD4-binding site and those that affect gp120-gp41 stability

Virology

Volumn 337, Issue 1, 2005, Pages 136-148

  Beddows, Simon ^a,b   Zheng, Natalie N ^c   Herrera, Carolina ^b   Michael, Elizabeth ^b   Barnes, Kelly ^b   Moore, John P ^b   Daniels, Rod S ^c   Weber, Jonathan N ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Antibody; CD4 binding site; Envelope; gp120; gp41; HIV; Mutants; Neutralization

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MUTANT PROTEIN; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIGEN BINDING; ARTICLE; BINDING SITE; CHIMERA; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR STABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION;

ANTIGENS, CD4; BINDING SITES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 19444376783     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2005.03.033     Document Type: Article

References (60)

1. S. Beddows, S. Lister, R. Cheingsong, C. Bruck, and J. Weber Comparison of the antibody repertoire generated in healthy volunteers following immunization with a monomeric recombinant gp120 construct derived from a CCR5/CXCR4-using human immunodeficiency virus type 1 isolate with sera from naturally infected individuals J. Virol. 73 2 1999 1740 1745
2. J.M. Binley, T. Wrin, B. Korber, M.B. Zwick, M. Wang, C. Chappey, G. Stiegler, R. Kunert, S. Zolla-Pazner, H. Katinger, C.J. Petropoulos, and D.R. Burton Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies J. Virol. 78 23 2004 13232 13252
3. D.R. Burton, J. Pyati, R. Koduri, S.J. Sharp, G.B. Thornton, P.W. Parren, L.S. Sawyer, R.M. Hendry, N. Dunlop, and P.L. Nara Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody Science 266 5187 1994 1024 1027
4. D.R. Burton, R.C. Desrosiers, R.W. Doms, W.C. Koff, P.D. Kwong, J.P. Moore, G.J. Nabel, J. Sodroski, I.A. Wilson, and R.T. Wyatt HIV vaccine design and the neutralizing antibody problem Nat. Immunol. 5 3 2004 233 236
5. J. Cao, L. Bergeron, E. Helseth, M. Thali, H. Repke, and J. Sodroski Effects of amino acid changes in the extracellular domain of the human immunodeficiency virus type 1 gp41 envelope glycoprotein J. Virol. 67 5 1993 2747 2755
6. M. Cayabyab, G.B. Karlsson, B.A. Etemad-Moghadam, W. Hofmann, T. Steenbeke, M. Halloran, J.W. Fanton, M.K. Axthelm, N.L. Letvin, and J.G. Sodroski Changes in human immunodeficiency virus type 1 envelope glycoproteins responsible for the pathogenicity of a multiply passaged simian-human immunodeficiency virus (SHIV-HXBc2) J. Virol. 73 2 1999 976 984
7. S.S. Chen, C.N. Lee, W.R. Lee, K. McIntosh, and T.H. Lee Mutational analysis of the leucine zipper-like motif of the human immunodeficiency virus type 1 envelope transmembrane glycoprotein J. Virol. 67 6 1993 3615 3619
8. C. Cheng-Mayer, A. Brown, J. Harouse, P.A. Luciw, and A.J. Mayer Selection for neutralization resistance of the simian/human immunodeficiency virus SHIVSF33A variant in vivo by virtue of sequence changes in the extracellular envelope glycoprotein that modify N-linked glycosylation J. Virol. 73 7 1999 5294 5300
9. A.J. Conley, M.K. Gorny, J.A. Kessler, L.J. Boots, M. Ossorio-Castro, S. Koenig, D.W. Lineberger, E.A. Emini, C. Williams, and S. Zolla-Pazner Neutralization of primary human immunodeficiency virus type 1 isolates by the broadly reactive anti-V3 monoclonal antibody, 447-52D J. Virol. 68 11 1994 6994 7000
10. A.J. Conley, J.A. Kessler II, L.J. Boots, P.M. McKenna, W.A. Schleif, E.A. Emini, G.E. Mark III, H. Katinger, E.K. Cobb, S.M. Lunceford, S.R. Rouse, and K.K. Murthy The consequence of passive administration of an anti-human immunodeficiency virus type 1 neutralizing monoclonal antibody before challenge of chimpanzees with a primary virus isolate J. Virol. 70 10 1996 6751 6758
11. R.I. Connor, K.E. Sheridan, C. Lai, L. Zhang, and D.D. Ho Characterization of the functional properties of env genes from long-term survivors of human immunodeficiency virus type 1 infection J. Virol. 70 8 1996 5306 5311
12. N.W. Douglas, G.H. Munro, and R.S. Daniels HIV/SIV glycoproteins: structure-function relationships J. Mol. Biol. 273 1 1997 122 149
13. M.P. D'Souza, D. Livnat, J.A. Bradac, and S.H. Bridges Evaluation of monoclonal antibodies to human immunodeficiency virus type 1 primary isolates by neutralization assays: performance criteria for selecting candidate antibodies for clinical trials. AIDS Clinical Trials Group Antibody Selection Working Group J. Infect. Dis. 175 5 1997 1056 1062
14. J.W. Dubay, S.J. Roberts, B. Brody, and E. Hunter Mutations in the leucine zipper of the human immunodeficiency virus type 1 transmembrane glycoprotein affect fusion and infectivity J. Virol. 66 8 1992 4748 4756
15. K.E. Follis, M. Trahey, R.A. La Casse, and J.H. Nunberg Continued utilization of CCR5 coreceptor by a newly derived T-cell line-adapted isolate of human immunodeficiency virus type 1 J. Virol. 72 9 1998 7603 7608
16. T.R. Fouts, J.M. Binley, A. Trkola, J.E. Robinson, and J.P. Moore Neutralization of the human immunodeficiency virus type 1 primary isolate JR-FL by human monoclonal antibodies correlates with antibody binding to the oligomeric form of the envelope glycoprotein complex J. Virol. 71 4 1997 2779 2785
17. D.A. Garber, G. Silvestri, and M.B. Feinberg Prospects for an AIDS vaccine: three big questions, no easy answers Lancet Infect. Dis. 4 7 2004 397 413
18. C.J. Gordon, M.A. Muesing, A.E. Proudfoot, C.A. Power, J.P. Moore, and A. Trkola Enhancement of human immunodeficiency virus type 1 infection by the CC-chemokine RANTES is independent of the mechanism of virus-cell fusion J. Virol. 73 1 1999 684 694
19. M.K. Gorny, A.J. Conley, S. Karwowska, A. Buchbinder, J.Y. Xu, E.A. Emini, S. Koenig, and S. Zolla-Pazner Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody J. Virol. 66 12 1992 7538 7542
20. R.D. Klausner, A.S. Fauci, L. Corey, G.J. Nabel, H. Gayle, S. Berkley, B.F. Haynes, D. Baltimore, C. Collins, R.G. Douglas, J. Esparza, D.P. Francis, N.K. Ganguly, J.L. Gerberding, M.I. Johnston, M.D. Kazatchkine, A.J. McMichael, M.W. Makgoba, G. Pantaleo, P. Piot, Y. Shao, E. Tramont, H. Varmus, and J.N. Wasserheit Medicine. The need for a global HIV vaccine enterprise Science 300 5628 2003 2036 2039
21. P.D. Kwong, R. Wyatt, J. Robinson, R.W. Sweet, J. Sodroski, and W.A. Hendrickson Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody Nature 393 6686 1998 648 659
22. C.C. LaBranche, T.L. Hoffman, J. Romano, B.S. Haggarty, T.G. Edwards, T.J. Matthews, R.W. Doms, and J.A. Hoxie Determinants of CD4 independence for a human immunodeficiency virus type 1 variant map outside regions required for coreceptor specificity J. Virol. 73 12 1999 10310 10319
23. R.A. LaCasse, K.E. Follis, T. Moudgil, M. Trahey, J.M. Binley, V. Planelles, S. Zolla-Pazner, and J.H. Nunberg Coreceptor utilization by human immunodeficiency virus type 1 is not a primary determinant of neutralization sensitivity J. Virol. 72 3 1998 2491 2495
24. M. Leavitt, E.J. Park, I.A. Sidorov, D.S. Dimitrov, and G.V. Quinnan Jr. Concordant modulation of neutralization resistance and high infectivity of the primary human immunodeficiency virus type 1 MN strain and definition of a potential gp41 binding site in gp120 J. Virol. 77 1 2003 560 570
25. P.F. Lin, W. Blair, T. Wang, T. Spicer, Q. Guo, N. Zhou, Y.F. Gong, H.G. Wang, R. Rose, G. Yamanaka, B. Robinson, C.B. Li, R. Fridell, C. Deminie, G. Demers, Z. Yang, L. Zadjura, N. Meanwell, and R. Colonno A small molecule HIV-1 inhibitor that targets the HIV-1 envelope and inhibits CD4 receptor binding Proc. Natl. Acad. Sci. U.S.A. 100 19 2003 11013 11018
26. J.R. Mascola, M.G. Lewis, G. Stiegler, D. Harris, T.C. Van Cott, D. Hayes, M.K. Louder, C.R. Brown, C.V. Sapan, S.S. Frankel, Y. Lu, M.L. Robb, H. Katinger, and D.L. Birx Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies J. Virol. 73 5 1999 4009 4018
27. J.R. Mascola, G. Stiegler, T.C. Van Cott, H. Katinger, C.B. Carpenter, C.E. Hanson, H. Beary, D. Hayes, S.S. Frankel, D.L. Birx, and M.G. Lewis Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies Nat. Med. 6 2 2000 207 210
28. H. Mo, L. Stamatatos, J.E. Ip, C.F. Barbas, P.W. Parren, D.R. Burton, J.P. Moore, and D.D. Ho Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12 J. Virol. 71 9 1997 6869 6874
29. D.C. Montefiori, R.G. Collman, T.R. Fouts, J.Y. Zhou, M. Bilska, J.A. Hoxie, J.P. Moore, and D.P. Bolognesi Evidence that antibody-mediated neutralization of human immunodeficiency virus type 1 by sera from infected individuals is independent of coreceptor usage J. Virol. 72 3 1998 1886 1893
30. J.P. Moore, Y. Cao, L. Qing, Q.J. Sattentau, J. Pyati, R. Koduri, J. Robinson, C.F. Barbas, D.R. Burton, and D.D. Ho Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120 J. Virol. 69 1 1995 101 109
31. J.P. Moore, Y. Cao, J. Leu, L. Qin, B. Korber, and D.D. Ho Inter- and intraclade neutralization of human immunodeficiency virus type: 1. genetic clades do not correspond to neutralization serotypes but partially correspond to gp120 antigenic serotypes J. Virol. 70 1 1996 427 444
32. T. Muster, F. Steindl, M. Purtscher, A. Trkola, A. Klima, G. Himmler, F. Ruker, and H. Katinger A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1 J. Virol. 67 11 1993 6642 6647
33. T. Muster, R. Guinea, A. Trkola, M. Purtscher, A. Klima, F. Steindl, P. Palese, and H. Katinger Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS J. Virol. 68 6 1994 4031 4034
34. P.N. Nyambi, J. Nkengasong, P. Lewi, K. Andries, W. Janssens, K. Fransen, L. Heyndrickx, P. Piot, and G. van der Groen Multivariate analysis of human immunodeficiency virus type 1 neutralization data J. Virol. 70 9 1996 6235 6243
35. W.A. O'Brien, S.H. Mao, Y. Cao, and J.P. Moore Macrophage-tropic and T-cell line-adapted chimeric strains of human immunodeficiency virus type 1 differ in their susceptibilities to neutralization by soluble CD4 at different temperatures J. Virol. 68 8 1994 5264 5269
36. R. Pantophlet, S.E. Ollmann, P. Poignard, P.W. Parren, I.A. Wilson, and D.R. Burton Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120 J. Virol. 77 1 2003 642 658
37. E.J. Park, and G.V. Quinnan Jr. Both neutralization resistance and high infectivity phenotypes are caused by mutations of interacting residues in the human immunodeficiency virus type 1 gp41 leucine zipper and the gp120 receptor- and coreceptor-binding domains J. Virol. 73 7 1999 5707 5713
38. E.J. Park, L.K. Vujcic, R. Anand, T.S. Theodore, and G.V. Quinnan Jr. Mutations in both gp120 and gp41 are responsible for the broad neutralization resistance of variant human immunodeficiency virus type 1 MN to antibodies directed at V3 and non-V3 epitopes J. Virol. 72 9 1998 7099 7107
39. E.J. Park, M.K. Gorny, S. Zolla-Pazner, and G.V. Quinnan Jr. A global neutralization resistance phenotype of human immunodeficiency virus type 1 is determined by distinct mechanisms mediating enhanced infectivity and conformational change of the envelope complex J. Virol. 74 9 2000 4183 4191
40. P. Pugach, S.E. Kuhmann, J. Taylor, A.J. Marozsan, A. Snyder, T. Ketas, S.M. Wolinsky, B.T. Korber, and J.P. Moore The prolonged culture of human immunodeficiency virus type 1 in primary lymphocytes increases its sensitivity to neutralization by soluble CD4 Virology 321 1 2004 8 22
41. J.D. Reeves, J.L. Miamidian, M.J. Biscone, F.-H. Lee, N. Ahmad, T.C. Pierson, and R.W. Doms Impact of mutations in the coreceptor binding site on human immunodeficiency virus type 1 fusion, infection, and entry inhibitor sensitivity J. Virol. 78 10 2004 5476 5485
42. M.S. Reitz Jr., C. Wilson, C. Naugle, R.C. Gallo, and M. Robert-Guroff Generation of a neutralization-resistant variant of HIV-1 is due to selection for a point mutation in the envelope gene Cell 54 1 1988 57 63
43. C.D. Rizzuto, R. Wyatt, N. Hernandez-Ramos, Y. Sun, P.D. Kwong, W.A. Hendrickson, and J. Sodroski A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding Science 280 5371 1998 1949 1953
44. P. Roben, J.P. Moore, M. Thali, J. Sodroski, C.F. Barbas, and D.R. Burton Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1 J. Virol. 68 8 1994 4821 4828
45. R.W. Sanders, B. Korber, M. Lu, B. Berkhout, and J.P. Moore Mutational analyses and natural variability of the gp41 ectodomain C.L. Kuiken B. Foley E. Freed B. Hahn B. Korber P.A. Marx F. McCutchan J.W. Mellors S. Wolinsky HIV Sequence Compendium 2002 2002 Theoretical Biology and Biophysics Group, Los Alamos National Laboratory Los Alamos, NM 43 68 LA-UR 03-3564
46. L.S. Sawyer, M.T. Wrin, L. Crawford-Miksza, B. Potts, Y. Wu, P.A. Weber, R.D. Alfonso, and C.V. Hanson Neutralization sensitivity of human immunodeficiency virus type 1 is determined in part by the cell in which the virus is propagated J. Virol. 68 3 1994 1342 1349
47. R. Shibata, T. Igarashi, N. Haigwood, A. Buckler-White, R. Ogert, W. Ross, R. Willey, M.W. Cho, and M.A. Martin Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys Nat. Med. 5 2 1999 204 210
48. Z. Si, M. Cayabyab, and J. Sodroski Envelope glycoprotein determinants of neutralization resistance in a simian-human immunodeficiency virus (SHIV-HXBc2P 3.2) derived by passage in monkeys J. Virol. 75 9 2001 4208 4218
49. M. Thali, U. Olshevsky, C. Furman, D. Gabuzda, J. Li, and J. Sodroski Effects of changes in gp120-CD4 binding affinity on human immunodeficiency virus type 1 envelope glycoprotein function and soluble CD4 sensitivity J. Virol. 65 9 1991 5007 5012
50. M. Thali, U. Olshevsky, C. Furman, D. Gabuzda, M. Posner, and J. Sodroski Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody J. Virol. 65 11 1991 6188 6193
51. M. Thali, J.P. Moore, C. Furman, M. Charles, D.D. Ho, J. Robinson, and J. Sodroski Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding J. Virol. 67 7 1993 3978 3988
52. A. Trkola, A.B. Pomales, H. Yuan, B. Korber, P.J. Maddon, G.P. Allaway, H. Katinger, C.F. Barbas, D.R. Burton, and D.D. Ho Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG J. Virol. 69 11 1995 6609 6617
53. A. Trkola, M. Purtscher, T. Muster, C. Ballaun, A. Buchacher, N. Sullivan, K. Srinivasan, J. Sodroski, J.P. Moore, and H. Katinger Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1 J. Virol. 70 2 1996 1100 1108
54. A. Trkola, T. Ketas, V.N. Kewalramani, F. Endorf, J.M. Binley, H. Katinger, J. Robinson, D.R. Littman, and J.P. Moore Neutralization sensitivity of human immunodeficiency virus type 1 primary isolates to antibodies and CD4-based reagents is independent of coreceptor usage J. Virol. 72 3 1998 1876 1885
55. R.S. Veazey, R.J. Shattock, M. Pope, J.C. Kirijan, J. Jones, Q. Hu, T. Ketas, P.A. Marx, P.J. Klasse, D.R. Burton, and J.P. Moore Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120 Nat. Med. 9 3 2003 343 346
56. B.A. Watkins, S. Buge, K. Aldrich, A.E. Davis, J. Robinson, M.S. Reitz Jr., and M. Robert-Guroff Resistance of human immunodeficiency virus type 1 to neutralization by natural antisera occurs through single amino acid substitutions that cause changes in antibody binding at multiple sites J. Virol. 70 12 1996 8431 8437
57. J. Weber, E.M. Fenyo, S. Beddows, P. Kaleebu, A. Bjorndal UNAIDS Neutralization serotypes of human immunodeficiency virus type 1 field isolates are not predicted by genetic subtype J. Virol. 70 11 1996 7827 7832
58. C. Wild, J.W. Dubay, T. Greenwell, T. Baird Jr., T.G. Oas, C. McDanal, E. Hunter, and T. Matthews Propensity for a leucine zipper-like domain of human immunodeficiency virus type 1 gp41 to form oligomers correlates with a role in virus-induced fusion rather than assembly of the glycoprotein complex Proc. Natl. Acad. Sci. U.S.A. 91 26 1994 12676 12680
59. T. Wrin, T.P. Loh, J.C. Vennari, H. Schuitemaker, and J.H. Nunberg Adaptation to persistent growth in the H9 cell line renders a primary isolate of human immunodeficiency virus type 1 sensitive to neutralization by vaccine sera J. Virol. 69 1 1995 39 48
60. M.B. Zwick, A.F. Labrijn, M. Wang, C. Spenlehauer, E.O. Saphire, J.M. Binley, J.P. Moore, G. Stiegler, H. Katinger, D.R. Burton, and P.W. Parren Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41 J. Virol. 75 22 2001 10892 10905