Structural comparison of HIV-1 envelope spikes with and without the V1/V2 loop

Journal of Virology

Volumn 85, Issue 6, 2011, Pages 2741-2750

  Hu, Guiqing ^a   Liu, Jun ^b   Taylor, Kenneth A ^a   Roux, Kenneth H ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ELECTRON TOMOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMAGE ANALYSIS; IMAGE PROCESSING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL TROPISM; VIRION; VIRUS CORE; VIRUS ENVELOPE; VIRUS MORPHOLOGY; VIRUS SPIKE; VIRUS STRAIN;

CRYOELECTRON MICROSCOPY; HIV ENVELOPE PROTEIN GP120; HIV-1; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTANT PROTEINS; SEQUENCE DELETION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79952368717     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01612-10     Document Type: Article

References (99)

1. Barnett, S. W., et al. 2001. The ability of an oligomeric human immunodeficiency virus type 1 (HIV-1) envelope antigen to elicit neutralizing antibodies against primary HIV-1 isolates is improved following partial deletion of the second hypervariable region. J. Virol. 75:5526-5540. (Pubitemid 32488146)
2. Barnett, S. W., I. K. Srivastava, J. B. Ulmer, J. J. Donnelly, and R. Rappuoli. 2005. Development of V2-deleted trimeric envelope vaccine candidates from human immunodeficiency virus type 1 (HIV-1) subtypes B and C. Microbes Infect. 7:1386-1391. (Pubitemid 41655968)
3. Beddows, S., et al. 2005. Evaluating the immunogenicity of a disulfide-stabilized, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 79:8812-8827. (Pubitemid 40934792)
4. Bewley, C. A., J. M. Louis, R. Ghirlando, and G. M. Clore. 2002. Design of a novel peptide inhibitor of HIV fusion that disrupts the internal trimeric coiled-coil of gp41. J. Biol. Chem. 277:14238-14245.
5. Binley, J. M., et al. 2000. A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J. Virol. 74:627-643. (Pubitemid 30036198)
6. Bontjer, I., et al. 2009. Optimization of human immunodeficiency virus type 1 envelope glycoproteins with V1/V2 deleted, using virus evolution. J. Virol. 83:368-383.
7. Cao, J., et al. 1997. Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J. Virol. 71:9808-9812. (Pubitemid 27492434)
8. Center, R. J., P. L. Earl, J. Lebowitz, P. Schuck, and B. Moss. 2000. The human immunodeficiency virus type 1 gp120 V2 domain mediates gp41-independent intersubunit contacts. J. Virol. 74:4448-4455. (Pubitemid 30237869)
9. Center, R. J., et al. 2002. Oligomeric structure of the human immunodeficiency virus type 1 envelope protein on the virion surface. J. Virol. 76:7863-7867. (Pubitemid 34761009)
10. Chan, D. C., D. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
11. Chen, B., et al. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-843.
12. Chertova, E., et al. 2002. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J. Virol. 76:5315-5325. (Pubitemid 34517882)
13. Davis, K. L., et al. 2009. Human immunodeficiency virus type 2 (HIV-2)/HIV-1 envelope chimeras detect high titers of broadly reactive HIV-1 V3-specific antibodies in human plasma. J. Virol. 83:1240-1259.
14. Derby, N. R., et al. 2006. Antibody response elicited in macaques immunized with human immunodeficiency virus type 1 (HIV-1) SF162-derived gp140 envelope immunogens: comparison with those elicited during homologous simian/human immunodeficiency virus SHIVSF162P4 and heterologous HIV-1 infection. J. Virol. 80:8745-8762. (Pubitemid 44384884)
15. Doms, R. W., and J. P. Moore. 2000. HIV-1 membrane fusion: targets of opportunity. J. Cell Biol. 151:F9-F13.
16. Edinger, A. L., et al. 2000. Characterization and epitope mapping of neutralizing monoclonal antibodies produced by immunization with oligomeric simian immunodeficiency virus envelope protein. J. Virol. 74:7922-7935. (Pubitemid 30641636)
17. Feig, M., J. Karanicolas, and C. L. Brooks III. 2004. MMTSB Tool Set: enhanced sampling and multiscale modeling methods for applications in structural biology. J. Mol. Graph. Model. 22:377-395.
18. Forsell, M. N., W. R. Schief, and R. T. Wyatt. 2009. Immunogenicity of HIV-1 envelope glycoprotein oligomers. Curr. Opin. HIV AIDS 4:380-387.
19. Frank, J., et al. 1996. Spider and Web: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116:190-199.
20. Gorny, M. K., et al. 2005. Identification of a new quaternary neutralizing epitope on human immunodeficiency virus type 1 virus particles. J. Virol. 79:5232-5237. (Pubitemid 40464273)
21. Grundner, C., et al. 2005. Analysis of the neutralizing antibody response elicited in rabbits by repeated inoculation with trimeric HIV-1 envelope glycoproteins. Virology 331:33-46. (Pubitemid 39593631)
22. Gzyl, J., et al. 2004. Effect of partial and complete variable loop deletions of the human immunodeficiency virus type 1 envelope glycoprotein on the breadth of gp160-specific immune responses. Virology 318:493-506. (Pubitemid 38224293)
23. Helseth, E., U. Olshevsky, C. Furman, and J. Sodroski. 1991. Human immunodeficiency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein. J. Virol. 65:2119-2123.
24. Ho, D. D., et al. 1991. Another discontinuous epitope on glycoprotein gp120 that is important in human immunodeficiency virus type 1 neutralization is identified by a monoclonal antibody. Proc. Natl. Acad. Sci. U. S. A. 88:8949-8952.
25. Hohn, M., et al. 2007. SPARX, a new environment for cryo-EM image processing. J. Struct. Biol. 157:47-55.
26. Huang, C., et al. 2005. Structure of a V3-containing HIV-1 gp120 core. Science 310:1025-1028. (Pubitemid 41611916)
27. Huang, C. C., et al. 2007. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317:1930-1934.
28. Hwang, S. S., T. J. Boyle, H. K. Lyerly, and B. R. Cullen. 1992. Identification of envelope V3 loop as the major determinant of CD4 neutralization sensitivity of HIV-1. Science 257:535-537.
29. Iyer, S. P. N., et al. 2007. Purified proteolytically mature HIV type 1 SOSIP gp140 envelope trimers. AIDS Res. Hum. Retroviruses 23:817-828.
30. Jin, T., F. Guo, Y. W. Chen, A. Howard, and Y. Z. Zhang. 2009. Crystal structure of Ara h 3, a major allergen in peanut. Mol. Immunol. 46:1796-1804.
31. Johnson, M. J. W. E., et al. 2002. A replication-competent, neutralization-sensitive variant of simian immunodeficiency virus lacking 100 amino acids of envelope. J. Virol. 76:2075-2086.
32. Kang, S. M., et al. 2005. Modified HIV envelope proteins with enhanced binding to neutralizing monoclonal antibodies. Virology 331:20-32.
33. Kang, Y. K., et al. 2009. Structural and immunogenicity studies of a cleaved, stabilized envelope trimer derived from subtype A HIV-1. Vaccine 27:5120-5132.
34. Koito, A., G. Harrowe, J. A. Levy, and C. Cheng-Mayer. 1994. Functional role of the V1/V2 region of human immunodeficiency virus type 1 envelope glycoprotein gp120 in infection of primary macrophages and soluble CD4 neutralization. J. Virol. 68:2253-2259. (Pubitemid 24091903)
35. Kolchinsky, P., E. Kiprilov, P. Bartley, R. Rubinstein, and J. Sodroski. 2001. Loss of a single N-linked glycan allows CD4-independent human immunodeficiency virus type 1 infection by altering the position of the gp120 V1/V2 variable loops. J. Virol. 75:3435-3443. (Pubitemid 32225906)
36. Krachmarov, C., et al. 2005. Antibodies that are cross-reactive for human immunodeficiency virus type 1 clade A and clade B V3 domains are common in patient sera from Cameroon, but their neutralization activity is usually restricted by epitope masking. J. Virol. 79:780-790. (Pubitemid 40053861)
37. Kwong, P. D., et al. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420:678-682. (Pubitemid 36764500)
38. Kwong, P. D., et al. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659. (Pubitemid 28289647)
39. Kwong, P. D., R. Wyatt, Q. J. Sattentau, J. Sodroski, and W. A. Hendrickson. 2000. Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus. J. Virol. 74:1961-1972. (Pubitemid 30434055)
40. Laakso, M. M., et al. 2007. V3 loop truncations in HIV-1 envelope impart resistance to coreceptor inhibitors and enhanced sensitivity to neutralizing antibodies. PLoS Pathog. 3:e117.
41. Lake, J. A., and K. R. Leonard. 1974. Structure and protein distribution for the capsid of Caulobacter crescentus bacteriophage φCbK. J. Mol. Biol. 86:499-518.
42. LaRosa, G. J., et al. 1990. Conserved sequence and structural elements in the HIV-1 principal neutralizing determinant. Science 249:932-935.
43. Letvin, N. L., et al. 2006. Preserved CD4+ central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312:1530-1533. (Pubitemid 43865893)
44. Li, M., et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125. (Pubitemid 41098552)
45. Lin, G., et al. 2007. Replication-competent variants of human immunodeficiency virus type 2 lacking the V3 loop exhibit resistance to chemokine receptor antagonists. J. Virol. 81:9956-9966. (Pubitemid 350067699)
46. Liu, J., A. Bartesaghi, M. J. Borgnia, G. Sapiro, and S. Subramaniam. 2008. Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109-113.
47. Liu, J., Y. Deng, A. K. Dey, J. P. Moore, and M. Lu. 2009. Structure of the HIV-1 gp41 membrane-proximal ectodomain region in a putative prefusion conformation. Biochemistry 48:2915-2923.
48. Lu, M., S. C. Blacklow, and P. S. Kim. 1995. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2:1075-1082.
49. Ly, A., and L. Stamatatos. 2000. V2 loop glycosylation of the human immunodeficiency virus type 1 SF162 envelope facilitates interaction of this protein with CD4 and CCR5 receptors and protects the virus from neutralization by anti-V3 loop and anti-CD4 binding site antibodies. J. Virol. 74:6769-6776. (Pubitemid 30470659)
50. Malvoisin, E., M. P. Kieny, and F. Wild. 1997. Self-association of truncated forms of HIV-1 gp120. Virus Res. 49:163-172. (Pubitemid 27252785)
51. Mascola, J. R., et al. 2005. Recommendations for the design and use of standard virus panels to assess neutralizing antibody responses elicited by candidate human immunodeficiency virus type 1 vaccines. J. Virol. 79:10103-10107. (Pubitemid 41098551)
52. Meissner, E. G., K. M. Duus, F. Gao, X. F. Yu, and L. Su. 2004. Characterization of a thymus-tropic HIV-1 isolate from a rapid progressor: role of the envelope. Virology 328:74-88. (Pubitemid 39221914)
53. Mikhailov, A. M., and B. K. Vainshtein. 1971. Electron microscope determination of the three-dimensional structure of the extended tail of the T6 bacteriophage. Soviet Phys. Crystallogr. 16:428-436.
54. Moore, J. P., and J. Sodroski. 1996. Antibody cross-competition analysis of the human immunodeficiency virus type 1 gp120 exterior envelope glycoprotein. J. Virol. 70:1863-1872. (Pubitemid 26062950)
55. Moore, P. L., et al. 2006. Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J. Virol. 80:2515-2528. (Pubitemid 43271557)
56. Morikita, T., et al. 1997. The V1/V2 region of human immunodeficiency virus type 1 modulates the sensitivity to neutralization by soluble CD4 and cellular tropism. AIDS Res. Hum. Retroviruses 13:1291-1299.
57. Myszka, D. G., et al. 2000. Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. U. S. A. 97:9026-9031.
58. Nabatov, A. A., et al. 2004. Intrapatient alterations in the human immunodeficiency virus type 1 gp120 V1V2 and V3 regions differentially modulate coreceptor usage, virus inhibition by CC/CXC chemokines, soluble CD4, and the b12 and 2G12 monoclonal antibodies. J. Virol. 78:524-530. (Pubitemid 37549764)
59. Owens, R. J., and R. W. Compans. 1990. The human immunodeficiency virus type 1 envelope glycoprotein precursor acquires aberrant intermolecular disulfide bonds that may prevent normal proteolytic processing. Virology 179:827-833.
60. Pan, Y., B. Ma, and R. Nussinov. 2005. CD4 binding partially locks the bridging sheet in gp120 but leaves the B2/3 strands flexible. J. Mol. Biol. 350:514-527.
61. Pancera, M., et al. 2005. Soluble mimetics of human immunodeficiency virus type 1 viral spikes produced by replacement of the native trimerization domain with a heterologous trimerization motif: characterization and ligand binding analysis. J. Virol. 79:9954-9969. (Pubitemid 41022337)
62. Pancera, M., et al. 2010. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl. Acad. Sci. U. S. A. 107:1166-1171.
63. Pantophlet, R., and D. R. Burton. 2006. Gp120: target for neutralizing HIV-1 antibodies. Annu. Rev. Immunol. 24:739-769.
64. Parren, P. W., J. P. Moore, D. R. Burton, and Q. J. Sattentau. 1999. The neutralizing antibody response to HIV-1: viral evasion and escape from humoral immunity. AIDS 13:S137-S162.
65. Pettersen, E. F., et al. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
66. Phogat, S., and R. Wyatt. 2007. Rational modifications of HIV-1 envelope glycoproteins for immunogen design. Curr. Pharm. Des. 13:213-227.
67. Pinter, A., et al. 2004. The V1/V2 domain of gp120 is a global regulator of the sensitivity of primary human immunodeficiency virus type 1 isolates to neutralization by antibodies commonly induced upon infection. J. Virol. 78:5205-5215. (Pubitemid 38581472)
68. Poignard, P., et al. 2003. Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J. Virol. 77:353-365. (Pubitemid 36004975)
69. Recht, B., B. Frangione, E. Franklin, and E. Loghem. 1981. Structural studies of a human gamma3 myeloma protein (Goe) that binds staph protein A. J. Immunol. 127:917-923. (Pubitemid 11051128)
70. Rusche, J. R., et al. 1988. Antibodies that inhibit fusion of human immunodeficiency virus-infected cells bind a 24-amino acid sequence of the viral envelope, gp120. Proc. Natl. Acad. Sci. U. S. A. 85:3198-3202.
71. Sanders, R., et al. 2002. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 76:8875-8889. (Pubitemid 34864082)
72. Saunders, C. J., et al. 2005. The V1, V2, and V3 regions of the human immunodeficiency virus type 1 envelope differentially affect the viral phenotype in an isolate-dependent manner. J. Virol. 79:9069-9080.
73. Saxton, W. O., W. Baumeister, and M. Hahn. 1984. Three-dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 13:57-70.
74. Schülke, N., et al. 2002. Oligomeric and conformational properties of a proteolytically mature, disulfide-stabilized human immunodeficiency virus type 1 gp140 envelope glycoprotein. J. Virol. 76:7760-7776. (Pubitemid 34760999)
75. Schweighardt, B., et al. 2007. Development of an HIV-1 reference panel of subtype B envelope clones isolated from the plasma of recently infected individuals. J. Acquir. Immune Defic. Syndr. 46:1-11.
76. Srivastava, I. K., et al. 2008. Comparative evaluation of trimeric envelope glycoproteins derived from subtype C and B HIV-1 R5 isolates. Virology 372:273-290. (Pubitemid 351284561)
77. Srivastava, I. K., K. VanDorsten, L. Vojtech, S. W. Barnett, and L. Stamatatos. 2003. Changes in the immunogenic properties of soluble gp140 human immunodeficiency virus envelope constructs upon partial deletion of the second hypervariable region. J. Virol. 77:2310-2320. (Pubitemid 36222754)
78. Stamatatos, L., and C. Cheng-Mayer. 1998. An envelope modification that renders a primary, neutralization-resistant clade B human immunodeficiency virus type 1 isolate highly susceptible to neutralization by sera from other clades. J. Virol. 72:7840-7845. (Pubitemid 28421774)
79. Stanisz, A. M., R. Lieberman, and J. M. Davie. 1984. IgA polymorphism in mice: individual light chains can pair covalently with some alpha heavy chains and non-covalently with others. Mol. Immunol. 21:815-818.
80. Sullivan, N., et al. 1998. CD4-induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization. J. Virol. 72:4694-4703. (Pubitemid 28215644)
81. Walker, L. M., et al. 2009. Broad and potent neutralization antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
82. Wei, X., et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312. (Pubitemid 36378357)
83. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-430. (Pubitemid 27227210)
84. Winkler, H., and K. A. Taylor. 1999. Multivariate statistical analysis of three-dimensional cross-bridge motifs in insect flight muscle. Ultramicroscopy 77:141-152.
85. Winkler, H., and K. A. Taylor. 2006. Accurate marker-free alignment with simultaneous geometry determination and reconstruction of tilt series in electron tomography. Ultramicroscopy 106:240-254.
86. Winkler, H., et al. 2009. Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes. J. Struct. Biol. 165:64-77.
87. Wolk, T., and M. Schreiber. 2006. N-Glycans in the gp120 V1/V2 domain of the HIV-1 strain NL4-3 are indispensable for viral infectivity and resistance against antibody neutralization. Med. Microbiol. Immunol. 195:165-172.
88. Wyatt, R., et al. 1997. Analysis of the interaction of the human immunodeficiency virus type 1 gp120 envelope glycoprotein with the gp41 transmembrane glycoprotein. J. Virol. 71:9722-9731. (Pubitemid 27492421)
89. Wyatt, R., et al. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711. (Pubitemid 28289663)
90. Wyatt, R., et al. 1995. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 69:5723-5733.
91. Yang, X., et al. 2002. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76:4634-4642. (Pubitemid 34309599)
92. York, J., and J. H. Nunberg. 2004. Role of hydrophobic residues in the central ectodomain of gp41 in maintaining the association between human immunodeficiency virus type 1 envelope glycoprotein subunits gp120 and gp41. J. Virol. 78:4921-4926.
93. Yuan, W., J. Bazick, and J. Sodroski. 2006. Characterization of the multiple conformational states of free monomeric and trimeric human immunodeficiency virus envelope glycoproteins after fixation by cross-linker. J. Virol. 80:6725-6737. (Pubitemid 44025172)
94. Yue, L., L. Shang, and E. Hunter. 2009. Truncation of the membrane-spanning domain of human immunodeficiency virus type 1 envelope glycoprotein defines elements required for fusion, incorporation, and infectivity. J. Virol. 83:11588-11598.
95. Zanetti, G., J. A. G. Briggs, K. Grunewald, Q. Sattentau, and S. D. Fuller. 2006. Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog. 2:e83.
96. Zhou, T., et al. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445:732-737. (Pubitemid 46279718)
97. Zhu, P., et al. 2003. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. U. S. A. 100:15812-15817.
98. Zhu, P., et al. 2006. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441:847-852.
99. Zhu, P., H. Winkler, E. Chertova, K. A. Taylor, and K. H. Roux. 2008. Cryoelectron tomography of HIV-1 envelope spikes: further evidence for tripod-like legs. PLoS Pathog. 4:e1000203.