Three-dimensional structures of soluble CD4-bound states of trimeric simian immunodeficiency virus envelope glycoproteins determined by using cryo-electron tomography

Journal of Virology

Volumn 85, Issue 23, 2011, Pages 12114-12123

  White, Tommi A ^a   Bartesaghi, Alberto ^a   Borgnia, Mario J ^a   de la Cruz, M Jason V ^a   Nandwani, Rachna ^a   Hoxie, James A ^b   Bess, Julian W ^c   Lifson, Jeffrey D ^c   Milne, Jacqueline L S ^a   Subramaniam, Sriram ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

17B ANTIBODY; 7D3 ANTIBODY; CD4 ANTIGEN; CHEMOKINE RECEPTOR; EPITOPE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; HETERODIMER; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ARTICLE; BINDING SITE; CELL SURFACE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN QUATERNARY STRUCTURE; SIMIAN IMMUNODEFICIENCY VIRUS; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; VIRION; VIRUS ENVELOPE; VIRUS ISOLATION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD4; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; ELECTRON MICROSCOPE TOMOGRAPHY; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, CCR5; RECOMBINANT PROTEINS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 81255213876     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05297-11     Document Type: Article

References (59)

1. Allan, J. S., J. Strauss, and D. W. Buck. 1990. Enhancement of SIV infection with soluble receptor molecules. Science 247:1084-1088.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Bartesaghi, A., G. Sapiro, and S. Subramaniam. 2005. An energy-based three-dimensional segmentation approach for the quantitative interpretation of electron tomograms. IEEE Trans. Image Process. 14:1314-1323.
4. Bartesaghi, A., et al. 2008. Classification and 3D averaging with missing wedge correction in biological electron tomography. J. Struct. Biol. 162:436-450.
5. Berger, E. A., J. D. Lifson, and L. E. Eiden. 1991. Stimulation of glycoprotein gp120 dissociation from the envelope glycoprotein complex of human immunodeficiency virus type 1 by soluble CD4 and CD4 peptide derivatives: implications for the role of the complementarity-determining region 3-like region in membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 88:8082-8086.
6. Chen, B., et al. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-841.
7. Clements, J. E., J. L. Mankowski, L. Gama, and M. C. Zink. 2008. The accelerated simian immunodeficiency virus macaque model of human immunodeficiency virus-associated neurological disease: from mechanism to treatment. J. Neurovirol. 14:309-317.
8. Cole, K. S., et al. 2001. Characterization of neutralization epitopes of simian immunodeficiency virus (SIV) recognized by rhesus monoclonal antibodies derived from monkeys infected with an attenuated SIV strain. Virology 290:59-73.
9. Crooks, E. T., et al. 2008. Relationship of HIV-1 and SIV envelope glycoprotein trimer occupation and neutralization. Virology 377:364-378.
10. Daar, E. S., X. L. Li, T. Moudgil, and D. D. Ho. 1990. High concentrations of recombinant soluble CD4 are required to neutralize primary human immunodeficiency virus type 1 isolates. Proc. Natl. Acad. Sci. U. S. A. 87:6574-6578.
11. Dalgleish, A. G., et al. 1984. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763-767.
12. Daniel, M. D., et al. 1985. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science 228:1201-1204.
13. Daniel, M. D., et al. 1987. Long-term persistent infection of macaque monkeys with the simian immunodeficiency virus. J. Gen. Virol. 68:3183-3189.
14. Deng, H., et al. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666.
15. Desrosiers, R. C. 1990. The simian immunodeficiency viruses. Annu. Rev. Immunol. 8:557-578.
16. Douglas, N. W., G. H. Munro, and R. S. Daniels. 1997. HIV/SIV glycoproteins: structure-function relationships. J. Mol. Biol. 273:122-149.
17. Earl, P. L., R. W. Doms, and B. Moss. 1992. Multimeric CD4 binding exhibited by human and simian immunodeficiency virus envelope protein dimers. J. Virol. 66:5610-5614.
18. 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.
19. Endres, M. J., et al. 1996. CD4-independent infection by HIV-2 is mediated by fusin/CXCR4. Cell 87:745-756.
20. Faith, S. A., et al. 2010. Induction of antibody-mediated neutralization in SIVmac239 by a naturally acquired V3 mutation. Virology 400:86-92.
21. Feng, Y., C. C. Broder, P. E. Kennedy, and E. A. Berger. 1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877.
22. Gallo, S. A., et al. 2003. The HIV Env-mediated fusion reaction. Biochim. Biophys. Acta 1614:36-50.
23. Gallo, S. A., K. Sackett, S. S. Rawat, Y. Shai, and R. Blumenthal. 2004. The stability of the intact envelope glycoproteins is a major determinant of sensitivity of HIV/SIV to peptidic fusion inhibitors. J. Mol. Biol. 340:9-14.
24. Garlick, R. L., R. J. Kirschner, F. M. Eckenrode, W. G. Tarpley, and C. S. Tomich. 1990. Escherichia coli expression, purification, and biological activity of a truncated soluble CD4. AIDS Res. Hum. Retroviruses 6:465-479.
25. Gazdar, A. F., et al. 1980. Mitogen requirements for the in vitro propagation of cutaneous T-cell lymphomas. Blood 55:409-417.
26. Groenink, M., J. P. Moore, S. Broersen, and H. Schuitemaker. 1995. Equal levels of gp120 retention and neutralization resistance of phenotypically distinct primary human immunodeficiency virus type 1 variants upon soluble CD4 treatment. J. Virol. 69:523-527.
27. Haim, H., et al. 2009. Soluble CD4 and CD4-mimetic compounds inhibit HIV-1 infection by induction of a short-lived activated state. PLoS Pathog. 5:e1000360.
28. Harris, A., et al. 2011. Trimeric HIV-1 glycoprotein gp140 immunogens and native HIV-1 envelope glycoproteins display the same closed and open quaternary molecular architectures. Proc. Natl. Acad. Sci. U. S. A. 108: 11440-11445.
29. Hirsch, V. M., and P. R. Johnson. 1994. Pathogenic diversity of simian immunodeficiency viruses. Virus Res. 32:183-203.
30. Hirsch, V. M., and J. D. Lifson. 2000. Simian immunodeficiency virus infection of monkeys as a model system for the study of AIDS pathogenesis, treatment, and prevention. Adv. Pharmacol. 49:437-477.
31. Hoxie, J. A., et al. 1986. Alterations in T4 (CD4) protein and mRNA synthesis in cells infected with HIV. Science 234:1123-1127.
32. Huang, C. C., et al. 2005. Structure of a V3-containing HIV-1 gp120 core. Science 310:1025-1028.
33. Kim, M., et al. 2001. The stoichiometry of trimeric SIV glycoprotein interaction with CD4 differs from that of anti-envelope antibody Fab fragments. J. Biol. Chem. 276:42667-42676.
34. Kremer, J. R., D. N. Mastronarde, and J. R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
35. 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.
36. LaBranche, C. C., et al. 1994. Biological, molecular, and structural analysis of a cytopathic variant from a molecularly cloned simian immunodeficiency virus. J. Virol. 68:5509-5522.
37. Letvin, N. L., et al. 1985. Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science 230:71-73.
38. 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.
39. Ludtke, S. J., P. R. Baldwin, and W. Chiu. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128:82-97.
40. Mansfield, K. G., and A. A. Lackner. 1997. Simian immunodeficiency virus-inoculated macaques acquire Mycobacterium avium from potable water during AIDS. J. Infect. Dis. 175:184-187.
41. Moore, J. P., J. A. McKeating, W. A. Norton, and Q. J. Sattentau. 1991. Direct measurement of soluble CD4 binding to human immunodeficiency virus type 1 virions: gp120 dissociation and its implications for virus-cell binding and fusion reactions and their neutralization by soluble CD4. J. Virol. 65:1133-1140.
42. Moore, J. P., J. A. McKeating, R. A. Weiss, and Q. J. Sattentau. 1990. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250:1139-1142.
43. O'Brien, W. A., S. H. Mao, Y. Cao, and J. P. Moore. 1994. 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. 68:5264-5269.
44. Orloff, S. L., M. S. Kennedy, A. A. Belperron, P. J. Maddon, and J. S. McDougal. 1993. Two mechanisms of soluble CD4 (sCD4)-mediated inhibition of human immunodeficiency virus type 1 (HIV-1) infectivity and their relation to primary HIV-1 isolates with reduced sensitivity to sCD4. J. Virol. 67:1461-1471.
45. Pettersen, E., et al. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
46. Raport, C. J., J. Gosling, V. L. Schweickart, P. W. Gray, and I. F. Charo. 1996. Molecular cloning and functional characterization of a novel human CC chemokine receptor (CCR5) for RANTES, MIP-1beta, and MIP-1alpha. J. Biol. Chem. 271:17161-17166.
47. Rizzuto, C. D., et al. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949-1953.
48. Rudensey, L. M., J. T. Kimata, E. M. Long, B. Chackerian, and J. Overbaugh. 1998. Changes in the extracellular envelope glycoprotein of variants that evolve during the course of simian immunodeficiency virus SIVMne infection affect neutralizing antibody recognition, syncytium formation, and macrophage tropism but not replication, cytopathicity, or CCR-5 coreceptor recognition. J. Virol. 72:209-217.
49. Samson, M., et al. 1996. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722-725.
50. Sasseville, V. G., and A. A. Lackner. 1997. Neuropathogenesis of simian immunodeficiency virus infection in macaque monkeys. J. Neurovirol. 3:1-9.
51. Sattentau, Q. J., and J. P. Moore. 1991. Conformational changes induced in the human immunodeficiency virus envelope glycoprotein by soluble CD4 binding. J. Exp. Med. 174:407-415.
52. Sattentau, Q. J., J. P. Moore, F. Vignaux, F. Traincard, and P. Poignard. 1993. Conformational changes induced in the envelope glycoproteins of the human and simian immunodeficiency viruses by soluble receptor binding. J. Virol. 67:7383-7393.
53. Schenten, D., et al. 1999. Effects of soluble CD4 on simian immunodeficiency virus infection of CD4-positive and CD4-negative cells. J. Virol. 73:5373-5380.
54. Smith, D. H., et al. 1987. Blocking of HIV-1 infectivity by a soluble, secreted form of the CD4 antigen. Science 238:1704-1707.
55. Stamatatos, L., A. Werner, and C. Cheng-Mayer. 1994. Differential regulation of cellular tropism and sensitivity to soluble CD4 neutralization by the envelope gp120 of human immunodeficiency virus type 1. J. Virol. 68:4973-4979.
56. Steckbeck, J. D., and K. S. Cole. 2006. Dissecting the humoral immune response to simian immunodeficiency virus: mechanisms of antibody-mediated virus neutralization. Immunol. Res. 36:51-60.
57. Trkola, A., et al. 1996. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384:184-187.
58. White, T. A., et al. 2010. Molecular architectures of trimeric SIV and HIV-1 envelope glycoproteins on intact viruses: strain-dependent variation in quaternary structure. PLoS Pathog. 6:e1001249.
59. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.