Subunit organization of the membrane-bound HIV-1 envelope glycoprotein trimer

Nature Structural and Molecular Biology

Volumn 19, Issue 9, 2012, Pages 893-899

  Mao, Youdong ^a   Wang, Liping ^a   Gu, Christopher ^a   Herschhorn, Alon ^a   Xiang, Shi Hua ^a,d   Haim, Hillel ^a   Yang, Xinzhen ^a   Sodroski, Joseph ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ENVELOPE PROTEIN; GLYCOPROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41;

ARTICLE; CRYOELECTRON MICROSCOPY; HOST; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE;

CELL LINE; CRYOELECTRON MICROSCOPY; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP160; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84866061123     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2351     Document Type: Article

References (60)

1. Barré-Sinoussi, F. et al. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune defciency syndrome (AIDS). Science 220, 868-871 (1983).
2. Allan, J.S. et al. Major glycoprotein antigens that induce antibodies in AIDS patients are encoded by HTLV-III. Science 228, 1091-1094 (1985).
3. Moulard, M. & Decroly, E. Maturation of HIV envelope glycoprotein precursors by cellular endoproteases. Biochim. Biophys. Acta 1469, 121-132 (2000).
4. Wyatt, R. & Sodroski, J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280, 1884-1888 (1998).
5. Barin, F. et al. Virus envelope protein of HTLV-III represents major target antigen for antibodies in AIDS patients. Science 228, 1094-1096 (1985).
6. Kwong, P.D. et al. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659 (1998).
7. Zhou, T. et al. Structural defnition of a conserved neutralization epitope on HIV-1 gp120. Nature 445, 732-737 (2007).
8. Pancera, M. et al. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl. Acad. Sci. USA 107, 1166-1171 (2010).
9. Weissenhorn, W., Dessen, A., Harrison, S.C., Skehel, J.J. & Wiley, D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387, 426-430 (1997).
10. Chan, D.C., Fass, D., Berger, J.M. & Kim, P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89, 263-273 (1997).
11. Buzon, V. et al. Crystal structure of HIV-1 gp41 including both fusion peptide and membrane proximal external regions. PLoS Pathog. 6, e1000880 (2010).
12. Zhu, P. et al. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441, 847-852 (2006).
13. Zanetti, G., Briggs, J.A.G., Grunewald, K., Sattentau, Q.J. & Fuller, S.D. Cryo-electron tomographic structure of an immunodefciency virus envelope complex in situ. PLoS Pathog. 2, e83 (2006).
14. Liu, J., Bartesaghi, A., Borgnia, M.J., Sapiro, G. & Subramanian, S. Molecular architecture of native HIV-1 gp120 trimers. Nature 455, 109-113 (2008).
15. White, T.A. et al. Molecular architectures of trimeric SIV and HIV-1 envelope glycoproteins on intact viruses: strain-dependent variation in quaternary structure. PLoS Pathog. 6, e1001249 (2010).
16. Wu, S.R. et al. Single-particle cryoelectron microscopy analysis reveals the HIV-1 spike as a tripod structure. Proc. Natl. Acad. Sci. USA 107, 18844-18849 (2010).
17. Harris, A. et al. 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. USA 108, 11440-11445 (2011).
18. Hu, G., Liu, J., Taylor, K.A. & Roux, K.H. Structural comparison of HIV-1 envelope spikes with and without the V1/V2 loop. J. Virol. 85, 2741-2750 (2011).
19. Frank, J. Three-dimensional Electron Microscopy of Macromolecular Assemblies: Visualization of Biological Molecules in Their Native State (Oxford Univ. Press, 2006).
20. Sigworth, F.J. A maximum-likelihood approach to single-particle image refnement. J. Struct. Biol. 122, 328-339 (1998).
21. Scheres, S.H.W. et al. Maximum-likelihood multi-reference refnement for electron microscopy images. J. Mol. Biol. 348, 139-149 (2005).
22. Liao, H.Y. & Frank, J. Defnition and estimation of resolution in single-particle reconstructions. Structure 18, 768-775 (2010).
23. Sattentau, Q.J. & Moore, J.P. Conformational changes induced in the human immunodefciency virus envelope glycoprotein by soluble CD4 binding. J. Exp. Med. 174, 407-415 (1991).
24. Myszka, D.G. et al. Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. USA 97, 9026-9031 (2000).
25. Yuan, W., Bazick, J. & Sodroski, J. Characterization of the multiple conformational states of free monomeric and trimeric human immunodefciency virus envelope glycoproteins after fxation by cross-linker. J. Virol. 80, 6725-6737 (2006).
26. Xiang, S.H. et al. A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immunodefciency virus envelope glycoprotein trimer. J. Virol. 84, 3147-3161 (2010).
27. Finzi, A. et al. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol. Cell 37, 656-667 (2010).
28. Xiang, S.H. et al. Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodefciency virus type 1 gp120 envelope glycoprotein. J. Virol. 76, 9888-9899 (2002).
29. Chen, B. et al. Structure of an unliganded simian immunodefciency virus gp120 core. Nature 433, 834-841 (2005).
30. McLellan, J.S. et al. Structure of HIV-1 gp120 V1V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
31. Mische, C.C. et al. An alternative conformation of the gp41 heptad repeat 1 region coiled coil exists in the human immunodefciency virus (HIV-1) envelope glycoprotein precursor. Virology 338, 133-143 (2005).
32. Helseth, E., Olshevsky, U., Furman, C. & Sodroski, J. Human immunodefciency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein. J. Virol. 65, 2119-2123 (1991).
33. Wang, S. et al. Interhelical interactions in the gp41 core: implications for activation of HIV-1 membrane fusion. Biochemistry 41, 7283-7292 (2002).
34. Dimitrov, A.S., Louis, J.M., Bewley, C.A., Clore, G.M. & Blumenthal, R. Conformational changes in HIV-1 gp41 in the course of HIV-1 envelope glycoprotein-mediated fusion and inactivation. Biochemistry 44, 12471-12479 (2005).
35. Sen, J. et al. Alanine scanning mutagenesis of HIV-1 gp41 heptad repeat 1: insight into the gp120-gp41 interaction. Biochemistry 49, 5057-5065 (2010).
36. Chertova, E. et al. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), is the primary determinant of SU content of purifed human immunodefciency virus type 1 and simian immunodefciency virus. J. Virol. 76, 5315-5325 (2002).
37. Rossio, J.L. et al. Inactivation of human immunodefciency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J. Virol. 72, 7992-8001 (1998).
38. Chakrabarti, B.K. et al. HIV type 1 Env precursor cleavage state affects recognition by both neutralizing and nonneutralizing gp41 antibodies. AIDS Res. Hum. Retroviruses 27, 877-887 (2011).
39. Pancera, M. & Wyatt, R. Selective recognition of oligomeric HIV-1 primary isolate envelope glycoproteins by potently neutralizing ligands requires effcient precursor cleavage. Virology 332, 145-156 (2005).
40. Edwards, T.G. et al. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodefciency virus type 1 envelope protein. J. Virol. 76, 2683-2691 (2002).
41. Harrison, S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 15, 690-698 (2008).
42. Kwon, Y.D. et al. Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops. Proc. Natl. Acad. Sci. USA 109, 5663-5668 (2012).
43. Musich, T. et al. A conserved determinant in the V1 loop of HIV-1 modulates the V3 loop to prime low CD4 use and macrophage infection. J. Virol. 85, 2397-2405 (2011).
44. Kolchinsky, P., Kiprilov, E., Bartley, P., Rubenstein, R. & Sodroski, J. Loss of a single N-linked glycan allows CD4-independent HIV-1 infection by altering the position of the gp120 V1/V2 variable loops. J. Virol. 75, 3435-3443 (2001).
45. Zhang, P.F. et al. A variable region 3 (V3) mutation determines a global neutralization phenotype and CD4-independent infectivity of a human immunodefciency virus type 1 envelope associated with a broadly cross-reactive, primary virus-neutralizing antibody response. J. Virol. 76, 644-655 (2002).
46. Walker, L.M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
47. Trkola, A. et al. Human monoclonal antibody 2G12 defnes a distinctive neutralization epitope on the gp120 glycoprotein of human immunodefciency virus type 1. J. Virol. 70, 1100-1108 (1996).
48. Wu, X. et al. Rational design of envelope identifes broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861 (2010).
49. Zhou, T. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817 (2010).
50. Zhang, X., Jin, L., Fang, Q., Hui, W.H. & Zhou, Z.H. 3.3 Å cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell 141, 472-482 (2010).
51. +-driven ATP synthase. Nature 481, 214-218 (2012).
52. Becker, T. et al. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326, 1369-1373 (2009).
53. Binley, J.M. et al. A recombinant human immunodefciency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfde bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J. Virol. 74, 627-643 (2000).
54. Pejchal, R. et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103 (2011).
55. Herschhorn, A., Marasco, W.A. & Hizi, A. Antibodies and lentiviruses that specifcally recognize a T cell epitope derived from HIV-1 Nef protein and presented by HLA-C. J. Immunol. 185, 7623-7632 (2010).
56. Huang, Z., Baldwin, P.R., Mullapudi, S. & Penczek, P.A. Automated determination of parameters describing power spectra of micrograph images in electron microscopy. J. Struct. Biol. 144, 79-94 (2003).
57. Mindell, J.A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
58. Shaikh, T.R. et al. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc. 3, 1941-1974 (2008).
59. Scheres, S.H.W., Nunez-Ramirez, R., Sorzano, C.O.S. & Carazo, J.M. Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc. 3, 977-990 (2008).
60. Pettersen, E.F. et al. UCSF Chimera\a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).