Enzyme digests eliminate nonfunctional Env from HIV-1 particle surfaces, leaving native Env trimers intact and viral infectivity unaffected

Journal of Virology

Volumn 85, Issue 12, 2011, Pages 5825-5839

  Crooks, Ema T ^a   Tong, Tommy ^a   Osawa, Keiko ^a   Binley, James M ^a  

^a TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 160; GLYCOPROTEIN GP 41; VIRUS ENVELOPE PROTEIN;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; VIRUS INFECTIVITY; VIRUS LIKE AGENT; VIRUS PARTICLE; VIRUS SHEDDING;

ANTIBODIES, MONOCLONAL; BINDING SITES; CELL LINE; ENDOPLASMIC RETICULUM; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GLYCOSIDE HYDROLASES; GLYCOSYLATION; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP160; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; PEPTIDE HYDROLASES; PROTEIN BINDING; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79958086672     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00154-11     Document Type: Article

References (84)

1. Abrahamyan, L. G., R. M. Markosyan, J. P. Moore, F. S. Cohen, and G. B. Melikyan. 2003. Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion. J. Virol. 77:5829-5836.
2. Berman, P. W., W. M. Nunes, and O. K. Haffar. 1988. Expression of membrane-associated and secreted variants of gp160 of human immunodeficiency virus type 1 in vitro and in continuous cell lines. J. Virol. 62:3135-3142.
3. Bhattacharyya, S., and T. J. Hope. 2011. Full-length Ebola glycoprotein accumulates in the endoplasmic reticulum. Virol. J. 8:11.
4. Binley, J., et al. 2010. Role of complex carbohydrates in human immunodeficiency virus type 1 infection and resistance to antibody neutralization. J. Virol. 84:5637-5655.
5. Binley, J. M., et al. 2003. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions. J. Virol. 77:5678-5684.
6. Binley, J. M., et al. 2008. Profiling the specificity of neutralizing antibodies in a large panel of HIV-1 plasmas from subtype B and C chronic infections. J. Virol. 82:11651-11668.
7. 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.
8. Binley, J. M., et al. 2002. Enhancing the proteolytic maturation of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 76:2606- 2616.
9. Binley, J. M., et al. 2004. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78:13232-13252.
10. Bosch, V., and M. Pawlita. 1990. Mutational analysis of the human immunodeficiency virus type 1 env gene product proteolytic cleavage site. J. Virol. 64:2337-2344.
11. Burton, D. R., et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024- 1027.
12. Calarese, D. A., et al. 2003. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300:2065-2071.
13. 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.
14. Chen, X., et al. 2005. Pseudovirion particle production by live poxvirus human immunodeficiency virus vaccine vector enhances humoral and cellular immune responses. J. Virol. 79:5537-5547.
15. 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.
16. Crooks, E. T., et al. 2008. Relationship of HIV-1 and SIV envelope glycoprotein trimer occupation and neutralization. Virology 377:364-378.
17. Crooks, E. T., et al. 2007. A comparative immunogenicity study of HIV-1 virus-like particles bearing various forms of envelope proteins, particles bearing no envelope and soluble monomeric gp120. Virology 366:245-262.
18. Crooks, E. T., et al. 2005. Characterizing anti-HIV monoclonal antibodies and immune sera by defining the mechanism of neutralization. Hum. Antibodies 14:101-113.
19. Cutalo, J. M., L. J. Deterding, and K. B. Tomer. 2004. Characterization of glycopeptides from HIV-I(SF2) gp120 by liquid chromatography mass spectrometry. J. Am. Soc. Mass Spectrom. 15:1545-1555.
20. Dewar, R. L., M. B. Vasudevachari, V. Natarajan, and N. P. Salzman. 1989. Biosynthesis and processing of human immunodeficiency virus type 1 envelope glycoproteins: effects of monensin on glycosylation and transport. J. Virol. 63:2452-2456.
21. Doores, K. J., et al. 2010. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc. Natl. Acad. Sci. U. S. A. 107: 13800-13805.
22. Earl, P. L., R. W. Doms, and B. Moss. 1990. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 87:648-652.
23. Earl, P. L., B. Moss, and R. W. Doms. 1991. Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency virus type 1 envelope protein. J. Virol. 65:2047-2055.
24. Eggink, D., et al. 2010. Lack of complex N-glycans on HIV-1 envelope glycoproteins preserves protein conformation and entry function. Virology 401:236-247.
25. Fenouillet, E., and J. C. Gluckman. 1992. Immunological analysis of human immunodeficiency virus type 1 envelope glycoprotein proteolytic cleavage. Virology 187:825-828.
26. Fenouillet, E., R. Miquelis, and R. Drillien. 1996. Biological properties of recombinant HIV envelope synthesized in CHO glycosylation-mutant cell lines. Virology 218:224-231.
27. Forthal, D. N., and C. Moog. 2009. Fc receptor-mediated antiviral antibodies. Curr. Opin. HIV AIDS 4:388-393.
28. Fouts, T. R., J. M. Binley, A. Trkola, J. E. Robinson, and J. P. Moore. 1997. 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. 71:2779- 2785.
29. Frost, S. D., et al. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. U. S. A. 102:18514-18519.
30. Gagneux, P., and A. Varki. 1999. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 9:747-755.
31. Geyer, H., C. Holschbach, G. Hunsmann, and J. Schneider. 1988. Carbohydrates of human immunodeficiency virus. Structures of oligosaccharides linked to the envelope glycoprotein 120. J. Biol. Chem. 263:11760-11767.
32. Go, E. P., et al. 2008. Glycosylation site-specific analysis of HIV envelope proteins (JR-FL and CON-S) reveals major differences in glycosylation site occupancy, glycoform profiles, and antigenic epitopes' accessibility. J. Proteome Res. 7:1660-1674.
33. Gray, E. S., P. L. Moore, R. A. Pantophlet, and L. Morris. 2007. N-linked glycan modifications in gp120 of human immunodeficiency virus type 1 subtype C render partial sensitivity to 2G12 antibody neutralization. J. Virol. 81:10769-10776.
34. Hammonds, J., et al. 2005. Induction of neutralizing antibodies against human immunodeficiency virus type 1 primary isolates by Gag-Env pseudovirion immunization. J. Virol. 79:14804-14814.
35. Haynes, B. F., and D. C. Montefiori. 2006. Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev. Vaccines 5:347-363.
36. Hioe, C. E., et al. 2010. Anti-V3 monoclonal antibodies display broad neutralizing activities against multiple HIV-1 subtypes. PLoS One 5:e10254.
37. 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.
38. Kieny, M. P., et al. 1988. Improved antigenicity of the HIV env protein by cleavage site removal. Protein Eng. 2:219-225.
39. Kornfeld, R., and S. Kornfeld. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664.
40. LaCasse, R. A., et al. 1999. Fusion-competent vaccines: broad neutralization of primary isolates of HIV. Science 283:357-362.
41. Land, A., D. Zonneveld, and I. Braakman. 2003. Folding of HIV-1 envelope glycoprotein involves extensive isomerization of disulfide bonds and conformation-dependent leader peptide cleavage. FASEB J. 17:1058-1067.
42. Larke, N., et al. 2007. Combined single-clade candidate HIV-1 vaccines induce T cell responses limited by multiple forms of in vivo immune interference. Eur. J. Immunol. 37:566-577.
43. Leaman, D. P., H. Kinkead, and M. B. Zwick. 2010. In-solution virus capture assay helps deconstruct heterogeneous antibody recognition of human immunodeficiency virus type 1. J. Virol. 84:3382-3395.
44. Li, M., et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccineelicited neutralizing antibodies. J. Virol. 79:10108-10125.
45. Li, M., et al. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776- 11790.
46. Li, Y., et al. 1996. Effects of inefficient cleavage of the signal sequence of HIV-1 gp 120 on its association with calnexin, folding, and intracellular transport. Proc. Natl. Acad. Sci. U. S. A. 93:9606-9611.
47. Li, Y., L. Luo, N. Rasool, and C. Y. Kang. 1993. Glycosylation is necessary for the correct folding of human immunodeficiency virus gp120 in CD4 binding. J. Virol. 67:584-588.
48. Li, Y., L. Luo, D. Y. Thomas, and C. Y. Kang. 2000. The HIV-1 Env protein signal sequence retards its cleavage and down-regulates the glycoprotein folding. Virology 272:417-428.
49. Ling, H., P. Xiao, O. Usami, and T. Hattori. 2004. Thrombin activates envelope glycoproteins of HIV type 1 and enhances fusion. Microbes Infect. 6:414-420.
50. McCune, J. M., et al. 1988. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53:55-67.
51. Means, R. E., and R. C. Desrosiers. 2000. Resistance of native, oligomeric envelope on simian immunodeficiency virus to digestion by glycosidases. J. Virol. 74:11181-11190.
52. Michalski, C. J., Y. Li, and C. Y. Kang. 2010. Induction of cytopathic effects and apoptosis in Spodoptera frugiperda cells by the HIV-1 Env glycoprotein signal peptide. Virus Genes 41:341-350.
53. Mizuochi, T., et al. 1990. Diversity of oligosaccharide structures on the envelope glycoprotein gp120 of human immunodeficiency virus 1 from the lymphoblastoid cell line H9. Presence of complex-type oligosaccharides with bisecting N-acetylglucosamine residues. J. Biol. Chem. 265:8519-8524.
54. Moore, J., J. McKeating, R. Weiss, and Q. Sattentau. 1990. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250:1139-1142.
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.
56. Nelson, J. D., et al. 2007. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J. Virol. 81:4033-4043.
57. Nyambi, P. N., et al. 1998. Mapping of epitopes exposed on intact human immunodeficiency virus type 1 (HIV-1) virions: a new strategy for studying the immunologic relatedness of HIV-1. J. Virol. 72:9384-9391.
58. Pantophlet, R., R. O. Aguilar-Sino, T. Wrin, L. A. Cavacini, and D. R. Burton. 2007. Analysis of the neutralization breadth of the anti-V3 antibody F425-B4e8 and re-assessment of its epitope fine specificity by scanning mutagenesis. Virology 364:441-453.
59. Phogat, S., R. T. Wyatt, and G. B. Karlsson Hedestam. 2007. Inhibition of HIV-1 entry by antibodies: potential viral and cellular targets. J. Intern. Med. 262:26-43.
60. 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.
61. Poon, B., et al. 2005. Induction of humoral immune responses following vaccination with envelope-containing, formaldehyde-treated, thermally inactivated human immunodeficiency virus type 1. J. Virol. 79:4927-4935.
62. Provine, N. M., W. B. Puryear, X. Wu, J. Overbaugh, and N. L. Haigwood. 2009. The infectious molecular clone and pseudotyped virus models of human immunodeficiency virus type 1 exhibit significant differences in virion composition with only moderate differences in infectivity and inhibition sensitivity. J. Virol. 83:9002-9007.
63. Rerks-Ngarm, S., et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
64. Sanders, R. W., et al. 2002. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76:7293-7305.
65. Sanders, R. W., 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.
66. Scanlan, C. N., et al. 2002. The broadly neutralizing anti-human immuno-deficiency virus type 1 antibody 2G12 recognizes a cluster of α1→2 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321.
67. Scanlan, C. N., et al. 2007. Inhibition of mammalian glycan biosynthesis produces non-self antigens for a broadly neutralising, HIV-1 specific antibody. J. Mol. Biol. 372:16-22.
68. Schief, W. R., Y. E. Ban, and L. Stamatatos. 2009. Challenges for structurebased HIV vaccine design. Curr. Opin. HIV AIDS 4:431-440.
69. Schulke, 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.
70. Skehel, J. J., et al. 1982. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 79:968-972.
71. Stein, B. S., and E. G. Engleman. 1990. Intracellular processing of the gp160 HIV-1 envelope precursor. Endoproteolytic cleavage occurs in a cis or medial compartment of the Golgi complex. J. Biol. Chem. 265:2640-2649.
72. Thomas, G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3:753-766.
73. Tobin, G. J., et al. 2008. Deceptive imprinting and immune refocusing in vaccine design. Vaccine 26:6189-6199.
74. Tomaras, G. D., et al. 2008. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 82:12449-12463.
75. Trkola, A., et al. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
76. Vidor, E. 2007. The nature and consequences of intra- and inter-vaccine interference. J. Comp. Pathol. 137(Suppl. 1):S62-S66.
77. Vzorov, A. N., D. Lea-Fox, and R. W. Compans. 1999. Immunogenicity of full-length and truncated SIV envelope proteins. Viral Immunol. 12:205- 215.
78. Walker, L. M., and D. R. Burton. 2010. Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr. Opin. Immunol. 22:358-366.
79. Wang, X., et al. 2010. The nature and combination of subunits used in epitope-based Schistosoma japonicum vaccine formulations affect their efficacy. Parasit. Vectors 3:109.
80. Willey, R. L., J. S. Bonifacino, B. J. Potts, M. A. Martin, and R. D. Klausner. 1988. Biosynthesis, cleavage, and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. Proc. Natl. Acad. Sci. U. S. A. 85:9580-9584.
81. Willey, R. L., T. Klimkait, D. M. Frucht, J. S. Bonifacino, and M. A. Martin. 1991. Mutations within the human immunodeficiency virus type 1 gp160 envelope glycoprotein alter its intracellular transport and processing. Virology 184:319-329.
82. Wu, X., et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
83. Xiang, S. H., N. Doka, R. K. Choudhary, J. Sodroski, and J. E. Robinson. 2002. Characterization of CD4-induced epitopes on the HIV type 1 gp120 envelope glycoprotein recognized by neutralizing human monoclonal antibodies. AIDS Res. Hum. Retroviruses 18:1207-1217.
84. Zhu, X., C. Borchers, R. J. Bienstock, and K. B. Tomer. 2000. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39:11194-11204.