Two N-linked glycosylation sites in the V2 and C2 regions of human immunodeficiency virus type 1 CRF01-AE envelope glycoprotein gp120 regulate viral neutralization susceptibility to the human monoclonal antibody specific for the CD4 binding domain

Journal of Virology

Volumn 84, Issue 9, 2010, Pages 4311-4320

  Utachee, Piraporn ^a   Nakamura, Shota ^a,b   Isarangkura na ayuthaya, Panasda ^a   Tokunaga, Kenzo ^c   Sawanpanyalert, Pathom ^a   Ikuta, Kazuyoshi ^a,b   Auwanit, Wattana ^a   Kameoka, Masanori ^a,b  

^a MINISTRY OF PUBLIC HEALTH   (Thailand)

^b OSAKA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G1 B12 ANTIBODY; UNCLASSIFIED DRUG; VIRUS VACCINE;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CLONE; CONTROLLED STUDY; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMORAL IMMUNITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; VIRUS ENVELOPE; VIRUS NEUTRALIZATION; VIRUS RECOMBINANT; VIRUS RESISTANCE; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; BINDING SITES; EPITOPES; GLYCOSYLATION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNOGLOBULIN G; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NEUTRALIZATION TESTS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

AVIAN ENCEPHALOMYELITIS VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77950816445     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02619-09     Document Type: Article

References (53)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291. (Pubitemid 16013975)
2. Barbas, C. F., III, T. A. Collet, W. Amberg, P. Roben, J. M. Binley, D. Hoekstra, D. Cababa, T. M. Jones, R. A. Williamson, G. R. Pilkington, N. L. Haigwood, E. Cabezas, A. C. Satterthwait, I. Sanz, and D. R. Burton. 1993. Molecular profile of an antibody response to HIV-1 as probed by combinatorial libraries. J. Mol. Biol. 230:812-823.
3. Binley, J. M., 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. 2004. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78:13232-13252. (Pubitemid 39507829)
4. Burton, D. R., C. F. Barbas III, M. A. Persson, S. Koenig, R. M. Chanock, and R. A. Lerner. 1991. A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc. Natl. Acad. Sci. U. S. A. 88:10134-10137.
5. Burton, D. R., J. Pyati, R. Koduri, S. J. Sharp, G. B. Thornton, P. W. Parren, L. S. Sawyer, R. M. Hendry, N. Dunlop, P. L. Nara, M. Lamacchia, E. Garratty, E. R. Stiehm, Y. J. Bryson, Y. Cao, J. P. Moore, D. D. Ho, and C. F. Barbas III. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027.
6. Chen, B., E. M. Vogan, H. Gong, J. J. Skehel, D. C. Wiley, and S. C. Harrison. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-841. (Pubitemid 40314887)
7. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
8. Duenas-Decamp, M. J., P. Peters, D. Burton, and P. R. Clapham. 2008. Natural resistance of human immunodeficiency virus type 1 to the CD4bs antibody b12 conferred by a glycan and an arginine residue close to the CD4 binding loop. J. Virol. 82:5807-5814.
9. Gaschen, B., J. Taylor, K. Yusim, B. Foley, F. Gao, D. Lang, V. Novitsky, B. Haynes, B. H. Hahn, T. Bhattacharya, and B. Korber. 2002. Diversity considerations in HIV-1 vaccine selection. Science 296:2354-2360. (Pubitemid 34734202)
10. 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.
11. Gnanakaran, S., D. Lang, M. Daniels, T. Bhattacharya, C. A. Derdeyn, and B. Korber. 2007. Clade-specific differences between human immunodefi- ciency virus type 1 clades B and C: diversity and correlations in C3-V4 regions of gp120. J. Virol. 81:4886-4891. (Pubitemid 46668687)
12. 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. (Pubitemid 44167156)
13. Hemelaar, J., E. Gouws, P. D. Ghys, and S. Osmanov. 2006. Global and regional distribution of HIV-1 genetic subtypes and recombinants in 2004. AIDS 20:W13-W23. (Pubitemid 44611051)
14. Kinomoto, M., M. Yokoyama, H. Sato, A. Kojima, T. Kurata, K. Ikuta, T. Sata, and K. Tokunaga. 2005. Amino acid 36 in the human immunodeficiency virus type 1 gp41 ectodomain controls fusogenic activity: implications for the molecular mechanism of viral escape from a fusion inhibitor. J. Virol. 79:5996-6004. (Pubitemid 40617206)
15. Koch, M., M. Pancera, P. D. Kwong, P. Kolchinsky, C. Grundner, L. Wang, W. A. Hendrickson, J. Sodroski, and R. Wyatt. 2003. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313:387-400. (Pubitemid 37045357)
16. Krissinel, E., and K. Henrick. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60:2256-2268.
17. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
18. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, M. Bilska, D. L. Kothe, J. F. Salazar-Gonzalez, X. Wei, J. M. Decker, B. H. Hahn, and D. C. Montefiori. 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)
19. Li, M., J. F. Salazar-Gonzalez, C. A. Derdeyn, L. Morris, C. Williamson, J. E. Robinson, J. M. Decker, Y. Li, M. G. Salazar, V. R. Polonis, K. Mlisana, S. A. Karim, K. Hong, K. M. Greene, M. Bilska, J. Zhou, S. Allen, E. Chomba, J. Mulenga, C. Vwalika, F. Gao, M. Zhang, B. T. Korber, E. Hunter, B. H. Hahn, and D. C. Montefiori. 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.
20. Li, Y., B. Cleveland, I. Klots, B. Travis, B. A. Richardson, D. Anderson, D. Montefiori, P. Polacino, and S. L. Hu. 2008. Removal of a single N-linked glycan in human immunodeficiency virus type 1 gp120 results in an enhanced ability to induce neutralizing antibody responses. J. Virol. 82:638-651.
21. Li, Y., S. A. Migueles, B. Welcher, K. Svehla, A. Phogat, M. K. Louder, X. Wu, G. M. Shaw, M. Connors, R. T. Wyatt, and J. R. Mascola. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13:1032-1034.
22. 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.
23. 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)
24. Malenbaum, S. E., D. Yang, L. Cavacini, M. Posner, J. Robinson, and C. Cheng-Mayer. 2000. The N-terminal V3 loop glycan modulates the interaction of clade A and B human immunodeficiency virus type 1 envelopes with CD4 and chemokine receptors. J. Virol. 74:11008-11016.
25. Mascola, J. R., and D. C. Montefiori. 2003. HIV-1: nature's master of disguise. Nat. Med. 9:393-394.
26. McCutchan, F. E. 2006. Global epidemiology of HIV. J. Med. Virol. 78(Suppl. 1):S7-S12.
27. Mizuochi, T., T. J. Matthews, M. Kato, J. Hamako, K. Titani, J. Solomon, and T. Feizi. 1990. Diversity of oligosaccharide structures on the envelope glycoprotein gp 120 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.
28. Mo, H., L. Stamatatos, J. E. Ip, C. F. Barbas, P. W. Parren, D. R. Burton, J. P. Moore, and D. D. Ho. 1997. Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12. J. Virol. 71:6869-6874.
29. Nabatov, A. A., G. Pollakis, T. Linnemann, A. Kliphius, M. I. Chalaby, and W. A. Paxton. 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.
30. Pantophlet, R., E. Ollmann Saphire, P. Poignard, P. W. Parren, I. A. Wilson, and D. R. Burton. 2003. 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. 77:642-658. (Pubitemid 36005001)
31. Parren, P. W., H. J. Ditzel, R. J. Gulizia, J. M. Binley, C. F. Barbas III, D. R. Burton, and D. E. Mosier. 1995. Protection against HIV-1 infection in hu-PBL-SCID mice by passive immunization with a neutralizing human monoclonal antibody against the gp120 CD4-binding site. AIDS 9:F1-F6.
32. Parren, P. W., P. A. Marx, A. J. Hessell, A. Luckay, J. Harouse, C. Cheng-Mayer, J. P. Moore, and D. R. Burton. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340-8347.
33. Patel, M. B., N. G. Hoffman, and R. Swanstrom. 2008. Subtype-specific conformational differences within the V3 region of subtype B and subtype C human immunodeficiency virus type 1 Env proteins. J. Virol. 82:903-916.
34. Pinter, A., W. J. Honnen, Y. He, M. K. Gorny, S. Zolla-Pazner, and S. C. Kayman. 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)
35. Poignard, P., R. Sabbe, G. R. Picchio, M. Wang, R. J. Gulizia, H. Katinger, P. W. Parren, D. E. Mosier, and D. R. Burton. 1999. Neutralizing antibodies have limited effects on the control of established HIV-1 infection in vivo. Immunity 10:431-438. (Pubitemid 29205479)
36. Posner, M. R., L. A. Cavacini, C. L. Emes, J. Power, and R. Byrn. 1993. Neutralization of HIV-1 by F105, a human monoclonal antibody to the CD4 binding site of gp120. J. Acquir. Immune Defic. Syndr. 6:7-14.
37. Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, M. Benenson, S. Gurunathan, J. Tartaglia, J. G. McNeil, D. P. Francis, D. Stablein, D. L. Birx, S. Chunsuttiwat, C. Khamboonruang, P. Thongcharoen, M. L. Robb, N. L. Michael, P. Kunasol, and J. H. Kim. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
38. Roben, P., J. P. Moore, M. Thali, J. Sodroski, C. F. Barbas III, and D. R. Burton. 1994. 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. 68:4821-4828. (Pubitemid 24226546)
39. Rong, R., F. Bibollet-Ruche, J. Mulenga, S. Allen, J. L. Blackwell, and C. A. Derdeyn. 2007. Role of V1V2 and other human immunodeficiency virus type 1 envelope domains in resistance to autologous neutralization during clade C infection. J. Virol. 81:1350-1359. (Pubitemid 46167856)
40. Samleerat, T., S. Thenin, G. Jourdain, N. Ngo-Giang-Huong, A. Moreau, P. Leechanachai, J. Ithisuknanth, K. Pagdi, P. Wannarit, S. Sangsawang, M. Lallemant, F. Barin, and M. Braibant. 2009. Maternal neutralizing antibodies against a CRF01-AE primary isolate are associated with a low rate of intrapartum HIV-1 transmission. Virology 387:388-394.
41. Saunders, C. J., R. A. McCaffrey, I. Zharkikh, Z. Kraft, S. E. Malenbaum, B. Burke, C. Cheng-Mayer, and L. Stamatatos. 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.
42. Teeraputon, S., S. Louisirirojchanakul, and P. Auewarakul. 2005. N-linked glycosylation in C2 region of HIV-1 envelope reduces sensitivity to neutralizing antibodies. Viral Immunol. 18:343-353. (Pubitemid 41106013)
43. Thali, M., U. Olshevsky, C. Furman, D. Gabuzda, M. Posner, and J. Sodroski. 1991. Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody. J. Virol. 65:6188-6193.
44. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
45. Trkola, A., A. B. Pomales, H. Yuan, B. Korber, P. J. Maddon, G. P. Allaway, H. Katinger, C. F. Barbas III, D. R. Burton, D. D. Ho, and J. P. Moore. 1995. Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG. J. Virol. 69:6609-6617.
46. Utachee, P., P. Jinnopat, P. Isarangkura-Na-Ayuthaya, U. C. de Silva, S. Nakamura, U. Siripanyaphinyo, N. Wichukchinda, K. Tokunaga, T. Yasunaga, P. Sawanpanyalert, K. Ikuta, W. Auwanit, and M. Kameoka. 2009. Genotypic characterization of CRF01-AE env genes derived from human immunodeficiency virus type 1-infected patients residing in central Thailand. AIDS Res. Hum. Retroviruses 25:229-236.
47. Utachee, P., P. Jinnopat, P. Isarangkura-Na-Ayuthaya, U. C. de Silva, S. Nakamura, U. Siripanyaphinyo, N. Wichukchinda, K. Tokunaga, T. Yasunaga, P. Sawanpanyalert, K. Ikuta, W. Auwanit, and M. Kameoka. 2009. Phenotypic studies on recombinant human immunodeficiency virus type 1 (HIV-1) containing CRF01-AE env gene derived from HIV-1-infected patient, residing in central Thailand. Microbes Infect. 11:334-343.
48. Veazey, R. S., 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. 2003. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9:343-346.
49. Walker, L. M., S. K. Phogat, P. Y. Chan-Hui, D. Wagner, P. Phung, J. L. Goss, T. Wrin, M. D. Simek, S. Fling, J. L. Mitcham, J. K. Lehrman, F. H. Priddy, O. A. Olsen, S. M. Frey, P. W. Hammond, S. Kaminsky, T. Zamb, M. Moyle, W. C. Koff, P. Poignard, and D. R. Burton. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
50. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar- Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
51. Wu, X., T. Zhou, S. O'Dell, R. T. Wyatt, P. D. Kwong, and J. R. Mascola. 2009. Mechanism of human immunodeficiency virus type 1 resistance to monoclonal antibody B12 that effectively targets the site of CD4 attachment. J. Virol. 83:10892-10907.
52. Zhou, T., L. Xu, B. Dey, A. J. Hessell, D. Van Ryk, S. H. Xiang, X. Yang, M. Y. Zhang, M. B. Zwick, J. Arthos, D. R. Burton, D. S. Dimitrov, J. Sodroski, R. Wyatt, G. J. Nabel, and P. D. Kwong. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445:732-737. (Pubitemid 46279718)
53. 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.