Proximal glycans outside of the epitopes regulate the presentation of HIV-1 envelope gp120 helper epitopes

Journal of Immunology

Volumn 182, Issue 10, 2009, Pages 6369-6378

  Li, Hualin ^a   Xu, Chong Feng ^a   Blais, Steven ^a   Wan, Qi ^a   Zhang, Hui Tang ^a   Landry, Samuel J ^b   Hioe, Catarina E ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; APC PROTEIN; EPITOPE; GLYCAN DERIVATIVE; GLYCOPROTEIN GP 120; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MUTANT PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; ELECTRIC POTENTIAL; ELECTRICITY; ENZYME REGULATION; HELPER VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOMODULATION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; SURFACE PROPERTY; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HIV ENVELOPE PROTEIN GP120; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; POLYSACCHARIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 70449534963     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804287     Document Type: Article

References (46)

1. Zhang, M., B. Gaschen, W. Blay, B. Foley, N. Haigwood, C. Kuiken, and B. Korber. 2004. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14: 1229-1246. (Pubitemid 39585357)
2. Fischer, P. B., G. B. Karlsson, T. D. Butters, R. A. Dwek, and F. M. Platt. 1996. N-butyldeoxynojirimycin-mediated inhibition of human immunodeficiency virus entry correlates with changes in antibody recognition of the V1/V2 region of gp120. J. Virol. 70: 7143-7152. (Pubitemid 26307431)
3. Fischer, P. B., G. B. Karlsson, R. A. Dwek, and F. M. Platt. 1996. N-butyldeoxynojirimycin- mediated inhibition of human immunodeficiency virus entry correlates with impaired gp120 shedding and gp41 exposure. J. Virol. 70: 7153-7160. (Pubitemid 26307432)
4. 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. (Pubitemid 23003026)
5. Morikawa, Y., J. P. Moore, and I. M. Jones. 1990. HIV-1 envelope protein gp120 expression by secretion in E. coli: assessment of CD4 binding and use in epitope mapping. J. Virol. Methods 29: 105-113. (Pubitemid 20234660)
6. 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.
7. Granados-Gonzalez, V., J. Claret, W. Berlier, N. Vincent, S. Urcuqui-Inchima, F. Lucht, C. Defontaine, A. Pinter, C. Genin, and S. Riffard. 2008. Opposite immune reactivity of serum IgG and secretory IgA to conformational recombinant proteins mimicking V1/V2 domains of three different HIV type 1 subtypes depending on glycosylation. AIDS Res. Hum. Retroviruses 24: 289-299. (Pubitemid 351282107)
8. Ho, Y. S., A. B. Abecasis, K. Theys, K. Deforche, D. E. Dwyer, M. Charleston, A. M. Vandamme, and N. K. Saksena. 2008. HIV-1 gp120 N-linked glycosylation differs between plasma and leukocyte compartments. Virol. J. 5: 14.
9. Mori, K., C. Sugimoto, S. Ohgimoto, E. E. Nakayama, T. Shioda, S. Kusagawa, Y. Takebe, M. Kano, T. Matano, T. Yuasa, et al. 2005. Influence of glycosylation on the efficacy of an Env-based vaccine against simian immunodeficiency virus SIVmac239 in a macaque AIDS model. J. Virol. 79: 10386-10396. (Pubitemid 41098579)
10. Mori, K., Y. Yasutomi, S. Ohgimoto, T. Nakasone, S. Takamura, T. Shioda, and Y. Nagai. 2001. Quintuple deglycosylation mutant of simian immunodeficiency virus SIVmac239 in rhesus macaques: robust primary replication, tightly contained chronic infection, and elicitation of potent immunity against the parental wild-type strain. J. Virol. 75: 4023-4028. (Pubitemid 32410114)
11. Li, H., P. C. Chien, Jr., M. Tuen, M. L. Visciano, S. Cohen, S. Blais, C. F. Xu, H. T. Zhang, and C. E. Hioe. 2008. Identification of an N-linked glycosylation in the C4 region of HIV-1 envelope gp120 that is critical for recognition of neighboring CD4 T cell epitopes. J. Immunol. 180: 4011-4021.
12. Doe, B., K. S. Steimer, and C. M. Walker. 1994. Induction of HIV-1 envelope (gp120)-specific cytotoxic T lymphocyte responses in mice by recombinant CHO cell-derived gp120 is enhanced by enzymatic removal of N-linked glycans. Eur. J. Immunol. 24: 2369-2376. (Pubitemid 24303080)
13. 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.
14. McCaffrey, R. A., C. Saunders, M. Hensel, and L. Stamatatos. 2004. N-linked glycosylation of the V3 loop and the immunologically silent face of gp120 protects human immunodeficiency virus type 1 SF162 from neutralization by antigp120 and anti-gp41 antibodies. J. Virol. 78: 3279-3295.
15. 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)
16. 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. (Pubitemid 44421177)
17. Perdomo, M. F., M. Levi, M. Sallberg, and A. Vahlne. 2008. Neutralization of HIV-1 by redirection of natural antibodies. Proc. Natl. Acad. Sci. USA 105: 12515-12520.
18. Sirois, S., M. Touaibia, K. C. Chou, and R. Roy. 2007. Glycosylation of HIV-1 gp120 V3 loop: towards the rational design of a synthetic carbohydrate vaccine. Curr. Med. Chem. 14: 3232-3242.
19. Wang, L. X. 2006. Toward oligosaccharide- and glycopeptide-based HIV vaccines. Curr. Opin. Drug Discov. Dev. 9: 194-206.
20. Calarese, D. A., C. N. Scanlan, M. B. Zwick, S. Deechongkit, Y. Mimura, R. Kunert, P. Zhu, M. R. Wormald, R. L. Stanfield, K. H. Roux, et al. 2003. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300: 2065-2071.
21. Sanders, R. W., M. Venturi, L. Schiffner, R. Kalyanaraman, H. Katinger, K. O. Lloyd, P. D. Kwong, and J. P. Moore. 2002. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76: 7293-7305.
22. + T cell epitope hotspots to exposed strands of HIV envelope glycoprotein suggests structural influences on antigen processing. Proc. Natl. Acad. Sci. USA 98: 4587-4592.
23. Mirano-Bascos, D., M. Tary-Lehmann, and S. J. Landry. 2008. Antigen structure influences helper T-cell epitope dominance in the human immune response to HIV envelope glycoprotein gp120. Eur. J. Immunol. 38: 1231-1237.
24. + Th responses to envelope and Gag proteins of simian immunodeficiency virus reveals an exclusion of broadly reactive Th epitopes from the glycosylated regions of envelope. J. Immunol. 168: 4001-4011.
25. + T cells specific for HIV type 1 envelope gp120 from chronically HIV type 1-infected subjects. AIDS Res. Hum. Retroviruses 19: 793-806.
26. Jones, G. J., P. von Hoegen, J. Weber, and A. D. Rees. 1999. Immunization with human immunodeficiency virus type 1 rgp120W61D in QS21/MPL adjuvant primes T cell proliferation and C-C chemokine production to multiple epitopes within variable and conserved domains of gp120W61D. J. Infect. Dis. 179: 558-566.
27. + T cell-proliferative responses to glycoprotein 120. AIDS Res. Hum. Retroviruses 16: 893-905.
28. Tuen, M., M. L. Visciano, P. C. Chien, Jr., S. Cohen, P. D. Chen, J. Robinson, Y. He, A. Pinter, M. K. Gorny, and C. E. Hioe. 2005. Characterization of antibodies that inhibit HIV gp120 antigen processing and presentation. Eur. J. Immunol. 35: 2541-2551. (Pubitemid 41404037)
29. 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, et al. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732-737. (Pubitemid 46279718)
30. 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.
31. Zolla-Pazner, S. 2004. Identifying epitopes of HIV-1 that induce protective antibodies. Nat. Rev. Immunol 4: 199-210. (Pubitemid 38339086)
32. Brown, B. K., L. Wieczorek, E. Sanders-Buell, A. Rosa Borges, M. L. Robb, D. L. Birx, N. L. Michael, F. E. McCutchan, and V. R. Polonis. 2008. Cross-clade neutralization patterns among HIV-1 strains from the six major clades of the pandemic evaluated and compared in two different models. Virology 375: 529-538.
33. Yuste, E., H. B. Sanford, J. Carmody, J. Bixby, S. Little, M. B. Zwick, T. Greenough, D. R. Burton, D. D. Richman, R. C. Desrosiers, and W. E. Johnson. 2006. Simian immunodeficiency virus engrafted with human immunodeficiency virus type 1 (HIV-1)-specific epitopes: replication, neutralization, and survey of HIV-1-positive plasma. J. Virol. 80: 3030-3041.
34. Mascola, J. R., S. W. Snyder, O. S. Weislow, S. M. Belay, R. B. Belshe, D. H. Schwartz, M. L. Clements, R. Dolin, B. S. Graham, G. J. Gorse, et al. 1996. Immunization with envelope subunit vaccine products elicits neutralizing antibodies against laboratory-adapted but not primary isolates of human immunodeficiency virus type 1: The National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. J. Infect. Dis. 173: 340-348.
35. Moore, J. P., Y. Cao, L. Qing, Q. J. Sattentau, J. Pyati, R. Koduri, J. Robinson, C. F. Barbas III, D. R. Burton, and D. D. Ho. 1995. Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120. J. Virol. 69: 101-109.
36. Pinter, A. 2007. Roles of HIV-1 Env variable regions in viral neutralization and vaccine development. Curr. HIV Res. 5: 542-553. (Pubitemid 351210988)
37. Hu, S. L., and L. Stamatatos. 2007. Prospects of HIV Env modification as an approach to HIV vaccine design. Curr. HIV Res. 5: 507-513.
38. Pantophlet, R., and D. R. Burton. 2006. GP120: target for neutralizing HIV-1 antibodies. Annu. Rev. Immunol. 24: 739-769.
39. Sjolander, S., A. Bolmstedt, L. Akerblom, P. Horal, S. Olofsson, B. Morein, and A. Sjolander. 1996. N-linked glycans in the CD4-binding domain of human immunodeficiency virus type 1 envelope glycoprotein gp160 are essential for the in vivo priming of T cells recognizing an epitope located in their vicinity. Virology 215: 124-133. (Pubitemid 126335599)
40. Watts, C. 2004. The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat. Immunol 5: 685-692. (Pubitemid 39023297)
41. Li, P., J. L. Gregg, N. Wang, D. Zhou, P. O'Donnell, J. S. Blum, and V. L. Crotzer. 2005. Compartmentalization of class II antigen presentation: contribution of cytoplasmic and endosomal processing. Immunol. Rev. 207: 206-217. (Pubitemid 41415019)
42. Bryant, P. W., A. M. Lennon-Dumenil, E. Fiebiger, C. Lagaudriere-Gesbert, and H. L. Ploegh. 2002. Proteolysis and antigen presentation by MHC class II molecules. Adv. Immunol. 80: 71-114. (Pubitemid 34625621)
43. Chen, B., E. M. Vogan, H. Gong, J. J. Skehel, D. C. Wiley, and S. C. Harrison. 2005. Determining the structure of an unliganded and fully glycosylated SIV gp120 envelope glycoprotein. Structure 13: 197-211. (Pubitemid 40247697)
44. Wyss, D. F., and G. Wagner. 1996. The structural role of sugars in glycoproteins. Curr. Opin. Biotechnol. 7: 409-416.
45. Wyss, D. F., J. S. Choi, J. Li, M. H. Knoppers, K. J. Willis, A. R. Arulanandam, A. Smolyar, E. L. Reinherz, and G. Wagner. 1995. Conformation and function of the N-linked glycan in the adhesion domain of human CD2. Science 269: 1273-1278.
46. Leonard, C. K., M. W. Spellman, L. Riddle, R. J. Harris, J. N. Thomas, and T. J. Gregory. 1990. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265: 10373-10382. (Pubitemid 20212763)