Table of Contents
ISRN AIDS
Volume 2012, Article ID 823605, 9 pages
http://dx.doi.org/10.5402/2012/823605
Research Article

Conservation, Compensation, and Evolution of N-Linked Glycans in the HIV-1 Group M Subtypes and Circulating Recombinant Forms

Medical Research Council Unit for Bioinformatics Capacity Development, South African National Bioinformatics Institute, University of the Western Cape, Private Bag X17, Belville 7535, South Africa

Received 18 October 2012; Accepted 25 November 2012

Academic Editors: Z. Banki and M. Gherardi

Copyright © 2012 Simon A. Travers. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Land and I. Braakman, “Folding of the human immunodeficiency virus type 1 envelope glycoprotein in the endoplasmic reticulum,” Biochimie, vol. 83, no. 8, pp. 783–790, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. Li, L. Luo, N. Rasool, and C. Y. Kang, “Glycosylation is necessary for the correct folding of human immunodeficiency virus gp120 in CD4 binding,” Journal of Virology, vol. 67, no. 1, pp. 584–588, 1993. View at Google Scholar · View at Scopus
  3. C. K. Leonard, M. W. Spellman, L. Riddle, R. J. Harris, J. N. Thomas, and T. J. Gregory, “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,” Journal of Biological Chemistry, vol. 265, no. 18, pp. 10373–10382, 1990. View at Google Scholar · View at Scopus
  4. T. Mizuochi, M. W. Spellman, M. Larkin, J. Solomon, L. J. Basa, and T. Feizi, “Carbohydrate structures of the human-immunodeficiency-virus (HIV) recombinant envelope glycoprotein gp120 produced in Chinese-hamster ovary cells,” Biochemical Journal, vol. 254, no. 2, pp. 599–603, 1988. View at Google Scholar · View at Scopus
  5. G. Myers, K. MacInnes, and B. Korber, “The emergence of simian/human immunodeficiency viruses,” AIDS Research and Human Retroviruses, vol. 8, no. 3, pp. 373–386, 1992. View at Google Scholar · View at Scopus
  6. X. Wei, J. M. Decker, S. Wang et al., “Antibody neutralization and escape by HIV-1,” Nature, vol. 422, no. 6929, pp. 307–312, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Ohgimoto, T. Shioda, K. Mori, E. E. Nakayama, H. Hu, and Y. Nagai, “Location-specific, unequal contribution of the N glycans in simian immunodeficiency virus gp120 to viral infectivity and removal of multiple glycans without disturbing infectivity,” Journal of Virology, vol. 72, no. 10, pp. 8365–8370, 1998. View at Google Scholar · View at Scopus
  8. K. Schønning, B. Jansson, S. Olofsson, and J. E. S. Hansen, “Rapid selection for an N-linked oligosaccharide by monoclonal antibodies directed against the V3 loop of human immunodeficiency virus type 1,” Journal of General Virology, vol. 77, no. 4, pp. 753–758, 1996. View at Google Scholar · View at Scopus
  9. A. Bolmstedt, J. Hinkula, E. Rowcliffe, M. Biller, B. Wahren, and S. Olofsson, “Enhanced immunogenicity of a human immunodeficiency virus type 1 env DNA vaccine by manipulating N-glycosylation signals: effects of elimination of the V3 N306 glycan,” Vaccine, vol. 20, no. 3-4, pp. 397–405, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Chackerian, L. M. Rudensey, and J. Overbaugh, “Specific N-linked and O-linked glycosylation modifications in the envelope V1 domain of simian immunodeficiency virus variants that evolve in the host alter recognition by neutralizing antibodies,” Journal of Virology, vol. 71, no. 10, pp. 7719–7727, 1997. View at Google Scholar · View at Scopus
  11. C. Cheng-Mayer, A. Brown, J. Harouse, P. A. Luciw, and A. J. Mayer, “Selection for neutralization resistance of the simian/human immunodeficiency virus SHIV(SF33A) variant in vivo by virtue of sequence changes in the extracellular envelope glycoprotein that modify N-linked glycosylation,” Journal of Virology, vol. 73, no. 7, pp. 5294–5300, 1999. View at Google Scholar · View at Scopus
  12. S. M. Kang, F. Shi Quan, C. Huang et al., “Modified HIV envelope proteins with enhanced binding to neutralizing monoclonal antibodies,” Virology, vol. 331, no. 1, pp. 20–32, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. R. A. McCaffrey, C. Saunders, M. Hensel, and L. Stamatatos, “N-linked glycosylation of the V3 loop and the immunologically silent face of gp120 protects human immunodeficiency virus type 1 SF162 from neutralization by anti-gp120 and anti-gp41 antibodies,” Journal of Virology, vol. 78, no. 7, pp. 3279–3295, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Sagar, X. Wu, S. Lee, and J. Overbaugh, “Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity,” Journal of Virology, vol. 80, no. 19, pp. 9586–9598, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. S. D. W. Frost, T. Wrin, D. M. Smith et al., “Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 51, pp. 18514–18519, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. C. A. Derdeyn, J. M. Decker, F. Bibollet-Ruche et al., “Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission,” Science, vol. 303, no. 5666, pp. 2019–2022, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Li, J. F. Salazar-Gonzalez, C. A. Derdeyn et al., “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,” Journal of Virology, vol. 80, no. 23, pp. 11776–11790, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. C. N. Scanlan, J. Offer, N. Zitzmann, and R. A. Dwek, “Exploiting the defensive sugars of HIV-1 for drug and vaccine design,” Nature, vol. 446, no. 7139, pp. 1038–1045, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Zhang, F. Hoffman, J. He et al., “Characterization of HIV-1 subtype C envelope glycoproteins from perinatally infected children with different courses of disease,” Retrovirology, vol. 3, article 73, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. P. D. Kwong, R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson, “Structure of an HIV gp 120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody,” Nature, vol. 393, no. 6686, pp. 648–659, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Wyatt, P. D. Kwong, E. Desjardins et al., “The antigenic structure of the HIV gp120 envelope glycoprotein,” Nature, vol. 393, no. 6686, pp. 705–711, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Pantophlet, E. Ollmann Saphire, P. Poignard, P. W. H. I. Parren, I. A. Wilson, and D. R. Burton, “Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120,” Journal of Virology, vol. 77, no. 1, pp. 642–658, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Balzarini, “Targeting the glycans of gp120: a novel approach aimed at the Achilles heel of HIV,” Lancet Infectious Diseases, vol. 5, no. 11, pp. 726–731, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Trkola, M. Purtscher, T. Muster et al., “Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1,” Journal of Virology, vol. 70, no. 2, pp. 1100–1108, 1996. View at Google Scholar · View at Scopus
  25. C. N. Scanlan, R. Pantophlet, M. R. Wormald et al., “The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1—>2 mannose residues on the outer face of gp120,” Journal of Virology, vol. 76, no. 14, pp. 7306–7321, 2002. View at Google Scholar · View at Scopus
  26. R. W. Sanders, M. Venturi, L. Schiffner et al., “The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120,” Journal of Virology, vol. 76, no. 14, pp. 7293–7305, 2002. View at Google Scholar · View at Scopus
  27. J. M. Binley, T. Wrin, B. Korber et al., “Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies,” Journal of Virology, vol. 78, no. 23, pp. 13232–13252, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. E. S. Gray, P. L. Moore, R. A. Pantophlet, and L. Morris, “N-linked glycan modifications in gp120 of human immunodeficiency virus type 1 subtype C render partial sensitivity to 2G12 antibody neutralization,” Journal of Virology, vol. 81, no. 19, pp. 10769–10776, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Bures, L. Morris, C. Williamson et al., “Regional clustering of shared neutralization determinants on primary isolates of Clade C human immunodeficiency virus type 1 from South Africa,” Journal of Virology, vol. 76, no. 5, pp. 2233–2244, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. L. M. Walker, M. Huber, K. J. Doores et al., “Broad neutralization coverage of HIV by multiple highly potent antibodies,” Nature, vol. 477, no. 7365, pp. 466–470, 2011. View at Publisher · View at Google Scholar
  31. R. Pejchal, K. J. Doores, L. M. Walker et al., “A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield,” Science, vol. 334, no. 6059, pp. 1097–1103, 2011. View at Publisher · View at Google Scholar
  32. A. Nandi, C. L. Lavine, P. Wang et al., “Epitopes for broad and potent neutralizing antibody responses during chronic infection with human immunodeficiency virus type 1,” Virology, vol. 396, no. 2, pp. 339–348, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. P. L. Moore, E. S. Gray, C. K. Wibmer et al., “Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape,” Nature Medicine, vol. 18, no. 11, pp. 1688–1692, 2012. View at Publisher · View at Google Scholar
  34. J. Balzarini, J. Neyts, D. Schols et al., “The mannose-specific plant lectins from Cymbidium hybrid and Epipactis helleborine and the (N-actylglucosamine)(n)-specific plant lectin from Urtica dioica are potent and selective inhibitors of human immunodeficiency virus and cytomegalovirus replication in vitro,” Antiviral Research, vol. 18, no. 2, pp. 191–207, 1992. View at Publisher · View at Google Scholar · View at Scopus
  35. M. R. Boyd, K. R. Gustafson, J. B. McMahon et al., “Discovery of cyanovirin-N, a novel human immunodeficiency virus- inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development,” Antimicrobial Agents and Chemotherapy, vol. 41, no. 7, pp. 1521–1530, 1997. View at Google Scholar · View at Scopus
  36. A. J. Bolmstedt, B. R. O'Keefe, S. R. Shenoy, J. B. Mcmahon, and M. R. Boyd, “Cyanovirin-N defines a new class of antiviral agent targeting N-linked, high-mannose glycans in an oligosaccharide-specific manner,” Molecular Pharmacology, vol. 59, no. 5, pp. 949–954, 2001. View at Google Scholar · View at Scopus
  37. H. R. Bokesch, B. R. O'Keefe, T. C. McKee et al., “A potent novel anti-HIV protein from the cultured cyanobacterium Scytonema varium,” Biochemistry, vol. 42, no. 9, pp. 2578–2584, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Balzarini, S. Hatse, K. Vermeire et al., “Mannose-specific plant lectins from the Amaryllidaceae family qualify as efficient microbicides for prevention of human immunodeficiency virus infection,” Antimicrobial Agents and Chemotherapy, vol. 48, no. 10, pp. 3858–3870, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. C. C. Tsai, P. Emau, Y. Jiang et al., “Cyanovirin-N gel as a topical microbicide prevents rectal transmission of SHIV89.6P in macaques,” AIDS Research and Human Retroviruses, vol. 19, no. 7, pp. 535–541, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Balzarini, K. Van Laethem, D. Daelemans et al., “Pradimicin A, a carbohydrate-binding nonpeptidic lead compound for treatment of infections with viruses with highly glycosylated envelopes, such as human immunodeficiency virus,” Journal of Virology, vol. 81, no. 1, pp. 362–373, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Witvrouw, V. Fikkert, A. Hantson et al., “Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirin N and concanavalin A,” Journal of Virology, vol. 79, no. 12, pp. 7777–7784, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Balzarini, K. Van Laethem, W. J. Peumans et al., “Mutational pathways, resistance profile, and side effects of cyanovirin relative to human immunodeficiency virus type 1 strains with N-glycan deletions in their gp120 envelopes,” Journal of Virology, vol. 80, no. 17, pp. 8411–8421, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. D. L. Robertson, J. P. Anderson, J. A. Bradac et al., “HIV-1 nomenclature proposal,” Science, vol. 288, no. 5463, pp. 55–57, 2000. View at Google Scholar · View at Scopus
  44. M. Peeters and P. M. Sharp, “Genetic diversity of HIV-1: the moving target,” AIDS, vol. 14, no. 3, pp. S129–S140, 2000. View at Google Scholar · View at Scopus
  45. L. Buonaguro, M. L. Tornesello, and F. M. Buonaguro, “Human immunodeficiency virus type 1 subtype distribution in the worldwide epidemic: pathogenetic and therapeutic implications,” Journal of Virology, vol. 81, no. 19, pp. 10209–10219, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Hemelaar, E. Gouws, P. D. Ghys, and S. Osmanov, “Global and regional distribution of HIV-1 genetic subtypes and recombinants in 2004,” AIDS, vol. 20, no. 16, pp. W13–W23, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Osmanov, C. Pattou, B. Schwardländer et al., “Estimated global distribution and regional spread of HIV-1 genetic subtypes in the year 2000,” Journal of Acquired Immune Deficiency Syndromes, vol. 29, no. 2, pp. 184–190, 2002. View at Google Scholar
  48. E. Menu, T. T. X. Lien, M. E. Lafon et al., “HIV type 1 Thai subtype E is predominant in South Vietnam,” AIDS Research and Human Retroviruses, vol. 12, no. 7, pp. 629–633, 1996. View at Google Scholar · View at Scopus
  49. K. Motomura, S. Kusagawa, K. Kato et al., “Emergence of new forms of human immunodeficiency virus type 1 intersubtype recombinants in central Myanmar,” AIDS Research and Human Retroviruses, vol. 16, no. 17, pp. 1831–1843, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Piyasirisilp, F. E. McCutchan, J. K. Carr et al., “A recent outbreak of human immunodeficiency virus type 1 infection in Southern China was initiated by two highly homogeneous, geographically separated strains, circulating recombinant form AE and a novel BC recombinant,” Journal of Virology, vol. 74, no. 23, pp. 11286–11295, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. F. E. McCutchan, J. K. Carr, M. Bajani et al., “Subtype G and multiple forms of A/G intersubtype recombinant human immunodeficiency virus type 1 in Nigeria,” Virology, vol. 254, no. 2, pp. 226–234, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Montavon, C. Toure-Kane, F. Liegeois et al., “Most env and gag subtype A HIV-1 viruses circulating in west and West Central Africa are similar to the' prototype AG recombinant virus IBNG,” Journal of Acquired Immune Deficiency Syndromes, vol. 23, no. 5, pp. 363–374, 2000. View at Google Scholar · View at Scopus
  53. M. Zhang, B. Gaschen, W. Blay et al., “Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin,” Glycobiology, vol. 14, no. 12, pp. 1229–1246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. A. F. Y. Poon, F. I. Lewis, S. L. Kosakovsky Pond, and S. D. W. Frost, “Evolutionary interactions between N-Linked glycosylation sites in the HIV-1 envelope,” PLoS Computational Biology, vol. 3, no. 1, article e11, pp. 0110–0119, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. W. P. Maddison and D. R. Maddison, MacClade, Sinauer, Sunderland, Mass, USA, 4.5 edition, 1992.
  56. L. Kasturi, H. Chen, and S. H. Shakin-Eshleman, “Regulation of N-linked core glycosylation: use of a site-directed mutagenesis approach to identify Asn-Xaa-Ser/Thr sequons that are poor oligosaccharide acceptors,” Biochemical Journal, vol. 323, no. 2, pp. 415–419, 1997. View at Google Scholar · View at Scopus
  57. C. C. Huang, M. Tang, M. Y. Zhang et al., “Structural biology: structure of a V3-containing HIV-1 gp120 core,” Science, vol. 310, no. 5750, pp. 1025–1028, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Bohne-Lang and C. W. Von der Lieth, “GlyProt: in silico glycosylation of proteins,” Nucleic Acids Research, vol. 33, no. 2, pp. W214–W219, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. X. Zhu, C. Borchers, R. J. Bienstock, and K. B. Tomer, “Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells,” Biochemistry, vol. 39, no. 37, pp. 11194–11204, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Trkola, A. B. Pomales, H. Yuan et al., “Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG,” Journal of Virology, vol. 69, no. 11, pp. 6609–6617, 1995. View at Google Scholar · View at Scopus
  61. A. Manrique, P. Rusert, B. Joos et al., “In vivo and in vitro escape from neutralizing antibodies 2G12, 2F5, and 4E10,” Journal of Virology, vol. 81, no. 16, pp. 8793–8808, 2007. View at Publisher · View at Google Scholar · View at Scopus