Defining Criteria for Oligomannose Immunogens for HIV Using Icosahedral Virus Capsid Scaffolds

Chemistry and Biology

Volumn 17, Issue 4, 2010, Pages 357-370

  Astronomo, Rena D ^a   Kaltgrad, Eiton ^a   Udit, Andrew K ^a   Wang, Sheng Kai ^a   Doores, Katie J ^a,b   Huang, Cheng Yuan ^a   Pantophlet, Ralph ^a   Paulson, James C ^a   Wong, Chi Huey ^a   Finn, M G ^a   Burton, Dennis R ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

CHEMBIO; MICROBIO

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MANNOSE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2G12; OLIGOSACCHARIDE;

ANIMAL; ARTICLE; CARBOHYDRATE ANALYSIS; CHEMISTRY; COLIPHAGE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; MOLECULAR GENETICS; MOSAIC VIRUS; RABBIT; VIRUS CAPSID;

AIDS VACCINES; ALLOLEVIVIRUS; ANIMALS; ANTIBODIES, MONOCLONAL; CAPSID; CARBOHYDRATE SEQUENCE; COMOVIRUS; HIV; HIV INFECTIONS; MANNOSE; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; RABBITS;

COWPEA MOSAIC VIRUS; ENTEROBACTERIOPHAGE QBETA; HUMAN IMMUNODEFICIENCY VIRUS; MIRIDAE; ORYCTOLAGUS CUNICULUS;

EID: 77951073160     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2010.03.012     Document Type: Article

References (66)

1. Astronomo R.D., Lee H.K., Scanlan C.N., Pantophlet R., Huang C.Y., Wilson I.A., Blixt O., Dwek R.A., Wong C.H., and Burton D.R. A glycoconjugate antigen based on the recognition motif of a broadly neutralizing human immunodeficiency virus antibody, 2G12, is immunogenic but elicits antibodies unable to bind to the self glycans of gp120. J. Virol. 82 (2008) 6359-6368
2. Binley J. Specificities of broadly neutralizing anti-HIV-1 sera. Curr. Opin. HIV AIDS 4 (2009) 364-372
3. Binley J.M., Wrin T., Korber B., Zwick M.B., Wang M., Chappey C., Stiegler G., Kunert R., Zolla-Pazner S., Katinger H., et al. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78 (2004) 13232-13252
4. Binley J.M., Lybarger E.A., Crooks E.T., Seaman M.S., Gray E., Davis K.L., Decker J.M., Wycuff D., Harris L., Hawkins N., et al. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82 (2008) 11651-11668
5. Blixt O., Head S., Mondala T., Scanlan C., Huflejt M.E., Alvarez R., Bryan M.C., Fazio F., Calarese D., Stevens J., et al. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. USA 101 (2004) 17033-17038
6. Burton D.R., Pyati J., Koduri R., Sharp S.J., Thornton G.B., Parren P.W., Sawyer L.S., Hendry R.M., Dunlop N., Nara P.L., et al. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266 (1994) 1024-1027
7. Calarese D.A., Scanlan C.N., Zwick M.B., Deechongkit S., Mimura Y., Kunert R., Zhu P., Wormald M.R., Stanfield R.L., Roux K.H., et al. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300 (2003) 2065-2071
8. Calarese D.A., Lee H.K., Huang C.Y., Best M.D., Astronomo R.D., Stanfield R.L., Katinger H., Burton D.R., Wong C.H., and Wilson I.A. Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12. Proc. Natl. Acad. Sci. USA 102 (2005) 13372-13377
9. Chatterji A., Ochoa W.F., Paine M., Ratna B.R., Johnson J.E., and Lin T. New addresses on an addressable virus nanoblock: uniquely reactive Lys residues on cowpea mosaic virus. Chem. Biol. 11 (2004) 855-863
10. Chen B., Vogan E.M., Gong H., Skehel J.J., Wiley D.C., and Harrison S.C. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433 (2005) 834-841
11. Corti D., Langedijk J.P., Hinz A., Seaman M.S., Vanzetta F., Fernandez-Rodriguez B.M., Silacci C., Pinna D., Jarrossay D., Balla-Jhagjhoorsingh S., et al. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One 5 (2010) e8805
12. Cutalo J.M., Deterding L.J., and Tomer K.B. Characterization of glycopeptides from HIV-I(SF2) gp120 by liquid chromatography mass spectrometry. J. Am. Soc. Mass Spectrom. 15 (2004) 1545-1555
13. Destito G., Yeh R., Rae C.S., Finn M.G., and Manchester M. Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells. Chem. Biol. 14 (2007) 1152-1162
14. Dhillon A.K., Donners H., Pantophlet R., Johnson W.E., Decker J.M., Shaw G.M., Lee F.H., Richman D.D., Doms R.W., Vanham G., et al. Dissecting the neutralizing antibody specificities of broadly neutralizing sera from human immunodeficiency virus type 1-infected donors. J. Virol. 81 (2007) 6548-6562
15. Dudkin V.Y., Orlova M., Geng X., Mandal M., Olson W.C., and Danishefsky S.J. Toward fully synthetic carbohydrate-based HIV antigen design: on the critical role of bivalency. J. Am. Chem. Soc. 126 (2004) 9560-9562
16. Dunlop D.C., Ulrich A., Appelmelk B.J., Burton D.R., Dwek R.A., Zitzmann N., and Scanlan C.N. Antigenic mimicry of the HIV envelope by AIDS-associated pathogens. AIDS 22 (2008) 2214-2217
17. Geng X., Dudkin V.Y., Mandal M., and Danishefsky S.J. In pursuit of carbohydrate-based HIV vaccines, part 2: the total synthesis of high-mannose-type gp120 fragments-evaluation of strategies directed to maximal convergence. Angew. Chem. Int. Ed. Engl. 43 (2004) 2562-2565
18. Gray E.S., Taylor N., Wycuff D., Moore P.L., Tomaras G.D., Wibmer C.K., Puren A., DeCamp A., Gilbert P.B., Wood B., et al. Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J. Virol. 83 (2009) 8925-8937
19. Hessell A.J., Rakasz E.G., Poignard P., Hangartner L., Landucci G., Forthal D.N., Koff W.C., Watkins D.I., and Burton D.R. Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog. 5 (2009) e1000433
20. Hong V., Presolski S.I., Ma C., and Finn M.G. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. Engl. 48 (2009) 9879-9883
21. Iacob R.E., Perdivara I., Przybylski M., and Tomer K.B. Mass spectrometric characterization of glycosylation of hepatitis C virus E2 envelope glycoprotein reveals extended microheterogeneity of N-glycans. J. Am. Soc. Mass Spectrom. 19 (2008) 428-444
22. Joao H.C., and Dwek R.A. Effects of glycosylation on protein structure and dynamics in ribonuclease B and some of its individual glycoforms. Eur. J. Biochem. 218 (1993) 239-244
23. Joyce J.G., Krauss I.J., Song H.C., Opalka D.W., Grimm K.M., Nahas D.D., Esser M.T., Hrin R., Feng M., Dudkin V.Y., et al. An oligosaccharide-based HIV-1 2G12 mimotope vaccine induces carbohydrate-specific antibodies that fail to neutralize HIV-1 virions. Proc. Natl. Acad. Sci. USA 105 (2008) 15684-15689
24. Kaltgrad E., Sen Gupta S., Punna S., Huang C.-Y., Chang A., Wong C.-H., Finn M.G., and Blixt O. Anti-carbohydrate antibodies elicited by polyvalent display on a viral scaffold. ChemBioChem 8 (2007) 1455-1462
25. Kaltgrad E., O'Reilly M.K., Liao L., Han S., Paulson J., and Finn M.G. On-virus construction of polyvalent glycan ligands for cell-surface receptors. J. Am. Chem. Soc. 130 (2008) 4578-4579
26. Kozlovska T.M., Cielens I., Vasiljeva I., Strelnikova A., Kazaks A., Dislers A., Dreilina D., Ose V., Gusars I., and Pumpens P. RNA phase Q β coat protein as a carrier for foreign epitopes. Intervirology 39 (1996) 9-15
27. Krauss I.J., Joyce J.G., Finnefrock A.C., Song H.C., Dudkin V.Y., Geng X., Warren J.D., Chastain M., Shiver J.W., and Danishefsky S.J. Fully synthetic carbohydrate HIV antigens designed on the logic of the 2G12 antibody. J. Am. Chem. Soc. 129 (2007) 11042-11044
28. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., and Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393 (1998) 648-659
29. Lee H.K., Scanlan C.N., Huang C.Y., Chang A.Y., Calarese D.A., Dwek R.A., Rudd P.M., Burton D.R., Wilson I.A., and Wong C.H. Reactivity-based one-pot synthesis of oligomannoses: defining antigens recognized by 2G12, a broadly neutralizing anti-HIV-1 antibody. Angew. Chem. Int. Ed. Engl. 43 (2004) 1000-1003
30. Lewis W.G., Magallon F.G., Fokin V.V., and Finn M.G. Discovery and characterization of catalysts for azide-alkyne cycloaddition by fluorescence quenching. J. Am. Chem. Soc. 126 (2004) 9152-9153
31. Li H., and Wang L.X. Design and synthesis of a template-assembled oligomannose cluster as an epitope mimic for human HIV-neutralizing antibody 2G12. Org. Biomol. Chem. 2 (2004) 483-488
32. Li Y., Svehla K., Louder M.K., Wycuff D., Phogat S., Tang M., Migueles S.A., Wu X., Phogat A., Shaw G.M., et al. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J. Virol. 83 (2009) 1045-1059
33. Liljas L., and Golmohammadi R. The crystal structure of bacteriophage Q β at 3.5 Å resolution. Structure 4 (1996) 543-554
34. Lin T., Porta C., Lomonossoff G., and Johnson J.E. Structure-based design of peptide presentation on a viral surface: the crystal structure of a plant/animal virus chimera at 2.8 Å resolution. Fold. Des. 1 (1996) 179-187
35. Lin T., Chen Z., Usha R., Stauffacher C.V., Dai J.-B., Schmidt T., and Johnson J.E. The refined crystal structure of cowpea mosaic virus at 2.8 Å resolution. Virology 265 (1999) 20-34
36. Lomonossoff G.P., and Hamilton W.D.O. Cowpea mosaic virus-based vaccines. Curr. Top. Microbiol. Immunol. 240 (1999) 177-189
37. Luallen R.J., Lin J., Fu H., Cai K.K., Agrawal C., Mboudjeka I., Lee F.H., Montefiori D., Smith D.F., Doms R.W., et al. An engineered Saccharomyces cerevisiae strain binds the broadly neutralizing human immunodeficiency virus type 1 antibody 2G12 and elicits mannose-specific gp120-binding antibodies. J. Virol. 82 (2008) 6447-6457
38. Mascola J.R., Stiegler G., VanCott T.C., Katinger H., Carpenter C.B., Hanson C.E., Beary H., Hayes D., Frankel S.S., Birx D.L., et al. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6 (2000) 207-210
39. Mehandru S., Vcelar B., Wrin T., Stiegler G., Joos B., Mohri H., Boden D., Galovich J., Tenner-Racz K., Racz P., et al. Adjunctive passive immunotherapy in human immunodeficiency virus type 1-infected individuals treated with antiviral therapy during acute and early infection. J. Virol. 81 (2007) 11016-11031
40. Miermont A., Barnhill H., Strable E., Lu X., Wall K.A., Wang Q., Finn M.G., and Huang X. Cowpea mosaic virus capsid, a promising carrier towards the development of carbohydrate based anti-tumor vaccines. Chem. Eur. J. 14 (2008) 4939-4947
41. Ni J., Song H., Wang Y., Stamatos N.M., and Wang L.X. Toward a carbohydrate-based HIV-1 vaccine: synthesis and immunological studies of oligomannose-containing glycoconjugates. Bioconjug. Chem. 17 (2006) 493-500
42. Prasuhn Jr. D.E., Yeh R.M., Obenaus A., Manchester M., and Finn M.G. Viral MRI contrast agents: coordination of Gd by native virions and attachment of Gd complexes by azide-alkyne cycloaddition. Chem. Commun. (Camb) (2007) 1269-1271
43. Prasuhn Jr. D.E., Singh P., Strable E., Brown S., Manchester M., and Finn M.G. Plasma clearance of bacteriophage Qβ particles as a function of surface charge. J. Am. Chem. Soc. 130 (2008) 1328-1334
44. Rostovtsev V.V., Green L.G., Fokin V.V., and Sharpless K.B. A stepwise Huisgen cycloaddition process: copper(I)-catalyzed regioselective ligation of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 41 (2002) 2596-2599
45. Sanders R.W., Venturi M., Schiffner L., Kalyanaraman R., Katinger H., Lloyd K.O., Kwong P.D., and Moore J.P. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76 (2002) 7293-7305
46. Scanlan C.N., Pantophlet R., Wormald M.R., Ollmann Saphire E., Stanfield R., Wilson I.A., Katinger H., Dwek R.A., Rudd P.M., and Burton D.R. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of α1→2 mannose residues on the outer face of gp120. J. Virol. 76 (2002) 7306-7321
47. Scanlan C.N., Pantophlet R., Wormald M.R., Saphire E.O., Calarese D., Stanfield R., Wilson I.A., Katinger H., Dwek R.A., Burton D.R., et al. The carbohydrate epitope of the neutralizing anti-HIV-1 antibody 2G12. Adv. Exp. Med. Biol. 535 (2003) 205-218
48. Scanlan C.N., Ritchie G.E., Baruah K., Crispin M., Harvey D.J., Singer B.B., Lucka L., Wormald M.R., Wentworth Jr. P., Zitzmann N., et al. Inhibition of mammalian glycan biosynthesis produces non-self antigens for a broadly neutralising, HIV-1 specific antibody. J. Mol. Biol. 372 (2007) 16-22
49. Sen Gupta S., Kuzelka J., Singh P., Lewis W.G., Manchester M., and Finn M.G. Accelerated bioorthogonal conjugation: a practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjug. Chem. 16 (2005) 1572-1579
50. Shenoy S.R., Barrientos L.G., Ratner D.M., O'Keefe B.R., Seeberger P.H., Gronenborn A.M., and Boyd M.R. Multisite and multivalent binding between cyanovirin-N and branched oligomannosides: calorimetric and NMR characterization. Chem. Biol. 9 (2002) 1109-1118
51. Stamatatos L., Morris L., Burton D.R., and Mascola J.R. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine?. Nat. Med. 15 (2009) 866-870
52. Strable E., Prasuhn Jr. D.E., Udit A.K., Brown S., Link A.J., Ngo J.T., Lander G., Quispe J., Potter C.S., Carragher B., et al. Unnatural amino acid incorporation into virus-like particles. Bioconjug. Chem. 19 (2008) 866-875
53. Trkola A., Pomales A.B., Yuan H., Korber B., Maddon P.J., Allaway G.P., Katinger H., Barbas III C.F., Burton D.R., Ho D.D., et al. Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG. J. Virol. 69 (1995) 6609-6617
54. Trkola A., Purtscher M., Muster T., Ballaun C., Buchacher A., Sullivan N., Srinivasan K., Sodroski J., Moore J.P., and Katinger H. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70 (1996) 1100-1108
55. Trkola A., Kuster H., Rusert P., Joos B., Fischer M., Leemann C., Manrique A., Huber M., Rehr M., Oxenius A., et al. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat. Med. 11 (2005) 615-622
56. Virgin H.W., and Walker B.D. Immunology and the elusive AIDS vaccine. Nature 464 (2010) 224-231
57. Walker L.M., Phogat S.K., Chan-Hui P.Y., Wagner D., Phung P., Goss J.L., Wrin T., Simek M.D., Fling S., Mitcham J.L., et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326 (2009) 285-289
58. Wang L.X. Toward oligosaccharide- and glycopeptide-based HIV vaccines. Curr. Opin. Drug Discov. Devel. 9 (2006) 194-206
59. Wang Q., Lin T., Tang L., Johnson J.E., and Finn M.G. Icosahedral virus particles as addressable nanoscale building blocks. Angew. Chem. Int. Ed. Engl. 41 (2002) 459-462
60. Wang L.X., Ni J., Singh S., and Li H. Binding of high-mannose-type oligosaccharides and synthetic oligomannose clusters to human antibody 2G12: implications for HIV-1 vaccine design. Chem. Biol. 11 (2004) 127-134
61. Wang J., Li H., Zou G., and Wang L.X. Novel template-assembled oligosaccharide clusters as epitope mimics for HIV-neutralizing antibody 2G12. Design, synthesis, and antibody binding study. Org. Biomol. Chem. 5 (2007) 1529-1540
62. Wang S.K., Liang P.H., Astronomo R.D., Hsu T.L., Hsieh S.L., Burton D.R., and Wong C.H. Targeting the carbohydrates on HIV-1: interaction of oligomannose dendrons with human monoclonal antibody 2G12 and DC-SIGN. Proc. Natl. Acad. Sci. USA 105 (2008) 3690-3695
63. Woods R.J., Pathiaseril A., Wormald M.R., Edge C.J., and Dwek R.A. The high degree of internal flexibility observed for an oligomannose oligosaccharide does not alter the overall topology of the molecule. Eur. J. Biochem. 258 (1998) 372-386
64. Wyatt R., and Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 (1998) 1884-1888
65. Wyatt R., Kwong P.D., Desjardins E., Sweet R.W., Robinson J., Hendrickson W.A., and Sodroski J.G. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393 (1998) 705-711
66. Zwick M.B., Labrijn A.F., Wang M., Spenlehauer C., Saphire E.O., Binley J.M., Moore J.P., Stiegler G., Katinger H., Burton D.R., et al. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75 (2001) 10892-10905