Erratum: Glycans Function as Anchors for Antibodies and Help Drive HIV Broadly Neutralizing Antibody Development (Immunity (2017) 47(3) (524–537.e3) (S1074761317303643)(10.1016/j.immuni.2017.08.006));Glycans Function as Anchors for Antibodies and Help Drive HIV Broadly Neutralizing Antibody Development

Immunity

Volumn 47, Issue 3, 2017, Pages 524-537.e3

  Andrabi, Raiees ^a   Su, Ching Yao ^a   Liang, Chi Hui ^a   Shivatare, Sachin S ^b   Briney, Bryan ^a   Voss, James E ^a   Nawazi, Salar Khan ^a   Wu, Chung Yi ^b   Wong, Chi Huey ^b   Burton, Dennis R ^a,c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b GENOMICS RESEARCH CENTER   (Taiwan)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

B cell affinity maturation; bnAbs; broadly neutralizing antibodies; Env glycans; glycan engineering; HIV envelope trimer; V2 apex epitope; virus escape

Indexed keywords

ALPHA 2,6 SIALIDASE; BROADLY NEUTRALIZING ANTIBODY CAP256.03; BROADLY NEUTRALIZING ANTIBODY CAP256.04; BROADLY NEUTRALIZING ANTIBODY CAP256.07; BROADLY NEUTRALIZING ANTIBODY CAP256.08; BROADLY NEUTRALIZING ANTIBODY CAP256.09; BROADLY NEUTRALIZING ANTIBODY CAP256.12; BROADLY NEUTRALIZING ANTIBODY CAP256.13; BROADLY NEUTRALIZING ANTIBODY CAP256.17; BROADLY NEUTRALIZING ANTIBODY CAP256.18; BROADLY NEUTRALIZING ANTIBODY CAP256.21; BROADLY NEUTRALIZING ANTIBODY CAP256.22; BROADLY NEUTRALIZING ANTIBODY CAP256.25; BROADLY NEUTRALIZING ANTIBODY CAP256.26; BROADLY NEUTRALIZING ANTIBODY CAP256.27; BROADLY NEUTRALIZING ANTIBODY CAP256.28; BROADLY NEUTRALIZING ANTIBODY CAP256.29; BROADLY NEUTRALIZING ANTIBODY CAP256.30; BROADLY NEUTRALIZING ANTIBODY CAP256.31; BROADLY NEUTRALIZING ANTIBODY CDRH2; BROADLY NEUTRALIZING ANTIBODY CH01; BROADLY NEUTRALIZING ANTIBODY PG16; BROADLY NEUTRALIZING ANTIBODY PG9; BROADLY NEUTRALIZING ANTIBODY PGT145; GLYCAN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; SIALIC ACID; UNCLASSIFIED DRUG; VIRUS SIALIDASE; EPITOPE; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN HEAVY CHAIN; N ACETYLNEURAMINIC ACID; PEPTIDE FRAGMENT; POLYSACCHARIDE; PROTEIN BINDING;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; FEMALE; GERMLINE MUTATION; HEAVY CHAIN; HEK293-F CELL LINE; HEK293S CELL LINE; HEK293T CELL LINE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE EVASION; IMMUNE RESPONSE; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SOMATIC MUTATION; TZM-BL CELL LINE; VIRUS ENVELOPE; VIRUS MUTANT; VIRUS NEUTRALIZATION; BINDING SITE; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MOLECULAR MODEL; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SERODIAGNOSIS; VIROLOGY;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIBODY AFFINITY; ANTIBODY FORMATION; BINDING SITES; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; MODELS, MOLECULAR; N-ACETYLNEURAMINIC ACID; NEUTRALIZATION TESTS; PEPTIDE FRAGMENTS; PHYLOGENY; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 85029172601     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.10.012     Document Type: Erratum

References (54)

1. Amin, M.N., McLellan, J.S., Huang, W., Orwenyo, J., Burton, D.R., Koff, W.C., Kwong, P.D., Wang, L.X., Synthetic glycopeptides reveal the glycan specificity of HIV-neutralizing antibodies. Nat. Chem. Biol. 9 (2013), 521–526.
2. Andrabi, R., Voss, J.E., Liang, C.H., Briney, B., McCoy, L.E., Wu, C.Y., Wong, C.H., Poignard, P., Burton, D.R., Identification of common features in prototype broadly neutralizing antibodies to HIV envelope V2 apex to facilitate vaccine design. Immunity 43 (2015), 959–973.
3. Behrens, A.J., Vasiljevic, S., Pritchard, L.K., Harvey, D.J., Andev, R.S., Krumm, S.A., Struwe, W.B., Cupo, A., Kumar, A., Zitzmann, N., et al. Composition and antigenic effects of individual glycan sites of a trimeric HIV-1 envelope glycoprotein. Cell Rep. 14 (2016), 2695–2706.
4. Bhiman, J.N., Anthony, C., Doria-Rose, N.A., Karimanzira, O., Schramm, C.A., Khoza, T., Kitchin, D., Botha, G., Gorman, J., Garrett, N.J., et al. Viral variants that initiate and drive maturation of V1V2-directed HIV-1 broadly neutralizing antibodies. Nat. Med. 21 (2015), 1332–1336.
5. Bonsignori, M., Hwang, K.K., Chen, X., Tsao, C.Y., Morris, L., Gray, E., Marshall, D.J., Crump, J.A., Kapiga, S.H., Sam, N.E., et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 85 (2011), 9998–10009.
6. Bonsignori, M., Liao, H.X., Gao, F., Williams, W.B., Alam, S.M., Montefiori, D.C., Haynes, B.F., Antibody-virus co-evolution in HIV infection: paths for HIV vaccine development. Immunol. Rev. 275 (2017), 145–160.
7. Briney, B., Sok, D., Jardine, J.G., Kulp, D.W., Skog, P., Menis, S., Jacak, R., Kalyuzhniy, O., de Val, N., Sesterhenn, F., et al. Tailored immunogens direct affinity maturation toward HIV neutralizing antibodies. Cell 166 (2016), 1459–1470.e11.
8. Briney, B., Le, K., Zhu, J., Burton, D.R., Clonify: unseeded antibody lineage assignment from next-generation sequencing data. Sci. Rep., 6, 2016, 23901.
9. Burton, D.R., Antibodies, viruses and vaccines. Nat. Rev. Immunol. 2 (2002), 706–713.
10. Cao, L., Diedrich, J.K., Kulp, D.W., Pauthner, M., He, L., Park, S.R., Sok, D., Su, C.Y., Delahunty, C.M., Menis, S., et al. Global site-specific N-glycosylation analysis of HIV envelope glycoprotein. Nat. Commun., 8, 2017, 14954.
11. Dimitrov, D.S., Therapeutic antibodies, vaccines and antibodyomes. MAbs 2 (2010), 347–356.
12. Doores, K.J., Burton, D.R., Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16. J. Virol. 84 (2010), 10510–10521.
13. Doria-Rose, N.A., Schramm, C.A., Gorman, J., Moore, P.L., Bhiman, J.N., DeKosky, B.J., Ernandes, M.J., Georgiev, I.S., Kim, H.J., Pancera, M., et al., NISC Comparative Sequencing Program. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509 (2014), 55–62.
14. Doria-Rose, N.A., Bhiman, J.N., Roark, R.S., Schramm, C.A., Gorman, J., Chuang, G.Y., Pancera, M., Cale, E.M., Ernandes, M.J., Louder, M.K., et al. New member of the V1V2-directed CAP256-VRC26 lineage that shows increased breadth and exceptional potency. J. Virol. 90 (2015), 76–91.
15. Dosenovic, P., von Boehmer, L., Escolano, A., Jardine, J., Freund, N.T., Gitlin, A.D., McGuire, A.T., Kulp, D.W., Oliveira, T., Scharf, L., et al. Immunization for HIV-1 broadly neutralizing antibodies in human Ig knockin mice. Cell 161 (2015), 1505–1515.
16. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004), 1792–1797.
17. Escolano, A., Steichen, J.M., Dosenovic, P., Kulp, D.W., Golijanin, J., Sok, D., Freund, N.T., Gitlin, A.D., Oliveira, T., Araki, T., et al. Sequential immunization elicits broadly neutralizing anti-HIV-1 antibodies in Ig knockin mice. Cell 166 (2016), 1445–1458.e12.
18. Falkowska, E., Le, K.M., Ramos, A., Doores, K.J., Lee, J.H., Blattner, C., Ramirez, A., Derking, R., van Gils, M.J., Liang, C.H., et al. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 40 (2014), 657–668.
19. Georgiev, I.S., Doria-Rose, N.A., Zhou, T., Kwon, Y.D., Staupe, R.P., Moquin, S., Chuang, G.Y., Louder, M.K., Schmidt, S.D., Altae-Tran, H.R., et al. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 340 (2013), 751–756.
20. Gorman, J., Soto, C., Yang, M.M., Davenport, T.M., Guttman, M., Bailer, R.T., Chambers, M., Chuang, G.Y., DeKosky, B.J., Doria-Rose, N.A., et al., NISC Comparative Sequencing Program. Structures of HIV-1 Env V1V2 with broadly neutralizing antibodies reveal commonalities that enable vaccine design. Nat. Struct. Mol. Biol. 23 (2016), 81–90.
21. Gristick, H.B., von Boehmer, L., West, A.P. Jr., Schamber, M., Gazumyan, A., Golijanin, J., Seaman, M.S., Fätkenheuer, G., Klein, F., Nussenzweig, M.C., Bjorkman, P.J., Natively glycosylated HIV-1 Env structure reveals new mode for antibody recognition of the CD4-binding site. Nat. Struct. Mol. Biol. 23 (2016), 906–915.
22. Huerta-Cepas, J., Dopazo, J., Gabaldón, T., ETE: a python environment for tree exploration. BMC Bioinformatics, 11, 2010, 24.
23. Jardine, J., Julien, J.P., Menis, S., Ota, T., Kalyuzhniy, O., McGuire, A., Sok, D., Huang, P.S., MacPherson, S., Jones, M., et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 340 (2013), 711–716.
24. Jardine, J.G., Ota, T., Sok, D., Pauthner, M., Kulp, D.W., Kalyuzhniy, O., Skog, P.D., Thinnes, T.C., Bhullar, D., Briney, B., et al. HIV-1 VACCINES. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science 349 (2015), 156–161.
25. Julien, J.P., Cupo, A., Sok, D., Stanfield, R.L., Lyumkis, D., Deller, M.C., Klasse, P.J., Burton, D.R., Sanders, R.W., Moore, J.P., et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342 (2013), 1477–1483.
26. Landais, E., Huang, X., Havenar-Daughton, C., Murrell, B., Price, M.A., Wickramasinghe, L., Ramos, A., Bian, C.B., Simek, M., Allen, S., et al. Broadly neutralizing antibody responses in a large longitudinal sub-Saharan HIV primary infection cohort. PLoS Pathog., 12, 2016, e1005369.
27. Lee, J.H., Andrabi, R., Su, C.Y., Yasmeen, A., Julien, J.P., Kong, L., Wu, N.C., McBride, R., Sok, D., Pauthner, M., et al. A broadly neutralizing antibody targets the dynamic HIV envelope trimer apex via a long, rigidified, and anionic β-hairpin structure. Immunity 46 (2017), 690–702.
28. Li, W., Godzik, A., Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22 (2006), 1658–1659.
29. Liao, H.X., Lynch, R., Zhou, T., Gao, F., Alam, S.M., Boyd, S.D., Fire, A.Z., Roskin, K.M., Schramm, C.A., Zhang, Z., et al., NISC Comparative Sequencing Program. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496 (2013), 469–476.
30. Lin, C.W., Tsai, M.H., Li, S.T., Tsai, T.I., Chu, K.C., Liu, Y.C., Lai, M.Y., Wu, C.Y., Tseng, Y.C., Shivatare, S.S., et al. A common glycan structure on immunoglobulin G for enhancement of effector functions. Proc. Natl. Acad. Sci. USA 112 (2015), 10611–10616.
31. MacLeod, D.T., Choi, N.M., Briney, B., Garces, F., Ver, L.S., Landais, E., Murrell, B., Wrin, T., Kilembe, W., Liang, C.H., et al., IAVI Protocol C Investigators & The IAVI African HIV Research Network. Early antibody lineage diversification and independent limb maturation lead to broad HIV-1 neutralization targeting the Env high-patch. Immunity 44 (2016), 1215–1226.
32. McGuire, A.T., Gray, M.D., Dosenovic, P., Gitlin, A.D., Freund, N.T., Petersen, J., Correnti, C., Johnsen, W., Kegel, R., Stuart, A.B., et al. Specifically modified Env immunogens activate B-cell precursors of broadly neutralizing HIV-1 antibodies in transgenic mice. Nat. Commun., 7, 2016, 10618.
33. McLellan, J.S., Pancera, M., Carrico, C., Gorman, J., Julien, J.P., Khayat, R., Louder, R., Pejchal, R., Sastry, M., Dai, K., et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480 (2011), 336–343.
34. Montefiori, D.C., Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr. Protoc. Immunol., Chapter 12, 2005, 11.
35. Moore, P.L., Gray, E.S., Wibmer, C.K., Bhiman, J.N., Nonyane, M., Sheward, D.J., Hermanus, T., Bajimaya, S., Tumba, N.L., Abrahams, M.R., et al. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat. Med. 18 (2012), 1688–1692.
36. Mouquet, H., Scharf, L., Euler, Z., Liu, Y., Eden, C., Scheid, J.F., Halper-Stromberg, A., Gnanapragasam, P.N., Spencer, D.I., Seaman, M.S., et al. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc. Natl. Acad. Sci. USA 109 (2012), E3268–E3277.
37. Pancera, M., Shahzad-Ul-Hussan, S., Doria-Rose, N.A., McLellan, J.S., Bailer, R.T., Dai, K., Loesgen, S., Louder, M.K., Staupe, R.P., Yang, Y., et al. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat. Struct. Mol. Biol. 20 (2013), 804–813.
38. Panico, M., Bouché L., Binet, D., O'Connor, M.J., Rahman, D., Pang, P.C., Canis, K., North, S.J., Desrosiers, R.C., Chertova, E., et al. Mapping the complete glycoproteome of virion-derived HIV-1 gp120 provides insights into broadly neutralizing antibody binding. Sci. Rep., 6, 2016, 32956.
39. Price, M.N., Dehal, P.S., Arkin, A.P., FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, 2010, e9490.
40. Pugach, P., Ozorowski, G., Cupo, A., Ringe, R., Yasmeen, A., de Val, N., Derking, R., Kim, H.J., Korzun, J., Golabek, M., et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B env gene. J. Virol. 89 (2015), 3380–3395.
41. Rappuoli, R., Bottomley, M.J., D'Oro, U., Finco, O., De Gregorio, E., Reverse vaccinology 2.0: Human immunology instructs vaccine antigen design. J. Exp. Med. 213 (2016), 469–481.
42. Sanders, R.W., Derking, R., Cupo, A., Julien, J.P., Yasmeen, A., de Val, N., Kim, H.J., Blattner, C., de la Peña, A.T., Korzun, J., et al. A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog., 9, 2013, e1003618.
43. Sanders, R.W., van Gils, M.J., Derking, R., Sok, D., Ketas, T.J., Burger, J.A., Ozorowski, G., Cupo, A., Simonich, C., Goo, L., et al. HIV-1 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science, 349, 2015, aac4223.
44. Seaman, M.S., Janes, H., Hawkins, N., Grandpre, L.E., Devoy, C., Giri, A., Coffey, R.T., Harris, L., Wood, B., Daniels, M.G., et al. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84 (2010), 1439–1452.
45. Shivatare, S.S., Chang, S.H., Tsai, T.I., Tseng, S.Y., Shivatare, V.S., Lin, Y.S., Cheng, Y.Y., Ren, C.T., Lee, C.C., Pawar, S., et al. Modular synthesis of N-glycans and arrays for the hetero-ligand binding analysis of HIV antibodies. Nat. Chem. 8 (2016), 338–346.
46. Sok, D., van Gils, M.J., Pauthner, M., Julien, J.P., Saye-Francisco, K.L., Hsueh, J., Briney, B., Lee, J.H., Le, K.M., Lee, P.S., et al. Recombinant HIV envelope trimer selects for quaternary-dependent antibodies targeting the trimer apex. Proc. Natl. Acad. Sci. USA 111 (2014), 17624–17629.
47. Steichen, J.M., Kulp, D.W., Tokatlian, T., Escolano, A., Dosenovic, P., Stanfield, R.L., McCoy, L.E., Ozorowski, G., Hu, X., Kalyuzhniy, O., et al. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 45 (2016), 483–496.
48. Tian, M., Cheng, C., Chen, X., Duan, H., Cheng, H.L., Dao, M., Sheng, Z., Kimble, M., Wang, L., Lin, S., et al. Induction of HIV neutralizing antibody lineages in mice with diverse precursor repertoires. Cell 166 (2016), 1471–1484.e18.
49. 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., Protocol G Principal Investigators. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326 (2009), 285–289.
50. Walker, L.M., Simek, M.D., Priddy, F., Gach, J.S., Wagner, D., Zwick, M.B., Phogat, S.K., Poignard, P., Burton, D.R., A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog., 6, 2010, e1001028.
51. Walker, L.M., Huber, M., Doores, K.J., Falkowska, E., Pejchal, R., Julien, J.P., Wang, S.K., Ramos, A., Chan-Hui, P.Y., Moyle, M., et al., Protocol G Principal Investigators. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477 (2011), 466–470.
52. Wang, C.C., Chen, J.R., Tseng, Y.C., Hsu, C.H., Hung, Y.F., Chen, S.W., Chen, C.M., Khoo, K.H., Cheng, T.J., Cheng, Y.S., et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc. Natl. Acad. Sci. USA 106 (2009), 18137–18142.
53. Wibmer, C.K., Bhiman, J.N., Gray, E.S., Tumba, N., Abdool Karim, S.S., Williamson, C., Morris, L., Moore, P.L., Viral escape from HIV-1 neutralizing antibodies drives increased plasma neutralization breadth through sequential recognition of multiple epitopes and immunotypes. PLoS Pathog., 9, 2013, e1003738.
54. Xiao, X., Chen, W., Feng, Y., Zhu, Z., Prabakaran, P., Wang, Y., Zhang, M.Y., Longo, N.S., Dimitrov, D.S., Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem. Biophys. Res. Commun. 390 (2009), 404–409.