Glycosylation benchmark profile for HIV-1 envelope glycoprotein production based on eleven Env trimers

Journal of Virology

Volumn 91, Issue 9, 2017, Pages

  Go, Eden P ^a   Ding, Haitao ^b   Zhang, Shijian ^c   Ringe, Rajesh P ^d   Nicely, Nathan ^e   Hua, David ^a   Steinbock, Robert T ^c   Golabek, Michael ^d   Alin, James ^e   Munir Alam, S ^e   Cupo, Albert ^d   Haynes, Barton F ^e   Kappes, John C ^b,f   Moore, John P ^d   Sodroski, Joseph G ^c   Desaire, Heather ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b University of Alabama at Birmingham   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Env; Glycopeptides; Human immunodeficiency virus

Indexed keywords

GLYCAN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; GLYCOPROTEIN GP 160; VIRUS ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN GP 41; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY;

AMINO ACID SEQUENCE; ARTICLE; CHO CELL LINE; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS 1; MASS SPECTROMETRY; PROTEIN CLEAVAGE; PROTEIN GLYCOSYLATION; PURIFICATION; T LYMPHOCYTE; VACCINE PRODUCTION; VIRUS STRAIN; ANIMAL; BENCHMARKING; CHEMISTRY; CRICETULUS; GLYCOSYLATION; HAMSTER; IMMUNE EVASION; IMMUNOLOGY;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; BENCHMARKING; CHO CELLS; CRICETINAE; CRICETULUS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; GLYCOSYLATION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV-1; IMMUNE EVASION;

EID: 85017545019     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02428-16     Document Type: Article

References (69)

1. UNAIDS. 2012. UNAIDS report on the global HIV/epidemic AIDS. United Nations Programme on HIV/AIDS, Geneva, Switzerland
2. Hoxie JA. 2010. Toward an antibody-based HIV-1 vaccine. Annu Rev Med 61:135-152. https://doi.org/10.1146/annurev.med.60.042507.164323
3. Klein E, Ho RJ. 2000. Challenges in the development of an effective HIV vaccine: current approaches and future directions. Clin Ther 22:295-314. https://doi.org/10.1016/S0149-2918(00)80034-X
4. Letvin NL. 2005. Progress toward an HIV vaccine. Annu Rev Med 56: 213-223. https://doi.org/10.1146/annurev.med.54.101601.152349
5. Mascola JR, Lewis MG, Stiegler G, Harris D, VanCott TC, Hayes D, Louder MK, Brown CR, Sapan CV, Frankel SS, Lu Y, Robb ML, Katinger H, Birx DL. 1999. Protection of Macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J Virol 73:4009-4018
6. Shibata R, Igarashi T, Haigwood N, Buckler-White A, Ogert R, Ross W, Willey R, Cho MW, Martin MA. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat Med 5:204-210. https://doi.org/10.1038/5568
7. Hessell AJ, Hangartner L, Hunter M, Havenith CE, Beurskens FJ, Bakker JM, Lanigan CM, Landucci G, Forthal DN, Parren PW, Marx PA, Burton DR. 2007. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449:101-104. https://doi.org/10.1038/nature06106
8. Hessell AJ, Rakasz EG, Tehrani DM, Huber M, Weisgrau KL, Landucci G, Forthal DN, Koff WC, Poignard P, Watkins DI, Burton DR. 2010. Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. J Virol 84:1302-1313. https://doi.org/10 .1128/JVI.01272-09
9. Ruprecht RM. 2009. Passive immunization with human neutralizing monoclonal antibodies against HIV-1 in macaque models: experimental approaches. Methods Mol Biol 525:559-566, xiv. https://doi.org/10 .1007/978-1-59745-554-1_31
10. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, Dunlop DC, Poignard P, Doyle LA, Cavacini L, Veazey RS, Moore JP. 2011. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci U S A 108:11181-11186. https://doi.org/10 .1073/pnas.1103012108
11. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, Evans DT, Montefiori DC, Karnasuta C, Sutthent R, Liao HX, DeVico AL, Lewis GK, Williams C, Pinter A, Fong Y, Janes H, DeCamp A, Huang Y, Rao M, Billings E, Karasavvas N, Robb ML, Ngauy V, de Souza MS, Paris R, Ferrari G, Bailer RT, Soderberg KA, Andrews C, Berman PW, Frahm N, De Rosa SC, Alpert MD, Yates NL, Shen X, Koup RA, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Michael NL, Kim JH. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 366:1275-1286. https://doi.org/10.1056/NEJMoa1113425
12. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, Premsri N, Namwat C, de Souza M, Adams E, Benenson M, Gurunathan S, Tartaglia J, McNeil JG, Francis DP, Stablein D, Birx DL, Chunsuttiwat S, Khamboonruang C, Thongcharoen P, Robb ML, Michael NL, Kunasol P, Kim JH. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361:2209-2220. https://doi.org/10.1056/NEJMoa0908492
13. Robey WG, Safai B, Oroszlan S, Arthur LO, Gonda MA, Gallo RC, Fischinger PJ. 1985. Characterization of envelope and core structural gene products of HTLV-III with sera from AIDS patients. Science 228:593-595. https://doi.org/10.1126/science.2984774
14. Allan JS, Coligan JE, Barin F, McLane MF, Sodroski JG, Rosen CA, Haseltine WA, Lee TH, Essex M. 1985. Major glycoprotein antigens that induce antibodies in AIDS patients are encoded by HTLV-III. Science 228: 1091-1094. https://doi.org/10.1126/science.2986290
15. Wyatt R, Sodroski J. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888. https://doi.org/10 .1126/science.280.5371.1884
16. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, Majeed S, Steenbeke TD, Venturi M, Chaiken I, Fung M, Katinger H, Parren PW, Robinson J, Van RD, Wang L, Burton DR, Freire E, Wyatt R, Sodroski J, Hendrickson WA, Arthos J. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420: 678-682. https://doi.org/10.1038/nature01188
17. McCaffrey RA, Saunders C, Hensel M, Stamatatos L. 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. https://doi.org/10 .1128/JVI.78.7.3279-3295.2004
18. Reitter JN, Means RE, Desrosiers RC. 1998. A role for carbohydrates in immune evasion in AIDS. Nat Med 4:679-684. https://doi.org/10.1038/nm0698-679
19. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, Salazar-Gonzalez JF, Salazar MG, Kilby JM, Saag MS, Komarova NL, Nowak MA, Hahn BH, Kwong PD, Shaw GM. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312. https://doi.org/10.1038/nature01470
20. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, Hendrickson WA, Sodroski JG. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711. https://doi.org/10.1038/31514
21. Leonard CK, Spellman MW, Riddle L, Harris RJ, Thomas JN, Gregory TJ. 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
22. Mizuochi T, Spellman MW, Larkin M, Solomon J, Basa LJ, Feizi T. 1988. Carbohydrate structures of the human-immunodeficiency-virus (HIV) recombinant envelope glycoprotein gp120 produced in Chinesehamster ovary cells. Biochem J 254:599-603. https://doi.org/10.1042/bj2540599
23. Zhu X, Borchers C, Bienstock RJ, Tomer KB. 2000. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39:11194-11204. https://doi.org/10.1021/bi000432m
24. Lee WR, Yu XF, Syu WJ, Essex M, Lee TH. 1992. Mutational analysis of conserved N-linked glycosylation sites of human immunodeficiency virus type 1 gp41. J Virol 66:1799-1803
25. Go EP, Herschhorn A, Gu C, Castillo-Menendez L, Zhang S, Mao Y, Chen H, Ding H, Wakefield JK, Hua D, Liao HX, Kappes JC, Sodroski J, Desaire H. 2015. Comparative analysis of the glycosylation profiles of membrane-anchored HIV-1 envelope glycoprotein trimers and soluble gp140. J Virol 89:8245- 8257. https://doi.org/10.1128/JVI.00628-15
26. Stansell E, Canis K, Haslam SM, Dell A, Desrosiers RC. 2011. Simian immunodeficiency virus from the sooty mangabey and rhesus macaque is modified with O-linked carbohydrate. J Virol 85:582-595. https://doi .org/10.1128/JVI.01871-10
27. Stansell E, Panico M, Canis K, Pang PC, Bouché L, Binet D, O'Connor MJ, Chertova E, Bess J, Lifson JD, Haslam SM, Morris HR, Desrosiers RC, Dell A. 2015. Gp120 on HIV-1 virions lacks O-linked carbohydrate. PLoS One 10:e0124784. https://doi.org/10.1371/journal.pone.0124784
28. Stewart-Jones G, Soto C, Lemmin T, Chuang GY, Druz A, Kong R, Thomas P, Wagh K, Zhou T, Behrens AJ, Bylund T, Choi C, Davison J, Georgiev I, Joyce M, Kwon Y, Pancera M, Taft J, Yang Y, Zhang B, Shivatare S, Shivatare V, Lee CC, Wu CY, Bewley C, Burton D, Koff W, Connors M, Crispin M, Baxa U, Korber B, Wong CH, Mascola J, Kwong P. 2016. Trimeric HIV-1-Env structures define glycan shields from clades A, B, and G. Cell 165:813- 826. https://doi.org/10.1016/j.cell.2016.04.010
29. Koch M, Pancera M, Kwong PD, Kolchinsky P, Grundner C, Wang L, Hendrickson WA, Sodroski J, Wyatt R. 2003. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313:387- 400. https://doi.org/10 .1016/S0042-6822(03)00294-0
30. Mao Y, Wang L, Gu C, Herschhorn A, Desormeaux A, Finzi A, Xiang SH, Sodroski JG. 2013. Molecular architecture of the uncleaved HIV-1 envelope glycoprotein trimer. Proc Natl Acad Sci U S A 110:12438-12443. https://doi.org/10.1073/pnas.1307382110
31. Haim H, Strack B, Kassa A, Madani N, Wang L, Courter JR, Princiotto A, McGee K, Pacheco B, Seaman MS, Smith AB III, Sodroski J. 2011. Contribution of intrinsic reactivity of the HIV-1 envelope glycoproteins to CD4-independent infection and global inhibitor sensitivity. PLoS Pathog 7:e1002101. https://doi.org/10.1371/journal.ppat.1002101
32. Haim H, Salas I, McGee K, Eichelberger N, Winter E, Pacheco B, Sodroski J. 2013. Modeling virus- and antibody-specific factors to predict human immunodeficiency virus neutralization efficiency. Cell Host Microbe 14: 547-558. https://doi.org/10.1016/j.chom.2013.10.006
33. Kong L, Sheppard NC, Stewart-Jones GBE, Robson CL, Chen H, Xu X, Krashias G, Bonomelli C, Scanlan CN, Kwong PD, Jeffs SA, Jones IM, Sattentau QJ. 2010. Expression-system-dependent modulation of HIV-1 envelope glycoprotein antigenicity and immunogenicity. J Mol Biol 403:131-147. https://doi.org/10.1016/j.jmb.2010.08.033
34. Bolmstedt A, Sjolander S, Hansen JE, Akerblom L, Hemming A, Hu SL, Morein B, Olofsson S. 1996. Influence of N-linked glycans in V4-V5 region of human immunodeficiency virus type 1 glycoprotein gp160 on induction of a virus-neutralizing humoral response. J Acquir Immune Defic Syndr Hum Retrovirol 12:213-220. https://doi.org/10.1097/00042560-199607000-00001
35. Kong L, Lee JH, Doores KJ, Murin CD, Julien JP, McBride R, Liu Y, Marozsan A, Cupo A, Klasse PJ, Hoffenberg S, Caulfield M, King CR, Hua Y, Le KM, Khayat R, Deller MC, Clayton T, Tien H, Feizi T, Sanders RW, Paulson JC, Moore JP, Stanfield RL, Burton DR, Ward AB, Wilson IA. 2013. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol 20:796-803. https://doi.org/10.1038/nsmb.2594
36. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien JP, Wang SK, Ramos A, Chan-Hui PY, Moyle M, Mitcham JL, Hammond PW, Olsen OA, Phung P, Fling S, Wong CH, Phogat S, Wrin T, Simek MD, Koff WC, Wilson IA, Burton DR, Poignard P. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470. https://doi.org/10.1038/nature10373
37. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang PS, Wang SK, Stanfield RL, Julien JP, Ramos A, Crispin M, Depetris R, Katpally U, Marozsan A, Cupo A, Maloveste S, Liu Y, McBride R, Ito Y, Sanders RW, Ogohara C, Paulson JC, Feizi T, Scanlan CN, Wong CH, Moore JP, Olson WC, Ward AB, Poignard P, Schief WR, Burton DR, Wilson IA. 2011. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334:1097-1103. https://doi.org/10.1126/science.1213256
38. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, Lehrman JK, Priddy FH, Olsen OA, Frey SM, Hammond PW, Kaminsky S, Zamb T, Moyle M, Koff WC, Poignard P, Burton DR. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289. https://doi.org/10.1126/science.1178746
39. McLellan JS, Pancera M, Carrico C, Gorman J, Julien JP, Khayat R, Louder R, Pejchal R, Sastry M, Dai K, O'Dell S, Patel N, Shahzad-Ul-Hussan S, Yang Y, Zhang B, Zhou T, Zhu J, Boyington JC, Chuang GY, Diwanji D, Georgiev I, Kwon YD, Lee D, Louder MK, Moquin S, Schmidt SD, Yang ZY, Bonsignori M, Crump JA, Kapiga SH, Sam NE, Haynes BF, Burton DR, Koff WC, Walker LM, Phogat S, Wyatt R, Orwenyo J, Wang LX, Arthos J, Bewley CA, Mascola JR, Nabel GJ, Schief WR, Ward AB, Wilson IA, Kwong PD. 2011. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480:336-343. https://doi.org/10.1038/nature10696
40. Alam SM, Dennison SM, Aussedat B, Vohra Y, Park PK, Fernandez-Tejada A, Stewart S, Jaeger FH, Anasti K, Blinn JH, Kepler TB, Bonsignori M, Liao HX, Sodroski JG, Danishefsky SJ, Haynes BF. 2013. Recognition of synthetic glycopeptides by HIV-1 broadly neutralizing antibodies and their unmutated ancestors. Proc Natl Acad Sci U S A 110:18214-18219. https://doi.org/10.1073/pnas.1317855110
41. Falkowska E, Le KM, Ramos A, Doores KJ, Lee JH, Blattner C, Ramirez A, Derking R, van Gils MJ, Liang CH, Mcbride R, von Bredow B, Shivatare SS, Wu CY, Chan-Hui PY, Liu Y, Feizi T, Zwick MB, Koff WC, Seaman MS, Swiderek K, Moore JP, Evans D, Paulson JC, Wong CH, Ward AB, Wilson IA, Sanders RW, Poignard P, Burton DR. 2014. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 40:657- 668. https://doi.org/10.1016/j.immuni.2014.04.009
42. Huang J, Kang BH, Pancera M, Lee JH, Tong T, Feng Y, Imamichi H, Georgiev IS, Chuang GY, Druz A, Doria-Rose NA, Laub L, Sliepen K, van Gils MJ, de la Peña AT, Derking R, Klasse PJ, Migueles SA, Bailer RT, Alam M, Pugach P, Haynes BF, Wyatt RT, Sanders RW, Binley JM, Ward AB, Mascola JR, Kwong PD, Connors M. 2014. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature 515:138-142. https://doi.org/10.1038/nature13601
43. Bonomelli C, Doores KJ, Dunlop DC, Thaney V, Dwek RA, Burton DR, Crispin M, Scanlan CN. 2011. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS One 6:e23521. https://doi.org/10.1371/journal.pone.0023521
44. Doores KJ, Bonomelli C, Harvey DJ, Vasiljevic S, Dwek RA, Burton DR, Crispin M, Scanlan CN. 2010. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sci U S A 107:13800-13805. https://doi.org/10.1073/pnas.1006498107
45. Yang W, Shah P, Toghi ES, Yang S, Sun S, Ao M, Rubin A, Jackson JB, Zhang H. 2014. Glycoform analysis of recombinant and human immunodeficiency virus envelope protein gp120 via higher energy collisional dissociation and spectral-aligning strategy. Anal Chem 86:6959-6967. https://doi.org/10.1021/ac500876p
46. Behrens AJ, Vasiljevic S, Pritchard LK, Harvey DJ, Andev RS, Krumm SA, Struwe WB, Cupo A, Kumar A, Zitzmann N, Seabright GE, Kramer HB, Spencer DI, Royle L, Lee JH, Klasse PJ, Burton DR, Wilson IA, Ward AB, Sanders RW, Moore JP, Doores KJ, Crispin M. 2016. Composition and antigenic effects of individual glycan sites of a trimeric HIV-1 envelope glycoprotein. Cell Rep 14:2695-2706. https://doi.org/10.1016/j.celrep .2016.02.058
47. Behrens AJ, Harvey DJ, Milne E, Cupo A, Kumar A, Zitzmann N, Struwe WB, Moore JP, Crispin M. 2 November 2016. Molecular architecture of the cleavage-dependent mannose patch on a soluble HIV-1 envelope glycoprotein trimer. J Virol https://doi.org/10.1128/JVI.01894-16
48. Panico M, Bouché L, Binet D, O'Connor MJ, Rahman D, Pang PC, Canis K, North SJ, Desrosiers RC, Chertova E, Keele BF, Bess JW, Jr, Lifson JD, Haslam SM, Dell A, Morris HR. 2016. Mapping the complete glycoproteome of virion-derived HIV-1 gp120 provides insights into broadly neutralizing antibody binding. Sci Rep 6:32956. https://doi.org/10.1038/srep32956
49. Go EP, Irungu J, Zhang Y, Dalpathado DS, Liao HX, Sutherland LL, Alam SM, Haynes BF, Desaire H. 2008. Glycosylation site-specific analysis of HIV envelope proteins (JR-FL and CON-S) reveals major differences in glycosylation site occupancy, glycoform profiles, and antigenic epitopes' accessibility. J Proteome Res 7:1660-1674. https://doi.org/10.1021/pr7006957
50. Go EP, Chang Q, Liao HX, Sutherland LL, Alam SM, Haynes BF, Desaire H. 2009. Glycosylation site-specific analysis of clade C HIV-1 envelope proteins. J Proteome Res 8:4231- 4242. https://doi.org/10.1021/pr9002728
51. Go EP, Hewawasam G, Liao HX, Chen H, Ping LH, Anderson JA, Hua DC, Haynes BF, Desaire H. 2011. Characterization of glycosylation profiles of HIV-1 transmitted/founder envelopes by mass spectrometry. J Virol 85:8270-8284. https://doi.org/10.1128/JVI.05053-11
52. Go EP, Hewawasam GS, Ma BJ, Liao HX, Haynes BF, Desaire H. 2011. Methods development for analysis of partially deglycosylated proteins and application to an HIV envelope protein vaccine candidate. Int J Mass Spectrom 305:209-216. https://doi.org/10.1016/j.ijms.2010.11.009
53. Go EP, Liao HX, Alam SM, Hua D, Haynes BF, Desaire H. 2013. Characterization of host-cell line specific glycosylation profiles of early transmitted/founder HIV-1 gp120 envelope proteins. J Proteome Res 12:1223-1234. https://doi.org/10.1021/pr300870t
54. Go EP, Rebecchi KR, Dalpathado DS, Bandu ML, Zhang Y, Desaire H. 2007. GlycoPep DB: a tool for glycopeptide analysis using a "Smart Search". Anal Chem 79:1708-1713. https://doi.org/10.1021/ac061548c
55. Pritchard LK, Vasiljevic S, Ozorowski G, Seabright GE, Cupo A, Ringe R, Kim HJ, Sanders RW, Doores KJ, Burton DR, Wilson IA, Ward AB, Moore JP, Crispin M. 2015. Structural constraints determine the glycosylation of HIV-1 envelope trimers. Cell Rep 11:1604-1613. https://doi.org/10.1016/j.celrep.2015.05.017
56. Ringe RP, Yasmeen A, Ozorowski G, Go EP, Pritchard LK, Guttman M, Ketas TA, Cottrell CA, Wilson IA, Sanders RW, Cupo A, Crispin M, Lee KK, Desaire H, Ward AB, Klasse PJ, Moore JP. 2015. Influences on the design and purification of soluble, recombinant native-like HIV-1 envelope glycoprotein trimers. J Virol 89:12189-12210. https://doi.org/10.1128/JVI .01768-15
57. Verkerke HP, Williams JA, Guttman M, Simonich CA, Liang Y, Filipavicius M, Hu S-L, Overbaugh J, Lee KK. 2016. Epitope-independent purification of native-like envelope trimers from diverse HIV-1 isolates. J Virol 90: 9471-9482. https://doi.org/10.1128/JVI.01351-16
58. Zambonelli C, Dey AK, Hilt S, Stephenson S, Go EP, Clark DF, Wininger M, Labranche C, Montefiori D, Liao HX, Swanstrom RI, Desaire H, Haynes BF, Carfi A, Barnett SW. 2016. Generation and characterization of a bivalent HIV-1 subtype C gp120 protein boost for proof-of-concept HIV vaccine efficacy trials in Southern Africa. PLoS One 11:e0157391. https://doi.org/10.1371/journal.pone.0157391
59. Go EP, Cupo A, Ringe R, Pugach P, Moore JP, Desaire H. 2015. Native conformation and canonical disulfide bond formation are interlinked properties of HIV-1 Env glycoproteins. J Virol 90:2884-2894. https://doi .org/10.1128/JVI.01953-15
60. Hildebrandt E, Ding H, Mulky A, Dai Q, Aleksandrov AA, Bajrami B, Diego PA, Wu X, Ray M, Naren AP, Riordan JR, Yao X, DeLucas LJ, Urbatsch IL, Kappes JC. 2015. A stable human-cell system overexpressing cystic fibrosis transmembrane conductance regulator recombinant protein at the cell surface. Mol Biotechnol 57:391- 405. https://doi.org/10.1007/s12033-014-9830-5
61. Ringe RP, Sanders RW, Yasmeen A, Kim HJ, Lee JH, Cupo A, Korzun J, Derking R, van Montfort T, Julien JP, Wilson IA, Klasse PJ, Ward AB, Moore JP. 2013. Cleavage strongly influences whether soluble HIV-1 envelope glycoprotein trimers adopt a native-like conformation. Proc Natl Acad Sci U S A 110:18256-18261. https://doi.org/10.1073/pnas.1314351110
62. Sanders RW, Derking R, Cupo A, Julien JP, Yasmeen A, de Val N, Kim HJ, Blattner C, de la Peña AT, Korzun J, Golabek M, de Los Reyes K, Ketas TJ, van Gils MJ, King CR, Wilson IA, Ward AB, Klasse PJ, Moore JP. 2013. 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:e1003618. https://doi.org/10 .1371/journal.ppat.1003618
63. Go EP, Hua D, Desaire H. 2014. Glycosylation and disulfide bond analysis of transiently and stably expressed clade C HIV-1 gp140 trimers in 293T cells identifies disulfide heterogeneity present in both proteins and differences in O-linked glycosylation. J Proteome Res 13:4012- 4027. https://doi.org/10.1021/pr5003643
64. Irungu J, Go EP, Dalpathado DS, Desaire H. 2007. Simplification of mass spectral analysis of acidic glycopeptides using GlycoPep ID. Anal Chem 79:3065-3074. https://doi.org/10.1021/ac062100e
65. Cooper CA, Gasteiger E, Packer NH. 2001. GlycoMod-a software tool for determining glycosylation compositions from mass spectrometric data. Proteomics 1:340-349. https://doi.org/10.1002/1615-9861 (200102)1:2+340::AID-PROT340=3.0.CO;2-B
66. Irungu J, Go EP, Zhang Y, Dalpathado DS, Liao HX, Haynes BF, Desaire H. 2008. Comparison of HPLC/ESI-FTICR MS versus MALDI-TOF/TOF MS for glycopeptide analysis of a highly glycosylated HIV envelope glycoprotein. J Am Soc Mass Spectrom 19:1209-1220. https://doi.org/10.1016/j .jasms.2008.05.010
67. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R. 2013. Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41:W597-W600. https://doi.org/10.1093/nar/gkt376
68. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
69. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R. 2010. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:W695-W699. https://doi.org/10.1093/nar/gkq313