Molecular Architecture of the cleavage- dependent mannose patch on a soluble HIV-1 envelope glycoprotein trimer

Journal of Virology

Volumn 91, Issue 2, 2017, Pages

  Behrens, Anna Janina ^a   Harvey, David J ^a   Milne, Emilia ^a   Cupo, Albert ^b   Kumar, Abhinav ^a   Zitzmann, Nicole ^a   Struwe, Weston B ^a   Moore, John P ^b   Crispin, Max ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Furin; Glycan; Glycosylation; Human immunodeficiency virus; Neutralizing antibodies; Oligosaccharides; Structure; Vaccines

Indexed keywords

GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MANNOSE; POLYSACCHARIDE; PROTEIN BINDING; VIRUS ENVELOPE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISULFIDE BOND; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHILICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; VIRUS SPIKE; CHEMISTRY; GLYCOSYLATION; METABOLISM; MOLECULAR MODEL; PROTEIN DEGRADATION; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION;

ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GLYCOSYLATION; HIV-1; HUMANS; MANNOSE; MODELS, MOLECULAR; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEOLYSIS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85008682118     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01894-16     Document Type: Article

References (79)

1. Lasky LA, Groopman JE, Fennie CW, Benz PM, Capon DJ, Dowbenko DJ, Nakamura GR, Nunes WM, Renz ME, Berman PW. 1986. Neutralization of the AIDS retrovirus by antibodies to a recombinant envelope glycoprotein. Science 233:209-212. https://doi.org/10.1126/science.3014647.
2. 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.
3. 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.
4. Moore JP, Sodroski J. 1996. Antibody cross-competition analysis of the human immunodeficiency virus type 1 gp120 exterior envelope glycoprotein. J Virol 70:1863-1872.
5. Zhang M, Gaschen B, Blay W, Foley B, Haigwood N, Kuiken C, Korber B. 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. https://doi.org/10.1093/glycob/cwh106.
6. Travers SA. 2012. Conservation, compensation, and evolution of N-linked glycans in the HIV-1 group M subtypes and circulating recombinant forms. ISRN AIDS 2012:823605. https://doi.org/10.5402/2012/823605.
7. 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.
8. 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.
9. Panico M, Bouche 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.
10. Pritchard LK, Harvey DJ, Bonomelli C, Crispin M, Doores KJ. 2015. Celland protein-directed glycosylation of native cleaved HIV-1 envelope. J Virol 89:8932-8944. https://doi.org/10.1128/JVI.01190-15.
11. Pritchard LK, Spencer DI, Royle L, Bonomelli C, Seabright GE, Behrens AJ, Kulp DW, Menis S, Krumm SA, Dunlop DC, Crispin DJ, Bowden TA, Scanlan CN, Ward AB, Schief WR, Doores KJ, Crispin M. 2015. Glycan clustering stabilizes the mannose patch of HIV-1 and preserves vulnerability to broadly neutralizing antibodies. Nat Commun 6:7479. https://doi.org/10.1038/ncomms8479.
12. Blattner C, Lee JH, Sliepen K, Derking R, Falkowska E, de la Pena AT, Cupo A, Julien JP, van Gils M, Lee PS, Peng W, Paulson JC, Poignard P, Burton DR, Moore JP, Sanders RW, Wilson IA, Ward AB. 2014. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 40:669-680. https://doi.org/10.1016/j.immuni.2014.04.008.
13. Falkowska E, Le KM, Ramos A, Doores KJ, Lee JH, Blattner C, Ramirez A, Derking R, van Gils MJ, Liang C-H, McBride R, von Bredow B, Shivatare SS, Wu C-Y, Chan-Hui P-Y, Liu Y, Feizi T, Zwick MB, Koff WC, Seaman MS, Swiderek K, Moore JP, Evans D, Paulson JC, Wong C-H, 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.
14. Garces F, Sok D, Kong L, McBride R, Kim HJ, Saye-Francisco KF, Julien J-P, Hua Y, Cupo A, Moore JP, Paulson JC, Ward AB, Burton DR, Wilson IA. 2014 Structural evolution of glycan recognition by a family of potent HIV antibodies. Cell 159:69-79. https://doi.org/10.1016/j.cell.2014.09.009.
15. 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.
16. McLellan JS, Pancera M, Carrico C, Gorman J, Julien J-P, 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 G-Y, Diwanji D, Georgiev I, Kwon YD, Lee D, Louder MK, Moquin S, Schmidt SD, Yang Z-Y, Bonsignori M, Crump JA, Kapiga SH, Sam NE, Haynes BF, Burton DR, Koff WC, Walker LM, Phogat S, Wyatt R, Orwenyo J, Wang L-X, 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.
17. Mouquet H, Scharf L, Euler Z, Liu Y, Eden C, Scheid JF, Halper-Stromberg A, Gnanapragasam PNP, Spencer DIR, Seaman MS, Schuitemaker H, Feizi T, Nussenzweig MC, Bjorkman PJ. 2012. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc Natl Acad Sci U S A 109:E3268-E3277. https://doi.org/10.1073/pnas.1217207109.
18. Pancera M, Shahzad-Ul-Hussan S, Doria-Rose NA, McLellan JS, Bailer RT, Dai K, Loesgen S, Louder MK, Staupe RP, Yang Y, Zhang B, Parks R, Eudailey J, Lloyd KE, Blinn J, Alam SM, Haynes BF, Amin MN, Wang L-X, Burton DR, Koff WC, Nabel GJ, Mascola JR, Bewley CA, Kwong PD. 2013. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat Struct Mol Biol 20:804-813. https://doi.org/10.1038/nsmb.2600.
19. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang P-S, Wang S-K, Stanfield RL, Julien J-P, 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 C-H, 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.
20. Scharf L, Scheid JF, Lee JH, West AP, Chen C, Gao H, Gnanapragasam PNP, Mares R, Seaman MS, Ward AB, Nussenzweig MC, Bjorkman PJ. 2014 Antibody 8ANC195 reveals a site of broad vulnerability on the HIV-1 envelope spike. Cell Rep 7:785-795. https://doi.org/10.1016/j.celrep.2014.04.001.
21. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien J-P, Wang S-K, Ramos A, Chan-Hui P-Y, Moyle M, Mitcham JL, Hammond PW, Olsen OA, Phung P, Fling S, Wong C-H, 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.
22. Huang J, Kang BH, Pancera M, Lee JH, Tong T, Feng Y, Georgiev IS, Chuang G-Y, Druz A, Doria-Rose NA, Laub L, Sliepen K, van Gils MJ, de la Peña AT, Derking R, Klasse P-J, 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.
23. Scanlan CN, Pantophlet R, Wormald MR, Ollmann Saphire E, Stanfield R, Wilson IA, Katinger H, Dwek RA, Rudd PM, Burton DR. 2002. 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. J Virol 76:7306-7321. https://doi.org/10.1128/JVI.76.14.7306-7321.2002.
24. Calarese DA, Scanlan CN, Zwick MB, Deechongkit S, Mimura Y, Kunert R, Zhu P, Wormald MR, Stanfield RL, Roux KH, Kelly JW, Rudd PM, Dwek RA, Katinger H, Burton DR, Wilson IA. 2003. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300:2065-2071. https://doi.org/10.1126/science.1083182.
25. Freund NT, Horwitz JA, Nogueira L, Sievers SA, Scharf L, Scheid JF, Gazumyan A, Liu C, Velinzon K, Goldenthal A, Sanders RW, Moore JP, Bjorkman PJ, Seaman MS, Walker BD, Klein F, Nussenzweig MC. 2015. A new glycan-dependent CD4-binding site neutralizing antibody exerts pressure on HIV-1 in vivo. PLoS Pathog 11:e1005238. https://doi.org/10.1371/journal.ppat.1005238.
26. Vollenweider F, Benjannet S, Decroly E, Savaria D, Lazure C, Thomas G, Chretien M, Seidah NG. 1996. Comparative cellular processing of the human immunodeficiency virus (HIV-1) envelope glycoprotein gp160 by the mammalian subtilisin/kexin-like convertases. Biochem J 314: 521-532. https://doi.org/10.1042/bj3140521.
27. Moulard M, Decroly E. 2000. Maturation of HIV envelope glycoprotein precursors by cellular endoproteases. Biochim Biophys Acta 1469: 121-132. https://doi.org/10.1016/S0304-4157(00)00014-9.
28. Decroly E, Wouters S, Di Bello C, Lazure C, Ruysschaert JM, Seidah NG. 1996 Identification of the paired basic convertases implicated in HIV gp160 processing based on in vitro assays and expression in CD4(+) cell lines. J Biol Chem 271:30442-30450. https://doi.org/10.1074/jbc.271.48.30442.
29. Decroly E, Vandenbranden M, Ruysschaert JM, Cogniaux J, Jacob GS, Howard SC, Marshall G, Kompelli A, Basak A, Jean F, Lazure C, Benjannet S, Chretien M, Day R, Seidah NG. 1994. The convertases furin and PC1 can both cleave the human immunodeficiency virus (HIV)-1 envelope glycoprotein gp160 into gp120 (HIV-I SU) and gp41 (HIV-I TM). J Biol Chem 269:12240-12247.
30. Franzusoff A, Volpe AM, Josse D, Pichuantes S, Wolf JR. 1995. Biochemical and genetic definition of the cellular protease required for HIV-1 gp160 processing. J Biol Chem 270:3154-3159. https://doi.org/10.1074/jbc.270.7.3154.
31. Hallenberger S, Bosch V, Angliker H, Shaw E, Klenk HD, Garten W. 1992. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360:358-361. https://doi.org/10.1038/360358a0.
32. Thomas G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat Rev Mol Cell Biol 3:753-766. https://doi.org/10.1038/nrm934.
33. Bass J, Turck C, Rouard M, Steiner DF. 2000. Furin-mediated processing in the early secretory pathway: sequential cleavage and degradation of misfolded insulin receptors. Proc Natl Acad Sci U S A 97:11905-11909. https://doi.org/10.1073/pnas.97.22.11905.
34. Binley JM, Sanders RW, Master A, Cayanan CS, Wiley CL, Schiffner L, Travis B, Kuhmann S, Burton DR, Hu SL, Olson WC, Moore JP. 2002. Enhancing the proteolytic maturation of human immunodeficiency virus type 1 envelope glycoproteins. J Virol 76:2606-2616. https://doi.org/10.1128/JVI.76.6.2606-2616.2002.
35. Sanders RW, Derking R, Cupo A, Julien JP, Yasmeen A, de Val N, Kim HJ, Blattner C, de la Pena 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.
36. Ringe RP, Sanders RW, Yasmeen A, Kim HJ, Lee JH, Cupo A, Korzun J, Derking R, van Montfort T, Julien J-P, 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.
37. Yasmeen A, Ringe R, Derking R, Cupo A, Julien JP, Burton DR, Ward AB, Wilson IA, Sanders RW, Moore JP, Klasse PJ. 2014. Differential binding of neutralizing and non-neutralizing antibodies to native-like soluble HIV-1 Env trimers, uncleaved Env proteins, and monomeric subunits. Retrovirology 11:41. https://doi.org/10.1186/1742-4690-11-41.
38. Georgiev IS, Joyce MG, Yang Y, Sastry M, Zhang B, Baxa U, Chen RE, Druz A, Lees CR, Narpala S, Schon A, Van Galen J, Chuang GY, Gorman J, Harned A, Pancera M, Stewart-Jones GB, Cheng C, Freire E, McDermott AB, Mascola JR, Kwong PD. 2015. Single-chain soluble BG505.SOSIP gp140 trimers as structural and antigenic mimics of mature closed HIV-1 Env. J Virol 89:5318-5329. https://doi.org/10.1128/JVI.03451-14.
39. 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.
40. 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.
41. 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.
42. Go EP, Liao H-X, 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.
43. 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.
44. Walker LM, Phogat SK, Chan-Hui P-Y, 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.
45. Pritchard LK, Spencer DI, Royle L, Vasiljevic S, Krumm SA, Doores KJ, Crispin M. 2015. Glycan microheterogeneity at the PGT135 antibody recognition site on HIV-1 gp120 reveals a molecular mechanism for neutralization resistance. J Virol 89:6952-6959. https://doi.org/10.1128/JVI.00230-15.
46. Doores KJ, Kong L, Krumm SA, Le KM, Sok D, Laserson U, Garces F, Poignard P, Wilson IA, Burton DR. 2015. Two classes of broadly neutralizing antibodies within a single lineage directed to the high-mannose patch of HIV envelope. J Virol 89:1105-1118. https://doi.org/10.1128/JVI.02905-14.
47. Doores KJ. 2015. The HIV glycan shield as a target for broadly neutralizing antibodies. FEBS J 282:4679-4691. https://doi.org/10.1111/febs.13530.
48. Alexandre KB, Gray ES, Lambson BE, Moore PL, Choge IA, Mlisana K, Karim SS, McMahon J, O'Keefe B, Chikwamba R, Morris L. 2010. Mannoserich glycosylation patterns on HIV-1 subtype C gp120 and sensitivity to the lectins, griffithsin, cyanovirin-N and scytovirin. Virology 402:187-196. https://doi.org/10.1016/j.virol.2010.03.021.
49. Coss KP, Vasiljevic S, Pritchard LK, Krumm SA, Glaze M, Madzorera S, Moore PL, Crispin M, Doores KJ. 5 October 2016. HIV-1 glycan density drives the persistence of the mannose patch within an infected individual. J Virol https://doi.org/10.1128/jvi.01542-16.
50. Behrens A-J, 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.
51. 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.
52. Crispin M, Doores KJ. 2015. Targeting host-derived glycans on enveloped viruses for antibody-based vaccine design. Curr Opin Virol 11: 63-69. https://doi.org/10.1016/j.coviro.2015.02.002.
53. Sanders RW, van Gils MJ, Derking R, Sok D, Ketas TJ, Burger JA, Ozorowski G, Cupo A, Simonich C, Goo L, Arendt H, Kim HJ, Lee JH, Pugach P, Williams M, Debnath G, Moldt B, van Breemen MJ, Isik G, Medina-Ramirez M, Back JW, Koff WC, Julien JP, Rakasz EG, Seaman MS, Guttman M, Lee KK, Klasse PJ, LaBranche C, Schief WR, Wilson IA, Overbaugh J, Burton DR, Ward AB, Montefiori DC, Dean H, Moore JP. 2015. HIV-1 vaccines. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 349:aac4223. https://doi.org/10.1126/science.aac4223.
54. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, Klasse PJ, Burton DR, Sanders RW, Moore JP, Ward AB, Wilson IA. 2013. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342: 1477-1483. https://doi.org/10.1126/science.1245625.
55. Lyumkis D, Julien JP, de Val N, Cupo A, Potter CS, Klasse PJ, Burton DR, Sanders RW, Moore JP, Carragher B, Wilson IA, Ward AB. 2013. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342:1484-1490. https://doi.org/10.1126/science.1245627.
56. Binley JM, Sanders RW, Clas B, Schuelke N, Master A, Guo Y, Kajumo F, Anselma DJ, Maddon PJ, Olson WC, Moore JP. 2000. A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J Virol 74:627-643. https://doi.org/10.1128/JVI.74.2.627-643.2000.
57. Khayat R, Lee JH, Julien J-P, Cupo A, Klasse PJ, Sanders RW, Moore JP, Wilson IA, Ward AB. 2013. Structural characterization of cleaved, soluble HIV-1 envelope glycoprotein trimers. J Virol 87:9865-9872. https://doi.org/10.1128/JVI.01222-13.
58. Klasse PJ, Depetris RS, Pejchal R, Julien J-P, Khayat R, Lee JH, Marozsan AJ, Cupo A, Cocco N, Korzun J, Yasmeen A, Ward AB, Wilson IA, Sanders RW, Moore JP. 2013. Influences on trimerization and aggregation of soluble, cleaved HIV-1 SOSIP envelope glycoprotein. J Virol 87: 9873-9885. https://doi.org/10.1128/JVI.01226-13.
59. Sanders RW, Vesanen M, Schuelke N, Master A, Schiffner L, Kalyanaraman R, Paluch M, Berkhout B, Maddon PJ, Olson WC, Lu M, Moore JP. 2002. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J Virol 76:8875-8889. https://doi.org/10.1128/JVI.76.17.8875-8889.2002.
60. Harvey DJ, Sobott F, Crispin M, Wrobel A, Bonomelli C, Vasiljevic S, Scanlan CN, Scarff CA, Thalassinos K, Scrivens JH. 2011. Ion mobility mass spectrometry for extracting spectra of N-glycans directly from incubation mixtures following glycan release: application to glycans from engineered glycoforms of intact, folded HIV gp120. J Am Soc Mass Spectrom 22:568-581. https://doi.org/10.1007/s13361-010-0053-0.
61. Lee JH, de Val N, Lyumkis D, Ward AB. 2015. Model building and refinement of a natively glycosylated HIV-1 Env protein by high-resolution cryoelectron microscopy. Structure 23:1943-1951. https://doi.org/10.1016/j.str.2015.07.020.
62. Mathys L, Francois KO, Quandte M, Braakman I, Balzarini J. 2014. Deletion of the highly conserved N-glycan at Asn260 of HIV-1 gp120 affects folding and lysosomal degradation of gp120, and results in loss of viral infectivity. PLoS One 9:e101181. https://doi.org/10.1371/journal.pone.0101181.
63. Moore JP, Willey RL, Lewis GK, Robinson J, Sodroski J. 1994. Immunological evidence for interactions between the first, second, and fifth conserved domains of the gp120 surface glycoprotein of human immunodeficiency virus type 1. J Virol 68:6836-6847.
64. 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.
65. 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.
66. Stansell E, Panico M, Canis K, Pang PC, Bouche 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.
67. Lee JH, Ozorowski G, Ward AB. 2016. Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science 351:1043-1048. https://doi.org/10.1126/science.aad2450.
68. Sliepen K, Sanders RW. 2016. HIV-1 envelope glycoprotein immunogens to induce broadly neutralizing antibodies. Expert Rev Vaccines 15: 349-365. https://doi.org/10.1586/14760584.2016.1129905.
69. de Taeye SW, Ozorowski G, Torrents de la Pena A, Guttman M, Julien JP, van den Kerkhof TL, Burger JA, Pritchard LK, Pugach P, Yasmeen A, Crampton J, Hu J, Bontjer I, Torres JL, Arendt H, DeStefano J, Koff WC, Schuitemaker H, Eggink D, Berkhout B, Dean H, LaBranche C, Crotty S, Crispin M, Montefiori DC, Klasse PJ, Lee KK, Moore JP, Wilson IA, Ward AB, Sanders RW. 2015. Immunogenicity of stabilized HIV-1 envelope trimers with reduced exposure of non-neutralizing epitopes. Cell 163: 1702-1715. https://doi.org/10.1016/j.cell.2015.11.056.
70. Sanders RW, Moore JP. Native-like Env trimers as a platform for HIV-1 vaccine design. Immunol Rev, in press.
71. Guttman M, Lee KK. 2013. A functional interaction between gp41 and gp120 is observed for monomeric but not oligomeric, uncleaved HIV-1 Env gp140. J Virol 87:11462-11475. https://doi.org/10.1128/JVI.01681-13.
72. Lynch RM, Wong P, Tran L, O'Dell S, Nason MC, Li Y, Wu X, Mascola JR. 2015 HIV-1 fitness cost associated with escape from the VRC01 class of CD4 binding site neutralizing antibodies. J Virol 89:4201-4213. https://doi.org/10.1128/JVI.03608-14.
73. Wibmer CK, Gorman J, Anthony CS, Mkhize NN, Druz A, York T, Schmidt SD, Labuschagne P, Louder MK, Bailer RT, Abdool Karim SS, Mascola JR, Williamson C, Moore PL, Kwong PD, Morris L. 2016. Structure of an N276-dependent HIV-1 neutralizing antibody targeting a rare V5 glycan hole adjacent to the CD4 binding site. J Virol 90:10220-10235. https://doi.org/10.1128/JVI.01357-16.
74. McGuire AT, Gray MD, Dosenovic P, Gitlin AD, Freund NT, Petersen J, Correnti C, Johnsen W, Kegel R, Stuart AB, Glenn J, Seaman MS, Schief WR, Strong RK, Nussenzweig MC, Stamatatos L. 2016. Specifically modified Env immunogens activate B-cell precursors of broadly neutralizing HIV-1 antibodies in transgenic mice. Nat Commun 7:10618. https://doi.org/10.1038/ncomms10618.
75. Jardine JG, Kulp DW, Havenar-Daughton C, Sarkar A, Briney B, Sok D, Sesterhenn F, Ereno-Orbea J, Kalyuzhniy O, Deresa I, Hu X, Spencer S, Jones M, Georgeson E, Adachi Y, Kubitz M, deCamp AC, Julien JP, Wilson IA, Burton DR, Crotty S, Schief WR. 2016. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science 351:1458-1463. https://doi.org/10.1126/science.aad9195.
76. Scharf L, West AP, Sievers SA, Chen C, Jiang S, Gao H, Gray MD, McGuire AT, Scheid JF, Nussenzweig MC, Stamatatos L, Bjorkman PJ. 2016. Structural basis for germline antibody recognition of HIV-1 immunogens. eLife 5:e13783. https://doi.org/10.7554/eLife.13783.
77. Julien J-P, Lee JH, Cupo A, Murin CD, Derking R, Hoffenberg S, Caulfield MJ, King CR, Marozsan AJ, Klasse PJ, Sanders RW, Moore JP, Wilson IA, Ward AB. 2013. Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc Natl Acad Sci U S A 110:4351-4356. https://doi.org/10.1073/pnas.1217537110.
78. Neville DC, Dwek RA, Butters TD. 2009. Development of a single column method for the separation of lipid-and protein-derived oligosaccharides. J Proteome Res 8:681-687. https://doi.org/10.1021/pr800704t.
79. Geiger T, Clarke S. 1987. Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J Biol Chem 262: 785-794.