Native conformation and canonical disulfide bond formation are interlinked properties of HIV-1 Env glycoproteins

Journal of Virology

Volumn 90, Issue 6, 2016, Pages 2884-2894

  Go, Eden P ^a   Cupo, Albert ^b   Ringe, Rajesh ^b   Pugach, Pavel ^b   Moore, John P ^b   Desaire, Heather ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN GP 140; DISULFIDE; RECOMBINANT PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; HUMAN IMMUNODEFICIENCY VIRUS 1; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; VIRION; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY;

ANIMALS; CHO CELLS; CRICETULUS; DISULFIDES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; MASS SPECTROMETRY; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

EID: 84961128015     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01953-15     Document Type: Article

References (48)

1. 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. http://dx.doi.org/10.1056/NEJMoa0908492.
2. Alam SM, Liao HX, Tomaras GD, Bonsignori M, Tsao CY, Hwang KK, Chen H, Lloyd KE, Bowman C, Sutherland L, Jeffries TL, Jr, Kozink DM, Stewart S, Anasti K, Jaeger FH, Parks R, Yates NL, Overman RG, Sinangil F, Berman PW, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Karasavva N, Rerks-Ngarm S, Kim JH, Michael NL, Zolla-Pazner S, Santra S, Letvin NL, Harrison SC, Haynes BF. 2013. Antigenicity and immunogenicity of RV144 vaccine AIDSVAX clade E envelope immunogen is enhanced by a gp120 N-terminal deletion. J Virol 87:1554-1568. http://dx.doi.org/10.1128/JVI.00718-12.
3. Du SX, Xu L, Zhang W, Tang S, Boenig RI, Chen H, Mariano EB, Zwick MB, Parren PW, Burton DR, Wrin T, Petropoulos CJ, Ballantyne JA, Chambers M, Whalen RG. 2011. A directed molecular evolution approach to improved immunogenicity of the HIV-1 envelope glycoprotein. PLoS One 6:e20927. http://dx.doi.org/10.1371/journal.pone.0020927.
4. Fouda GG, Amos JD, Wilks AB, Pollara J, Ray CA, Chand A, Kunz EL, Liebl BE, Whitaker K, Carville A, Smith S, Colvin L, Pickup DJ, Staats HF, Overman G, Eutsey-Lloyd K, Parks R, Chen H, Labranche C, Barnett S, Tomaras GD, Ferrari G, Montefiori DC, Liao HX, Letvin NL, Haynes BF, Permar SR. 2013. Mucosal immunization of lactating female rhesus monkeys with a transmitted/founder HIV-1 envelope induces strong Env-specific IgA antibody responses in breast milk. J Virol 87: 6986-6999. http://dx.doi.org/10.1128/JVI.00528-13.
5. Fouda GG, Cunningham CK, McFarland EJ, Borkowsky W, Muresan P, Pollara J, Song LY, Liebl BE, Whitaker K, Shen X, Vandergrift NA, Overman RG, Yates NL, Moody MA, Fry C, Kim JH, Michael NL, Robb M, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Liao HX, Haynes BF, Montefiori DC, Ferrari G, Tomaras GD, Permar SR. 2015. Infant HIV type 1 gp120 vaccination elicits robust and durable anti-V1V2 immunoglobulin G responses and only rare envelope-specific immunoglobulin A responses. J Infect Dis 211:508-517. http://dx.doi.org/10.1093/infdis/jiu444.
6. Kassa A, Dey AK, Sarkar P, Labranche C, Go EP, Clark DF, Sun Y, Nandi A, Hartog K, Desaire H, Montefiori D, Carfi A, Srivastava IK, Barnett SW. 2013. Stabilizing exposure of conserved epitopes by structure guided insertion of disulfide bond in HIV-1 envelope glycoprotein. PLoS One 8:e76139. http://dx.doi.org/10.1371/journal.pone.0076139.
7. Wen Y, Stephenson S, Zambonelli C, Hilt S, Wininger M, Dey A, Barnett S, Carfi A. 2012. Simple, scalable and robust purification of two HIV-1 subtype C gp120 monomer subunit antigens for phase II clinical trial in Republic of South Africa. Retrovirology 9(Suppl 2):P356. http://dx.doi.org/10.1186/1742-4690-9-S2-P356.
8. Mascola JR. 2015. HIV. The modern era of HIV-1 vaccine development. Science 349:139-140. http://dx.doi.org/10.1126/science.aac7800.
9. Mouquet H. 2015. Tailored immunogens for rationally designed antibody-based HIV-1 vaccines. Trends Immunol 36:437-439. http://dx.doi.org/10.1016/j.it.2015.07.001.
10. Ward AB, Wilson IA. 2015. Insights into the trimeric HIV-1 envelope glycoprotein structure. Trends Biochem Sci 40:101-107. http://dx.doi.org/10.1016/j.tibs.2014.12.006.
11. AlSalmi W, Mahalingam M, Ananthaswamy N, Hamlin C, Flores D, Gao G, Rao VB. 2015. A new approach to produce HIV-1 envelope trimers: both cleavage and proper glycosylation are essential to generate authentic trimers. J Biol Chem 290:19780-19795. http://dx.doi.org/10.1074/jbc.M115.656611.
12. Georgiev IS, Joyce MG, Yang Y, Sastry M, Zhang B, Baxa U, Chen RE, Druz A, Lees CR, Narpala S, Schön 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. http://dx.doi.org/10.1128/JVI.03451-14.
13. Guttman M, Lee KK. 2013.Afunctional interaction between gp41 and gp120 is observed for monomeric but not oligomeric, uncleaved HIV-1 Env gp140. J Virol 87:11462-11475. http://dx.doi.org/10.1128/JVI.01681-13.
14. 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. http://dx.doi.org/10.1016/j.celrep.2015.05.017.
15. 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. http://dx.doi.org/10.1128/JVI.01768-15.
16. 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. http://dx.doi.org/10.1073/pnas.1314351110.
17. 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. http://dx.doi.org/10.1371/journal.pone.0023521.
18. 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. http://dx.doi.org/10.1073/pnas.1006498107.
19. 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. http://dx.doi.org/10.1128/JVI.00628-15.
20. 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. http://dx.doi.org/10.1038/ncomms8479.
21. Pritchard LK, Harvey DJ, Bonomelli C, Crispin M, Doores KJ. 2015. Cell-and protein-directed glycosylation of native cleaved HIV-1 envelope. J Virol 89:8932-8944. http://dx.doi.org/10.1128/JVI.01190-15.
22. Gallaher WR, Ball JM, Garry RF, Griffin MC, Montelaro RC. 1989. A general-model for the transmembrane proteins of HIV and other retroviruses. AIDS Res Hum Retroviruses 5:431-440. http://dx.doi.org/10.1089/aid.1989.5.431.
23. Go EP, Zhang Y, Menon S, Desaire H. 2011. Analysis of the disulfide bond arrangement of the HIV-1 envelope protein CON-S gp140 ΔCFI shows variability in the V1 and V2 regions. J Proteome Res 10:578-591. http://dx.doi.org/10.1021/pr100764a.
24. 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. http://dx.doi.org/10.1021/pr5003643.
25. 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.
26. Peisajovich SG, Blank L, Epand RF, Epand RM, Shai Y. 2003. On the interaction between gp41 and membranes: the immunodominant loop stabilizes gp41 helical hairpin conformation. J Mol Biol 326:1489-1501. http://dx.doi.org/10.1016/S0022-2836(03)00040-8.
27. Kwon YD, Pancera M, Acharya P, Georgiev IS, Crooks ET, Gorman J, Joyce MG, Guttman M, Ma X, Narpala S, Soto C, Terry DS, Yang Y, Zhou T, Ahlsen G, Bailer RT, Chambers M, Chuang GY, Doria-Rose NA, Druz A, Hallen MA, Harned A, Kirys T, Louder MK, O'Dell S, Ofek G, Osawa K, Prabhakaran M, Sastry M, Stewart-Jones GB, Stuckey J, Thomas PV, Tittley T, Williams C, Zhang B, Zhao H, Zhou Z, Donald BR, Lee LK, Zolla-Pazner S, Baxa U, Schön A, Freire E, Shapiro L, Lee KK, Arthos J, Munro JB, Blanchard SC, Mothes W, Binley JM, Mc Dermott AB, Mascola JR, Kwong PD. 2015. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat Struct Mol Biol 22:522-531. http://dx.doi.org/10.1038/nsmb.3051.
28. 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. http://dx.doi.org/10.1126/science.1245625.
29. 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. http://dx.doi.org/10.1126/science.1245627.
30. Pancera M, Zhou T, Druz A, Georgiev IS, Soto C, Gorman J, Huang J, Acharya P, Chuang GY, Ofek G, Stewart-Jones GB, Stuckey J, Bailer RT, Joyce MG, Louder MK, Tumba N, Yang Y, Zhang B, Cohen MS, Haynes BF, Mascola JR, Morris L, Munro JB, Blanchard SC, Mothes W, Connors M, Kwong PD. 2014. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514:455-461. http://dx.doi.org/10.1038/nature13808.
31. Finzi A, Pacheco B, Zeng X, Kwon YD, Kwong PD, Sodroski J. 2010. Conformational characterization of aberrant disulfide-linked HIV-1 gp120 dimers secreted from overexpressing cells. J Virol Methods 168: 155-161. http://dx.doi.org/10.1016/j.jviromet.2010.05.008.
32. Owens RJ, Compans RW. 1990. The human immunodeficiency virus type 1 envelope glycoprotein precursor acquires aberrant intermolecular disulfide bonds that may prevent normal proteolytic processing. Virology 179:827-833. http://dx.doi.org/10.1016/0042-6822(90)90151-G.
33. Clark DF, Go EP, Desaire H. 2013. Simple approach to assign disulfide connectivity using extracted ion chromatograms of electron transfer dissociation spectra. Anal Chem 85:1192-1199. http://dx.doi.org/10.1021/ac303124w.
34. 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. http://dx.doi.org/10.1371/journal.ppat.1003618.
35. Chung NP, Matthews K, Kim HJ, Ketas TJ, Golabek M, de Los Reyes K, Korzun J, Yasmeen A, Sanders RW, Klasse PJ, Wilson IA, Ward AB, Marozsan AJ, Moore JP, Cupo A. 2014. Stable 293 T and CHO cell lines expressing cleaved, stable HIV-1 envelope glycoprotein trimers for structural and vaccine studies. Retrovirology 11:33. http://dx.doi.org/10.1186/1742-4690-11-33.
36. 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. http://dx.doi.org/10.1186/1742-4690-11-41.
37. Kitamura R, Matsuoka K, Matsushima E, Kawaguchi Y. 2001. Improvement in precision of the liquid chromatographic-electrospray ionization tandem mass spectrometric analysis of 3=-C-ethynylcytidine in rat plasma. J Chromatogr B Biomed Sci Appl 754:113-119. http://dx.doi.org/10.1016/S0378-4347(00)00588-0.
38. Shi G. 2003. Application of co-eluting structural analog internal standards for expanded linear dynamic range in liquid chromatography/electrospray mass spectrometry. Rapid Commun Mass Spectrom 17:202-206. http://dx.doi.org/10.1002/rcm.897.
39. Xu RN, Fan L, Rieser MJ, El-Shourbagy TA. 2007. Recent advances in high-throughput quantitative bioanalysis by LC-MS/MS. J Pharm Biomed Anal 44:342-355. http://dx.doi.org/10.1016/j.jpba.2007.02.006.
40. 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 neutralizing antibodies induced by native-like envelope trimers. Science 349:aac4223. http://dx.doi.org/10.1126/science.aac4223.
41. Tong T, Crooks ET, Osawa K, Binley JM. 2012. HIV-1 virus-like particles bearing pure Env trimers expose neutralizing epitopes but occlude nonneutralizing epitopes. J Virol 86:3574-3587. http://dx.doi.org/10.1128/JVI.06938-11.
42. Pancera M, Wyatt R. 2005. Selective recognition of oligomeric HIV-1 primary isolate envelope glycoproteins by potently neutralizing ligands requires efficient precursor cleavage. Virology 332:145-156. http://dx.doi.org/10.1016/j.virol.2004.10.042.
43. Herrera C, Spenlehauer C, Fung MS, Burton DR, Beddows S, Moore JP. 2003. Nonneutralizing antibodies to the CD4-binding site on the gp120 subunit of human immunodeficiency virus type 1 do not interfere with the activity of a neutralizing antibody against the same site. J Virol 77:1084-1091. http://dx.doi.org/10.1128/JVI.77.2.1084-1091.2003.
44. Crooks ET, Tong T, Osawa K, Binley JM. 2011. Enzyme digests eliminate nonfunctional Env from HIV-1 particle surfaces, leaving native Env trimers intact and viral infectivity unaffected. J Virol 85:5825-5839. http://dx.doi.org/10.1128/JVI.00154-11.
45. Blattner C, Lee JH, Sliepen K, Derking R, Falkowska E, de la Peña 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. http://dx.doi.org/10.1016/j.immuni.2014.04.008.
46. Pugach P, Ozorowski G, Cupo A, Ringe R, Yasmeen A, de Val N, Derking R, Kim HJ, Korzun J, Golabek M, de Los Reyes K, Ketas TJ, Julien JP, Burton DR, Wilson IA, Sanders RW, Klasse PJ, Ward AB, Moore JP. 2015. A native-like SOSIP.664 trimer based on an HIV-1 subtype B env gene. J Virol 89:3380-3395. http://dx.doi.org/10.1128/JVI.03473-14.
47. Julien JP, Lee JH, Ozorowski G, Hua Y, Torrents de la Peña A, de Taeye SW, Nieusma T, Cupo A, Yasmeen A, Golabek M, Pugach P, Klasse PJ, Moore JP, Sanders RW, Ward AB, Wilson IA. 2015. Design and structure of two HIV-1 clade C SOSIP.664 trimers that increase the arsenal of native-like Env immunogens. Proc Natl Acad Sci U S A 112:11947-11952. http://dx.doi.org/10.1073/pnas.1507793112.
48. Guenaga J, de Val N, Tran K, Feng Y, Satchwell K, Ward AB, Wyatt RT. 2015. Well-ordered trimeric HIV-1 subtype B and C soluble spike mimetics generated by negative selection display native-like properties. PLoS Pathog 11:e1004570. http://dx.doi.org/10.1371/journal.ppat.1004570.