Influences on Trimerization and Aggregation of Soluble, Cleaved HIV-1 SOSIP Envelope Glycoprotein

Journal of Virology

Volumn 87, Issue 17, 2013, Pages 9873-9885

  Klasse, Per Johan ^a   Depetris, Rafael S ^a   Pejchal, Robert ^b   Julien, Jean Philippe ^b   Khayat, Reza ^b,c   Lee, Jeong Hyun ^b   Marozsan, Andre J ^a   Cupo, Albert ^a   Cocco, Nicolette ^a   Korzun, Jacob ^a   Yasmeen, Anila ^a   Ward, Andrew B ^b   Wilson, Ian A ^b   Sanders, Rogier W ^a,b   Moore, John P ^a,d  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c CITY COLLEGE OF NEW YORK   (United States)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; DETERGENT; ENVELOPE PROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; MEMBRANE PROTEIN; PROTEIN SOSIP; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANTIBODY COMBINING SITE; ANTIGENICITY; ARTICLE; BINDING KINETICS; GENOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMOBILIZATION; MEMBRANE PROXIMAL EXTERNAL REGION; MEMBRANE STRUCTURE; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN PROCESSING; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD4; BINDING SITES; DETERGENTS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HEK293 CELLS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS; SEQUENCE DELETION; SOLUBILITY;

EID: 84883308389     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01226-13     Document Type: Article

References (71)

1. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, Godzik A, Kaufmann DE, McElrath MJ, Nussenzweig MC, Pulendran B, Scanlan CN, Schief WR, Silvestri G, Streeck H, Walker BD, Walker LM, Ward AB, Wilson IA, Wyatt R. 2012. A blueprint for HIV vaccine discovery. Cell Host Microbe 12:396-407.
2. Burton DR, Desrosiers RC, Doms RW, Koff WC, Kwong PD, Moore JP, Nabel GJ, Sodroski J, Wilson IA, Wyatt RT. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5:233-236.
3. Klasse PJ, Sanders RW, Cerutti A, Moore JP. 2012. How can HIV-type- 1-Env immunogenicity be improved to facilitate antibody-based vaccine development? AIDS Res. Hum. Retroviruses 28:1-15.
4. Moore, JP. 2012. HIV-1 Env antibodies: are we in a bind or going blind? Nat. Med. 18:346-348.
5. Harris A, Borgnia MJ, Shi D, Bartesaghi A, He H, Pejchal R, Kang YK, Depetris R, Marozsan AJ, Sanders RW, Klasse PJ, Milne JL, Wilson IA, Olson WC, Moore JP, Subramaniam S. 2011. Trimeric HIV-1 glycoprotein gp140 immunogens and native HIV-1 envelope glycoproteins display the same closed and open quaternary molecular architectures. Proc. Natl. Acad. Sci. U. S. A. 108:11440-11445.
6. Hu G, Liu J, Taylor KA, Roux KH. 2011. Structural comparison of HIV-1 envelope spikes with and without the V1/V2 loop. J. Virol. 85: 2741-2750.
7. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S. 2008. Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109- 113.
8. Tran EE, Borgnia MJ, Kuybeda O, Schauder DM, Bartesaghi A, Frank GA, Sapiro G, Milne JL, Subramaniam S. 2012. Structural mechanism of trimeric HIV-1 envelope glycoprotein activation. PLoS Pathog. 8:e1002797. doi:10.1371/journal.ppat.1002797.
9. Layne SP, Merges MJ, Dembo M, Spouge JL, Conley SR, Moore JP, Raina JL, Renz H, Gelderblom HR, Nara PL. 1992. Factors underlying spontaneous inactivation and susceptibility to neutralization of human immunodeficiency virus. Virology 189:695-714.
10. McKeating JA, McKnight A, Moore JP. 1991. Differential loss of envelope glycoprotein gp120 from virions of human immunodeficiency virus type 1 isolates: effects on infectivity and neutralization. J. Virol. 65:852- 860.
11. Ruprecht CR, Krarup A, Reynell L, Mann AM, Brandenberg OF, Berlinger L, Abela IA, Regoes RR, Gunthard HF, Rusert P, Trkola A. 2011. MPER-specific antibodies induce gp120 shedding and irreversibly neutralize HIV-1. J. Exp. Med. 208:439-454.
12. Yang X, Wyatt R, Sodroski J. 2001. Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J. Virol. 75:1165-1171.
13. Sundling C, Forsell MN, O'Dell S, Feng Y, Chakrabarti B, Rao SS, Lore K, Mascola JR, Wyatt RT, Douagi I, Karlsson Hedestam GB. 2010. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J. Exp. Med. 207:2003-2017.
14. Gao F, Weaver EA, Lu Z, Li Y, Liao HX, Ma B, Alam SM, Scearce RM, Sutherland LL, Yu JS, Decker JM, Shaw GM, Montefiori DC, Korber BT, Hahn BH, Haynes BF. 2005. Antigenicity and immunogenicity of a synthetic human immunodeficiency virus type 1 group M consensus envelope glycoprotein. J. Virol. 79:1154-1163.
15. Earl PL, Broder CC, Long D, Lee SA, Peterson J, Chakrabarti S, Doms RW, Moss B. 1994. Native oligomeric human immunodeficiency virus type 1 envelope glycoprotein elicits diverse monoclonal antibody reactivities. J. Virol. 68:3015-3026.
16. Center RJ, Earl PL, Lebowitz J, Schuck P, Moss B. 2000. The human immunodeficiency virus type 1 gp120 V2 domain mediates gp41- independent intersubunit contacts. J. Virol. 74:4448-4455.
17. 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.
18. Beddows S, Franti M, Dey AK, Kirschner M, Iyer SPN, Fisch DC, Ketas T, Yuste E, Desrosiers RC, Klasse PJ, Maddon PJ, Olson WC, Moore JP. 2007. A comparative immunogenicity study in rabbits of disulfidestabilized, proteolytically cleaved, soluble trimeric human immunodeficiency virus type 1 gp140, trimeric cleavage-defective gp140 and monomeric gp120. Virology 360:329-340.
19. Yang X, Lee J, Mahony EM, Kwong PD, Wyatt R, Sodroski J. 2002. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76:4634-4642.
20. Srivastava IK, VanDorsten K, Vojtech L, Barnett SW, Stamatatos L. 2003. Changes in the immunogenic properties of soluble gp140 human immunodeficiency virus envelope constructs upon partial deletion of the second hypervariable region. J. Virol. 77:2310-2320.
21. Nkolola JP, Peng H, Settembre EC, Freeman M, Grandpre LE, Devoy C, Lynch DM, La Porte A, Simmons NL, Bradley R, Montefiori DC, Seaman MS, Chen B, Barouch DH. 2010. Breadth of neutralizing antibodies elicited by stable, homogeneous clade A and clade C HIV-1 gp140 envelope trimers in guinea pigs. J. Virol. 84:3270-3279.
22. Earl PL, Sugiura W, Montefiori DC, Broder CC, Lee SA, Wild C, Lifson J, Moss B. 2001. Immunogenicity and protective efficacy of oligomeric human immunodeficiency virus type 1 gp140. J. Virol. 75:645-653.
23. 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.
24. Sanders RW, Dankers MM, Busser E, Caffrey M, Moore JP, Berkhout B. 2004. Evolution of the HIV-1 envelope glycoproteins with a disulfide bond between gp120 and gp41. Retrovirology 1:3. doi:10.1186/1742-4690 -1-3.
25. Sanders RW, Busser E, Moore JP, Lu M, Berkhout B. 2004. Evolutionary repair of HIV type 1 gp41 with a kink in the N-terminal helix leads to restoration of the six-helix bundle structure. AIDS Res. Hum. Retroviruses 20:742-749.
26. Binley JM, Cayanan CS, Wiley C, Schulke N, Olson WC, Burton DR. 2003. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions. J. Virol. 77:5678-5684.
27. Abrahamyan LG, Markosyan RM, Moore JP, Cohen FS, Melikyan GB. 2003. Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion. J. Virol. 77:5829-5836.
28. 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.
29. Khayat R, Lee JH, Julien JP, 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.
30. Julien JP, Sok D, Khayat R, Lee JH, Doores KJ, Walker LM, Ramos A, Diwanji DC, Pejchal R, Cupo A, Katpally U, Depetris RS, Stanfield RL, McBride R, Marozsan AJ, Paulson JC, Sanders RW, Moore JP, Burton DR, Poignard P, Ward AB, Wilson IA. 2013. Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans. PLoS Pathog. 9:e1003342. doi:10.1371/journal.ppat.1003342.
31. Julien JP, 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.
32. Depetris RS, Julien JP, Khayat R, Lee JH, Pejchal R, Katpally U, Cocco N, Kachare M, Massi E, David KB, Cupo A, Marozsan AJ, Olson WC, Ward AB, Wilson IA, Sanders RW, Moore JP. 2012. Partial enzymatic deglycosylation preserves the structure of cleaved recombinant HIV-1 envelope glycoprotein trimers. J. Biol. Chem. 287:24239-24254.
33. Beddows S, Kirschner M, Campbell-Gardener L, Franti M, Dey AK, Iyer SPN, Maddon PJ, Paluch M, Master A, Overbaugh J, VanCott T, Olson WC, Moore JP. 2006. Construction and characterization of soluble, cleaved, and stabilized trimeric Env proteins based on HIV type 1 Env subtype A. AIDS Res. Hum. Retroviruses 22:569-579.
34. Bontjer I, Melchers M, Eggink D, David K, Moore JP, Berkhout B, Sanders RW. 2010. Stabilized HIV-1 envelope glycoprotein trimers lacking the V1V2 domain, obtained by virus evolution. J. Biol. Chem. 285: 36456-36470.
35. Bontjer I, Land A, Eggink D, Verkade E, Tuin K, Baldwin C, Pollakis G, Paxton WA, Braakman I, Berkhout B, Sanders RW. 2009. Optimization of human immunodeficiency virus type 1 envelope glycoproteins with V1/V2 deleted, using virus evolution. J. Virol. 83:368-383.
36. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, Finzi A, Kwon YD, Scheid JF, Shi W, Xu L, Yang Y, Zhu J, Nussenzweig MC, Sodroski J, Shapiro L, Nabel GJ, Mascola JR, Kwong PD. 2010. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329:811-817.
37. 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.
38. Allaway GP, Davis-Bruno KL, Beaudry GA, Garcia EB, Wong EL, Ryder AM, Hasel KW, Gauduin MC, Koup RA, McDougal JS, Maddon PJ. 1995. Expression and characterization of CD4-IgG(2), a novel heterotetramer that neutralizes primary HIV type-1 isolates. AIDS Res. Hum. Retroviruses 11:533-539.
39. Kirschner M, Monrose V, Paluch M, Techodamrongsin N, Rethwilm A, Moore JP. 2006. The production of cleaved, trimeric human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein vaccine antigens and infectious pseudoviruses using linear polyethylenimine as a transfection reagent. Protein Expr. Purif. 48:61-68.
40. Iyer SPN, Franti M, Krauchuk AA, Fisch DN, Ouattara AA, Roux KH, Krawiec L, Dey AK, Beddows S, Maddon PJ, Moore JP, Olson WC. 2007. Purified, proteolytically mature HIV type 1 SOSIP gp140 envelope trimers. AIDS Res. Hum. Retroviruses 23:817-828.
41. Schagger H, von Jagow G. 1991. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199:223-231.
42. Suloway C, Pulokas J, Fellmann D, Cheng A, Guerra F, Quispe J, Stagg S, Potter CS, Carragher B. 2005. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151:41-60.
43. Voss NR, Yoshioka CK, Radermacher M, Potter CS, Carragher B. 2009. DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166:205-213.
44. Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142:334-347.
45. Hohn M, Tang G, Goodyear G, Baldwin PR, Huang Z, Penczek PA, Yang C, Glaeser RM, Adams PD, Ludtke SJ. 2007. SPARX, a new environment for cryo-EM image processing. J. Struct. Biol. 157:47-55.
46. 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.
47. Sanders RW, Schiffner L, Master A, Kajumo F, Guo Y, Dragic T, Moore JP, Binley JM. 2000. Variable-loop-deleted variants of the human immunodeficiency virus type 1 envelope glycoprotein can be stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits. J. Virol. 74:5091-5100.
48. Pejchal R, Gach JS, Brunel FM, Cardoso RM, Stanfield RL, Dawson PE, Burton DR, Zwick MB, Wilson IA. 2009. A conformational switch in human immunodeficiency virus gp41 revealed by the structures of overlapping epitopes recognized by neutralizing antibodies. J. Virol. 83:8451- 8462.
49. Kim M, Sun ZY, Rand KD, Shi X, Song L, Cheng Y, Fahmy AF, Majumdar S, Ofek G, Yang Y, Kwong PD, Wang JH, Engen JR, Wagner G, Reinherz EL. 2011. Antibody mechanics on a membrane-bound HIV segment essential for GP41-targeted viral neutralization. Nat. Struct. Mol. Biol. 18:1235-1243.
50. Alam SM, Morelli M, Dennison SM, Liao HX, Zhang R, Xia SM, Rits-Volloch S, Sun L, Harrison SC, Haynes BF, Chen B. 2009. Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 106:20234-20239.
51. Sun ZY, Oh KJ, Kim M, Yu J, Brusic V, Song L, Qiao Z, Wang JH, Wagner G, Reinherz EL. 2008. HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28:52-63.
52. Montero M, Gulzar N, Klaric KA, Donald JE, Lepik C, Wu S, Tsai S, Julien JP, Hessell AJ, Wang S, Lu S, Burton DR, Pai EF, Degrado WF, Scott JK. 2012. Neutralizing epitopes in the membrane-proximal external region of HIV-1 gp41 are influenced by the transmembrane domain and the plasma membrane. J. Virol. 86:2930-2941.
53. Song L, Sun ZY, Coleman KE, Zwick MB, Gach JS, Wang JH, Reinherz EL, Wagner G, Kim M. 2009. Broadly neutralizing anti-HIV-1 antibodies disrupt a hinge-related function of gp41 at the membrane interface. Proc. Natl. Acad. Sci. U. S. A. 106:9057-9062.
54. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, Alam SM, Wang T, Yang Y, Zhang B, Migueles SA, Wyatt R, Haynes BF, Kwong PD, Mascola JR, Connors M. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491:406-412.
55. Dey AK, David KB, Ray N, Ketas TJ, Klasse PJ, Doms RW, Moore JP. 2008. N-terminal substitutions in HIV-1 gp41 reduce the expression of non-trimeric envelope glycoproteins on the virus. Virology 372:187-200.
56. Dey AK, David KB, Klasse PJ, Moore JP. 2007. Specific amino acids in the N-terminus of the gp41 ectodomain contribute to the stabilization of a soluble, cleaved gp140 envelope glycoprotein from human immunodeficiency virus type 1. Virology 360:199-208.
57. Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, Pietzsch J, Ott RG, Anthony RM, Zebroski H, Hurley A, Phogat A, Chakrabarti B, Li Y, Connors M, Pereyra F, Walker BD, Wardemann H, Ho D, Wyatt RT, Mascola JR, Ravetch JV, Nussenzweig MC. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIVinfected individuals. Nature 458:636-640.
58. Falkowska E, Ramos A, Feng Y, Zhou T, Moquin S, Walker LM, Wu X, Seaman MS, Wrin T, Kwong PD, Wyatt RT, Mascola JR, Poignard P, Burton DR. 2012. PGV04, an HIV-1 gp120 CD4 binding site antibody, is broad and potent in neutralization but does not induce conformational changes characteristic of CD4. J. Virol. 86:4394-4403.
59. 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.
60. Kong LK, Lee JH, Doores KJ, Murin CD, Julien JP, McBride R, Liu Y, Marozsan A, Cupo A, Klasse PJ, Hoffenberg S, Caulfield MJ, King CR, Hua Y, Khoa ML, Khayat R, Deller MC, Clayton T, Tien H, Feizi T, Sanders RW, Paulson JP, Moore JP, Stanfield RL, Burton DR, Ward AB, Wilson IA. 26 May 2013. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat. Struct. Mol. Biol. [E-pub ahead of print.] doi:10.1038/nsmb.2594.
61. Ringe R, Bhattacharya J. 2012. Association of enhanced HIV-1 neutralization by a single Y681H substitution in gp41 with increased gp120-CD4 interaction and macrophage infectivity. PLoS One 7:e37157.
62. Liu L, Cimbro R, Lusso P, Berger EA. 2011. Intraprotomer masking of third variable loop (V3) epitopes by the first and second variable loops (V1V2) within the native HIV-1 envelope glycoprotein trimer. Proc. Natl. Acad. Sci. U. S. A. 108:20148-20153.
63. Lovelace E, Xu H, Blish CA, Strong R, Overbaugh J. 2011. The role of amino acid changes in the human immunodeficiency virus type 1 transmembrane domain in antibody binding and neutralization. Virology 421: 235-244.
64. Klasse PJ, McKeating JA, Schutten M, Reitz MS, Jr, Robert-Guroff M. 1993. An immune-selected point mutation in the transmembrane protein of human immunodeficiency virus type 1 (HXB2-Env:Ala 582(Thr)) decreases viral neutralization by monoclonal antibodies to the CD4- binding site. Virology 196:332-337.
65. Blish CA, Nguyen MA, Overbaugh J. 2008. Enhancing exposure of HIV-1 neutralization epitopes through mutations in gp41. PLoS Med. 5:e9. doi:10.1371/journal.pmed.0050009.
66. Back NK, Smit L, Schutten M, Nara PL, Tersmette M, Goudsmit J. 1993. Mutations in human immunodeficiency virus type 1 gp41 affect sensitivity to neutralization by gp120 antibodies. J. Virol. 67:6897-6902.
67. Thali M, Charles M, Furman C, Cavacini L, Posner M, Robinson J, Sodroski J. 1994. Resistance to neutralization by broadly reactive antibodies to the human immunodeficiency virus type 1 gp120 glycoprotein conferred by a gp41 amino acid change. J. Virol. 68:674-680.
68. Hinz A, Schoehn G, Quendler H, Hulsik DL, Stiegler G, Katinger H, Seaman MS, Montefiori D, Weissenhorn W. 2009. Characterization of a trimeric MPER containing HIV-1 gp41 antigen. Virology 390:221-227.
69. Ofek G, Tang M, Sambor A, Katinger H, Mascola JR, Wyatt R, Kwong PD. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737.
70. Muster T, Guinea R, Trkola A, Purtscher M, Klima A, Steindl F, Palese P, Katinger H. 1994. Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. J. Virol. 68:4031-4034.
71. Mische CC, Yuan W, Strack B, Craig S, Farzan M, Sodroski J. 2005. An alternative conformation of the gp41 heptad repeat 1 region coiled coil exists in the human immunodeficiency virus (HIV-1) envelope glycoprotein precursor. Virology 338:133-143.