Tyrosine-sulfated V2 peptides inhibit HIV-1 infection via coreceptor mimicry

EBioMedicine

Volumn 10, Issue , 2016, Pages 45-54

  Cimbro, Raffaello ^a   Peterson, Francis C ^b   Liu, Qingbo ^a   Guzzo, Christina ^a   Zhang, Peng ^a   Miao, Huiyi ^a   Van Ryk, Donald ^a   Ambroggio, Xavier ^a   Hurt, Darrell E ^a   De Gioia, Luca ^c   Volkman, Brian F ^b   Dolan, Michael A ^a   Lusso, Paolo ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Coreceptors; Envelope; HIV 1; Immune evasion; Inhibitors; Molecular mimicry; Peptides; Trimer

Indexed keywords

GLYCOPROTEIN GP 120; PEPTIDE; TYROSINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; PEPTIDE FRAGMENT; PROTEIN BINDING; TYROSINE O-SULFATE;

ARTICLE; CD4+ T LYMPHOCYTE; CELL VIABILITY ASSAY; CIRCULAR DICHROISM; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIZE EXCLUSION CHROMATOGRAPHY; SPECTROPHOTOMETRY; VIRUS INFECTION; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMISTRY; DRUG EFFECTS; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MOLECULAR DOCKING; MOLECULAR MIMICRY; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; PROTEIN CONFORMATION; VIROLOGY;

AMINO ACID SEQUENCE; ANTI-HIV AGENTS; ANTIGENS, CD4; BINDING SITES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR MIMICRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, CCR5; TYROSINE;

EID: 85028268790     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.06.037     Document Type: Article

References (49)

1. Alsahafi, N., Debbeche, O., Sodroski, J., Finzi, A., Effects of the I559P gp41 change on the conformation and function of the human immunodeficiency virus (HIV-1) membrane envelope glycoprotein trimer. PLoS One, 10, 2015, e0122111.
2. Auerbach, D.J., Lin, Y., Miao, H., Cimbro, R., DiFiore, M.J., Gianolini, M.E., Furci, L., Biswas, P., Fauci, A.S., Lusso, P., Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 9569–9574.
3. Bartesaghi, A., Merk, A., Borgnia, M.J., Milne, J.L., Subramaniam, S., Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat. Struct. Mol. Biol. 20 (2013), 1352–1357.
4. Burton, D.R., Ahmed, R., Barouch, D.H., Butera, S.T., Crotty, S., Godzik, A., Kaufmann, D.E., McElrath, M.J., Nussenzweig, M.C., Pulendran, B., Scanlan, C.N., Schief, W.R., Silvestri, G., Streeck, H., Walker, B.D., Walker, L.M., Ward, A.B., Wilson, I.A., Wyatt, R., A blueprint for HIV vaccine discovery. Cell Host Microbe 12 (2012), 396–407.
5. Cao, J., Sullivan, N., Desjardin, E., Parolin, C., Robinson, J., Wyatt, R., Sodroski, J., Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J. Virol. 71 (1997), 9808–9812.
6. Chen, L., Kwon, Y.D., Zhou, T., Wu, X., O'Dell, S., Cavacini, L., Hessell, A.J., Pancera, M., Tang, M., Xu, L., Yang, Z.Y., Zhang, M.Y., Arthos, J., Burton, D.R., Dimitrov, D.S., Nabel, G.J., Posner, M.R., Sodroski, J., Wyatt, R., Mascola, J.R., Kwong, P.D., Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326 (2009), 1123–1127.
7. Choe, H., Li, W., Wright, P.L., Vasilieva, N., Venturi, M., Huang, C.C., Grundner, C., Dorfman, T., Zwick, M.B., Wang, L., Rosenberg, E.S., Kwong, P.D., Burton, D.R., Robinson, J.E., Sodroski, J.G., Farzan, M., Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell 114 (2003), 161–170.
8. Cimbro, R., Gallant, T.R., Dolan, M.A., Guzzo, C., Zhang, P., Lin, Y., Miao, H., Van Ryk, D., Arthos, J., Gorshkova, I., Brown, P.H., Hurt, D.E., Lusso, P., Tyrosine sulfation in the second variable loop (V2) of HIV-1 gp120 stabilizes V2–V3 interaction and modulates neutralization sensitivity. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 3152–3157.
9. Cormier, E.G., Persuh, M., Thompson, D.A., Lin, S.W., Sakmar, T.P., Olson, W.C., Dragic, T., Specific interaction of CCR5 amino-terminal domain peptides containing sulfotyrosines with HIV-1 envelope glycoprotein gp120. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 5762–5767.
10. Cormier, E.G., Tran, D.N., Yukhayeva, L., Olson, W.C., Dragic, T., Mapping the determinants of the CCR5 aminoterminal sulfopeptide interaction with soluble human immunodeficiency virus type 1 gp120-CD4 complexes. J. Virol. 75 (2001), 5541–5549.
11. Farzan, M., Mirzabekov, T., Kolchinsky, P., Wyatt, R., Cayabyab, M., Gerard, N.P., Gerard, C., Sodroski, J., Choe, H., Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96 (1999), 667–676.
12. Farzan, M., Vasilieva, N., Schnitzler, C.E., Chung, S., Robinson, J., Gerard, N.P., Gerard, C., Choe, H., Sodroski, J., A tyrosine-sulfated peptide based on the N terminus of CCR5 interacts with a CD4-enhanced epitope of the HIV-1 gp120 envelope glycoprotein and inhibits HIV-1 entry. J. Biol. Chem. 275 (2000), 33516–33521.
13. Garces, F., Lee, J.H., de Val, N., de la Pena, A.T., Kong, L., Puchades, C., Hua, Y., Stanfield, R.L., Burton, D.R., Moore, J.P., Sanders, R.W., Ward, A.B., Wilson, I.A., Affinity maturation of a potent family of HIV antibodies is primarily focused on accommodating or avoiding glycans. Immunity 43 (2015), 1053–1063.
14. Gardner, M.R., Kattenhorn, L.M., Kondur, H.R., von Schaewen, M., Dorfman, T., Chiang, J.J., Haworth, K.G., Decker, J.M., Alpert, M.D., Bailey, C.C., Neale, E.S. Jr., Fellinger, C.H., Joshi, V.R., Fuchs, S.P., Martinez-Navio, J.M., Quinlan, B.D., Yao, A.Y., Mouquet, H., Gorman, J., Zhang, B., Poignard, P., Nussenzweig, M.C., Burton, D.R., Kwong, P.D., Piatak, M. Jr., Lifson, J.D., Gao, G., Desrosiers, R.C., Evans, D.T., Hahn, B.H., Ploss, A., Cannon, P.M., Seaman, M.S., Farzan, M., AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges. Nature 519 (2015), 87–91.
15. Gorny, M.K., Stamatatos, L., Volsky, B., Revesz, K., Williams, C., Wang, X.H., Cohen, S., Staudinger, R., Zolla-Pazner, S., Identification of a new quaternary neutralizing epitope on human immunodeficiency virus type 1 virus particles. J. Virol. 79 (2005), 5232–5237.
16. Hu, G., Liu, J., Taylor, K.A., Roux, K.H., Structural comparison of HIV-1 envelope spikes with and without the V1/V2 loop. J. Virol. 85 (2011), 2741–2750.
17. Huang, C.C., Lam, S.N., Acharya, P., Tang, M., Xiang, S.H., Hussan, S.S., Stanfield, R.L., Robinson, J., Sodroski, J., Wilson, I.A., Wyatt, R., Bewley, C.A., Kwong, P.D., Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317 (2007), 1930–1934.
18. Huang, C.C., Tang, M., Zhang, M.Y., Majeed, S., Montabana, E., Stanfield, R.L., Dimitrov, D.S., Korber, B., Sodroski, J., Wilson, I.A., Wyatt, R., Kwong, P.D., Structure of a V3-containing HIV-1 gp120 core. Science 310 (2005), 1025–1028.
19. 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., Ward, A.B., Wilson, I.A., Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342 (2013), 1477–1483.
20. Kwon, Y.D., Finzi, A., Wu, X., Dogo-Isonagie, C., Lee, L.K., Moore, L.R., Schmidt, S.D., Stuckey, J., Yang, Y., Zhou, T., Zhu, J., Vicic, D.A., Debnath, A.K., Shapiro, L., Bewley, C.A., Mascola, J.R., Sodroski, J.G., Kwong, P.D., Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops0. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 5663–5668.
21. Kwon, Y.D., Pancera, M., Acharya, P., Georgiev, I.S., Crooks, E.T., Gorman, J., Joyce, M.G., Guttman, M., Ma, X., Narpala, S., Soto, C., Terry, D.S., Yang, Y., Zhou, T., Ahlsen, G., Bailer, R.T., Chambers, M., Chuang, G.Y., Doria-Rose, N.A., Druz, A., Hallen, M.A., Harned, A., Kirys, T., Louder, M.K., O'Dell, S., Ofek, G., Osawa, K., Prabhakaran, M., Sastry, M., Stewart-Jones, G.B., Stuckey, J., Thomas, P.V., Tittley, T., Williams, C., Zhang, B., Zhao, H., Zhou, Z., Donald, B.R., Lee, L.K., Zolla-Pazner, S., Baxa, U., Schön, A., Freire, E., Shapiro, L., Lee, K.K., Arthos, J., Munro, J.B., Blanchard, S.C., Mothes, W., Binley, J.M., McDermott, A.B., Mascola, J.R., Kwong, P.D., Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat. Struct. Mol. Biol. 22 (2015), 522–531.
22. Kwong, P.D., Doyle, M.L., Casper, D.J., Cicala, C., Leavitt, S.A., Majeed, S., Steenbeke, T.D., Venturi, M., Chaiken, I., Fung, M., Katinger, H., Parren, P.W., Robinson, J., Van Ryk, D., Wang, L., Burton, D.R., Freire, E., Wyatt, R., Sodroski, J., Hendrickson, W.A., Arthos, J., HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420 (2002), 678–682.
23. Kwong, P.D., Wyatt, R., Majeed, S., Robinson, J., Sweet, R.W., Sodroski, J., Hendrickson, W.A., Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8 (2000), 1329–1339.
24. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J., Hendrickson, W.A., Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393 (1998), 648–659.
25. Lee, H.L., Ozorowski, G., Ward, A.B., Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science 351 (2016), 1043–1048.
26. Liao, H.X., Bonsignori, M., Alam, S.M., McLellan, J.S., Tomaras, G.D., Moody, M.A., Kozink, D.M., Hwang, K.K., Chen, X., Tsao, C.Y., Liu, P., Lu, X., Parks, R.J., Montefiori, D.C., Ferrari, G., Pollara, J., Rao, M., Peachman, K.K., Santra, S., Letvin, N.L., Karasavvas, N., Yang, Z.Y., Dai, K., Pancera, M., Gorman, J., Wiehe, K., Nicely, N.I., Rerks-Ngarm, S., Nitayaphan, S., Kaewkungwal, J., Pitisuttithum, P., Tartaglia, J., Sinangil, F., Kim, J.H., Michael, N.L., Kepler, T.B., Kwong, P.D., Mascola, J.R., Nabel, G.J., Pinter, A., Zolla-Pazner, S., Haynes, B.F., Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38 (2013), 176–186.
27. Liu, J., Bartesaghi, A., Borgnia, M.J., Sapiro, G., Subramaniam, S., Molecular architecture of native HIV-1 gp 120 trimers. Nature 455 (2008), 109–113.
28. Liu, L., Cimbro, R., Lusso, P., Berger, E.A., 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 (2011), 20148–20153.
29. Lyumkis, D., Julien, J.P., de Val, N., Cupo, A., Potter, C.S., Klasse, P.J., Burton, D.R., Sanders, R.W., Moore, J.P., Carragher, B., Wilson, I.A., Ward, A.B., Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342 (2013), 1484–1490.
30. Martin, L., Stricher, F., Missé, D., Sironi, F., Pugniere, M., Barthe, P., Prado-Gotor, R., Freulon, I., Magne, X., Roumestand, C., Menez, A., Lusso, P., Veas, F., Vita, C., Rational design of a CD4 mimic that inhibits HIV-1 entry and exposes cryptic neutralization epitopes. Nat. Biotechnol. 21 (2003), 71–76.
31. Mascola, J.R., Haynes, B.F., HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol. Rev. 254 (2013), 225–244.
32. McLellan, J.S., 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, J.C., Chuang, G.Y., Diwanji, D., Georgiev, I., Kwon, Y.D., Lee, D., Louder, M.K., Moquin, S., Schmidt, S.D., Yang, Z.Y., Bonsignori, M., Crump, J.A., Kapiga, S.H., Sam, N.E., Haynes, B.F., Burton, D.R., Koff, W.C., Walker, L.M., Phogat, S., Wyatt, R., Orwenyo, J., Wang, L.X., Arthos, J., Bewley, C.A., Mascola, J.R., Nabel, G.J., Schief, W.R., Ward, A.B., Wilson, I.A., Kwong, P.D., Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480 (2011), 336–343.
33. Moore, P.L., Gray, E.S., Sheward, D., Madiga, M., Ranchobe, N., Lai, Z., Honnen, W.J., Nonyane, M., Tumba, N., Hermanus, T., Sibeko, S., Mlisana, K., Abdool Karim, S.S., Williamson, C., Pinter, A., Morris, L., CAPRISA 002 Study, Potent and broad neutralization of HIV-1 subtype C by plasma antibodies targeting a quaternary epitope including residues in the V2 loop. J. Virol. 85 (2011), 3128–3141.
34. Pancera, M., Majeed, S., Ban, Y.E., Chen, L., Huang, C.C., Kong, L., Kwon, Y.D., Stuckey, J., Zhou, T., Robinson, J.E., Schief, W.R., Sodroski, J., Wyatt, R., Kwong, P.D., Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl. Acad. Sci. U S A 107 (2010), 1166–1171.
35. 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., Zhang, B., Parks, R., Eudailey, J., Lloyd, K.E., Blinn, J., Alam, S.M., Haynes, B.F., Amin, M.N., Wang, L.X., Burton, D.R., Koff, W.C., Nabel, G.J., Mascola, J.R., Bewley, C.A., Kwong, P.D., Structural basis for diverse N-glycan recognition by HIV-1–neutralizing V1–V2–directed antibody PG16. Nat. Struct. Mol. Biol. 20 (2013), 804–813.
36. Pancera, M., Zhou, T., Druz, A., Georgiev, I.S., Soto, C., Gorman, J., Huang, J., Acharya, P., Chuang, G.Y., Ofek, G., Stewart-Jones, G.B., Stuckey, J., Bailer, R.T., Joyce, M.G., Louder, M.K., Tumba, N., Yang, Y., Zhang, B., Cohen, M.S., Haynes, B.F., Mascola, J.R., Morris, L., Munro, J.B., Blanchard, S.C., Mothes, W., Connors, M., Kwong, P.D., Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514 (2014), 455–461.
37. Pejchal, R., Walker, L.M., Stanfield, R.L., Phogat, S.K., Koff, W.C., Poignard, P., Burton, D.R., Wilson, I.A., Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 11483–11488.
38. Pinter, A., Honnen, W.J., He, Y., Gorny, M.K., Zolla-Pazner, S., Kayman, S.C., The V1/V2 domain of gp120 is a global regulator of the sensitivity of primary human immunodeficiency virus type 1 isolates to neutralization by antibodies commonly induced upon infection. J. Virol. 78 (2004), 5205–5215.
39. Salzwedel, K., Smith, E., Dey, B., Berger, E., Sequential CD4/coreceptor interactions in human immunodeficiency virus type 1 Env function: soluble CD4 activates Env for coreceptor-dependent fusion and reveals blocking activities of antibodies against cryptic conserved epitopes on gp120. J. Virol. 74 (2000), 326–333.
40. 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., Golabek, M., de Los, R.K., Ketas, T.J., van Gils, M.J., King, C.R., Wilson, I.A., Ward, A.B., Klasse, P.J., Moore, J.P., 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.
41. Spurrier, B., Sampson, J., Gorny, M.K., Zolla-Pazner, S., Kong, X.P., Functional implications of the binding mode of a human conformation-dependent V2 monoclonal antibody against HIV. J. Virol. 88 (2014), 4100–4112.
42. Stewart-Jones, G.B., Soto, C., Lemmin, T., Chuang, G.Y., Druz, A., Kong, R., Thomas, P.V., Wagh, K., Zhou, T., Behrens, A.J., Bylund, T., Choi, C.W., Davison, J.R., Georgiev, I.S., Joyce, M.G., Kwon, Y.D., Pancera, M., Taft, J., Yang, Y., Zhang, B., Shivatare, S.S., Shivatare, V.S., Lee, C.C., Wu, C.Y., Bewley, C.A., Burton, D.R., Koff, W.C., Connors, M., Crispin, M., Baxa, U., Korber, B.T., Wong, C.H., Mascola, J.R., Kwong, P.D., Trimeric HIV-1-Env structures define glycan shields from clades A, B, and G. Cell 165 (2016), 813–826.
43. Sullivan, N., Thali, M., Furman, C., Ho, D.D., Sodroski, J., Effect of amino acid changes in the V1/V2 region of the human immunodeficiency virus type 1 gp120 glycoprotein on subunit association, syncytium formation, and recognition by a neutralizing antibody. J. Virol. 67 (1993), 3674–3679.
44. 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., Mitcham, J.L., Hammond, P.W., Olsen, O.A., Phung, P., Fling, S., Wong, C.H., Phogat, S., Wrin, T., Simek, M.D., Protocol G Principal Investigators, WC, K., IA, W., DR, B., Poignard, P., Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477 (2011), 466–470.
45. 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., Lehrman, J.K., Priddy, F.H., Olsen, O.A., Frey, S.M., Hammond, P.W., Protocol G Principal Investigators, Kaminsky, S., Zamb, T., Moyle, M., WC, K., Poignard, P., Burton, D.R., Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326 (2009), 285–289.
46. White, T.A., Bartesaghi, A., Borgnia, M.J., Meyerson, J.R., de la Cruz, M.J., Bess, J.W., Nandwani, R., Hoxie, J.A., Lifson, J.D., Milne, J.L., Subramaniam, S., Molecular architectures of trimeric SIV and HIV-1 envelope glycoproteins on intact viruses: strain-dependent variation in quaternary structure. PLoS Pathog., 6, 2010, e1001249.
47. Wu, S.R., Löving, R., Lindqvist, B., Hebert, H., Koeck, P.J., Sjöberg, M., Garoff, H., Single-particle cryoelectron microscopy analysis reveals the HIV-1 spike as a tripod structure. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 18844–18849.
48. Wyatt, R., Sodroski, J., The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 (1998), 1884–1888.
49. Xiang, S.H., Finzi, A., Pacheco, B., Alexander, K., Yuan, W., Rizzuto, C., Huang, C.C., Kwong, P.D., Sodroski, J., A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immunodeficiency virus envelope glycoprotein trimer. J. Virol. 84 (2010), 3147–3161.