A Twin-Cysteine Motif in the V2 Region of gp120 Is Associated with SIV Envelope Trimer Stabilization

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Bohl, Christopher ^a,b   Bowder, Dane ^a,b   Thompson, Jesse ^a   Abrahamyan, Levon ^a,b   Gonzalez Ramirez, Sandra ^a,b   Mao, Youdong ^c,d   Sodroski, Joseph ^c,d,e,f   Wood, Charles ^a,b   Xiang, Shi hua ^a,b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; GLYCOPROTEIN GP 120; MUTANT PROTEIN; VIRUS ENVELOPE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL FUSION; CONTROLLED STUDY; DISULFIDE BOND; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; LIGAND BINDING; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROMOTER REGION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECEPTOR BINDING; SIMIAN IMMUNODEFICIENCY VIRUS; TWIN CYSTEINE MOTIF; VIRUS ENTRY; VIRUS INFECTION; VIRUS SHEDDING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL FUSION; CELL LINE; CYSTEINE; HUMANS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PHYLOGENY; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECEPTORS, VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL ENVELOPE PROTEINS;

EID: 84880710594     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069406     Document Type: Article

References (45)

1. Hemelaar J, (2011) The origin and diversity of the HIV-1 pandemic. Trends Mol Med 18: 182-192.
2. Sharp PM, Hahn BH, (2011) Origins of HIV and the AIDS Pandemic. Cold Spring Harb Perspect Med 1: a006841.
3. Hahn BH, Shaw GM, De Cock KM, Sharp PM, (2000) AIDS as a zoonosis: scientific and public health implications. Science 287: 607-614.
4. Van Heuverswyn F, Peeters M, (2007) The origins of HIV and implications for the global epidemic. Curr Infect Dis Rep 9: 338-346.
5. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, et al. (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220: 868-871.
6. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557.
7. Stevenson M, (2003) HIV-1 pathogenesis. Nat Med 9: 853-860.
8. Rambaut A, Posada D, Crandall KA, Holmes EC, (2004) The causes and consequences of HIV evolution. Nat Rev Genet 5: 52-61.
9. Pandrea I, Apetrei C, (2010) Where the wild things are: pathogenesis of SIV infection in African nonhuman primate hosts. Curr HIV/AIDS Rep 7: 28-36.
10. Pandrea I, Silvestri G, Apetrei C, (2009) AIDS in african nonhuman primate hosts of SIVs: a new paradigm of SIV infection. Curr HIV Res 7: 57-72.
11. Lackner AA, Veazey RS, (2007) Current concepts in AIDS pathogenesis: insights from the SIV/macaque model. Annu Rev Med 58: 461-476.
12. Etienne L, Nerrienet E, LeBreton M, Bibila GT, Foupouapouognigni Y, et al. (2011) Characterization of a new simian immunodeficiency virus strain in a naturally infected Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology 8: 4.
13. Finzi A, Pacheco B, Xiang SH, Pancera M, Herschhorn A, et al. (2012) Lineage-Specific Differences between Human and Simian Immunodeficiency Virus Regulation of gp120 Trimer Association and CD4 Binding. J Virol 86: 8974-8986.
14. Hirsch VM, (2004) What can natural infection of African monkeys with simian immunodeficiency virus tell us about the pathogenesis of AIDS? AIDS Rev 6: 40-53.
15. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, et al. (2006) Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313: 523-526.
16. Burton DR, Desrosiers RC, Doms RW, Koff WC, Kwong PD, et al. (2004) HIV vaccine design and the neutralizing antibody problem. Nat Immunol 5: 233-236.
17. Walker LM, Burton DR, (2010) Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr Opin Immunol 22: 358-366.
18. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, et al. (1998) The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393: 705-711.
19. Moore JP, Sattentau QJ, Wyatt R, Sodroski J, (1994) Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J Virol 68: 469-484.
20. Kwong PD, Mascola JR, Nabel GJ, (2012) Rational Design of Vaccines to Elicit Broadly Neutralizing Antibodies to HIV-1. Cold Spring Harb Perspect Med 1: a007278.
21. Kwong PD, Wyatt R, Majeed S, Robinson J, Sweet RW, et al. (2000) Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8: 1329-1339.
22. Kwon YD, Finzi A, Wu X, Dogo-Isonagie C, Lee LK, et al. (2012) Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops. Proc Natl Acad Sci U S A 109: 5663-5668.
23. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
24. Zanetti G, Briggs JA, Grunewald K, Sattentau QJ, Fuller SD, (2006) Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog 2: e83.
25. Zhu P, Liu J, Bess J Jr, Chertova E, Lifson JD, et al. (2006) Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441: 847-852.
26. White TA, Bartesaghi A, Borgnia MJ, Meyerson JR, de la Cruz MJ, et al. (2010) Molecular architectures of trimeric SIV and HIV-1 envelope glycoproteins on intact viruses: strain-dependent variation in quaternary structure. PLoS Pathog 6: e1001249.
27. Julien JP, Lee JH, Cupo A, Murin CD, Derking R, et al. (2013) Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc Natl Acad Sci U S A 110: 4351-4356.
28. Hu G, Liu J, Taylor KA, Roux KH, (2010) Structural comparison of HIV-1 envelope spikes with and without the V1/V2 loop. J Virol 85: 2741-2750.
29. Mao Y, Wang L, Gu C, Herschhorn A, Xiang SH, et al. (2012) Subunit organization of the membrane-bound HIV-1 envelope glycoprotein trimer. Nat Struct Mol Biol.
30. Gorny MK, Pan R, Williams C, Wang XH, Volsky B, et al. (2012) Functional and immunochemical cross-reactivity of V2-specific monoclonal antibodies from HIV-1-infected individuals. Virology 427: 198-207.
31. Ringe R, Phogat S, Bhattacharya J, (2012) Subtle alteration of residues including N-linked glycans in V2 loop modulate HIV-1 neutralization by PG9 and PG16 monoclonal antibodies. Virology 426: 34-41.
32. Moore PL, Gray ES, Sheward D, Madiga M, Ranchobe N, et al. (2011) 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: 3128-3141.
33. Rolland M, Edlefsen PT, Larsen BB, Tovanabutra S, Sanders-Buell E, et al. (2012) Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 490: 417-420.
34. Doria-Rose NA, Georgiev I, O'Dell S, Chuang GY, Staupe RP, et al. (2012) A short segment of the HIV-1 gp120 V1/V2 region is a major determinant of resistance to V1/V2 neutralizing antibodies. J Virol 86: 8319-8323.
35. McElrath MJ, Haynes BF, (2010) Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 33: 542-554.
36. McLellan JS, Pancera M, Carrico C, Gorman J, Julien JP, et al. (2011) Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480: 336-343.
37. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, et al. (2005) Determining the structure of an unliganded and fully glycosylated SIV gp120 envelope glycoprotein. Structure 13: 197-211.
38. Go EP, Zhang Y, Menon S, Desaire H, (2011) Analysis of the disulfide bond arrangement of the HIV-1 envelope protein CON-S gp140 DeltaCFI shows variability in the V1 and V2 regions. J Proteome Res 10: 578-591.
39. Gregory T, Hoxie J, Watanabe C, Spellman M, (1991) Structure and function in recombinant HIV-1 gp120 and speculation about the disulfide bonding in the gp120 homologs of HIV-2 and SIV. Adv Exp Med Biol 303: 1-14.
40. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, et al. (2010) 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: 1166-1171.
41. Kolchinsky P, Kiprilov E, Bartley P, Rubinstein R, Sodroski J, (2001) Loss of a single N-linked glycan allows CD4-independent human immunodeficiency virus type 1 infection by altering the position of the gp120 V1/V2 variable loops. J Virol 75: 3435-3443.
42. Pinter A, Honnen WJ, Kayman SC, Trochev O, Wu Z, (1998) Potent neutralization of primary HIV-1 isolates by antibodies directed against epitopes present in the V1/V2 domain of HIV-1 gp120. Vaccine 16: 1803-1811.
43. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
44. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
45. Korber B, Foley BT, Kuiken C, Pillai SK, Sodroski JG (1998) Numbering Positions in HIV Relative to HXB2CG. Human Retroviruses and AIDS: 102-111.