Tyrosine sulfation in the second variable loop (V2) of HIV-1 gp120 stabilizes V2-V3 interaction and modulates neutralization sensitivity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 8, 2014, Pages 3152-3157

  Cimbro, Raffaello ^a,c   Gallant, Thomas R ^a   Dolan, Michael A ^a   Guzzo, Christina ^a   Zhang, Peng ^a   Lin, Yin ^a   Miao, Huiyi ^a   Van Ryk, Donald ^a   Arthos, James ^a   Gorshkova, Inna ^b   Brown, Patrick H ^b   Hurt, Darrell E ^a   Lusso, Paolo ^a  

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

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; CH01 ANTIBODY; CHEMOKINE RECEPTOR CCR5; FROXIPROST; GLYCOPROTEIN GP 120; NEUTRALIZING ANTIBODY; PG16 ANTIBODY; PG9 ANTIBODY; PGT145 ANTIBODY; PROTEIN ANTIBODY; SOLUBLE CD4 ANTIGEN; SULFOTRANSFERASE; TYROSINE; TYROSYL SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ARTICLE; CD4+ T LYMPHOCYTE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RECEPTOR BINDING; STRUCTURAL HOMOLOGY; SULFATION; VIRION; VIRUS NEUTRALIZATION;

BLOTTING, WESTERN; FLOW CYTOMETRY; HEK293 CELLS; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; NEUTRALIZATION TESTS; PROTEIN CONFORMATION; SURFACE PLASMON RESONANCE; TYROSINE;

EID: 84896855620     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314718111     Document Type: Article

References (48)

1. Burton DR, et al. (2012) A blueprint for HIV vaccine discovery. Cell Host Microbe 12(4): 396-407.
2. Mascola JR, Haynes BF (2013) HIV-1 neutralizing antibodies: Understanding nature's pathways. Immunol Rev 254(1):225-244.
3. Wyatt R, Sodroski J (1998) The HIV-1 envelope glycoproteins: Fusogens, antigens, and immunogens. Science 280(5371):1884-1888. (Pubitemid 28299385)
4. Kwong PD, et al. (2002) HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420(6916):678-682. (Pubitemid 36764500)
5. Myszka DG, et al. (2000) Energetics of the HIV gp120-CD4 binding reaction. Proc Natl Acad Sci USA 97(16):9026-9031. (Pubitemid 30626667)
6. Kwong PD, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393(6686): 648-659. (Pubitemid 28289647)
7. Kwong PD, et al. (2000) Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8(12):1329-1339. (Pubitemid 32149759)
8. Huang CC, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310(5750):1025-1028.
9. Chen L, et al. (2009) Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326(5956):1123-1127.
10. Pancera M, 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 USA 107(3):1166-1171.
11. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455(7209):109-113.
12. White TA, 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(12):e1001249.
13. 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(6):2741-2750.
14. Harris A, et al. (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 USA 108(28):11440-11445.
15. Julien JP, et al. (2013) Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc Natl Acad Sci USA 110(11):4351-4356.
16. Bartesaghi A, Merk A, Borgnia MJ, Milne JL, Subramaniam S (2013) Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat Struct Mol Biol 20(12):1352-1357.
17. Lyumkis D, et al. (2013) Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342(6165):1484-1490.
18. Julien JP, et al. (2013) Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342(6165):1477-1483.
19. Sullivan N, Thali M, Furman C, Ho DD, Sodroski J (1993) 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(6):3674-3679. (Pubitemid 23143755)
20. Xiang SH, et al. (2010) A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immunodeficiency virus envelope glycoprotein trimer. J Virol 84(7):3147-3161.
21. Kwon YD, 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 USA 109(15):5663-5668.
22. Walker LM, et al.; Protocol G Principal Investigators (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326(5950):285-289.
23. Walker LM, et al.; Protocol G Principal Investigators (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477(7365):466-470.
24. Cao J, et al. (1997) Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J Virol 71(12):9808-9812. (Pubitemid 27492434)
25. Pinter A, et al. (2004) 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(10):5205-5215. (Pubitemid 38581472)
26. 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 USA 108(50):20148-20153.
27. Rusert P, et al. (2011) Interaction of the gp120 V1V2 loop with a neighboring gp120 unit shields the HIV envelope trimer against cross-neutralizing antibodies. J Exp Med 208(7):1419-1433.
28. Ghiara JB, Stura EA, Stanfield RL, Profy AT, Wilson IA (1994) Crystal structure of the principal neutralization site of HIV-1. Science 264(5155):82-85. (Pubitemid 24146010)
29. Liao HX, et al. (2013) Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38(1):176-186.
30. McLellan JS, et al. (2011) Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480(7377):336-343.
31. Pancera M, et al. (2013) Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat Struct Mol Biol 20(7):804- 813.
32. Sanders RW, et al. (2013) A next-generation cleaved, soluble HIV-1 Env Trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not nonneutralizing antibodies. PLoS Pathog 9(9):e1003618.
33. Zolla-Pazner S, Cardozo T (2010) Structure-function relationships of HIV-1 envelope sequence-variable regions refocus vaccine design. Nat Rev Immunol 10(7):527-535.
34. Huang CC, et al. (2007) Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317(5846):1930- 1934.
35. Farzan M, et al. (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96(5):667-676. (Pubitemid 29122809)
36. Farzan M, et al. (2000) 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(43):33516-33521.
37. Choe H, et al. (2003) Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell 114(2):161-170. (Pubitemid 36936910)
38. Cavacini LA, et al. (2003) Conformational changes in env oligomer induced by an antibody dependent on the V3 loop base. AIDS 17(5):685-689.
39. Lusso P, et al. (2005) Cryptic nature of a conserved, CD4-inducible V3 loop neutralization epitope in the native envelope glycoprotein oligomer of CCR5-restricted, but not CXCR4-using, primary human immunodeficiency virus type 1 strains. J Virol 79(11):6957-6968. (Pubitemid 40677327)
40. Bonsignori M, et al. (2011) Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J Virol 85(19):9998-10009.
41. Zhou T, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329(5993):811-817.
42. Trkola A, et al. (1996) Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70(2):1100-1108. (Pubitemid 26029030)
43. Moore KL (2003) The biology and enzymology of protein tyrosine O-sulfation. J Biol Chem 278(27):24243-24246.
44. Pejchal R, et al. (2010) Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1. Proc Natl Acad Sci USA 107(25):11483-11488.
45. Edson CM (1993) Tyrosine sulfation of varicella-zoster virus envelope glycoprotein gpl. Virology 197(1):159-165.
46. Mascola JR, et al. (2005) Recommendations for the design and use of standard virus panels to assess neutralizing antibody responses elicited by candidate human immunodeficiency virus type 1 vaccines. J Virol 79(16):10103-10107. (Pubitemid 41098551)
47. Pitisuttithum P, et al.; Bangkok Vaccine Evaluation Group (2006) Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis 194(12): 1661-1671. (Pubitemid 44901996)
48. Rerks-Ngarm S, et al.; MOPH-TAVEG Investigators (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361(23):2209-2220.