Conformational characterization of aberrant disulfide-linked HIV-1 gp120 dimers secreted from overexpressing cells

Journal of Virological Methods

Volumn 168, Issue 1-2, 2010, Pages 155-161

  Finzi, Andrés ^a,b   Pacheco, Beatriz ^a,b   Zeng, Xin ^a,e   Kwon, Young Do ^d   Kwong, Peter D ^d   Sodroski, Joseph ^a,b,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

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

^e WILLIAMS COLLEGE   (United States)

Author keywords

CD4; Conformational change; Envelope glycoprotein; HIV 1; Virus entry

Indexed keywords

CHEMOKINE RECEPTOR; DIMER; EPITOPE; GLYCOPROTEIN GP 120; DISULFIDE; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SECRETION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RECEPTOR BINDING; CELL LINE; CHEMISTRY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SITE DIRECTED MUTAGENESIS;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

CELL LINE; DISULFIDES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 77955093635     PISSN: 01660934     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jviromet.2010.05.008     Document Type: Article

References (46)

1. Alkhatib G., Combadiere C., Broder C.C., Feng Y., Kennedy P.E., Murphy P.M., Berger E.A. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 1996, 272:1955-1958.
2. Allan J.S., Coligan J.E., Barin F., McLane M.F., Sodroski J.G., Rosen C.A., Haseltine W.A., Lee T.H., Essex M. Major glycoprotein antigens that induce antibodies in AIDS patients are encoded by HTLV-III. Science 1985, 228:1091-1094.
3. Boots L.J., McKenna P.M., Arnold B.A., Keller P.M., Gorny M.K., Zolla-Pazner S., Robinson J.E., Conley A.J. Anti-human immunodeficiency virus type 1 human monoclonal antibodies that bind discontinuous epitopes in the viral glycoproteins can identify mimotopes from recombinant phage peptide display libraries. AIDS Res. Hum. Retroviruses 1997, 13:1549-1559.
4. Center R.J., Earl P.L., Lebowitz J., Schuck P., Moss B. The human immunodeficiency virus type 1 gp120 V2 domain mediates gp41-independent intersubunit contacts. J. Virol. 2000, 74:4448-4455.
5. Chan D.C., Fass D., Berger J.M., Kim P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997, 89:263-273.
6. Choe H., Farzan M., Sun Y., Sullivan N., Rollins B., Ponath P.D., Wu L., Mackay C.R., LaRosa G., Newman W., Gerard N., Gerard C., Sodroski J. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 1996, 85:1135-1148.
7. Chowdhury I.H., Koyanagi Y., Takamatsu K., Yoshida O., Kobayashi S., Yamamoto N. Evaluation of anti-human immunodeficiency virus effect of recombinant CD4-immunoglobulin in vitro: a good candidate for AIDS treatment. Med. Microbiol. Immunol. 1991, 180:183-192.
8. Dalgleish A.G., Beverley P.C., Clapham P.R., Crawford D.H., Greaves M.F., Weiss R.A. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984, 312:763-767.
9. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R.E., Hill C.M., Davis C.B., Peiper S.C., Schall T.J., Littman D.R., Landau N.R. Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996, 381:661-666.
10. Doms R.W., Earl P.L., Moss B. The assembly of the HIV-1 env glycoprotein into dimers and tetramers. Adv. Exp. Med. Biol. 1991, 300:203-219. (discussion 220-1).
11. Doranz B.J., Rucker J., Yi Y., Smyth R.J., Samson M., Peiper S.C., Parmentier M., Collman R.G., Doms R.W. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 1996, 85:1149-1158.
12. Dragic T., Litwin V., Allaway G.P., Martin S.R., Huang Y., Nagashima K.A., Cayanan C., Maddon P.J., Koup R.A., Moore J.P., Paxton W.A. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 1996, 381:667-673.
13. Earl P.L., Doms R.W., Moss B. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:648-652.
14. Farzan M., Choe H., Desjardins E., Sun Y., Kuhn J., Cao J., Archambault D., Kolchinsky P., Koch M., Wyatt R., Sodroski J. Stabilization of human immunodeficiency virus type 1 envelope glycoprotein trimers by disulfide bonds introduced into the gp41 glycoprotein ectodomain. J. Virol. 1998, 72:7620-7625.
15. Feng Y., Broder C.C., Kennedy P.E., Berger E.A. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 1996, 272:872-877.
16. Finzi A., Xiang S.-H., Pacheco B., Wang L., Haight J., Kassa A., Danek B., Pancera M., Kwong P.D., Sodroski J. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol. Cell 2010, 37:656-667.
17. Hallenberger S., Tucker S.P., Owens R.J., Bernstein H.B., Compans R.W. Secretion of a truncated form of the human immunodeficiency virus type 1 envelope glycoprotein. Virology 1993, 193:510-514.
18. Helseth E., Olshevsky U., Furman C., Sodroski J. Human immunodeficiency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein. J. Virol. 1991, 65:2119-2123.
19. Kang C.Y., Hariharan K., Nara P.L., Sodroski J., Moore J.P. Immunization with a soluble CD4-gp120 complex preferentially induces neutralizing anti-human immunodeficiency virus type 1 antibodies directed to conformation-dependent epitopes of gp120. J. Virol. 1994, 68:5854-5862.
20. Kassa A., Finzi A., Pancera M., Courter J.R., Smith A.B., Sodroski J. Identification of a human immunodeficiency virus (HIV-1) envelope glycoprotein variant resistant to cold inactivation. J. Virol. 2009, 83:4476-4488.
21. Kassa A., Madani N., Schon A., Haim H., Finzi A., Xiang S.H., Wang L., Princiotto A., Pancera M., Courter J., Smith A.B., Freire E., Kwong P.D., Sodroski J. Transitions to and from the CD4-bound conformation are modulated by a single-residue change in the human immunodeficiency virus type 1 gp120 inner domain. J. Virol. 2009, 83:8364-8378.
22. Klatzmann D., Champagne E., Chamaret S., Gruest J., Guetard D., Hercend T., Gluckman J.C., Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 1984, 312:767-768.
23. Korber B., Foley B.T., Kuiken C., Pillai S.K., Sodroski J.G. Numbering positions in HIV relative to HXB2CG. Human Retroviruses and AIDS 1998, pp. III, 102-111.
24. 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 2000, 8:1329-1339.
25. 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 1998, 393:648-659.
26. Kwong P.D., Doyle M.L., Casper D.J., Cicala C., Leavitt S., Majeed S., Steenbeke T., Venturi M., Chaiken I., Fung M., Katinger H., Parren P., Robinson J., Wang L., Burton D.R., Freire E., Wyatt R., Sodroski J., Hendrickson W.A., Arthos J. HIV-1 evades neutralization through conformational masking of receptor-binding sites. Nature 2002, 420:678-682.
27. Lu M., Blacklow S.C., Kim P.S. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 1995, 2:1075-1082.
28. McDougal J.S., Kennedy M.S., Sligh J.M., Cort S.P., Mawle A., Nicholson J.K.A. Binding of HTLV-III/LAV to T4+ T cells by a complex of the 110K viral protein and the T4 molecules. Science 1986, 231:382-385.
29. Moore J.P., Sattentau Q.J., Wyatt R., Sodroski J. Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J. Virol. 1994, 68:469-484.
30. Moore J.P., Sodroski J. Antibody cross-competition analysis of the human immunodeficiency virus type 1 gp120 exterior envelope glycoprotein. J. Virol. 1996, 70:1863-1872.
31. Myszka D., Sweet R.W., Hensley P., Brigham-Burke M., Kwong P.D., Hendrickson W.A., Wyatt R., Sodroski J., Doyle M. Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:9026-9031.
32. Owens R.J., Compans R.W. The human immunodeficiency virus type 1 envelope glycoprotein precursor acquires aberrant intermolecular disulfide bonds that may prevent normal proteolytic processing. Virology 1990, 179:827-833.
33. Robey W.G., Safai B., Oroszlan S., Arthur L.O., Gonda M.A., Gallo R.C., Fischinger P.J. Characterization of envelope and core structural gene products of HTLV-III with sera from AIDS patients. Science 1985, 228:593-595.
34. Schawaller M., Smith G.E., Skehel J.J., Wiley D.C. Studies with crosslinking reagents on the oligomeric structure of the env glycoprotein of HIV. Virology 1989, 172:367-369.
35. Thali M., Olshevsky U., Furman C., Gabuzda D., Posner M., Sodroski J. Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody. J. Virol. 1991, 65:6188-6193.
36. Thali M., Moore J.P., Furman C., Charles M., Ho D.D., Robinson J., Sodroski J. Characteriization of conserved human immunodeficiency virus type 1gp120 neutralization epitopes exposed upon gp120-CD4 binding. J. Virol. 1993, 67:3978-3988.
37. Thomas D.J., Wall J.S., Hainfeld J.F., Kaczorek M., Booy F.P., Trus B.L., Eiserling F.A., Steven A.C. gp160, the envelope glycoprotein of human immunodeficiency virus type 1, is a dimer of 125-kilodalton subunits stabilized through interactions between their gp41 domains. J. Virol. 1991, 65:3797-3803.
38. Trkola A., Dragic T., Arthos J., Binley J.M., Olson W.C., Allaway G.P., Cheng-Mayer C., Robinson J., Maddon P.J., Moore J.P. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 1996, 384:184-187.
39. Weissenhorn W., Dessen A., Harrison S.C., Skehel J.J., Wiley D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 1997, 387:426-430.
40. Wu L., Gerard N.P., Wyatt R., Choe H., Parolin C., Ruffing N., Borsetti A., Cardoso A.A., Desjardins E., Newman W., Gerard C., Sodroski J. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 1996, 384:179-183.
41. Wyatt R., Moore J., Accola M., Desjardins E., Robinson J., Sodroski J. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 1995, 69:5723-5733.
42. Xiang S.H., Kwong P.D., Gupta R., Rizzuto C.D., Casper D.J., Wyatt R., Wang L., Hendrickson W.A., Doyle M.L., Sodroski J. Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodeficiency virus type 1 gp120 envelope glycoprotein. J. Virol. 2002, 76:9888-9899.
43. 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 envelop glycoprotein trimer. J. Virol. 2010, 84:3147-3161.
44. Yang X., Tomov V., Kurteva S., Wang L., Ren X., Gorny M.K., Zolla-Pazner S., Sodroski J. Characterization of the outer domain of the gp120 glycoprotein from human immunodeficiency virus type 1. J. Virol. 2004, 78:12975-12986.
45. Zhou T., Xu L., Dey B., Hessell A.J., Van Ryk D., Xiang S.H., Yang X., Zhang M.Y., Zwick M.B., Arthos J., Burton D.R., Dimitrov D.S., Sodroski J., Wyatt R., Nabel G.J., Kwong P.D. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 2007, 445:732-737.
46. Zhu P., Chertova E., Bess J., Lifson J.D., Arthur L.O., Liu J., Taylor K.A., Roux K.H. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15812-15817.