Structural Basis of the Cross-Reactivity of Genetically Related Human Anti-HIV-1 mAbs: Implications for Design of V3-Based Immunogens

Structure

Volumn 17, Issue 11, 2009, Pages 1538-1546

  Burke, Valicia ^a   Williams, Constance ^a   Sukumaran, Madhav ^a   Kim, Seung Sup ^a   Li, Huiguang ^a   Wang, Xiao Hong ^b   Gorny, Miroslaw K ^a   Zolla Pazner, Susan ^a,b   Kong, Xiang Peng ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

MICROBIO; MOLIMMUNO; PROTEINS

Indexed keywords

ARGININE; GLYCOPROTEIN GP 120; GLYCYLPROLYLGLYCYLARGININE; GLYCYLPROLYLGLYCYLGLUTAMINE; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY 447 52D; MONOCLONAL ANTIBODY 537 10D; TETRAPEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; BINDING SITE; CONTROLLED STUDY; CROSS REACTION; DRUG STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROGEN BOND; IMMUNOGLOBULIN VARIABLE REGION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; BASE SEQUENCE; CROSS REACTIONS; CRYSTALLIZATION; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; VACCINES, SYNTHETIC; X-RAY DIFFRACTION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 70350714115     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.09.012     Document Type: Article

References (60)

1. Abagyan R.A., Totrov M., and Kuznetsov D. ICM - A new method for protein modeling and design: Applications to docking and structure prediction from the distorted native conformation. J. Comput. Chem. 15 (1994) 488-506
2. Bell C.H., Pantophlet R., Schiefner A., Cavacini L.A., Stanfield R.L., Burton D.R., and Wilson I.A. Structure of antibody F425-B4e8 in complex with a V3 peptide reveals a new binding mode for HIV-1 neutralization. J. Mol. Biol. 375 (2008) 969-978
3. Binley J.M., Wrin T., Korber B., Zwick M.B., Wang M., Chappey C., Stiegler G., Kunert R., Zolla-Pazner S., Katinger H., et al. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78 (2004) 13232-13252
4. Binley J.M., Lybarger E.A., Crooks E.T., Seaman M.S., Gray E., Davis K.L., Decker J.M., Wycuff D., Harris L., Hawkins N., et al. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82 (2008) 11651-11668
5. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
6. Burton D.R. A vaccine for HIV type 1: the antibody perspective. Proc. Natl. Acad. Sci. USA 94 (1997) 10018-10023
7. Burton D.R., Desrosiers R.C., Doms R.W., Koff W.C., Kwong P.D., Moore J.P., Nabel G.J., Sodroski J., Wilson I.A., and Wyatt R.T. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5 (2004) 233-236
8. Cardozo T., Swetnam J., Pinter A., Krachmarov C., Nadas A., Almond D., and Zolla-Pazner S. Worldwide distribution of HIV-1 epitopes recognized by human anti-V3 monoclonal antibodies. AIDS Res. Hum. Retroviruses 25 (2009) 441-450
9. Carrow E.W., Vujcic L.K., Glass W.L., Seamon K.B., Rastogi S.C., Hendry R.M., Boulos R., Nzila N., and Quinnan Jr. G.V. High prevalence of antibodies to the gp120 V3 region principal neutralizing determinant of HIV-1MN in sera from Africa and the Americas. AIDS Res. Hum. Retroviruses 7 (1991) 831-838
10. Conley A.J., Gorny M.K., Kessler II J.A., Boots L.J., Ossorio-Castro M., Koenig S., Lineberger D.W., Emini E.A., Williams C., and Zolla-Pazner S. Neutralization of primary human immunodeficiency virus type 1 isolates by the broadly reactive anti-V3 monoclonal antibody, 447-52D. J. Virol. 68 (1994) 6994-7000
11. Davis K.L., Bibollet-Ruche F., Li H., Decker J.M., Kutsch O., Morris L., Salomon A., Pinter A., Hoxie J.A., Hahn B.H., et al. Human immunodeficiency virus type 2 (HIV-2)/HIV-1 envelope chimeras detect high titers of broadly reactive HIV-1 V3-specific antibodies in human plasma. J. Virol. 83 (2009) 1240-1259
12. DeLano W.L. The PyMOL User's Manual (2002), DeLano Scientific, Palo Alto
13. Dhillon A.K., Stanfield R.L., Gorny M.K., Williams C., Zolla-Pazner S., and Wilson I.A. Structure determination of an anti-HIV-1 Fab 447-52D-peptide complex from an epitaxially twinned data set. Acta Crystallogr. D Biol. Crystallogr. D64 (2008) 792-802
14. Douek D.C., Kwong P.D., and Nabel G.J. The rational design of an AIDS vaccine. Cell 124 (2006) 677-681
15. Fellouse F.A., Wiesmann C., and Sidhu S.S. Synthetic antibodies from a four-amino-acid code: a dominant role for tyrosine in antigen recognition. Proc. Natl. Acad. Sci. USA 101 (2004) 12467-12472
16. Gaschen B., Korber B.T., and Foley B.T. Global variation in the HIV-1 V3 region. In: Kuiken C.L., Foley B., Hahn B., Marx P.A., McCutchan F., Mellors J.W., Mullins J.I., Wolinsky S., and Korber B. (Eds). Human Retroviruses and AIDS 1999 (1999), Los Alamos National Laboratory, Los Alamos, NM 593-789
17. Gigler A., Dorsch S., Hemauer A., Williams C., Kim S., Young N.S., Zolla-Pazner S., Wolf H., Gorny M.K., and Modrow S. Generation of neutralizing human monoclonal antibodies against parvovirus B19 proteins. J. Virol. 73 (1999) 1974-1979
18. Gorny M., and Zolla-Pazner S. Human Monoclonal Antibodies that Neutralize HIV-1. In: Korber B., Brander C., Haynes B.F., Koup R.A., Moore J.P., Walker B., and Watkins D.I. (Eds). HIV Immunology and HIV/SIV Vaccine Databases 2003 (2003), Los Alamos National Laboratory, Los Alamos, NM 37-51
19. Gorny M.K., Gianakakos V., Sharpe S., and Zolla-Pazner S. Generation of human monoclonal antibodies to human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 86 (1989) 1624-1628
20. Gorny M.K., Conley A.J., Karwowska S., Buchbinder A., Xu J.Y., Emini E.A., Koenig S., and Zolla-Pazner S. Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J. Virol. 66 (1992) 7538-7542
21. Gorny M.K., Xu J.Y., Karwowska S., Buchbinder A., and Zolla-Pazner S. Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. J. Immunol. 150 (1993) 635-643
22. Gorny M.K., Williams C., Volsky B., Revesz K., Cohen S., Polonis V.R., Honnen W.J., Kayman S.C., Krachmarov C., Pinter A., and Zolla-Pazner S. Human monoclonal antibodies specific for conformation-sensitive epitopes of V3 neutralize human immunodeficiency virus type 1 primary isolates from various clades. J. Virol. 76 (2002) 9035-9045
23. Gorny M.K., Revesz K., Williams C., Volsky B., Louder M.K., Anyangwe C.A., Krachmarov C., Kayman S.C., Pinter A., Nadas A., et al. The v3 loop is accessible on the surface of most human immunodeficiency virus type 1 primary isolates and serves as a neutralization epitope. J. Virol. 78 (2004) 2394-2404
24. Gorny M.K., Williams C., Volsky B., Revesz K., Wang X.H., Burda S., Kimura T., Konings F.A., Nadas A., Anyangwe C.A., et al. Cross-clade neutralizing activity of human anti-V3 monoclonal antibodies derived from the cells of individuals infected with non-B clades of human immunodeficiency virus type 1. J. Virol. 80 (2006) 6865-6872
25. Gorny M.K., Wang X.H., Williams C., Volsky B., Revesz K., Witover B., Burda S., Urbanski M., Nyambi P., Krachmarov C., et al. Preferential use of the VH5-51 gene segment by the human immune response to code for antibodies against the V3 domain of HIV-1. Mol. Immunol. 46 (2009) 917-926
26. Goudsmit J., Debouck C., Meloen R.H., Smit L., Bakker M., Asher D.M., Wolff A.V., Gibbs Jr. C.J., and Gajdusek D.C. Human immunodeficiency virus type 1 neutralization epitope with conserved architecture elicits early type-specific antibodies in experimentally infected chimpanzees. Proc. Natl. Acad. Sci. USA 85 (1988) 4478-4482
27. 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., et al. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317 (2007) 1930-1934
28. 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., et al. Structure of a V3-containing HIV-1 gp120 core. Science 310 (2005) 1025-1028
29. Ivanoff L.A., Dubay J.W., Morris J.F., Roberts S.J., Gutshall L., Sternberg E.J., Hunter E., Matthews T.J., and Petteway Jr. S.R. V3 loop region of the HIV-1 gp120 envelope protein is essential for virus infectivity. Virology 187 (1992) 423-432
30. Javaherian K., Langlois A.J., McDanal C., Ross K.L., Eckler L.I., Jellis C.L., Profy A.T., Rusche J.R., Bolognesi D.P., Putney S.D., et al. Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc. Natl. Acad. Sci. USA 86 (1989) 6768-6772
31. Javaherian K., Langlois A.J., LaRosa G.J., Profy A.T., Bolognesi D.P., Herlihy W.C., Putney S.D., and Matthews T.J. Broadly neutralizing antibodies elicited by the hypervariable neutralizing determinant of HIV-1. Science 250 (1990) 1590-1593
32. Jones T.A. Interactive electron-density map interpretation: from INTER to O. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2115-2125
33. Kabat E.A., Wu T.T., Perry H.M., and Gottesman K.S. Sequences of Proteins of Immunological Interest. Fifth Edition (1991), National Institutes of Health, Bethesda, MD
34. Karlsson Hedestam G.B., Fouchier R.A., Phogat S., Burton D.R., Sodroski J., and Wyatt R.T. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6 (2008) 143-155
35. Krachmarov C.P., Kayman S.C., Honnen W.J., Trochev O., and Pinter A. V3-specific polyclonal antibodies affinity purified from sera of infected humans effectively neutralize primary isolates of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 17 (2001) 1737-1748
36. Krachmarov C., Pinter A., Honnen W.J., Gorny M.K., Nyambi P.N., Zolla-Pazner S., and Kayman S.C. Antibodies that are cross-reactive for human immunodeficiency virus type 1 clade a and clade B v3 domains are common in patient sera from Cameroon, but their neutralization activity is usually restricted by epitope masking. J. Virol. 79 (2005) 780-790
37. Krachmarov C.P., Honnen W.J., Kayman S.C., Gorny M.K., Zolla-Pazner S., and Pinter A. Factors determining the breadth and potency of neutralization by V3-specific human monoclonal antibodies derived from subjects infected with clade A or clade B strains of human immunodeficiency virus type 1. J. Virol. 80 (2006) 7127-7135
38. Kuiken C.L., Foley B., Hahn B., Marx P.A., McCutchan F., Mellors J.W., Mullins J.I., Wolinsky S., and Korber B. Human Retroviruses and AIDS 1999: A Compilation and Analysis of Nucleic Acid and Amino Acid Sequences (1999), Theoretical Biology and Biophysics Group, Los Alamos National Laborator, Los Alamos, NM
39. Kwong P.D., and Wilson I.A. HIV-1 and influenza antibodies: seeing antigens in new ways. Nat. Immunol. 10 (2009) 573-578
40. Law M., Cardoso R.M., Wilson I.A., and Burton D.R. Antigenic and immunogenic study of membrane-proximal external region-grafted gp120 antigens by a DNA prime-protein boost immunization strategy. J. Virol. 81 (2007) 4272-4285
41. Leonard C.K., Spellman M.W., Riddle L., Harris R.J., Thomas J.N., and Gregory T.J. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265 (1990) 10373-10382
42. Lewis C.M., Hollis G.F., Mark III G.E., Tung J.S., and Ludmerer S.W. Use of a novel mutagenesis strategy, optimized residue substitution, to decrease the off-rate of an anti-gp120 antibody. Mol. Immunol. 32 (1995) 1065-1072
43. McKeating J.A., Gow J., Goudsmit J., Pearl L.H., Mulder C., and Weiss R.A. Characterization of HIV-1 neutralization escape mutants. AIDS 3 (1989) 777-784
44. Otwinowski Z., and Minor W. Processing of X-ray Diffraction Data Collected in Oscillation Mode. In: Carter Jr. C.W., and Sweet R.M. (Eds). Methods in Enzymology, Macromolecular Crystallography Part A (1997), Academic Press, New York 307-326
45. Palker T.J., Clark M.E., Langlois A.J., Matthews T.J., Weinhold K.J., Randall R.R., Bolognesi D.P., and Haynes B.F. Type-specific neutralization of the human immunodeficiency virus with antibodies to env-encoded synthetic peptides. Proc. Natl. Acad. Sci. USA 85 (1988) 1932-1936
46. Ratner L., Fisher A., Jagodzinski L.L., Mitsuya H., Liou R.S., Gallo R.C., and Wong-Staal F. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res. Hum. Retroviruses 3 (1987) 57-69
47. Resch W., Hoffman N., and Swanstrom R. Improved success of phenotype prediction of the human immunodeficiency virus type 1 from envelope variable loop 3 sequence using neural networks. Virology 288 (2001) 51-62
48. Sharon M., Kessler N., Levy R., Zolla-Pazner S., Gorlach M., and Anglister J. Alternative conformations of HIV-1 V3 loops mimic beta hairpins in chemokines, suggesting a mechanism for coreceptor selectivity. Structure 11 (2003) 225-236
49. Stanfield R.L., and Wilson I.A. Structural studies of human HIV-1 V3 antibodies. Hum. Antibodies 14 (2005) 73-80
50. Stanfield R.L., Gorny M.K., Williams C., Zolla-Pazner S., and Wilson I.A. Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure 12 (2004) 193-204
51. Stanfield R.L., Gorny M.K., Zolla-Pazner S., and Wilson I.A. Crystal structures of human immunodeficiency virus type 1 (HIV-1) neutralizing antibody 2219 in complex with three different V3 peptides reveal a new binding mode for HIV-1 cross-reactivity. J. Virol. 80 (2006) 6093-6105
52. Teng N.N., Lam K.S., Calvo Riera F., and Kaplan H.S. Construction and testing of mouse-human heteromyelomas for human monoclonal antibody production. Proc. Natl. Acad. Sci. USA 80 (1983) 7308-7312
53. Vogel T., Kurth R., and Norley S. The majority of neutralizing Abs in HIV-1-infected patients recognize linear V3 loop sequences. Studies using HIV-1MN multiple antigenic peptides. J. Immunol. 153 (1994) 1895-1904
54. Wyatt R., and Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 (1998) 1884-1888
55. Zolla-Pazner S. Identifying epitopes of HIV-1 that induce protective antibodies. Nat. Rev. Immunol. 4 (2004) 199-210
56. Zolla-Pazner S. Improving on nature: focusing the immune response on the V3 loop. Hum. Antibodies 14 (2005) 69-72
57. Zolla-Pazner S., Zhong P., Revesz K., Volsky B., Williams C., Nyambi P., and Gorny M.K. The cross-clade neutralizing activity of a human monoclonal antibody is determined by the GPGR V3 motif of HIV type 1. AIDS Res. Hum. Retroviruses 20 (2004) 1254-1258
58. Zolla-Pazner S., Cohen S.S., Krachmarov C., Wang S., Pinter A., and Lu S. Focusing the immune response on the V3 loop, a neutralizing epitope of the HIV-1 gp120 envelope. Virology 372 (2008) 233-246
59. Zolla-Pazner S., Cohen S., Pinter A., Krachmarov C., Wrin T., Wang S., and Lu S. Cross-clade neutralizing antibodies against HIV-1 induced in rabbits by focusing the immune response on a neutralizing epitope. Virology 392 (2009) 82-93
60. Zwart G., Langedijk H., van der Hoek L., de Jong J.J., Wolfs T.F., Ramautarsing C., Bakker M., de Ronde A., and Goudsmit J. Immunodominance and antigenic variation of the principal neutralization domain of HIV-1. Virology 181 (1991) 481-489