Structural analysis of the unmutated ancestor of the HIV-1 envelope V2 region antibody CH58 isolated from an RV144 vaccine efficacy trial vaccinee

EBioMedicine

Volumn 2, Issue 7, 2015, Pages 713-722

  Nicely, Nathan I ^a   Wiehe, Kevin ^a   Kepler, Thomas B ^b   Jaeger, Frederick H ^a   Dennison, S Moses ^a   Rerks Ngarm, Supachai ^c   Nitayaphan, Sorachai ^d   Pitisuttithum, Punnee ^e   Kaewkungwal, Jaranit ^e   Robb, Merlin L ^f   O'Connell, Robert J ^d   Michael, Nelson L ^g   Kim, Jerome H ^g   Liao, Hua Xin ^a   Munir Alam, S ^a   Hwang, Kwan Ki ^a   Bonsignori, Mattia ^a   Haynes, Barton F ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY   (United States)

^c MINISTRY OF PUBLIC HEALTH   (Thailand)

^d ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^e MAHIDOL UNIVERSITY   (Thailand)

^f Henry Jackson Foundation   (United States)

^g WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

Antibody maturation; Germline; Gp120; HIV 1; RV 144; Unmutated ancestor; V2

Indexed keywords

ASPARTIC ACID; GLUTAMIC ACID; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MONOCLONAL ANTIBODY CH58; UNCLASSIFIED DRUG; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; PEPTIDE;

AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY REACTION; APPARENT DISSOCIATION CONSTANT; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CIRCULAR DICHROISM; COMPLEMENTARITY DETERMINING REGION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INTERFEROMETRY; LIGAND BINDING; MATURATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; VACCINATION; VIRUS NEUTRALIZATION; ANTIBODY AFFINITY; CHEMISTRY; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; MUTATION; PROTEIN CONFORMATION; TREATMENT OUTCOME; X RAY CRYSTALLOGRAPHY;

AIDS VACCINES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIBODY AFFINITY; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; EPITOPE MAPPING; HIV ANTIBODIES; HIV ANTIGENS; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDES; PROTEIN CONFORMATION; TREATMENT OUTCOME;

EID: 84951574208     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.06.016     Document Type: Article

References (50)

1. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Alam S.M., McAdams M., Boren D., Rak M., Scearce R.M., Gao F., Camacho Z.T., Gewirth D., Kelsoe G., Chen P., et al. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J. Immunol. 2007, 178:4424-4435.
3. Alam S.M., Liao H.X., Dennison S.M., Jaeger F., Parks R., Anasti K., Foulger A., Donathan M., Lucas J., Verkoczy L., et al. Differential reactivity of germ line allelic variants of a broadly neutralizing HIV-1 antibody to a gp41 fusion intermediate conformation. J. Virol. 2011, 85:11725-11731.
4. Arthos J., Cicala C., Martinelli E., Macleod K., Van Ryk D., Wei D., Xiao Z., Veenstra T.D., Conrad T.P., Lempicki R.A., et al. HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 2008, 9:301-309.
5. Babor M., Kortemme T. Multi-constraint computational design suggests that native sequences of germline antibody H3 loops are nearly optimal for conformational flexibility. Proteins 2009, 75:846-858.
6. Boehr D.D., Nussinov R., Wright P.E. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 2009, 5:789-796.
7. Bonsignori M., Pollara J., Moody M.A., Alpert M.D., Chen X., Hwang K.K., Gilbert P.B., Huang Y., Gurley T.C., Kozink D.M., et al. Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J. Virol. 2012, 86:11521-11532.
8. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:486-501.
9. Fera D., Schmidt A.G., Haynes B.F., Gao F., Liao H.X., Kepler T.B., Harrison S.C. Affinity maturation in an HIV broadly neutralizing B-cell lineage through reorientation of variable domains. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:10275-10280.
10. Foote J., Milstein C. Conformational isomerism and the diversity of antibodies. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10370-10374.
11. Gibbs E., Oger J. A biosensor-based characterization of the affinity maturation of the immune response against interferon-beta and correlations with neutralizing antibodies in treated multiple sclerosis patients. J. Interf. Cytokine Res. 2008, 28:713-723.
12. Gibbs E., Karim M.E., Oger J., the Steering Committee of the B.s. Antibody dissociation rates are predictive of neutralizing antibody (NAb) course: a comparison of interferon beta-1b-treated Multiple Sclerosis (MS) patients with transient versus sustained NAbs. Clin. Immunol. 2014, 157:91-101.
13. Harris L.J., Skaletsky E., McPherson A. Crystallization of intact monoclonal antibodies. Proteins 1995, 23:285-289.
14. Haynes B.F., Gilbert P.B., McElrath M.J., Zolla-Pazner S., Tomaras G.D., Alam S.M., Evans D.T., Montefiori D.C., Karnasuta C., Sutthent R., et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 2012, 366:1275-1286.
15. Jelicic K., Cimbro R., Nawaz F., Huang da W., Zheng X., Yang J., Lempicki R.A., Pascuccio M., Van Ryk D., Schwing C., et al. The HIV-1 envelope protein gp120 impairs B cell proliferation by inducing TGF-beta1 production and FcRL4 expression. Nat. Immunol. 2013, 14:1256-1265.
16. Jimenez R., Salazar G., Baldridge K.K., Romesberg F.E. Flexibility and molecular recognition in the immune system. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:92-97.
17. 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., et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 2013, 342:1477-1483.
18. Karasavvas N., Billings E., Rao M., Williams C., Zolla-Pazner S., Bailer R.T., Koup R.A., Madnote S., Arworn D., Shen X., et al. The Thai Phase III HIV Type 1 Vaccine trial (RV144) regimen induces antibodies that target conserved regions within the V2 loop of gp120. AIDS Res. Hum. Retrovir. 2012, 28:1444-1457.
19. Klein F., Diskin R., Scheid J.F., Gaebler C., Mouquet H., Georgiev I.S., Pancera M., Zhou T., Incesu R.B., Fu B.Z., et al. Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 2013, 153:126-138.
20. Kwong P.D., Mascola J.R. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 2012, 37:412-425.
21. Liao H.X., Sutherland L.L., Xia S.M., Brock M.E., Scearce R.M., Vanleeuwen S., Alam S.M., McAdams M., Weaver E.A., Camacho Z., et al. A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 2006, 353:268-282.
22. 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., et al. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 2013, 38:176-186.
23. Liu P., Williams L.D., Shen X., Bonsignori M., Overman R.G., Moody M.A., Liao H.X., Stieh D.J., McCotter K.L., French A.L., et al. Capacity for infectious HIV-1 virion capture differs by envelope antibody specificity. J. Virol. 2014, 88:5165-5170.
24. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., Richardson J.S., Richardson D.C. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003, 50:437-450.
25. Manivel V., Sahoo N.C., Salunke D.M., Rao K.V. Maturation of an antibody response is governed by modulations in flexibility of the antigen-combining site. Immunity 2000, 13:611-620.
26. Mascola J.R., Haynes B.F. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol. Rev. 2013, 254:225-244.
27. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 1968, 33:491-497.
28. McLellan J.S., Pancera M., Carrico C., Gorman J., Julien J.P., Khayat R., Louder R., Pejchal R., Sastry M., Dai K., et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 2011, 480:336-343.
29. Nicely N.I., Dennison S.M., Spicer L., Scearce R.M., Kelsoe G., Ueda Y., Chen H., Liao H.X., Alam S.M., Haynes B.F. Crystal structure of a non-neutralizing antibody to the HIV-1 gp41 membrane-proximal external region. Nat. Struct. Mol. Biol. 2010, 17:1492-1494.
30. North B., Lehmann A., Dunbrack R.L. A new clustering of antibody CDR loop conformations. J. Mol. Biol. 2011, 406:228-256.
31. Otwinowski A., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods in enzymology 276. Macromol. Crystallogr. A 1997, 307-326.
32. 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., et al. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat. Struct. Mol. Biol. 2013, 20:804-813.
33. Pancera M., Zhou T., Druz A., Georgiev I.S., Soto C., Gorman J., Huang J., Acharya P., Chuang G.Y., Ofek G., et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 2014, 514:455-461.
34. Perez L.G., Chen H., Liao H.X., Montefiori D.C. Envelope glycoprotein binding to the integrin alpha4beta7 is not a general property of most HIV-1 strains. J. Virol. 2014, 88:10767-10777.
35. Rerks-Ngarm S., Pitisuttithum P., Nitayaphan S., Kaewkungwal J., Chiu J., Paris R., Premsri N., Namwat C., de Souza M., Adams E., et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 2009, 361:2209-2220.
36. Rolland M., Edlefsen P.T., Larsen B.B., Tovanabutra S., Sanders-Buell E., Hertz T., deCamp A.C., Carrico C., Menis S., Magaret C.A., et al. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 2012, 490:417-420.
37. Sagawa T., Oda M., Ishimura M., Furukawa K., Azuma T. Thermodynamic and kinetic aspects of antibody evolution during the immune response to hapten. Mol. Immunol. 2003, 39:801-808.
38. Scheid J.F., Mouquet H., Ueberheide B., Diskin R., Klein F., Oliveira T.Y., Pietzsch J., Fenyo D., Abadir A., Velinzon K., et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 2011, 333:1633-1637.
39. Schmidt A.G., Xu H., Khan A.R., O'Donnell T., Khurana S., King L.R., Manischewitz J., Golding H., Suphaphiphat P., Carfi A., et al. Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:264-269.
40. Tassaneetrithep B., Tivon D., Swetnam J., Karasavvas N., Michael N.L., Kim J.H., Marovich M., Cardozo T. Cryptic determinant of alpha4beta7 binding in the V2 loop of HIV-1 gp120. PLoS ONE 2014, 9:e108446.
41. Terwilliger T.C., Grosse-Kunstleve R.W., Afonine P.V., Moriarty N.W., Zwart P.H., Hung L.W., Read R.J., Adams P.D. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 2008, 64:61-69.
42. Urzhumtseva L., Afonine P.V., Adams P.D., Urzhumtsev A. Crystallographic model quality at a glance. Acta Crystallogr. D Biol. Crystallogr. 2009, 65:297-300.
43. 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., et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 2009, 326:285-289.
44. Wiehe K., Easterhoff D., Luo K., Nicely N.I., Bradley T., Jaeger F.H., Dennison S.M., Zhang R., Lloyd K.E., Stolarchuk C., et al. Phylogenetic Conservation of Antibody Light Chain-restricted Recognition of the Site of Immune Pressure in an HIV-1 Vaccine Trial Immunity 2014, (in press).
45. Wu X., Zhou T., Zhu J., Zhang B., Georgiev I., Wang C., Chen X., Longo N.S., Louder M., McKee K., et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 2011, 333:1593-1602.
46. Xu H., Schmidt A.G., O'Donnell T., Therkelsen M.D., Kepler T.B., Moody M.A., Haynes B.F., Liao H., Harrison S.C., Shaw D.E. Key mutations stabilize antigen-binding conformation during affinity maturation of a broadly neutralizing influenza antibody lineage. Proteins 2014, 83:771-780.
47. Zeller Y., Mechtersheimer S., Altevogt P. Critical amino acid residues of the alpha4 subunit for alpha4beta7 integrin function. J. Cell. Biochem. 2001, 83:304-319.
48. Zhou T., Georgiev I., Wu X., Yang Z.Y., Dai K., Finzi A., Kwon Y.D., Scheid J.F., Shi W., Xu L., et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 2010, 329:811-817.
49. Zhou T., Zhu J., Wu X., Moquin S., Zhang B., Acharya P., Georgiev I.S., Altae-Tran H.R., Chuang G.Y., Joyce M.G., et al. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 2013, 39:245-258.
50. Zimmermann J., Oakman E.L., Thorpe I.F., Shi X., Abbyad P., Brooks C.L., Boxer S.G., Romesberg F.E. Antibody evolution constrains conformational heterogeneity by tailoring protein dynamics. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13722-13727.