Affinity maturation in an HIV broadly neutralizing B-cell lineage through reorientation of variable domains

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

Volumn 111, Issue 28, 2014, Pages 10275-10280

  Fera, Daniela ^a   Schmidt, Aaron G ^a   Haynes, Barton F ^c   Gao, Feng ^c   Liao, Hua Xin ^c   Kepler, Thomas B ^d   Harrison, Stephen C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BOSTON UNIVERSITY   (United States)

Author keywords

Antibody structure; HIV gp120; Protein evolution; Somatic hypermutation

Indexed keywords

CD4 ANTIGEN; GLYCOPROTEIN GP 120;

ANTIBODY AFFINITY; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL LINEAGE; CELL MATURATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS; HYDROGEN BOND; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION;

ANTIBODY STRUCTURE; HIV GP120; PROTEIN EVOLUTION; SOMATIC HYPERMUTATION;

ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTES; BINDING SITES; CELL LINE; CRYSTALLOGRAPHY, X-RAY; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84904361849     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1409954111     Document Type: Article

References (35)

1. Stamatatos L, Morris L, Burton DR, Mascola JR (2009) Neutralizing antibodies generated during natural HIV-1 infection: Good news for an HIV-1 vaccine? Nat Med 15(8):866-870.
2. Doria-Rose NA, et al. (2009) Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J Virol 83(1):188-199.
3. Simek MD, et al. (2009) Human immunodeficiency virus type 1 elite neutralizers: Individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J Virol 83(14):7337-7348.
4. Kwong PD, Mascola JR, Nabel GJ (2013) Broadly neutralizing antibodies and the search for an HIV-1 vaccine: The end of the beginning. Nat Rev Immunol 13(9):693-701.
5. Julien JP, Lee PS, Wilson IA (2012) Structural insights into key sites of vulnerability on HIV-1 Env and influenza HA. Immunol Rev 250(1):180-198.
6. Eisen HN, Siskind GW (1964) Variations in affinities of antibodies during the immune response. Biochemistry 3:996-1008.
7. McKean D, et al. (1984) Generation of antibody diversity in the immune response of BALB/c mice to influenza virus hemagglutinin. Proc Natl Acad Sci USA 81(10):3180-3184. (Pubitemid 14110702)
8. Jacob J, Kelsoe G, Rajewsky K, Weiss U (1991) Intraclonal generation of antibody mutants in germinal centres. Nature 354(6352):389-392. (Pubitemid 21896846)
9. Liao HX, et al. (2009) High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J Virol Methods 158(1-2):171-179.
10. Wardemann H, et al. (2003) Predominant autoantibody production by early human B cell precursors. Science 301(5638):1374-1377. (Pubitemid 37075812)
11. Wrammert J, et al. (2008) Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453(7195):667-671. (Pubitemid 351769295)
12. Haynes BF, Kelsoe G, Harrison SC, Kepler TB (2012) B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat Biotechnol 30(5):423-433.
13. Liao HX, et al.; NISC Comparative Sequencing Program (2013) Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496(7446):469-476.
14. Kepler TB (2013) Reconstructing a B-cell clonal lineage. I. Statistical inference of unobserved ancestors [v1; ref status: indexed, http://f1000r.es/z6] . F1000Research 2:103.
15. Gao F, et al. (2014) Cooperation of B cell lineages in induction of HIV broad neutralizing antibodies. Cell, in press.
16. Zhou T, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329(5993):811-817.
17. Doria-Rose NA, et al.; NISC Comparative Sequencing Program (2014) Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509(7498):55-62.
18. Schmidt AG, et al. (2013) Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody. Proc Natl Acad Sci USA 110(1):264-269.
19. Hsu HJ, et al. (2014) Antibody variable domain interface and framework sequence requirements for stability and function by high-throughput experiments. Structure 22(1):22-34.
20. Narayanan A, Sellers BD, Jacobson MP (2009) Energy-based analysis and prediction of the orientation between light- and heavy-chain antibody variable domains. J Mol Biol 388(5):941-953.
21. Wu TT, Kabat EA (1970) An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J Exp Med 132(2):211-250.
22. Wagner SD, Milstein C, Neuberger MS (1995) Codon bias targets mutation. Nature 376(6543):732.
23. Klein F, et al. (2013) Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 153(1):126-138.
24. Sabin C, et al. (2010) Crystal structure and size-dependent neutralization properties of HK20, a human monoclonal antibody binding to the highly conserved heptad repeat 1 of gp41. PLoS Pathog 6(11):e1001195.
25. Corti D, et al. (2011) A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333(6044):850-856.
26. 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.
27. Kong L, et al. (2013) Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol 20(7):796-803.
28. Hong M, et al. (2013) Antibody recognition of the pandemic H1N1 Influenza virus hemagglutinin receptor binding site. J Virol 87(22):12471-12480.
29. Zhou T, et al.; NISC Comparative Sequencing Program (2013) Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39(2):245-258.
30. 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.
31. West AP, Jr., Diskin R, Nussenzweig MC, Bjorkman PJ (2012) Structural basis for germline gene usage of a potent class of antibodies targeting the CD4-binding site of HIV-1 gp120. Proc Natl Acad Sci USA 109(30):E2083-E2090.
32. Morea V, Tramontano A, Rustici M, Chothia C, Lesk AM(1998) Conformations of the third hypervariable region in the VH domain of immunoglobulins. J Mol Biol 275(2):269-294. (Pubitemid 28030004)
33. Lyumkis D, et al. (2013) Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342(6165):1484-1490.
34. Julien JP, et al. (2013) Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342(6165):1477-1483.
35. 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.