Computational prediction of broadly neutralizing HIV-1 antibody epitopes from neutralization activity data

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Ferguson, Andrew L ^a   Falkowska, Emilia ^b,c   Walker, Laura M ^c   Seaman, Michael S ^d   Burton, Dennis R ^b,c   Chakraborty, Arup K ^b,e,f  

^a University of Illinois at Urbana Champaign   (United States)

^b HARVARD UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; NEUTRALIZING ANTIBODY;

AMINO ACID SEQUENCE; ANTIBODY STRUCTURE; ANTIGEN STRUCTURE; ARTICLE; CONTROLLED STUDY; DATA ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; MATHEMATICAL COMPUTING; NONHUMAN; PREDICTION; PROCESS DEVELOPMENT; PROTEIN CONFORMATION; THEORETICAL STUDY; VIRUS NEUTRALIZATION; VIRUS SPIKE;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; EPITOPES; HIV ANTIBODIES; HIV-1; HUMANS; MODELS, MOLECULAR; PREDICTIVE VALUE OF TESTS; PROTEIN CONFORMATION;

EID: 84891813057     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080562     Document Type: Article

References (79)

1. De Cock KM, Jaffe HW, Curran JW (2011) Reflections on 30 years of AIDS. Emerging Infectious Diseases 17: 1044-1048.
2. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. New England Journal of Medicine 361: 2209-2220.
3. Plotkin SA (2010) Correlates of protection induced by vaccination. Clinical and Vaccine Immunology 17: 1055-1065.
4. Plotkin SA (2008) Correlates of vaccine-induced immunity. Clinical infectious diseases 47: 401-409.
5. Amanna IJ, Messaoudi I, Slifka MK (2008) Protective immunity following vaccination: how is it defined? Human Vaccines 4: 316-319.
6. Robbins JB, Schneerson R, Szu SC (1995) Perspective: hypothesis: serum IgG antibody is sufficient to confer protection against infectious diseases by inactivating the inoculum. Journal of Infectious Diseases 171: 1387-1398.
7. Mascola JR, Lewis MG, Stiegler G, Harris D, VanCott TC, et al. (1999) Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6 PD by passive transfer of neutralizing antibodies. Journal of Virology 73: 4009-4018.
8. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, et al. (2000) Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nature Medicine 6: 207-210.
9. Parren PW, Marx PA, Hessell AJ, Luckay A, Harouse J, et al. (2001) Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. Journal of Virology 75: 8340-8347.
10. Hessell AJ, Rakasz EG, Tehrani DM, Huber M, Weisgrau KL, et al. (2010) Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. Journal of Virology 84: 1302-1313.
11. Hessell AJ, Rakasz EG, Poignard P, Hangartner L, Landucci G, et al. (2009) Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathogens 5: e1000433.
12. Moldt B, Rakasz EG, Schultz N, Chan-Hui P-Y, Swiderek K, et al. (2012) Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proceedings of the National Academy of Sciences of the United States of America 109: 18921-18925.
13. Nishimura Y, Igarashi T, Haigwood NL, Sadjadpour R, Donau OK, et al. (2003) Transfer of neutralizing IgG to macaques 6 h but not 24 h after SHIV infection confers sterilizing protection: implications for HIV-1 vaccine development. Proceedings of the National Academy of Sciences of the United States of America 100: 15131-15136.
14. Stamatatos L, Morris L, Burton DR, Mascola JR (2009) Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nature Medicine 15: 866-870.
15. Walker BD, Burton DR (2008) Toward an AIDS vaccine. Science 320: 760-764.
16. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, et al. (2012) A blueprint for HIV vaccine discovery. Cell Host & Microbe 12: 396-407.
17. Kwong PD, Mascola JR (2012) Human Antibodies that Neutralize HIV-1: Identification, Structures, and B Cell Ontogenies. Immunity 37: 412-425.
18. Schief WR, Ban Y-EA, Stamatatos L (2009) Challenges for structure-based HIV vaccine design. Current Opinion in HIV and AIDS 4: 431-440.
19. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
20. Westwood OMR, Hay FC (2001) Epitope Mapping: A practical approach. Oxford: Oxford University Press. 284 p.
21. Mayrose I, Shlomi T, Rubinstein ND, Gershoni JM, Ruppin E, et al. (2007) Epitope mapping using combinatorial phage-display libraries: a graph-based algorithm. Nucleic Acids Research 35: 69-78.
22. Paes C, Ingalls J, Kampani K, Sulli C, Kakkar E, et al. (2009) Atomic-level mapping of antibody epitopes on a GPCR. Journal of the American Chemical Society 131: 6952-6954.
23. Lafuente EM, Reche PA (2009) Prediction of MHC-peptide binding: a systematic and comprehensive overview. Current Pharmaceutical Design 15: 3209-3220.
24. You L, Zhang P, Boden M, Brusic V (2007) Understanding prediction systems for HLA-binding peptides and T-cell epitope identification. In: Rajapakse, J C., Schmidt, B, Volkert, G., editors. Pattern Recognition in Bioinformatics (2nd IAPR International Workshop). Berlin Heidelberg: Springer. 337-348.
25. Bublil EM, Freund NT, Mayrose I, Penn O, Roitburd-Berman A, et al. (2007) Stepwise prediction of conformational discontinuous B-cell epitopes using the Mapitope algorithm. Proteins: Structure, Function, and Bioinformatics 68: 294-304.
26. Yamaguchi-Kabata Y, Gojobori T (2000) Reevaluation of amino acid variability of the human immunodeficiency virus type 1 gp120 envelope glycoprotein and prediction of new discontinuous epitopes. Journal of Virology 74: 4335-4350.
27. Söllner J, Mayer B (2006) Machine learning approaches for prediction of linear B-cell epitopes on proteins. Journal of Molecular Recognition 19: 200-208.
28. Wu TT, Johnson G (2004) HIV vaccine candidates. Drugs of Today 40: 949-955.
29. EL-Manzalawy Y, Honavar V (2010) Recent advances in B-cell epitope prediction methods. Immunome Research 6: 1-9.
30. Taylor PD, Flower DR (2007) Immunoinformatics and Computational Vaccinology: A Brief Introduction. In: Flower, D R., Timmis, J., editors. In Silico Immunology New York: Springer. pp. 23-46.
31. Ponomarenko JV, Van Regenmortel MHV (2009) B cell epitope prediction. Structural Bioinformatics : 849-879.
32. Davies MN, Flower DR (2007) Harnessing bioinformatics to discover new vaccines. Drug Discovery Today 12: 389-395.
33. Pancera M, Majeed S, Ban Y-EA., Chen L, Huang C-C, et al. (2010) Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proceedings of the National Academy of Sciences of the United States of America 107: 1166-1171.
34. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
35. Mao Y, Wang L, Gu C, Herschhorn A, Xiang S-H, et al. (2012) Subunit organization of the membrane-bound HIV-1 envelope glycoprotein trimer. Nature Structural and Molecular Biology 19: 893-899.
36. Enshell-Seijffers D, Denisov D, Groisman B, Smelyanski L, Meyuhas R, et al. (2003) The mapping and reconstitution of a conformational discontinuous B-cell epitope of HIV-1. Journal of Molecular Biology 334: 87-101.
37. Bublil EM, Yeger-Azuz S, Gershoni JM (2006) Computational prediction of the cross-reactive neutralizing epitope corresponding to the monoclonal antibody b12 specific for HIV-1 gp120. The FASEB Journal 20: 1762-1774.
38. Bhasin M, Raghava GPS (2004) Prediction of CTL epitopes using QM, SVM and ANN techniques. Vaccine 22: 3195-3204.
39. Candès EJ, Wakin MB (2008) An introduction to compressive sampling. IEEE Signal Processing Magazine 25: 21-30.
40. Rossi F, Lendasse A, Francois D, Wertz V, Verleysen M (2006) Mutual information for the selection of relevant variables in spectrometric nonlinear modelling. Chemometrics and Intelligent Laboratory Systems 80: 215-226.
41. AlQuraishi M, McAdams HH (2011) Direct inference of protein-DNA interactions using compressed sensing methods. Proceedings of the National Academy of Sciences of the United States of America 108: 14819-14824.
42. Wright J, Yang AY, Ganesh A, Sastry SS, Ma Y (2009) Robust face recognition via sparse representation. IEEE Transactions on Pattern Analysis and Machine Intelligence 31: 210-227.
43. Duarte MF, Davenport MA, Takhar D, Laska JN, Sun T, et al. (2008) Single-pixel imaging via compressive sampling. IEEE Signal Processing Magazine 25: 83-91.
44. nd Ed). Hoboken: John Wiley & Sons. 776 p.
45. Dunn SD, Wahl LM, Gloor GB (2008) Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction. Bioinformatics 24: 333-340.
46. Martin LC, Gloor GB, Dunn SD, Wahl LM (2005) Using information theory to search for co-evolving residues in proteins. Bioinformatics 21: 4116-4124.
47. Doytchinova IA, Flower DR (2007) Predicting class I major histocompatibility complex (MHC) binders using multivariate statistics: comparison of discriminant analysis and multiple linear regression. Journal of Chemical Information and Modeling 47: 234-238.
48. Söllner J (2006) Selection and combination of machine learning classifiers for prediction of linear B-cell epitopes on proteins. Journal of Molecular Recognition 19: 209-214.
49. Cunningham BC, Wells JA (1993) Comparison of a structural and a functional epitope. Journal of Molecular Biology 234: 554-563.
50. Lavoie TB, Kam-Morgan LNW, Hartman AB, Mallett CP, Sheriff S, et al. (1989) Structure-Function Relationships in High Affinity Antibodies to Lysozyme. In: Smith-Gill, S J., Sercarz, E E., editors. The Immune Response to Structurally Defined Proteins: The Lysozyme Model. Schenectady: Adenine Press. pp. 151-168.
51. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, et al. (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466-470.
52. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang P-S, et al. (2011) A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334: 1097-1103.
53. Zou H, Hastie T (2005) Regularization and variable selection via the elastic net. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 67: 301-320.
54. Postler TS, Desrosiers RC (2013) The tale of the long tail: the cytoplasmic domain of HIV-1 gp41. Journal of Virology 87: 2-15.
55. Kalia V, Sarkar S, Gupta P, Montelaro RC (2005) Antibody neutralization escape mediated by point mutations in the intracytoplasmic tail of human immunodeficiency virus type 1 gp41. Journal of Virology 79: 2097-2107.
56. Trkola A, Purtscher M, Muster T, Ballaun C, Buchacher A, et al. (1996) Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. Journal of Virology 70: 1100-1108.
57. Binley JM, Ban YEA, Crooks ET, Eggink D, Osawa K, et al. (2010) Role of complex carbohydrates in human immunodeficiency virus type 1 infection and resistance to antibody neutralization. Journal of Virology 84: 5637-5655.
58. McLellan JS, Pancera M, Carrico C, Gorman J, Julien J-P, et al. (2011) Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480: 336-343.
59. Walker LM, Phogat SK, Chan-Hui P-Y, Wagner D, Phung P, et al. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326: 285-289.
60. Julien J-P, Lee JH, Cupo A, Murin CD, Derking R, et al. (2013) Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proceedings of the National Academy of Sciences of the United States of America 110: 4351-4356.
61. Perez-Sweeney B, DeSalle R, Ho JL (2010) An introduction to a novel population genetic approach for HIV characterization. Infection, Genetics and Evolution 10: 1155-1164.
62. Crawley MJ (2011) Statistics: An Introduction using R. ChichesterEngland: John Wiley & Sons. 342 p.
63. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57: 289-300.
64. Sok D, Doores KJ, Briney B, Le KM, Saye KF, et al. (in preparation) Promiscuous glycan recognition by antibodies to the high-mannose patch of gp120 facilitates broad neutralization of HIV.
65. Dossal C, Peyré G, Fadili J (2010) A numerical exploration of compressed sampling recovery. Linear Algebra and its Applications 432: 1663-1679.
66. Foucart S, Lai MJ (2009) Sparsest solutions of underdetermined linear systems via lq-minimization for 0
67. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, et al. (2005) Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. Journal of Virology 79: 10108-10125.
68. Pantophlet R, Ollmann Saphire E, Poignard P, Parren PWHI, Wilson IA, et al. (2003) Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. Journal of Virology 77: 642-658.
69. Hoffman NG, Schiffer CA, Swanstrom R (2003) Covariation of amino acid positions in HIV-1 protease. Virology 314: 536-548.
70. Doytchinova IA, Blythe MJ, Flower DR (2002) Additive method for the prediction of protein-peptide binding affinity. Application to the MHC class I molecule HLA-A*0201. Journal of Proteome Research 1: 263-272.
71. Doytchinova IA, Walshe V, Borrow P, Flower DR (2005) Towards the chemometric dissection of peptide-HLA-A*0201 binding affinity: comparison of local and global QSAR models. Journal of Computer-Aided Molecular Design 19: 203-212.
72. Efron B, Hastie T, Johnstone I, Tibshirani R (2004) Least angle regression. The Annals of Statistics 32: 407-451.
73. Baraniuk RG (2007) Compressive sensing. IEEE Signal Processing Magazine 24: 118-121.
74. Divekar A, Ersoy O (2010) Theory and Applications of Compressive Sensing. ECE Technical Reports. Paper 402. 66 p. Available: http://docs.lib.purdue.edu/ ecetr/402. Accessed 29 March 2013.
75. Figueiredo MAT, Nowak RD, Wright SJ (2007) Gradient projection for sparse reconstruction: Application to compressed sensing and other inverse problems. IEEE Journal of Selected Topics in Signal Processing 1: 586-597.
76. Tibshirani R (1996) Regression shrinkage and selection via the lasso. Journal of the Royal Statistical Society. Series B (Methodological) 58: 267-288.
77. Salvador S, Chan P (2004) Determining the number of clusters/segments in hierarchical clustering/segmentation algorithms. Proceedings of the 16th IEEE International Conference on Tools with Artificial Intelligence 576-584.
78. nd Ed). New York: Springer. 746 p.
79. Sjöstrand K (2005) Matlab implementation of LASSO, LARS, the elastic net and SPCA (v.2). Informatics and Mathematical Modelling, Technical University of Denmark. Available: http://www2.imm.dtu.dk/pubdb/p.php?3897. Accessed 29 March 2013.