OptMAVEn - A new framework for the de novo design of antibody variable region models targeting specific antigen epitopes

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Li, Tong ^a   Pantazes, Robert J ^a   Maranas, Costas D ^a  

^a The Pennsylvania State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCOPROTEIN GP 120; HEMAGGLUTININ; ANTIBODY; ANTIGEN; IMMUNOGLOBULIN VARIABLE REGION;

ANTIGEN BINDING; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CONCEPTUAL FRAMEWORK; HUMAN IMMUNODEFICIENCY VIRUS; HYDROGEN BOND; IMMUNOGENICITY; INFLUENZA VIRUS; MATHEMATICAL MODEL; METHODOLOGY; MOLECULAR EVOLUTION; NONHUMAN; OPTIMAL METHOD FOR ANTIBODY VARIABLE REGION ENGINEERING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; VIRUS NEUTRALIZATION; ANTIBODY AFFINITY; CHEMICAL STRUCTURE; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY;

ANTIBODIES; ANTIBODY AFFINITY; ANTIGENS; EPITOPES; HUMANS; IMMUNOGLOBULIN VARIABLE REGION; MODELS, MOLECULAR;

EID: 84937737866     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105954     Document Type: Article

References (66)

1. Beck A, Wurch T, Bailly C, Corvaia N (2010) Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol 10: 345-352.
2. Nelson AL, Reichert JM (2009) Development trends for therapeutic antibody fragments. Nat Biotechnol 27: 331-337.
3. Carter PJ (2006) Potent antibody therapeutics by design. Nat Rev Immunol 6: 343-357.
4. Morrison SL, Johnson MJ, Herzenberg LA, Oi VT (1984) Chimeric human antibody molecules: mouse antigen-binding domains with human constant region domains. Proc Natl Acad Sci U S A 81: 6851-6855. (Pubitemid 15221019)
5. Boulianne GL, Hozumi N, Shulman MJ (1984) Production of functional chimaeric mouse/human antibody. Nature 312: 643-646. (Pubitemid 15218335)
6. Jackel C, Kast P, Hilvert D (2008) Protein design by directed evolution. Annu Rev Biophys 37: 153-173.
7. Hoogenboom HR (2005) Selecting and screening recombinant antibody libraries. Nat Biotechnol 23: 1105-1116.
8. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228: 1315-1317.
9. Hoess RH (2001) Protein design and phage display. Chem Rev 101: 3205-3218.
10. Brenke R, Hall DR, Chuang GY, Comeau SR, Bohnuud T, et al. (2012) Application of asymmetric statistical potentials to antibody-protein docking. Bioinformatics 28: 2608-2614.
11. Chaudhury S, Berrondo M, Weitzner BD, Muthu P, Bergman H, et al. (2011) Benchmarking and analysis of protein docking performance in Rosetta v3.2. PLoS One 6: e22477.
12. Krawczyk K, Baker T, Shi J, Deane CM (2013) Antibody i-Patch prediction of the antibody binding site improves rigid local antibody-antigen docking. Protein Eng Des Sel 26: 621-629.
13. Simonelli L, Pedotti M, Beltramello M, Livoti E, Calzolai L, et al. (2013) Rational engineering of a human anti-dengue antibody through experimentally validated computational docking. PLoS One 8: e55561.
14. Sellers BD, Nilmeier JP, Jacobson MP (2010) Antibodies as a model system for comparative model refinement. Proteins 78: 2490-2505.
15. Sivasubramanian A, Sircar A, Chaudhury S, Gray JJ (2009) Toward high-resolution homology modeling of antibody Fv regions and application to antibody-antigen docking. Proteins 74: 497-514.
16. Li T, Tracka MB, Uddin S, Casas-Finet J, Jacobs DJ, et al. (2014) Redistribution of Flexibility in Stabilizing Antibody Fragment Mutants Follows Le Chatelier's Principle. PLoS One 9: e92870.
17. Li T, Verma D, Tracka MB, Casas-Finet J, Livesay DR, et al. (2013) Thermodynamic Stability and Flexibility Characteristics of Antibody Fragment Complexes. Protein Pept Lett.
18. Lippow SM, Wittrup KD, Tidor B (2007) Computational design of antibody-affinity improvement beyond in vivo maturation. Nat Biotechnol 25: 1171-1176. (Pubitemid 47538113)
19. Barderas R, Desmet J, Timmerman P, Meloen R, Casal JI (2008) Affinity maturation of antibodies assisted by in silico modeling. Proc Natl Acad Sci U S A 105: 9029-9034.
20. Clark LA, Boriack-Sjodin PA, Eldredge J, Fitch C, Friedman B, et al. (2006) Affinity enhancement of an in vivo matured therapeutic antibody using structure-based computational design. Protein Sci 15: 949-960.
21. Pantazes RJ, Maranas CD (2010) OptCDR: a general computational method for the design of antibody complementarity determining regions for targeted epitope binding. Protein Eng Des Sel 23: 849-858.
22. Yu CM, Peng HP, Chen IC, Lee YC, Chen JB, et al. (2012) Rationalization and design of the complementarity determining region sequences in an antibody-antigen recognition interface. PLoS One 7: e33340.
23. Lazar GA, Desjarlais JR, Jacinto J, Karki S, Hammond PW (2007) A molecular immunology approach to antibody humanization and functional optimization. Mol Immunol 44: 1986-1998.
24. Zhang D, Chen CF, Zhao BB, Gong LL, Jin WJ, et al. (2013) A novel antibody humanization method based on epitopes scanning and molecular dynamics simulation. PLoS One 8: e80636.
25. Pantazes RJ, Maranas CD (2013) MAPs: a database of modular antibody parts for predicting tertiary structures and designing affinity matured antibodies. BMC Bioinformatics 14: 168.
26. Saraf MC, Moore GL, Goodey NM, Cao VY, Benkovic SJ, et al. (2006) IPRO: an iterative computational protein library redesign and optimization procedure. Biophys J 90: 4167-4180. (Pubitemid 43846131)
27. Nielsen M, Lundegaard C, Worning P, Lauemoller SL, Lamberth K, et al. (2003) Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci 12: 1007-1017. (Pubitemid 36505435)
28. Parker AS, Choi Y, Griswold KE, Bailey-Kellogg C (2013) Structure-guided deimmunization of therapeutic proteins. J Comput Biol 20: 152-165.
29. Jardine J, Julien JP, Menis S, Ota T, Kalyuzhniy O, et al. (2013) Rational HIV immunogen design to target specific germline B cell receptors. Science 340: 711-716.
30. Schmidt AG, Xu H, Khan AR, O'Donnell T, Khurana S, et al. (2013) Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody. Proc Natl Acad Sci U S A 110: 264-269.
31. Livesay DR, Subramaniam S (2004) Conserved sequence and structure association motifs in antibody-protein and antibody-hapten complexes. Protein Eng Des Sel 17: 463-472. (Pubitemid 39280047)
32. Jespers LS, Roberts A, Mahler SM, Winter G, Hoogenboom HR (1994) Guiding the selection of human antibodies from phage display repertoires to a single epitope of an antigen. Biotechnology (N Y) 12: 899-903.
33. Liao HX, Lynch R, Zhou T, Gao F, Alam SM, et al. (2013) Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469-476.
34. Abhinandan KR, Martin AC (2007) Analyzing the "degree of humanness" of antibody sequences. J Mol Biol 369: 852-862. (Pubitemid 46709913)
35. Hwang WY, Foote J (2005) Immunogenicity of engineered antibodies. Methods 36: 3-10. (Pubitemid 40558811)
36. Gao SH, Huang K, Tu H, Adler AS (2013) Monoclonal antibody humanness score and its applications. BMC Biotechnol 13: 55.
37. Vanommeslaeghe K, Hatcher E, Acharya C, Kundu S, Zhong S, et al. (2010) CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem 31: 671-690.
38. Ehrenmann F, Giudicelli V, Duroux P, Lefranc MP (2011) IMGT/Collier de Perles: IMGT standardized representation of domains (IG, TR, and IgSF variable and constant domains, MH and MhSF groove domains). Cold Spring Harb Protoc 2011: 726-736.
39. Lefranc MP (2011) IMGT unique numbering for the variable (V), constant (C), and groove (G) domains of IG, TR, MH, IgSF, and MhSF. Cold Spring Harb Protoc 2011: 633-642.
40. Lefranc MP (2011) IMGT Collier de Perles for the variable (V), constant (C), and groove (G) domains of IG, TR, MH, IgSF, and MhSF. Cold Spring Harb Protoc 2011: 643-651.
41. Lefranc MP, Pommie C, Kaas Q, Duprat E, Bosc N, et al. (2005) IMGT unique numbering for immunoglobulin and T cell receptor constant domains and Ig superfamily C-like domains. Dev Comp Immunol 29: 185-203. (Pubitemid 39575119)
42. ILOG (2013) ILOG CPLEX 12.4 User's Manual. ILOG Inc, Mountain View, CA, USA.
43. Willis JR, Briney BS, DeLuca SL, Crowe JE, Jr., Meiler J (2013) Human germline antibody gene segments encode polyspecific antibodies. PLoS Comput Biol 9: e1003045.
44. Yin J, Beuscher AEt, Andryski SE, Stevens RC, Schultz PG (2003) Structural plasticity and the evolution of antibody affinity and specificity. J Mol Biol 330: 651-656.
45. Whittle JR, Zhang R, Khurana S, King LR, Manischewitz J, et al. (2011) Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci U S A 108: 14216-14221.
46. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811-817.
47. Humphris EL, Kortemme T (2007) Design of multi-specificity in protein interfaces. PLoS Comput Biol 3: e164.
48. James LC, Roversi P, Tawfik DS (2003) Antibody multispecificity mediated by conformational diversity. Science 299: 1362-1367. (Pubitemid 36254643)
49. Reche PA, Reinherz EL (2003) Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 331: 623-641. (Pubitemid 36937150)
50. Fleishman SJ, Whitehead TA, Ekiert DC, Dreyfus C, Corn JE, et al. (2011) Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332: 816-821.
51. Lingwood D, McTamney PM, Yassine HM, Whittle JR, Guo X, et al. (2012) Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 489: 566-570.
52. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE Jr, et al. (2010) Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328: 357-360.
53. 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.
54. Walker LM, Phogat SK, Chan-Hui PY, 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.
55. Miller BR, Demarest SJ, Lugovskoy A, Huang F, Wu X, et al. (2010) Stability engineering of scFvs for the development of bispecific and multivalent antibodies. Protein Eng Des Sel 23: 549-557.
56. 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: 693-701.
57. Corti D, Lanzavecchia A (2013) Broadly neutralizing antiviral antibodies. Annu Rev Immunol 31: 705-742.
58. Burkovitz A, Sela-Culang I, Ofran Y (2014) Large-scale analysis of somatic hypermutations in antibodies reveals which structural regions, positions and amino acids are modified to improve affinity. FEBS J 281: 306-319.
59. Wu TT, Johnson G, Kabat EA (1993) Length distribution of CDRH3 in antibodies. Proteins 16: 1-7. (Pubitemid 23129868)
60. Hong M, Lee PS, Hoffman RM, Zhu X, Krause JC, et al. (2013) Antibody recognition of the pandemic H1N1 Influenza virus hemagglutinin receptor binding site. J Virol 87: 12471-12480.
61. Xu R, Krause JC, McBride R, Paulson JC, Crowe JE, Jr., et al. (2013) A recurring motif for antibody recognition of the receptor-binding site of influenza hemagglutinin. Nat Struct Mol Biol 20: 363-370.
62. Einhauer A, Jungbauer A (2001) The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J Biochem Biophys Methods 49: 455-465. (Pubitemid 33022564)
63. Schneider G (2013) De novo molecular design. John Wiley & Sons, Inc: 480.
64. Sciretti D, Bruscolini P, Pelizzola A, Pretti M, Jaramillo A (2009) Computational protein design with side-chain conformational entropy. Proteins 74: 176-191.
65. Lazaridis T, Karplus M (1999) Effective energy function for proteins in solution. Proteins 35: 133-152. (Pubitemid 29165128)
66. Jaramillo A, Wodak SJ (2005) Computational protein design is a challenge for implicit solvation models. Biophys J 88: 156-171. (Pubitemid 40070666)