Affinity improvement of a therapeutic antibody by structure-based computational design: Generation of electrostatic interactions in the transition state stabilizes the antibody-antigen complex

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Kiyoshi, Masato ^a   Caaveiro, Jose M M ^a   Miura, Eri ^a   Nagatoishi, Satoru ^a   Nakakido, Makoto ^a   Soga, Shinji ^b   Shirai, Hiroki ^b   Kawabata, Shigeki ^b   Tsumoto, Kouhei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b ASTELLAS PHARMA INC   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

11K2 ANTIBODY; ANTIBODY; ARGININE; ASPARTIC ACID; GLUTAMIC ACID; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG;

ANTIBODY AFFINITY; ANTIBODY ENGINEERING; ANTIGEN ANTIBODY COMPLEX; ARTICLE; BINDING AFFINITY; COMPUTER MODEL; DRUG SCREENING; DRUG STRUCTURE; IN VITRO STUDY; MUTATION; PREDICTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE; THERMODYNAMICS; WILD TYPE;

ANTIBODIES; ANTIBODY AFFINITY; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS; CHEMOKINE CCL2; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84900334163     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087099     Document Type: Article

References (45)

1. Adair JR (1992) Engineering antibodies for therapy. Immunol Rev 130: 5-40.
2. Lawson AD (2012) Antibody-enabled small-molecule drug discovery. Nat Rev Drug Discov 11: 519-525.
3. Muda M, Gross AW, Dawson JP, He C, Kurosawa E, et al. (2011) Therapeutic assessment of SEED: a new engineered antibody platform designed to generate mono- and bispecific antibodies. Protein Eng Des Sel 24: 447-454.
4. Beck A (2011) Biosimilar, biobetter and next generation therapeutic antibodies. MAbs 3: 107-110.
5. Kawa S, Onda M, Ho M, Kreitman RJ, Bera TK, et al. (2011) The improvement of an anti-CD22 immunotoxin: conversion to single-chain and disulfide stabilized form and affinity maturation by alanine scan. MAbs 3: 479-486.
6. Constantinou A, Epenetos AA, Hreczuk-Hirst D, Jain S, Deonarain MP (2008) Modulation of antibody pharmacokinetics by chemical polysialylation. Bioconjug Chem 19: 643-650. (Pubitemid 351431395)
7. Hagihara Y, Saerens D (2012) Improvement of single domain antibody stability by disulfide bond introduction. Methods Mol Biol 911: 399-416.
8. Renaut L, Monnet C, Dubreuil O, Zaki O, Crozet F, et al. (2012) Affinity maturation of antibodies: optimized methods to generate high-quality ScFv libraries and isolate IgG candidates by high-throughput screening. Methods Mol Biol 907: 451-461.
9. Acchione M, Kwon H, Jochheim CM, Atkins WM (2012) Impact of linker and conjugation chemistry on antigen binding, Fc receptor binding and thermal stability of model antibody-drug conjugates. MAbs 4: 362-372.
10. Shiroishi M, Tsumoto K, Tanaka Y, Yokota A, Nakanishi T, et al. (2007) Structural consequences of mutations in interfacial Tyr residues of a protein antigen-antibody complex. The case of HyHEL-10-HEL. J Biol Chem 282: 6783-6791. (Pubitemid 47100841)
11. 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.
12. Park H, Jeon YH (2011) Free energy perturbation approach for the rational engineering of the antibody for human hepatitis B virus. J Mol Graph Model 29: 643-649.
13. Kuroda D, Shirai H, Jacobson MP, Nakamura H (2012) Computer-aided antibody design. Protein Eng Des Sel 25: 507-521.
14. Kusano KF, Nakamura K, Kusano H, Nishii N, Banba K, et al. (2004) Significance of the level of monocyte chemoattractant protein-1 in human atherosclerosis. Circ J 68: 671-676.
15. Tominaga T, Miyazaki D, Sasaki S, Mihara S, Komatsu N, et al. (2009) Blocking mast cell-mediated type I hypersensitivity in experimental allergic conjunctivitis by monocyte chemoattractant protein-1/CCR2. Invest Ophthalmol Vis Sci 50: 5181-5188.
16. Hayashida K, Nanki T, Girschick H, Yavuz S, Ochi T, et al. (2001) Synovial stromal cells from rheumatoid arthritis patients attract monocytes by producing MCP-1 and IL-8. Arthritis Res 3: 118-126. (Pubitemid 32237038)
17. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242. (Pubitemid 30047768)
18. Reid C, Rushe M, Jarpe M, van Vlijmen H, Dolinski B, et al. (2006) Structure activity relationships of monocyte chemoattractant proteins in complex with a blocking antibody. Protein Eng Des Sel 19: 317-324. (Pubitemid 43999642)
19. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797. (Pubitemid 47321791)
20. Kabat E, Wu TT, Perry H, Gottesman K, Foeller C (1991) Sequences of proteins of immunological interest. Bethesda, National Institutes of Health, 2719 p.
21. Chothia C, Lesk AM (1987) Canonical structures for the hypervariable regions of immunoglobulins. J Mol Biol 196: 901-917. (Pubitemid 17127946)
22. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5.6.
23. Nagao C, Izako N, Soga S, Khan SH, Kawabata S, et al. (2012) Computational design, construction, and characterization of a set of specificity determining residues in protein-protein interactions. Proteins 80: 2426-2436.
24. Umetsu M, Tsumoto K, Hara M, Ashish K, Goda S, et al. (2003) How additives influence the refolding of immunoglobulin-folded proteins in a stepwise dialysis system. Spectroscopic evidence for highly efficient refolding of a single-chain Fv fragment. J Biol Chem 278: 8979-8987. (Pubitemid 36800375)
25. Tsumoto K, Shinoki K, Kondo H, Uchikawa M, Juji T, et al. (1998) Highly efficient recovery of functional single-chain Fv fragments from inclusion bodies overexpressed in Escherichia coli by controlled introduction of oxidizing reagent - application to a human single-chain Fv fragment. J Immunol Methods 219: 119-129. (Pubitemid 28513157)
26. Morton TA, Myszka DG (1998) Kinetic analysis of macromolecular interactions using surface plasmon resonance biosensors. Methods Enzymol 295: 268-294. (Pubitemid 29349918)
27. Ross PD, Subramanian S (1981) Thermodynamics of protein association reactions: forces contributing to stability. Biochemistry 20: 3096-3102.
28. Sakamoto S, Caaveiro JM, Sano E, Tanaka Y, Kudou M, et al. (2009) Contributions of interfacial residues of human Interleukin15 to the specificity and affinity for its private alpha-receptor. J Mol Biol 389: 880-894.
29. Cleland WW, Northrop DB (1999) Energetics of substrate binding, catalysis, and product release. Methods Enzymol 308: 3-27. (Pubitemid 29418897)
30. Lutgens E, Faber B, Schapira K, Evelo CT, van Haaften R, et al. (2005) Gene profiling in atherosclerosis reveals a key role for small inducible cytokines: validation using a novel monocyte chemoattractant protein monoclonal antibody. Circulation 111: 3443-3452. (Pubitemid 40923398)
31. Lippow SM, Wittrup KD, Tidor B (2007) Computational design of antibody-affinity improvement beyond in vivo maturation. Nat Biotechnol 25: 1171-1176. (Pubitemid 47538113)
32. Marvin JS, Lowman HB (2003) Redesigning an antibody fragment for faster association with its antigen. Biochemistry 42: 7077-7083. (Pubitemid 36706491)
33. 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.
34. Midelfort KS, Hernandez HH, Lippow SM, Tidor B, Drennan CL, et al. (2004) Substantial energetic improvement with minimal structural perturbation in a high affinity mutant antibody. J Mol Biol 343: 685-701. (Pubitemid 39311615)
35. Selzer T, Albeck S, Schreiber G (2000) Rational design of faster associating and tighter binding protein complexes. Nat Struct Biol 7: 537-541. (Pubitemid 30445907)
36. Schreiber G, Haran G, Zhou HX (2009) Fundamental aspects of protein-protein association kinetics. Chem Rev 109: 839-860.
37. Northrup SH, Boles JO, Reynolds JC (1988) Brownian dynamics of cytochrome c and cytochrome c peroxidase association. Science 241: 67-70.
38. Schreiber G (2002) Kinetic studies of protein-protein interactions. Curr Opin Struct Biol 12: 41-47.
39. Volkov AN, Worrall JA, Holtzmann E, Ubbink M (2006) Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc Natl Acad Sci U S A 103: 18945-18950. (Pubitemid 350002808)
40. James LC, Tawfik DS (2005) Structure and kinetics of a transient antibody binding intermediate reveal a kinetic discrimination mechanism in antigen recognition. Proc Natl Acad Sci U S A 102: 12730-12735. (Pubitemid 41279434)
41. Lipschultz CA, Yee A, Mohan S, Li Y, Smith-Gill SJ (2002) Temperature differentially affects encounter and docking thermodynamics of antibody - antigen association. J Mol Recognit 15: 44-52. (Pubitemid 34220202)
42. Chodera JD, Mobley DL (2013) Entropy-enthalpy compensation: role and ramifications in biomolecular ligand recognition and design. Annu Rev Biophys 42: 121-142.
43. Baron R, McCammon JA (2013) Molecular recognition and ligand association. Annu Rev Phys Chem 64: 151-175.
44. Dunbrack RL Jr (2002) Rotamer libraries in the 21st century. Curr Opin Struct Biol 12: 431-440.
45. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.