Engineering protein therapeutics: Predictive performances of a structure-based virtual affinity maturation protocol

Journal of Chemical Information and Modeling

Volumn 52, Issue 8, 2012, Pages 2204-2214

  Oberlin, Michael ^a   Kroemer, Romano ^a   Mikol, Vincent ^a   Minoux, Hervé ^a   Tastan, Erdogan ^a   Baurin, Nicolas ^a  

^a SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; FREE ENERGY; PROTEINS;

AFFINITY MATURATION; CONFORMATIONAL SAMPLINGS; DEAD-END ELIMINATION; FREE ENERGY OF BINDING; INTERFACE RESIDUES; PREDICTIVE PERFORMANCE; PROTEIN COMPLEXES; PROTEIN THERAPEUTICS;

BINDING ENERGY;

PROTEIN;

ARTICLE; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER INTERFACE; GENETICS; METABOLISM; METHODOLOGY; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; THERMODYNAMICS;

COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEINS; THERMODYNAMICS; USER-COMPUTER INTERFACE;

EID: 84865478898     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci3001474     Document Type: Article

References (46)

1. Bugelski, P. J.; Martin, P. L. Concordance of preclinical and clinical pharmacology and toxicology of therapeutic monoclonal antibodies and fusion proteins: cell surface targets Br. J. Pharmacol. 2012, 166 (3) 823-846
2. Martin, P. L.; Bugelski, P. J. Concordance of preclinical and clinical pharmacology and toxicology of monoclonal antibodies and fusion proteins: soluble targets Br. J. Pharmacol. 2012, 166 (3) 806-822
3. Honig, P. K. The right medicines - just not enough of them Clin. Pharmacol. Ther. 2012, 91 (3) 369-372
4. Reichert, J. M. Monoclonal antibodies as innovative therapeutics Curr. Pharm. Biotechnol. 2008, 9 (6) 423-430
5. Levin, A. M.; Weiss, G. A. Optimizing the affinity and specificity of proteins with molecular display Mol. Biosyst. 2006, 2 (1) 49-57
6. Zhu, Z.; Hattori, K.; Zhang, H.; Jimenez, X.; Ludwig, D. L.; Dias, S.; Kussie, P.; Koo, H.; Kim, H. J.; Lu, D.; Liu, M.; Tejada, R.; Friedrich, M.; Bohlen, P.; Witte, L.; Rafii, S. Inhibition of human leukemia in an animal model with human antibodies directed against vascular endothelial growth factor receptor 2. Correlation between antibody affinity and biological activity Leukemia 2003, 17 (3) 604-611 (Pubitemid 36395655)
7. Wu, T. T.; Kabat, E. A. 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. 1970, 132 (2) 211-250
8. Foote, J.; Winter, G. Antibody framework residues affecting the conformation of the hypervariable loops J. Mol. Biol. 1992, 224 (2) 487-499
9. Chen, R.; Tong, W.; Mintseris, J.; Li, L.; Weng, Z. ZDOCK predictions for the CAPRI challenge Proteins 2003, 52 (1) 68-73 (Pubitemid 36648852)
10. Stura, E. A.; Graille, M.; Housden, N. G.; Gore, M. G. Protein L mutants for the crystallization of antibody fragments Acta Crystallogr., Sect. D: Biol. Crystallogr. 2002, 58 (Pt 10 Pt 1) 1744-1748 (Pubitemid 35181082)
11. Voigt, C. A.; Gordon, D. B.; Mayo, S. L. Trading accuracy for speed: A quantitative comparison of search algorithms in protein sequence design J. Mol. Biol. 2000, 299 (3) 789-803
12. Desmet, J.; De Maeyer, M.; Hazes, B.; Lasters, I. The dead-end elimination theorem and its use in protein side-chain positioning Nature 1992, 356 (6369) 539-542
13. Goldstein, R. F. Efficient rotamer elimination applied to protein side-chains and related spin glasses Biophys. J. 1994, 66 (5) 1335-1340 (Pubitemid 24145131)
14. Leach, A. R.; Lemon, A. P. Exploring the conformational space of protein side chains using dead-end elimination and the A* algorithm Proteins 1998, 33 (2) 227-239 (Pubitemid 28457975)
15. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A.; Cheatham, T. E., 3rd Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33 (12) 889-897 (Pubitemid 32056774)
16. Lippow, S. M.; Wittrup, K. D.; Tidor, B. Computational design of antibody-affinity improvement beyond in vivo maturation Nat. Biotechnol. 2007, 25 (10) 1171-1176 (Pubitemid 47538113)
17. Clark, L. A.; Boriack-Sjodin, P. A.; Eldredge, J.; Fitch, C.; Friedman, B.; Hanf, K. J.; Jarpe, M.; Liparoto, S. F.; Li, Y.; Lugovskoy, A.; Miller, S.; Rushe, M.; Sherman, W.; Simon, K.; Van Vlijmen, H. Affinity enhancement of an in vivo matured therapeutic antibody using structure-based computational design Protein Sci. 2006, 15 (5) 949-960
18. Huang, N.; Shoichet, B. K.; Irwin, J. J. Benchmarking sets for molecular docking J. Med. Chem. 2006, 49 (23) 6789-6801 (Pubitemid 44749746)
19. Cross, S.; Baroni, M.; Carosati, E.; Benedetti, P.; Clementi, S. FLAP: GRID molecular interaction fields in virtual screening. validation using the DUD data set J. Chem. Inf. Model. 2010, 50 (8) 1442-1450
20. Paulsen, J. L.; Anderson, A. C. Scoring ensembles of docked protein:ligand interactions for virtual lead optimization J. Chem. Inf. Model. 2009, 49 (12) 2813-2819
21. David, M. P.; Asprer, J. J.; Ibana, J. S.; Concepcion, G. P.; Padlan, E. A. A study of the structural correlates of affinity maturation: antibody affinity as a function of chemical interactions, structural plasticity and stability Mol. Immunol. 2007, 44 (6) 1342-1351 (Pubitemid 44415958)
22. Li, L.; Zhao, B.; Cui, Z.; Gan, J.; Sakharkar, M. K.; Kangueane, P. Identification of hot spot residues at protein-protein interface Bioinformation 2006, 1 (4) 121-126
23. Diller, D. J.; Humblet, C.; Zhang, X.; Westerhoff, L. M. Computational alanine scanning with linear scaling semiempirical quantum mechanical methods Proteins 2010, 78 (10) 2329-2337
24. Peled, J. U.; Kuang, F. L.; Iglesias-Ussel, M. D.; Roa, S.; Kalis, S. L.; Goodman, M. F.; Scharff, M. D. The biochemistry of somatic hypermutation Annu. Rev. Immunol. 2008, 26, 481-511 (Pubitemid 351600383)
25. Liu, M.; Schatz, D. G. Balancing AID and DNA repair during somatic hypermutation Trends Immunol. 2009, 30 (4) 173-181
26. Bostrom, J.; Yu, S. F.; Kan, D.; Appleton, B. A.; Lee, C. V.; Billeci, K.; Man, W.; Peale, F.; Ross, S.; Wiesmann, C.; Fuh, G. Variants of the antibody herceptin that interact with HER2 and VEGF at the antigen binding site Science 2009, 323 (5921) 1610-1614
27. Huo, S.; Massova, I.; Kollman, P. A. Computational alanine scanning of the 1:1 human growth hormone-receptor complex J. Comput. Chem. 2002, 23 (1) 15-27 (Pubitemid 34063126)
28. Zoete, V.; Irving, M. B.; Michielin, O. MM-GBSA binding free energy decomposition and T cell receptor engineering J. Mol. Recognit. 2010, 23 (2) 142-152
29. Chaparro-Riggers, J.; Liang, H.; Devay, R. M.; Bai, L.; Sutton, J. E.; Chen, W.; Geng, T.; Lindquist, K.; Casas, M. G.; Boustany, L. M.; Brown, C. L.; Chabot, J.; Gomes, B.; Garzone, P.; Rossi, A.; Strop, P.; Shelton, D.; Pons, J.; Rajpal, A. Increasing Serum Half-life and Extending Cholesterol Lowering in Vivo by Engineering Antibody with pH-sensitive Binding to PCSK9 J. Biol. Chem. 2012, 287 (14) 11090-11097
30. Bhat, T. N.; Bentley, G. A.; Boulot, G.; Greene, M. I.; Tello, D.; Dall'Acqua, W.; Souchon, H.; Schwarz, F. P.; Mariuzza, R. A.; Poljak, R. J. Bound water molecules and conformational stabilization help mediate an antigen-antibody association Proc. Natl. Acad. Sci. U.S.A. 1994, 91 (3) 1089-1093 (Pubitemid 24048514)
31. Braden, B. C.; Souchon, H.; Eisele, J. L.; Bentley, G. A.; Bhat, T. N.; Navaza, J.; Poljak, R. J. Three-dimensional structures of the free and the antigen-complexed Fab from monoclonal anti-lysozyme antibody D44.1 J. Mol. Biol. 1994, 243 (4) 767-781 (Pubitemid 24341717)
32. Li, Y.; Li, H.; Smith-Gill, S. J.; Mariuzza, R. A. Three-dimensional structures of the free and antigen-bound Fab from monoclonal antilysozyme antibody HyHEL-63(,) Biochemistry 2000, 39 (21) 6296-6309 (Pubitemid 30347133)
33. Li, S.; Schmitz, K. R.; Jeffrey, P. D.; Wiltzius, J. J.; Kussie, P.; Ferguson, K. M. Structural basis for inhibition of the epidermal growth factor receptor by cetuximab Cancer Cell 2005, 7 (4) 301-311 (Pubitemid 40544648)
34. Karpusas, M.; Ferrant, J.; Weinreb, P. H.; Carmillo, A.; Taylor, F. R.; Garber, E. A. Crystal structure of the alpha1beta1 integrin I domain in complex with an antibody Fab fragment J. Mol. Biol. 2003, 327 (5) 1031-1041 (Pubitemid 36363710)
35. Buckle, A. M.; Schreiber, G.; Fersht, A. R. Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0-A resolution Biochemistry 1994, 33 (30) 8878-8889 (Pubitemid 24257995)
36. Chemical Computing Group MOE (Molecular Operating Environment), v2009.10; Montreal, Canada, 2009.
37. Labute, P. Protonate3D: assignment of ionization states and hydrogen coordinates to macromolecular structures Proteins 2009, 75 (1) 187-205
38. De Maeyer, M.; Desmet, J.; Lasters, I. All in one: a highly detailed rotamer library improves both accuracy and speed in the modelling of sidechains by dead-end elimination Folding Des. 1997, 2 (1) 53-66 (Pubitemid 127740451)
39. Brooks, B. R.; Brooks, C. L., 3rd; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30 (10) 1545-1614
40. MacKerell, A. D., Jr.; Banavali, N.; Foloppe, N. Development and current status of the CHARMM force field for nucleic acids Biopolymers 2000, 56 (4) 257-265 (Pubitemid 34105873)
41. Case, D. A.; Cheatham, T. E., 3rd; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M., Jr.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26 (16) 1668-1688 (Pubitemid 43076180)
42. Luo, R.; David, L.; Gilson, M. K. Accelerated Poisson-Boltzmann calculations for static and dynamic systems J. Comput. Chem. 2002, 23 (13) 1244-1253 (Pubitemid 35009216)
43. Tan, C.; Tan, Y. H.; Luo, R. Implicit nonpolar solvent models J. Phys. Chem. B 2007, 111 (42) 12263-12274 (Pubitemid 350046101)
44. Li, Y.; Liu, Z.; Wang, R. Test MM-PB/SA on true conformational ensembles of protein-ligand complexes J. Chem. Inf. Model. 2010, 50 (9) 1682-1692
45. Pokala, N.; Handel, T. M. Energy functions for protein design: adjustment with protein-protein complex affinities, models for the unfolded state, and negative design of solubility and specificity J. Mol. Biol. 2005, 347 (1) 203-227 (Pubitemid 40283639)
46. Potapov, V.; Cohen, M.; Schreiber, G. Assessing computational methods for predicting protein stability upon mutation: good on average but not in the details Protein Eng., Des. Sel. 2009, 22 (9) 553-560