Molecular simulations of the pairwise interaction of monoclonal antibodies

Journal of Physical Chemistry B

Volumn 118, Issue 46, 2014, Pages 13132-13141

  Lapelosa, Mauro ^a   Patapoff, Thomas W ^a   Zarraga, Isidro E ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; BINDING ENERGY; BOLTZMANN EQUATION; DIMERS; ELECTROSTATICS; MOLECULAR STRUCTURE; MONOCLONAL ANTIBODIES; POISSON EQUATION; SURFACE PLASMON RESONANCE; VAN DER WAALS FORCES; VISCOSITY;

CONFORMATIONAL SAMPLINGS; FREE ENERGY LANDSCAPE; MOLECULAR SIMULATIONS; MONOCLONAL ANTIBODIES (MABS); MOST PROBABLE CONFIGURATIONS; POISSON-BOLTZMANN EQUATIONS; SECOND VIRIAL COEFFICIENTS; VAN DER WAALS INTERACTIONS;

FREE ENERGY;

MONOCLONAL ANTIBODY;

CHEMISTRY; METABOLISM; MOLECULAR DYNAMICS; PH; PRINCIPAL COMPONENT ANALYSIS; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY; THERMODYNAMICS; VISCOSITY;

ANTIBODIES, MONOCLONAL; HYDROGEN-ION CONCENTRATION; MOLECULAR DYNAMICS SIMULATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; THERMODYNAMICS; VISCOSITY;

EID: 84913558330     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp508729z     Document Type: Article

References (53)

1. Harris, R. J.; Shire, S. J.; Winter, C. Commercial Manufacturing Scale Formulation and Analytical Characterization of Therapeutic Recombinant Antibodies. Drug Dev. Res. 2004, 61, 137-154.
2. Shire, S. J.; Shahrokh, Z.; Liu, J. Challenges in the Development of High Protein Concentration Formulations. J. Pharm. Sci. 2004, 93, 1390-1402.
3. Connolly, B. D.; Petry, C.; Yadav, S.; Demeule, B.; Ciaccio, N.; Moore, J. M. R.; Shire, S. J.; Gokarn, Y. R. Weak Interactions Govern the Viscosity of Concentrated Antibody Solutions: High-Throughput Analysis Using the Diffusion Interaction Parameter. Biophys. J. 2012, 103, 69-78.
4. Castellanos, M.; Pathak, J.; Leach, W.; Bishop, S.; Colby, R. Explaining the Non-Newtonian Character of Aggregating Monoclonal Antibody Solutions Using Small-Angle Neutron Scattering. Biophys. J. 2014, 107, 469-476.
5. Yearley, E. J.; Zarraga, I. E.; Shire, S. J.; Scherer, T. M.; Gokarn, Y.; Wagner, N. J.; Liu, Y. Small-Angle Neutron Scattering Characterization of Monoclonal Antibody Conformations and Interactions at High Concentrations. Biophys. J. 2013, 105, 720-731.
6. Jensen, M. R.; Ortega-Roldan, J.-L.; Salmon, L.; van Nuland, N.; Blackledge, M. Characterizing Weak Protein-Protein Complexes by NMR Residual Dipolar Couplings. Eur. Biophys. J. 2011, 40, 1371-1381.
7. Gilson, M. K. Theory of Electrostatic Interactions in Macromolecules. Curr. Opin. Struct. Biol. 1995, 5, 216-223.
8. Janin, J. The Kinetics of Protein-Protein Recognition. Proteins 1997, 28, 153-161.
9. McCoy, A. J.; Chandana Epa, V.; Colman, P. M. Electrostatic Complementarity at Protein-Protein Interfaces. J. Mol. Biol. 1997, 268, 570-584.
10. Carter, P. J. Potent Antibody Therapeutics by Design. Nat. Rev. Immunol. 2006, 6, 343-357.
11. Carter, P. J.; Hazuda, D.; Wells, J. A. Next Generation Therapeutics. Curr. Opin. Chem. Biol. 2013, 17, 317-319.
12. Deperalta, G.; Alvarez, M.; Bechtel, C.; Dong, K.; McDonald, R.; Ling, V. Structural Analysis of a Therapeutic Monoclonal Antibody Dimer by Hydroxyl Radical Footprinting. MAbs 2013, 5, 86-101.
13. Moore, J. M.; Patapoff, T. W.; Cromwell, M. E. Kinetics and Thermodynamics of Dimer Formation and Dissociation for a Recombinant Humanized Monoclonal Antibody to Vascular Endothelial Growth Factor. Biochemistry 1999, 38, 13960-13967.
14. Paul, R.; Graff-Meyer, A.; Stahlberg, H.; Lauer, M. E.; Rufer, A. C.; Beck, H.; Briguet, A.; Schnaible, V.; Buckel, T.; Boeckle, S. Structure and Function of Purified Monoclonal Antibody Dimers Induced by Different Stress Conditions. Pharm. Res. 2012, 29, 2047-2059.
15. Zarraga, I. E.; Taing, R.; Zarzar, J.; Luoma, J.; Hsiung, J.; Patel, A.; Lim, F. J. High Shear Rheology and Anisotropy in Concentrated Solutions of Monoclonal Antibodies. J. Pharm. Sci. 2013, 102, 2538-2549.
16. Lilyestrom, W. G.; Yadav, S.; Shire, S. J.; Scherer, T. M. Monoclonal Antibody Self-Association, Cluster Formation, and Rheology at High Concentrations. J. Phys. Chem. B 2013, 117, 6373-6384.
17. Liu, J.; Nguyen, M. D. H.; Andya, J. D.; Shire, S. J. Reversible Self-Association Increases the Viscosity of a Concentrated Monoclonal Antibody in Aqueous Solution. J. Pharm. Sci. 2005, 94, 1928-1940.
18. Scherer, T. M.; Liu, J.; Shire, S. J.; Minton, A. P. Intermolecular Interactions of IgG1 Monoclonal Antibodies at High Concentrations Characterized by Light Scattering. J. Phys. Chem. B 2010, 114, 12948-12957.
19. Yadav, S.; Liu, J.; Shire, S. J.; Kalonia, D. S. Specific Interactions in High Concentration Antibody Solutions Resulting in High Viscosity. J. Pharm. Sci. 2010, 99, 1152-1168.
20. Yadav, S.; Shire, S. J.; Kalonia, D. S. Factors Affecting the Viscosity in High Concentration Solutions of Different Monoclonal Antibodies. J. Pharm. Sci. 2010, 99, 4812-4829.
21. Yadav, S.; Laue, T. M.; Kalonia, D. S.; Singh, S. N.; Shire, S. J. The Influence of Charge Distribution on Self-Association and Viscosity Behavior of Monoclonal Antibody Solutions. Mol. Pharm. 2012, 9, 791-802.
22. Mandell, J. G.; Roberts, V. A.; Pique, M. E.; Kotlovyi, V.; Mitchell, J. C.; Nelson, E.; Tsigelny, I.; Ten Eyck, L. F. Protein Docking Using Continuum Electrostatics and Geometric Fit. Protein Eng. 2001, 14, 105-113.
23. Smith, G. R.; Sternberg, M. J. Prediction of Protein-Protein Interactions by Docking Methods. Curr. Opin. Struct. Biol. 2002, 12, 28-35.
24. Neal, B. L.; Asthagiri, D.; Lenhoff, A. M. Molecular Origins of Osmotic Second Virial Coefficients of Proteins. Biophys. J. 1998, 75, 2469-2477.
25. Asthagiri, D.; Neal, B. L.; Lenhoff, A. M. Calculation of Short-Range Interactions between Proteins. Biophys. Chem. 1999, 78, 219-231.
26. Elcock, A. H.; McCammon, J. A. Calculation of Weak Protein-Protein Interactions: The pH Dependence of the Second Virial Coefficient. Biophys. J. 2001, 80, 613-625.
27. Elcock, A. H.; Sept, D.; McCammon, J. A. Computer Simulation of Protein-Protein Interactions. J. Phys. Chem. B 2001, 105, 1504-1518.
28. Madura, J. D.; Briggs, J. M.; Wade, R. C.; Davis, M. E.; Luty, B. A.; Ilin, A.; Antosiewicz, J.; Gilson, M. K.; Bagheri, B.; Scott, L. R.; McCammon, J. A. Electrostatics and Diffusion of Molecules in Solution: Simulations with the University of Houston Brownian Dynamics Program. Comput. Phys. Commun. 1995, 91, 57-95.
29. Stark, A. C.; Andrews, C. T.; Elcock, A. H. Toward Optimized Potential Functions for Protein-Protein Interactions in Aqueous Solutions: Osmotic Second Virial Coefficient Calculations Using the MARTINI Coarse-Grained Force Field. J. Chem. Theory Comput. 2013, 9, 4176-4185.
30. Chaudhri, A.; Zarraga, I. E.; Kamerzell, T. J.; Brandt, J. P.; Patapoff, T. W.; Shire, S. J.; Voth, G. A. Coarse-Grained Modeling of the Self-Association of Therapeutic Monoclonal Antibodies. J. Phys. Chem. B 2012, 116, 8045-8057.
31. Baker, N. A. Poisson-Boltzmann Methods for Biomolecular Electrostatics. Methods Enzymol. 2004, 383, 94-118.
32. Gilson, M. K.; Honig, B. Calculation of the Total Electrostatic Energy of a Macromolecular System: Solvation Energies, Binding Energies, and Conformational Analysis. Proteins 1988, 4, 7-18.
33. Nicholls, A.; Honig, B. A Rapid Finite Difference Algorithm, Utilizing Successive Over-Relaxation to Solve the Poisson-Boltzmann Equation. J. Comput. Chem. 1991, 12, 435-445.
34. Saphire, E. O.; Parren, P. W.; Pantophlet, R.; Zwick, M. B.; Morris, G. M.; Rudd, P. M.; Dwek, R. A.; Stanfield, R. L.; Burton, D. R.; Wilson, I. A. Crystal Structure of a Neutralizing Human IGG against HIV-1: a Template for Vaccine Design. Science 2001, 293, 1155-1159.
35. Eswar, N.; Webb, B.; Marti-Renom, M. A.; Madhusudhan, M. S.; Eramian, D.; Shen, M.-Y.; Pieper, U.; Sali, A. Comparative Protein Structure Modeling using Modeller. Curr. Protoc. Bioinf. 2006, Chapter 5, Unit 5.6.
36. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters. Proteins 2006, 65, 712-725.
37. Case, D. A.; Darden, T. A.; Cheatham, T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; et al., Amber 11. University of California: San Francisco, CA, 2010.
38. Dolinsky, T. J.; Czodrowski, P.; Li, H.; Nielsen, J. E.; Jensen, J. H.; Klebe, G.; Baker, N. A. PDB2PQR: Expanding and Upgrading Automated Preparation of Biomolecular Structures for Molecular Simulations. Nucleic Acids Res. 2007, 35, W522-W525.
39. Søndergaard, C. R.; Olsson, M. H. M.; Rostkowski, M.; Jensen, J. H. Improved Treatment of Ligands and Coupling Effects in Empirical Calculation and Rationalization of pKa Values. J. Chem. Theory Comput. 2011, 7, 2284-2295.
40. David, C. C.; Jacobs, D. J. Principal Component Analysis: a Method for Determining the Essential Dynamics of Proteins. Methods Mol. Biol. 2014, 1084, 193-226.
41. The PyMOL Molecular Graphics System, version 1.6; Schrödinger, LLC: New York, 2010.
42. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics. J. Mol. Graph. 1996, 14, 33-38.
43. Yearley, E.; Godfrin, P.; Perevozchikova, T.; Zhang, H.; Falus, P.; Porcar, L.; Nagao, M.; Curtis, J.; Gawande, P.; Taing, R.; Zarraga, I.; Wagner, N.; Liu, Y. Observation of Small Cluster Formation in Concentrated Monoclonal Antibody Solutions and Its Implications to Solution Viscosity. Biophys. J. 2014, 106, 1763-1770.
44. Chopra, G.; Summa, C. M.; Levitt, M. Solvent Dramatically Affects Protein Structure Refinement. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 20239-20244.
45. Kanai, S.; Liu, J.; Patapoff, T. W.; Shire, S. J. Reversible Self-Association of a Concentrated Monoclonal Antibody Solution Mediated by Fab-Fab Interaction That Impacts Solution Viscosity. J. Pharm. Sci. 2008, 97, 4219-4227.
46. Singh, S.; Yadav, S.; Shire, S.; Kalonia, D. Dipole-Dipole Interaction in Antibody Solutions: Correlation with Viscosity Behavior at High Concentration. Pharm. Res. 2014, 1-10.
47. Camacho, C. J.; Weng, Z.; Vajda, S.; DeLisi, C. Free Energy Landscapes of Encounter Complexes in Protein-Protein Association. Biophys. J. 1999, 76, 1166-1178.
48. Camacho, C. J.; Vajda, S. Protein Docking along Smooth Association Pathways. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 10636-10641.
49. Kim, Y. C.; Tang, C.; Clore, G. M.; Hummer, G. Replica Exchange Simulations of Transient Encounter Complexes in Protein-Protein Association. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 12855-12860.
50. Gallicchio, E.; Lapelosa, M.; Levy, R. M. The Binding Energy Distribution Analysis Method (BEDAM) for the Estimation of Protein-Ligand Binding Affinities. J. Chem. Theory Comput. 2010, 6, 2961-2977.
51. Lapelosa, M.; Gallicchio, E.; Levy, R. M. Conformational Transitions and Convergence of Absolute Binding Free Energy Calculations. J. Chem. Theory Comput. 2012, 8, 47-60.
52. Kamerzell, T. J.; Kanai, S.; Liu, J.; Shire, S. J.; Wang, Y. J. Increasing IgG Concentration Modulates the Conformational Heterogeneity and Bonding Network That Influence Solution Properties. J. Phys. Chem. B 2009, 113, 6109-6118.
53. Velev, O. D.; Kaler, E. W.; Lenhoff, A. M. Protein Interactions in Solution Characterized by Light and Neutron Scattering: Comparison of Lysozyme and Chymotrypsinogen. Biophys. J. 1998, 75, 2682-2697.