The role of electrostatics in protein-protein interactions of a monoclonal antibody

Molecular Pharmaceutics

Volumn 11, Issue 7, 2014, Pages 2475-2489

  Roberts, D ^a   Keeling, R ^a   Tracka, M ^b   Van Der Walle, C F ^b   Uddin, S ^b   Warwicker, J ^a   Curtis, R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b MEDIMMUNE   (United States)

Author keywords

diffusion interaction parameters; electrostatics; monoclonal antibody; osmotic second virial coefficients; protein protein interactions

Indexed keywords

MONOCLONAL ANTIBODY; SODIUM CHLORIDE; PROTEIN; SOLUTION AND SOLUBILITY;

ALKALINITY; ARTICLE; CRYSTAL STRUCTURE; DIPOLE; ELECTRIC POTENTIAL; HINGE REGION; HYDRODYNAMICS; IONIC STRENGTH; ISOELECTRIC POINT; MOLECULAR WEIGHT; PH; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REFRACTION INDEX; SEDIMENTATION; SEDIMENTATION RATE; STATIC ELECTRICITY; SURFACE PROPERTY; TEMPERATURE; TITRIMETRY; VALIDITY; CHEMISTRY; LIGHT; OSMOLARITY; PROTEIN DOMAIN; RADIATION SCATTERING; SOLUTION AND SOLUBILITY;

ANTIBODIES, MONOCLONAL; HYDROGEN-ION CONCENTRATION; LIGHT; OSMOLAR CONCENTRATION; PHARMACEUTICAL SOLUTIONS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEINS; SCATTERING, RADIATION; STATIC ELECTRICITY;

EID: 84903973465     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp5002334     Document Type: Article

References (77)

1. Saluja, A.; Fesinmeyer, R. M.; Hogan, S.; Brems, D. N.; Gokarn, Y. R. Diffusion and Sedimentation Interaction Parameters for Measuring the Second Virial Coefficient and Their Utility as Predictors of Protein Aggregation Biophys. J. 2010, 99, 2657-2665
2. 2) at Low Concentrations and Aggregation Propensity and Viscosity at High Concentrations Pharm. Res. 2012, 29, 397-410
3. He, F.; Woods, C. E.; Becker, G. W.; Narhi, L. O.; Razinkov, V. I. High-Throughput Assessment of Thermal and Colloidal Stability Parameters for Monoclonal Antibody Formulations J. Pharm. Sci. 2011, 100, 5126-5141
4. Mason, B. D.; Zhang, L.; Remmele, J.; Richard, L.; Zhang, J. Opalescence of an IgG2 Monoclonal Antibody Solution as it Relates to Liquid-Liquid Phase Separation J. Pharm. Sci. 2011, 100, 4587-4596
5. Mason, B. D.; Zhang-van Enk, J.; Zhang, L.; Remmele, R. L.; Zhang, J. Liquid-Liquid Phase Separation of a Monoclonal Antibody and Nonmonotonic Influence of Hofmeister Anions Biophys. J. 2010, 99, 3792-3800
6. Salinas, B. A.; Sathish, H. A.; Bishop, S. M.; Harn, N.; Carpenter, J. F.; Randolph, T. W. Understanding and Modulating Opalescence and Viscosity in a Monoclonal Antibody Formulation J. Pharm. Sci. 2010, 99, 82-93
7. Nishi, H.; Miyajima, M.; Nakagami, H.; Noda, M.; Uchiyama, S.; Fukui, K. Phase Separation of an IgG1 Antibody Solution under a Low Ionic Strength Condition Pharm. Res. 2010, 27, 1348-1360
8. Ahamed, T.; Esteban, B. N. A.; Ottens, M.; van Dedem, G. W. K.; van der Wielen, L. A. M.; Bisschops, M. A. T.; Lee, A.; Pham, C.; Thommes, J. Phase behavior of an intact monoclonal antibody Biophys. J. 2007, 93, 610-619
9. Lewus, R. A.; Darcy, P. A.; Lenhoff, A. M.; Sandler, S. I. Interactions and Phase Behavior of a Monoclonal Antibody Biotechnol. Prog. 2011, 27, 280-289
10. Sukumar, M.; Doyle, B. L.; Combs, J. L.; Pekar, A. H. Opalescent appearance of an IgG1 antibody at high concentrations and its relationship to noncovalent association Pharm. Res. 2004, 21, 1087-1093
11. Jezek, J.; Rides, M.; Derham, B.; Moore, J.; Cerasoli, E.; Simler, R.; Perez-Ramirez, B. Viscosity of concentrated therapeutic protein compositions Adv. Drug Delivery Rev. 2011, 63, 1107-1117
12. Saluja, A.; Badkar, A. V.; Zeng, D. L.; Kalonia, D. S. Ultrasonic rheology of a monoclonal antibody (IgG(2)) solution: Implications for physical stability of proteins in high concentration formulations J. Pharm. Sci. 2007, 96, 3181-3195
13. Yadav, S.; Shire, S. J.; Kalonia, D. S. Viscosity behavior of high-concentration monoclonal antibody solutions: Correlation with interaction parameter and electroviscous effects J. Pharm. Sci. 2012, 101, 998-1011
14. 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
15. 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
16. 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
17. 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
18. Neergaard, M. S.; Kalonia, D. S.; Parshad, H.; Nielsen, A. D.; Moller, E. H.; van de Weert, M. Viscosity of high concentration protein formulations of monoclonal antibodies of the IgG1 and IgG4 subclass-Prediction of viscosity through protein-protein interaction measurements Eur. J. Pharm. Sci. 2013, 49, 400-410
19. Chi, E. Y.; Krishnan, S.; Kendrick, B. S.; Chang, B. S.; Carpenter, J. F.; Randolph, T. W. Roles of conformational stability and colloidal stability in the aggregation of recombinant human granulocyte colony-stimulating factor Protein Sci. 2003, 12, 903-913
20. Olsen, S. N.; Andersen, K. B.; Randolph, T. W.; Carpenter, J. F.; Westh, P. Role of electrostatic repulsion on colloidal stability of Bacillus halmapalus alpha-amylase Biochim. Biophys. Acta, Proteins Proteomics 2009, 1794, 1058-1065
21. Saito, S.; Hasegawa, J.; Kobayashi, N.; Tomitsuka, T.; Uchiyama, S.; Fukui, K. Effects of Ionic Strength and Sugars on the Aggregation Propensity of Monoclonal Antibodies: Influence of Colloidal and Conformational Stabilities Pharm. Res. 2013, 30, 1263-1280
22. Le Brun, V.; Friess, W.; Bassarab, S.; Muhlau, S.; Garidel, P. A critical evaluation of self-interaction chromatography as a predictive tool for the assessment of protein-protein interactions in protein formulation development: A case study of a therapeutic monoclonal antibody Eur. J. Pharm. Biopharm. 2010, 75, 16-25
23. Jimenez, M.; Rivas, G.; Minton, A. P. Quantitative characterization of weak self-association in concentrated solutions of immunoglobulin G via the measurement of sedimentation equilibrium and osmotic pressure Biochemistry 2007, 46, 8373-8378
24. Pathak, J. A.; Sologuren, R. R.; Narwal, R. Do Clustering Monoclonal Antibody Solutions Really Have a Concentration Dependence of Viscosity? Biophys. J. 2013, 104, 913-923
25. Chari, R.; Jerath, K.; Badkar, A. V.; Kalonia, D. S. Long- and Short-Range Electrostatic Interactions Affect the Rheology of Highly Concentrated Antibody Solutions Pharm. Res. 2009, 26, 2607-2618
26. 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
27. Kumar, V.; Dixit, N.; Zhou, L. L.; Fraunhofer, W. Impact of short range hydrophobic interactions and long range electrostatic forces on the aggregation kinetics of a monoclonal antibody and a dual-variable domain immunoglobulin at low and high concentrations Int. J. Pharm. 2011, 421, 82-93
28. Neal, B. L.; Asthagiri, D.; Velev, O. D.; Lenhoff, A. M.; Kaler, E. W. Why is the osmotic second virial coefficient related to protein crystallization? J. Cryst. Growth 1999, 196, 377-387
29. 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
30. Song, X. Y.; Zhao, X. F. The van der Waals interaction between protein molecules in an electrolyte solution J. Chem. Phys. 2004, 120, 2005-2009
31. Pellicane, G.; Smith, G.; Sarkisov, L. Molecular Dynamics Characterization of Protein Crystal Contacts in Aqueous Solutions Phys. Rev. Lett. 2008, 101 248102
32. McManus, J. J.; Lomakin, A.; Ogun, O.; Pande, A.; Basan, M.; Pande, J.; Benedek, G. B. Altered phase diagram due to a single point mutation in human gamma D-crystallin Proc. Natl. Acad. Sci. U.S.A 2007, 104, 16856-16861
33. 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. Pharmaceutics 2012, 9, 791-802
34. Lehermayr, C.; Mahler, H.-C.; Maeder, K.; Fischer, S. Assessment of Net Charge and Protein-Protein Interactions of Different Monoclonal Antibodies J. Pharm. Sci. 2011, 100, 2551-2562
35. Felderhof, B. U. Diffusion of Interacting Brownian Particles J. Phys. A: Math. Gen. 1978, 11, 929-937
36. Kuehner, D. E.; Heyer, C.; Ramsch, C.; Fornefeld, U. M.; Blanch, H. W.; Prausnitz, J. M. Interactions of lysozyme in concentrated electrolyte solutions from dynamic light-scattering measurements Biophys. J. 1997, 73, 3211-3224
37. Batchelor, G. K. Brownian Diffusion of Particles With Hydrodynamic Interaction J. Fluid Mech. 1976, 74, 1-29
38. Phillies, G. D. J. Numerical Interpretation of the Concentration- dependence of Micelle Diffusion-coefficients J. Colloid Interface Sci. 1987, 119, 518-523
39. Ooi, T. Light Scattering From Multi-component Systems J. Polym. Sci. 1958, 28, 459-462
40. Casassa, E. F.; Eisenberg, H. Thermodynamic Analysis of Multicomponent Solutions Adv. Protein Chem. 1964, 19, 287-395
41. Vrij, A.; Overbeek, J. T. Scattering of Light By Charged Colloidal Particles In Salt Solutions J. Colloid. Sci. 1962, 17, 570.
42. Berne, B.; Pecora, R. Dynamic Light Scattering, With Applications to Chemistry, Biology, and Physics; John Wiley & Sons: New York, 1976.
43. Delgado, A. V.; Gonzalez-Caballero, E.; Hunter, R. J.; Koopal, L. K.; Lyklema, J. Measurement and interpretation of electrokinetic phenomena-(IUPAC technical report) Pure Appl. Chem. 2005, 77, 1753-1805
44. Warwicker, J. Continuum Dielectric Modeling of the Protein Solvent System, and Calculation of the Long-range Electrostatic-field of the Enzyme Phosphoglycerate Mutase J. Theor. Biol. 1986, 121, 199-210
45. Neal, B. L.; Asthagiri, D.; Lenhoff, A. M. Molecular origins of osmotic second virial coefficients of proteins Biophys. J. 1998, 75, 2469-2477
46. Gruenberger, A.; Lai, P.-K.; Blanco, M. A.; Roberts, C. J. Coarse-Grained Modeling of Protein Second Osmotic Virial Coefficients: Sterics and Short-Ranged Attractions J. Phys. Chem. B 2013, 117, 763-770
47. Rosenbaum, D.; Zamora, P. C.; Zukoski, C. F. Phase behavior of small attractive colloidal particles Phys. Rev. Lett. 1996, 76, 150-153
48. Piazza, R.; Peyre, V.; Degiorgio, V. "Sticky hard spheres" model of proteins near crystallization: A test based on the osmotic compressibility of lysozyme solutions Phys. Rev. E 1998, 58, R2733-R2736
49. Tardieu, A.; Le Verge, A.; Malfois, M.; Bonnete, F.; Finet, S.; Ries-Kautt, M.; Belloni, L. Proteins in solution: From X-ray scattering intensities to interaction potentials J. Cryst. Growth 1999, 196, 193-203
50. Zhang, F.; Roth, R.; Wolf, M.; Roosen-Runge, F.; Skoda, M. W. A.; Jacobs, R. M. J.; Stzucki, M.; Schreiber, F. Charge-controlled metastable liquid-liquid phase separation in protein solutions as a universal pathway towards crystallization Soft Matter 2012, 8, 1313-1316
51. Hunter, R. J. Foundations of Colloid Science; Oxford University Press: New York, 2001.
52. Arzensek, D.; Kuzman, D.; Podgornik, R. Colloidal interactions between monoclonal antibodies in aqueous solutions J. Colloid Interface Sci. 2012, 384, 207-216
53. Muschol, M.; Rosenberger, F. Interactions in undersaturated and supersaturated lysozyme solutions: Static and dynamic light scattering results J. Chem. Phys. 1995, 103, 10424-10432
54. Curtis, R. A.; Prausnitz, J. M.; Blanch, H. W. Protein-protein and protein-salt interactions in aqueous protein solutions containing concentrated electrolytes Biotechnol. Bioeng. 1998, 57, 11-21
55. Eberstein, W.; Georgalis, Y.; Saenger, W. Molecular-interactions In Crystallizing Lysozyme Solutions Studied By Photon-correlation Spectroscopy J. Cryst. Growth 1994, 143, 71-78
56. Petsev, D. N.; Denkov, N. D. Diffusion of Charged Colloidal Particles At Low-volume Fraction-Theoretical-model and Light-scattering Experiments J. Colloid Interface Sci. 1992, 149, 329-344
57. Zhang, L.; Tan, H.; Fesinmeyer, R. M.; Li, C.; Catrone, D.; Le, D.; Remmele, J.; Richard, L.; Zhang, J. Antibody solubility behavior in monovalent salt solutions reveals specific anion effects at low ionic strength J. Pharm. Sci. 2012, 101, 965-977
58. Medda, L.; Barse, B.; Cugia, F.; Bostrom, M.; Parsons, D. F.; Ninham, B. W.; Monduzzi, M.; Salis, A. Hofmeister Challenges: Ion Binding and Charge of the BSA Protein as Explicit Examples Langmuir 2012, 28, 16355-16363
59. Goto, Y.; Takahashi, N.; Fink, A. L. Mechanism of Acid-induced Folding of Proteins Biochemistry 1990, 29, 3480-3488
60. Ramos, C. H. I.; Baldwin, R. L. Sulfate anion stabilization of native ribonuclease A both by anion binding and by the Hofmeister effect Protein Sci. 2002, 11, 1771-1778
61. Ebel, C.; Faou, P.; Kernel, B.; Zaccai, G. Relative role of anions and cations in the stabilization of halophilic malate dehydrogenase Biochemistry 1999, 38, 9039-9047
62. Sedlak, E.; Stagg, L.; Wittung-Stafshede, P. Effect of Hofmeister ions on protein thermal stability: Roles of ion hydration and peptide groups? Arch. Biochem. Biophys. 2008, 479, 69-73
63. Dubin, S. B.; Clark, N. A.; Benedek, G. B. Measurement of Rotational Diffusion Coefficient of Lysozyme By Depolarized Light Scattering: Configuration of Lysozyme In Solution J. Chem. Phys. 1971, 54, 5158-5164
64. Abramo, M. C.; Caccamo, C.; Costa, D.; Pellicane, G.; Ruberto, R.; Wanderlingh, U. Effective interactions in lysozyme aqueous solutions: A small-angle neutron scattering and computer simulation study J. Chem. Phys. 2012, 136, 035103
65. Blanco, M. A.; Sahin, E.; Li, Y.; Roberts, C. J. Reexamining protein-protein and protein-solvent interactions from Kirkwood-Buff analysis of light scattering in multi-component solutions J. Chem. Phys. 2011, 134 225103
66. Dumetz, A. C.; Chockla, A. M.; Kaler, E. W.; Lenhoff, A. M. Effects of pH on protein-protein interactions and implications for protein phase behavior Biochim. Biophys. Acta, Proteins Proteomics 2008, 1784, 600-610
67. Dumetz, A. C.; Snellinger-OBrien, A. M.; Kaler, E. W.; Lenhoff, A. M. Patterns of protein-protein interactions in salt solutions and implications for protein crystallization Protein Sci. 2007, 16, 1867-1877
68. Tessier, P. M.; Johnson, H. R.; Pazhianur, R.; Berger, B. W.; Prentice, J. L.; Bahnson, B. J.; Sandler, S. I.; Lenhoff, A. M. Predictive crystallization of ribonuclease A via rapid screening of osmotic second virial coefficients Proteins 2003, 50, 303-311
69. 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
70. Piazza, R.; Iacopini, S.; Galliano, M. BLGA protein solutions at high ionic strength: Vanishing attractive interactions and "frustrated" aggregation Europhys. Lett. 2002, 59, 149-154
71. Bratko, D.; Striolo, A.; Wu, J. Z.; Blanch, H. W.; Prausnitz, J. M. Orientation-averaged pair potentials between dipolar proteins or colloids J. Phys. Chem. B 2002, 106, 2714-2720
72. Phillies, G. D. Excess Chemical Potential of Dilute-solutions of Spherical Polyelectrolytes J. Chem. Phys. 1974, 60, 2721-2731
73. Persson, B. A.; Jonsson, B.; Lund, M. Enhanced Protein Steering: Cooperative Electrostatic and van der Waals Forces in Antigen-Antibody Complexes J. Phys. Chem. B 2009, 113, 10459-10464
74. Grigsby, J. J.; Blanch, H. W.; Prausnitz, J. M. Cloud-point temperatures for lysozyme in electrolyte solutions: effect of salt type, salt concentration and pH Biophys. Chem. 2001, 91, 231-243
75. Broide, M. L.; Tominc, T. M.; Saxowsky, M. D. Using phase transitions to investigate the effect of salts on protein interactions Phys. Rev. E 1996, 53, 6325-6335
76. Seyrek, E.; Dubin, P. L.; Tribet, C.; Gamble, E. A. Ionic strength dependence of protein-polyelectrolyte interactions Biomacromolecules 2003, 4, 273-282
77. Harding, S. E.; Johnson, P. The Concentration-dependence of Macromolecular Parameters Biochem. J. 1985, 231, 543-547