Linking the solution viscosity of an IgG2 monoclonal antibody to its structure as a function of pH and temperature

Journal of Pharmaceutical Sciences

Volumn 102, Issue 12, 2013, Pages 4291-4304

  Cheng, Weiqiang ^a   Joshi, Sangeeta B ^a   Jain, Nishant Kumar ^a   He, Feng ^b   Kerwin, Bruce A ^b   Volkin, David B ^a   Middaugh, C Russell ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b AMGEN INC   (United States)

Author keywords

Fluorescence spectroscopy; FT IR; high concentration; monoclonal antibody; partial specific volume; absorption spectroscopy; protein; structure; viscosity; zeta potential

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; BUFFER; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G2 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ARTICLE; FLUORESCENCE SPECTROSCOPY; INFRARED SPECTROSCOPY; LIGHT SCATTERING; PH; PROTEIN AGGREGATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; TEMPERATURE; TRANSITION TEMPERATURE; ULTRAVIOLET ABSORPTION SPECTROSCOPY; VISCOMETRY; VISCOSITY; ZETA POTENTIAL;

FLUORESCENCE SPECTROSCOPY; FT-IR; HIGH CONCENTRATION; MONOCLONAL ANTIBODY; PARTIAL SPECIFIC VOLUME; ABSORPTION SPECTROSCOPY; PROTEIN; STRUCTURE; VISCOSITY; ZETA POTENTIAL;

HYDROGEN-ION CONCENTRATION; IMMUNOGLOBULIN G; PROTEIN CONFORMATION; PROTEIN STABILITY; SPECTROMETRY, FLUORESCENCE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TEMPERATURE; VISCOSITY;

EID: 84888205177     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23748     Document Type: Article

References (62)

1. Nelson AL, Dhimolea E, Reichert JM,. 2010. Development trends for human monoclonal antibody therapeutics. Nat Rev Drug Discov 9 (10): 767-774.
2. Shire SJ, Shahrokh Z, Liu J,. 2004. Challenges in the development of high protein concentration formulations. J Pharm Sci 93 (6): 1390-1402.
3. Liu J, Nguyen MD, Andya JD, Shire SJ,. 2005. Reversible self-association increases the viscosity of a concentrated monoclonal antibody in aqueous solution. J Pharm Sci 94 (9): 1928-1940.
4. Kanai S, Liu J, Patapoff TW, Shire SJ,. 2008. Reversible self-association of a concentrated monoclonal antibody solution mediated by Fab-Fab interaction that impacts solution viscosity. J Pharm Sci 97 (10): 4219-4227.
5. Yadav S, Laue TM, Kalonia DS, Singh SN, Shire SJ,. 2012. The influence of charge distribution on self-association and viscosity behavior of monoclonal antibody solutions. Mol Pharm 9 (4): 791-802.
6. Saito S, Hasegawa J, Kobayashi N, Kishi N, Uchiyama S, Fukui K,. 2012. Behavior of monoclonal antibodies: Relation between the second virial coefficient (B22) at low concentrations and aggregation propensity and viscosity at high concentrations. Pharm Res 29 (2): 397-410.
7. Yadav S, Shire SJ, Kalonia DS,. 2010. Factors affecting the viscosity in high concentration solutions of different monoclonal antibodies. J Pharm Sci 99 (12): 4812-4829.
8. Yadav S, Liu J, Shire SJ, Kalonia DS,. 2010. Specific interactions in high concentration antibody solutions resulting in high viscosity. J Pharm Sci 99 (3): 1152-1168.
9. George A, Wilson WW,. 1994. Predicting protein crystallization from a dilute solution property. Acta Crystallogr D Biol Crystallogr 50 (Pt 4): 361-365.
10. Jing Z, Liu XY,. 2003. Effect of protein-protein interactions on protein aggregation kinetics. J Chem Phys 119 (20): 10972-10976.
11. Jia Y, Narayanan J, Liu XY, Liu Y,. 2005. Investigation on the mechanism of crystallization of soluble protein in the presence of nonionic surfactant. Biophys J 89 (6): 4245-4251.
12. Yadav S, Scherer TM, Shire SJ, Kalonia DS,. 2011. Use of dynamic light scattering to determine second virial coefficient in a semidilute concentration regime. Anal Biochem 411 (2): 292-296.
13. Tessier PM, Lenhoff AM, Sandler SI,. 2002. Rapid measurement of protein osmotic second virial coefficients by self-interaction chromatography. Biophys J 82 (3): 1620-1631.
14. Tessier PM, Sandler SI, Lenhoff AM,. 2004. Direct measurement of protein osmotic second virial cross coefficients by cross-interaction chromatography. Protein Sci 13 (5): 1379-1390.
15. Yadav S, Shire SJ, Kalonia DS,. 2011. Viscosity analysis of high concentration bovine serum albumin aqueous solutions. Pharm Res 28 (8): 1973-1983.
16. Yadav S, Shire SJ, Kalonia DS,. 2012. Viscosity behavior of high-concentration monoclonal antibody solutions: Correlation with interaction parameter and electroviscous effects. J Pharm Sci 101 (3): 998-1011.
17. Yadav S, Sreedhara A, Kanai S, Liu J, Lien S, Lowman H, Kalonia DS, Shire SJ,. 2011. Establishing a link between amino acid sequences and self-associating and viscoelastic behavior of two closely related monoclonal antibodies. Pharm Res 28 (7): 1750-1764.
18. Guo Z, Chen A, Nassar RA, Helk B, Mueller C, Tang Y, Gupta K, Klibanov AM,. 2012. Structure-activity relationship for hydrophobic salts as viscosity-lowering excipients for concentrated solutions of monoclonal antibodies. Pharm Res 29 (11): 3102-3109.
19. Du W, Klibanov AM,. 2011. Hydrophobic salts markedly diminish viscosity of concentrated protein solutions. Biotechnol Bioeng 108 (3): 632-636.
20. He F, Woods CE, Litowski JR, Roschen LA, Gadgil HS, Razinkov VI, Kerwin BA,. 2011. Effect of sugar molecules on the viscosity of high concentration monoclonal antibody solutions. Pharm Res 28 (7): 1552-1560.
21. Galush WJ, Le LN, Moore JM,. 2012. Viscosity behavior of high-concentration protein mixtures. J Pharm Sci 101 (3): 1012-1020.
22. Liu C, Vailhe C, Samuel N, Min Q,. 2009. A simple and reproducible approach to characterize protein stability using rheology. Int J Pharm 374 (1-2): 1-4.
23. Kamerzell TJ, Kanai S, Liu J, Shire SJ, Wang YJ,. 2009. Increasing IgG concentration modulates the conformational heterogeneity and bonding network that influence solution properties. J Phys Chem B 113 (17): 6109-6118.
24. Daumantas M, Christoph GB, Victor AB, Rex EL,. 1999. 1-Anilino-8- naphthalene sulfonate as a protein conformational tightening agent. Biopolymers 49 (6): 451-458.
25. Cheng W, Joshi SB, He F, Brems DN, He B, Kerwin BA, Volkin DB, Middaugh CR,. 2012. Comparison of high-throughput biophysical methods to identify stabilizing excipients for a model IgG2 monoclonal antibody: Conformational stability and kinetic aggregation measurements. J Pharm Sci 101 (5): 1701-1720.
26. Stothart PH,. 1984. Determination of partial specific volume and absolute concentration by densimetry. Biochem J 219 (3): 1049-1052.
27. He F, Becker GW, Litowski JR, Narhi LO, Brems DN, Razinkov VI,. 2010. High-throughput dynamic light scattering method for measuring viscosity of concentrated protein solutions. Anal Biochem 399 (1): 141-143.
28. Kestin J, Sokolov M, Wakeham WA,. 1978. Viscosity of liquid water in the range -8°C to 150°C. J Phys Chem Ref Data 7: 941.
29. Susi H, Byler DM,. 1983. Protein structure by Fourier transform infrared spectroscopy: Second derivative spectra. Biochem Biophys Res Commun 115 (1): 391-397.
30. Murphy BM, Zhang N, Payne RW, Davis JM, Abdul-Fattah AM, Matsuura JE, Herman AC, Manning MC,. 2012. Structure, stability, and mobility of a lyophilized IgG1 monoclonal antibody as determined using second-derivative infrared spectroscopy. J Pharm Sci 101 (1): 81-91.
31. Clark AH, Saunderson DH, Suggett A,. 1981. Infrared and laser-Raman spectroscopic studies of thermally-induced globular protein gels. Int J Pept Protein Res 17 (3): 353-364.
32. Byler DM, Susi H,. 1986. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25 (3): 469-487.
33. Ismail AA, Mantsch HH, Wong PT,. 1992. Aggregation of chymotrypsinogen: Portrait by infrared spectroscopy. Biochim Biophys Acta 1121 (1-2): 183-188.
34. Kueltzo LA, Ersoy B, Ralston JP, Middaugh CR,. 2003. Derivative absorbance spectroscopy and protein phase diagrams as tools for comprehensive protein characterization: A bGCSF case study. J Pharm Sci 92 (9): 1805-1820.
35. Esfandiary R, Hunjan JS, Lushington GH, Joshi SB, Middaugh CR,. 2009. Temperature dependent 2nd derivative absorbance spectroscopy of aromatic amino acids as a probe of protein dynamics. Protein Sci 18 (12): 2603-2614.
36. Stryer L,. 1965. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites. J Mol Biol 13 (2): 482-495.
37. Sharafy S, Muszkat KA,. 1971. Viscosity dependence of fluorescence quantum yields. J Am Chem Soc 93 (17): 4119-4125.
38. Chari R, Jerath K, Badkar AV, Kalonia DS,. 2009. Long- and short-range electrostatic interactions affect the rheology of highly concentrated antibody solutions. Pharm Res 26 (12): 2607-2618.
39. Wang W, Singh S, Zeng DL, King K, Nema S,. 2007. Antibody structure, instability, and formulation. J Pharm Sci 96 (1): 1-26.
40. Surewicz WK, Mantsch HH, Chapman D,. 1993. Determination of protein secondary structure by Fourier transform infrared spectroscopy: A critical assessment. Biochemistry 32 (2): 389-394.
41. Goldberg ME, Chaffotte AF,. 2005. Undistorted structural analysis of soluble proteins by attenuated total reflectance infrared spectroscopy. Protein Sci 14 (11): 2781-2792.
42. Harn N, Allan C, Oliver C, Middaugh CR,. 2007. Highly concentrated monoclonal antibody solutions: Direct analysis of physical structure and thermal stability. J Pharm Sci 96 (3): 532-546.
43. Bhambhani A, Kissmann JM, Joshi SB, Volkin DB, Kashi RS, Middaugh CR,. 2012. Formulation design and high-throughput excipient selection based on structural integrity and conformational stability of dilute and highly concentrated IgG1 monoclonal antibody solutions. J Pharm Sci 101 (3): 1120-1135.
44. Matulis D, Lovrien R,. 1998. 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys J 74 (1): 422-429.
45. Gasymov OK, Glasgow BJ,. 2007. ANS fluorescence: Potential to augment the identification of the external binding sites of proteins. Biochim Biophys Acta 1774 (3): 403-411.
46. Chakraborty S, Peng Z,. 2000. Hierarchical unfolding of the alpha-lactalbumin molten globule: Presence of a compact intermediate without a unique tertiary fold. J Mol Biol 298 (1): 1-6.
47. Buchner J, Renner M, Lilie H, Hinz HJ, Jaenicke R, Kiefhabel T, Rudolph R,. 1991. Alternatively folded states of an immunoglobulin. Biochemistry 30 (28): 6922-6929.
48. Semisotnov GV, Rodionova NA, Razgulyaev OI, Uversky VN, Gripas AF, Gilmanshin RI,. 1991. Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 31 (1): 119-128.
49. Bateman JB, Weneck EJ, Eshler DC,. 1959. Determination of particle size and concentration from spectrophotometric transmission. J Colloid Sci 14 (3): 308-329.
50. Sukumar M, Doyle BL, Combs JL, Pekar AH,. 2004. Opalescent appearance of an IgG1 antibody at high concentrations and its relationship to noncovalent association. Pharm Res 21 (7): 1087-1093.
51. Sahin E, Weiss WF 4th, Kroetsch AM, King KR, Kessler RK, Das TK, Roberts CJ,. 2012. Aggregation and pH-temperature phase behavior for aggregates of an IgG2 antibody. J Pharm Sci 101 (5): 1678-1687.
52. Barbut S,. 1995. Effects of calcium level on the structure of pre-heated whey protein isolate gels. LWT-Food Sci Technol 28 (6): 598-603.
53. Doi E,. 1993. Gels and gelling of globular proteins. Trends Food Sci Technol 4 (1): 1-5.
54. Lee S, Tikhomirova A, Shalvardjian N, Chalikian TV,. 2008. Partial molar volumes and adiabatic compressibilities of unfolded protein states. Biophys Chem 134 (3): 185-199.
55. Gekko K, Hasegawa Y,. 1986. Compressibility-structure relationship of globular proteins. Biochemistry 25 (21): 6563-6571.
56. Kamerzell TJ, Ramsey JD, Middaugh CR,. 2008. Immunoglobulin dynamics, conformational fluctuations, and nonlinear elasticity and their effects on stability. J Phys Chem B 112 (10): 3240-3250.
57. Monkos K,. 1996. Viscosity of bovine serum albumin aqueous solutions as a function of temperature and concentration. Int J Biol Macromol 18 (1-2): 61-68.
58. Monkos K, Turczynski B,. 1999. A comparative study on viscosity of human, bovine and pig IgG immunoglobulins in aqueous solutions. Int J Biol Macromol 26 (2-3): 155-159.
59. Haidekker MA, Theodorakis EA,. 2010. Environment-sensitive behavior of fluorescent molecular rotors. J Biol Eng 4: 11.
60. Sutharsan J, Lichlyter D, Wright NE, Dakanali M, Haidekker MA, Theodorakis EA,. 2010. Molecular rotors: Synthesis and evaluation as viscosity sensors. Tetrahedron 66 (14): 2582-2588.
61. Santiago PS, Carvalho JW, Domingues MM, Santos NC, Tabak M,. 2010. Thermal stability of extracellular hemoglobin of Glossoscolex paulistus: Determination of activation parameters by optical spectroscopic and differential scanning calorimetric studies. Biophys Chem 152 (1-3): 128-138.
62. Kurganov BI, Lyubarev AE, Sanchez-Ruiz JM, Shnyrov VL,. 1997. Analysis of differential scanning calorimetry data for proteins. Criteria of validity of one-step mechanism of irreversible protein denaturation. Biophys Chem 69 (2-3): 125-135.