Evaluation of a non-arrhenius model for therapeutic monoclonal antibody aggregation

Journal of Pharmaceutical Sciences

Volumn 100, Issue 7, 2011, Pages 2526-2542

  Kayser, Veysel ^a   Chennamsetty, Naresh ^a   Voynov, Vladimir ^a   Helk, Bernhard ^b   Forrer, Kurt ^b   Trout, Bernhardt L ^a  

^a USA   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Mathematical model; Protein aggregation

Indexed keywords

MONOCLONAL ANTIBODY;

ARTICLE; CONFORMATION; ELECTRON MICROSCOPY; FLUORESCENCE SPECTROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH TEMPERATURE; LIGHT SCATTERING;

EID: 79955591497     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.22493     Document Type: Article

References (92)

1. Wang W, Singh S, Zeng DL, King K, Nema S. 2007. Antibody structure, instability, and formulation. J Pharm Sci 96(1):1-26.
2. Presta LG. 2006. Engineering of therapeutic antibodies to minimize immunogenicity and optimize function. Adv Drug Deliv Rev 58(5-6):640-656.
3. Chester K, Pedley B, Tolner B, Violet J, Mayer A, Sharma S, Boxer G, Green A, Nagl S, Begent R. 2004. Engineering antibodies for clinical applications in cancer. Tumor Biol 25(1-2):91-98.
4. Chowdhury PS, Wu H. 2005. Tailor-made antibody therapeutics. Methods 36(1):11-24.
5. Drugs@FDA: Search Results for 'mAb'. Last accessed in 2009.
6. Shire SJ, Shahrokh Z, Liu J. 2004. Challenges in the development of high protein concentration formulations. J Pharm Sci 93(6):1390-1402.
7. Liu J, Nguyen MDH, 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.
8. 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.
9. Carter PJ. 2006. Potent antibody therapeutics by design. Nat Rev Immunol 6(5):343-357.
10. Hwang WYK, Foote J. 2005. Immunogenicity of engineered antibodies. Methods 36(1):3-10.
11. Lee JC. 2000. Biopharmaceutical formulation. Curr Opin Biotechnol 11(1):81-84.
12. Wu H, Dall'Acqua WF. 2005. Humanized antibodies and their applications. Methods 36(1):1-2.
13. Purohit VS, Middaugh CR, Balasubramanian SV. 2006. Influence of aggregation on immunogenicity of recombinant human factor VIII in hemophilia A mice. J Pharm Sci 95(2):358-371.
14. Weiss IV WF, Young TM, Roberts CJ. 2009. Principles, approaches, and challenges for predicting protein aggregation rates and shelf life. J Pharm Sci 98(4):1246-1277.
15. Hartmann WK, Saptharishi N, Yang XY, Mitra G, Soman G. 2004. Characterization and analysis of thermal denaturation of antibodies by size exclusion high-performance liquid chromatography with quadruple detection. Anal Biochem 325(2):227-239.
16. McCarthy D, Goddard DH, Pell BK, Holborow EJ. 1981. Intrinsically stable IgG aggregates. J Immunol Methods 41(1):63-74.
17. McCarthy DA, Drake AF. 1989. Spectroscopic studies on IgG aggregate formation. Mol Immunol 26(9):875-881.
18. Roberts CJ. 2003. Kinetics of irreversible protein aggregation: Analysis of extended Lumry-Eyring models and implications for predicting protein shelf life. J Phys Chem B 107(5):1194-1207.
19. Roberts CJ, Darrington RT, Whitley MB. 2003. Irreversible aggregation of recombinant bovine granulocyte-colony stimulating factor (bG-CSF) and implications for predicting protein shelf life. J Pharm Sci 92(5):1095-1111.
20. Sahin E, Grillo AO, Perkins MD, Roberts CJ. 2010. Comparative effects of pH and ionic strength on protein-protein interactions, unfolding, and aggregation for IgG1 antibodies. J Pharm Sci 99(12):4830-4848.
21. Banks DD, Hambly DM, Scavezze JL, Siska CC, Stackhouse NL, Gadgil HS. 2009. The effect of sucrose hydrolysis on the stability of protein therapeutics during accelerated formulation studies. J Pharm Sci 98(12):4501-4510.
22. Brych SR, Gokarn YR, Hultgen H, Stevenson RJ, Rajan R, Matsumura M. 2010. Characterization of antibody aggregation: Role of buried, unpaired cysteines in particle formation. J Pharm Sci 99(2):764-781.
23. Mahler H-C, Senner F, Maeder K, Mueller R. 2009. Surface activity of a monoclonal antibody. J Pharm Sci 98(12):4525-4533.
24. Rosenqvist E, Jøssang T, Feder J. 1987. Thermal properties of human IgG. Mol Immunol 24(5):495-501.
25. Bernacki JP, Murphy RM. 2009. Model discrimination and mechanistic interpretation of kinetic data in protein aggregation studies. Biophys J 96(7):2871-2887.
26. Gadgil HS, Bondarenko PV, Pipes G, Rehder D, McAuley A, Perico N, Dillon T, Ricci M, Treuheit M. 2007. The LC/MS analysis of glycation of IgG molecules in sucrose containing formulations. J Pharm Sci 96(10):2607-2621.
27. Jefferis R. 2009. Glycosylation of antibody therapeutics: Optimisation for purpose. Recombinant proteins from plants. Humana Press, NY. pp 223-238.
28. Kayser V, Chennamsetty N, Voynov V, Forrer K, Helk B, Trout BL. 2011. Glycosylation influences on the aggregation propensity of therapeutic monoclonal antibodies. Biotechnol J 6:38-44.
29. Kameoka D, Masuzaki E, Ueda T, Imoto T. 2007. Effect of buffer species on the unfolding and the aggregation of humanized IgG. J Biochem 142(3):383-391.
30. Jøssang T, Feder J, Rosenqvist E. 1985. Heat aggregation kinetics of human IgG. J Chem Phys 82(1):574-589.
31. Yoshioka S, Aso Y, Izutsu K-I, Kojima S. 1994. Is stability prediction possible for protein drugs? Denaturation kinetics of β-galactosidase in solution. Pharm Res 11(12):1721-1725.
32. Weijers M, Barneveld PA, Cohen Stuart MA, Visschers RW. 2003. Heat-induced denaturation and aggregation of ovalbumin at neutral pH described by irreversible first-order kinetics. Protein Sci 12(12):2693-2703.
33. Carrotta R, Manno M, Bulone D, Martorana V, Biagio PLS. 2005. Protofibril formation of amyloid β-protein at low pH via a non-cooperative elongation mechanism. J Biol Chem 280(34):30001-30008.
34. Ramani K, Purohit V, Middaugh CR, Balasubramanian SV. 2005. Aggregation kinetics of recombinant human FVIII (rFVIII). J Pharm Sci 94(9):2023-2029.
35. Smith MI, Sharp JS, Roberts CJ. 2007. Nucleation and growth of insulin fibrils in bulk solution and at hydrophobic polystyrene surfaces. Biophys J 93(6):2143-2151.
36. Perico N, Purtell J, Dillon TM, Ricci MS. 2009. Conformational implications of an inversed pH-dependent antibody aggregation. J Pharm Sci 98(9):3031-3042.
37. Randolph TW, Carpenter JF. 2007. Engineering challenges of protein formulations. AIChE J 53(8):1902-1907.
38. Carpenter JF, Randolph TW, Jiskoot W, Crommelin DJA, Middaugh CR, Winter G. 2010. Potential inaccurate quantitation and sizing of protein aggregates by size exclusion chromatography: Essential need to use orthogonal methods to assure the quality of therapeutic protein products. J Pharm Sci 99(5):2200-2208.
39. Remmele RLJ, Callahan WJ, Krishnan S, Zhou L, Bondarenko PV, Nichols AC, Kleemann GR, Pipes GD, Park S, Fodor S, Kras E, Brems DN. 2006. Active dimer of epratuzumab provides insight into the complex nature of an antibody aggregate. J Pharm Sci 95(1):126-145.
40. Di Marco VB, Bombi GG. 2001. Mathematical functions for the representation of chromatographic peaks. J Chromatogr A 931(1-2):1-30.
41. Li J. 2002. Comparison of the capability of peak functions in describing real chromatographic peaks. J Chromatogr A 952(1-2):63-70.
42. Nikitas P, Pappa-Louisi A, Papageorgiou A. 2001. On the equations describing chromatographic peaks and the problem of the deconvolution of overlapped peaks. J Chromatogr A 912(1):13-29.
43. O'Connor DV, Phillips D. 1984. Time-correlated single-photon counting. London: Academic press.
44. Ahrer K, Buchacher A, Iberer G, Josic D, Jungbauer A. 2003. Analysis of aggregates of human immunoglobulin G using size-exclusion chromatography, static and dynamic light scattering. J Chromatogr A 1009(1-2):89-96.
45. Kayser V, Chennamsetty N, Voynov V, Helk B, Trout BL. 2010. Tryptophan-tryptophan energy transfer and classification of tryptophan residues in proteins: Therapeutic monoclonal antibody as a model. J Fluorescence. DOI: 10.1007/s10895-010-0715-0.
46. Krishnan S, Chi EY, Webb JN, Chang BS, Shan D, Goldenberg M, Manning MC, Randolph TW, Carpenter JF. 2002. Aggregation of granulocyte colony stimulating factor under physiological conditions: Characterization and thermodynamic inhibition. Biochemistry 41(20):6422-6431.
47. Frieden C. 2007. Protein aggregation processes: In search of the mechanism. Protein Sci 16(11):2334-2344.
48. Uversky VN, Li J, Fink AL. 2001. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J Biol Chem 276:10737-10744.
49. Andreu JM, Timasheff SN. 1999. The measurement of cooperative protein self-assembly by turbidity and other techniques. Methods Enzymol 130:47-59.
50. Oosawa F, Asakura S. 1975. Thermodynamics of the polymerization of protein. London: Academic Press.
51. Lakowicz JR. 2006. Principles of fluorescence spectroscopy. New York: Springer.
52. Stryer LS. 1965. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin: A fluorescent probe of non-polar binding sites. J Mol Biol 13:482-495.
53. Fink, AL, Ed. 2001. Molten globule. In Encyclopedia of life sciences. John Wiley & Sons, Ltd.: New Jersey, pp 1-6.
54. Goto Y, Fink AL. 1989. Conformational states in β-lactamase: Molten-globule states at acidic and alkaline pH with high salt. Biochemistry 28(3):945-952.
55. Goto Y, Takahashi N, Fink AL. 1990. Mechanism of acid-induced folding of proteins. Biochemistry 29(14):3480-3488.
56. Pace CN. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 131:266-280.
57. Hulett JR. 1964. Deviations from the Arrhenius equation. Q Rev Chem Soc18:227-242.
58. Waterman KC, Adami RC. 2005. Accelerated aging: Prediction of chemical stability of pharmaceuticals. Int J Pharm 293(1-2):101-125.
59. Bunnett JF. 1974. From kinetics data to reaction mechanism. In Investigation of rates and mechanisms of reactions Part 1: General considerations and reactions at conventional rates; Lewis ES, Ed. 3rd ed., New York: John Wiley & Sons, 367-488.
60. Chan HS, Dill KA. 1998. Protein folding in the landscape perspective: Chevron plots and non-Arrhenius kinetics. Proteins: Struct, Funct, and Genet 30(1):2-33.
61. Angell CA, Ngai KL, McKenna GB, McMillan PF, Martin SW. 2000. Relaxation in glass forming liquids and amorphous solids. J Appl Phys 88(6):3113-3157.
62. Tolgyesi F, Ullrich B, Fidy J. 1999. Tryptophan phosphorescence signals characteristic changes in protein dynamics at physiological temperatures. Biochimica et Biophysica Acta (BBA) - Protein Struct Mol Enzymol 1435(1-2):1-6.
63. Magari RT, Murphy KP, Fernandez T. 2002. Accelerated stability model for predicting shelf-life. J Clin Lab Anal 16(5):221-226.
64. Ertel KD, Carstensen JT. 1990. Examination of a modified Arrhenius relationship for pharmaceutical stability prediction. Int J Pharm 61:9-14.
65. King S-YP, Kung M-S, Fung H-L. 1984. Statistical prediction of drug stability based on nonlinear parameter estimation. J Pharm Sci 73(5):657-662.
66. Chen BL, Baase WA, Schellman JA. 1989. Low-temperature unfolding of a mutant of phage T4 lysozyme. 2. Kinetic investigations. Biochemistry 28(2):691-699.
67. Chen BL, Schellman JA. 1989. Low-temperature unfolding of a mutant of phage T4 lysozyme. 1. Equilibrium studies. Biochemistry 28(2):685-691.
68. Matagne A, Jamin M, Chung EW, Robinson CV, Radford SE, Dobson CM. 2000. Thermal unfolding of an intermediate is associated with non-Arrhenius kinetics in the folding of hen lysozyme. J Mol Biol 297(1):193.
69. Fulcher GS. 1925. Analysis of recent measurements of the viscosity of glasses. J Am Ceram Soc 8:339-355.
70. Tammann G, Hesse G. 1926. Die abhaengigkeit der viscositaet von der temperatur bei unterkuehlten fluessigkeiten. Z Anorg Allg Chem 156:245-257.
71. Vogel H. 1921. Das temperaturabhaengigkeitsgesetz der viskositaet von fluessigkeiten. Phys Z 22:645-646.
72. Duggleby RG. 1984. Regression-analysis of nonlinear Arrhenius plots-An empirical-model and a computer-program. Comput Biol Med 14(4):447-455.
73. Roberts CJ. 2006. Nonnative protein aggregation: Pathways, kinetics, and stability prediction. In Misbehaving proteins: Protein (mis)folding, aggregation, and stability; Murphy RM, Tsai AM, Eds. New York: Springer Science + Business Media, LLC, pp 17-46.
74. Remmele RLJ, Balaban DJ, Zhang J, Shoshitaishvili A, Durst MJ. 2005. Method and apparatus for predicting aggregation kinetics of a biologically active material. Application: WO 2005/103686 A1: Amgen. pp 99.
75. IUPAC. 1996. Compendium of chemical terminology 68. 2nd ed., pp 174.
76. Privalov PL, Dragan AI. 2007. Microcalorimetry of biological macromolecules. Biophys Chem 126(1-3):16-24.
77. Privalov PL, Potekhin SA, Hirs CHW, Timasheff SN. 1986. Scanning microcalorimetry in studying temperature-induced changes in proteins. Methods in enzymology 131:4-51.
78. Bohmer R, Ngai KL, Angell CA, Plazek DJ. 1993. Nonexponential relaxations in strong and fragile glass formers. J Chem Phys 99(5):4201-4209.
79. Green JL, Fan J, Angell CA. 1994. The protein-glass analogy: New insight from homopeptide comparisons. J Phys Chem 98(51):13780-13790.
80. Byrne N, Wang L-M, Belieres J-P, Angell CA. 2007. Reversible folding-unfolding, aggregation protection, and multi-year stabilization, in high concentration protein solutions, using ionic liquids. Chem Commun (26):2714-2716.
81. Yoshioka S, Aso Y, Kojima S. 2001. Usefulness of the Kohlrausch-Williams-Watts stretched exponential function to describe protein aggregation in lyophilized formulations and the temperature dependence near the glass transition temperature. Pharm Res 18(3):256-260.
82. Peleg M, Engel R, Gonzalez-Martinez C, Corradini MG. 2002. Non-Arrhenius and non-WLF kinetics in food systems. J Sci Food Agric 82(12):1346-1355.
83. Angell CA. 1966. Free volume-entropy interpretation of the electrical conductance of aqueous electrolyte solutions in the concentration range 2-20 N. J Phys Chem 70(12):3988-3997.
84. Schiraldi A. 2002. Comparison between WLF and VTF expressions and related physical meaning. Spec Pub-Royal Soc Chem 281(Amorphous Food Pharm Syst):131-136.
85. Liu H, Jiang B, Liu M, Mao M, Mao X-a. 2007. The first application of the Vogel-Fulcher-Tammann equation to biological problem: A new interpretation of the temperature dependent hydrogen exchange rates of the thrombin-binding DNA. Phys Lett A 361:248-251.
86. Bond MD, Panek ME, Zhang Z, Wang D, Mehndiratta P, Zhao H, Gunton K, Ni A, Nedved ML, Burman S, Volkin DB. 2009. Evaluation of a dual-wavelength size exclusion HPLC method with improved sensitivity to detect protein aggregates and its use to better characterize degradation pathways of an IgG1 monoclonal antibody. J Pharm Sci 99(6):2582-2597.
87. Qi P, Volkin DB, Zhao H, Nedved ML, Hughes R, Bass R, Yi SC, Panek ME, Wang D, DalMonte P, Bond MD. 2009. Characterization of the photodegradation of a human IgG1 monoclonal antibody formulated as a high-concentration liquid dosage form. J Pharm Sci 98(9):3117-3130.
88. Bryant RAR, Hansen DE. 1996. Direct measurement of the uncatalyzed rate of hydrolysis of a peptide bond. J Am Chem Soc 118(23):5498-5499.
89. Caflisch A. 2006. Computational models for the prediction of polypeptide aggregation propensity. Curr Opin Chem Biol 10(5):437-444.
90. Tartaglia GG, Cavalli A, Pellarin R, Caflisch A. 2005. Prediction of aggregation rate and aggregation-prone segments in polypeptide sequences. Protein Sci 14(10):2723-2734.
91. Tartaglia GG, Vendruscolo M. 2008. The Zyggregator method for predicting protein aggregation propensities. Chem Soc Rev 37(7):1395-1401.
92. Fernandez-Escamilla A-M, Rousseau F, Schymkowitz J, Serrano L. 2004. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotech 22(10):1302-1306.