Forced degradation of therapeutic proteins

Journal of Pharmaceutical Sciences

Volumn 101, Issue 3, 2012, Pages 895-913

  Hawe, Andrea ^a,b   Wiggenhorn, Michael ^b   van de Weert, Marco ^c   Garbe, Joerg H O ^d   Mahler, Hanns Christian ^d   Jiskoot, Wim ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b Coriolis Pharma ^*  (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Analysis; Comparability studies; Deamidation; Forced degradation (stress testing); Oxidation; Protein aggregation; Protein formulation; Protein structure; Proteins stability

Indexed keywords

IMMUNOGLOBULIN G;

FREEZE DRYING; FREEZE THAWING; HUMIDITY; HYDROLYSIS; INCUBATION TEMPERATURE; LIGHT; LIGHT STRESS; MECHANICAL STRESS; OXIDATION; PH; PHOTODEGRADATION; PHOTOLYSIS; PROCESS CONTROL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN UNFOLDING; REVIEW; SHEAR STRENGTH; SHELF LIFE; TEMPERATURE STRESS; TRANSPORT STRESS;

EID: 84855864033     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.22812     Document Type: Review

References (170)

1. Barandun S, Kistler P, Jeunet F, Isliker H. 1962. Intravenous administration of human gamma-globulin. Vox Sang 7:157-174.
2. Ellis EF, Henney CS. 1969. Adverse reactions following administration of human gamma globulin. J Allergy 43(1):45-54.
3. Jacquemin MG, Saint-Remy JMR. 1998. Factor VIII immunogenicity. Haemophilia 4(4):552-557.
4. Milner RD. 1985. Growth hormone 1985. Br Med J (Clin Res Ed) 291(6509):1593-1594.
5. Cromwell ME, Hilario E, Jacobson F. 2006. Protein aggregation and bioprocessing. AAPS J 8(3):E572-E579.
6. Manning MC, Chou DK, Murphy BM, Payne RW, Katayama DS. 2010. Stability of protein pharmaceuticals: An update. Pharm Res 27(4):544-575.
7. Wang W, Nema S, Teagarden D. 2010. Protein aggregation-pathways and influencing factors. Int J Pharm 390(2):89-99.
8. Q1A(R2). 2003. Stability testing of new drug substances and products (second revision). Fed Regis 68(225):65717-65718.
9. Q5C. 1996. Quality of biotechnological products: Stability testing of biotechnological/biological products. Fed Regis 61:36466-36474.
10. Capelle MA, Gurny R, Arvinte T. 2007. High throughput screening of protein formulation stability: practical considerations. Eur J Pharm Biopharm 65(2):131-148.
11. Capelle MA, Gurny R, Arvinte T. 2009. A high throughput protein formulation platform: Case study of Salmon calcitonin. Pharm Res 26(1):118-128.
12. Zhao H, Graf O, Milovic N, Luan XS, Bluemel M, Smolny M, Forrer K. 2010. Formulation development of antibodies using robotic system and high-throughput laboratory (HTL). J Pham Sci 99(5):2279-2294.
13. Treuheit MJ, Kosky AA, Brems DN. 2002. Inverse relationship of protein concentration and aggregation. Pharm Res 19(4):511-516.
14. Wang W, Wang YJ, Wang DQ. 2008. Dual effects of Tween 80 on protein stability. Int J Pharm 347(1-2):31-38.
15. Luo Q, Joubert MK, Stevenson R, Ketchem RR, Narhi LO, Wypych J. 2011. Chemical modifications in therapeutic protein aggregates generated under different stress conditions. J Biol Chem 286(28):25134-25144.
16. Joubert MK, Luo Q, Nashed-Samuel Y, Wypych J, Narhi LO. 2011. Classification and characterization of therapeutic antibody aggregates. J Biol Chem 286(28):25118-25133.
17. Carpenter JF, Randolph TW, Jiskoot W, Crommelin DJA, Middaugh CR, Winter G, Fan YX, Kirshner S, Verthelyi D, Kozlowski S, Clouse KA, Swann PG, Rosenberg A, Cherney B. 2009. Overlooking subvisible particles in therapeutic protein products: Gaps that may compromise product quality. J Pharm Sci 98(4):1201-1205.
18. Mahler HC, Friess W, Grauschopf U, Kiese S. 2009. Protein aggregation: Pathways, induction factors and analysis. J Pharm Sci 98(9):2909-2934.
19. Philo JS. 2006. Is any measurement method optimal for all aggregate sizes and types? AAPS J 8(3):E564-E571.
20. Philo JS. 2009. A critical review of methods for size characterization of non-particulate protein aggregates. Curr Pharm Biotechnol 10(4):359-372.
21. den Engelsman J, Garidel P, Smulders R, Koll H, Smith B, Bassarab S, Seidl A, Hainzl O, Jiskoot W. 2010. Strategies for the assessment of protein aggregates in pharmaceutical biotech product development. Pharm Res 28(4):920-933.
22. Carpenter JF, Randolph TW, Jiskoot W, Crommelin DJ, 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.
23. Q5E. 2004. Comparability of biotechnological/biological products subject to changes in their manufacturing process. Fed Regis 70(125):37861-37862.
24. Klick S, Mujselaar PG, Waterval J, Eichinger T, Korn C, Gerding TK, Debets AJ, Sänger-van de Griend C, van den Beld C, Somsen GW, De Jong GJ. 2005. Toward a generic approach for stress testing of drug substance and drug product. Pharm Technol 29:48-64.
25. Q1B. 1997. Stability testing: Photostability testing of new drug substances and products. Fed Regis 62(95):27115-27122.
26. ASTM. 2007. D 999-08: Standard test methods for vibration testing of shipping containers. ASTM International.
27. ASTM. 2008. D 4169-09: Standard practice for performance testing of shipping containers and systems. ASTM International.
28. Jaenicke R. 1991. Protein stability and molecular adaptation to extreme conditions. Eur J Biochem 202(3):715-728.
29. Jaenicke R. 2000. Stability and stabilization of globular proteins in solution. J Biotechnol 79(3):193-203.
30. Schellman JA. 1997. Temperature, stability, and the hydrophobic interaction. Biophys J 73(6):2960-2964.
31. Schoen A, Velazquez-Campoy A. 2005. Calorimetry. In Methods for structural analysis of protein pharmaceuticals, Jiskoot W, Crommelin DJA, Eds. Arlington, VA: AAPS Press, pp. 573-589.
32. Burton L, Gandhi R, Duke G, Paborji M. 2007. Use of microcalorimetry and its correlation with size exclusion chromatography for rapid screening of the physical stability of large pharmaceutical proteins in solution. Pharm Dev Technol 12(3):265-273.
33. Remmele RL, Gombotz WR. 2000. Differential scanning calorimetry-A practical tool for elucidating stability of liquid biopharmaceuticals. Pharm Tech Eur 12:56-s65.
34. Vermeer AW, Norde W. 2000. The thermal stability of immunoglobulin: unfolding and aggregation of a multi-domain protein. Biophys J 78(1):394-404.
35. Matheus S, Friess W, Mahler HC. 2006. FTIR and nDSC as analytical tools for high-concentration protein formulations. Pharm Res 23(6):1350-1363.
36. Garidel P, Hegyi M, Bassarab S, Weichel M. 2008. A rapid, sensitive and economical assessment of monoclonal antibody conformational stability by intrinsic tryptophan fluorescence spectroscopy. Biotechnol J 3(9-10):1201-1211.
37. He F, Hogan S, Latypov RF, Narhi LO, Razinkov VI. 2010. High throughput thermostability screening of monoclonal antibody formulations. J Pharm Sci 99(4):1707-1720.
38. Fischer B. 1996. Folding of lysozyme. EXS 75:143-161.
39. Sharma VK, Kalonia DS. 2003. Temperature- and pH-induced multiple partially unfolded states of recombinant human interferon-alpha2a: Possible implications in protein stability. Pharm Res 20(11):1721-1729.
40. Ionescu RM, Vlasak J, Price C, Kirchmeier M. 2008. Contribution of variable domains to the stability of humanized IgG1 monoclonal antibodies. J Pharm Sci 97(4):1414-1426.
41. Vermeer AW, Norde W, van Amerongen A. 2000. The unfolding/denaturation of immunogammaglobulin of isotype 2b and its F(ab) and F(c) fragments. Biophys J 79(4):2150-2154.
42. Weiss WFT, Young TM, Roberts CJ. 2009. Principles, approaches, and challenges for predicting protein aggregation rates and shelf life. J Pharm Sci 98(4):1246-1277.
43. McCarthy D, Goddard DH, Embling PH, Holborow EJ. 1981. A simple procedure for assessing the stability of heat-aggregated IgG preparations. J Immunol Methods 41(1):75-79.
44. McCarthy D, Goddard DH, Pell BK, Holborow EJ. 1981. Intrinsically stable IgG aggregates. J Immunol Methods 41(1):63-74.
45. McCarthy DA, Drake AF. 1989. Spectroscopic studies on IgG aggregate formation. Mol Immunol 26(9):875-881.
46. 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.
47. Remmele RL, Jr., Nightlinger NS, Srinivasan S, Gombotz WR. 1998. Interleukin-1 receptor (IL-1R) liquid formulation development using differential scanning calorimetry. Pharm Res 15(2):200-208.
48. Goldberg DS, Bishop SM, Shah AU, Sathish HA. 2010. Formulation development of therapeutic monoclonal antibodies using high-throughput fluorescence and static light scattering techniques: Role of conformational and colloidal stability. J Pharm Sci 100(4)1306-1315.
49. Huus K, Havelund S, Olsen HB, van de Weert M, Frokjaer S. 2006. Chemical and thermal stability of insulin: Effects of zinc and ligand binding to the insulin zinc-hexamer. Pharm Res 23(11):2611-2620.
50. Singh S, Singh J. 2003. Effect of polyols on the conformational stability and biological activity of a model protein lysozyme. AAPS PharmSciTech 4(3):E42.
51. m (FTIR) measurements of high-concentration IgG1 antibody formulations as a formulation development tool. Pharm Res 23(7):1617-1627.
52. Papadimitrou A. 2001. Liquid pharmaceutical composition containing an erythropoietin derivative. PCT/EP2001/005187.
53. m plateau: a matter of thermal reversibility. Biochemistry 38(16):5241-5247.
54. Hawe A, Poole R, Romeijn S, Kasper P, van der Heijden R, Jiskoot W. 2009. Towards heat-stable oxytocin formulations: Analysis of degradation kinetics and identification of degradation products. Pharm Res 26(7):1679-1688.
55. 1H NMR. J Pharm Biomed Anal 29(3):487-494.
56. Thirumangalathu R, Krishnan S, Bondarenko P, Speed-Ricci M, Randolph TW, Carpenter JF, Brems DN. 2007. Oxidation of methionine residues in recombinant human interleukin-1 receptor antagonist: implications of conformational stability on protein oxidation kinetics. Biochemistry 46(21):6213-6224.
57. Fatouros A, Osterberg T, Mikaelsson M. 1997. Recombinant factor VIII SQ-inactivation kinetics in aqueous solution and the influence of disaccharides and sugar alcohols. Pharm Res 14(12):1679-1684.
58. 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.
59. Yoshioka S, Aso Y, Izutsu K, Kojima S. 1994. Is stability prediction possible for protein drugs-denaturation kinetics of beta-galactosidase in solution. Pharm Res 11(12):1721-1725.
60. Kayser V, Chennamsetty N, Voynov V, Helk B, Forrer K, Trout BL. 2011. Evaluation of a non-Arrhenius model for therapeutic monoclonal antibody aggregation. J Pharm Sci 100(7):2526-2542.
61. 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.
62. Bhatnagar BS, Bogner RH, Pikal MJ. 2007. Protein stability during freezing: separation of stresses and mechanisms of protein stabilization. Pharm Dev Technol 12(5):505-523.
63. Chang BS, Kendrick BS, Carpenter JF. 1996. Surface-induced denaturation of proteins during freezing and its inhibition by surfactants. J Pharm Sci 85(12):1325-1330.
64. Kueltzo LA, Wang W, Randolph TW, Carpenter JF. 2008. Effects of solution conditions, processing parameters, and container materials on aggregation of a monoclonal antibody during freeze-thawing. J Pharm Sci 97(5):1801-1812.
65. Sarciaux JM, Mansour S, Hageman MJ, Nail SL. 1999. Effects of buffer composition and processing conditions on aggregation of bovine IgG during freeze-drying. J Pharm Sci 88(12):1354-1361.
66. Strambini GB, Gabellieri E. 1996. Proteins in frozen solutions: Evidence of ice-induced partial unfolding. Biophys J 70(2):971-976.
67. Privalov PL. 1990. Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25(4):281-305.
68. Singh SK, Kolhe P, Mehta AP, Chico SC, Lary AL, Huang M. 2011. Frozen state storage instability of a monoclonal antibody: Aggregation as a consequence of trehalose crystallization and protein unfolding. Pharm Res 28(4):873-885.
69. Sundaramurthi P, Suryanarayanan R. 2010. Trehalose crystallization during freeze-drying: implications on lyoprotection. J Phys Chem Lett 1(2):510-514.
70. Piedmonte DM, Summers C, McAuley A, Karamujic L, Ratnaswamy G. 2007. Sorbitol crystallization can lead to protein aggregation in frozen protein formulations. Pharm Res 24(1):136-146.
71. Izutsu K, Heller MC, Randolph TW, Carpenter JF. 1998. Effect of salts and sugars on phase separation of polyvinylpyrrolidone-dextran solutions induced by freeze-concentration. J Chem Soc, Faraday Trans 94(3):411-417.
72. Maity H, Karkaria C, Davagnino J. 2009. Mapping of solution components, pH changes, protein stability and the elimination of protein precipitation during freeze-thawing of fibroblast growth factor 20. Int J Pharm 378(1-2):122-135.
73. Anchordoquy TJ, Carpenter JF. 1996. Polymers protect lactate dehydrogenase during freeze-drying by inhibiting dissociation in the frozen state. Arch Biochem Biophys 332(2):231-238.
74. Eriksson JH, Hinrichs WL, de Jong GJ, Somsen GW, Frijlink HW. 2003. Investigations into the stabilization of drugs by sugar glasses: III. The influence of various high-pH buffers. Pharm Res 20(9):1437-1443.
75. Kolhe P, Badkar A. 2011. Protein and solute distribution in drug substance containers during frozen storage and post-thawing: A tool to understand and define freezing-thawing parameters in biotechnology process development. Biotechnol Prog 27(2):494-504.
76. Pikal-Cleland KA, Cleland JL, Anchordoquy TJ, Carpenter JF. 2002. Effect of glycine on pH changes and protein stability during freeze-thawing in phosphate buffer systems. J Pharm Sci 91(9):1969-1979.
77. Gomez G, Pikal MJ, Rodriguez-Hornedo N. 2001. Effect of initial buffer composition on pH changes during far-from-equilibrium freezing of sodium phosphate buffer solutions. Pharm Res 18(1):90-97.
78. Pikal-Cleland KA, Rodriguez-Hornedo N, Amidon GL, Carpenter JF. 2000. Protein denaturation during freezing and thawing in phosphate buffer systems: Monomeric and tetrameric beta-galactosidase. Arch Biochem Biophys 384(2):398-406.
79. Eckhardt BM, Oeswein JQ, Bewley TA. 1991. Effect of freezing on aggregation of human growth hormone. Pharm Res 8(11):1360-1364.
80. Hawe A, Kasper JC, Friess W, Jiskoot W. 2009. Structural properties of monoclonal antibody aggregates induced by freeze-thawing and thermal stress. Eur J Pharm Sci 38(2):79-87.
81. Natalello A, Santarella R, Doglia SM, de Marco A. 2008. Physical and chemical perturbations induce the formation of protein aggregates with different structural features. Protein Expr Purif 58(2):356-361.
82. Singh KS, Kolhe P, Wang W, Nema S. 2009. Freezing of biologics-A practitioner's review. Part II: Practical advice. Bioprocess Intl 7(10):34-42.
83. Singh SK, Kolhe P, Wang W, Nema S. 2009. Freezing of biologics-A practitioner's review. Part I: Fundamental aspects. Bioprocess Intl 7(9):32-44.
84. Jiang G, Akers M, Jain M, Guo J, Distler A, Swift R, Wadhwa MV, Jameel F, Patro S, Freund E. 2007. Mechanistic studies of glass vial breakage for frozen formulations. I. Vial breakage caused by crystallizable excipient mannitol. PDA J Pharm Sci Technol 61(6):441-451.
85. Cavatur RK, Vemuri NM, Pyne A, Chrzan Z, Toledo-Velasquez D, Suryanarayanan R. 2002. Crystallization behavior of mannitol in frozen aqueous solutions. Pharm Res 19(6):894-900.
86. Cao E, Chen Y, Cui Z, Foster PR. 2003. Effect of freezing and thawing rates on denaturation of proteins in aqueous solutions. Biotechnol Bioeng 82(6):684-690.
87. Kerwin BA, Heller MC, Levin SH, Randolph TW. 1998. Effects of Tween 80 and sucrose on acute short-term stability and long-term storage at -20 degrees C of a recombinant hemoglobin. J Pharm Sci 87(9):1062-1068.
88. Kreilgaard L, Jones LS, Randolph TW, Frokjaer S, Flink JM, Manning MC, Carpenter JF. 1998. Effect of Tween 20 on freeze-thawing- and agitation-induced aggregation of recombinant human factor XIII. J Pharm Sci 87(12):1597-1603.
89. Patapoff TW. 2010. Presentationon freeze-thawing of biologics at AAPS National Biotech Conference, San Francisco, CA.
90. Bam NB, Cleland JL, Yang J, Manning MC, Carpenter JF, Kelley RF, Randolph TW. 1998. Tween protects recombinant human growth hormone against agitation-induced damage via hydrophobic interactions. J Pharm Sci 87(12):1554-1559.
91. 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.
92. Eppler A, Weigandt M, Hanefeld A, Bunjes H. 2010. Relevant shaking stress conditions for antibody preformulation development. Eur J Pharm Biopharm 74(2):139-147.
93. Kiese S, Pappenberger A, Friess W, Mahler HC. 2010. Equilibrium studies of protein aggregates and homogeneous nucleation in protein formulation. J Pharm Sci 99(2):632-644.
94. Kiese S, Pappenberger A, Friess W, Mahler HC. 2008. Shaken, not stirred: Mechanical stress testing of an IgG1 antibody. J Pharm Sci 97(10):4347-4366.
95. Mahler HC, Muller R, Friess W, Delille A, Matheus S. 2005. Induction and analysis of aggregates in a liquid IgG1-antibody formulation. Eur J Pharm Biopharm 59(3):407-417.
96. Mahler HC, Senner F, Maeder K, Mueller R. 2009. Surface activity of a monoclonal antibody. J Pharm Sci 98(12):4525-4533.
97. Sluzky V, Klibanov AM, Langer R. 1992. Mechanism of insulin aggregation and stabilization in agitated aqueous solutions. Biotechnol Bioeng 40(8):895-903.
98. Maruyama T, Katoh S, Nakajima M, Nabetani H. 2001. Mechanism of bovine serum albumin aggregation during ultrafiltration. Biotechnol Bioeng 75(2):233-238.
99. Colombie S, Gaunand A, Lindet B. 2001. Lysozyme inactivation under mechanical stirring: effect of physical and molecular interfaces. Enzyme Microb Technol 28(9-10):820-826.
100. Ishikawa T, Kobayashi N, Osawa C, Sawa E, Wakamatsu K. 2010. Prevention of stirring-induced microparticle formation in monoclonal antibody solutions. Biol Pharm Bull 33(6):1043-1046.
101. Toth SI, Smith LA, Ahmed SA. 2009. Extreme sensitivity of botulinum neurotoxin domains towards mild agitation. J Pharm Sci 98(9):3302-3311.
102. Tyagi AK, Randolph TW, Dong A, Maloney KM, Hitscherich C, Jr., Carpenter JF. 2009. IgG particle formation during filling pump operation: A case study of heterogeneous nucleation on stainless steel nanoparticles. J Pharm Sci 98(1):94-104.
103. Meireles M, Aimar P, Sanchez V. 1991. Albumin denaturation during ultrafiltration: Effects of operating conditions and consequences on membrane fouling. Biotechnol Bioeng 38(5):528-534.
104. Morar-Mitrica S, Brisbane C, Nesta DP, Ketkar A. 2009. Biophysical approaches to the detection and characterization of particles in an antibody solution. Am Pharm Rev 12(7):34-38.
105. Loksztejn A, Dzwolak W. 2010. Vortex-induced formation of insulin amyloid superstructures probed by time-lapse atomic force microscopy and circular dichroism spectroscopy. J Mol Biol 395(3):643-655.
106. Charman SA, Mason KL, Charman WN. 1993. Techniques for assessing the effects of pharmaceutical excipients on the aggregation of porcine growth hormone. Pharm Res 10(7):954-962.
107. Katakam M, Banga AK. 1997. Use of poloxamer polymers to stabilize recombinant human growth hormone against various processing stresses. Pharm Dev Technol 2(2):143-149.
108. Gulseren I, Guzey D, Bruce BD, Weiss J. 2007. Structural and functional changes in ultrasonicated bovine serum albumin solutions. Ultrason Sonochem 14(2):173-183.
109. Stathopulos PB, Scholz GA, Hwang YM, Rumfeldt JA, Lepock JR, Meiering EM. 2004. Sonication of proteins causes formation of aggregates that resemble amyloid. Protein Sci 13(11):3017-3027.
110. Ashton L, Dusting J, Imomoh E, Balabani S, Blanch EW. 2009. Shear-induced unfolding of lysozyme monitored in situ. Biophys J 96(10):4231-4236.
111. Biddlecombe JG, Craig AV, Zhang H, Uddin S, Mulot S, Fish BC, Bracewell DG. 2007. Determining antibody stability: Creation of solid-liquid interfacial effects within a high shear environment. Biotechnol Prog 23(5):1218-1222.
112. Biddlecombe JG, Smith G, Uddin S, Mulot S, Spencer D, Gee C, Fish BC, Bracewell DG. 2009. Factors influencing antibody stability at solid-liquid interfaces in a high shear environment. Biotechnol Prog 25(5):1499-1507.
113. Maa YF, Hsu CC. 1996. Effect of high shear on proteins. Biotechnol Bioeng 51(4):458-465.
114. Maa YF, Hsu CC. 1997. Protein denaturation by combined effect of shear and air-liquid interface. Biotechnol Bioeng 54(6):503-512.
115. Thomas CR, Geer D. 2010. Effect of shear on proteins on solution. Biotechnol Lett 33(3):443-456.
116. Bee JS, Stevenson JL, Mehta B, Svitel J, Pollastrini J, Platz R, Freund E, Carpenter JF, Randolph TW. 2009. Response of a concentrated monoclonal antibody formulation to high shear. Biotechnol Bioeng 103(5):936-943.
117. Clarkson JR, Cui ZF, Darton RC. 1999. Protein denaturation in foam. J Colloid Interface Sci 215(2):333-338.
118. Rathore N, Rajan RS. 2008. Current perspectives on stability of protein drug products during formulation, fill and finish operations. Biotechnol Prog 24(3):504-514.
119. Bee JS, Chiu D, Sawicki S, Stevenson JL, Chatterjee K, Freund E, Carpenter JF, Randolph TW. 2009. Monoclonal antibody interactions with micro- and nanoparticles: Adsorption, aggregation, and accelerated stress studies. J Pharm Sci 98(9):3218-3238.
120. Lam XM, Yang JY, Cleland JL. 1997. Antioxidants for prevention of methionine oxidation in recombinant monoclonal antibody HER2. J Pharm Sci 86(11):1250-1255.
121. Huang M, Horwitz TS, Zweiben C, Singh SK. 2011. Impact of extractables/leachables from filters on stability of protein formulations. J Pharm Sci 100(11):4617-4630.
122. Bee JS, Randolph TW, Carpenter JF, Bishop SM, Dimitrova MN. 2011. Effects of surfaces and leachables on the stability of biopharmaceuticals. J Pharm Sci. Online first DOI:10.1002/jps.22597.
123. Duncan MR, Lee JM, Warchol MP. 1995. Influence of surfactants upon protein/peptide adsorption to glass and polypropylene. Int J Pharm 120:179-188.
124. Johnston TP. 1996. Adsorption of recombinant human granulocyte colony stimulating factor (rhG-CSF) to polyvinyl chloride, polypropylene, and glass: Effect of solvent additives. PDA J Pharm Sci Technol 50(4):238-245.
125. Zhou B, Pellett S, Tepp WH, Zhou H, Johnson EA, Janda KD. 2008. Delineating the susceptibility of botulinum neurotoxins to denaturation through thermal effects. FEBS Lett 582(10):1526-1531.
126. Bee JS, Davis M, Freund E, Carpenter JF, Randolph TW. 2010. Aggregation of a monoclonal antibody induced by adsorption to stainless steel. Biotechnol Bioeng 105(1):121-129.
127. Jones LS, Kaufmann A, Middaugh CR. 2005. Silicone oil induced aggregation of proteins. J Pharm Sci 94(4):918-927.
128. Ludwig DB, Carpenter JF, Hamel JB, Randolph TW. 2010. Protein adsorption and excipient effects on kinetic stability of silicone oil emulsions. J Pharm Sci 99(4):1721-1733.
129. Thirumangalathu R, Krishnan S, Ricci MS, Brems DN, Randolph TW, Carpenter JF. 2009. Silicone oil- and agitation-induced aggregation of a monoclonal antibody in aqueous solution. J Pharm Sci 98(9):3167-3181.
130. Jiang Y, Nashed-Samuel Y, Li C, Liu W, Pollastrini J, Mallard D, Wen ZQ, Fujimori K, Pallitto M, Donahue L, Chu G, Torraca G, Vance A, Mire-Sluis T, Freund E, Davis J, Narhi L. 2009. Tungsten-induced protein aggregation: solution behavior. J Pharm Sci 98(12):4695-4710.
131. Zhou S, Zhang B, Sturm E, Teagarden DL, Schoneich C, Kolhe P, Lewis LM, Muralidhara BK, Singh SK. 2010. Comparative evaluation of disodium edetate and diethylenetriaminepentaacetic acid as iron chelators to prevent metal-catalyzed destabilization of a therapeutic monoclonal antibody. J Pharm Sci 99(10):4239-4250.
132. Auge KB, Blake-Haskins AW, Devine S, Rizvi S, Li YM, Hesselberg M, Orvisky E, Affleck RP, Spitznagel TM, Perkins MD. 2011. Demonstrating the stability of albinterferon alfa-2b in the presence of silicone oil. J Pharm Sci Online first DOI:10.1002/jps.22704.
133. Kerwin BA. 2008. Polysorbates 20 and 80 used in the formulation of protein biotherapeutics: structure and degradation pathways. J Pharm Sci 97(8):2924-2935.
134. Wasylaschuk WR, Harmon PA, Wagner G, Harman AB, Templeton AC, Xu H, Reed RA. 2007. Evaluation of hydroperoxides in common pharmaceutical excipients. J Pharm Sci 96(1):106-116.
135. Majumdar S, Ford BM, Mar KD, Sullivan VJ, Ulrich RG, D'Souza A J. 2011. Evaluation of the effect of syringe surfaces on protein formulations. J Pharm Sci 100(7):2563-2573.
136. Liu D, Ren D, Huang H, Dankberg J, Rosenfeld R, Cocco MJ, Li L, Brems DN, Remmele RL. 2008. Structure and stability changes of human IgG1 Fc as a consequence of methionine oxidation. Biochemistry 47(18):5088-5100.
137. Hawkins CL, Davies MJ. 2001. Generation and propagation of radical reactions on proteins. Biochim Biophys Acta 1504(2-3):196-219.
138. Stadtman ER. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 62:797-821.
139. Hovorka S, Schoneich C. 2001. Oxidative degradation of pharmaceuticals: theory, mechanisms and inhibition. J Pharm Sci 90(3):253-269.
140. Ji JA, Zhang B, Cheng W, Wang YJ. 2009. Methionine, tryptophan, and histidine oxidation in a model protein, PTH: Mechanisms and stabilization. J Pharm Sci 98(12):4485-4500.
141. Zhao F, Ghezzo-Schoneich E, Aced GI, Hong J, Milby T, Schoneich C. 1997. Metal-catalyzed oxidation of histidine in human growth hormone. Mechanism, isotope effects, and inhibition by a mild denaturing alcohol. J Biol Chem 272(14):9019-9029.
142. Jensen JL, Kolvenbach C, Roy S, Schoneich C. 2000. Metal-catalyzed oxidation of brain-derived neurotrophic factor (BDNF): analytical challenges for the identification of modified sites. Pharm Res 17(2):190-196.
143. Ph. Eur. 2007. Interferon alfa-2 concentrated solution. Eur Pharmacopoiea 62:2150-2153.
144. Chu JW, Brooks BR, Trout BL. 2004. Oxidation of methionine residues in aqueous solutions: Free methionine and methionine in granulocyte colony-stimulating factor. J Am Chem Soc 126(50):16601-16607.
145. Hermeling S, Aranha L, Damen JM, Slijper M, Schellekens H, Crommelin DJ, Jiskoot W. 2005. Structural characterization and immunogenicity in wild-type and immune tolerant mice of degraded recombinant human interferon alpha2b. Pharm Res 22(12):1997-2006.
146. Mulinacci F, Capelle MA, Gurny R, Drake AF, Arvinte T. 2011. Stability of human growth hormone: Influence of methionine oxidation on thermal folding. J Pharm Sci 100(2):451-463.
147. Mulinacci F, Bell SE, Capelle MA, Gurny R, Arvinte T. 2011. Oxidized recombinant human growth hormone that maintains conformational integrity. J Pharm Sci 100(1):110-122.
148. Griffiths SW, Cooney CL. 2002. Relationship between protein structure and methionine oxidation in recombinant human alpha 1-antitrypsin. Biochemistry 41(20):6245-6252.
149. 2 in its falloff range and of its secondary reactions. Phys Chem Chem Phys 4(18):4392-4398.
150. Keck RG. 1996. The use of t-butyl hydroperoxide as a probe for methionine oxidation in proteins. Anal Biochem 236(1):56-62.
151. Li S, Nguyen TH, Schoneich C, Borchardt RT. 1995. Aggregation and precipitation of human relaxin induced by metal-catalyzed oxidation. Biochemistry 34(17):5762-5772.
152. Kerwin BA, Remmele RL, Jr. 2007. Protect from light: Photodegradation and protein biologics. J Pharm Sci 96(6):1468-1479.
153. Baertschi SW, Alsante KM, Tonnesen HH. 2010. A critical assessment of the ICH guideline on photostability testing of new drug substances and products (Q1B): Recommendation for revision. J Pharm Sci 99(7):2934-2940.
154. Parti R, Ardosa J, Yang L, Mankarious S. 2000. In vitro stability of recombinant human factor VIII (recombinate). Haemophilia 6(5):513-522.
155. Kim HH, Lee YM, Suh JK, Song NW. 2007. Photodegradation mechanism and reaction kinetics of recombinant human interferon-alpha2a. Photochem Photobiol Sci 6(2):171-180.
156. 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.
157. Chang JY, Xiao NJ, Zhu M, Zhang J, Hoff E, Russell SJ, Katta V, Shire SJ. 2010. Leachables from saline-containing IV bags can alter therapeutic protein properties. Pharm Res 27(11):2402-2413.
158. Jenke DR, Zietlow D, Garber MJ, Sadain S, Reiber D, Terbush W. 2007. Accumulation of organic compounds leached from plastic materials used in biopharmaceutical process containers. PDA J Pharm Sci Technol 61(4):286-302.
159. Nuijen B, Bouma M, Manada C, Jimeno JM, Lazaro LL, Bult A, Beijnen JH. 2001. Compatibility and stability of the investigational polypeptide marine anticancer agent kahalalide F in infusion devices. Invest New Drugs 19(4):273-281.
160. Stickelmeyer MP, Graf CJ, Frank BH, Ballard RL, Storms SM. 2000. Stability of U-10 and U-50 dilutions of insulin lispro. Diabetes Technol Ther 2(1):61-66.
161. Corbo DC, Suddith RL, Sharma B, Naso RB. 1992. Stability, potency, and preservative effectiveness of epoetin alfa after addition of a bacteriostatic diluent. Am J Hosp Pharm 49(6):1455-1458.
162. Ohls RK, Christensen RD. 1996. Stability of human recombinant epoetin alfa in commonly used neonatal intravenous solutions. Ann Pharmacother 30(5):466-468.
163. Ling J, Hu M., Hagerup T, Campbell RK. 1999. Lispro insulin: Adsorption and stability in selected intravenous devices. Diabetes Edu 25(2):237-245.
164. Tzannis ST, Hrushesky WJ, Wood PA, Przybycien TM. 1996. Irreversible inactivation of interleukin 2 in a pump-based delivery environment. Proc Natl Acad Sci USA 93(11):5460-5465.
165. Vlasveld LT, Beijnen JH, Sein JJ, Rankin EM, Melief CJ, Hekman A. 1993. Reconstitution of recombinant interleukin-2 (rIL-2): |A comparative study of various rIL-2 muteins. Eur J Cancer 29A(14):1977-1979.
166. McLeod AG, Walker IR, Zheng S, Hayward CP. 2000. Loss of factor VIII activity during storage in PVC containers due to adsorption. Haemophilia 6(2):89-92.
167. Maddux NR, Joshi SB, Volkin DB, Ralston JP, Middaugh CR. 2011. Multidimensional methods for the formulation of biopharmaceuticals and vaccines. J Pharm Sci Online first DOI:10.1002/jps.22618.
168. 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.
169. Quan C, Alcala E, Petkovska I, Matthews D, Canova-Davis E, Taticek R, Ma S. 2008. A study in glycation of a therapeutic recombinant humanized monoclonal antibody: Where it is, how it got there, and how it affects charge-based behavior. Anal Biochem 373(2):179-191.
170. Harris RJ, Kabakoff B, Macchi FD, Shen FJ, Kwong M, Andya JD, Shire SJ, Bjork N, Totpal K, Chen AB. 2001. Identification of multiple sources of charge heterogeneity in a recombinant antibody. J Chromatogr B 752(2):233-245.