Physicochemical factors of bioprocessing impact the stability of therapeutic proteins

Adam, 2021, Effects of shear rate and protein concentration on amyloidogenesis via interfacial shear, J. Phys. Chem. B, 125, 10355, 10.1021/acs.jpcb.1c05171 Alam, 2019, Deamidation can compromise antibody colloidal stability and enhance aggregation in a pH-dependent manner, Mol. Pharm., 16, 1939, 10.1021/acs.molpharmaceut.8b01311 Alam, 2020, Unique impacts of methionine oxidation, tryptophan oxidation, and asparagine deamidation on antibody stability and aggregation, J. Pharm. Sci., 109, 656, 10.1016/j.xphs.2019.10.051 Amritkar, 2020, Engineering staphylococcal protein A for high-throughput affinity purification of monoclonal antibodies, Biotechnol. Adv., 44, 107632, 10.1016/j.biotechadv.2020.107632 Arosio, 2012, On the role of salt type and concentration on the stability behavior of a monoclonal antibody solution, Biophys. Chem., 168-169, 19, 10.1016/j.bpc.2012.05.004 Balaraj, 2017, Surface shear viscosity as a macroscopic probe of amyloid fibril formation at a fluid interface, Soft Matter, 13, 1780, 10.1039/C6SM01831A Bandi, 2019, 2D NMR analysis of the effect of asparagine deamidation versus methionine oxidation on the structure, stability, aggregation, and function of a therapeutic protein, Mol. Pharm., 16, 4621, 10.1021/acs.molpharmaceut.9b00719 Bansal, 2020, Impact of mAb aggregation on its biological activity: rituximab as a case study, J. Pharm. Sci., 109, 2684, 10.1016/j.xphs.2020.05.015 Bansal, 2020, Population balance modelling of aggregation of monoclonal antibody based therapeutic proteins, Chem. Eng. Sci., 216, 115479, 10.1016/j.ces.2020.115479 Bee, 2010, Aggregation of a monoclonal antibody induced by adsorption to stainless steel, Biotechnol. Bioeng., 105, 121, 10.1002/bit.22525 Benson, 2020, Amyloid nomenclature 2020: update and recommendations by the International Society of Amyloidosis (ISA) nomenclature committee, Amyloid, 27, 217, 10.1080/13506129.2020.1835263 Borzova, 2016, Kinetics of thermal denaturation and aggregation of bovine serum albumin, PLoS One, 11, 10.1371/journal.pone.0153495 Bouchard, 2000, Formation of insulin amyloid fibrils followed by FTIR simultaneously with CD and electron microscopy, Protein Sci., 9, 1960, 10.1110/ps.9.10.1960 Brummitt, 2011, Predicting accelerated aggregation rates for monoclonal antibody formulations, and challenges for low-temperature predictions, J. Pharm. Sci., 100, 4234, 10.1002/jps.22633 Campesi, 2009, Determination of the average shear rate in a stirred and aerated tank bioreactor, Bioprocess Biosyst. Eng., 32, 241, 10.1007/s00449-008-0242-4 Cao, 2019, Food protein amyloid fibrils: origin, structure, formation, characterization, applications and health implications, Adv. Colloid Interf. Sci., 269, 334, 10.1016/j.cis.2019.05.002 Chaudhary, 2021, Protein immobilization on graphene oxide or reduced graphene oxide surface and their applications: influence over activity, structural and thermal stability of protein, Adv. Colloid Interf. Sci., 289, 102367, 10.1016/j.cis.2021.102367 Cromwell, 2006, Protein aggregation and bioprocessing, AAPS J., 8, E572, 10.1208/aapsj080366 Defante, 2020, The impact of the metal interface on the stability and quality of a therapeutic fusion protein, Mol. Pharm., 17, 569 Doran, 2013 Eronina, 2020, Effect of arginine on stability and aggregation of muscle glycogen phosphorylase b, Int. J. Biol. Macromol., 165, 365, 10.1016/j.ijbiomac.2020.09.101 Farruggia, 2001, The participation of human serum albumin domains in chemical and thermal unfolding, J. Protein Chem., 20, 81, 10.1023/A:1011000317042 Fernandez-Cerezo, 2020, The prediction of the operating conditions on the permeate flux and on protein aggregation during membrane processing of monoclonal antibodies, J. Membr. Sci., 596, 117606, 10.1016/j.memsci.2019.117606 Fukuda, 2014, Thermodynamic and fluorescence analyses to determine mechanisms of IgG1 stabilization and destabilization by arginine, Pharm. Res., 31, 992, 10.1007/s11095-013-1221-2 Gancar, 2020, Amyloid aggregation of insulin: an interaction study of green tea constituents, Sci. Rep., 10, 1, 10.1038/s41598-020-66033-6 Grigolato, 2020, Synergistic effects of flow and interfaces on antibody aggregation, Biotechnol. Bioeng., 117, 417, 10.1002/bit.27212 Grigolato, 2021, The role of surfaces on amyloid formation, Biophys. Chem., 270, 106533, 10.1016/j.bpc.2020.106533 Gupta, 2014, Intermediate conformation between native β-sheet and non-native α-helix is a precursor of trifluoroethanol-induced aggregation of human carbonic anhydrase-II, Biochem. Biophys. Res. Commun., 449, 126, 10.1016/j.bbrc.2014.04.160 Ha, 2022, Factors affecting the quality of therapeutic proteins in recombinant Chinese hamster ovary cell culture, Biotechnol. Adv., 54, 107831, 10.1016/j.biotechadv.2021.107831 Hamilton-Brown, 2008, How does shear affect Aβ fibrillogenesis?, J. Phys. Chem. B, 112, 16249, 10.1021/jp805257n Hasan, 2020, Surface modification of Ti6Al4V by forming hybrid self-assembled monolayers and its effect on collagen-I adsorption, osteoblast adhesion and integrin expression, Appl. Surf. Sci., 505, 144611, 10.1016/j.apsusc.2019.144611 Hasan, 2018, Effect of functional groups of self-assembled monolayers on protein adsorption and initial cell adhesion, ACS Biomater. Sci. Eng., 4, 3224, 10.1021/acsbiomaterials.8b00795 Hasan, 2018, Surface functionalization of Ti6Al4V via self-assembled monolayers for improved protein adsorption and fibroblast adhesion, Langmuir, 34, 3494, 10.1021/acs.langmuir.7b03152 Hédoux, 2012, In situ monitoring of proteins during lyophilization using micro-Raman spectroscopy: a description of structural changes induced by dehydration, J. Pharm. Sci., 101, 2316, 10.1002/jps.23172 Hill, 2006, Shear flow induces amyloid fibril formation, Biomacromolecules, 7, 10, 10.1021/bm0505078 Homchaudhuri, 2006, Slow aggregation of lysozyme in alkaline pH monitored in real time employing the fluorescence anisotropy of covalently labelled dansyl probe, FEBS Lett., 580, 2097, 10.1016/j.febslet.2006.03.012 Israeli-Ruimy, 2017, Complexity of the Ruminococcus flavefaciens FD-1 cellulosome reflects an expansion of family-related protein-protein interactions, Sci. Rep., 7, 42355, 10.1038/srep42355 Jayaraman, 2014, Agitation-induced aggregation and subvisible particulate formation in model proteins, Eur. J. Pharm. Biopharm., 87, 299, 10.1016/j.ejpb.2014.01.004 Jha, 2013, Characterization of amyloid formation by glucagon-like peptides: role of basic residues in heparin-mediated aggregation, Biochemistry, 52, 8800, 10.1021/bi401398k Jin, 2019, Protein aggregation and mitigation strategy in low pH viral inactivation for monoclonal antibody purification, mAbs, 11, 1479, 10.1080/19420862.2019.1658493 Kalonia, 2018, Protein adsorption and layer formation at the stainless steel–solution interface mediates shear-induced particle formation for an IgG1 monoclonal antibody, Mol. Pharm., 15, 1319, 10.1021/acs.molpharmaceut.7b01127 Kannan, 2019, Linking aggregation and interfacial properties in monoclonal antibody-surfactant formulations, J. Colloid Interface Sci., 550, 128, 10.1016/j.jcis.2019.04.060 Karmakar, 2019, Proline functionalized gold nanoparticles modulates lysozyme fibrillation, Colloids Surf. B: Biointerfaces, 174, 401, 10.1016/j.colsurfb.2018.11.032 Khan, 2019, Millimolar concentration of sodium dodecyl sulfate inhibit thermal aggregation in hen egg white lysozyme via increased α-helicity, Colloids Surf. A Physicochem. Eng. Asp., 572, 167, 10.1016/j.colsurfa.2019.03.085 Kim, 2020, Do not flick or drop off-label use plastic syringes in handling therapeutic proteins before administration, Int. J. Pharm., 587, 119704, 10.1016/j.ijpharm.2020.119704 Koepf, 2017, The film tells the story: physical-chemical characteristics of IgG at the liquid-air interface, Eur. J. Pharm. Biopharm., 119, 396, 10.1016/j.ejpb.2017.07.006 Kuzman, 2021, Long-term stability predictions of therapeutic monoclonal antibodies in solution using Arrhenius-based kinetics, Sci. Rep., 11, 20534, 10.1038/s41598-021-99875-9 Le Basle, 2020, Physicochemical stability of monoclonal antibodies: a review, J. Pharm. Sci., 109, 169, 10.1016/j.xphs.2019.08.009 Lee, 2007, A three-stage kinetic model of amyloid fibrillation, Biophys. J., 92, 3448, 10.1529/biophysj.106.098608 Liu, 1999, Oligopeptide-repeat expansions modulate ‘protein-only’inheritance in yeast, Nature, 400, 573, 10.1038/23048 Loveday, 2010, Tuning the properties of β-lactoglobulin nanofibrils with pH, NaCl and CaCl2, Int. Dairy J., 20, 571, 10.1016/j.idairyj.2010.02.014 Mahler, 2009, Protein aggregation: pathways, induction factors and analysis, J. Pharm. Sci., 98, 2909, 10.1002/jps.21566 Manikwar, 2013, Correlating excipient effects on conformational and storage stability of an IgG1 monoclonal antibody with local dynamics as measured by hydrogen/deuterium-exchange mass spectrometry, J. Pharm. Sci., 102, 2136, 10.1002/jps.23543 Maruyama, 2001, Mechanism of bovine serum albumin aggregation during ultrafiltration, Biotechnol. Bioeng., 75, 233, 10.1002/bit.10001 Myers, 1996, Hydrogen bonding stabilizes globular proteins, Biophys. J., 71, 2033, 10.1016/S0006-3495(96)79401-8 Ni, 2015, Effect of temperature, calcium and protein concentration on aggregation of whey protein isolate: formation of gel-like micro-particles, Int. Dairy J., 51, 8, 10.1016/j.idairyj.2015.07.003 Nielsen, 2001, Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism, Biochemistry, 40, 6036, 10.1021/bi002555c Nitika, 2021, Raman spectroscopy for in situ, real time monitoring of protein aggregation in lyophilized biotherapeutic products, Int. J. Biol. Macromol., 179, 309, 10.1016/j.ijbiomac.2021.02.214 Noormägi, 2015, Insulin fibrillization at acidic and physiological pH values is controlled by different molecular mechanisms, Protein J., 34, 398, 10.1007/s10930-015-9634-x Pal, 2020, Thermal stability modulation of the native and chemically-unfolded state of bovine serum albumin by amino acids, Phys. Chem. Chem. Phys., 22, 179, 10.1039/C9CP04887A Pandey, 2012 Pandey, 2011, Hybrid surface from self-assembled layer and its effect on protein adsorption, Mater. Sci. Eng. C, 257, 4731 Pandey, 2012, Surface chemistry at the nanometer scale influences insulin aggregation, Colloids Surf. B: Biointerfaces, 100, 69, 10.1016/j.colsurfb.2012.05.022 Pandey, 2013, Properties of adsorbed bovine serum albumin and fibrinogen on self-assembled monolayers, J. Phys. Chem. C, 117, 6151, 10.1021/jp309483p Paul, 2018, Identification of process conditions influencing protein aggregation in Chinese hamster ovary cell culture, Biotechnol. Bioeng., 115, 1173, 10.1002/bit.26534 Pérez, 2006, Shear rate in stirred tank and bubble column bioreactors, Chem. Eng. J., 124, 1, 10.1016/j.cej.2006.07.002 Pham, 2020, Protein aggregation and immunogenicity of biotherapeutics, Int. J. Pharm., 585, 119523, 10.1016/j.ijpharm.2020.119523 Poland, 2002, Contribution of secondary structure to the heat capacity and enthalpy distribution of the unfolded state in proteins, Biopolymers Original Res. Biomol., 63, 59 Pronchik, 2010, In vitro formation of amyloid from α-synuclein is dominated by reactions at hydrophobic interfaces, J. Am. Chem. Soc., 132, 9797, 10.1021/ja102896h Quevedo, 2020, Denaturation behavior and kinetics of single-and multi-component protein systems at extrusion-like conditions, Polymers, 12, 2145, 10.3390/polym12092145 Ray, 2014, Design of heat shock-resistant surfaces to prevent protein aggregation: enhanced chaperone activity of immobilized α-crystallin, Bioconjug. Chem., 25, 888, 10.1021/bc500097q Rechendorff, 2006, Enhancement of protein adsorption induced by surface roughness, Langmuir, 22, 10885, 10.1021/la0621923 Roberts, 2014, Protein aggregation and its impact on product quality, Curr. Opin. Biotechnol., 30, 211, 10.1016/j.copbio.2014.08.001 Roffi, 2021, Adsorbed protein film on pump surfaces leads to particle formation during fill-finish manufacturing, Biotechnol. Bioeng., 118, 2947, 10.1002/bit.27801 Ross, 2004, Protein aggregation and neurodegenerative disease, Nat. Med., 10, S10, 10.1038/nm1066 Roy, 2019, The effect of the stoichiometric ratio of zinc towards the fibrillation of bovine serum albumin (BSA): a mechanistic insight, Int. J. Biol. Macromol., 123, 409, 10.1016/j.ijbiomac.2018.11.120 Santos, 2020, pH-dependent aggregation in intrinsically disordered proteins is determined by charge and lipophilicity, Cells, 9, 145, 10.3390/cells9010145 Senga, 2018, Suppression of aggregation of therapeutic monoclonal antibodies during storage by removal of aggregation precursors using a specific adsorbent of non-native IgG conformers, Bioconjug. Chem., 29, 3250, 10.1021/acs.bioconjchem.8b00360 Serio, 2000, Nucleated conformational conversion and the replication of conformational information by a prion determinant, Science, 289, 1317, 10.1126/science.289.5483.1317 Shah, 2020, Micro-and macro-viscosity relations in high concentration antibody solutions, Eur. J. Pharm. Biopharm., 153, 211, 10.1016/j.ejpb.2020.06.007 Sharma, 2021, Shear-induced aggregation of amyloid β (1–40) in a parallel plate geometry, J. Biomol. Struct. Dyn., 39, 6415, 10.1080/07391102.2020.1798814 Sharma, 2021, Thermomechanical process induces unfolding and fibrillation of bovine serum albumin, Food Hydrocoll., 112, 106294, 10.1016/j.foodhyd.2020.106294 Sheu, 2003, Energetics of hydrogen bonds in peptides, Proc. Natl. Acad. Sci., 100, 12683, 10.1073/pnas.2133366100 Shmool, 2021, An experimental approach probing the conformational transitions and energy landscape of antibodies: a glimmer of hope for reviving lost therapeutic candidates using ionic liquid, Chem. Sci., 12, 9528, 10.1039/D1SC02520A Simpson, 2020, Protein folding and assembly in confined environments: implications for protein aggregation in hydrogels and tissues, Biotechnol. Adv., 42, 107573, 10.1016/j.biotechadv.2020.107573 Singh, 2017, Deciphering the mechanistic insight into the stoichiometric ratio dependent behavior of Cu(II) on BSA fibrillation, Int. J. Biol. Macromol., 97, 662, 10.1016/j.ijbiomac.2017.01.045 Singh, 2018, Therapeutic advancement in Alzheimer disease: new hopes on the horizon?, CNS Neurol. Disord. Drug Targets (Formerly Curr. Drug Targets CNS Neurol. Dis.), 17, 571 Singla, 2016, Aggregation kinetics for IgG1-based monoclonal antibody therapeutics, AAPS J., 18, 689, 10.1208/s12248-016-9887-0 Smirnova, 2015, pH-responsive modulation of insulin aggregation and structural transformation of the aggregates, Biochimie, 109, 49, 10.1016/j.biochi.2014.12.006 Spadiut, 2020, Spatially resolved effects of protein freeze-thawing in a small-scale model using monoclonal antibodies, Pharmaceutics, 12, 382, 10.3390/pharmaceutics12040382 Stefani, 2004, Protein misfolding and aggregation: new examples in medicine and biology of the dark side of the protein world, Biochim. Biophys. Acta (BBA) - Mol. Basis Dis., 1739, 5, 10.1016/j.bbadis.2004.08.004 Svilenov, 2020, Orthogonal techniques to study the effect of pH, sucrose, and arginine salts on monoclonal antibody physical stability and aggregation during long-term storage, J. Pharm. Sci., 109, 584, 10.1016/j.xphs.2019.10.065 Tein, 2020, Competitive surface activity of monoclonal antibodies and nonionic surfactants at the air–water interface determined by interfacial rheology and neutron reflectometry, Langmuir, 36, 7814, 10.1021/acs.langmuir.0c00797 Thorat, 2020, Freezing-induced protein aggregation-role of pH shift and potential mitigation strategies, J. Control. Release, 323, 591, 10.1016/j.jconrel.2020.04.033 Torisu, 2017, Synergistic effect of cavitation and agitation on protein aggregation, J. Pharm. Sci., 106, 521, 10.1016/j.xphs.2016.10.015 Trumbore, 2020, Shear-induced amyloid aggregation in the brain: V. Are Alzheimer’s and other amyloid diseases initiated in the lower brain and brainstem by cerebrospinal fluid flow stresses?, J. Alzheimers Dis. (Preprint), 1 Trumbore, 2021, Shear-induced amyloid aggregation in the brain: V. Are Alzheimer’s and other amyloid diseases initiated in the lower brain and brainstem by cerebrospinal fluid flow stresses?, J. Alzheimers Dis., 79, 979, 10.3233/JAD-201025 Vetter, 2020, Cumulative deamidations of the major lens protein γS-crystallin increase its aggregation during unfolding and oxidation, Protein Sci., 29, 1945, 10.1002/pro.3915 Vuillemin, 2021, Improvement of the transglycosylation efficiency of a lacto-N-biosidase from bifidobacterium bifidum by protein engineering, Appl. Sci., 11, 11493, 10.3390/app112311493 Wälchli, 2020, Relationship of PEG-induced precipitation with protein-protein interactions and aggregation rates of high concentration mAb formulations at 5 C, Eur. J. Pharm. Biopharm., 151, 53, 10.1016/j.ejpb.2020.03.011 Wälchli, 2020, Understanding mAb aggregation during low pH viral inactivation and subsequent neutralization, Biotechnol. Bioeng., 117, 687, 10.1002/bit.27237 Walinda, 2020, Visualizing protein motion in Couette flow by all-atom molecular dynamics, Biochim. Biophys. Acta (BBA) Gen. Subj., 1864, 129383, 10.1016/j.bbagen.2019.06.006 Wechalekar, 2016, Systemic amyloidosis, Lancet, 387, 2641, 10.1016/S0140-6736(15)01274-X Wijayanti, 2019, Thermal denaturation, aggregation, and methods of prevention, 185 Xiao, 2020, Damage of proteins at the air/water interface: surface tension characterizes globulin interface stability, Int. J. Pharm., 584, 119445, 10.1016/j.ijpharm.2020.119445 Xu, 2020, Applications of small molecules in modulating productivity and product quality of recombinant proteins produced using cell cultures, Biotechnol. Adv., 43, 107577, 10.1016/j.biotechadv.2020.107577 Yao, 2020, Discovery and mechanism of a pH-dependent dual-binding-site switch in the interaction of a pair of protein modules, Sci. Adv., 6, 10.1126/sciadv.abd7182 Zaman, 2014, Nanoparticles in relation to peptide and protein aggregation, Int. J. Nanomedicine, 9, 899 Zeuner, 2019, Synthesis of human milk oligosaccharides: protein engineering strategies for improved enzymatic transglycosylation, Molecules, 24, 10.3390/molecules24112033 Zheng, 2017, Investigating the degradation behaviors of a therapeutic monoclonal antibody associated with pH and buffer species, AAPS PharmSciTech, 18, 42, 10.1208/s12249-015-0403-0