Multi-Attribute Method (MAM): An Emerging Analytical Workflow for Biopharmaceutical Characterization, Batch Release and cGMP Purity Testing at the Peptide and Intact Protein Level

References

• Baedeker, M.; Ringel, M. S.; Schulze, U. 2021 FDA Approvals: Value Driven by COVID-19 Vaccines. Nat. Rev. Drug Discov. 2022, 21, 90. DOI: 10.1038/d41573-022-00015-3.
   PubMed Web of Science ®Google Scholar
• Mullard, A. FDA Approves 100th Monoclonal Antibody Product. Nat. Rev. Drug Discov. 2021, 20, 491–495. DOI: 10.1038/d41573-021-00079-7.
   PubMed Web of Science ®Google Scholar
• Mullard, A. 2021 FDA Approvals. Nat. Rev. Drug Discov. 2022, 21, 83–88. DOI: 10.1038/d41573-022-00001-9.
   PubMed Web of Science ®Google Scholar
• Shu, S. A.; Wang, J.; Tao, M. H.; Leung, P. S. Gene Therapy for Autoimmune Disease. Clin. Rev. Allergy Immunol. 2015, 49, 163–176. DOI: 10.1007/s12016-014-8451-x.
   PubMed Web of Science ®Google Scholar
• Islam, M. A.; Kundu, S.; Hassan, R. Gene Therapy Approaches in an Autoimmune Demyelinating Disease: Multiple Sclerosis. Curr. Gene Ther. 2020, 19, 376–385. DOI: 10.2174/1566523220666200306092556.
   PubMed Web of Science ®Google Scholar
• Yasunaga, M. Antibody Therapeutics and Immunoregulation in Cancer and Autoimmune Disease. Semin. Cancer Biol. 2020, 64, 1–12. DOI: 10.1016/j.semcancer.2019.06.001.
   PubMed Web of Science ®Google Scholar
• Shim, H. Bispecific Antibodies and Antibody-Drug Conjugates for Cancer Therapy: Technological Considerations. Biomolecules. 2020, 10, biom10030360. DOI: 10.3390/biom10030360.
   Web of Science ®Google Scholar
• Kaplon, H.; Chenoweth, A.; Crescioli, S.; Reichert, J. M. Antibodies to Watch in 2022. MAbs. 2022, 14, 2014296. DOI: 10.1080/19420862.2021.2014296.
   PubMed Web of Science ®Google Scholar
• Lee, K. P.; Koshelev, M. V.; Team, D. C.; Pacha, O, D3CODE Team The Effect of Biologic Therapy for Immune-Mediated Inflammatory Diseases on Clinical Outcomes of COVID-19 in the Greater Houston Area: A Retrospective Chart Review. J. Am. Acad. Dermatol. 2022, 87, 658–660.
   PubMed Web of Science ®Google Scholar
• Das, T. K.; Narhi, L. O.; Sreedhara, A.; Menzen, T.; Grapentin, C.; Chou, D. K.; Antochshuk, V.; Filipe, V. Stress Factors in mAb Drug Substance Production Processes: Critical Assessment of Impact on Product Quality and Control Strategy. J. Pharm. Sci. 2020, 109, 116–133. DOI: 10.1016/j.xphs.2019.09.023.
   PubMed Web of Science ®Google Scholar
• Wen, Y.; Jawa, V. The Impact of Product and Process Related Critical Quality Attributes on Immunogenicity and Adverse Immunological Effects of Biotherapeutics. J. Pharm. Sci. 2021, 110, 1025–1041. DOI: 10.1016/j.xphs.2020.12.003.
   PubMed Web of Science ®Google Scholar
• Xu, Y.; Wang, D.; Mason, B.; Rossomando, T.; Li, N.; Liu, D.; Cheung, J. K.; Xu, W.; Raghava, S.; Katiyar, A.; et al. Structure, Heterogeneity and Developability Assessment of Therapeutic Antibodies. MAbs. 2019, 11, 239–264. DOI: 10.1080/19420862.2018.1553476.
   PubMed Web of Science ®Google Scholar
• Beck, A.; Liu, H. Macro- and Micro-Heterogeneity of Natural and Recombinant IgG Antibodies. Antibodies 2019, 8, antib8010018. DOI: 10.3390/antib8010018.
   Web of Science ®Google Scholar
• Yu, L. X.; Amidon, G.; Khan, M. A.; Hoag, S. W.; Polli, J.; Raju, G. K.; Woodcock, J. Understanding Pharmaceutical Quality by Design. Aaps J. 2014, 16, 771–783. DOI: 10.1208/s12248-014-9598-3.
   PubMed Web of Science ®Google Scholar
• Lasdun, A. M.; Kurumbail, R. R.; Leimgruber, N. K.; Rathore, A. S. Validatibility of a Capillary Isoelectric Focusing Method for Impurity Quantitation. J. Chromatogr. A. 2001, 917, 147–158. DOI: 10.1016/s0021-9673(01)00662-8.
   PubMed Web of Science ®Google Scholar
• Suba, D.; Urbanyi, Z.; Salgo, A. Capillary Isoelectric Focusing Method Development and Validation for Investigation of Recombinant Therapeutic Monoclonal Antibody. J. Pharm. Biomed. Anal. 2015, 114, 53–61. DOI: 10.1016/j.jpba.2015.04.037.
   PubMed Web of Science ®Google Scholar
• Loughney, J. W.; Minsker, K.; Ha, S.; Rustandi, R. R. Development of an Imaged Capillary Isoelectric Focusing Method for Characterizing the Surface Charge of mRNA Lipid Nanoparticle Vaccines. Electrophoresis. 2019, 40, 2602–2609. DOI: 10.1002/elps.201900063.
   PubMed Web of Science ®Google Scholar
• Racaityte, K.; Kiessig, S.; Kalman, F. Application of Capillary Zone Electrophoresis and Reversed-Phase High-Performance Liquid Chromatography in the Biopharmaceutical Industry for the Quantitative Analysis of the Monosaccharides Released from a Highly Glycosylated Therapeutic Protein. J. Chromatogr. A. 2005, 1079, 354–365. DOI: 10.1016/j.chroma.2005.03.080.
   PubMed Web of Science ®Google Scholar
• Esterman, A. L.; Katiyar, A.; Krishnamurthy, G. Implementation of USP Antibody Standard for System Suitability in Capillary Electrophoresis Sodium Dodecyl Sulfate (CE-SDS) for Release and Stability Methods. J. Pharm. Biomed. Anal. 2016, 128, 447–454. DOI: 10.1016/j.jpba.2016.06.006.
   PubMed Web of Science ®Google Scholar
• Hong, P.; Koza, S.; Bouvier, E. S. Size-Exclusion Chromatography for the Analysis of Protein Biotherapeutics and Their Aggregates. J. Liq. Chromatogr. Relat. Technol. 2012, 35, 2923–2950. DOI: 10.1080/10826076.2012.743724.
   PubMed Web of Science ®Google Scholar
• Goyon, A.; Sciascera, L.; Clarke, A.; Guillarme, D.; Pell, R. Extending the Limits of Size Exclusion Chromatography: Simultaneous Separation of Free Payloads and Related Species from Antibody Drug Conjugates and Their Aggregates. J. Chromatogr. A. 2018, 1539, 19–29. DOI: 10.1016/j.chroma.2018.01.039.
   PubMed Web of Science ®Google Scholar
• Fekete, S.; Beck, A.; Veuthey, J. L.; Guillarme, D. Ion-Exchange Chromatography for the Characterization of Biopharmaceuticals. J. Pharm. Biomed. Anal. 2015, 113, 43–55. DOI: 10.1016/j.jpba.2015.02.037.
   PubMed Web of Science ®Google Scholar
• Trappe, A.; Fussl, F.; Carillo, S.; Zaborowska, I.; Meleady, P.; Bones, J. Rapid Charge Variant Analysis of Monoclonal Antibodies to Support Lead Candidate Biopharmaceutical Development. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2018, 1095, 166–176. DOI: 10.1016/j.jchromb.2018.07.037.
   PubMed Web of Science ®Google Scholar
• Melmer, M.; Stangler, T.; Schiefermeier, M.; Brunner, W.; Toll, H.; Rupprechter, A.; Lindner, W.; Premstaller, A. HILIC Analysis of Fluorescence-Labeled N-Glycans from Recombinant Biopharmaceuticals. Anal. Bioanal. Chem. 2010, 398, 905–914. DOI: 10.1007/s00216-010-3988-x.
   PubMed Web of Science ®Google Scholar
• Zhu-Shimoni, J.; Yu, C.; Nishihara, J.; Wong, R. M.; Gunawan, F.; Lin, M.; Krawitz, D.; Liu, P.; Sandoval, W.; Vanderlaan, M. Host Cell Protein Testing by ELISAs and the Use of Orthogonal Methods. Biotechnol. Bioeng. 2014, 111, 2367–2379. DOI: 10.1002/bit.25327.
   PubMed Web of Science ®Google Scholar
• Apostol, I.; Bondarenko, P. V.; Ren, D.; Semin, D. J.; Wu, C.-H.; Zhang, Z.; Goudar, C. T. Enabling Development, Manufacturing, and Regulatory Approval of Biotherapeutics through Advances in Mass Spectrometry. Curr. Opin. Biotechnol. 2021, 71, 206–215. DOI: 10.1016/j.copbio.2021.08.001.
   PubMed Web of Science ®Google Scholar
• Rogstad, S.; Faustino, A.; Ruth, A.; Keire, D.; Boyne, M.; Park, J. A Retrospective Evaluation of the Use of Mass Spectrometry in FDA Biologics License Applications. J. Am. Soc. Mass Spectrom. 2017, 28, 786–794. DOI: 10.1007/s13361-016-1531-9.
   PubMed Web of Science ®Google Scholar
• Rogers, R. S.; Nightlinger, N. S.; Livingston, B.; Campbell, P.; Bailey, R.; Balland, A. Development of a Quantitative Mass Spectrometry Multi-Attribute Method for Characterization, Quality Control Testing and Disposition of Biologics. MAbs. 2015, 7, 881–890. DOI: 10.1080/19420862.2015.1069454.
   PubMed Web of Science ®Google Scholar
• Rogers, R. S.; Abernathy, M.; Richardson, D. D.; Rouse, J. C.; Sperry, J. B.; Swann, P.; Wypych, J.; Yu, C.; Zang, L.; Deshpande, R. A View on the Importance of Multi-Attribute Method for Measuring Purity of Biopharmaceuticals and Improving Overall Control Strategy. Aaps J. 2017, 20, 7. DOI: 10.1208/s12248-017-0168-3.
   PubMed Web of Science ®Google Scholar
• Xu, X.; Qiu, H.; Li, N. LC-MS Multi-Attribute Method for Characterization of Biologics. J. Appl. Bioanal. 2017, 3, 21–25. DOI: 10.17145/jab.17.003.
   Google Scholar
• Dong, J.; Migliore, N.; Mehrman, S. J.; Cunningham, J.; Lewis, M. J.; Hu, P. High-Throughput, Automated Protein a Purification Platform with Multiattribute LC-MS Analysis for Advanced Cell Culture Process Monitoring. Anal. Chem. 2016, 88, 8673–8679. DOI: 10.1021/acs.analchem.6b01956.
   PubMed Web of Science ®Google Scholar
• Liu, Y.; Fernandez, J.; Pu, Z.; Zhang, H.; Cao, L.; Aguilar, I.; Ritz, D.; Luo, R.; Read, A.; Laures, A.; et al. Simultaneous Monitoring and Comparison of Multiple Product Quality Attributes for Cell Culture Processes at Different Scales Using a LC/MS/MS Based Multi-Attribute Method. J. Pharm. Sci. 2020, 109, 3319–3329. DOI: 10.1016/j.xphs.2020.07.029.
   PubMed Web of Science ®Google Scholar
• Jakes, C.; Millán-Martín, S.; Carillo, S.; Scheffler, K.; Zaborowska, I.; Bones, J. Tracking the Behavior of Monoclonal Antibody Product Quality Attributes Using a Multi-Attribute Method Workflow. J. Am. Soc. Mass Spectrom. 2021, 32, 1998–2012. DOI: 10.1021/jasms.0c00432.
   PubMed Web of Science ®Google Scholar
• Sokolowska, I.; Mo, J.; Rahimi Pirkolachahi, F.; McVean, C.; Meijer, L. A. T.; Switzar, L.; Balog, C.; Lewis, M. J.; Hu, P. Implementation of a High-Resolution Liquid Chromatography-Mass Spectrometry Method in Quality Control Laboratories for Release and Stability Testing of a Commercial Antibody Product. Anal. Chem. 2020, 92, 2369–2373. DOI: 10.1021/acs.analchem.9b05036.
   PubMed Web of Science ®Google Scholar
• Evans, A. R.; Hebert, A. S.; Mulholland, J.; Lewis, M. J.; Hu, P. ID-MAM: A Validated Identity and Multi-Attribute Monitoring Method for Commercial Release and Stability Testing of a Bispecific Antibody. Anal. Chem. 2021, 93, 9166–9173. DOI: 10.1021/acs.analchem.1c01029.
   PubMed Web of Science ®Google Scholar
• Hao, Z.; Moore, B.; Ren, C.; Sadek, M.; Macchi, F.; Yang, L.; Harris, J.; Yee, L.; Liu, E.; Tran, V.; et al. Multi-Attribute Method Performance Profile for Quality Control of Monoclonal Antibody Therapeutics. J. Pharm. Biomed. Anal. 2021, 205, 114330. DOI: 10.1016/j.jpba.2021.114330.
   PubMed Web of Science ®Google Scholar
• Numao, E.; Yanagisawa, K.; Hosono, M.; Yagi, Y.; Nishimura, K.; Yamazaki, K. Development of a Comprehensive Approach for Performance Evaluation of a Quantitative Multi‑Attribute Method as a Quality Control Method. Anal. Sci. 2022, 38, 739–747. DOI: 10.1007/s44211-022-00090-x.
   PubMed Web of Science ®Google Scholar
• Song, Y. E.; Dubois, H.; Hoffmann, M.; D Eri, S.; Fromentin, Y.; Wiesner, J.; Pfenninger, A.; Clavier, S.; Pieper, A.; Duhau, L.; Roth, U. Automated Mass Spectrometry Multi-Attribute Method Analyses for Process Development and Characterization of mAbs. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2021, 1166, 122540. DOI: 10.1016/j.jchromb.2021.122540.
   PubMed Web of Science ®Google Scholar
• Ogata, Y.; Quizon, P. M.; Nightlinger, Pongkwan, N. S.; Sitasuwan, P.; Snodgrass, C.; Lee, L. A.; Meyer, J. D.; Rogers, R. S. eAutomated Multi-Attribute Method Sample Preparation Using High-Throughput Buffer Exchange Tips. Rapid Commun Mass Spectrom. 2021, 2021, e9222.
   Google Scholar
• Millán-Martín, S.; Jakes, C.; Carillo, S.; Buchanan, T.; Guender, M.; Kristensen, D. B.; Sloth, T. M.; Orgaard, M.; Cook, K.; Bones, J. Inter-Laboratory Study of an Optimised Peptide Mapping Workflow Using Automated Trypsin Digestion for Monitoring Monoclonal Antibody Product Quality Attributes. Anal. Bioanal. Chem. 2020, 412, 6833–6848. DOI: 10.1007/s00216-020-02809-z.
   PubMed Web of Science ®Google Scholar
• Butré, C. I.; D’Atri, V.; Diemer, H.; Colas, O.; Wagner, E.; Beck, A.; Cianferani, S.; Guillarme, D.; Delobel, A. Interlaboratory Evaluation of a User-Friendly Benchtop Mass Spectrometer for Multiple-Attribute Monitoring Studies of a Monoclonal Antibody. Molecules. 2023, 28, 2855. DOI: 10.3390/molecules28062855.
   PubMed Web of Science ®Google Scholar
• Zhang, Z.; Chan, P. K.; Richardson, J.; Shah, B. An Evaluation of Instrument Types for Mass Spectrometry-Based Multi-Attribute Analysis of Biotherapeutics. MAbs. 2020, 12, 1783062. DOI: 10.1080/19420862.2020.1783062.
   PubMed Web of Science ®Google Scholar
• Arndt, J. R.; Wormwood Moser, K. L.; Van Aken, G.; Doyle, R. M.; Talamantes, T.; DeBord, D.; Maxon, L.; Stafford, G.; Fjeldsted, J.; Miller, B.; Sherman, M. High-Resolution Ion-Mobility-Enabled Peptide Mapping for High-Throughput Critical Quality Attribute Monitoring. J. Am. Soc. Mass Spectrom. 2021, 32, 2019–2032. DOI: 10.1021/jasms.0c00434.
   PubMed Web of Science ®Google Scholar
• Yang, H.; Sato, M.; Quintyn, R.; Crone, C.; Kraegenbring, J.; Scheffler, K.; Du, M. An Integrated LC-MS System Performance Evaluation Test for Peptide Mapping and Monitoring, AN000336. Thermo Fisher Scientific, 2021. https://assets.thermofisher.com/TFS-Assets/CMD/Application-Notes/an-000336-lcms-protein-digest-peptide-mapping-monitoring-an000336-na-en.pdf.
   Google Scholar
• ThermoFisherScientific, HR Multi-Attribute Method: A comprehensive workflow for the assessment of critical quality attributes. BR72912-EN 0519M., 2019.
   Google Scholar
• Qian, C.; Niu, B.; Jimenez, R. B.; Wang, J.; Albarghouthi, M. Fully Automated Peptide Mapping Multi-Attribute Method by Liquid Chromatography-Mass Spectrometry with Robotic Liquid Handling System. J. Pharm. Biomed. Anal. 2021, 198, 113988. DOI: 10.1016/j.jpba.2021.113988.
   PubMed Web of Science ®Google Scholar
• Bern, M.; Kil, Y. J.; Becker, C. Byonic: Advanced Peptide and Protein Identification Software. Curr. Protoc. Bioinform. 2012, 40, 13.20.1–13.20.14. DOI: 10.1002/0471250953.bi1320s40.
   Google Scholar
• Mesmin, C.; Manache-Alberici, L.; Jones, J. Validation of LC-MS Multi-Attribute Method (MAM) Supporting Biopharma Process Characterization. BioPharm International.com, 2020. https://www.biopharminternational.com/view/validation-lc-ms-multi-attribute-method-mam-supporting-biopharma-process-characterization.
   Google Scholar
• Mouchahoir, T.; Schiel, J. E.; Rogers, R.; Heckert, A.; Place, B. J.; Ammerman, A.; Li, X.; Robinson, T.; Schmidt, B.; Chumsae, C. M.; et al. New Peak Detection Performance Metrics from the MAM Consortium Interlaboratory Study. J. Am. Soc. Mass Spectrom. 2021, 32, 913–928. DOI: 10.1021/jasms.0c00415.
   PubMed Web of Science ®Google Scholar
• Ranbaduge, N, Y. Y.Q Extending the Capabilities of the BioAccord LC-MS System with a Streamlined Workflow for Compliant-Ready Multi-Attribute Method (MAM), 720006963. WATERS 2020. https://www.waters.com/content/dam/waters/en/app-notes/2020/720006963/720006963-en.pdf.
   Google Scholar
• Zhang, Z.; Zhang, F.; McCarthy, S. Enabling Single-Software Multiple Attribute Methodology (MAM) for Assessment of Biopharmaceutical Product Quality Attributes. Application of BioPharmaView™ 3.0 Software for a Streamlined MAM Workflow. SCIEX 2017. https://sciex.com/content/dam/SCIEX/pdf/tech-notes/all/MAM-Overview.pdf.
   Google Scholar
• Buettner, A.; Maier, M.; Bonnington, L.; Bulau, P.; Reusch, D. Multi-Attribute Monitoring of Complex Erythropoetin Beta Glycosylation by GluC Liquid Chromatography-Mass Spectrometry Peptide Mapping. Anal. Chem. 2020, 92, 7574–7580. DOI: 10.1021/acs.analchem.0c00124.
   PubMed Web of Science ®Google Scholar
• Guan, X.; Eris, T.; Zhang, L.; Ren, D.; Ricci, M. S.; Thiel, T.; Goudar, C. T. A High-Resolution Multi-Attribute Method for Product Characterization, Process Characterization, and Quality Control of Therapeutic Proteins. Anal. Biochem. 2022, 643, 114575. DOI: 10.1016/j.ab.2022.114575.
   PubMed Web of Science ®Google Scholar
• Puranik, A.; Rasam, P.; Dandekar, P.; Jain, R. Development and Optimization of a LC-MS Based Multi-Attribute Method (MAM) Workflow for Characterization of Therapeutic Fc-Fusion Protein. Anal. Biochem. 2023, 660, 114969. DOI: 10.1016/j.ab.2022.114969.
   PubMed Web of Science ®Google Scholar
• Rogers, R.; Swenson, S.; Khuu-Duong, K.; Zhang, T. Mass Spectrometry-Based Process Analytical Technologies for Cell Therapies; MAM Consortium, 2021. https://mamconsortium.org.
   Google Scholar
• Wang, T.; Lucey, J. A. Use of Multi-Angle Laser Light Scattering and Size-Exclusion Chromatography to Characterize the Molecular Weight and Types of Aggregates Present in Commercial Whey Protein Products. J. Dairy Sci. 2003, 86, 3090–3101. DOI: 10.3168/jds.S0022-0302(03)73909-5.
   PubMed Web of Science ®Google Scholar
• ThermoFisherScientific, Orbitrap Exploris MX mass detector BR000169-EN 1021M. 2021.
   Google Scholar
• Yang, H.; Sato, M.; Quintyn, R.; Crone, C.; Kraegenbring, J.; Scheffler, K.; Du, M. The MAM 2.0 Workflow Enables Seamless Transition from Research and Development to Quality Control (AN000463); ThermoFisher Scientific, 2022. https://assets.thermofisher.com/TFS-Assets/CMD/Application-Notes/an-000463-lc-ms-mam-workflow-an000463-na-en.pdf.
   Google Scholar
• Millan-Martin, S.; Jakes, C.; Carillo, S.; Rogers, R.; Ren, D.; Bones, J. Comprehensive Multi-Attribute Method Workflow for Biotherapeutic Characterization and Current Good Manufacturing Practices Testing. Nat. Protoc. 2023, 18, 1056–1089. DOI: 10.1038/s41596-022-00785-5.
   PubMed Web of Science ®Google Scholar
• Ren, D.; Pipes, G. D.; Liu, D.; Shih, L.-Y.; Nichols, A. C.; Treuheit, M. J.; Brems, D. N.; Bondarenko, P. V. An Improved Trypsin Digestion Method Minimizes Digestion-Induced Modifications on Proteins. Anal. Biochem. 2009, 392, 12–21. DOI: 10.1016/j.ab.2009.05.018.
   PubMed Web of Science ®Google Scholar
• Wang, Y.; Li, X.; Liu, Y. H.; Richardson, D.; Li, H.; Shameem, M.; Yang, X. Simultaneous Monitoring of Oxidation, Deamidation, Isomerization, and Glycosylation of Monoclonal Antibodies by Liquid Chromatography-Mass Spectrometry Method with Ultrafast Tryptic Digestion. MAbs. 2016, 8, 1477–1486. DOI: 10.1080/19420862.2016.1226715.
   PubMed Web of Science ®Google Scholar
• Xu, W.; Jimenez, R. B.; Mowery, R.; Luo, H.; Cao, M.; Agarwal, N.; Ramos, I.; Wang, X.; Wang, J. J. A Quadrupole Dalton-Based Multi-Attribute Method for Product Characterization, Process Development, and Quality Control of Therapeutic Proteins. MAbs. 2017, 9, 1186–1196. DOI: 10.1080/19420862.2017.1364326.
   PubMed Web of Science ®Google Scholar
• Yang, Y.; Strahan, A.; Li, C.; Shen, A.; Liu, H.; Ouyang, J.; Katta, V.; Francissen, K.; Zhang, B. Detecting Low Level Sequence Variants in Recombinant Monoclonal Antibodies. MAbs. 2010, 2, 285–298. DOI: 10.4161/mabs.2.3.11718.
   PubMed Web of Science ®Google Scholar
• Li, X.; Rawal, B.; Rivera, S.; Letarte, S.; Richardson, D. D. Improvements on Sample Preparation and Peptide Separation for Reduced Peptide Mapping Based Multi-Attribute Method Analysis of Therapeutic Monoclonal Antibodies Using Lysyl Endopeptidase Digestion. J. Chromatogr. A. 2022, 1675, 463161. DOI: 10.1016/j.chroma.2022.463161.
   PubMed Web of Science ®Google Scholar
• Xu, C.; Khanal, S.; Pierson, N. A.; Quiroz, J.; Kochert, B.; Yang, X.; Wylie, D.; Strulson, C. A. Development, Validation, and Implementation of a Robust and Quality Control-Friendly Focused Peptide Mapping Method for Monitoring Oxidation of co-Formulated Monoclonal Antibodies. Anal. Bioanal. Chem. 2022, 414, 8317–8330. DOI: 10.1007/s00216-022-04366-z.
   PubMed Web of Science ®Google Scholar
• Stavenhagen, K.; Gahoual, R.; Dominguez-Vega, E.; Palmese, A.; Hipgrave-Ederveen, A. L.; Cutillo, F.; Palinsky, W.; Bierau, H.; Wuhrer, M. Site-Specific N- and O-Glycosylation Analysis of Atacicept. MAbs. 2019, 11, 1053–1063. DOI: 10.1080/19420862.2019.1630218.
   PubMed Web of Science ®Google Scholar
• Guapo, F.; Strasser, L.; Millán-Martín, S.; Anderson, I.; Bones, J. Fast and Efficient Digestion of Adeno Associated Virus (AAV) Capsid Proteins for Liquid Chromatography Mass Spectrometry (LC-MS) Based Peptide Mapping and Post Translational Modification Analysis (PTMs). J. Pharm. Biomed. Anal. 2022, 207, 114427. DOI: 10.1016/j.jpba.2021.114427.
   PubMed Web of Science ®Google Scholar
• Sitasuwan, P.; Powers, T. W.; Medwid, T.; Huang, Y.; Bare, B.; Lee, L. A. Enhancing the Multi-Attribute Method through an Automated and High-Throughput Sample Preparation. MAbs. 2021, 13, e1978131. DOI: 10.1080/19420862.2021.1978131.
   PubMed Web of Science ®Google Scholar
• Kristensen, D. B.; Orgaard, M.; Sloth, T. M.; Christoffersen, N. S.; Leth-Espensen, K. Z.; Jensen, P. F. Optimized Multi-Attribute Method Workflow Addressing Missed Cleavages and Chromatographic Tailing/Carry-Over of Hydrophobic Peptides. Anal. Chem. 2022, 94, 17195–17204. DOI: 10.1021/acs.analchem.2c03820.
   PubMed Web of Science ®Google Scholar
• Liu, Y.; Zhang, C.; Chen, J.; Fernandez, J.; Vellala, P.; Kulkarni, T. A.; Aguilar, I.; Ritz, D.; Lan, K.; Patel, P.; Liu, A. A Fully Integrated Online Platform for Real Time Monitoring of Multiple Product Quality Attributes in Biopharmaceutical Processes for Monoclonal Antibody Therapeutics. J. Pharm. Sci. 2022, 111, 358–367. DOI: 10.1016/j.xphs.2021.09.011.
   PubMed Web of Science ®Google Scholar
• Ren, D. Advancing Mass Spectrometry Technology in cGMP Environments. Trends Biotechnol. 2020, 38, 1051–1053. DOI: 10.1016/j.tibtech.2020.06.007.
   PubMed Web of Science ®Google Scholar
• ThermoFisherScientific, Thermo Scientific SIEVE Software for Differential Expression Analysis BR63141_E12/09S. 2009.
   Google Scholar
• Millán-Martín, S.; Carillo, S.; Jakes, C.; Yang, H.; Sato, M.; Quintyn, R.; Crone, C.; Kraegenbring, J.; Scheffler, K.; Du, M.; Bones, B. Development of a Robust Multi-Attribute Method Suitable for Implementation in a QC environment (AN000753); ThermoFisher Scientific, 2022. https://assets.thermofisher.com/TFS-Assets/CMD/Application-Notes/an-000753-lc-hram-ms-multi-attribute-method-quality-control-an000753-na-en.pdf.
   Google Scholar
• Liu, H.; Quintyn, R.; Rontree, J. A High-Resolution Accurate Mass Multi-Attribute Method for Critical Quality Attribute Monitoring and New Peak Detection (AN72916). ThermoFisher Scientific, 2019. https://assets.thermofisher.com/TFS-Assets/CMD/Application-Notes/an-72916-lc-ms-multi-attribute-method-cqa-mab-an72916-en.pdf.
   Google Scholar
• Rogers, R. Implementation of a Quantitative Mass Spectrometry Multi-Attribute Method (MAM) for Characterization, Quality Control Testing and Disposition of Biotherapeutics (Just Biotherapeutics); MAM Consortium, 2016. https://mamconsortium.org.
   Google Scholar
• Carvalho, S. B.; Gomes, R. A.; Pfenninger, A.; Fischer, M.; Strotbek, M.; Isidro, I. A.; Tugc, U. N.; Gomes-Alves, P. Multi Attribute Method Implementation Using a High Resolution Mass Spectrometry Platform: From Sample Preparation to Batch Analysis. PLoS One. 2022, 17, e0262711. DOI: 10.1371/journal.pone.0262711.
   PubMed Web of Science ®Google Scholar
• Niu, B.; Lu, Y.; Chen, X.; Xu, W. Using New Peak Detection to Solve Sequence Variants Analysis Challenges in Bioprocess Development. J. Am. Soc. Mass Spectrom. 2023, 34, 401–408. DOI: 10.1021/jasms.2c00292.
   PubMedGoogle Scholar
• Sadek, M.; Moore, B. N.; Yu, C.; Ruppe, N.; Abdun-Nabi, A.; Hao, Z.; Alvarez, M.; Dahotre, S.; Deperalta, G. A Robust Purity Method for Biotherapeutics Using New Peak Detection in an LC-MS-Based Multi-Attribute Method. J. Am. Soc. Mass Spectrom. 2023, 34, 484–492. DOI: 10.1021/jasms.2c00355.
   PubMedGoogle Scholar
• Yan, Y.; Xing, T.; Wang, S.; Li, N. Versatile, Sensitive, and Robust Native LC-MS Platform for Intact Mass Analysis of Protein Drugs. J. Am. Soc. Mass Spectrom. 2020, 31, 2171–2179. DOI: 10.1021/jasms.0c00277.
   PubMed Web of Science ®Google Scholar
• Vimer, S.; Ben-Nissan, G.; Sharon, M. Mass Spectrometry Analysis of Intact Proteins from Crude Samples. Anal. Chem. 2020, 92, 12741–12749. DOI: 10.1021/acs.analchem.0c02162.
   PubMedGoogle Scholar
• Jones, J.; Pack, L.; Hunter, J. H.; Valliere-Douglass, J. F. Native Size-Exclusion Chromatography-Mass Spectrometry: Suitability for Antibody-Drug Conjugate Drug-to-Antibody Ratio Quantitation across a Range of Chemotypes and Drug-Loading Levels. MAbs. 2020, 12, 1682895. DOI: 10.1080/19420862.2019.1682895.
   PubMed Web of Science ®Google Scholar
• Fussl, F.; Strasser, L.; Carillo, S.; Bones, J. Native LC-MS for Capturing Quality Attributes of Biopharmaceuticals on the Intact Protein Level. Curr. Opin. Biotechnol. 2021, 71, 32–40. DOI: 10.1016/j.copbio.2021.05.008.
   PubMed Web of Science ®Google Scholar
• Carillo, S.; Criscuolo, A.; Fussl, F.; Cook, K.; Bones, J. Intact Multi-Attribute Method (iMAM): A Flexible Tool for the Analysis of Monoclonal Antibodies. Eur. J. Pharm. Biopharm. 2022, 177, 241–248. DOI: 10.1016/j.ejpb.2022.07.005.
   PubMed Web of Science ®Google Scholar
• Liu, P.; Zhu, X.; Wu, W.; Ludwig, R.; Song, H.; Li, R.; Zhou, J.; Tao, L.; Leone, A. M. Subunit Mass Analysis for Monitoring Multiple Attributes of Monoclonal Antibodies. Rapid Commun. Mass Spectrom. 2019, 33, 31–40. DOI: 10.1002/rcm.8301.
   PubMed Web of Science ®Google Scholar
• Lanter, C.; Lev, M.; Cao, L.; Loladze, V. Rapid Intact Mass Based Multi-Attribute Method in Support of mAb Upstream Process Development. J. Biotechnol. 2020, 321, 96. DOI: 10.1016/j.jbiotec.2020.04.001.
   PubMed Web of Science ®Google Scholar
• Carillo, S.; Jakes, C.; Fussl, F.; Sutton, J.; Kraegenbring, J.; Crone, C.; Scheffler, K.; Bones, J. At-Line Monoclonal Antibody Analysis using Affinity-Chromatography with Mass Spectrometry Detection and Fully Compliant Data Acquisition and Processing. 69th ASMS 2021., 2021.
   Google Scholar
• Jakes, C.; Füssl, F.; Zaborowska, I.; Bones, J. Rapid Analysis of Biotherapeutics Using Protein a Chromatography Coupled to Orbitrap Mass Spectrometry. Anal. Chem. 2021, 93, 13505–13512. DOI: 10.1021/acs.analchem.1c02365.
   PubMedGoogle Scholar
• Martelet, A.; Garrigue, V.; Zhang, Z.; Genet, B.; Guttman, A. Multi-Attribute Method Based Characterization of Antibody Drugconjugates (ADC) at the Intact and Subunit Levels. J. Pharm. Biomed. Anal. 2021, 201, 1.
   Web of Science ®Google Scholar
• Chen, T. H.; Yang, Y.; Zhang, Z. R.; Fu, C. X.; Zhang, Q. Y.; Williams, J. D.; Wirth, M. J. Native Reversed-Phase Liquid Chromatography: A Technique for LCMS of Intact Antibody-Drug Conjugates. Anal. Chem. 2019, 91, 2805–2812. DOI: 10.1021/acs.analchem.8b04699.
   PubMed Web of Science ®Google Scholar
• Deslignière, E.; Ehkirch, A.; Botzanowski, T.; Beck, A.; Hernandez-Alba, O.; Cianférani, S. Toward Automation of Collision-Induced Unfolding Experiments through Online Size Exclusion Chromatography Coupled to Native Mass Spectrometry. Anal. Chem. 2020, 92, 12900–12908. DOI: 10.1021/acs.analchem.0c01426.
   PubMedGoogle Scholar
• Fussl, F.; Cook, K.; Scheffler, K.; Farrell, A.; Mittermayr, S.; Bones, J. Charge Variant Analysis of Monoclonal Antibodies Using Direct Coupled pH Gradient Cation Exchange Chromatography to High-Resolution Native Mass Spectrometry. Anal. Chem. 2018, 90, 4669–4676. DOI: 10.1021/acs.analchem.7b05241.
   PubMed Web of Science ®Google Scholar
• Yan, Y.; Xing, T.; Wang, S.; Daly, T. J.; Li, N. Online Coupling of Analytical Hydrophobic Interaction Chromatography with Native Mass Spectrometry for the Characterization of Monoclonal Antibodies and Related Products. J. Pharm. Biomed. Anal. 2020, 186, 113313. DOI: 10.1016/j.jpba.2020.113313.
   PubMed Web of Science ®Google Scholar
• Gargano, A. F. G.; Roca, L. S.; Fellers, R. T.; Bocxe, M.; Dominguez-Vega, E.; Somsen, G. W. Capillary HILIC-MS: A New Tool for Sensitive Top-Down Proteomics. Anal. Chem. 2018, 90, 6601–6609. DOI: 10.1021/acs.analchem.8b00382.
   PubMed Web of Science ®Google Scholar
• Carillo, S.; Jakes, C.; Bones, J. In-Depth Analysis of Monoclonal Antibodies Using Microfluidiccapillary Electrophoresis and Native Mass Spectrometry. J. Pharm. Biomed. 2020, 185, 1.
   Web of Science ®Google Scholar
• McDowall, R. D. Practical Computer Validation for Pharmaceutical Laboratories. J. Pharm. Biomed. Anal. 1995, 14, 13–22. DOI: 10.1016/0731-7085(95)01629-5.
   PubMed Web of Science ®Google Scholar
• Hussain, K. A Practical Approach to Computerized System Validation. In Handbook of Research on Distributed Medical Informatics and E-Health; Athina A. Lazakidou and Konstantinos M. Siassiakos, Eds.; IGI Global, 2009; pp. 456–469. DOI: 10.4018/978-1-60566-002-8.ch032.
   Google Scholar
• Forsberg, K.; Mooz, H. The Relationship of System Engineering to the Project Cycle. In INCOSE International Symposium; Wiley Online Library: Hoboken, NJ, USA, 1991; Volume 1, pp. 57–65. DOI: 10.1002/j.2334-5837.1991.tb01484.x.
   Google Scholar
• eCFR:211.165, 21 CFR 211.165 -Testing and release for distribution. Available at https://www.ecfr.gov/current/title-21/chapter-I/subchapter-C/part-211/subpart-I/section-211.165.,. 2023.
   Google Scholar
• eCFR:211.194, 21 CFR 211.194 - Laboratory records. https://www.ecfr.gov/current/title-21/chapter-I/subchapter-C/part-211/subpart-J/section-211.194.,. 2023.
   Google Scholar
• Rogstad, S.; Yan, H.; Wang, X.; Powers, D.; Brorson, K.; Damdinsuren, B.; Lee, S. Multi-Attribute Method for Quality Control of Therapeutic Proteins. Anal. Chem. 2019, 91, 14170–14177. DOI: 10.1021/acs.analchem.9b03808.
   PubMed Web of Science ®Google Scholar
• FDA, Quality Considerations for the Multi-Attribute Method (MAM) for Therapeutic Proteins. https://www.fda.gov/science-research/fda-grand-rounds/quality-considerations-multi-attribute-method-mam-therapeutic-proteins-10132022. 2022.
   Google Scholar
• EFPIA Use of Multi Attribute Method by Mass Spectrometry as a QC Release and Stability Tool for Biopharmaceuticals – Regulatory Considerations. European Federation of Pharmaceutical Industries and Associations (EFPIA) 2022. https://www.efpia.eu/media/676706/efpia-regulatory-position-paper_mam-as-qc-tool_final.pdf.
   Google Scholar
• USP, https://www.usp.org/news/us-pharmacopeia-awarded-fda-funding-to-create-a-multi-attribute-method-knowledge-base. 2022.
   Google Scholar