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Journal of Immunology Research
Volume 2016, Article ID 6262383, 6 pages
http://dx.doi.org/10.1155/2016/6262383
Review Article

Emerging Technologies and Generic Assays for the Detection of Anti-Drug Antibodies

1Regeneron Pharmaceuticals, Inc., 777 Old Saw Mill River Road, Tarrytown, NY 10591, USA
2UCB Pharma, Slough, Berkshire SL1 14EN, UK
3Department of Biochemical & Cellular Pharmacology, Genentech Inc., South San Francisco, CA 94080, USA

Received 20 April 2016; Revised 26 May 2016; Accepted 9 June 2016

Academic Editor: Eyad Elkord

Copyright © 2016 Michael A. Partridge et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Shankar, C. Pendley, and K. E. Stein, “A risk-based bioanalytical strategy for the assessment of antibody immune responses against biological drugs,” Nature Biotechnology, vol. 25, no. 5, pp. 555–561, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. A. R. Mire-Sluis, Y. C. Barrett, V. Devanarayan et al., “Recommendations for the design and optimization of immunoassays used in the detection of host antibodies against biotechnology products,” Journal of Immunological Methods, vol. 289, no. 1-2, pp. 1–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Myler, T. Felix, J. Zhu, M. Hruska, and S. P. Piccoli, “Measuring biotherapeutics with endogenous counterparts and pre-existing antibodies: an interferon case study,” Bioanalysis, vol. 6, no. 8, pp. 1113–1122, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. K. A. Van Schie, G.-J. Wolbink, and T. Rispens, “Cross-reactive and pre-existing antibodies to therapeutic antibodies—effects on treatment and immunogenicity,” mAbs, vol. 7, no. 4, pp. 662–671, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Gorovits, J. McNally, C. Fiorotti, and S. Leung, “Protein-based matrix interferences in ligand-binding assays,” Bioanalysis, vol. 6, no. 8, pp. 1131–1140, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. S. M. Tatarewicz, G. Juan, S. J. Swanson, and M. S. Moxness, “Epitope characterization of pre-existing and developing antibodies to an aglycosylated monoclonal antibody therapeutic of G1m17,1 allotype,” Journal of Immunological Methods, vol. 382, no. 1-2, pp. 93–100, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Ben-Horin, M. Yavzori, L. Katz et al., “The immunogenic part of infliximab is the F(ab')2, but measuring antibodies to the intact infliximab molecule is more clinically useful,” Gut, vol. 60, no. 1, pp. 41–48, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Rispens, H. De Vrieze, E. De Groot et al., “Antibodies to constant domains of therapeutic monoclonal antibodies: anti-hinge antibodies in immunogenicity testing,” Journal of Immunological Methods, vol. 375, no. 1-2, pp. 93–99, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. C. H. Chung, B. Mirakhur, E. Chan et al., “Cetuximab-induced anaphylaxis and IgE specific for galactose-α-1,3- galactose,” The New England Journal of Medicine, vol. 358, no. 11, pp. 1109–1117, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Xue and B. Rup, “Evaluation of pre-existing antibody presence as a risk factor for posttreatment anti-drug antibody induction: analysis of human clinical study data for multiple biotherapeutics,” The AAPS Journal, vol. 15, no. 3, pp. 893–896, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Carrasco-Triguero, C. Mahood, M. Milojic-Blair et al., “Overcoming soluble target interference in an anti-therapeutic antibody screening assay for an antibody-drug conjugate therapeutic,” Bioanalysis, vol. 4, no. 16, pp. 2013–2026, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. Z. D. Zhong, S. Dinnogen, M. Hokom et al., “Identification and inhibition of drug target interference in immunogenicity assays,” Journal of Immunological Methods, vol. 355, no. 1-2, pp. 21–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Nishimoto, K. Terao, T. Mima, H. Nakahara, N. Takagi, and T. Kakehi, “Mechanisms and pathologic significances in increase in serum interleukin-6 (IL-6) and soluble IL-6 receptor after administration of an anti-IL-6 receptor antibody, tocilizumab, in patients with rheumatoid arthritis and Castleman disease,” Blood, vol. 112, no. 10, pp. 3959–3964, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. M. H. Hart, H. De Vrieze, D. Wouters et al., “Differential effect of drug interference in immunogenicity assays,” Journal of Immunological Methods, vol. 372, no. 1-2, pp. 196–203, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. T. E. Barger, D. Wrona, T. J. Goletz, and D. T. Mytych, “A detailed examination of the antibody prevalence and characteristics of anti-ESA antibodies,” Nephrology Dialysis Transplantation, vol. 27, no. 10, pp. 3892–3899, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. P. A. Van Schouwenburg, T. Rispens, and G. J. Wolbink, “Immunogenicity of anti-TNF biologic therapies for rheumatoid arthritis,” Nature Reviews Rheumatology, vol. 9, no. 3, pp. 164–172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. P. A. Van Schouwenburg, C. L. Krieckaert, M. Nurmohamed et al., “IgG4 production against adalimumab during long term treatment of RA patients,” Journal of Clinical Immunology, vol. 32, no. 5, pp. 1000–1006, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. P. A. Van Schouwenburg, C. L. Krieckaert, T. Rispens, L. Aarden, G. J. Wolbink, and D. Wouters, “Long-term measurement of anti-adalimumab using pH-shift-anti-idiotype antigen binding test shows predictive value and transient antibody formation,” Annals of the Rheumatic Diseases, vol. 72, no. 10, pp. 1680–1686, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Eriksson, C. Agaton, R. Kånge et al., “Microfluidic analysis of antibody specificity in a compact disk format,” Journal of Proteome Research, vol. 5, no. 7, pp. 1568–1574, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. I. Magana, C. R. Macaraeg, L. Zhang, M. Ma, and T. M. Thway, “Validation of a microfluidic platform to measure total therapeutic antibodies and incurred sample reanalysis performance,” Bioanalysis, vol. 6, no. 19, pp. 2623–2633, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. X. F. Liu, X. Wang, R. J. Weaver et al., “Validation of a gyrolab assay for quantification of rituximab in human serum,” Journal of Pharmacological and Toxicological Methods, vol. 65, no. 3, pp. 107–114, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Salimi-Moosavi, P. Rathanaswami, S. Rajendran, M. Toupikov, and J. Hill, “Rapid affinity measurement of protein-protein interactions in a microfluidic platform,” Analytical Biochemistry, vol. 426, no. 2, pp. 134–141, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. A. M. Given, P. M. Whalen, P. J. O'Brien, and C. A. Ray, “Development and validation of an alpha fetoprotein immunoassay using Gyros technology,” Journal of Pharmaceutical and Biomedical Analysis, vol. 64-65, pp. 8–15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Mikulskis, D. Yeung, M. Subramanyam, and L. Amaravadi, “Solution ELISA as a platform of choice for development of robust, drug tolerant immunogenicity assays in support of drug development,” Journal of Immunological Methods, vol. 365, no. 1-2, pp. 38–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. H. W. Smith, A. Butterfield, and D. Sun, “Detection of antibodies against therapeutic proteins in the presence of residual therapeutic protein using a solid-phase extraction with acid dissociation (SPEAD) sample treatment prior to ELISA,” Regulatory Toxicology and Pharmacology, vol. 49, no. 3, pp. 230–237, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Spengler, M. Adler, A. Jonas, and C. M. Niemeyer, “Immuno-PCR assays for immunogenicity testing,” Biochemical and Biophysical Research Communications, vol. 387, no. 2, pp. 278–282, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Jani, E. Savino, and J. Goyal, “Feasibility of immuno-PCR technology platforms as an ultrasensitive tool for the detection of anti-drug antibodies,” Bioanalysis, vol. 7, no. 3, pp. 285–294, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. J. S. Bourdage, C. A. Cook, D. L. Farrington, J. S. Chain, and R. J. Konrad, “An Affinity Capture Elution (ACE) assay for detection of anti-drug antibody to monoclonal antibody therapeutics in the presence of high levels of drug,” Journal of Immunological Methods, vol. 327, no. 1-2, pp. 10–17, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Sickert, K. Kroeger, C. Zickler et al., “Improvement of drug tolerance in immunogenicity testing by acid treatment on Biacore,” Journal of Immunological Methods, vol. 334, no. 1-2, pp. 29–36, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Mora, A. Given Chunyk, M. Dysinger et al., “Next generation ligand binding assays—review of emerging technologies’ capabilities to enhance throughput and multiplexing,” The AAPS Journal, vol. 16, no. 6, pp. 1175–1184, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. M. T. Furlong, Z. Ouyang, S. Wu et al., “A universal surrogate peptide to enable LC-MS/MS bioanalysis of a diversity of human monoclonal antibody and human Fc-fusion protein drug candidates in pre-clinical animal studies,” Biomedical Chromatography, vol. 26, no. 8, pp. 1024–1032, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Li, R. Ortiz, L. Tran et al., “General LC-MS/MS method approach to quantify therapeutic monoclonal antibodies using a common whole antibody internal standard with application to preclinical studies,” Analytical Chemistry, vol. 84, no. 3, pp. 1267–1273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Jiang, W. Xu, C. A. Titsch et al., “Innovative use of LC-MS/MS for simultaneous quantitation of neutralizing antibody, residual drug, and human immunoglobulin G in immunogenicity assay development,” Analytical Chemistry, vol. 86, no. 5, pp. 2673–2680, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Neubert, C. Grace, K. Rumpel, and I. James, “Assessing immunogenicity in the presence of excess protein therapeutic using immunoprecipitation and quantitative mass spectrometry,” Analytical Chemistry, vol. 80, no. 18, pp. 6907–6914, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. L.-Z. Chen, D. Roos, and E. Philip, “Development of immunocapture-LC/MS assay for simultaneous ADA isotyping and semiquantitation,” Journal of Immunology Research, vol. 2016, Article ID 7682472, 14 pages, 2016. View at Publisher · View at Google Scholar
  36. K. Stubenrauch, K. MacKeben, R. Vogel, and J. Heinrich, “Generic anti-drug antibody assay with drug tolerance in serum samples from mice exposed to human antibodies,” Analytical Biochemistry, vol. 430, no. 2, pp. 193–199, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Stubenrauch, U. Wessels, U. Essig, R. Vogel, and J. Schleypen, “Evaluation of a generic immunoassay with drug tolerance to detect immune complexes in serum samples from cynomolgus monkeys after administration of human antibodies,” Journal of Pharmaceutical and Biomedical Analysis, vol. 52, no. 2, pp. 249–254, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Carrasco-Triguero, H. Davis, Y. Zhu et al., “Application of a plug-and-play immunogenicity assay in cynomolgus monkey serum for ADCs at early stages of drug development,” Journal of Immunology Research, vol. 2016, Article ID 2618575, 14 pages, 2016. View at Publisher · View at Google Scholar
  39. A. C. Bautista, H. Salimi-Moosavi, and V. Jawa, “Universal immunoassay applied during early development of large molecules to understand impact of immunogenicity on biotherapeutic exposure,” The AAPS Journal, vol. 14, no. 4, pp. 843–849, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. C. Bautista, L. Zhou, and V. Jawa, “Universal immunogenicity validation and assessment during early biotherapeutic development to support a green laboratory,” Bioanalysis, vol. 5, no. 20, pp. 2495–2507, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. X. Hu, L. Miller, S. Richman et al., “A novel PEGylated interferon beta-1a for multiple sclerosis: safety, pharmacology, and biology,” Journal of Clinical Pharmacology, vol. 52, no. 6, pp. 798–808, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Myler, M. W. Hruska, S. Srinivasan et al., “Anti-PEG antibody bioanalysis: a clinical case study with PEG-IFN-λ-1a and PEG-IFN-α2a in naive patients,” Bioanalysis, vol. 7, no. 9, pp. 1093–1106, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. J. T. White, M. Crossman, K. Richter, M. Berman, J. Goyal, and M. Subramanyam, “Immunogenicity evaluation strategy for a second-generation therapeutic, PEG-IFN-β-1a,” Bioanalysis, vol. 7, no. 21, pp. 2801–2811, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Schellekens, W. E. Hennink, and V. Brinks, “The immunogenicity of polyethylene glycol: facts and fiction,” Pharmaceutical Research, vol. 30, no. 7, pp. 1729–1734, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Dong, J. R. Mora, C. Brockus et al., “Development of a generic anti-PEG antibody assay using bioscale’s acoustic membrane microparticle technology,” The AAPS Journal, vol. 17, no. 6, pp. 1511–1516, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. S. D. Chilewski, W. M. Dickerson, J. R. Mora, A. Saab, and E. M. Alderman, “Evaluation of acoustic membrane microparticle (Ammp) technology for a sensitive ligand binding assay to support pharmacokinetic determinations of a biotherapeutic,” The AAPS Journal, vol. 16, no. 6, pp. 1366–1371, 2014. View at Publisher · View at Google Scholar · View at Scopus