Immunogenicity of therapeutic proteins: The use of animal models

Pharmaceutical Research

Volumn 28, Issue 10, 2011, Pages 2379-2385

  Brinks, Vera ^a   Jiskoot, Wim ^b   Schellekens, Huub ^a,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

animal models; immunogenicity; therapeutic proteins

Indexed keywords

ALTEPLASE; BETA1A INTERFERON; INSULIN LISPRO; NEUTRALIZING ANTIBODY; PIG INSULIN; RECOMBINANT GROWTH HORMONE; RECOMBINANT PROTEIN; THERAPEUTIC PROTEIN; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ANTIBODY RESPONSE; CELLULAR IMMUNITY; CROSS REACTION; DRUG EFFICACY; DRUG RESEARCH; DRUG SAFETY; DRUG SCREENING; EXPERIMENTAL ANIMAL; EXPERIMENTAL MODEL; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; NONHUMAN; PREDICTION; PREDICTIVE VALUE; PRIMATE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REVIEW; RHESUS MONKEY; TRANSGENIC MOUSE;

ANIMALS; BIOLOGICAL AGENTS; DRUG EVALUATION, PRECLINICAL; HUMANS; MODELS, ANIMAL; PREDICTIVE VALUE OF TESTS; PROTEINS;

EID: 80054738932     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-011-0523-5     Document Type: Review

References (40)

1. Clarke JB. Mechanisms of adverse drug reactions to biologics. Handbook Exp Pharmacol. 2010: 453-74
2. H Schellekens 2010 The immunogenicity of therapeutic proteins Discov Med 9 560 564 20587346
3. MK de Vries E Brouwer IE van der Horst-Bruinsma A Spoorenberg JC van Denderen A Jamnitski MT Nurmohamed BA Dijkmans LA Aarden GJ Wolbink 2009 Decreased clinical response to adalimumab in ankylosing spondylitis is associated with antibody formation Ann Rheum Dis 68 1787 1788 19822712 10.1136/ard.2009.109702
4. H Schellekens 2002 Immunogenicity of therapeutic proteins: clinical implications and future prospects Clin Ther 24 1720 1740 12501870 10.1016/S0149-2918(02)80075-3 1:CAS:528:DC%2BD38Xpslekurw%3D (Pubitemid 35440946)
5. H Schellekens 2005 Immunologic mechanisms of EPO-associated pure red cell aplasia Best Pract Res Clin Haematol 18 473 480 15792922 10.1016/j.beha.2005. 01.016 1:CAS:528:DC%2BD2MXisFGrsLs%3D (Pubitemid 40425360)
6. GJ Wolbink LA Aarden BA Dijkmans 2009 Dealing with immunogenicity of biologicals: assessment and clinical relevance Curr Opin Rheumatol 21 211 215 19399992 10.1097/BOR.0b013e328329ed8b
7. NK Bender CE Heilig B Droll J Wohlgemuth FP Armbruster B Heilig 2007 Immunogenicity, efficacy and adverse events of adalimumab in RA patients Rheumatol Int 27 269 274 17006705 10.1007/s00296-006-0183-7 1:CAS:528: DC%2BD2sXivFOntg%3D%3D (Pubitemid 46088257)
8. A Vultaggio A Matucci F Nencini S Pratesi P Parronchi O Rossi S Romagnani E Maggi 2010 Anti-infliximab IgE and non-IgE antibodies and induction of infusion-related severe anaphylactic reactions Allergy 65 657 661 19951375 10.1111/j.1398-9995.2009.02280.x 1:CAS:528:DC%2BC3cXmtVKjtLo%3D
9. EMA. Guideline on immunogenicity assessment of biotechnology-derived therapeutic proteins. 2007. Ref Type: Conference Proceeding
10. M Sauerborn V Brinks W Jiskoot H Schellekens 2010 Immunological mechanism underlying the immune response to recombinant human protein therapeutics Trends Pharmacol Sci 31 53 59 19963283 10.1016/j.tips.2009.11.001 1:CAS:528: DC%2BC3cXhtlejsbo%3D
11. AJ Jones 2002 The use of an animal immunogenicity model in the development of protropin somatrem (methionyl human growth hormone) Dev Biol (Basel) 109 107 118 1:CAS:528:DC%2BD38XovF2gs74%3D
12. JL Ottesen P Nilsson J Jami D Weilguny M Duhrkop D Bucchini S Havelund JM Fogh 1994 The potential immunogenicity of human insulin and insulin analogues evaluated in a transgenic mouse model Diabetologia 37 1178 1185 7895946 10.1007/BF00399790 1:CAS:528:DyaK2MXjvVKnt7o%3D (Pubitemid 24356756)
13. MM van Beers M Sauerborn F Gilli S Hermeling V Brinks H Schellekens W Jiskoot 2010 Hybrid transgenic immune tolerant mouse model for assessing the breaking of B cell tolerance by human interferon beta J Immunol Methods 352 32 37 19857496 10.1016/j.jim.2009.10.005
14. CM Zwickl HW Smith JL Zimmermann D Wierda 1995 Immunogenicity of biosynthetic human LysPro insulin compared to native-sequence human and purified porcine insulins in rhesus monkeys immunized over a 6-week period Arzneimittelforschung 45 524 528 7779155 1:CAS:528:DyaK2MXls1OjtLs%3D
15. CM Zwickl BL Hughes KS Piroozi HW Smith D Wierda 1996 Immunogenicity of tissue plasminogen activators in rhesus monkeys: antibody formation and effects on blood level and enzymatic activity Fundam Appl Toxicol 30 243 254 8812272 10.1006/faat.1996.0062 1:CAS:528:DyaK28XitlSmt7g%3D (Pubitemid 26115484)
16. Center for Biologics Evaluation and Research. Meeting of the biological response modifiers advisory committee. July 15, Bethesda MD. Food and Drug Administration. 1999. Ref Type: Conference Proceeding
17. CM Zwickl KS Cocke RN Tamura LM Holzhausen GT Brophy PH Bick D Wierda 1991 Comparison of the immunogenicity of recombinant and pituitary human growth hormone in rhesus monkeys Fundam Appl Toxicol 16 275 287 2055359 10.1016/0272-0590(91)90112-H 1:CAS:528:DyaK3MXhtFGhsrg%3D
18. S Hermeling L Aranha JM Damen M Slijper H Schellekens DJ Crommelin W Jiskoot 2005 Structural characterization and immunogenicity in wild-type and immune tolerant mice of degraded recombinant human interferon alpha2b Pharm Res 22 1997 2006 16184451 10.1007/s11095-005-8177-9 1:CAS:528:DC%2BD2MXhtlemtbnP (Pubitemid 41821578)
19. E Koren LA Zuckerman AR Mire-Sluis 2002 Immune responses to therapeutic proteins in humans-clinical significance, assessment and prediction Curr Pharm Biotechnol 3 349 360 12463417 10.2174/1389201023378175 1:CAS:528: DC%2BD38XovF2qsb8%3D (Pubitemid 35364009)
20. A Jaber R Driebergen G Giovannoni H Schellekens J Simsarian M Antonelli 2007 The Rebif new formulation story: it's not trials and error Drugs R D 8 335 348 17963425 10.2165/00126839-200708060-00002 1:CAS:528:DC%2BD2sXhsVCntbjJ (Pubitemid 350014786)
21. F Bellomi A Muto G Palmieri C Focaccetti C Dianzani M Mattei A Jaber G Antonelli 2007 Immunogenicity comparison of interferon beta-1a preparations using the BALB/c mouse model: assessment of a new formulation for use in multiple sclerosis New Microbiol 30 241 246 17802901 1:CAS:528: DC%2BD2sXhtVWnsrzL (Pubitemid 47264881)
22. van Beers MM, Sauerborn M, Gilli F, Brinks V, Schellekens H, Jiskoot W. Aggregated recombinant human interferon beta induces antibodies but no memory in immune-tolerant transgenic mice. Pharm Res. 2010
23. N Katsutani S Yoshitake H Takeuchi JC Kelliher RC Couch H Shionoya 1992 Immunogenic properties of structurally modified human tissue plasminogen activators in chimpanzees and mice Fundam Appl Toxicol 19 555 562 1426714 10.1016/0272-0590(92)90094-X 1:CAS:528:DyaK3sXlt1WjtQ%3D%3D (Pubitemid 23013126)
24. TA Stewart PG Hollingshead SL Pitts R Chang LE Martin H Oakley 1989 Transgenic mice as a model to test the immunogenicity of proteins altered by site-specific mutagenesis Mol Biol Med 6 275 281 2482920 1:CAS:528: DyaK3cXhtlemu70%3D (Pubitemid 20108304)
25. PJ Whiteley JP Lake RF Selden JA Kapp 1989 Tolerance induced by physiological levels of secreted proteins in transgenic mice expressing human insulin J Clin Invest 84 1550 1554 2681269 10.1172/JCI114331 1:CAS:528:DyaK3cXhtVCq (Pubitemid 19272243)
26. S Hermeling W Jiskoot D Crommelin C Bornaes H Schellekens 2005 Development of a transgenic mouse model immune tolerant for human interferon beta Pharm Res 22 847 851 15948027 10.1007/s11095-005-4578-z 1:CAS:528:DC%2BD2MXltVKnu74%3D (Pubitemid 40898093)
27. A Bertolotto F Deisenhammer P Gallo SP Solberg 2004 Immunogenicity of interferon beta: differences among products J Neurol 251 Suppl 2 II15 II24 15264108
28. HJ Lee G Riley O Johnson JL Cleland N Kim M Charnis L Bailey E Duenas A Shahzamani M Marian AJ Jones SD Putney 1997 In vivo characterization of sustained-release formulations of human growth hormone J Pharmacol Exp Ther 281 1431 1439 9190880 1:CAS:528:DyaK2sXktVOls78%3D (Pubitemid 27258404)
29. AH Fradkin JF Carpenter TW Randolph 2009 Immunogenicity of aggregates of recombinant human growth hormone in mouse models J Pharm Sci 98 3247 3264 19569057 10.1002/jps.21834 1:CAS:528:DC%2BD1MXptl2itL0%3D
30. NS Fineberg SE Fineberg JH Anderson MA Birkett RG Gibson S Hufferd 1996 Immunologic effects of insulin lispro [Lys (B28), Pro (B29) human insulin] in IDDM and NIDDM patients previously treated with insulin Diabetes 45 1750 1754 8922361 10.2337/diabetes.45.12.1750 1:CAS:528:DyaK28XntlGisLc%3D (Pubitemid 26398955)
31. H Gunn 1997 Immunogenicity of recombinant human interleukin-3 Clin Immunol Immunopathol 83 5 7 9073525 10.1006/clin.1996.4302 1:CAS:528: DyaK2sXitlejtr4%3D (Pubitemid 27128385)
32. H Schellekens 2005 Factors influencing the immunogenicity of therapeutic proteins Nephrol Dial Transplant 20 Suppl 6 vi3 vi9 15958824 10.1093/ndt/gfh1092 1:CAS:528:DC%2BD2MXovV2mu7c%3D
33. AS De Groot DW Scott 2007 Immunogenicity of protein therapeutics Trends Immunol 28 482 490 17964218 10.1016/j.it.2007.07.011 (Pubitemid 350087812)
34. H Schellekens 2008 The immunogenicity of therapeutic proteins and the Fabry antibody standardization initiative Clin Ther 30 Suppl B S50 S51 18395140 10.1016/S0149-2918(08)80041-0 (Pubitemid 351458360)
35. WF Weiss TM Young CJ Roberts 2009 Principles, approaches, and challenges for predicting protein aggregation rates and shelf life J Pharm Sci 98 1246 1277 18683878 10.1002/jps.21521 1:CAS:528:DC%2BD1MXktlSisLc%3D
36. A Braun L Kwee MA Labow J Alsenz 1997 Protein aggregates seem to play a key role among the parameters influencing the antigenicity of interferon alpha (IFN-alpha) in normal and transgenic mice Pharm Res 14 1472 1478 9358564 10.1023/A:1012193326789 1:CAS:528:DyaK2sXntFehtL0%3D (Pubitemid 27481082)
37. S Hermeling H Schellekens C Maas MF Gebbink DJ Crommelin W Jiskoot 2006 Antibody response to aggregated human interferon alpha2b in wild-type and transgenic immune tolerant mice depends on type and level of aggregation J Pharm Sci 95 1084 1096 16552750 10.1002/jps.20599 1:CAS:528:DC%2BD28Xkslejur8%3D (Pubitemid 43723167)
38. Rifkin RA, Maggio ET, Dike S, Kerr DA, Levy M. n-Dodecyl-beta-D: -maltoside inhibits aggregation of human interferon-beta-1b and reduces its immunogenicity. J Neuroimmune Pharmacol. 2010
39. P Perini A Facchinetti P Bulian AR Massaro DD Pascalis A Bertolotto G Biasi P Gallo 2001 Interferon-beta (INF-beta) antibodies in interferon-beta1a- and interferon-beta1b-treated multiple sclerosis patients. Prevalence, kinetics, cross-reactivity, and factors enhancing interferon-beta immunogenicity in vivo Eur Cytokine Netw 12 56 61 11282547 1:CAS:528:DC%2BD3MXivFGltLs%3D (Pubitemid 32281190)
40. N Gao P Jennings D Yuan 2008 Requirements for the natural killer cell-mediated induction of IgG1 and IgG2a expression in B lymphocytes Int Immunol 20 645 657 18339657 10.1093/intimm/dxn021 1:CAS:528:DC%2BD1cXmsFOgsbo%3D (Pubitemid 351619234)