Analytical FcRn affinity chromatography for functional characterization of monoclonal antibodies

mAbs

Volumn 5, Issue 4, 2013, Pages 576-586

  Schlothauer, Tilman ^a   Rueger, Petra ^a   Stracke, Jan Olaf ^a   Hertenberger, Hubert ^a   Fingas, Felix ^a   Kling, Lothar ^a   Emrich, Thomas ^a   Drabner, Georg ^a   Seeber, Stefan ^a   Auer, Johannes ^a   Koch, Stefan ^a   Papadimitriou, Apollon ^a  

^a ROCHE DIAGNOSTICS GMBH   (Germany)

Author keywords

Affinity chromatography; Antibody; Column; Degradation; FcRn; Methionine oxidation; Neonatal fc receptor; pH gradient; Pharmacokinetics; PK

Indexed keywords

ADALIMUMAB; CETUXIMAB; FC RECEPTOR; IMMUNOGLOBULIN G; INFLIXIMAB; MONOCLONAL ANTIBODY; MONOMER; MUTANT PROTEIN; NEONATAL FC RECEPTOR; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ANTIBODY ENGINEERING; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; GEL PERMEATION CHROMATOGRAPHY; MALE; MOUSE; NONHUMAN; PH; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE; WILD TYPE;

AFFINITY CHROMATOGRAPHY; ANTIBODY; COLUMN; DEGRADATION; FCRN; METHIONINE OXIDATION; NEONATAL FC RECEPTOR; PH GRADIENT; PHARMACOKINETICS; PK;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; CHROMATOGRAPHY, AFFINITY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MICE, TRANSGENIC; MUTATION; RECEPTORS, FC; SURFACE PLASMON RESONANCE;

EID: 84880128931     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.24981     Document Type: Article

References (41)

1. Nelson AL, Dhimolea E, Reichert JM. Development trends for human monoclonal antibody therapeutics. Nat Rev Drug Discov 2010; 9:767-74; PMID:20811384; http://dx.doi.org/10.1038/nrd3229
2. Reichert JM. Which are the antibodies to watch in 2012? MAbs 2012; 4:1-3; PMID:22327425; http://dx.doi.org/10.4161/mabs.4.1.18719
3. Mahmood I, Green MD. Pharmacokinetic and pharmacodynamic considerations in the development of therapeutic proteins. Clin Pharmacokinet 2005; 44:331-47; PMID:15828849; http://dx.doi.org/10.2165/00003088-200544040-00001
4. Vázquez-Rey M, Lang DA. Aggregates in monoclonal antibody manufacturing processes. Biotechnol Bioeng 2011; 108:1494-508; PMID:21480193; http://dx.doi.org/10.1002/bit.23155
5. Filpula D. Antibody engineering and modification technologies. Biomol Eng 2007; 24:201-15; PMID:17466589; http://dx.doi.org/10.1016/j.bioeng.2007.03.004
6. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008; 8:34-47; PMID:18064051; http://dx.doi.org/10. 1038/nri2206
7. Kuo TT, Baker K, Yoshida M, Qiao SW, Aveson VG, Lencer WI, et al. Neonatal Fc receptor: from immunity to therapeutics. J Clin Immunol 2010; 30:777-89; PMID:20886282; http://dx.doi.org/10.1007/s10875-010-9468-4
8. Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 2007; 7:715-25; PMID:17703228; http://dx.doi.org/10.1038/nri2155
9. Martin WL, West AP Jr., Gan L, Bjorkman PJ. Crystal structure at 2.8 A of an FcRn/heterodimeric Fc complex: mechanism of pH-dependent binding. Mol Cell 2001; 7:867-77; PMID:11336709; http://dx.doi.org/10.1016/S1097-2765(01)00230-1
10. Goebl NA, Babbey CM, Datta-Mannan A, Witcher DR, Wroblewski VJ, Dunn KW. Neonatal Fc receptor mediates internalization of Fc in transfected human endothelial cells. Mol Biol Cell 2008; 19:5490-505; PMID:18843053; http://dx.doi.org/10.1091/mbc.E07-02-0101
11. Kim JK, Tsen MF, Ghetie V, Ward ES. Identifying amino acid residues that influence plasma clearance of murine IgG1 fragments by site-directed mutagenesis. Eur J Immunol 1994; 24:542-8; PMID:8125126; http://dx.doi.org/10. 1002/eji.1830240308
12. Ober RJ, Martinez C, Lai X, Zhou J, Ward ES. Exocytosis of IgG as mediated by the receptor, FcRn: an analysis at the single-molecule level. Proc Natl Acad Sci U S A 2004; 101:11076-81; PMID:15258288; http://dx.doi.org/10. 1073/pnas.0402970101
13. Ober RJ, Martinez C, Vaccaro C, Zhou J, Ward ES. Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn. J Immunol 2004; 172:2021-9; PMID:14764666
14. Sánchez LM, Penny DM, Bjorkman PJ. Stoichiometry of the interaction between the major histocompatibility complex-related Fc receptor and its Fc ligand. Biochemistry 1999; 38:9471-6; PMID:10413524; http://dx.doi.org/10.1021/bi9907330
15. Huber AH, Kelley RF, Gastinel LN, Bjorkman PJ. Crystallization and stoichiometry of binding of a complex between a rat intestinal Fc receptor and Fc. J Mol Biol 1993; 230:1077-83; PMID:8478919; http://dx.doi.org/10.1006/jmbi. 1993.1220
16. Ward ES, Martinez C, Vaccaro C, Zhou J, Tang Q, Ober RJ. From sorting endosomes to exocytosis: association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol Biol Cell 2005; 16:2028-38; PMID:15689494; http://dx.doi.org/10.1091/mbc.E04-08-0735
17. Wang W, Lu P, Fang Y, Hamuro L, Pittman T, Carr B, et al. Monoclonal antibodies with identical Fc sequences can bind to FcRn differentially with pharmacokinetic consequences. Drug Metab Dispos 2011; 39:1469-77; PMID:21610128; http://dx.doi.org/10.1124/dmd.111.039453
18. Datta-Mannan A, Chow CK, Dickinson C, Driver D, Lu J, Witcher DR, et al. FcRn affinity-pharmacokinetic relationship of five human IgG4 antibodies engineered for improved in vitro FcRn binding properties in cynomolgus monkeys. Drug Metab Dispos 2012; 40:1545-55; PMID:22584253; http://dx.doi.org/10.1124/ dmd.112.045864
19. Vaughn DE, Bjorkman PJ. High-affinity binding of the neonatal Fc receptor to its IgG ligand requires receptor immobilization. Biochemistry 1997; 36:9374-80; PMID:9235980; http://dx.doi.org/10.1021/bi970841r
20. Raghavan M, Wang Y, Bjorkman PJ. Effects of receptor dimerization on the interaction between the class I major histocompatibility complex-related Fc receptor and IgG. Proc Natl Acad Sci U S A 1995; 92:11200-4; PMID:7479965; http://dx.doi.org/10.1073/pnas.92.24.11200
21. Martin WL, Bjorkman PJ. Characterization of the 2:1 complex between the class I MHC-related Fc receptor and its Fc ligand in solution. Biochemistry 1999; 38:12639-47; PMID:10504233; http://dx.doi.org/10.1021/bi9913505
22. Pollastrini J, Dillon TM, Bondarenko P, Chou RY. Field flow fractionation for assessing neonatal Fc receptor and Fcγ receptor binding to monoclonal antibodies in solution. Anal Biochem 2011; 414:88-98; PMID:21385563; http://dx.doi.org/10.1016/j.ab.2011.03.001
23. Gurbaxani B, Dela Cruz LL, Chintalacharuvu K, Morrison SL. Analysis of a family of antibodies with different half-lives in mice fails to find a correlation between affinity for FcRn and serum half-life. Mol Immunol 2006; 43:1462-73; PMID:16139891; http://dx.doi.org/10.1016/j.molimm.2005.07.032
24. Gurbaxani BM, Morrison SL. Development of new models for the analysis of Fc-FcRn interactions. Mol Immunol 2006; 43:1379-89; PMID:16183124; http://dx.doi.org/10.1016/j.molimm.2005.08.002
25. Gurbaxani B. Mathematical modeling as accounting: predicting the fate of serum proteins and therapeutic monoclonal antibodies. Clin Immunol 2007; 122:121-4; PMID:17126081; http://dx.doi.org/10.1016/j.clim.2006.10.001
26. Yeung YA, Leabman MK, Marvin JS, Qiu J, Adams CW, Lien S, et al. Engineering human IgG1 affinity to human neonatal Fc receptor: impact of affinity improvement on pharmacokinetics in primates. J Immunol 2009; 182:7663-71; PMID:19494290; http://dx.doi.org/10.4049/jimmunol.0804182
27. Vaccaro C, Zhou J, Ober RJ, Ward ES. Engineering the Fc region of immunoglobulin G to modulate in vivo antibody levels. Nat Biotechnol 2005; 23:1283-8; PMID:16186811; http://dx.doi.org/10.1038/nbt1143
28. Dall'Acqua WF, Kiener PA, Wu H. Properties of human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn). J Biol Chem 2006; 281:23514-24; PMID:16793771; http://dx.doi.org/10.1074/jbc.M604292200
29. Petkova SB, Akilesh S, Sproule TJ, Christianson GJ, Al Khabbaz H, Brown AC, et al. Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: potential application in humorally mediated autoimmune disease. Int Immunol 2006; 18:1759-69; PMID:17077181; http://dx.doi.org/10.1093/intimm/dxl110
30. Pan H, Chen K, Chu L, Kinderman F, Apostol I, Huang G. Methionine oxidation in human IgG2 Fc decreases binding affinities to protein A and FcRn. Protein Sci 2009; 18:424-33; PMID:19165723; http://dx.doi.org/10.1002/pro.45
31. Bertolotti-Ciarlet A, Wang W, Lownes R, Pristatsky P, Fang Y, McKelvey T, et al. Impact of methionine oxidation on the binding of human IgG1 to Fc Rn and Fc gamma receptors. Mol Immunol 2009; 46:1878-82; PMID:19269032; http://dx.doi.org/10.1016/j.molimm.2009.02.002
32. Wang W, Vlasak J, Li Y, Pristatsky P, Fang Y, Pittman T, et al. Impact of methionine oxidation in human IgG1 Fc on serum half-life of monoclonal antibodies. Mol Immunol 2011; 48:860-6; PMID:21256596; http://dx.doi.org/10. 1016/j.molimm.2010.12.009
33. Vaughn DE, Bjorkman PJ. Structural basis of pH-dependent antibody binding by the neonatal Fc receptor. Structure 1998; 6:63-73; PMID:9493268; http://dx.doi.org/10.1016/S0969-2126(98)00008-2
34. Spiekermann GM, Finn PW, Ward ES, Dumont J, Dickinson BL, Blumberg RS, et al. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J Exp Med 2002; 196:303-10; PMID:12163559; http://dx.doi.org/10.1084/jem.20020400
35. Zalevsky J, Chamberlain AK, Horton HM, Karki S, Leung IWL, Sproule TJ, et al. Enhanced antibody half-life improves in vivo activity. Nat Biotechnol 2010; 28:157-9; PMID:20081867; http://dx.doi.org/10.1038/nbt.1601
36. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C. Sequences of proteins of immunological interest. 5th edition, U.S. Public Health Services, National Institute of Health (NIH) 1991; publication no. 91-3242, Bethesda, MD.
37. Qiao SW, Kobayashi K, Johansen FE, Sollid LM, Andersen JT, Milford E, et al. Dependence of antibody-mediated presentation of antigen on FcRn. Proc Natl Acad Sci U S A 2008; 105:9337-42; PMID:18599440; http://dx.doi.org/10.1073/pnas. 0801717105
38. Ji Z, Lee JY, Pan Z, Jiang B, Tian B. Progressive lengthening of 3′ untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc Natl Acad Sci U S A 2009; 106:7028-33; PMID:19372383; http://dx.doi.org/10.1073/pnas.0900028106
39. Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 2007; 7:715-25; PMID:17703228; http://dx.doi.org/10.1038/nri2155
40. Roopenian DC, Christianson GJ, Sproule TJ, Brown AC, Akilesh S, Jung N, et al. The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J Immunol 2003; 170:3528-33; PMID:12646614
41. Roopenian DC, Christianson GJ, Sproule TJ. Human FcRn transgenic mice for pharmacokinetic evaluation of therapeutic antibodies. Methods Mol Biol 2010; 602:93-104; PMID:20012394; http://dx.doi.org/10.1007/978-1-60761-058-8-6