The neonatal Fc receptor (FcRn) binds independently to both sites of the IgG homodimer with identical affinity

mAbs

Volumn 7, Issue 2, 2015, Pages 331-343

  Abdiche, Yasmina Noubia ^a   Yeung, Yik Andy ^a   Chaparro Riggers, Javier ^a   Barman, Ishita ^a   Strop, Pavel ^a   Chin, Sherman Michael ^a   Pham, Amber ^a   Bolton, Gary ^a   McDonough, Dan ^a   Lindquist, Kevin ^a   Pons, Jaume ^a   Rajpal, Arvind ^a  

^a PFIZER INC   (United States)

Author keywords

FcRn; IgG; Label free biosensor; Neonatal Fc receptor; SPR

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; FC RECEPTOR, NEONATAL; HLA ANTIGEN CLASS 1; IMMUNOGLOBULIN FC FRAGMENT;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CLEARANCE; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; HUMAN; MOUSE; NONHUMAN; PH; PLASMA HALF LIFE; RAT; STOICHIOMETRY; SURFACE PLASMON RESONANCE; ANIMAL; CHEMISTRY; IMMUNOLOGY; MACACA FASCICULARIS; SPECIES DIFFERENCE;

ANIMALS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MACACA FASCICULARIS; MICE; RATS; RECEPTORS, FC; SPECIES SPECIFICITY; SURFACE PLASMON RESONANCE;

EID: 84924528149     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2015.1008353     Document Type: Article

References (40)

1. RoopenianDC, 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
2. Rath T, Baker K, Dumont JA, Peters RT, Jiang H, Qiao SW, LencerWI, Pierce GF, Blumberg RS. Fc-fusion proteins and FcRn: structural insights for longer-lasting and more effective therapeutics. Crit Rev Biotechnol 2013; doi:10.3109/07388551.2013.834293; PMID:24156398
3. Yeung YA, Leabman MK, Marvin JS, Qiu J, Adams CW, Lien S, Starovasnik MA, Lowman HB. 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
4. Burmeister WP, Huber AH, Bjorkman PJ. Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature 1994; 372:379-83; PMID:7969498; http://dx.doi.org/10.1038/372379a0
5. Popov S, Hubbard JG, Kim J, Ober B, Ghetie V, Ward ES. The stoichiometry and affinity of the interaction of murine Fc fragments with the MHC class I-related receptor, FcRn. Mol Immunol 1996; 33:521-30; PMID:8700168; http://dx.doi.org/10.1016/0161-5890(96)00004-1
6. Schuck P, Radu CG, Ward ES. Sedimentation equilibrium analysis of recombinant mouse FcRn with murine IgG1. Mol Immunol 1999; 36:1117-25; PMID:10698313; http://dx.doi.org/10.1016/S0161-5890(99)00093-0
7. 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
8. Sánchez LM, Penny DM, Bjorkman PJ. Stoichiometry of the interaction between the major histocompatibility complex-related Fc receptor and its Fc ligand. Biochemistry 1999; 38:9471-76; PMID:10413524; http://dx.doi.org/10.1021/bi9907330
9. West AP Jr, Bjorkman PJ. Crystal structure and immunoglobulin G binding properties of the human major histocompatibility complex-related Fc receptor. Biochemistry 2000; 39:9698-08; PMID:10933786; http:// dx.doi.org/10.1021/bi000749m
10. 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 USA 1995; 92:11200-204; PMID:7479965; http://dx.doi.org/10.1073/ pnas.92.24.11200
11. Oganesyan V, Damschroder MM, Cook KE, Li Q, Gao C, Wu H, Dall'Acqua WF. Structural insights into neonatal Fc receptor-based recycling mechanisms. J Biol Chem 2014; 289:7812-24; PMID:24469444; http://dx.doi.org/10.1074/jbc.M113.537563
12. 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
13. Bitonti AJ, Dumont JA, Low SC, Peters RT, Kropp KE, Palombella VJ, Stattel JM, Lu Y, Tan CA, Song JJ et al. Pulmonary delivery of an erythropoietin Fc fusion protein in non-human primates through an immunoglobulin transport pathway. Proc Natl Acad Sci USA 2004; 101:9763-68; PMID:15210944; http://dx.doi. org/10.1073/pnas.0403235101
14. Kamei DT, Lao BJ, Ricci MS, Deshpande R, Xu H, Tidor B, Lauffenburger DA. Quantitative methods for developing Fc mutants with extended half-lives. Biotechnol Bioeng 2005; 92:748-60; PMID:16136591; http://dx.doi.org/10.1002/bit.20624
15. 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
16. Kacskovics I, Kis Z, Mayer B, West AP Jr, Tiangco NE, Tilahun M, Cervenak L, Bjorkman PJ, Goldsby RA, Szenci O, et al. FcRn mediates elongated serum halflife of human IgG in cattle. Int Immunol 2006; 18:525-36; PMID:16481343; http://dx.doi.org/ 10.1093/intimm/dxh393
17. Datta-Mannan A, Witcher DR, Tang Y, Watkins J, Jiang W, Wroblewski VJ. Humanized IgG1 variants with differential binding properties to the neonatal Fc receptor: relationship to pharmacokinetics in mice and primates. Drug Metab Dispos 2007; 35:86-94; PMID:17050651; http://dx.doi.org/10.1124/dmd. 106.011734
18. Andersen JT, Daba MB, Berntzen G, Michaelsen TE, Sandlie I. Cross-species binding analyses of mouse and human neonatal Fc receptor show dramatic differences in immunoglobulin G and albumin binding. J Biol Chem 2010; 285:4826-36; PMID:20018855; http:// dx.doi.org/10.1074/jbc.M109.081828
19. Deng R, Loyet KM, Lien S, Iyer S, DeForge LE, Theil FP, Lowman HB, Fielder PJ, Prabhu S. Pharmacokinetics of humanized monoclonal anti-tumor necrosis factor-{alpha} antibody and its neonatal Fc receptor variants in mice and cynomolgus monkeys. Drug Metab Dispos 2010; 38:600-05; PMID:20071453; http://dx.doi.org/10.1124/dmd.109.031310
20. Suzuki T, Ishii-Watabe A, Tada M, Kobayashi T, Kanayasu-Toyoda T, Kawanishi T, Yamaguchi T. Importance of neonatal FcR in regulating the serum half-life of therapeutic proteins containing the Fc domain of human IgG1: a comparative study of the affinity of monoclonal antibodies and Fc-fusion proteins to human neonatal FcR. J Immunol 2010; 184:1968-76; PMID:20083659; http://dx.doi.org/ 10.4049/jimmunol.0903296
21. Magistrelli G, Malinge P, Anceriz N, Desmurs M, Venet S, Calloud S, Daubeuf B, Kosco-Vilbois M, Fischer N. Robust recombinant FcRn production in mammalian cells enabling oriented immobilization for IgG binding studies. J Immunol Methods 2012; 375:20-9; PMID:21939661; http://dx.doi.org/ 10.1016/j.jim.2011.09.002
22. WangW, Lu P, Fang Y, Hamuro L, Pittman T, Carr B, Hochman J, Prueksaritanont T. 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
23. Andersen JT, Foss S, Kenanova VE, Olafsen T, Leikfoss IS, Roopenian DC, Wu AM, Sandlie I. Anti-carcinoembryonic antigen single-chain variable fragment antibody variants bind mouse and human neonatal Fc receptor with different affinities that reveal distinct cross-species differences in serum half-life. J Biol Chem 2012; 287:22927-37; PMID:22570488; http://dx.doi. org/10.1074/jbc.M112.355131
24. Neuber T, Frese K, Jaehrling J, Jäger S, Daubert D, Felderer K, LinnemannM, Höhne A, Kaden S, Kölln J, et al Characterization and screening of IgG binding to the neonatal Fc receptor. mAbs 2014; 6:928-42; PMID:24802048; http:// dx.doi.org/10.4161/mabs.28744
25. Myszka DG. Improving biosensor analysis. J Mol Recognit 1999; 12:279-84; PMID:10556875; http://dx. doi.org/10.1002/(SICI)1099-1352(199909/10) 12:5%3c279::AID-JMR473%3e3.0.CO;2-3
26. Jakoi ER, Cambier J, Saslow S. Transepithelial transport of maternal antibody: purification of IgG receptor from newborn rat intestine. J Immunol 1985; 135:3360-64; PMID:2931482
27. Hobbs SM, Jackson LE, Peppard JV. Binding of subclasses of rat immunoglobulin G to detergent-isolated Fc receptor from neonatal rat intestine. J Biol Chem 1987; 262:8041-46; PMID:3597360
28. Ober RJ, Radu CG, Ghetie V, Ward ES. Differences in promiscuity for antibody-FcRn interactions across species: implications for therapeutic antibodies. Int Immunol 2001; 13:1551-59; PMID:11717196; http:// dx.doi.org/10.1093/intimm/13.12.1551
29. Strop P, Ho WH, Boustany LM, Abdiche YN, Lindquist KC, Farias SE, Rickert M, Appah CT, Pascua E, Radcliffe T, et al. Generating bispecific human IgG1 and IgG2 antibodies from any antibody pair. J Mol Biol 2012; 420:204-19; PMID:22543237; http://dx. doi.org/10.1016/j.jmb.2012.04.020
30. Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, Briggs J, Xie D, Lai J, Stadlen A, Li B, et al. High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J Biol Chem 2001; 276:6591-604; PMID:11096108; http://dx.doi.org/10.1074/jbc. M009483200
31. Walsh ST, Jevitts LM, Sylvester JE, Kossiakoff AA. Site2 binding energetics of the regulatory step of growth hormone-induced receptor homodimerization. Protein Sci 2003; 12:1960-70; PMID:12930995; http://dx.doi.org/10.1110/ps.03133903
32. Armour KL, Clark MR, Hadley AG, Williamson LM. Recombinant human IgG molecules lacking Fcgamma receptor binding and monocyte triggering activities. Eur J Immunol 1999; 29:2613-24; PMID:10458776; http://dx.doi.org/10.1002/(SICI)1521-4141(199908) 29:08%3c2613::AID-IMMU2613%3e3.0.CO;2-J
33. Abdiche YN, Lindquist KC, Pinkerton A, Pons J, Rajpal A. Expanding the ProteOn XPR36 biosensor into a 36-ligand array expedites protein interaction analysis. Anal Biochem 2011; 411:139-51; PMID:21168382; http://dx.doi.org/10.1016/j.ab.2010.12.020
34. Drake AW, Tang ML, Papalia GA, Landes G, Haak-Frendscho M, Klakamp SL. Biacore surface matrix effects on the binding kinetics and affinity of an antigen/ antibody complex. Anal Biochem 2012; 429:58-69; PMID:22766435; http://dx.doi.org/10.1016/j.ab.2012.06.024
35. 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
36. Igawa T, Tsunoda H, Tachibana T, Maeda A, Mimoto F, Moriyama C, Nanami M, Sekimori Y, Nabuchi Y, Aso Y, et al. Reduced elimination of IgG antibodies by engineering the variable region. Protein Eng Des Sel 2010; 23:385-92; PMID:20159773; http://dx.doi.org/ 10.1093/protein/gzq009
37. Tesar DB, Tiangco NE, Bjorkman PJ. Ligand valency affects transcytosis, recycling and intracellular trafficking mediated by the neonatal Fc receptor. Traffic 2006; 7:1127-2; PMID:17004319; http://dx.doi.org/ 10.1111/j.1600-0854.2006.00457.x
38. Bee C, Abdiche YN, Pons J, Rajpal A. Determining the binding affinity of therapeutic monoclonal antibodies towards their native unpurified antigens in human serum. PLoS One 2013; 8(11):e80501; PMID:24223227; http://dx.doi.org/10.1371/journal.pone.0080501
39. Bravman T, Bronner V, Lavie K, Notcovich A, Papalia GA, Myszka DG. See comment in PubMed Commons belowExploring "one-shot" kinetics and small molecule analysis using the ProteOn XPR36 array biosensor. Anal Biochem 2006; 358:281-88; PMID:16962556; http://dx.doi.org/10.1016/j.ab.2006.08.005
40. Gastinel LN, Simister NE, Bjorkman PJ. Expression and crystallization of a soluble and functional form of an Fc receptor related to class I histocompatibility molecules. Proc Natl Acad Sci USA 1992; 89:638-42; PMID:1530991; http://dx.doi.org/10.1073/pnas.89.2.638