Utility of a human FcRn transgenic mouse model in drug discovery for early assessment and prediction of human pharmacokinetics of monoclonal antibodies

References

• Reichert JM. Antibodies to watch in 2015. mAbs 2015; 7:1–8; PMID:25484055; http://dx.doi.org/10.4161/19420862.2015.988944
   PubMed Web of Science ®Google Scholar
• Shi S. Biologics: an update and challenge of their pharmacokinetics. Curr Drug Metab 2014; 15:271–90; PMID:24745789; http://dx.doi.org/10.2174/138920021503140412212905
   PubMed Web of Science ®Google Scholar
• Hotzel I, Theil FP, Bernstein LJ, Prabhu S, Deng R, Quintana L, Lutman J, Sibia R, Chan P, Bumbaca D, et al. A strategy for risk mitigation of antibodies with fast clearance. mAbs 2012; 4:753–60; PMID:23778268; http://dx.doi.org/10.4161/mabs.22189
   PubMed Web of Science ®Google Scholar
• Oitate M, Masubuchi N, Ito T, Yabe Y, Karibe T, Aoki T, Murayama N, Kurihara A, Okudaira N, Izumi T.. Prediction of human pharmacokinetics of therapeutic monoclonal antibodies from simple allometry of monkey data. Drug Metab Pharmacokinet 2011; 26:423–30; PMID:21606605; http://dx.doi.org/10.2133/dmpk.DMPK-11-RG-011
   PubMed Web of Science ®Google Scholar
• Deng R, Iyer S, Theil FP, Mortensen DL, Fielder PJ, Prabhu S. Projecting human pharmacokinetics of therapeutic antibodies from nonclinical data: what have we learned? mAbs 2011; 3:61–6; PMID:20962582; http://dx.doi.org/10.4161/mabs.3.1.13799
   PubMed Web of Science ®Google Scholar
• Dong JQ, Salinger DH, Endres CJ, Gibbs JP, Hsu CP, Stouch BJ, Hurh E, Gibbs MA.. Quantitative prediction of human pharmacokinetics for monoclonal antibodies: retrospective analysis of monkey as a single species for first-in-human prediction. Clin Pharmacokinet 2011; 50:131–42; PMID:21241072; http://dx.doi.org/10.2165/11537430-000000000-00000
   PubMed Web of Science ®Google Scholar
• Ling J, Zhou H, Jiao Q, Davis HM. Interspecies scaling of therapeutic monoclonal antibodies: initial look. J Clin Pharmacol 2009; 49:1382–402; PMID:19837907; http://dx.doi.org/10.1177/0091270009337134
   PubMed Web of Science ®Google Scholar
• Mager DE. Target-mediated drug disposition and dynamics. Biochem Pharmacol 2006; 72:1–10; PMID:16469301; http://dx.doi.org/10.1016/j.bcp.2005.12.041
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Roopenian DC, Christianson GJ, Sproule TJ, Brown AC, Akilesh S, Jung N, Petkova S, Avanessian L, Choi EY, Shaffer DJ, 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; http://dx.doi.org/10.4049/jimmunol.170.7.3528
   PubMed Web of Science ®Google Scholar
• Challa DK, Velmurugan R, Ober RJ, Sally Ward E. FcRn: from molecular interactions to regulation of IgG pharmacokinetics and functions. Curr Top Microbiol Immunol 2014; 382:249–72; PMID:25116104
   PubMed Web of Science ®Google Scholar
• Wines BD, Powell MS, Parren PW, Barnes N, Hogarth PM. The IgG Fc contains distinct Fc receptor (FcR) binding sites: the leukocyte receptors Fc gamma RI and Fc gamma RIIa bind to a region in the Fc distinct from that recognized by neonatal FcR and protein A. J Immunol 2000; 164:5313–8; PMID:10799893; http://dx.doi.org/10.4049/jimmunol.164.10.5313
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Ward ES, Zhou J, Ghetie V, Ober RJ. Evidence to support the cellular mechanism involved in serum IgG homeostasis in humans. Int Immunol 2003; 15:187–95; PMID:12578848; http://dx.doi.org/10.1093/intimm/dxg018
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.4049/jimmunol.172.4.2021
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Petkova SB, Akilesh S, Sproule TJ, Christianson GJ, Al Khabbaz H, Brown AC, Presta LG, Meng YG, Roopenian DC.. 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
   PubMed Web of Science ®Google Scholar
• Zalevsky J, Chamberlain AK, Horton HM, Karki S, Leung IW, Sproule TJ, Lazar GA, Roopenian DC, Desjarlais JR.. Enhanced antibody half-life improves in vivo activity. Nat Biotechnol 2010; 28:157–9; PMID:20081867; http://dx.doi.org/10.1038/nbt.1601
   PubMed Web of Science ®Google Scholar
• Robbie GJ, Criste R, Dall'acqua WF, Jensen K, Patel NK, Losonsky GA, Griffin MP. A novel investigational Fc-modified humanized monoclonal antibody, motavizumab-YTE, has an extended half-life in healthy adults. Antimicrob Agents Chemother 2013; 57:6147–53; PMID:24080653; http://dx.doi.org/10.1128/AAC.01285-13
   PubMed Web of Science ®Google Scholar
• Zhu X, Meng G, Dickinson BL, Li X, Mizoguchi E, Miao L, Wang Y, Robert C, Wu B, Smith PD, et al. MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J Immunol 2001; 166:3266–76; PMID:11207281; http://dx.doi.org/10.4049/jimmunol.166.5.3266
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Akilesh S, Christianson GJ, Roopenian DC, Shaw AS. Neonatal FcR expression in bone marrow-derived cells functions to protect serum IgG from catabolism. J Immunol 2007; 179:4580–8; PMID:17878355; http://dx.doi.org/10.4049/jimmunol.179.7.4580
   PubMed Web of Science ®Google Scholar
• Borvak J, Richardson J, Medesan C, Antohe F, Radu C, Simionescu M, Ghetie V, Ward ES.. Functional expression of the MHC class I-related receptor, FcRn, in endothelial cells of mice. Int Immunol 1998; 10:1289–98; PMID:9786428; http://dx.doi.org/10.1093/intimm/10.9.1289
   PubMed Web of Science ®Google Scholar
• Dickinson BL, Badizadegan K, Wu Z, Ahouse JC, Zhu X, Simister NE, Blumberg RS, Lencer WI.. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J Clin Invest 1999; 104:903–11; PMID:10510331; http://dx.doi.org/10.1172/JCI6968
   PubMed Web of Science ®Google Scholar
• Shah U, Dickinson BL, Blumberg RS, Simister NE, Lencer WI, Walker WA. Distribution of the IgG Fc receptor, FcRn, in the human fetal intestine. Pediatr Res 2003; 53:295–301; PMID:12538789; http://dx.doi.org/10.1203/00006450-200302000-00015
   PubMed Web of Science ®Google Scholar
• Hornby PJ, Cooper PR, Kliwinski C, Ragwan E, Mabus JR, Harman B, Thompson S, Kauffman AL, Yan Z, Tam SH, et al. Human and non-human primate intestinal FcRn expression and immunoglobulin G transcytosis. Pharma Res 2014; 31:908–22; PMID:24072267; http://dx.doi.org/10.1007/s11095-013-1212-3
   PubMed Web of Science ®Google Scholar
• Chen N, Wang W, Fauty S, Fang Y, Hamuro L, Hussain A, Prueksaritanont T.. The effect of the neonatal Fc receptor on human IgG biodistribution in mice. mAbs 2014; 6:502–8; PMID:24492305; http://dx.doi.org/10.4161/mabs.27765
   PubMed Web of Science ®Google Scholar
• Yip V, Palma E, Tesar DB, Mundo EE, Bumbaca D, Torres EK, Reyes NA, Shen BQ, Fielder PJ, Prabhu S,. Quantitative cumulative biodistribution of antibodies in mice: effect of modulating binding affinity to the neonatal Fc receptor. mAbs 2014; 6:689–96; PMID:24572100; http://dx.doi.org/10.4161/mabs.28254
   PubMed Web of Science ®Google Scholar
• Tam SH, McCarthy SG, Brosnan K, Goldberg KM, Scallon BJ. Correlations between pharmacokinetics of IgG antibodies in primates vs. FcRn-transgenic mice reveal a rodent model with predictive capabilities. mAbs 2013; 5:397–405; PMID:23549129; http://dx.doi.org/10.4161/mabs.23836
   PubMed Web of Science ®Google Scholar
• Wang W, 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
   PubMed Web of Science ®Google Scholar
• Haraya K, Tachibana T, Nanami M, Ishigai M. Application of human FcRn transgenic mice as a pharmacokinetic screening tool of monoclonal antibody. Xenobiotica 2014; 44:1127–34; PMID:25030041; http://dx.doi.org/10.3109/00498254.2014.941963
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Ober RJ, Radu CG, Ghetie V, Ward ES. Differences in promiscuity for antibody-FcRn interactions across species: implications for therapeutic antibodies. Int Immunol 2001; 13:1551–9; PMID:11717196; http://dx.doi.org/10.1093/intimm/13.12.1551
   PubMed Web of Science ®Google Scholar
• Kelly RL, Sun T, Jain T, Caffry I, Yu Y, Cao Y, Lynaugh H, Brown M, Vásquez M, Wittrup KD, et al. High throughput cross-interaction measures for human IgG1 antibodies correlate with clearance rates in mice. mAbs 2015; 7:770–7; PMID:26047159; http://dx.doi.org/10.1080/19420862.2015.1043503
   PubMed Web of Science ®Google Scholar
• Joyce AP, Wang M, Lawrence-Henderson R, Filliettaz C, Leung SS, Xu X, O'Hara DM. One mouse, one pharmacokinetic profile: quantitative whole blood serial sampling for biotherapeutics. Pharma Res 2014; 31:1823–33; PMID:24464271; http://dx.doi.org/10.1007/s11095-013-1286-y
   PubMed Web of Science ®Google Scholar
• Van Oortmerssen GA. Biological Significance, Genetics and Evolutionary Origin of Variability in Behaviour Within and Between Inbred Strains of Mice (Mus Musculus). Behaviour 1971; 38:1–91; PMID:5100645; http://dx.doi.org/10.1163/156853971X00014
   PubMed Web of Science ®Google Scholar
• Borrok MJ, Wu Y, Beyaz N, Yu XQ, Oganesyan V, Dall'Acqua WF, Tsui P. pH-dependent binding engineering reveals an FcRn affinity threshold that governs IgG recycling. J Biol Chem 2015; 290:4282–90; PMID:25538249; http://dx.doi.org/10.1074/jbc.M114.603712
   PubMed Web of Science ®Google Scholar
• Dall'Acqua WF, Woods RM, Ward ES, Palaszynski SR, Patel NK, Brewah YA, Wu H, Kiener PA, Langermann S.. Increasing the affinity of a human IgG1 for the neonatal Fc receptor: biological consequences. J Immunol 2002; 169:5171–80; PMID:12391234; http://dx.doi.org/10.4049/jimmunol.169.9.5171
   PubMed Web of Science ®Google Scholar
• Proetzel G, Roopenian DC. Humanized FcRn mouse models for evaluating pharmacokinetics of human IgG antibodies. Methods 2014; 65:148–53; PMID:23867339; http://dx.doi.org/10.1016/j.ymeth.2013.07.005
   PubMed Web of Science ®Google Scholar
• Shah DK, Betts AM. Towards a platform PBPK model to characterize the plasma and tissue disposition of monoclonal antibodies in preclinical species and human. J Pharmacokinet Pharmacodyn 2012; 39:67–86; PMID:22143261; http://dx.doi.org/10.1007/s10928-011-9232-2
   PubMed Web of Science ®Google Scholar
• Chen Y, Balthasar JP. Evaluation of a catenary PBPK model for predicting the in vivo disposition of mAbs engineered for high-affinity binding to FcRn. AAPS J 2012; 14:850–9; PMID:22956476; http://dx.doi.org/10.1208/s12248-012-9395-9
   PubMed Web of Science ®Google Scholar
• Fan Y-Y, Neubert H. Quantitative Analysis of Human Neonatal Fc Receptor (FcRn) Tissue Expression in Transgenic Mice by Online Peptide Immuno-Affinity LC-HRMS. Anal Chem 2016; 88:4239–47; PMID:27012525; http://dx.doi.org/10.1021/acs.analchem.5b03900
   PubMed Web of Science ®Google Scholar
• Adolph EF. Quantitative Relations in the Physiological Constitutions of Mammals. Science 1949; 109:579–85; PMID:17835379; http://dx.doi.org/10.1126/science.109.2841.579
   PubMed Web of Science ®Google Scholar
• Kleiber M. Body size and metabolic rate. Physiol Rev 1947; 27:511–41; PMID:20267758
   PubMed Web of Science ®Google Scholar
• Shen BQ, Xu K, Liu L, Raab H, Bhakta S, Kenrick M, Parsons-Reponte KL, Tien J, Yu SF, Mai E, et al. Conjugation site modulates the in vivo stability and therapeutic activity of antibody-drug conjugates. Nat Biotechnol 2012; 30:184–9; PMID:22267010; http://dx.doi.org/10.1038/nbt.2108
   PubMed Web of Science ®Google Scholar
• Hamblett KJ, Senter PD, Chace DF, Sun MM, Lenox J, Cerveny CG, Kissler KM, Bernhardt SX, Kopcha AK, Zabinski RF, et al. Effects of drug loading on the antitumor activity of a monoclonal antibody drug conjugate. Clin Cancer Res 2004; 10:7063–70; PMID:15501986; http://dx.doi.org/10.1158/1078-0432.CCR-04-0789
   PubMed Web of Science ®Google Scholar
• Polson AG, Calemine-Fenaux J, Chan P, Chang W, Christensen E, Clark S, de Sauvage FJ, Eaton D, Elkins K, Elliott JM, et al. Antibody-drug conjugates for the treatment of non-Hodgkin's lymphoma: target and linker-drug selection. Cancer Res 2009; 69:2358–64; PMID:19258515; http://dx.doi.org/10.1158/0008-5472.CAN-08-2250
   PubMed Web of Science ®Google Scholar
• Chapman AP, Antoniw P, Spitali M, West S, Stephens S, King DJ. Therapeutic antibody fragments with prolonged in vivo half-lives. Nat Biotechnol 1999; 17:780–3; PMID:10429243; http://dx.doi.org/10.1038/11717
   PubMed Web of Science ®Google Scholar
• Dayde D, Ternant D, Ohresser M, Lerondel S, Pesnel S, Watier H, Le Pape A, Bardos P, Paintaud G, Cartron G. et al. Tumor burden influences exposure and response to rituximab: pharmacokinetic-pharmacodynamic modeling using a syngeneic bioluminescent murine model expressing human CD20. Blood 2009; 113:3765–72; PMID:19029438; http://dx.doi.org/10.1182/blood-2008-08-175125
   PubMed Web of Science ®Google Scholar
• Palandra J, Finelli A, Zhu M, Masferrer J, Neubert H. Highly specific and sensitive measurements of human and monkey interleukin 21 using sequential protein and tryptic peptide immunoaffinity LC-MS/MS. Anal Chem 2013; 85:5522–9; PMID:23638938; http://dx.doi.org/10.1021/ac4006765
   PubMed Web of Science ®Google Scholar
• Neubert H, Muirhead D, Kabir M, Grace C, Cleton A, Arends R. Sequential protein and peptide immunoaffinity capture for mass spectrometry-based quantification of total human beta-nerve growth factor. Anal Chem 2013; 85:1719–26; PMID:23249404; http://dx.doi.org/10.1021/ac303031q
   PubMed Web of Science ®Google Scholar
• Chen J, Wang M, Joyce A, DeFranco D, Kavosi M, Xu X, O'Hara DM. Comparison of succinimidyl [(125)I]iodobenzoate with iodogen iodination methods to study pharmacokinetics and ADME of biotherapeutics. Pharmaceutical research 2014; 31:2810–21; PMID:24844406; http://dx.doi.org/10.1007/s11095-014-1378-3
   PubMed Web of Science ®Google Scholar
• Lin LI. A concordance correlation coefficient to evaluate reproducibility. Biometrics 1989; 45:255–68; PMID:2720055; http://dx.doi.org/10.2307/2532051
   PubMed Web of Science ®Google Scholar