Genetically engineered humanized mouse models for preclinical antibody studies

BioDrugs

Volumn 28, Issue 2, 2014, Pages 171-180

  Proetzel, Gabriele ^a   Wiles, Michael V ^a   Roopenian, Derry C ^a  

^a JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; FC RECEPTOR; HYBRID PROTEIN; MONOCLONAL ANTIBODY; NEONATAL FC RECEPTOR; NUCLEASE; TAL EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; FC RECEPTOR, NEONATAL; HLA ANTIGEN CLASS 1;

ARTHRITIS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; EMBRYONIC STEM CELL; GENETIC ENGINEERING; GENETICALLY ENGINEERED MOUSE STRAIN; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSGENIC MOUSE; TUMOR XENOGRAFT; ANIMAL; ANIMAL MODEL; HUMAN; IMMUNOLOGY; MOUSE; PROCEDURES;

ANIMALS; ANTIBODIES, MONOCLONAL; GENETIC ENGINEERING; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; RECEPTORS, FC;

EID: 84897037852     PISSN: 11738804     EISSN: 1179190X     Source Type: Journal    
DOI: 10.1007/s40259-013-0071-0     Document Type: Review

References (80)

1. Murray WS. The Breeding Behavior of the Dilute Brown Stock of Mice (Little dba). Am J Cancer. 1934;20(3):573-93. doi:10.1158/ajc.1934.573.
2. Festing MF. Inbred strains should replace outbred stocks in toxicology, safety testing, and drug development. Toxicol Pathol. 2010;38(5):681-90. doi:10.1177/0192623310373776.
3. Festing MF. Improving toxicity screening and drug development by using genetically defined strains. Methods Mol Biol. 2010;602:1-21. doi:10.1007/978-1-60761-058-8-1.
4. Beck JA, Lloyd S, Hafezparast M, Lennon-Pierce M, Eppig JT, Festing MF, et al. Genealogies of mouse inbred strains. Nat Genet. 2000;24(1):23-5. doi:10.1038/71641. (Pubitemid 30041415)
5. Anderson MG, Smith RS, Hawes NL, Zabaleta A, Chang B, Wiggs JL, et al. Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice. Nat Genet. 2002;30(1):81-5. doi:10.1038/ng794.
6. Serreze DV, Chapman HD, Varnum DS, Gerling I, Leiter EH, Shultz LD. Initiation of autoimmune diabetes in NOD/Lt mice is MHC class I-dependent. J Immunol. 1997;158(8):3978-86. (Pubitemid 127488759)
7. Jaenisch R. Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc Natl Acad Sci USA. 1976;73(4):1260-4.
8. Gordon JW, Ruddle FH. Integration and stable germ line transmission of genes injected into mouse pronuclei. Science. 1981; 214(4526):1244-6. (Pubitemid 12167330)
9. Costantini F, Lacy E. Introduction of a rabbit beta-globin gene into the mouse germ line. Nature. 1981;294(5836):92-4. (Pubitemid 12208163)
10. Wagner EF, Stewart TA, Mintz B. The human beta-globin gene and a functional viral thymidine kinase gene in developing mice. Proc Natl Acad Sci USA. 1981;78(8):5016-20. (Pubitemid 12225613)
11. Brinster RL, Chen HY, Warren R, Sarthy A, Palmiter RD. Regulation of metallothionein-thymidine kinase fusion plasmids injected into mouse eggs. Nature. 1982;296(5852):39-42. (Pubitemid 12159989)
12. Doetschman T, Maeda N, Smithies O. Targeted mutation of the HPRT gene in mouse embryonic stem cells. Proc Natl Acad Sci USA. 1988;85(22):8583-7. (Pubitemid 19025002)
13. Thomas KR, Folger KR, Capecchi MR. High frequency targeting of genes to specific sites in the mammalian genome. Cell. 1986;44(3):419-28. (Pubitemid 16043333)
14. Nishijima H, Yasunari T, Nakayama T, Adachi N, Shibahara K. Improved applications of the tetracycline-regulated gene depletion system. Biosci Trends. 2009;3(5):161-7.
15. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA. 1992;89(12):5547-51.
16. Feil R, Wagner J, Metzger D, Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun. 1997;237(3):752-7. doi:10.1006/bbrc.1997.7124. (Pubitemid 27434760)
17. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823-6. doi:10.1126/science.1232033.
18. Barrangou R. RNA-mediated programmable DNA cleavage. Nat Biotech. 2012;30(9):836-8. doi:10.1038/nbt.2357.
19. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819-23.
20. Shen B, Zhang J, Wu H, Wang J, Ma K, Li Z, et al. Generation of gene-modified mice via Cas9/RNA-mediated gene targeting. Cell Res. 2013;23(5):720-3. doi:10.1038/cr.2013.46.
21. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/cas-mediated genome engineering. Cell. 2013;153(4):910-8.
22. Carbery ID, Ji D, Harrington A, Brown V, Weinstein EJ, Liaw L, et al. Targeted genome modification in mice using zinc-finger nucleases. Genetics. 2010;186(2):451-9. doi:10.1534/genetics.110.117002.
23. Cui X, Ji D, Fisher DA, Wu Y, Briner DM, Weinstein EJ. Targeted integration in rat and mouse embryos with zinc-finger nucleases. Nat Biotechnol. 2011;29(1):64-7. doi:10.1038/nbt.1731.
24. Wang H, Hu YC, Markoulaki S, Welstead GG, Cheng AW, Shivalila CS, et al. TALEN-mediated editing of the mouse Y chromosome. Nat Biotechnol. 2013;31(6):530-2. doi:10.1038/nbt.2595.
25. Davies B, Davies G, Preece C, Puliyadi R, Szumska D, Bhattacharya S. Site specific mutation of the Zic2 locus by microinjection of TALEN mRNA in mouse CD1, C3H and C57BL/6Joocytes. PLoS One. 2013;8(3):e60216. doi:10.1371/journal. pone.0060216.
26. Qiu Z, Liu M, Chen Z, Shao Y, Pan H, Wei G, et al. High-efficiency and heritable gene targeting in mouse by transcription activator-like effector nucleases. Nucleic Acids Res. 2013;41(11):e120. doi:10.1093/nar/gkt258.
27. Sung YH, Baek IJ, Kim DH, Jeon J, Lee J, Lee K, et al. Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol. 2013;31(1):23-4. doi:10.1038/nbt.2477.
28. Meyer M, Ortiz O, Hrabe de Angelis M, Wurst W, Kuhn R. Modeling disease mutations by gene targeting in one-cell mouse embryos. Proc Natl Acad Sci USA. 2012;109(24):9354-9. doi:10.1073/pnas.1121203109.
29. Wefers B, Meyer M, Ortiz O, Hrabe de Angelis M, Hansen J, Wurst W, et al. Direct production of mouse disease models by embryo microinjection of TALENs and oligodeoxynucleotides. Proc Natl Acad Sci USA. 2013;110(10):3782-7. doi:10.1073/pnas.1218721110.
30. Gaj T, Gersbach CA, Barbas CF, 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013. doi:10.1016/j.tibtech. 2013.04.004.
31. Simister NE, Mostov KE. An Fc receptor structurally related to MHC class I antigens. Nature. 1989;337(6203):184-7. doi:10.1038/337184a0. (Pubitemid 19025381)
32. Ahouse JJ, Hagerman CL, Mittal P, Gilbert DJ, Copeland NG, Jenkins NA, et al. Mouse MHC class I-like Fc receptor encoded outside the MHC. J Immunol. 1993;151(11):6076-88. (Pubitemid 23340354)
33. Raghavan M, Gastinel LN, Bjorkman PJ. The class I major histocompatibility complex related Fc receptor shows pH-dependent stability differences correlating with immunoglobulin binding and release. Biochemistry. 1993;32(33):8654-60. (Pubitemid 23270453)
34. Burmeister WP, Gastinel LN, Simister NE, Blum ML, Bjorkman PJ. Crystal structure at 2.2 A resolution of the MHC-related neonatal Fc receptor. Nature. 1994;372(6504):336-43. doi:10.1038/372336a0.
35. Burmeister WP, Huber AH, Bjorkman PJ. Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature. 1994;372(6504):379-83. doi:10.1038/372379a0. (Pubitemid 24363442)
36. Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol. 2007;7(9):715-25. (Pubitemid 47327396)
37. Ghetie V, Ward ES. FcRn: the MHC class I-related receptor that is more than an IgG transporter. Immunol Today. 1997;18(12):592-8. (Pubitemid 28012280)
38. Ghetie V, Ward ES. Multiple roles for the major histocompatibility complex class I- related receptor FcRn. Annu Rev Immunol. 2000;18:739-66. (Pubitemid 30365396)
39. Tzaban S, Massol RH, Yen E, Hamman W, Frank SR, Lapierre LA, et al. The recycling and transcytotic pathways for IgG transport by FcRn are distinct and display an inherent polarity. J Cell Biol. 2009;185(4):673-84. doi:10.1083/jcb.200809122.
40. Anderson CL, Chaudhury C, Kim J, Bronson CL, Wani MA, Mohanty S. Perspective-FcRn transports albumin: relevance to immunology and medicine. Trends Immunol. 2006;27(7):343-8. doi:10.1016/j.it.2006.05.004. (Pubitemid 43963476)
41. Kuo TT, de Muinck EJ, Claypool SM, Yoshida M, Nagaishi T, Aveson VG, et al. N-glycan moieties in neonatal Fc receptor determine steady-state membrane distribution and directional transport of IgG. J Biol Chem. 2009;284(13):8292- 300. doi:10.1074/jbc.M805877200.
42. Baker K, Qiao SW, Kuo TT, Aveson VG, Platzer B, Andersen JT, et al. Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b ? dendritic cells. Proc Natl Acad Sci USA. 2011;108(24):9927-32. doi:10.1073/pnas.1019037108.
43. Kobayashi K, Qiao SW, Yoshida M, Baker K, Lencer WI, Blumberg RS. An FcRn-dependent role for anti-flagellin immunoglobulin G in pathogenesis of colitis in mice. Gastroenterology. 2009;137(5):1746-56 e1. doi:10.1053/j.gastro. 2009.07.059.
44. Liu X, Lu L, Yang Z, Palaniyandi S, Zeng R, Gao LY, et al. The neonatal FcR-mediated presentation of immune-complexed antigen is associated with endosomal and phagosomal pH and antigen stability in macrophages and dendritic cells. J Immunol. 2011;186(8):4674-86. doi:10.4049/jimmunol.1003584.
45. Vegh A, Farkas A, Kovesdi D, Papp K, Cervenak J, Schneider Z, et al. FcRn overexpression in transgenic mice results in augmented APC activity and robust immune response with increased diversity of induced antibodies. PLoS One. 2012;7(4):e36286. doi:10.1371/journal.pone.0036286.
46. 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(12):1551-9. (Pubitemid 33133882)
47. Chaudhury C, Mehnaz S, Robinson JM, Hayton WL, Pearl DK, Roopenian DC, et al. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J Exp Med. 2003;197(3):315-22. (Pubitemid 36184238)
48. 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-Fccoupled drugs. J Immunol. 2003;170(7):3528-33. (Pubitemid 36359219)
49. 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(12):1759-69. (Pubitemid 44884038)
50. Roopenian DC, Christianson GJ, Sproule TJ. Human FcRn transgenic mice for pharmacokinetic evaluation of therapeutic antibodies. Methods Mol Biol. 2010;602:93-104.
51. Stein C, Kling L, Proetzel G, Roopenian DC, de Angelis MH, Wolf E, et al. Clinical chemistry of human FcRn transgenic mice. Mamm Genome. 2012;23(3-4):259-69. doi:10.1007/s00335-011-9379-6.
52. Zalevsky J, Chamberlain AK, Horton HM, Karki S, Leung IW, Sproule TJ, et al. Enhanced antibody half-life improves in vivo activity. Nat Biotechnol. 2010;28(2):157-9. doi:10.1038/nbt.1601.
53. Lloyd KC. A knockout mouse resource for the biomedical research community. Ann N Y Acad Sci. 2011;1245:24-6. doi:10.1111/j.1749-6632.2011.06311. x.
54. Ayadi A, Birling MC, Bottomley J, Bussell J, Fuchs H, Fray M, et al. Mouse large-scale phenotyping initiatives: overview of the European Mouse Disease Clinic (EUMODIC) and of the Wellcome Trust Sanger Institute Mouse Genetics Project. Mamm Genome. 2012;23(9-10):600-10. doi:10.1007/s00335-012- 9418-y.
55. Austin CP, Battey JF, Bradley A, Bucan M, Capecchi M, Collins FS, et al. The knockout mouse project. Nat Genet. 2004;36(9):921-4. doi:10.1038/ng0904-921. (Pubitemid 351319639)
56. Auwerx J, Avner P, Baldock R, Ballabio A, Balling R, Barbacid M, et al. The European dimension for the mouse genome mutagenesis program. Nat Genet. 2004;36(9):925-7. doi:10.1038/ng0904-925. (Pubitemid 351319640)
57. McMurray F, Moir L, Cox RD. From mice to humans. Curr Diab Rep. 2012;12(6):651-8. doi:10.1007/s11892-012-0323-2.
58. Lewandoski M. Conditional control of gene expression in the mouse. Nat Rev Genet. 2001;2(10):743-55. doi:10.1038/35093537. (Pubitemid 33685572)
59. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292(5819):154-6. (Pubitemid 11050741)
60. Santiago Y, Chan E, Liu PQ, Orlando S, Zhang L, Urnov FD, et al. Targeted gene knockout in mammalian cells by using engineered zinc-finger nucleases. Proc Natl Acad Sci USA. 2008;105(15):5809-14. doi:10.1073/pnas.0800940105. (Pubitemid 351758454)
61. Meyer M, de Angelis MH, Wurst W, Kuhn R. Gene targeting by homologous recombination in mouse zygotes mediated by zincfinger nucleases. Proc Natl Acad Sci USA. 2010;107(34):15022-6. doi:10.1073/pnas.1009424107.
62. Reyon D, Khayter C, Regan MR, Joung JK, Sander JD. Engineering designer transcription activator-like effector nucleases (TALENs) by REAL or REAL-Fast assembly. In: Ausubel FM et al, editor. Current protocols in molecular biology. 2012;Chapter 12.
63. Joung JK, Sander JD. TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol. 2013;14(1):49-55. doi:10.1038/nrm3486.
64. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol. 2011;29(2):143-8. doi:10.1038/nbt.1755.
65. Fujii W, Kawasaki K, Sugiura K, Naito K. Efficient generation of large-scale genome-modified mice using gRNA and CAS9 endonuclease. Nucleic Acids Res. 2013. doi:10.1093/nar/gkt772.
66. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell. 2013;154(6):1370-9. doi:10.1016/j.cell.2013.08.022.
67. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotech. 2013;advance online publication. doi:10.1038/nbt.2623. http://www.nature.com/nbt/journal/vaop/ncurrent/abs/nbt.2623.html. supplementaryinformation.
68. 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(3):1-9.
69. Dumont JA, Liu T, Low SC, Zhang X, Kamphaus G, Sakorafas P, et al. Prolonged activity of a recombinant factor VIII-Fc fusion protein in hemophilia A mice and dogs. Blood. 2012;119(13):3024-30. doi:10.1182/blood-2011-08-367813.
70. Wunder A, Muller-Ladner U, Stelzer EH, Funk J, Neumann E, Stehle G, et al. Albumin-based drug delivery as novel therapeutic approach for rheumatoid arthritis. J Immunol. 2003;170(9):4793-801. (Pubitemid 36519989)
71. Fiehn C. Methotrexate transport mechanisms: the basis for targeted drug delivery and ss-folate-receptor-specific treatment. Clin Exp Rheumatol. 2010;28(5 Suppl 61):S40-5.
72. Muller MR, Saunders K, Grace C, Jin M, Piche-Nicholas N, Steven J et al. Improving the pharmacokinetic properties of biologics by fusion to an anti-HSA shark VNAR domain. mAbs. 2012;4(6):673-85. doi:10.4161/mabs.22242.
73. Stork R, Campigna E, Robert B, Müller D, Kontermann RE. Biodistribution of a bispecific single-chain diabody and its halflife extended derivatives. J Biol Chem. 2009;284(38):25612-9. doi:10.1074/jbc.M109.027078.
74. Andersen JT, Pehrson R, Tolmachev V, Daba MB, Abrahmsen L, Ekblad C. Extending half-life by indirect targeting of the neonatal Fc receptor (FcRn) using a minimal albumin binding domain. J Biol Chem. 2011;286(7):5234-41.
75. Muller D, Karle A, Meissburger B, Hofig I, Stork R, Kontermann RE. Improved pharmacokinetics of recombinant bispecific antibody molecules by fusion to human serum albumin. J Biol Chem. 2007;282(17):12650-60. doi:10.1074/jbc.M700820200. (Pubitemid 47100581)
76. Dennis MS, Zhang M, Meng YG, Kadkhodayan M, Kirchhofer D, Combs D, et al. Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J Biol Chem. 2002;277(38):35035-43. doi:10.1074/jbc.M205854200.
77. Nguyen A, Reyes AE 2nd, Zhang M, McDonald P, Wong WL, Damico LA, et al. The pharmacokinetics of an albumin-binding Fab (AB.Fab) can be modulated as a function of affinity for albumin. Protein Eng Des Sel. 2006;19(7):291-7. doi:10.1093/protein/gzl011. (Pubitemid 43999639)
78. 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(7):4826-36. doi:10.1074/jbc.M109.081828.
79. Petkova SB, Konstantinov KN, Sproule TJ, Lyons BL, Awwami MA, Roopenian DC. Human antibodies induce arthritis in mice deficient in the low-affinity inhibitory IgG receptor Fc gamma RIIB. J Exp Med. 2006;203(2):275-80. doi:10.1084/jem.20051951. (Pubitemid 43290836)
80. Akilesh S, Petkova S, Sproule TJ, Shaffer DJ, Christianson GJ, Roopenian D. The MHC class I-like Fc receptor promotes humorally mediated autoimmune disease. J Clin Investig. 2004;113(9):1328-33. doi:10.1172/jci200418838. (Pubitemid 39069932)