High-affinity IgG antibodies develop naturally in Ig-knockout rats carrying germline human IgH/Igκ/Igλ loci bearing the rat CH region

Journal of Immunology

Volumn 190, Issue 4, 2013, Pages 1481-1490

  Osborn, Michael J ^a   Ma, Biao ^a   Avis, Suzanne ^a   Binnie, Ashleigh ^a   Dilley, Jeanette ^b   Yang, Xi ^b   Lindquist, Kevin ^b   Ménoret, Séverine ^c   Iscache, Anne Laure ^c   Ouisse, Laure Hélène ^c   Rajpal, Arvind ^b   Anegon, Ignacio ^c   Neuberger, Michael S ^d   Buelow, Roland ^e   Brüggemann, Marianne ^a,e  

^a Recombinant Antibody Technology Ltd   (United Kingdom)

^b PFIZER INC   (United States)

^c INSERM   (France)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^e Open Monoclonal Technology Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LAMBDA CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; BREEDING; CELL MATURATION; CONTROLLED STUDY; EMBRYO; FEMALE; FLOW CYTOMETRY; GENE INACTIVATION; GENE LOCUS; GERM LINE; HOMOZYGOSITY; HUMAN; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; SOMATIC MUTATION; VDJ RECOMBINATION; WILD TYPE;

ANIMALS; BINDING SITES, ANTIBODY; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CHROMOSOMES, ARTIFICIAL, YEAST; GENES, OVERLAPPING; GERM CELLS; HUMANS; IGG DEFICIENCY; IMMUNOGLOBULIN CONSTANT REGIONS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN KAPPA-CHAINS; IMMUNOGLOBULIN LAMBDA-CHAINS; MICE; MICE, TRANSGENIC; RATS; RATS, TRANSGENIC;

EID: 84873553070     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203041     Document Type: Article

References (56)

1. Chan, A. C., and P. J. Carter. 2010. Therapeutic antibodies for autoimmunity and inflammation. Nat. Rev. Immunol. 10: 301-316.
2. Enever, C., T. Batuwangala, C. Plummer, and A. Sepp. 2009. Next generation immunotherapeutics-honing the magic bullet. Curr. Opin. Biotechnol. 20: 405-411.
3. Corti, D., J. Voss, S. J. Gamblin, G. Codoni, A. Macagno, D. Jarrossay, S. G. Vachieri, D. Pinna, A. Minola, F. Vanzetta, et al. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333: 850-856.
4. Mouquet, H., F. Klein, J. F. Scheid, M. Warncke, J. Pietzsch, T. Y. Oliveira, K. Velinzon, M. S. Seaman, and M. C. Nussenzweig. 2011. Memory B cell antibodies to HIV-1 gp140 cloned from individuals infected with clade A and B viruses. PLoS ONE 6: e24078.
5. Becker, P. D., N. Legrand, C. M. van Geelen, M. Noerder, N. D. Huntington, A. Lim, E. Yasuda, S. A. Diehl, F. A. Scheeren, M. Ott, et al. 2010. Generation of human antigen-specific monoclonal IgM antibodies using vaccinated "human immune system" mice. PLoS ONE 5: e13137.
6. Riechmann, L., M. Clark, H. Waldmann, and G. Winter. 1988. Reshaping human antibodies for therapy. Nature 332: 323-327.
7. Brüggemann, M., and M. S. Neuberger. 1988. Novel antibodies by DNA manipulation. Prog. Allergy 45: 91-105.
8. Brüggemann, M., G. Winter, H. Waldmann, and M. S. Neuberger. 1989. The immunogenicity of chimeric antibodies. J. Exp. Med. 170: 2153-2157.
9. Brüggemann, M., J. A. Smith, M. J. Osborn, and X. Zou. 2007. Part I: Selecting and shaping the antibody molecule, selection strategies III: transgenic mice. In Handbook of Therapeutic Antibodies. S. Dübel, ed. Wiley-VCH Verlag, Weinheim, Germany. p. 69-93.
10. Green, L. L. 1999. Antibody engineering via genetic engineering of the mouse: XenoMouse strains are a vehicle for the facile generation of therapeutic human monoclonal antibodies. J. Immunol. Methods 231: 11-23.
11. Ishida, I., K. Tomizuka, H. Yoshida, T. Tahara, N. Takahashi, A. Ohguma, S. Tanaka, M. Umehashi, H. Maeda, C. Nozaki, et al. 2002. Production of human monoclonal and polyclonal antibodies in TransChromo animals. Cloning Stem Cells 4: 91-102.
12. Kuroiwa, Y., P. Kasinathan, Y. J. Choi, R. Naeem, K. Tomizuka, E. J. Sullivan, J. G. Knott, A. Duteau, R. A. Goldsby, B. A. Osborne, et al. 2002. Cloned transchromosomic calves producing human immunoglobulin. Nat. Biotechnol. 20: 889-894.
13. Lonberg, N. 2005. Human antibodies from transgenic animals. Nat. Biotechnol. 23: 1117-1125.
14. Lonberg, N. 2008. Fully human antibodies from transgenic mouse and phage display platforms. Curr. Opin. Immunol. 20: 450-459.
15. Brüggemann, M., H. M. Caskey, C. Teale, H. Waldmann, G. T. Williams, M. A. Surani, and M. S. Neuberger. 1989. A repertoire of monoclonal antibodies with human heavy chains from transgenic mice. Proc. Natl. Acad. Sci. USA 86: 6709-6713.
16. Lonberg, N., L. D. Taylor, F. A. Harding, M. Trounstine, K. M. Higgins, S. R. Schramm, C. C. Kuo, R. Mashayekh, K. Wymore, J. G. McCabe, et al. 1994. Antigen-specific human antibodies from mice comprising four distinct genetic modifications. Nature 368: 856-859.
17. Nicholson, I. C., X. Zou, A. V. Popov, G. P. Cook, E. M. Corps, S. Humphries, C. Ayling, B. Goyenechea, J. Xian, M. J. Taussig, et al. 1999. Antibody repertoires of four- and five-feature translocus mice carrying human immunoglobulin heavy chain and k and l light chain yeast artificial chromosomes. J. Immunol. 163: 6898-6906.
18. Kitamura, D., J. Roes, R. Kühn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin m chain gene. Nature 350: 423-426.
19. Pruzina, S., G. T. Williams, G. Kaneva, S. L. Davies, A. Martín-López, M. Brüggemann, S. M. Vieira, S. A. Jeffs, Q. J. Sattentau, and M. S. Neuberger. 2011. Human monoclonal antibodies to HIV-1 gp140 from mice bearing YACbased human immunoglobulin transloci. Protein Eng. Des. Sel. 24: 791-799.
20. Marchuk, D., and F. S. Collins. 1988. pYAC-RC, a yeast artificial chromosome vector for cloning DNA cut with infrequently cutting restriction endonucleases. Nucleic Acids Res. 16: 7743.
21. Kaur, R., B. Ma, and B. P. Cormack. 2007. A family of glycosylphosphatidylinositollinked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. USA 104: 7628-7633.
22. Nelson, D. L., and B. H. Brownstein. 1994. YAC Libraries: A User's Guide. Freeman and Company, New York.
23. Popov, A. V., C. Bützler, J. P. Frippiat, M. P. Lefranc, and M. Brüggemann. 1996. Assembly and extension of yeast artificial chromosomes to build up a large locus. Gene 177: 195-201.
24. Popov, A. V., X. Zou, J. Xian, I. C. Nicholson, and M. Brüggemann. 1999. A human immunoglobulin l locus is similarly well expressed in mice and humans. J. Exp. Med. 189: 1611-1620.
25. Gietz, D., and R. A. Woods. 1998. Transformation of yeast by the lithium acetate single-stranded carrier DNA/PEG method. Methods Microbiol. 26: 53-66.
26. Peterson, K. R. 2007. Preparation of intact yeast artificial chromosome DNA for transgenesis of mice. Nat. Protoc. 2: 3009-3015.
27. Beverley, S. M. 1988. Characterization of the "unusual" mobility of large circular DNAs in pulsed field-gradient electrophoresis. Nucleic Acids Res. 16: 925-939.
28. Kawasaki, K., S. Minoshima, E. Nakato, K. Shibuya, A. Shintani, S. Asakawa, T. Sasaki, H. G. Klobeck, G. Combriato, H. G. Zachau, and N. Shimizu. 2001. Evolutionary dynamics of the human immunoglobulin kappa locus and the germline repertoire of the Vk genes. Eur. J. Immunol. 31: 1017-1028.
29. Wagner, S. D., G. Gross, G. P. Cook, S. L. Davies, and M. S. Neuberger. 1996. Antibody expression from the core region of the human IgH locus reconstructed in transgenic mice using bacteriophage P1 clones. Genomics 35: 405-414.
30. Sambrook, J., and D. W. Russell. 2001. Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
31. Gu, H., D. Wilson, and J. Inselburg. 1992. Recovery of DNA from agarose gels using a modified Elutrap. J. Biochem. Biophys. Methods 24: 45-50.
32. Davies, N. P., A. V. Popov, X. Zou, and M. Brüggemann. 1996. Human antibody repertoires in transgenic mice: manipulation and transfer of YACs. In Antibody Engineering: A Practical Approach. J. McCafferty, H. R. Hoogenboom, and D. J. Chiswell, eds. IRL, Oxford, U.K., p. 59-76.
33. Yang, X. W., P. Model, and N. Heintz. 1997. Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat. Biotechnol. 15: 859-865.
34. Brüggemann, M., C. Teale, M. Clark, C. Bindon, and H. Waldmann. 1989. A matched set of rat/mouse chimeric antibodies. Identification and biological properties of rat H chain constant regions μ, γ1, γ2a, γ2b, γ2c, ε, and α. J. Immunol. 142: 3145-3150.
35. Ménoret, S., A. L. Iscache, L. Tesson, S. Rémy, C. Usal, M. J. Osborn, G. J. Cost, M. Brüggemann, R. Buelow, and I. Anegon. 2010. Characterization of immunoglobulin heavy chain knockout rats. Eur. J. Immunol. 40: 2932-2941.
36. Meisner, L. F., and J. A. Johnson. 2008. Protocols for cytogenetic studies of human embryonic stem cells. Methods 45: 133-141.
37. Kishiro, Y., M. Kagawa, I. Naito, and Y. Sado. 1995. A novel method of preparing rat-monoclonal antibody-producing hybridomas by using rat medial iliac lymph node cells. Cell Struct. Funct. 20: 151-156.
38. Davies, N. P., I. R. Rosewell, and M. Brüggemann. 1992. Targeted alterations in yeast artificial chromosomes for inter-species gene transfer. Nucleic Acids Res. 20: 2693-2698.
39. Davies, N. P., I. R. Rosewell, J. C. Richardson, G. P. Cook, M. S. Neuberger, B. H. Brownstein, M. L. Norris, and M. Brüggemann. 1993. Creation of mice expressing human antibody light chains by introduction of a yeast artificial chromosome containing the core region of the human immunoglobulin k locus. Biotechnology (N. Y.) 11: 911-914.
40. 3 interval exhibits B cell-specific enhancer function in early development. J. Immunol. 166: 3315-3323.
41. Choi, T. K., P. W. Hollenbach, B. E. Pearson, R. M. Ueda, G. N. Weddell, C. G. Kurahara, C. S. Woodhouse, R. M. Kay, and J. F. Loring. 1993. Transgenic mice containing a human heavy chain immunoglobulin gene fragment cloned in a yeast artificial chromosome. Nat. Genet. 4: 117-123.
42. Geurts, A. M., G. J. Cost, Y. Freyvert, B. Zeitler, J. C. Miller, V. M. Choi, S. S. Jenkins, A. Wood, X. Cui, X. Meng, et al. 2009. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325: 433.
43. Flisikowska, T., I. S. Thorey, S. Offner, F. Ros, V. Lifke, B. Zeitler, O. Rottmann, A. Vincent, L. Zhang, S. Jenkins, et al. 2011. Efficient immunoglobulin gene disruption and targeted replacement in rabbit using zinc finger nucleases. PLoS ONE 6: e21045.
44. Lefranc, M.-P., and G. Lefranc. 2001. The Immunoglobulin FactsBook. Academic Press, London, p. 45-68.
45. Reynaud, S., L. Delpy, L. Fleury, H. L. Dougier, C. Sirac, and M. Cogné. 2005. Interallelic class switch recombination contributes significantly to class switching in mouse B cells. J. Immunol. 174: 6176-6183.
46. Bazin, H., A. Beckers, and P. Querinjean. 1974. Three classes and four (sub) classes of rat immunoglobulins: IgM, IgA, IgE and IgG1, IgG2a, IgG2b, IgG2c. Eur. J. Immunol. 4: 44-48.
47. McGhee, J. R., S. M. Michalek, and V. K. Ghanta. 1975. Rat immunoglobulins in serum and secretions: purification of rat IgM, IgA and IgG and their quantitation in serum, colostrum, milk and saliva. Immunochemistry 12: 817-823.
48. Lu, H., M. Wang, J. C. Gunsolley, H. A. Schenkein, and J. G. Tew. 1994. Serum immunoglobulin G subclass concentrations in periodontally healthy and diseased individuals. Infect. Immun. 62: 1677-1682.
49. Nimmerjahn, F., and J. V. Ravetch. 2007. Fc-receptors as regulators of immunity. Adv. Immunol. 96: 179-204.
50. Rowland, S. L., K. Tuttle, R. M. Torres, and R. Pelanda. 2012. Antigen and cytokine receptor signals guide the development of the naïve mature B cell repertoire. Immunol. Res. In press.
51. Pinaud, E., A. A. Khamlichi, C. Le Morvan, M. Drouet, V. Nalesso, M. Le Bert, and M. Cogné. 2001. Localization of the 39 IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 15: 187-199.
52. Zhang, B., A. Alaie-Petrillo, M. Kon, F. Li, and L. A. Eckhardt. 2007. Transcription of a productively rearranged Ig VDJCa does not require the presence of HS4 in the IgH 39 regulatory region. J. Immunol. 178: 6297-6306.
53. Dariavach, P., G. T. Williams, K. Campbell, S. Pettersson, and M. S. Neuberger. 1991. The mouse IgH 39-enhancer. Eur. J. Immunol. 21: 1499-1504.
54. Brüggemann, M., C. Spicer, L. Buluwela, I. Rosewell, S. Barton, M. A. Surani, and T. H. Rabbitts. 1991. Human antibody production in transgenic mice: expression from 100 kb of the human IgH locus. Eur. J. Immunol. 21: 1323-1326.
55. Mendez, M. J., L. L. Green, J. R. Corvalan, X. C. Jia, C. E. Maynard-Currie, X. D. Yang, M. L. Gallo, D. M. Louie, D. V. Lee, K. L. Erickson, et al. 1997. Functional transplant of megabase human immunoglobulin loci recapitulates human antibody response in mice. Nat. Genet. 15: 146-156.
56. Bruggemann, M. 2004. Human monoclonal antibodies from translocus mice. In Molecular Biology of B Cells. T. Honjo and M. S. Neuberger, eds. Academic Press, New York, p. 547-561.