Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: Potential application in humorally mediated autoimmune disease

International Immunology

Volumn 18, Issue 12, 2006, Pages 1759-1769

  Petkova, Stefka B ^a   Akilesh, Shreeram ^a,c   Sproule, Thomas J ^a   Christianson, Gregory J ^a   Al Khabbaz, Hana ^a   Brown, Aaron C ^a   Presta, Leonard G ^b,d   Meng, Y Gloria ^b   Roopenian, Derry C ^a  

^a JACKSON LABORATORY   (United States)

^b GENENTECH INC   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; FC RECEPTOR; FCRN RECEPTOR; IMMUNOGLOBULIN G1 MONOCLONAL ANTIBODY 4D5; MONOCLONAL ANTIBODY; TRASTUZUMAB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY ENGINEERING; ARTHRITIS; ARTICLE; AUTOIMMUNE DISEASE; BINDING AFFINITY; CONTROLLED STUDY; DRUG RECEPTOR BINDING; FEMALE; HUMORAL IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MUTANT; NONHUMAN; PLASMA HALF LIFE; PRIORITY JOURNAL; TRANSGENE; WILD TYPE;

ANIMALS; ANTIBODIES; ARTHRITIS; AUTOIMMUNE DISEASES; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; GENETIC ENGINEERING; HALF-LIFE; HUMANS; IMMUNOGLOBULIN G; MICE; RECEPTORS, FC; TREATMENT OUTCOME;

EID: 33845364560     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxl110     Document Type: Article

References (58)

1. Spiegelberg, H. L. and Weigle, W. O. 1965. Studies on the catabolism of gamma-G subunits and chains. J. Immunol. 95:1034.
2. Spiegelberg, H. L. and Fishkin, B. G. 1972. The catabolism of human G immunoglobulins of different heavy chain subclasses. 3. The catabolism of heavy chain disease proteins and of Fc fragments of myeloma proteins. Clin. Exp. Immunol. 10:599.
3. Spiegelberg, H. L. 1989. Biological role of different antibody classes. Int. Arch. Allergy Appl. Immunol. 90:(Suppl. 1)22.
4. Morell, A., Terry, W. D. and Waldmann, T. A. 1970. Metabolic properties of IgG subclasses in man. J. Clin. Invest. 49:673.
5. Spiegelberg, H. L. and Grey, H. M. 1968. Catabolism of human gamma-G immunoglobulins of different heavy chain subclasses. II. Catabolism of gamma-G myeloma proteins in heterologous species. J. Immunol. 101:711.
6. Fahey, J. L. and Robinson, A. G. 1963. Factors controlling serum gamma-globulin concentration. J. Exp. Med. 118:845.
7. Brambell, F. W., Hemmings, W. A. and Morris, I. G. 1964. A theoretical model of gamma-globulin catabolism. Nature 203:1352.
8. Brambell, F. W. 1966. The transmission of immunity from mother to young and the catabolism of immunoglobulins. Lancet 2:1087.
9. Raghavan,M. and Bjorkman, P. J. 1996. Fc receptors and their interactions with immunoglobulins. Annu. Rev. Cell Dev. Biol. 12:181.
10. Simister, N. E. and Mostov, K. E. 1989. An Fc receptor structurally related to MHC class I antigens. Nature 337:184.
11. Roopenian, D. C., Christianson, G. J., Sproule, T. J. et al. 2003. The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J. Immunol. 170:3528.
12. Israel, E. J., Wilsker, D. F., Hayes, K. C., Schoenfeld, D. and Simister, N. E. 1996. Increased clearance of IgG in mice that lack beta 2-microglobulin: Possible protective role of FcRn. Immunology 89:573.
13. Junghans, R. P. 1997. Finally! the Brambell receptor (FcRB). Mediator of transmission of immunity and protection from catabolism for IgG. Immunol. Res. 16:29.
14. Ghetie, V., Popov, S., Borvak, J. et al. 1997. Increasing the serum persistence of an IgG fragment by random mutagenesis. Nat. Biotechnol. 15:637.
15. Kim, J. K., Tsen, M. F., Ghetie, V. and Ward, E. S. 1994. Identifying amino acid residues that influence plasma clearance of murine IgG1 fragments by site-directed mutagenesis. Eur. J. Immunol. 24:542.
16. Popov, S., Hubbard, J. G., Kim, J., Ober, B., Ghetie, V. and Ward, E. S. 1996. The stoichiometry and affinity of the interaction of murine Fc fragments with the MHC class I-related receptor, FcRn. Mol. Immunol. 33:521.
17. Junghans, R. P. and Anderson, C. L. 1996. The protection receptor for IgG catabolism is the beta2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl Acad. Sci. USA 93:5512.
18. Ghetie, V., Hubbard, J. G., Kim, J. K., Tsen, M. F., Lee, Y. and Ward, E. S. 1996. Abnormally short serum half-lives of IgG in beta 2-microglobulin-deficient mice. Eur. J. Immunol. 26:690.
19. Roberts, D. M., Guenthert, M. and Rodewald, R. 1990. Isolation and characterization of the Fc receptor from the fetal yolk sac of the rat. J. Cell Biol. 111:1867.
20. Ober, R. J., Martinez, C., Vaccaro, C., Zhou, J. and Ward, E. S. 2004. Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn. J. Immunol. 172:2021.
21. Raghavan, M., Chen, M. Y., Gastinel, L. N. and Bjorkman, P. J. 1994. Investigation of the interaction between the class I MHC-related Fc receptor and its immunoglobulin G ligand. Immunity 1:303.
22. Kim, J. K., Tsen, M. F., Ghetie, V. and Ward, E. S. 1994. Localization of the site of the murine IgG1 molecule that is involved in binding to the murine intestinal Fc receptor. Eur. J. Immunol. 24:2429.
23. Martin, W. L., West, A. P. Jr, Gan, L. and Bjorkman, P. J. 2001. Crystal structure at 2.8 A of an FcRn/heterodimeric Fc complex: Mechanism of pH-dependent binding. Mol. Cell. 7:867.
24. Ghetie, V. and Ward, E. S. 1997. FcRn: The MHC class I-related receptor that is more than an IgG transporter. Immunol. Today 18:592.
25. Waldmann, T. A. and Jones, E. A. 1972. The role of cell-surface receptors in the transport and catabolism of immunoglobulins. CIBA Found. Symp. 9:5.
26. Simister, N. E. and Ahouse, J. C. 1996. The structure and evolution of FcRn. Res. Immunol. 147:333.
27. Simister, N. E., Jacobowitz Israel, E., Ahouse, J. C. and Story, C. M. 1997. New functions of the MHC class I-related Fc receptor, FcRn. Biochem. Soc. Trans. 25:481.
28. Ghetie, V. and Ward, E. S. 2000. Multiple roles for the major histocompatibility complex class I-related receptor FcRn. Annu. Rev. Immunol. 18:739.
29. Ober, R. J., Martinez, C., Lai, X., Zhou, J. and Ward, E. S. 2004. Exocytosis of IgG as mediated by the receptor, FcRn: An analysis at the single-molecule level. Proc. Natl Acad. Sci. USA 101:11076.
30. Waldmann, T. A. and Strober, W. 1969. Metabolism of immunoglobulins. Prog. Allergy 13:1.
31. Akilesh, S., Petkova, S., Sproule, T. J., Shaffer, D. J., Christianson, G. J. and Roopenian, D. 2004. The MHC class I-like Fc receptor promotes humorally mediated autoimmune disease. J. Clin. Invest. 113:1328. V
32. Liu, Z., Roopenian, D. C., Zhou, X. et al. 1997. Beta2-microglobulin- deficient mice are resistant to bullous pemphigoid. J. Exp. Med. 186:777.
33. Presta, L. G., Shields, R. L., Namenuk, A. K., Hong, K. and Meng, Y. G. 2002. Engineering therapeutic antibodies for improved function. Biochem. Soc. Trans. 30:487.
34. Medesan, C., Matesoi, D., Radu, C., Ghetie, V. and Ward, E. S. 1997. Delineation of the amino acid residues involved in transcytosis and catabolism of mouse IgG1. J. Immunol. 158:2211.
35. Ober, R. J., Radu, C. G., Ghetie, V. and Ward, E. S. 2001. Differences in promiscuity for antibody-FcRn interactions across species: implications for therapeutic antibodies. Int. Immunol. 13:1551.
36. Hinton, P. R., Johlfs, M. G., Xiong, J. M. et al. 2004. Engineered human IgG antibodies with longer serum half-lives in primates. J. Biol. Chem. 279:6213.
37. Shields, R. L., Namenuk, A. K., Hong, K. et al. 2001. 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. 276:6591.
38. Dall'Acqua, W. F., Woods, R. M., Ward, E. S. et al. 2002. Increasing the affinity of a human IgG1 for the neonatal Fc receptor: Biological consequences. J. Immunol. 169:5171.
39. Vaccaro, C., Zhou, J., Ober, R. J. and Ward, E. S. 2005. Engineering the Fc region of immunoglobulin G to modulate in vivo antibody levels. Nat. Biotechnol. 23:1283.
40. Hinton, P. R., Xiong, J. M., Johlfs, M. G., Tang, M. T., Keller, S. and Tsurushita, N. 2006. An engineered human IgG1 antibody with longer serum half-life. J. Immunol. 176:346.
41. Zhou, J., Mateos, F., Ober, R. J. and Sally Ward, E. 2005. Conferring the binding properties of the mouse MHC class I-related receptor, FcRn, onto the human ortholog by sequential rounds of site-directed mutagenesis. J. Mol. Biol. 345:1071.
42. Carter, P., Presta, L., Gorman, C. M. et al. 1992. Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc. Natl Acad. Sci. USA 89:4285.
43. Kabat, E. A. 1988. Antibody complementarity and antibody structure. J. Immunol. 141:S25.
44. Foote, J. and Winter, G. 1992. Antibody framework residues affecting the conformation of the hypervariable loops. J. Mol. Biol. 224:487.
45. Chaudhury, C., Mehnaz, S., Robinson, J. M. et al. 2003. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J. Exp. Med. 197:315.
46. Takai, T., Ono, M., Hikida, M., Ohmori, H. and Ravetch, J. V. 1996. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 379:346.
47. Petkova, S. B., Konstantinov, K. N., Sproule, S. J., Lyons, B. L., Al Awwami, M. and Roopenian, D. C. 2006. Human antibodies induce arthritis in mice deficient in the low-affinity inhibitory IgG receptor FcgRIIB. J. Exp. Med. 203:275.
48. Firan, M., Bawdon, R., Radu, C. et al. 2001. The MHC class I-related receptor, FcRn, plays an essential role in the maternofetal transfer of gamma-globulin in humans. Int. Immunol. 13:993.
49. Gurbaxani, B., Dela Cruz, L. L., Chintalacharuvu, K. and Morrison, S. L. 2006. Analysis of a family of antibodies with different halflives in mice fails to find a correlation between affinity for FcRn and serum half-life. Mol. Immunol. 43:1462.
50. Christianson, G. J., Blankenburg, R. L., Duffy, T. M. et al. 1996. Beta2-microglobulin dependence of the lupus-like autoimmune syndrome of MRL-Ipr mice. J. Immunol. 156:4932.
51. Christianson, G. J., Brooks, W., Vekasi, S. et al. 1997. Beta 2- microglobulin-deficient mice are protected from hypergammaglobulinemia and have defective antibody responses because of increased IgG catabolism. J. Immunol. 159:4781.
52. Jin, F. and Balthasar, J. P. 2005. Mechanisms of intravenous immunoglobulin action in immune thrombocytopenic purpura. Hum. Immunol. 66:403.
53. Ning, L., Zhao, M., Hilario-Vargas, J. et al. 2005. Complete FcRn dependence for IVIG therapy in autoimmune skin blistering diseases. J. Clin. Invest. 203:647.
54. Simister, N. E. and Story, C. M. 1997. Human placental Fc receptors and the transmission of antibodies from mother to fetus. J. Reprod. Immunol. 37:1.
55. Story, C. M., Mikulska, J. E. and Simister, N. E. 1994. A major histocompatibility complex class I-like Fc receptor cloned from human placenta: Possible role in transfer of immunoglobulin G from mother to fetus. J. Exp. Med. 180:2377.
56. Simister, N. E. 2003. Placental transport of immunoglobulin G. Vaccine 21:3365.
57. Bitonti, A. J., Dumont, J. A., Low, S. C. et al. 2004. Pulmonary delivery of an erythropoietin Fc fusion protein in non-human primates through an immunoglobulin transport pathway. Proc. Natl Acad. Sci. USA 101:9763.
58. Yoshida, M., Claypool, S. M., Wagner, J. S. et al. 2004. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20:769.