A mutant human IgG molecule with only one C1q binding site can activate complement and induce lysis of target cells

European Journal of Immunology

Volumn 36, Issue 1, 2006, Pages 129-138

  Michaelsen, Terje E ^a,b   Thommesen, John E ^b   Ihle, Oistein ^a   Gregers, Tone F ^b,c   Sandin, Randi H ^a   Brekke, Ole Henrik ^b,d   Sandlie, Inger ^b  

^a NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d Invitrogen Dynal Bead Based Separations   (Norway)

Author keywords

Antibodies; Complement system; Cytotoxicity

Indexed keywords

COMPLEMENT COMPONENT C1Q; FC RECEPTOR; HYBRID PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G3; MUTANT PROTEIN; PEPTIDE;

AFFINITY CHROMATOGRAPHY; ARTICLE; BINDING SITE; COMPLEMENT ACTIVATION; CYTOLYSIS; GENE MUTATION; HEAVY CHAIN; IMMUNOGLOBULIN STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ISOLATION;

BINDING SITES, ANTIBODY; CHROMATOGRAPHY, AFFINITY; COMPLEMENT ACTIVATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOBLOTTING; IMMUNOGLOBULIN G; MEMBRANE GLYCOPROTEINS; MUTATION; POLYMERASE CHAIN REACTION; RECEPTORS, COMPLEMENT; TRANSFECTION;

EID: 30944443974     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200535178     Document Type: Article

References (47)

1. Burton, D. R., Boyd, J., Brampton, A. D., Easterbrook-Smith, S. B., Emanuel, E. J., Novotny, J., Rademacher, T. W. et al., The C1q receptor site on immunoglobulin G. Nature 1980. 288: 338-344.
2. Colomb, M. and Porter, R. R., Characterization of a plasmin-digest fragment of rabbit immunoglobulin gamma that binds antigen and complement. Biochem. J. 1975. 145: 177-183.
3. Connell, G. E. and Porter, R. R., A new enzymic fragment (Facb) of rabbit immunoglobulin G. Biochem. J. 1971. 124: 53P.
4. Painter, R. H., Foster, D. B., Gardner, B. and Hughes-Jones, N. C., Functional affinity constants of subfragments of immunoglobulin G for C1q. Mol. Immunol. 1982. 19: 127-131.
5. Tao, M. H., Canfield, S. M. and Morrison, S. L., The differential ability of human IgG1 and IgG4 to activate complement is determined by the COOH-terminal sequence of the CH2 domain. J. Exp. Med. 1991. 173: 1025-1028.
6. Yasmeen, D., Ellerson, J. R., Dorrington, K. J. and Painter, R. H., The structure and function of immunoglobulin domains. IV. The distribution of some effector functions among the Cgamma2 and Cgamma3 homology regions of human immunoglobulin G1. J. Immunol. 1976. 116: 518-526.
7. Idusogie, E. E., Presta, L. G., Gazzano-Santoro, H., Totpal, K., Wong, P. Y., Ultsch, M., Meng, Y. G. et al., Mapping of the C1q binding site on rituxan, a chimeric antibody with a human IgG1 Fc. J. Immunol. 2000. 164: 4178-4184.
8. Thommesen, J. E., Michaelsen, T. E., Loset, G. A., Sandlie, I. and Brekke, O. H., Lysine 322 in the human IgG3 C(H)2 domain is crucial for antibody dependent complement activation. Mol. Immunol. 2000. 37: 995-1004.
9. Canfield, S. M. and Morrison, S. L., The binding affinity of human IgG for its high affinity Fc receptor is determined by multiple amino acids in the CH2 domain and is modulated by the hinge region. J. Exp. Med. 1991. 173: 1483-1491.
10. Chappel, M. S., Isenman, D. E., Everett, M., Xu, Y. Y., Dorrington, K. J. and Klein, M. H., Identification of the Fc gamma receptor class I binding site in human IgG through the use of recombinant IgG1/IgG2 hybrid and point-mutated antibodies. Proc. Natl. Acad. Sci. USA 1991. 88: 9036-9040.
11. Duncan, A. R., Woof, J. M., Partridge, L. J., Burton, D. R. and Winter, G., Localization of the binding site for the human high-affinity Fc receptor on IgG. Nature 1988. 332: 563-564.
12. Lund, J., Winter, G., Jones, P. T., Pound, J. D., Tanaka, T., Walker, M. R., Artymiuk, P. J. et al., Human Fc gamma RI and Fc gamma RII interact with distinct but overlapping sites on human IgG. J. Immunol. 1991. 147: 2657-2662.
13. Radaev, S., Motyka, S., Fridman, W. H., Sautes-Fridman, C. and Sun, P. D., The structure of a human type III Fcgamma receptor in complex with Fc. J. Biol. Chem. 2001. 276: 16469-16477.
14. Kishore, U. and Reid, K. B., C1q: structure, function, and receptors. Immunopharmacology 2000. 49: 159-170.
15. Kishore, U., Ghai, R., Greenhough, T. J., Shrive, A. K., Bonifati, D. M., Gadjeva, M. G., Waters, P. et al., Structural and functional anatomy of the globular domain of complement protein C1q. Immunol. Lett. 2004. 95: 113-128.
16. Gaboriaud, C., Juanhuix, J., Gruez, A., Lacroix, M., Darnault, C., Pignol, D., Verger, D. et al., The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J. Biol. Chem. 2003. 278: 46974-46982.
17. Gaboriaud, C., Thielens, N. M., Gregory, L. A., Rossi, V., Fontecilla-Camps, J. C. and Arlaud, G. J., Structure and activation of the C1 complex of complement: unraveling the puzzle. Trends Immunol. 2004. 25: 368-373.
18. Clark, M., Bindon, C., Dyer, M., Friend, P., Hale, G., Cobbold, S., Caine, R. et al., The improved lyric function and in vivo efficacy of monovalent monoclonal CD3 antibodies. Eur. J. Immunol. 1989. 19: 381-388.
19. Udaka, K., Okada, M. and Utsumi, S., Co-operation between the pair of C gamma 2 domains in C1q-binding by rabbit IgG. Mol. Immunol. 1986. 23: 1103-1110.
20. Utsumi, S., Okada, M., Udaka, K. and Amano, T., Preparation and biologic characterization of fragments containing dimeric and monomeric C gamma 2 domain of rabbit IgG. Mol. Immunol. 1985. 22: 811-819.
21. Brekke, O. H., Bremnes, B., Sandin, R., Aase, A., Michaelsen, T. E. and Sandlie, I., Human IgG3 can adopt the disulfide bond pattern characteristic for IgG1 without resembling it in complement mediated cell lysis. Mol. Immunol. 1993. 30: 1419-1425.
22. Carney, W. P., Petit, D., Hamer, P., Der, C. J., Finkel, T., Cooper, G. M., Lefebvre, M. et al., Monoclonal antibody specific for an activated RAS protein. Proc. Natl. Acad. Sci. USA 1986. 83: 7485-7489.
23. Duhamel, R. C., Schur, P. H., Brendel, K. and Meezan, E., pH gradient elution of human IgG1, IgG2 and IgG4 from protein A-sepharose. J. Immunol. Methods 1979. 31: 211-217.
24. Koolwijk, P., Spierenburg, G. T., Frasa, H., Boot, J. H., van de Winkel, J. G. and Bast, B. J., Interaction between hybrid mouse monoclonal antibodies and the human high-affinity IgG FcR, huFc gamma RI, on U937. Involvement of only one of the mIgG heavy chains in receptor binding. J. Immunol. 1989. 143: 1656-1662.
25. Duncan, A. R. and Winter, G., The binding site for C1q on IgG. Nature 1988. 332: 738-740.
26. Morgan, A., Jones, N. D., Nesbitt, A. M., Chaplin, L., Bodmer, M. W. and Emtage, J. S., The N-terminal end of the CH2 domain of chimeric human IgG1 anti-HLA-DR is necessary for C1q, Fc gamma RI and Fc gamma RIII binding. Immunology 1995. 86: 319-324.
27. Brekke, O. H., Michaelsen, T. E. and Sandlie, I., The structural requirements for complement activation by IgG: does it hinge on the hinge? Immunol. Today 1995. 16: 85-90.
28. Brekke, O. H., Michaelsen, T. E., Sandin, R. and Sandlie, I., Activation of complement by an IgG molecule without a genetic hinge. Nature 1996. 383: 103.
29. Isenman, D. E., Dorrington, R. J. and Painter, R. H., The structure and function of immunoglobulin domains. II. The importance of interchain disulfide bonds and the possible role of molecular flexibility in the interaction between immunoglobulin G and complement. J. Immunol. 1975. 114: 1726-1729.
30. Michaelsen, T. E., Brekke, O. H., Aase, A., Sandin, R. H., Bremnes, B. and Sandlie, I., One disulfide bond in front of the second heavy chain constant region is necessary and sufficient for effector functions of human IgG3 without a genetic hinge. Proc. Natl. Acad. Sci. USA 1994. 91: 9243-9247.
31. Aase, A. and Michaelsen, T. E., The use of a hapten-Fab conjugate to sensitize target cells for antibody-dependent complement-mediated lysis and antibody-dependent cell-mediated cytotoxicity. J. Immunol. Methods 1991. 136: 185-191.
32. Lucisano Valim, Y. M. and Lachmann, P. J., The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: a systematic study using chimaeric anti-NIP antibodies with human Fc regions. Clin. Exp. Immunol. 1991. 84: 1-8.
33. Michaelsen, T. E., Garred, P. and Aase, A., Human IgG subclass pattern of inducing complement-mediated cytolysis depends on antigen concentration and to a lesser extent on epitope patchiness, antibody affinity and complement concentration. Eur. J. Immunol. 1991. 21: 11-16.
34. Koolwijk, P., Boot, J. H., Griep, R. and Bast, B. J., Binding of the human complement subcomponent C1q to hybrid mouse monoclonal antibodies. Mol. Immunol. 1991. 28: 567-576.
35. Yamawaki-Kataoka, Y., Miyata, T. and Honjo, T., The complete nucleotide sequence of mouse immunoglobin gamma 2a gene and evolution of heavy chain genes: further evidence for intervening sequence-mediated domain transfer. Nucleic Acids Res. 1981. 9: 1365-1381.
36. Saphire, E. O., Patten, P. W., Pantophlet, R., Zwick, M. B., Morris, G. M., Rudd, P. M., Dwek, R. A. et al., Crystal structure of a neutralizing human IGG against HIV-1: a template for vaccine design. Science 2001. 293: 1155-1159.
37. Harris, L. J., Skaletsky, E. and McPherson, A., Crystallographic structure of an intact IgG1 monoclonal antibody. J. Mol. Biol. 1998. 275: 861-872.
38. Harris, L. J., Larson, S. B., Hasel, R. W. and McPherson, A., Refined structure of an intact IgG2a monoclonal antibody. Biochemistry 1997. 36: 1581-1597.
39. Saphire, E. O., Stanfield, R. L., Crispin, M. D., Parren, P. W., Rudd, P. M., Dwek, R. A., Burton, D. R. et al., Contrasting IgG structures reveal extreme asymmetry and flexibility. J. Mol. Biol. 2002. 319: 9-18.
40. Barbacid, M., ras genes. Annu. Rev. Biochem. 1987. 56: 779-827.
41. Kunkel, T. A., Roberts, J. D. and Zakour, R. A., Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987. 154: 367-382.
42. Rasmussen, I. B., Lunde, E., Michaelsen, T. E., Bogen, B. and Sandlie, I., The principle of delivery of T cell epitopes to antigen-presenting cells applied to peptides from influenza virus, ovalbumin, and hen egg lysozyme: implications for peptide vaccination. Proc. Natl. Acad. Sci. USA 2001. 98: 10296-10301.
43. Norderhaug, L., Olafsen, T., Michaelsen, T. E. and Sandlie, I., Versatile vectors for transient and stable expression of recombinant antibody molecules in mammalian cells. J. Immunol. Methods 1997. 204: 77-87.
44. Michaelsen, T. E., Aase, A., Westby, C. and Sandlie, I., Enhancement of complement activation and cytolysis of human IgG3 by deletion of hinge exons. Scand. J. Immunol. 1990. 32: 517-528.
45. Michaelsen, T. E., Ihle, O., Beckstrom, K. J., Herstad, T. K., Kolberg, J., Hoiby, E. A. and Aase, A., Construction and functional activities of chimeric mouse-human immunoglobulin G and immunoglobulin M antibodies against the Neisseria meningitidis PorA P1.7 and P1.16 epitopes. Infect. Immun. 2003. 71: 5714-5723.
46. Michaelsen, T. E., Aase, A., Norderhaug, L. and Sandlie, I., Antibody dependent cell-mediated cytotoxicity induced by chimeric mouse-human IgG subclasses and IgG3 antibodies with altered hinge region. Mol. Immunol. 1992. 29: 319-326.
47. Sandlie, I., Aase, A., Westby, C. and Michaelsen, T. E., C1q binding to chimeric monoclonal IgG3 antibodies consisting of mouse variable regions and human constant regions with shortened hinge containing 15 to 47 amino acids. Eur. J. Immunol. 1989. 19: 1599-1603.