Insights into IgA-mediated immune responses from the crystal structures of human FcαRI and its complex with IgA1-Fc

Nature

Volumn 423, Issue 6940, 2003, Pages 614-620

  Herr, Andrew B ^a   Ballister, Edward R ^a,b,c   Bjorkman, Pamela J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b La Salle High School   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; CARBOHYDRATES; CRYSTAL STRUCTURE;

PHAGOCYTOSIS;

IMMUNOLOGY;

CARBOHYDRATE; FC RECEPTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTEGRIN RECEPTOR;

MEDICINE;

ANTIGEN BINDING; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; DISULFIDE BOND; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; PHAGOCYTOSIS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANTIGENS, CD; CRYSTALLOGRAPHY, X-RAY; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN FRAGMENTS; IMMUNOGLOBULIN G; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, FC; SIGNAL TRANSDUCTION;

EID: 0037497304     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature01685     Document Type: Article

References (50)

1. Monteiro, R. C. & Van De Winkel, J. G. IgA Fc receptors. Annu. Rev. Immunol. 21, 177-204 (2003).
2. Brandtzaeg, P. et al. Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunol. Today 20, 141-151 (1999).
3. Norderhaug, I. N., Johansen, F. E., Schjerven, H. & Brandtzaeg, P. Regulation of the formation and external transport of secretory immunoglobulins. Crit. Rev. Immunol. 19, 481-508 (1999).
4. Monteiro, R. C., Kubagawa, H. & Cooper, M. D. Cellular distribution, regulation, and biochemical nature of ah Fcα receptor in humans. J. Exp. Med. 171, 597-613 (1990).
5. Vidarsson, G. et al. Activity of human IgG and IgA subclasses in immune defense against Neisseria meningitidis serogroup B. J. Immunol. 166, 6250-6256 (2001).
6. van Egmond, M. et al. FcQRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nature Med. 6, 680-685 (2000).
7. van Spriel, A. B. et al. Mac-1 (CD11b/CDI8) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood 97, 2478-2486 (2001).
8. Motegi, Y. & Kita, H. Interaction with secretory component stimulates effector functions of human eosinophils but not of neutrophils. J. Immunol 161, 4340-4346 (1998).
9. Wende, H., Colonna, M., Ziegler, A. & Volz, A. Organization of the leukocyte receptor cluster (LRC) on human chromosome 19q13.4. Mamm. Genome 10, 154-160 (1999).
10. Garman, S. C., Wurzburg, B. A., Tarchevskaya, S. S., Kinet, J. P. & Jardetzky, T. S. Structure of the Fc fragment of human IgE bound to its high-affinity receptor FcεRIα. Nature 406, 259-266 (2000).
11. Sondermann, P., Huber, R., Oosthuizen, V. & Jacob, U. The 3.2-Å crystal structure of the human IgGI Fc fragment-FcγRIII complex. Nature 406, 267-273 (2000).
12. Herr, A. B., White, C. L., Milburn, C., Wu, C. & Bjorkman, P. J. Bivalent binding of IgA1 to FcαRI suggests a mechanism for cytokine activation of IgA phagocytosis. J. Mol. Biol. 327, 645-657 (2003).
13. Pleass, R. J., Dunlop, J. I., Anderson, C. M. & Woof, J. M. Identification of residues in the CH2/CH3 domain interface of IgA essential for interaction with the human Fcα receptor (FcαR) CD89. J. Biol. Chem. 274, 23508-23514 (1999).
14. Carayannopoulos, L., Hexham, J. M. & Capra, J. D. Localization of the binding site for the monocyte immunoglobulin (Ig) A-Fc receptor (CD89) to the domain boundary between Cα2 and Cα3 in human IgA1. J. Exp. Med. 183, 1579-1586 (1996).
15. Martin, W. L., West, A. P. Jr, Gan, L. & Bjorkman, P. J. Crystal structure at 2.8 Å of an FcRn/ heterodimeric Fc complex: mechanism of pH-dependent binding. Mol. Cell 7, 867-877 (2001).
16. Chapman, T. L., Heikema, A. P., West, A. P. & Bjorkman, P. J. Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity 13, 727-736 (2000).
17. Garman, S. C., Kinet, J. P. & Jardetzky, T. S. Crystal structure of the human high-affinity IgE receptor. Cell 95, 951-961 (1998).
18. Maxwell, K. F. et al. Crystal structure of the human leukocyte Fc receptor, FcγyRIIa. Nature Struct. Biol. 6, 437-442 (1999).
19. Sondermann, P., Huber, R. & Jacob, U. Crystal structure of the soluble form of the human Fcγreceptor IIb: a new member of the immunoglobulin superfamily at 1.7 Å resolution. EMBO J. 18, 1095-1103 (1999).
20. Fan, Q. R. et al. Structure of the inhibitory receptor for human natural killer cells resembles haematopoietic receptors. Nature 389, 96-100 (1997).
21. Huber, R., Deisenhofer, J., Colman, P. M., Matsushima, M. & Palm, W. Crystallographic structure studies of an IgG molecule and an Fc fragment. Nature 264, 415-420 (1976).
22. Wan, T. et al. The crystal structure of IgE Fc reveals an asymmetrically bent conformation. Nature Immunol. 3, 681-686 (2002).
23. Wurzburg, B. A., Garman, S. C. & Jardetzky, T. S. Structure of the human IgE-Fc Cε3-Cε4 reveals conformational flexibility in the antibody effector domains. Immunity 13, 375-385 (2000).
24. Putnam, F. W., Liu, Y. S. & Low, T. L. Primary structure of a human IgA1 immunoglobulin. IV. Streptococcal IgA1 protease, digestion, Fab and Fc fragments, and the complete amino acid sequence of the α1 heavy chain. J. Biol. Chem. 254, 2865-2874 (1979).
25. Yang, C., Kratzin, H., Gotz, H. & Hilschmann, N. Rule of antibody structure. Primary structure of a human monoclonal IgA-immunoglobulin (myeloma protein Tro). VII. Purification and characterization of the disulfide bridges. Hoppe-Seyler's Z. Physiol. Chem. 360, 1919-1940 (1979).
26. Morton, H. C. et al. Immunoglobulin-binding sites of human FcαRI (CD89) and bovine Fcγ2R are located in their membrane-distal extracellular domains. J. Exp. Med. 189, 1715-1722 (1999).
27. Wines, B. D. et al. Identification of residues in the first domain of human Fcα receptor essential for interaction with IgA. J. Immunol. 162, 2146-2153 (1999).
28. Wines, B. D., Sardjono, C. T., Trist, H. M., Lay, C. S. & Hogarth, P. M. The interaction of FcαRI with IgA and its implications for ligand binding by immunoreceptors of the leukocyte receptor cluster. J. Immunol. 166, 1781-1789 (2001).
29. Garman, S. C., Sechi, S., Kinet, J. P. & Jardetzky, T. S. The analysis of the human high affinity IgE receptor FcεRIα from multiple crystal forms. J. Mol. Biol. 311, 1049-1062 (2001).
30. Deisenhofer, J. Crystallographic refinement and atomic models ofa human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-Å resolution. Biochemistry 20, 2361-2370 (1981).
31. Sauer-Eriksson, A. E., Kleywegt, G. J., Uhlen, M. & Jones, T. A. Crystal structure of the C2 fragment of streptococcal protein G in complex with the Fc domain of human IgG. Structure 3, 265-278 (1995).
32. Corper, A. L. et al. Structure of human IgM rheumatoid factor Fab bound to its autoantigen IgG Fc reveals a novel topology of antibody-antigen interaction. Nature Struct. Biol. 4, 374-381 (1997).
33. DeLano, W. L., Ultsch, M. H., de Vos, A. M. & Wells, J. A. Convergent solutions to binding at a protein-protein interface. Science 287, 1279-1283 (2000).
34. Saphire, E. O. et al. Contrasting IgG structures reveal extreme asymmetry and flexibility. J. Mol. Biol. 319, 9-18 (2002).
35. Shogren, R., Gerken, T. A. & Jentoft, N. Role of glycosylation on the conformation and chain dimensions of O-linked glycoproteins: light-scattering studies of ovine submaxillary mucin. Biochemistry 28, 5525-5536 (1989).
36. Iikura, M. et al. Secretory IgA induces degranulation of IL-3-primed basophils. J. Immunol. 161, 1510-1515 (1998).
37. Hexham, J. M. et al. A human immunoglobulin (Ig)A Cα3 domain motif directs polymeric Ig receptor-mediated secretion. J. Exp. Med. 189, 747-752 (1999).
38. White, K. D. & Capra, J. D. Targeting mucosal sites by polymeric immunoglobulin receptor-directed peptides. J. Exp. Med. 196, 551-555 (2002).
39. Bracke, M., Lammers, J. W., Coffer, P. J. & Koenderman, L. Cytokine-induced inside-out activation of FcαR (CD89) is mediated by a single serine residue (S263) in the intracellular domain of the receptor. Blood 97, 3478-3483 (2001).
40. Weisbart, R. H., Kacena, A., Schuh, A. & Golde, D. W. GM-CSF induces human neutrophil IgA-mediated phagocytosis by an IgA Fc receptor activation mechanism. Nature 332, 647-648 (1988).
41. Otwinowski, Z. & Minor, W. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
42. Terwilliger, T. C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D 55, 849-861 (1999).
43. De La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494 (1997).
44. Collaborative Computational Project No. 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
45. Brunger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
46. Navaza, J. AMoRe: an automated package for molecular replacement. Acta Crystallogr. A 50, 157-163 (1994).
47. McDonald, I. K. & Thornton, J. M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793 (1994).
48. Su, X. D. et al. Crystal structure of hemolin: a horseshoe shape with implications for homophilic adhesion. Science 281, 991-995 (1998).
49. Kraulis, P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950 (1991).
50. Merritt, E. A. & Murphy, M. E. P. Raster3D Version 2.0, a program for photorealistic molecular graphics. Acta Crystallogr. D 50, 869-873 (1994).