The solution structure of rabbit igg accounts for its interactions with the Fc receptor and complement C1q and its conformational stability

Journal of Molecular Biology

Volumn 425, Issue 3, 2013, Pages 506-523

  Rayner, Lucy E ^a   Kadkhodayi Kholghi, Nilufar ^a   Heenan, Richard K ^b   Gor, Jayesh ^a   Dalby, Paul A ^a   Perkins, Stephen J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b RUTHERFORD APPLETON LABORATORY   (United Kingdom)

Author keywords

analytical ultracentrifugation; constrained modeling; Keywords; neutron scattering; rabbit IgG; X ray scattering

Indexed keywords

COMPLEMENT COMPONENT C1Q; FC RECEPTOR; IMMUNOGLOBULIN G;

ARTICLE; DIMERIZATION; IMMUNOGLOBULIN STRUCTURE; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RABBIT; RADIATION SCATTERING; SEDIMENTATION RATE; ULTRACENTRIFUGATION;

ORYCTOLAGUS CUNICULUS;

EID: 84872869869     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.11.019     Document Type: Article

References (61)

1. R.G. Hamilton The Human IgG Subclasses 2001 Calbiochem Corporation La Jolla, CA
2. X. Wang, T.K. Das, S.K. Singh, and S. Kumar Potential aggregation prone regions in biotherapeutics: a survey of commercial monoclonal antibodies MAbs 1 2009 254 267
3. O.H. Brekke, T.E. Michaelson, and I. Sandlie The structural requirements for complement activation by IgG: does it hinge on the hinge? Immunol. Today 16 1995 85 90
4. L.J. Harris, E. Skaletsky, and A. McPherson Crystallographic structure of an intact IgG1 monoclonal antibody J. Mol. Biol. 275 1998 861 872
5. E.O. Saphire, P.W.H.I. Parren, R. Pantophlet, M.B. Zwick, G.M. Morris, and P.M. Rudd Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design Science 293 2001 1155 1159
6. L.W. Guddat, J.N. Herron, and A.B. Edmundson Three-dimensional structure of a human immunoglobulin with a hinge deletion Proc. Natl Acad. Sci. USA 90 1993 4271 4275
7. L.J. Harris, S.B. Larson, K.W. Hassel, J. Day, A. Greenwood, and A. McPherson The three-dimensional structure of an intact monoclonal antibody for canine lymphoma Nature 360 1992 369 372
8. Y. Abe, J. Gor, D.G. Bracewell, S.J. Perkins, and P.A. Dalby Masking of the Fc region is human IgG4 by constrained X-ray scattering modeling: implications for antibody function and therapy Biochem. J. 432 2010 101 111
9. M.O. Mayans, W.J. Coadwell, D. Beale, D. Symons, and S.J. Perkins Demonstration by pulsed neutron scattering that the arrangement of the Fab and Fc fragments in the overall structures of bovine IgG1 and IgG2 in solution is similar Biochem. J. 311 1995 283 291
10. M.K. Boehm, J.M. Woof, M.A. Kerr, and S.J. Perkins The Fab and Fc fragments of IgA1 exhibit a different arrangement from that in IgG: a study by X-ray and neutron solution scattering and homology modeling J. Mol. Biol. 286 1999 1421 1447
11. P.B. Furtado, P.W. Whitty, A. Robertson, J.T. Eaton, A. Almogren, and M.A. Kerr Solution structure determination of monomeric human IgA2 by X-ray and neutron scattering, analytical ultracentrifugation and constrained modeling: a comparison with monomeric human IgA1 J. Mol. Biol. 338 2004 921 941
12. Z. Sun, A. Almogren, P.B. Furtado, B. Chowdhury, M.A. Kerr, and S.J. Perkins Semi-extended solution structure of human myeloma immunoglobulin D determined by constrained X-ray scattering J. Mol. Biol. 353 2005 155 173
13. J.L. Dangl, T.G. Wensel, S.L. Morrison, L. Stryer, L.A. Herzenberg, and V.T. Oi Segmental flexibility and complement fixation of genetically engineered chimeric human, rabbit and mouse antibodies EMBO J. 7 1988 1989 1994
14. M.E. Noelken, C.A. Nelson, C.E. Buckley III, and C. Tanford Gross conformation of rabbit 7 S γ-immunoglobulin and its papain-cleaved fragments J. Biol. Chem. 240 1965 218 224
15. E. Girardi, M.D. Holdom, A.D. Davies, B.J. Sutton, and A.J. Beavil The crystal structure of rabbit IgG-Fc Biochem. J. 417 2009 77 83
16. S.J. Perkins, and A. Bonner Structure determinations of human and chimaeric antibodies by solution scattering and constrained molecular modeling Biochem. Soc. Trans. 36 2008 37 42
17. A.I. Okemefuna, R. Nan, J. Gor, and S.J. Perkins Electrostatic interactions contribute to the folded-back conformation of wild-type human factor H J. Mol. Biol. 391 2009 98 118
18. S.J. Perkins Protein volumes and hydration effects Eur. J. Biochem. 157 1986 169 180
19. S.J. Perkins X-ray and neutron scattering analyses of hydration shells: a molecular interpretation based on sequence predictions and modeling fits Biophys. Chem. 93 2001 129 139
20. L. Gregory, K.G. Davies, B. Sheth, J. Boyd, R. Jefferis, C. Nave, and D.R. Burton The solution conformations of the subclasses of human IgG deduced from sedimentation and small angle X-ray scattering studies Mol. Immunol. 24 1987 821 829
21. E. Longman, K. Kreusel, S.B. Tendler, I. Fiebrig, K. King, and J. Adair Estimating domain orientation of two human antibody IgG4 chimeras by crystallohydrodynamics Eur. Biophys. J. 32 2003 503 510
22. Y. Lu, S.E. Harding, T.E. Michaelsen, E. Longman, K.G. Davis, and A. Ortega Solution conformation of wild-type and mutant IgG3 and IgG4 immunoglobulins using crystallohydrodynamics: possible implications for complement activation Biophys. J. 93 2007 3733 3744
23. J.S. Richardson, and D.C. Richardson Principles and patterns of protein conformation G.D. Fasman, Prediction of Protein Structure and the Principles of Protein Conformation 1989 Plenum Press New York, NY 1 98
24. S.J. Perkins, A.I. Okemefuna, R. Nan, K. Li, and A. Bonner Constrained solution scattering modeling of human antibodies and complement proteins reveals novel biological insights J. R. Soc.; Interface 6 2009 S679 S696
25. A.I. Okemefuna, L. Stach, S.R. Rana, A.J.Z. Buetas, J. Gor, and S.J. Perkins C-reactive protein exists in an NaCl concentration-dependent pentamer-decamer equilibrium in physiological buffer J. Biol. Chem. 285 2010 1041 1052
26. Ha allotypes of the rabbit Mol. Immunol. 21 1984 1067 1081
27. Ha locus in natural populations of rabbit (Oryctolagus cuniculus L.) J. Immunol. 172 2004 1044 1053
28. K.E. Bernstein, C.B. Alexander, and R.G. Mage Nucleotide sequence of a rabbit IgG heavy chain from the recombinant F-I haplotype Immunogenetics 18 1983 387 397
29. L. Emorine, J.A. Sogn, D. Trinh, T.J. Kindt, and E.E. Max A genomic gene encoding the b5 rabbit immunoglobulin κ constant region: implications for latent allotype phenomenon Proc. Natl Acad. Sci. USA 81 1984 1789 1793
30. W. van der Loo, F. Mougel, C. Bouton, M.S. Sanchez, and M. Monnerot The allotypic patchwork pattern of the rabbit IGKC1 allele b5wf: genic exchange or common ancestry? Immunogenetics 49 1999 7 14
31. M.A. Akimenko, O. Heidmann, and F. Rougeon Complex allotypes of the rabbit immunoglobulin κ light chains are encoded by structural alleles Nucleic Acids Res. 12 1984 4691 4701
32. A. Benammar, and P.A. Cazenave A second rabbit κ isotype J. Exp. Med. 156 1982 585 595
33. M. Popokov, N. Jendreyko, G. Gonzalez-Sapienza, R.G. Mage, C. Rader, and C.F. Barbas III Human/mouse cross-reactive anti-VEGF receptor 2 recombinant antibodies selected from an immune b9 allotype rabbit antibody library J. Immunol. Methods 288 2004 149 164
34. M.W. Fanger, and D.G. Smyth The oligosaccharide units of rabbit immunoglobulin G Biochem. J. 127 1972 757 765
35. 125I protein A: applications to the quantitative determination of fluid phase and cell-bound IgG J. Immunol. Methods 18 1977 281 293
36. J.V. Ravetch, and J.-P. Kinet Fc receptors Annu. Rev. Immunol. 9 1991 457 492
37. A. Tamm, and R.E. Schmidt IgG binding sites on human Fcγ receptors Int. Rev. Immunol. 16 1997 57 85
38. S. Radaev, and P. Sun Recognition of immunoglobulins by Fcγ receptors Mol. Immunol. 38 2001 1073 1083
39. M. Daëron Fc receptor biology Annu. Rev. Immunol. 15 1997 203 234
40. P. Sondermann, R. Huber, V. Oosthuizen, and U. Jacob The 3.2 Å crystal structure of the human IgG1 Fc fragment-FcγRIII complex Nature 406 2000 267 273
41. S. Krapp, Y. Minura, R. Jefferis, R. Huber, and P. Sondermann Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity J. Mol. Biol. 325 2003 979 989
42. F. Nimmerjahn, and J.V. Ravetch Fcγ receptors as regulators of immune responses Nat. Rev.; Immunol. 8 2008 34 47
43. S. Radaev, S. Motykai, W.-H. Fridman, C. Sautes-Fridman, and P.D. Sun The structure of a human type III Fcγ receptor in complex with Fc J. Biol. Chem. 276 2001 16469 16477
44. S. Schneider, and W. Zacharias Atomic resolution model of the antibody Fc interaction with the complement C1q component Mol. Immunol. 51 2012 66 72
45. M.E.M. Cromwell, E. Hilario, and F. Jacobson Protein aggregation and bioprocessing AAPS J. 8 2006 E572 E579
46. M. Sukumar, B.L. Doyle, J.L. Combs, and A.H. Pekar Opalescent appearance of an IgG1 antibody at high concentrations and its relationship to noncovalent association Pharm. Res. 21 2004 1087 1093
47. Luecke, H.; Glabe, G. G. & Arai, H. (2010). Crystal structure of amyloid prefibrillar-oligomer-specific rabbit Fab. Protein Data Bank accession code 3NL4.
48. T.S. Raju, J.B. Briggs, S.M. Borge, and A.J. Jones Species-specific variation in glycosylation of IgG: evidence for the species-specific sialylation and branch-specific galactosylation and importance for engineering recombinant glycoprotein therapeutics Glycobiology 10 2000 477 486
49. T.M. Laue, B.D. Shah, T.M. Ridgeway, and S.L. Pelletier Computer-Aided interpretation of analytical sedimentation data for proteins S.E. Harding, A.J. Rowe, J.C. Horton, Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992 The Royal Society of Chemistry Cambridge, U.K 90 125
50. P. Schuck Sedimentation analysis of non-interacting and self-Associating solutes using numerical solutions to the Lamm equation Biophys. J. 75 1998 1503 1512
51. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78 2000 1606 1619
52. T. Narayanan, O. Diat, and P. Bosecke SAXS and USAXS on the high brilliance beamline at the ESRF Nucl. Instrum. Methods Phys. Res.; Sect. A 467-468 2001 1005 1009
53. R.K. Heenan, S.E. Rogers, D. Turner, A.E. Terry, J. Treadgold, and S.M. King Small angle neutron scattering using Sans2d Neutron News 22 2011 19 21
54. O. Glatter, and O. Kratky Small Angle X-ray Scattering 1982 Academic Press New York, NY
55. I. Pilz, O. Kratky, A. Licht, and M. Sela Shape and volume of anti-poly(d-Alanyl) antibodies in the presence and absence of tetra-d-Alanine as followed by small-Angle X-ray scattering Biochemistry 12 1973 4998 5005
56. A.V. Semenyuk, and D.I. Svergun GNOM - a program package for small-Angle scattering data-processing J. Appl. Crystallogr. 24 1991 537 540
57. A.W. Ashton, M.K. Boehm, J.R. Gallimore, M.B. Pepys, and S.J. Perkins Pentameric and decameric structures in solution of the serum amyloid P component by X-ray and neutron scattering and molecular modeling analyses J. Mol. Biol. 272 1997 408 422
58. S.J. Perkins, and H. Weiss Low resolution structural studies of mitochondrial ubiquinol:cytochrome c reductase in detergent solutions by neutron scattering J. Mol. Biol. 168 1983 847 866
59. J. Garcia de la Torre, S. Navarro, M.C.L. Martinez, F.G. Diaz, and J.L. Cascales HYDRO: a computer program for the prediction of hydrodynamic properties of macromolecules Biophys. J. 67 1994 530 531
60. J. GarciadelaTorre, M.L. Huertas, and B. Carrasco Calculation of hydrodynamic properties of globular proteins from their atomic-level structure Biophys. J. 78 2000 719 730
61. D. Schneidman-Duhovny, Y. Inbar, R. Nussinov, and H.J. Wolfson PatchDock and SymmDock: servers for rigid and symmetric docking Nucleic Acids Res. 33 2005 W363 W367