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Molecular basis for immune complex recognition: a comparison of Fc-receptor structures.

Sondermann P, Kaiser J, Jacob U
J Mol Biol 309 737-49 (2001)
Cited: 79 times
EuropePMC logo PMID: 11397093

Abstract

Once antigen is opsonised by IgG it is removed from the circulation by Fcgamma-receptor expressing cells. Fcgamma-receptors are type I transmembrane molecules that carry extracellular parts consisting of two or three immunoglobulin domains. Previously solved structures of Fc-receptors reveal that the N-terminal two Ig-like domains are arranged in a steep angle forming a heart-shaped structure. The crystal structure of the FcgammaRIII/hIgG1-Fc-fragment demonstrated that the Fc-fragment is recognised through loops of the C-terminal receptor domain of the FcgammaRIII. As the overall structure of the FcRs and their Ig ligands are very similar we modelled the Ig complexes with FcgammaRI, FcgammaRII and FcepsilonRIalpha based on the FcgammaRIII/hIgG1-Fc-fragment structure. The obtained models are consistent with the observed biochemical data and may explain the observed specificity and affinities.

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  3. FcγRIIA-specific DARPins as novel tools in blood cell analysis and platelet aggregation. Riechert V, Hein S, Visser M, Zimmermann M, Wesche J, Adams PA, Theuerkauf SA, Jamali A, Wangorsch A, Reuter A, Pasternak AO, Hartmann J, Greinacher A, Herrera-Carrillo E, Berkhout B, Cichutek K, Buchholz CJ. J Biol Chem 299 104743 (2023)


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  1. Fcgamma receptors as regulators of immune responses. Nimmerjahn F, Ravetch JV. Nat Rev Immunol 8 34-47 (2008)
  2. The biology of IGE and the basis of allergic disease. Gould HJ, Sutton BJ, Beavil AJ, Beavil RL, McCloskey N, Coker HA, Fear D, Smurthwaite L. Annu Rev Immunol 21 579-628 (2003)
  3. The role of IgG Fc receptors in antibody-dependent enhancement. Bournazos S, Gupta A, Ravetch JV. Nat Rev Immunol 20 633-643 (2020)
  4. FcgammaR polymorphisms: Implications for function, disease susceptibility and immunotherapy. van Sorge NM, van der Pol WL, van de Winkel JG. Tissue Antigens 61 189-202 (2003)
  5. Human antibody-Fc receptor interactions illuminated by crystal structures. Woof JM, Burton DR. Nat Rev Immunol 4 89-99 (2004)
  6. Fc glycans of therapeutic antibodies as critical quality attributes. Reusch D, Tejada ML. Glycobiology 25 1325-1334 (2015)
  7. Interaction sites on human IgG-Fc for FcgammaR: current models. Jefferis R, Lund J. Immunol Lett 82 57-65 (2002)
  8. Fcγ Receptor Function and the Design of Vaccination Strategies. Bournazos S, Ravetch JV. Immunity 47 224-233 (2017)
  9. Fc receptor homologs: newest members of a remarkably diverse Fc receptor gene family. Davis RS, Dennis G, Odom MR, Gibson AW, Kimberly RP, Burrows PD, Cooper MD. Immunol Rev 190 123-136 (2002)
  10. Fcγ receptor pathways during active and passive immunization. Bournazos S, Ravetch JV. Immunol Rev 268 88-103 (2015)
  11. Recognition of immunoglobulins by Fcgamma receptors. Radaev S, Sun P. Mol Immunol 38 1073-1083 (2002)
  12. FcgammaRIIB, FcgammaRIIIB, and systemic lupus erythematosus. Niederer HA, Clatworthy MR, Willcocks LC, Smith KG. Ann N Y Acad Sci 1183 69-88 (2010)
  13. Diversification of IgG effector functions. Bournazos S, Ravetch JV. Int Immunol 29 303-310 (2017)
  14. The Role and Function of Fcγ Receptors on Myeloid Cells. Bournazos S, Wang TT, Ravetch JV. Microbiol Spectr 4 (2016)
  15. Engineering therapeutic monoclonal antibodies. Liu XY, Pop LM, Vitetta ES. Immunol Rev 222 9-27 (2008)
  16. Fc gamma receptors: glycobiology and therapeutic prospects. Hayes JM, Wormald MR, Rudd PM, Davey GP. J Inflamm Res 9 209-219 (2016)
  17. Glycosylation: impact, control and improvement during therapeutic protein production. Costa AR, Rodrigues ME, Henriques M, Oliveira R, Azeredo J. Crit Rev Biotechnol 34 281-299 (2014)
  18. Structural analysis of Fc/FcγR complexes: a blueprint for antibody design. Caaveiro JM, Kiyoshi M, Tsumoto K. Immunol Rev 268 201-221 (2015)
  19. An extended family of Fc receptor relatives. Davis RS, Ehrhardt GR, Leu CM, Hirano M, Cooper MD. Eur J Immunol 35 674-680 (2005)
  20. Crystallizable Fragment Glycoengineering for Therapeutic Antibodies Development. Li W, Zhu Z, Chen W, Feng Y, Dimitrov DS. Front Immunol 8 1554 (2017)
  21. Anti-retroviral antibody FcγR-mediated effector functions. Bournazos S, Ravetch JV. Immunol Rev 275 285-295 (2017)
  22. Molecular aspects of human FcgammaR interactions with IgG: functional and therapeutic consequences. Sibéril S, Dutertre CA, Boix C, Bonnin E, Ménez R, Stura E, Jorieux S, Fridman WH, Teillaud JL. Immunol Lett 106 111-118 (2006)
  23. Antibody engineering for therapeutics. Presta L. Curr Opin Struct Biol 13 519-525 (2003)
  24. Genetics of SLE: functional relevance for monocytes/macrophages in disease. Byrne JC, Ní Gabhann J, Lazzari E, Mahony R, Smith S, Stacey K, Wynne C, Jefferies CA. Clin Dev Immunol 2012 582352 (2012)
  25. Designing proteins for therapeutic applications. Lazar GA, Marshall SA, Plecs JJ, Mayo SL, Desjarlais JR. Curr Opin Struct Biol 13 513-518 (2003)
  26. Antiviral Functions of Monoclonal Antibodies against Chikungunya Virus. Jin J, Simmons G. Viruses 11 E305 (2019)
  27. Antibody-Dependent Enhancement (ADE) and the role of complement system in disease pathogenesis. Thomas S, Smatti MK, Ouhtit A, Cyprian FS, Almaslamani MA, Thani AA, Yassine HM. Mol Immunol 152 172-182 (2022)
  28. Engineered CD3 antibodies for immunosuppression. Renders L, Valerius T. Clin Exp Immunol 133 307-309 (2003)
  29. Next generation of multispecific antibody engineering. Keri D, Walker M, Singh I, Nishikawa K, Garces F. Antib Ther 7 37-52 (2024)

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  1. Engineered antibody Fc variants with enhanced effector function. Lazar GA, Dang W, Karki S, Vafa O, Peng JS, Hyun L, Chan C, Chung HS, Eivazi A, Yoder SC, Vielmetter J, Carmichael DF, Hayes RJ, Dahiyat BI. Proc Natl Acad Sci U S A 103 4005-4010 (2006)
  2. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Mol Immunol 44 1524-1534 (2007)
  3. In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity. Thomann M, Schlothauer T, Dashivets T, Malik S, Avenal C, Bulau P, Rüger P, Reusch D. PLoS One 10 e0134949 (2015)
  4. Impact of methionine oxidation on the binding of human IgG1 to Fc Rn and Fc gamma receptors. Bertolotti-Ciarlet A, Wang W, Lownes R, Pristatsky P, Fang Y, McKelvey T, Li Y, Li Y, Drummond J, Prueksaritanont T, Vlasak J. Mol Immunol 46 1878-1882 (2009)
  5. The crystal structure of IgE Fc reveals an asymmetrically bent conformation. Wan T, Beavil RL, Fabiane SM, Beavil AJ, Sohi MK, Keown M, Young RJ, Henry AJ, Owens RJ, Gould HJ, Sutton BJ. Nat Immunol 3 681-686 (2002)
  6. Structural basis for Fc gammaRIIa recognition of human IgG and formation of inflammatory signaling complexes. Ramsland PA, Farrugia W, Bradford TM, Sardjono CT, Esparon S, Trist HM, Powell MS, Tan PS, Cendron AC, Wines BD, Scott AM, Hogarth PM. J Immunol 187 3208-3217 (2011)
  7. The importance of human FcgammaRI in mediating protection to malaria. McIntosh RS, Shi J, Jennings RM, Chappel JC, de Koning-Ward TF, Smith T, Green J, van Egmond M, Leusen JH, Lazarou M, van de Winkel J, Jones TS, Crabb BS, Holder AA, Pleass RJ. PLoS Pathog 3 e72 (2007)
  8. Conformational changes in IgE contribute to its uniquely slow dissociation rate from receptor FcɛRI. Holdom MD, Davies AM, Nettleship JE, Bagby SC, Dhaliwal B, Girardi E, Hunt J, Gould HJ, Beavil AJ, McDonnell JM, Owens RJ, Sutton BJ. Nat Struct Mol Biol 18 571-576 (2011)
  9. Structural basis for binding of human IgG1 to its high-affinity human receptor FcγRI. Kiyoshi M, Caaveiro JM, Kawai T, Tashiro S, Ide T, Asaoka Y, Hatayama K, Tsumoto K. Nat Commun 6 6866 (2015)
  10. Quantitative evaluation of fucose reducing effects in a humanized antibody on Fcγ receptor binding and antibody-dependent cell-mediated cytotoxicity activities. Chung S, Quarmby V, Gao X, Ying Y, Lin L, Reed C, Fong C, Lau W, Qiu ZJ, Shen A, Vanderlaan M, Song A. MAbs 4 326-340 (2012)
  11. Analysis of binding sites in human C-reactive protein for Fc{gamma}RI, Fc{gamma}RIIA, and C1q by site-directed mutagenesis. Bang R, Marnell L, Mold C, Stein MP, Clos KT, Chivington-Buck C, Clos TW. J Biol Chem 280 25095-25102 (2005)
  12. Crystal structure of Fcγ receptor I and its implication in high affinity γ-immunoglobulin binding. Lu J, Ellsworth JL, Hamacher N, Oak SW, Sun PD. J Biol Chem 286 40608-40613 (2011)
  13. The chicken leukocyte receptor complex encodes a primordial, activating, high-affinity IgY Fc receptor. Viertlboeck BC, Schweinsberg S, Hanczaruk MA, Schmitt R, Du Pasquier L, Herberg FW, Göbel TW. Proc Natl Acad Sci U S A 104 11718-11723 (2007)
  14. Carbohydrate and domain architecture of an immature antibody glycoform exhibiting enhanced effector functions. Crispin M, Bowden TA, Coles CH, Harlos K, Aricescu AR, Harvey DJ, Stuart DI, Jones EY. J Mol Biol 387 1061-1066 (2009)
  15. Differential binding to human FcgammaRIIa and FcgammaRIIb receptors by human IgG wildtype and mutant antibodies. Armour KL, van de Winkel JG, Williamson LM, Clark MR. Mol Immunol 40 585-593 (2003)
  16. CODV-Ig, a universal bispecific tetravalent and multifunctional immunoglobulin format for medical applications. Steinmetz A, Vallée F, Beil C, Lange C, Baurin N, Beninga J, Capdevila C, Corvey C, Dupuy A, Ferrari P, Rak A, Wonerow P, Kruip J, Mikol V, Rao E. MAbs 8 867-878 (2016)
  17. An unusual Fc receptor-related protein expressed in human centroblasts. Facchetti F, Cella M, Festa S, Fremont DH, Colonna M. Proc Natl Acad Sci U S A 99 3776-3781 (2002)
  18. Cis interaction between sialylated FcγRIIA and the αI-domain of Mac-1 limits antibody-mediated neutrophil recruitment. Saggu G, Okubo K, Chen Y, Vattepu R, Tsuboi N, Rosetti F, Cullere X, Washburn N, Tahir S, Rosado AM, Holland SM, Anthony RM, Sen M, Zhu C, Mayadas TN. Nat Commun 9 5058 (2018)
  19. Structural characterization of GASDALIE Fc bound to the activating Fc receptor FcγRIIIa. Ahmed AA, Keremane SR, Vielmetter J, Bjorkman PJ. J Struct Biol 194 78-89 (2016)
  20. Chimeric anti-CD14 IGG2/4 Hybrid antibodies for therapeutic intervention in pig and human models of inflammation. Lau C, Gunnarsen KS, Høydahl LS, Andersen JT, Berntzen G, Pharo A, Lindstad JK, Ludviksen JK, Brekke OL, Barratt-Due A, Nielsen EW, Stokes CR, Espevik T, Sandlie I, Mollnes TE. J Immunol 191 4769-4777 (2013)
  21. Anti-CD20-interferon-β fusion protein therapy of murine B-cell lymphomas. Trinh KR, Vasuthasawat A, Steward KK, Yamada RE, Timmerman JM, Morrison SL. J Immunother 36 305-318 (2013)
  22. The crystal structure of CHIR-AB1: a primordial avian classical Fc receptor. Arnon TI, Kaiser JT, West AP, Olson R, Diskin R, Viertlboeck BC, Göbel TW, Bjorkman PJ. J Mol Biol 381 1012-1024 (2008)
  23. A new ligand for immunoglobulin g subdomains by screening of a synthetic peptide library. Verdoliva A, Marasco D, De Capua A, Saporito A, Bellofiore P, Manfredi V, Fattorusso R, Pedone C, Ruvo M. Chembiochem 6 1242-1253 (2005)
  24. Soluble FcgammaRIIa inhibits rheumatoid factor binding to immune complexes. Wines BD, Gavin A, Powell MS, Steinitz M, Buchanan RR, Mark Hogarth P. Immunology 109 246-254 (2003)
  25. Herpesviral Fcgamma receptors: culprits attenuating antiviral IgG? Budt M, Reinhard H, Bigl A, Hengel H. Int Immunopharmacol 4 1135-1148 (2004)
  26. Efficient expression and purification of human aglycosylated Fcgamma receptors in Escherichia coli. Jung ST, Kang TH, Georgiou G. Biotechnol Bioeng 107 21-30 (2010)
  27. Identification of cyclic peptides able to mimic the functional epitope of IgG1-Fc for human Fc gammaRI. Bonetto S, Spadola L, Buchanan AG, Jermutus L, Lund J. FASEB J 23 575-585 (2009)
  28. Hypogalactosylation of immunoglobulin G in rheumatoid arthritis: relationship to HLA-DRB1 shared epitope, anticitrullinated protein antibodies, rheumatoid factor, and correlation with inflammatory activity. Schwedler C, Häupl T, Kalus U, Blanchard V, Burmester GR, Poddubnyy D, Hoppe B. Arthritis Res Ther 20 44 (2018)
  29. The structure of Fc receptor/Ig complexes: considerations on stoichiometry and potential inhibitors. Sondermann P, Oosthuizen V. Immunol Lett 82 51-56 (2002)
  30. Structure of a Therapeutic Full-Length Anti-NPRA IgG4 Antibody: Dissecting Conformational Diversity. Blech M, Hörer S, Kuhn AB, Kube S, Göddeke H, Kiefer H, Zang Y, Alber Y, Kast SM, Westermann M, Tully MD, Schäfer LV, Garidel P. Biophys J 116 1637-1649 (2019)
  31. An FcgammaRIIa-binding peptide that mimics the interaction between FcgammaRIIa and IgG. Cendron AC, Wines BD, Brownlee RT, Ramsland PA, Pietersz GA, Hogarth PM. Mol Immunol 45 307-319 (2008)
  32. Mapping of the binding site for FcμR in human IgM-Fc. Nyamboya RA, Sutton BJ, Calvert RA. Biochim Biophys Acta Proteins Proteom 1868 140266 (2020)
  33. The quality of chimpanzee T-cell activation and simian immunodeficiency virus/human immunodeficiency virus susceptibility achieved via antibody-mediated T-cell receptor/CD3 stimulation is a function of the anti-CD3 antibody isotype. Bibollet-Ruche F, McKinney BA, Duverger A, Wagner FH, Ansari AA, Kutsch O. J Virol 82 10271-10278 (2008)
  34. Effect of trastuzumab interchain disulfide bond cleavage on Fcγ receptor binding and antibody-dependent tumour cell phagocytosis. Suzuki M, Yamanoi A, Machino Y, Ootsubo M, Izawa K, Kohroki J, Masuho Y. J Biochem 159 67-76 (2016)
  35. Integrative Pan-Cancer Analysis Confirmed that FCGR3A is a Candidate Biomarker Associated With Tumor Immunity. Li L, Huang Z, Du K, Liu X, Li C, Wang D, Zhang Y, Wang C, Li J. Front Pharmacol 13 900699 (2022)
  36. Single molecule Förster resonance energy transfer studies of the effect of EndoS deglycosylation on the structure of IgG. Piraino MS, Kelliher MT, Aburas J, Southern CA. Immunol Lett 167 29-33 (2015)
  37. Efficient expression of recombinant soluble human FcγRI in mammalian cells and its characterization. Asaoka Y, Tanaka T, Tsumoto K, Tomita M, Ide T. Protein Expr Purif 82 155-161 (2012)
  38. Efficient recovery of a functional extracellular domain of bovine IgG2 Fc receptor (boFcgamma2R) from inclusion bodies by a rapid dilution refolding system. Zhang G, Xi J, Wang X, Guo J, Zhang H, Yang Y, Qiao S, Wang L, Zhang H, He L, Zhu Y. J Immunol Methods 334 21-28 (2008)
  39. Expression, purification and characterization of a functional extracellular domain of porcine FcgammaRII. Tian X, Wang A, Qiao S, Zhang G, Xi J, Li X, Liu Y, Xu Y. Protein Expr Purif 68 12-17 (2009)
  40. Inhibitory affinity modulation of FcγRIIA ligand binding by glycosphingolipids by inside-out signaling. Okubo K, Brenner MD, Cullere X, Saggu G, Patchen ML, Bose N, Mihori S, Yuan Z, Lowell CA, Zhu C, Mayadas TN. Cell Rep 35 109142 (2021)
  41. Negative design for improved therapeutic proteins. Desjarlais JR, Lazar GA. Trends Biotechnol 21 425-427 (2003)
  42. Structured to reduce the mitogenicity of anti-CD3 antibody based on computer-guided molecular design. Lv M, Li Y, Yu M, Sun Y, Lin Z, Qiao C, Luo Q, Gu X, Huang Y, Feng J, Shen B. Int J Biochem Cell Biol 39 1142-1155 (2007)
  43. Systematic Analysis of the Expression and Prognosis of Fcγ Receptors in Clear Cell Renal Cell Carcinoma. Nie W, Yao Y, Luo B, Zhu J, Li S, Yang X, Luo T, Liu W, Yan S. Front Oncol 12 755936 (2022)
  44. A homogeneous bioluminescent immunoassay for parallel characterization of binding between a panel of antibodies and a family of Fcγ receptors. Nath N, Godat B, Flemming R, Urh M. Sci Rep 12 12185 (2022)
  45. Fc Gamma Receptor IIIB NA1/NA2/SH Polymorphisms Are Associated with Malaria Susceptibility and Antibody Levels to P. falciparum Merozoite Antigens in Beninese Children. Fall AKDJ, Courtin D, Adamou R, Edslev S, Hansen A, Domingo N, Christiansen M, Adu B, Milet J, Garcia A, Theisen M, Migot-Nabias F, Dechavanne C. Int J Mol Sci 23 14882 (2022)
  46. Function-structure approach reveals novel insights on the interplay of Immunoglobulin G 1 proteoforms and Fc gamma receptor IIa allotypes. Lippold S, Mistry K, Lenka S, Whang K, Liu P, Pitschi S, Kuhne F, Reusch D, Cadang L, Knaupp A, Izadi S, Dunkle A, Yang F, Schlothauer T. Front Immunol 14 1260446 (2023)
  47. Inhibitory Fc-Gamma IIb Receptor Signaling Induced by Multivalent IgG-Fc Is Dependent on Sialylation. Beneduce C, Nguyen S, Washburn N, Schaeck J, Meccariello R, Holte K, Ortiz D, Manning AM, Bosques CJ, Kurtagic E. Cells 12 2130 (2023)


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