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Implications of the near-planar solution structure of human myeloma dimeric IgA1 for mucosal immunity and IgA nephropathy.

Bonner A, Furtado PB, Almogren A, Kerr MA, Perkins SJ
J Immunol 180 1008-18 (2008)
Cited: 36 times
EuropePMC logo PMID: 18178841

Abstract

IgA is unique in being able to form a diverse range of polymeric structures. Increases in the levels of dimeric IgA1 (dIgA1) in serum have been implicated in diseases such as IgA nephropathy. We have determined the solution structure for dIgA1 by synchrotron x-ray and neutron scattering and analytical ultracentrifugation. The Guinier radius of gyration (RG) of 7.60-8.65 nm indicated that the two monomers within dIgA1 are arranged in an extended conformation. The distance distribution curve P(r) gave an overall length (L) of 22-26 nm. These results were confirmed by the sedimentation coefficient and frictional ratio of dIgA1. Constrained scattering modeling starting from the IgA1 monomer solution structure revealed a near-planar dimer structure for dIgA1. The two Fc regions form a slightly bent arrangement in which they form end-to-end contacts, and the J chain was located at this interface. This structure was refined by optimizing the position of the four Fab regions. From this, the best-fit solution structures show that the four Fab Ag-binding sites are independent of one another, and the two Fc regions are accessible to receptor binding. This arrangement allows dIgA1 to initiate specific immune responses by binding to FcalphaRI receptors, while still retaining Ag-binding ability, and to be selectively transported to mucosal surfaces by binding to the polymeric Ig receptor to form secretory IgA. A mechanism for the involvement of dIgA1 oligomers in the pathology of IgA nephropathy is discussed in the light of this near-planar structure.

Reviews - 2qtj mentioned but not cited (1)

  1. IgA and FcαRI: Pathological Roles and Therapeutic Opportunities. Breedveld A, van Egmond M. Front Immunol 10 553 (2019)

Articles - 2qtj mentioned but not cited (5)

  1. Protein structure analysis of the interactions between SARS-CoV-2 spike protein and the human ACE2 receptor: from conformational changes to novel neutralizing antibodies. Mercurio I, Tragni V, Busto F, De Grassi A, Pierri CL. Cell Mol Life Sci 78 1501-1522 (2021)
  2. The nonplanar secretory IgA2 and near planar secretory IgA1 solution structures rationalize their different mucosal immune responses. Bonner A, Almogren A, Furtado PB, Kerr MA, Perkins SJ. J. Biol. Chem. 284 5077-5087 (2009)
  3. Structural requirements for the interaction of human IgM and IgA with the human Fcalpha/mu receptor. Ghumra A, Shi J, Mcintosh RS, Rasmussen IB, Braathen R, Johansen FE, Sandlie I, Mongini PK, Areschoug T, Lindahl G, Lewis MJ, Woof JM, Pleass RJ. Eur. J. Immunol. 39 1147-1156 (2009)
  4. Allosteric Effects between the Antibody Constant and Variable Regions: A Study of IgA Fc Mutations on Antigen Binding. Su CT, Lua WH, Ling WL, Gan SK. Antibodies (Basel) 7 (2018)
  5. Design of a peptide for immunodetection of IgA antigliadin antibody for the purpose of screening of celiac disease. Bhattacharyya R, Sharma N, Banerjee D. Bioinformation 8 87-91 (2012)


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  1. Are anti-HIV IgAs good guys or bad guys? Zhou M, Ruprecht RM. Retrovirology 11 109 (2014)
  2. Antibody-mediated immune exclusion of HIV. Ruprecht RM, Lakhashe SK. Curr Opin HIV AIDS 12 222-228 (2017)
  3. IgA: Structure, Function, and Developability. de Sousa-Pereira P, Woof JM. Antibodies (Basel) 8 (2019)
  4. Pathogenesis of IgA Nephropathy: Current Understanding and Implications for Development of Disease-Specific Treatment. Knoppova B, Reily C, King RG, Julian BA, Novak J, Green TJ. J Clin Med 10 4501 (2021)
  5. Antibody Fc-chimerism and effector functions: When IgG takes advantage of IgA. Cottignies-Calamarte A, Tudor D, Bomsel M. Front Immunol 14 1037033 (2023)
  6. IgA and FcαRI: Versatile Players in Homeostasis, Infection, and Autoimmunity. van Gool MMJ, van Egmond M. Immunotargets Ther 9 351-372 (2020)

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  1. Anti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission. Watkins JD, Sholukh AM, Mukhtar MM, Siddappa NB, Lakhashe SK, Kim M, Reinherz EL, Gupta S, Forthal DN, Sattentau QJ, Villinger F, Corti D, Ruprecht RM, CAVD Project Group. AIDS 27 F13-20 (2013)
  2. Secretory IgA: Designed for Anti-Microbial Defense. Brandtzaeg P. Front Immunol 4 222 (2013)
  3. Location of secretory component on the Fc edge of dimeric IgA1 reveals insight into the role of secretory IgA1 in mucosal immunity. Bonner A, Almogren A, Furtado PB, Kerr MA, Perkins SJ. Mucosal Immunol 2 74-84 (2009)
  4. Secretory immunity with special reference to the oral cavity. Brandtzaeg P. J Oral Microbiol 5 (2013)
  5. Constrained solution scattering modelling of human antibodies and complement proteins reveals novel biological insights. Perkins SJ, Okemefuna AI, Nan R, Li K, Bonner A. J R Soc Interface 6 Suppl 5 S679-96 (2009)
  6. Design and characterization of structured protein linkers with differing flexibilities. Klein JS, Jiang S, Galimidi RP, Keeffe JR, Bjorkman PJ. Protein Eng. Des. Sel. 27 325-330 (2014)
  7. Masking of the Fc region in human IgG4 by constrained X-ray scattering modelling: implications for antibody function and therapy. Abe Y, Gor J, Bracewell DG, Perkins SJ, Dalby PA. Biochem. J. 432 101-111 (2010)
  8. Aggregate complexes of HIV-1 induced by multimeric antibodies. Stieh DJ, King DF, Klein K, Liu P, Shen X, Hwang KK, Ferrari G, Montefiori DC, Haynes B, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Michael NL, Robb ML, Kim JH, Denny TN, Tomaras GD, Shattock RJ. Retrovirology 11 78 (2014)
  9. Near-planar solution structures of mannose-binding lectin oligomers provide insight on activation of lectin pathway of complement. Miller A, Phillips A, Gor J, Wallis R, Perkins SJ. J. Biol. Chem. 287 3930-3945 (2012)
  10. Simplifying the synthesis of SIgA: combination of dIgA and rhSC using affinity chromatography. Moldt B, Saye-Francisco K, Schultz N, Burton DR, Hessell AJ. Methods 65 127-132 (2014)
  11. Functional and structural characterisation of human colostrum free secretory component. Almogren A, Bonner A, Perkins SJ, Kerr MA. Mol. Immunol. 46 1534-1541 (2009)
  12. The solution structures of native and patient monomeric human IgA1 reveal asymmetric extended structures: implications for function and IgAN disease. Hui GK, Wright DW, Vennard OL, Rayner LE, Pang M, Yeo SC, Gor J, Molyneux K, Barratt J, Perkins SJ. Biochem. J. 471 167-185 (2015)
  13. SCT: a suite of programs for comparing atomistic models with small-angle scattering data. Wright DW, Perkins SJ. J Appl Crystallogr 48 953-961 (2015)
  14. Maternal gatekeepers: How maternal antibody Fc characteristics influence passive transfer and infant protection. Langel SN, Otero CE, Martinez DR, Permar SR. PLoS Pathog 16 e1008303 (2020)
  15. Effects of Acanthopanax senticosus supplementation on innate immunity and changes of related immune factors in healthy mice. Zhang Y, Zhang Y, Liu Z. Innate Immun 27 461-469 (2021)
  16. FcαRI binding at the IgA1 CH2-CH3 interface induces long-range conformational changes that are transmitted to the hinge region. Posgai MT, Tonddast-Navaei S, Jayasinghe M, Ibrahim GM, Stan G, Herr AB. Proc. Natl. Acad. Sci. U.S.A. 115 E8882-E8891 (2018)
  17. Structural insights into secretory immunoglobulin A and its interaction with a pneumococcal adhesin. Wang Y, Wang G, Li Y, Zhu Q, Shen H, Gao N, Xiao J. Cell Res 30 602-609 (2020)
  18. Efficient N-Glycosylation of the Heavy Chain Tailpiece Promotes the Formation of Plant-Produced Dimeric IgA. Göritzer K, Goet I, Duric S, Maresch D, Altmann F, Obinger C, Strasser R. Front Chem 8 346 (2020)
  19. News Glomerular disease: sugars and immune complex formation in IgA nephropathy. Barratt J, Eitner F. Nat Rev Nephrol 5 612-614 (2009)
  20. High ambient humidity aggravates ammonia-induced respiratory mucosal inflammation by eliciting Th1/Th2 imbalance and NF-κB pathway activation in laying hens. Wang C, Bing A, Liu H, Wang X, Zhao J, Lin H, Jiao H. Poult Sci 101 102028 (2022)
  21. Human IgA Monoclonal Antibodies That Neutralize Poliovirus, Produced by Hybridomas and Recombinant Expression. Puligedda RD, Vigdorovich V, Kouiavskaia D, Kattala CD, Zhao JY, Al-Saleem FH, Chumakov K, Sather DN, Dessain SK. Antibodies (Basel) 9 (2020)
  22. Conversion of monoclonal IgG to dimeric and secretory IgA restores neutralizing ability and prevents infection of Omicron lineages. Marcotte H, Cao Y, Zuo F, Simonelli L, Sammartino JC, Pedotti M, Sun R, Cassaniti I, Hagbom M, Piralla A, Yang J, Du L, Percivalle E, Bertoglio F, Schubert M, Abolhassani H, Sherina N, Guerra C, Borte S, Rezaei N, Kumagai-Braesch M, Xue Y, Su C, Yan Q, He P, Grönwall C, Klareskog L, Calzolai L, Cavalli A, Wang Q, Robbiani DF, Hust M, Shi Z, Feng L, Svensson L, Chen L, Bao L, Baldanti F, Xiao J, Qin C, Hammarström L, Yang X, Varani L, Xie XS, Pan-Hammarström Q. Proc Natl Acad Sci U S A 121 e2315354120 (2024)
  23. Cooperation Between Systemic IgG1 and Mucosal Dimeric IgA2 Monoclonal Anti-HIV Env Antibodies: Passive Immunization Protects Indian Rhesus Macaques Against Mucosal SHIV Challenges. Gong S, Lakhashe SK, Hariraju D, Scinto H, Lanzavecchia A, Cameroni E, Corti D, Ratcliffe SJ, Rogers KA, Xiao P, Fontenot J, Villinger F, Ruprecht RM. Front Immunol 12 705592 (2021)
  24. Detailed Structure and Pathophysiological Roles of the IgA-Albumin Complex in Multiple Myeloma. Kawata Y, Hirano H, Takahashi R, Miyano Y, Kimura A, Sato N, Morita Y, Kimura H, Fujita K. Int J Mol Sci 22 1766 (2021)


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