High microbiota reactivity of adult human intestinal IgA requires somatic mutations

被引:59
作者
Kabbert, Johanna [1 ]
Benckert, Julia [2 ,5 ,6 ,7 ,8 ]
Rollenske, Tim [3 ]
Hitch, Thomas C. A. [4 ]
Clavel, Thomas [4 ]
Cerovic, Vuk [1 ]
Wardemann, Hedda [3 ]
Pabst, Oliver [1 ]
机构
[1] Rhein Westfalische TH Aachen Univ, Inst Mol Med, Aachen, Germany
[2] Max Planck Inst Infect Biol, Max Planck Res Grp Mol Immunol, Berlin, Germany
[3] German Canc Res Ctr, B Cell Immunol, Heidelberg, Germany
[4] Rhein Westfalische TH Aachen Univ, Inst Med Microbiol, Funct Microbiome Res Grp, Aachen, Germany
[5] Charite Univ Med Berlin, Berlin, Germany
[6] Free Univ Berlin, Berlin, Germany
[7] Humboldt Univ, Berlin, Germany
[8] Berlin Inst Hlth, Berlin, Germany
关键词
MEMORY B-CELLS; IMMUNOGLOBULIN-A; SECRETORY IGA; BACTERIA; GUT; ANTIBODIES; SEQUENCES;
D O I
10.1084/jem.20200275
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
The gut is home to the body's largest population of plasma cells. In healthy individuals, IgA is the dominating isotype, whereas patients with inflammatory bowel disease also produce high concentrations of IgG. In the gut lumen, secretory IgA binds pathogens and toxins but also the microbiota. However, the antigen specificity of IgA and IgG for the microbiota and underlying mechanisms of antibody binding to bacteria are largely unknown. Here we show that microbiota binding is a defining property of human intestinal antibodies in both healthy and inflamed gut. Some bacterial taxa were commonly targeted by different monoclonal antibodies, whereas others selectively bound single antibodies. Interestingly, individual human monoclonal antibodies from both healthy and inflamed intestines bound phylogenetically unrelated bacterial species. This microbiota cross-species reactivity did not correlate with antibody polyreactivity but was crucially dependent on the accumulation of somatic mutations. Therefore, our data suggest that a system of affinity-matured, microbiota cross-species-reactive IgA is a common aspect of SIgA-microbiota interactions in the gut.
引用
收藏
页数:18
相关论文
共 35 条
  • [1] The human immunoglobulin A Fc receptor FcαRI: a multifaceted regulator of mucosal immunity
    Bakema, J. E.
    van Egmond, M.
    [J]. MUCOSAL IMMUNOLOGY, 2011, 4 (06) : 612 - 624
  • [2] IgA-Producing Plasma Cells Originate From Germinal Centers That Are Induced by B-Cell Receptor Engagement in Humans
    Barone, Francesca
    Vossenkamper, Anna
    Boursier, Laurent
    Su, Wen
    Watson, Alan
    John, Susan
    Dunn-Walters, Deborah K.
    Fields, Paul
    Wijetilleka, Sonali
    Edgeworth, Jonathan D.
    Spencer, Jo
    [J]. GASTROENTEROLOGY, 2011, 140 (03) : 947 - 956
  • [3] The majority of intestinal IgA+ and IgG+ plasmablasts in the human gut are antigen-specific
    Benckert, Julia
    Schmolka, Nina
    Kreschel, Cornelia
    Zoller, Markus Josef
    Sturm, Andreas
    Wiedenmann, Bertram
    Wardemann, Hedda
    [J]. JOURNAL OF CLINICAL INVESTIGATION, 2011, 121 (05) : 1946 - 1955
  • [4] Circulating Human CD27-IgA+ Memory B Cells Recognize Bacteria with Polyreactive Igs
    Berkowska, Magdalena A.
    Schickel, Jean-Nicolas
    Grosserichter-Wagener, Christina
    de Ridder, Dick
    Ng, Yen Shing
    van Dongen, Jacques J. M.
    Meffre, Eric
    van Zelm, Menno C.
    [J]. JOURNAL OF IMMUNOLOGY, 2015, 195 (04) : 1417 - 1426
  • [5] Mucosal Immunity: Induction, Dissemination, and Effector Functions
    Brandtzaeg, P.
    [J]. SCANDINAVIAN JOURNAL OF IMMUNOLOGY, 2009, 70 (06) : 505 - 515
  • [6] B cell superantigens in the human intestinal microbiota
    Bunker, Jeffrey J.
    Drees, Christoph
    Watson, Andrea R.
    Plunkett, Catherine H.
    Nagler, Cathryn R.
    Schneewind, Olaf
    Eren, A. Murat
    Bendelac, Albert
    [J]. SCIENCE TRANSLATIONAL MEDICINE, 2019, 11 (507)
  • [7] Natural polyreactive IgA antibodies coat the intestinal microbiota
    Bunker, Jeffrey J.
    Erickson, Steven A.
    Flynn, Theodore M.
    Henry, Carole
    Koval, Jason C.
    Meisel, Marlies
    Jabri, Bana
    Antonopoulos, Dionysios A.
    Wilson, Patrick C.
    Bendelac, Albert
    [J]. SCIENCE, 2017, 358 (6361)
  • [8] Innate and Adaptive Humoral Responses Coat Distinct Commensal Bacteria with Immunoglobulin A
    Bunker, Jeffrey J.
    Flynn, Theodore M.
    Koval, Jason C.
    Shaw, Dustin G.
    Meisel, Marlies
    McDonald, Benjamin D.
    Ishizuka, Isabel E.
    Dent, Alexander L.
    Wilson, Patrick C.
    Jabri, Bana
    Antonopoulos, Dionysios A.
    Bendelac, Albert
    [J]. IMMUNITY, 2015, 43 (03) : 541 - 553
  • [9] Associating microbiome composition with environmental covariates using generalized UniFrac distances
    Chen, Jun
    Bittinger, Kyle
    Charlson, Emily S.
    Hoffmann, Christian
    Lewis, James
    Wu, Gary D.
    Collman, Ronald G.
    Bushman, Frederic D.
    Li, Hongzhe
    [J]. BIOINFORMATICS, 2012, 28 (16) : 2106 - 2113
  • [10] Diard M., 2019, BIORXIV, DOI [10.1101/824821, DOI 10.1101/824821]