IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42469-y.html
   My bibliography  Save this article

SIgA structures bound to Streptococcus pyogenes M4 and human CD89 provide insights into host-pathogen interactions

Author

Listed:
  • Qianqiao Liu

    (University of Illinois Urbana-Champaign)

  • Beth M. Stadtmueller

    (University of Illinois Urbana-Champaign
    University of Illinois Urbana-Champaign
    University of Illinois)

Abstract

Immunoglobulin (Ig) A functions as monomeric IgA in the serum and Secretory (S) IgA in mucosal secretions. Host IgA Fc receptors (FcαRs), including human FcαR1/CD89, mediate IgA effector functions; however, human pathogen Streptococcus pyogenes has evolved surface-protein virulence factors, including M4, that also engage the CD89-binding site on IgA. Despite human mucosa serving as a reservoir for pathogens, SIgA interactions with CD89 and M4 remain poorly understood. Here we report cryo-EM structures of M4-SIgA and CD89-SIgA complexes, which unexpectedly reveal different SIgA-binding stoichiometry for M4 and CD89. Structural data, supporting experiments, and modeling indicate that copies of SIgA bound to S. pyogenes M4 will adopt similar orientations on the bacterium surface and leave one host FcαR binding site open. Results suggest unappreciated functional consequences associated with SIgA binding to host and bacterial FcαRs relevant to understanding host-microbe co-evolution, IgA effector functions and improving the outcomes of group A Streptococcus infection.

Suggested Citation

  • Qianqiao Liu & Beth M. Stadtmueller, 2023. "SIgA structures bound to Streptococcus pyogenes M4 and human CD89 provide insights into host-pathogen interactions," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42469-y
    DOI: 10.1038/s41467-023-42469-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42469-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42469-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Patrick Bryant & Gabriele Pozzati & Arne Elofsson, 2022. "Author Correction: Improved prediction of protein-protein interactions using AlphaFold2," Nature Communications, Nature, vol. 13(1), pages 1-1, December.
    2. Patrick Bryant & Gabriele Pozzati & Arne Elofsson, 2022. "Improved prediction of protein-protein interactions using AlphaFold2," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Lotta Happonen & Simon Hauri & Gabriel Svensson Birkedal & Christofer Karlsson & Therese Neergaard & Hamed Khakzad & Pontus Nordenfelt & Mats Wikström & Magdalena Wisniewska & Lars Björck & Lars Malms, 2019. "A quantitative Streptococcus pyogenes–human protein–protein interaction map reveals localization of opsonizing antibodies," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Andrew B. Herr & Edward R. Ballister & Pamela J. Bjorkman, 2003. "Insights into IgA-mediated immune responses from the crystal structures of human FcαRI and its complex with IgA1-Fc," Nature, Nature, vol. 423(6940), pages 614-620, June.
    5. Kathrin Moor & Médéric Diard & Mikael E. Sellin & Boas Felmy & Sandra Y. Wotzka & Albulena Toska & Erik Bakkeren & Markus Arnoldini & Florence Bansept & Alma Dal Co & Tom Völler & Andrea Minola & Blan, 2017. "High-avidity IgA protects the intestine by enchaining growing bacteria," Nature, Nature, vol. 544(7651), pages 498-502, April.
    6. Pauline Macheboeuf & Cosmo Buffalo & Chi-yu Fu & Annelies S. Zinkernagel & Jason N. Cole & John E. Johnson & Victor Nizet & Partho Ghosh, 2011. "Streptococcal M1 protein constructs a pathological host fibrinogen network," Nature, Nature, vol. 472(7341), pages 64-68, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Marin Matic & Pasquale Miglionico & Manae Tatsumi & Asuka Inoue & Francesco Raimondi, 2023. "GPCRome-wide analysis of G-protein-coupling diversity using a computational biology approach," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Genki Hibi & Taro Shiraishi & Tatsuki Umemura & Kenji Nemoto & Yusuke Ogura & Makoto Nishiyama & Tomohisa Kuzuyama, 2023. "Discovery of type II polyketide synthase-like enzymes for the biosynthesis of cispentacin," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Kazutoshi Tani & Ryo Kanno & Xuan-Cheng Ji & Itsusei Satoh & Yuki Kobayashi & Malgorzata Hall & Long-Jiang Yu & Yukihiro Kimura & Akira Mizoguchi & Bruno M. Humbel & Michael T. Madigan & Zheng-Yu Wang, 2023. "Rhodobacter capsulatus forms a compact crescent-shaped LH1–RC photocomplex," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    4. Andreas Lackner & Michael Müller & Magdalena Gamperl & Delyana Stoeva & Olivia Langmann & Henrieta Papuchova & Elisabeth Roitinger & Gerhard Dürnberger & Richard Imre & Karl Mechtler & Paulina A. Lato, 2023. "The Fgf/Erf/NCoR1/2 repressive axis controls trophoblast cell fate," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Patrick Bryant & Gabriele Pozzati & Wensi Zhu & Aditi Shenoy & Petras Kundrotas & Arne Elofsson, 2022. "Predicting the structure of large protein complexes using AlphaFold and Monte Carlo tree search," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Brooke M. Britton & Remy A. Yovanno & Sara F. Costa & Joshua McCausland & Albert Y. Lau & Jie Xiao & Zach Hensel, 2023. "Conformational changes in the essential E. coli septal cell wall synthesis complex suggest an activation mechanism," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Patrick Bryant & Frank Noé, 2024. "Structure prediction of alternative protein conformations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    8. Christoph Buhlheller & Theo Sagmeister & Christoph Grininger & Nina Gubensäk & Uwe B. Sleytr & Isabel Usón & Tea Pavkov-Keller, 2024. "SymProFold: Structural prediction of symmetrical biological assemblies," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Hélène Bret & Jinmei Gao & Diego Javier Zea & Jessica Andreani & Raphaël Guerois, 2024. "From interaction networks to interfaces, scanning intrinsically disordered regions using AlphaFold2," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Zhiye Guo & Jian Liu & Jeffrey Skolnick & Jianlin Cheng, 2022. "Prediction of inter-chain distance maps of protein complexes with 2D attention-based deep neural networks," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    11. Tânia F. Custódio & Maxime Killer & Dingquan Yu & Virginia Puente & Daniel P. Teufel & Alexander Pautsch & Gisela Schnapp & Marc Grundl & Jan Kosinski & Christian Löw, 2023. "Molecular basis of TASL recruitment by the peptide/histidine transporter 1, PHT1," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    12. Devlina Chakravarty & Joseph W. Schafer & Ethan A. Chen & Joseph F. Thole & Leslie A. Ronish & Myeongsang Lee & Lauren L. Porter, 2024. "AlphaFold predictions of fold-switched conformations are driven by structure memorization," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    13. Cyril Planchais & Luis M. Molinos-Albert & Pierre Rosenbaum & Thierry Hieu & Alexia Kanyavuz & Dominique Clermont & Thierry Prazuck & Laurent Lefrou & Jordan D. Dimitrov & Sophie Hüe & Laurent Hocquel, 2023. "HIV-1 treatment timing shapes the human intestinal memory B-cell repertoire to commensal bacteria," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Arman Izadi & Yasaman Karami & Eleni Bratanis & Sebastian Wrighton & Hamed Khakzad & Maria Nyblom & Berit Olofsson & Lotta Happonen & Di Tang & Martin Sundwall & Magdalena Godzwon & Yashuan Chao & Ale, 2024. "The hinge-engineered IgG1-IgG3 hybrid subclass IgGh47 potently enhances Fc-mediated function of anti-streptococcal and SARS-CoV-2 antibodies," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    15. Alejandro Gomez Toledo & Eleni Bratanis & Erika Velásquez & Sounak Chowdhury & Berit Olofsson & James T. Sorrentino & Christofer Karlsson & Nathan E. Lewis & Jeffrey D. Esko & Mattias Collin & Oonagh , 2023. "Pathogen-driven degradation of endogenous and therapeutic antibodies during streptococcal infections," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Qu Chen & Rajesh Menon & Lesley J. Calder & Pavel Tolar & Peter B. Rosenthal, 2022. "Cryomicroscopy reveals the structural basis for a flexible hinge motion in the immunoglobulin M pentamer," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    17. Jian Sun & Guangchen Zhang & Zhibo Cui & Ximan Kong & Xiaoyu Yu & Rui Gui & Yuqing Han & Zhuan Li & Hong Lang & Yuchen Hua & Xuemin Zhang & Quan Xu & Liang Tang & Zhengjin Xu & Dianrong Ma & Wenfu Che, 2022. "Regain flood adaptation in rice through a 14-3-3 protein OsGF14h," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42469-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.