IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48770-8.html
   My bibliography  Save this article

Binding of Akkermansia muciniphila to mucin is O-glycan specific

Author

Listed:
  • Janneke Elzinga

    (Wageningen University & Research
    Faculty of Health Sciences, University of Copenhagen)

  • Yoshiki Narimatsu

    (Faculty of Health Sciences, University of Copenhagen
    GlycoDisplay ApS)

  • Noortje Haan

    (Faculty of Health Sciences, University of Copenhagen
    Leiden University Medical Center)

  • Henrik Clausen

    (Faculty of Health Sciences, University of Copenhagen)

  • Willem M. Vos

    (Wageningen University & Research
    Faculty of Medicine, University of Helsinki)

  • Hanne L. P. Tytgat

    (Wageningen University & Research
    Nestlé Research)

Abstract

The intestinal anaerobic bacterium Akkermansia muciniphila is specialized in the degradation of mucins, which are heavily O-glycosylated proteins that constitute the major components of the mucus lining the intestine. Despite that adhesion to mucins is considered critical for the persistence of A. muciniphila in the human intestinal tract, our knowledge of how this intestinal symbiont recognizes and binds to mucins is still limited. Here, we first show that the mucin-binding properties of A. muciniphila are independent of environmental oxygen concentrations and not abolished by pasteurization. We then dissected the mucin-binding properties of pasteurized A. muciniphila by use of a recently developed cell-based mucin array that enables display of the tandem repeats of human mucins with distinct O-glycan patterns and structures. We found that A. muciniphila recognizes the unsialylated LacNAc (Galβ1-4GlcNAcβ1-R) disaccharide selectively on core2 and core3 O-glycans. This disaccharide epitope is abundantly found on human colonic mucins capped by sialic acids, and we demonstrated that endogenous A. muciniphila neuraminidase activity can uncover the epitope and promote binding. In summary, our study provides insights into the mucin-binding properties important for colonization of a key mucin-foraging bacterium.

Suggested Citation

  • Janneke Elzinga & Yoshiki Narimatsu & Noortje Haan & Henrik Clausen & Willem M. Vos & Hanne L. P. Tytgat, 2024. "Binding of Akkermansia muciniphila to mucin is O-glycan specific," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48770-8
    DOI: 10.1038/s41467-024-48770-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48770-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48770-8?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. Rebecca Nason & Christian Büll & Andriana Konstantinidi & Lingbo Sun & Zilu Ye & Adnan Halim & Wenjuan Du & Daniel M. Sørensen & Fabien Durbesson & Sanae Furukawa & Ulla Mandel & Hiren J. Joshi & Leo , 2021. "Display of the human mucinome with defined O-glycans by gene engineered cells," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    2. Louise E. Tailford & C. David Owen & John Walshaw & Emmanuelle H. Crost & Jemma Hardy-Goddard & Gwenaelle Le Gall & Willem M. de Vos & Garry L. Taylor & Nathalie Juge, 2015. "Discovery of intramolecular trans-sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    3. Lucy I. Crouch & Marcelo V. Liberato & Paulina A. Urbanowicz & Arnaud Baslé & Christopher A. Lamb & Christopher J. Stewart & Katie Cooke & Mary Doona & Stephanie Needham & Richard R. Brady & Janet E. , 2020. "Prominent members of the human gut microbiota express endo-acting O-glycanases to initiate mucin breakdown," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Louis J. Cohen & Sun M. Han & Pearson Lau & Daniela Guisado & Yupu Liang & Toshiki G. Nakashige & Thamina Ali & David Chiang & Adeeb Rahman & Sean F. Brady, 2022. "Unraveling function and diversity of bacterial lectins in the human microbiome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Bashar Shuoker & Michael J. Pichler & Chunsheng Jin & Hiroka Sakanaka & Haiyang Wu & Ana Martínez Gascueña & Jining Liu & Tine Sofie Nielsen & Jan Holgersson & Eva Nordberg Karlsson & Nathalie Juge & , 2023. "Sialidases and fucosidases of Akkermansia muciniphila are crucial for growth on mucin and nutrient sharing with mucus-associated gut bacteria," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Víctor Taleb & Qinghua Liao & Yoshiki Narimatsu & Ana García-García & Ismael Compañón & Rafael Junqueira Borges & Andrés Manuel González-Ramírez & Francisco Corzana & Henrik Clausen & Carme Rovira & R, 2022. "Structural and mechanistic insights into the cleavage of clustered O-glycan patches-containing glycoproteins by mucinases of the human gut," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    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. Joann Chongsaritsinsuk & Alexandra D. Steigmeyer & Keira E. Mahoney & Mia A. Rosenfeld & Taryn M. Lucas & Courtney M. Smith & Alice Li & Deniz Ince & Fiona L. Kearns & Alexandria S. Battison & Marie A, 2023. "Glycoproteomic landscape and structural dynamics of TIM family immune checkpoints enabled by mucinase SmE," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Bashar Shuoker & Michael J. Pichler & Chunsheng Jin & Hiroka Sakanaka & Haiyang Wu & Ana Martínez Gascueña & Jining Liu & Tine Sofie Nielsen & Jan Holgersson & Eva Nordberg Karlsson & Nathalie Juge & , 2023. "Sialidases and fucosidases of Akkermansia muciniphila are crucial for growth on mucin and nutrient sharing with mucus-associated gut bacteria," Nature Communications, Nature, vol. 14(1), pages 1-16, 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:15:y:2024:i:1:d:10.1038_s41467-024-48770-8. 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.