IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31205-7.html
   My bibliography  Save this article

Cell surface glycan engineering reveals that matriglycan alone can recapitulate dystroglycan binding and function

Author

Listed:
  • M. Osman Sheikh

    (University of Georgia)

  • Chantelle J. Capicciotti

    (University of Georgia
    Queen’s University)

  • Lin Liu

    (University of Georgia)

  • Jeremy Praissman

    (University of Georgia)

  • Dahai Ding

    (University of Georgia
    University of Georgia)

  • Daniel G. Mead

    (University of Georgia)

  • Melinda A. Brindley

    (University of Georgia)

  • Tobias Willer

    (The University of Iowa
    Roy J. and Lucille A. Carver College of Medicine, The University of Iowa)

  • Kevin P. Campbell

    (The University of Iowa
    Roy J. and Lucille A. Carver College of Medicine, The University of Iowa)

  • Kelley W. Moremen

    (University of Georgia
    University of Georgia)

  • Lance Wells

    (University of Georgia
    University of Georgia)

  • Geert-Jan Boons

    (University of Georgia
    University of Georgia
    Utrecht University)

Abstract

α-Dystroglycan (α-DG) is uniquely modified on O-mannose sites by a repeating disaccharide (-Xylα1,3-GlcAβ1,3-)n termed matriglycan, which is a receptor for laminin-G domain-containing proteins and employed by old-world arenaviruses for infection. Using chemoenzymatically synthesized matriglycans printed as a microarray, we demonstrate length-dependent binding to Laminin, Lassa virus GP1, and the clinically-important antibody IIH6. Utilizing an enzymatic engineering approach, an N-linked glycoprotein was converted into a IIH6-positive Laminin-binding glycoprotein. Engineering of the surface of cells deficient for either α-DG or O-mannosylation with matriglycans of sufficient length recovers infection with a Lassa-pseudovirus. Finally, free matriglycan in a dose and length dependent manner inhibits viral infection of wildtype cells. These results indicate that matriglycan alone is necessary and sufficient for IIH6 staining, Laminin and LASV GP1 binding, and Lassa-pseudovirus infection and support a model in which it is a tunable receptor for which increasing chain length enhances ligand-binding capacity.

Suggested Citation

  • M. Osman Sheikh & Chantelle J. Capicciotti & Lin Liu & Jeremy Praissman & Dahai Ding & Daniel G. Mead & Melinda A. Brindley & Tobias Willer & Kevin P. Campbell & Kelley W. Moremen & Lance Wells & Geer, 2022. "Cell surface glycan engineering reveals that matriglycan alone can recapitulate dystroglycan binding and function," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31205-7
    DOI: 10.1038/s41467-022-31205-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31205-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31205-7?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. Isabelle Gerin & Benoît Ury & Isabelle Breloy & Céline Bouchet-Seraphin & Jennifer Bolsée & Mathias Halbout & Julie Graff & Didier Vertommen & Giulio G. Muccioli & Nathalie Seta & Jean-Marie Cuisset &, 2016. "ISPD produces CDP-ribitol used by FKTN and FKRP to transfer ribitol phosphate onto α-dystroglycan," Nature Communications, Nature, vol. 7(1), pages 1-15, September.
    2. Michael Katz & Jonathan Weinstein & Maayan Eilon-Ashkenazy & Katrin Gehring & Hadas Cohen-Dvashi & Nadav Elad & Sarel J. Fleishman & Ron Diskin, 2022. "Structure and receptor recognition by the Lassa virus spike complex," Nature, Nature, vol. 603(7899), pages 174-179, March.
    3. Daniel E. Michele & Rita Barresi & Motoi Kanagawa & Fumiaki Saito & Ronald D. Cohn & Jakob S. Satz & James Dollar & Ichizo Nishino & Richard I. Kelley & Hannu Somer & Volker Straub & Katherine D. Math, 2002. "Post-translational disruption of dystroglycan–ligand interactions in congenital muscular dystrophies," Nature, Nature, vol. 418(6896), pages 417-421, July.
    4. Matthew M. Goddeeris & Biming Wu & David Venzke & Takako Yoshida-Moriguchi & Fumiaki Saito & Kiichiro Matsumura & Steven A. Moore & Kevin P. Campbell, 2013. "LARGE glycans on dystroglycan function as a tunable matrix scaffold to prevent dystrophy," Nature, Nature, vol. 503(7474), pages 136-140, November.
    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. Jia-Ru Wei & Zhao-Zhe Hao & Chuan Xu & Mengyao Huang & Lei Tang & Nana Xu & Ruifeng Liu & Yuhui Shen & Sarah A. Teichmann & Zhichao Miao & Sheng Liu, 2022. "Identification of visual cortex cell types and species differences using single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    2. Maayan Eilon-Ashkenazy & Hadas Cohen-Dvashi & Sarah Borni & Ron Shaked & Rivka Calinsky & Yaakov Levy & Ron Diskin, 2024. "The structure of the Lujo virus spike complex," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    3. Hideki Tokuoka & Rieko Imae & Hitomi Nakashima & Hiroshi Manya & Chiaki Masuda & Shunsuke Hoshino & Kazuhiro Kobayashi & Dirk J. Lefeber & Riki Matsumoto & Takashi Okada & Tamao Endo & Motoi Kanagawa , 2022. "CDP-ribitol prodrug treatment ameliorates ISPD-deficient muscular dystrophy mouse model," Nature Communications, Nature, vol. 13(1), pages 1-13, 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:13:y:2022:i:1:d:10.1038_s41467-022-31205-7. 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.