IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50959-w.html
   My bibliography  Save this article

A protein O-GlcNAc glycosyltransferase regulates the antioxidative response in Yersinia pestis

Author

Listed:
  • Shiyang Cao

    (Academy of Military Medical Sciences)

  • Tong Wang

    (Academy of Military Medical Sciences)

  • Yifan Ren

    (Academy of Military Medical Sciences)

  • Gengshan Wu

    (Academy of Military Medical Sciences)

  • Yuan Zhang

    (Academy of Military Medical Sciences)

  • Yafang Tan

    (Academy of Military Medical Sciences)

  • Yazhou Zhou

    (Academy of Military Medical Sciences)

  • Hongyan Chen

    (Academy of Military Medical Sciences)

  • Yu Zhang

    (Academy of Military Medical Sciences)

  • Yajun Song

    (Academy of Military Medical Sciences)

  • Ruifu Yang

    (Academy of Military Medical Sciences)

  • Zongmin Du

    (Academy of Military Medical Sciences)

Abstract

Post-translational addition of O-linked N-acetylglucosamine (O-GlcNAc) to proteins is commonly associated with a variety of stress responses and cellular processes in eukaryotes, but its potential roles in bacteria are unclear. Here, we show that protein HmwC acts as an O-GlcNAc transferase (OGT) responsible for O-GlcNAcylation of multiple proteins in Yersinia pestis, a flea-borne pathogen responsible for plague. We identify 64 O-GlcNAcylated proteins (comprising 65 sites) with differential abundance under conditions mimicking the mammalian host (Mh) and flea vector (Fv) environments. Deletion of hmwC, encoding a putative OGT, structurally distinct from any existing member of the GT41 family, results in reduced O-GlcNAcylation, reduced growth, and alterations in virulence properties and survival under stress. Purified HmwC can modify target proteins in vitro using UDP-GlcNAc as sugar donor. One of the target proteins, OsdY, promotes Y. pestis survival under oxidative stress conditions. Thus, our results support that regulation of antioxidative responses through O-GlcNAcylation may be a conserved process shared by prokaryotes and eukaryotes.

Suggested Citation

  • Shiyang Cao & Tong Wang & Yifan Ren & Gengshan Wu & Yuan Zhang & Yafang Tan & Yazhou Zhou & Hongyan Chen & Yu Zhang & Yajun Song & Ruifu Yang & Zongmin Du, 2024. "A protein O-GlcNAc glycosyltransferase regulates the antioxidative response in Yersinia pestis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50959-w
    DOI: 10.1038/s41467-024-50959-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50959-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-50959-w?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. Michael B. Lazarus & Yunsun Nam & Jiaoyang Jiang & Piotr Sliz & Suzanne Walker, 2011. "Structure of human O-GlcNAc transferase and its complex with a peptide substrate," Nature, Nature, vol. 469(7331), pages 564-567, January.
    2. Jorge E. Galán & Hans Wolf-Watz, 2006. "Protein delivery into eukaryotic cells by type III secretion machines," Nature, Nature, vol. 444(7119), pages 567-573, 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. Lisa M Schechter & Joy C Valenta & David J Schneider & Alan Collmer & Eric Sakk, 2012. "Functional and Computational Analysis of Amino Acid Patterns Predictive of Type III Secretion System Substrates in Pseudomonas syringae," PLOS ONE, Public Library of Science, vol. 7(4), pages 1-13, April.
    2. Ping Lu & Yusong Liu & Maozhou He & Ting Cao & Mengquan Yang & Shutao Qi & Hongtao Yu & Haishan Gao, 2023. "Cryo-EM structure of human O-GlcNAcylation enzyme pair OGT-OGA complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Sara Saleh & Sandra Van Puyvelde & An Staes & Evy Timmerman & Barbara Barbé & Jan Jacobs & Kris Gevaert & Stijn Deborggraeve, 2019. "Salmonella Typhi, Paratyphi A, Enteritidis and Typhimurium core proteomes reveal differentially expressed proteins linked to the cell surface and pathogenicity," PLOS Neglected Tropical Diseases, Public Library of Science, vol. 13(5), pages 1-16, May.
    4. Yejun Wang & Ming'an Sun & Hongxia Bao & Aaron P White, 2013. "T3_MM: A Markov Model Effectively Classifies Bacterial Type III Secretion Signals," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-12, March.
    5. Richard W. Meek & James N. Blaza & Jil A. Busmann & Matthew G. Alteen & David J. Vocadlo & Gideon J. Davies, 2021. "Cryo-EM structure provides insights into the dimer arrangement of the O-linked β-N-acetylglucosamine transferase OGT," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    6. Vishnu Raman & Nele Van Dessel & Christopher L. Hall & Victoria E. Wetherby & Samantha A. Whitney & Emily L. Kolewe & Shoshana M. K. Bloom & Abhinav Sharma & Jeanne A. Hardy & Mathieu Bollen & Aleyde , 2021. "Intracellular delivery of protein drugs with an autonomously lysing bacterial system reduces tumor growth and metastases," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    7. Shivesh Kumar & Yan Wang & Ye Zhou & Lucas Dillard & Fay-Wei Li & Carly A. Sciandra & Ning Sui & Rodolfo Zentella & Emily Zahn & Jeffrey Shabanowitz & Donald F. Hunt & Mario J. Borgnia & Alberto Barte, 2023. "Structure and dynamics of the Arabidopsis O-fucosyltransferase SPINDLY," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Duc T. Huynh & Kalina N. Tsolova & Abigail J. Watson & Sai Kwan Khal & Jordan R. Green & Di Li & Jimin Hu & Erik J. Soderblom & Jen-Tsan Chi & Chantell S. Evans & Michael Boyce, 2023. "O-GlcNAcylation regulates neurofilament-light assembly and function and is perturbed by Charcot-Marie-Tooth disease mutations," Nature Communications, Nature, vol. 14(1), pages 1-17, 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_s41467-024-50959-w. 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.