IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28555-7.html
   My bibliography  Save this article

Xrn1 is a deNADding enzyme modulating mitochondrial NAD-capped RNA

Author

Listed:
  • Sunny Sharma

    (Rutgers University)

  • Jun Yang

    (Rutgers University)

  • Ewa Grudzien-Nogalska

    (Rutgers University)

  • Jessica Shivas

    (Rutgers University)

  • Kelvin Y. Kwan

    (Rutgers University)

  • Megerditch Kiledjian

    (Rutgers University)

Abstract

The existence of non-canonical nicotinamide adenine diphosphate (NAD) 5′-end capped RNAs is now well established. Nevertheless, the biological function of this nucleotide metabolite cap remains elusive. Here, we show that the yeast Saccharomyces cerevisiae cytoplasmic 5′-end exoribonuclease Xrn1 is also a NAD cap decapping (deNADding) enzyme that releases intact NAD and subsequently degrades the RNA. The significance of Xrn1 deNADding is evident in a deNADding deficient Xrn1 mutant that predominantly still retains its 5′-monophosphate exonuclease activity. This mutant reveals Xrn1 deNADding is necessary for normal growth on non-fermenting sugar and is involved in modulating mitochondrial NAD-capped RNA levels and may influence intramitochondrial NAD levels. Our findings uncover a contribution of mitochondrial NAD-capped RNAs in overall NAD regulation with the deNADding activity of Xrn1 fulfilling a central role.

Suggested Citation

  • Sunny Sharma & Jun Yang & Ewa Grudzien-Nogalska & Jessica Shivas & Kelvin Y. Kwan & Megerditch Kiledjian, 2022. "Xrn1 is a deNADding enzyme modulating mitochondrial NAD-capped RNA," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28555-7
    DOI: 10.1038/s41467-022-28555-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28555-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28555-7?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. Jeremy G. Bird & Yu Zhang & Yuan Tian & Natalya Panova & Ivan Barvík & Landon Greene & Min Liu & Brian Buckley & Libor Krásný & Jeehiun K. Lee & Craig D. Kaplan & Richard H. Ebright & Bryce E. Nickels, 2016. "The mechanism of RNA 5′ capping with NAD+, NADH and desphospho-CoA," Nature, Nature, vol. 535(7612), pages 444-447, July.
    2. Hana Cahová & Marie-Luise Winz & Katharina Höfer & Gabriele Nübel & Andres Jäschke, 2015. "NAD captureSeq indicates NAD as a bacterial cap for a subset of regulatory RNAs," Nature, Nature, vol. 519(7543), pages 374-377, March.
    3. Yaqing Zhang & David Kuster & Tobias Schmidt & Daniel Kirrmaier & Gabriele Nübel & David Ibberson & Vladimir Benes & Hans Hombauer & Michael Knop & Andres Jäschke, 2020. "Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    4. Won-Ki Huh & James V. Falvo & Luke C. Gerke & Adam S. Carroll & Russell W. Howson & Jonathan S. Weissman & Erin K. O'Shea, 2003. "Global analysis of protein localization in budding yeast," Nature, Nature, vol. 425(6959), pages 686-691, October.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Xufeng Wang & Dongli Yu & Jiancheng Yu & Hao Hu & Runlai Hang & Zachary Amador & Qi Chen & Jijie Chai & Xuemei Chen, 2024. "Toll/interleukin-1 receptor (TIR) domain-containing proteins have NAD-RNA decapping activity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    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. José Vicente Gomes-Filho & Ruth Breuer & Hector Gabriel Morales-Filloy & Nadiia Pozhydaieva & Andreas Borst & Nicole Paczia & Jörg Soppa & Katharina Höfer & Andres Jäschke & Lennart Randau, 2023. "Identification of NAD-RNA species and ADPR-RNA decapping in Archaea," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Louis-François Handfield & Yolanda T Chong & Jibril Simmons & Brenda J Andrews & Alan M Moses, 2013. "Unsupervised Clustering of Subcellular Protein Expression Patterns in High-Throughput Microscopy Images Reveals Protein Complexes and Functional Relationships between Proteins," PLOS Computational Biology, Public Library of Science, vol. 9(6), pages 1-19, June.
    3. Maya Dinur-Mills & Merav Tal & Ophry Pines, 2008. "Dual Targeted Mitochondrial Proteins Are Characterized by Lower MTS Parameters and Total Net Charge," PLOS ONE, Public Library of Science, vol. 3(5), pages 1-8, May.
    4. Verena Kohler & Andreas Kohler & Lisa Larsson Berglund & Xinxin Hao & Sarah Gersing & Axel Imhof & Thomas Nyström & Johanna L. Höög & Martin Ott & Claes Andréasson & Sabrina Büttner, 2024. "Nuclear Hsp104 safeguards the dormant translation machinery during quiescence," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Jian Cui & Jinghua Liu & Yuhua Li & Tieliu Shi, 2011. "Integrative Identification of Arabidopsis Mitochondrial Proteome and Its Function Exploitation through Protein Interaction Network," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-16, January.
    6. Xiaomei Wu & Erli Pang & Kui Lin & Zhen-Ming Pei, 2013. "Improving the Measurement of Semantic Similarity between Gene Ontology Terms and Gene Products: Insights from an Edge- and IC-Based Hybrid Method," PLOS ONE, Public Library of Science, vol. 8(5), pages 1-11, May.
    7. Kiyan Shabestary & Cinzia Klemm & Benedict Carling & James Marshall & Juline Savigny & Marko Storch & Rodrigo Ledesma-Amaro, 2024. "Phenotypic heterogeneity follows a growth-viability tradeoff in response to amino acid identity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Michelle Lindström & Lihua Chen & Shan Jiang & Dan Zhang & Yuan Gao & Ju Zheng & Xinxin Hao & Xiaoxue Yang & Arpitha Kabbinale & Johannes Thoma & Lisa C. Metzger & Deyuan Y. Zhang & Xuefeng Zhu & Huis, 2022. "Lsm7 phase-separated condensates trigger stress granule formation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Alex N Nguyen Ba & Bob Strome & Jun Jie Hua & Jonathan Desmond & Isabelle Gagnon-Arsenault & Eric L Weiss & Christian R Landry & Alan M Moses, 2014. "Detecting Functional Divergence after Gene Duplication through Evolutionary Changes in Posttranslational Regulatory Sequences," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-15, December.
    10. Yosuke Ito & Yuhei Chadani & Tatsuya Niwa & Ayako Yamakawa & Kodai Machida & Hiroaki Imataka & Hideki Taguchi, 2022. "Nascent peptide-induced translation discontinuation in eukaryotes impacts biased amino acid usage in proteomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    11. Oliver M Crook & Aikaterini Geladaki & Daniel J H Nightingale & Owen L Vennard & Kathryn S Lilley & Laurent Gatto & Paul D W Kirk, 2020. "A semi-supervised Bayesian approach for simultaneous protein sub-cellular localisation assignment and novelty detection," PLOS Computational Biology, Public Library of Science, vol. 16(11), pages 1-21, November.
    12. Julia P. Schessner & Vincent Albrecht & Alexandra K. Davies & Pavel Sinitcyn & Georg H. H. Borner, 2023. "Deep and fast label-free Dynamic Organellar Mapping," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Arthur Fischbach & Angela Johns & Kara L. Schneider & Xinxin Hao & Peter Tessarz & Thomas Nyström, 2023. "Artificial Hsp104-mediated systems for re-localizing protein aggregates," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Md. Abdulla Al Mamun & Wei Cao & Shugo Nakamura & Jun-ichi Maruyama, 2023. "Large-scale identification of genes involved in septal pore plugging in multicellular fungi," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Nebojsa Jukic & Alma P. Perrino & Frédéric Humbert & Aurélien Roux & Simon Scheuring, 2022. "Snf7 spirals sense and alter membrane curvature," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. Joke J F A van Vugt & Martijn de Jager & Magdalena Murawska & Alexander Brehm & John van Noort & Colin Logie, 2009. "Multiple Aspects of ATP-Dependent Nucleosome Translocation by RSC and Mi-2 Are Directed by the Underlying DNA Sequence," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-14, July.
    17. Stefan A. Hoffmann & Yizhi Cai, 2024. "Engineering stringent genetic biocontainment of yeast with a protein stability switch," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    18. Rory M Donovan & Jose-Juan Tapia & Devin P Sullivan & James R Faeder & Robert F Murphy & Markus Dittrich & Daniel M Zuckerman, 2016. "Unbiased Rare Event Sampling in Spatial Stochastic Systems Biology Models Using a Weighted Ensemble of Trajectories," PLOS Computational Biology, Public Library of Science, vol. 12(2), pages 1-25, February.
    19. Nicola M. Moloney & Konstantin Barylyuk & Eelco Tromer & Oliver M. Crook & Lisa M. Breckels & Kathryn S. Lilley & Ross F. Waller & Paula MacGregor, 2023. "Mapping diversity in African trypanosomes using high resolution spatial proteomics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Chung-Chi Liao & Yi-Sen Wang & Wen-Chieh Pi & Chun-Hsiung Wang & Yi-Min Wu & Wei-Yi Chen & Kuo-Chiang Hsia, 2023. "Structural convergence endows nuclear transport receptor Kap114p with a transcriptional repressor function toward TATA-binding protein," 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:13:y:2022:i:1:d:10.1038_s41467-022-28555-7. 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.