IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29787-3.html
   My bibliography  Save this article

An evolutionarily conserved stop codon enrichment at the 5′ ends of mammalian piRNAs

Author

Listed:
  • Susanne Bornelöv

    (University of Cambridge, Li Ka Shing Centre)

  • Benjamin Czech

    (University of Cambridge, Li Ka Shing Centre)

  • Gregory J. Hannon

    (University of Cambridge, Li Ka Shing Centre)

Abstract

PIWI-interacting RNAs (piRNAs) are small RNAs required to recognize and silence transposable elements. The 5’ ends of mature piRNAs are defined through cleavage of long precursor transcripts, primarily by Zucchini (Zuc). Zuc-dependent cleavage typically occurs immediately upstream of a uridine. However, Zuc lacks sequence preference in vitro, pointing towards additional unknown specificity factors. Here, we examine murine piRNAs and reveal a strong and specific enrichment of three sequences (UAA, UAG, UGA)—corresponding to stop codons—at piRNA 5’ ends. Stop codon sequences are also enriched immediately after piRNA processing intermediates, reflecting their Zuc-dependent tail-to-head arrangement. Further analyses reveal that a Zuc in vivo cleavage preference at four sequences (UAA, UAG, UGA, UAC) promotes 5’ end stop codons. This observation is conserved across mammals and possibly further. Our work provides new insights into Zuc-dependent cleavage and may point to a previously unrecognized connection between piRNA biogenesis and the translational machinery.

Suggested Citation

  • Susanne Bornelöv & Benjamin Czech & Gregory J. Hannon, 2022. "An evolutionarily conserved stop codon enrichment at the 5′ ends of mammalian piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29787-3
    DOI: 10.1038/s41467-022-29787-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29787-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29787-3?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. Chad B. Stein & Pavol Genzor & Sanga Mitra & Alexandra R. Elchert & Jonathan J. Ipsaro & Leif Benner & Sushil Sobti & Yijun Su & Molly Hammell & Leemor Joshua-Tor & Astrid D. Haase, 2019. "Decoding the 5′ nucleotide bias of PIWI-interacting RNAs," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    2. Angélique Girard & Ravi Sachidanandam & Gregory J. Hannon & Michelle A. Carmell, 2006. "A germline-specific class of small RNAs binds mammalian Piwi proteins," Nature, Nature, vol. 442(7099), pages 199-202, July.
    3. Rippei Hayashi & Jakob Schnabl & Dominik Handler & Fabio Mohn & Stefan L. Ameres & Julius Brennecke, 2016. "Genetic and mechanistic diversity of piRNA 3′-end formation," Nature, Nature, vol. 539(7630), pages 588-592, November.
    4. Jonathan J. Ipsaro & Astrid D. Haase & Simon R. Knott & Leemor Joshua-Tor & Gregory J. Hannon, 2012. "The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis," Nature, Nature, vol. 491(7423), pages 279-283, November.
    5. Deqiang Ding & Jiali Liu & Kunzhe Dong & Uros Midic & Rex A. Hess & Huirong Xie & Elena Y. Demireva & Chen Chen, 2017. "PNLDC1 is essential for piRNA 3′ end trimming and transposon silencing during spermatogenesis in mice," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    6. Hiroshi Nishimasu & Hirotsugu Ishizu & Kuniaki Saito & Satoshi Fukuhara & Miharu K. Kamatani & Luc Bonnefond & Naoki Matsumoto & Tomohiro Nishizawa & Keita Nakanaga & Junken Aoki & Ryuichiro Ishitani , 2012. "Structure and function of Zucchini endoribonuclease in piRNA biogenesis," Nature, Nature, vol. 491(7423), pages 284-287, November.
    7. Meetali Singh & Eric Cornes & Blaise Li & Piergiuseppe Quarato & Loan Bourdon & Florent Dingli & Damarys Loew & Simone Proccacia & Germano Cecere, 2021. "Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    8. Natsuko Izumi & Keisuke Shoji & Yutaka Suzuki & Susumu Katsuma & Yukihide Tomari, 2020. "Zucchini consensus motifs determine the mechanism of pre-piRNA production," Nature, Nature, vol. 578(7794), pages 311-316, February.
    9. James S. Parker & S. Mark Roe & David Barford, 2005. "Structural insights into mRNA recognition from a PIWI domain–siRNA guide complex," Nature, Nature, vol. 434(7033), pages 663-666, March.
    10. Alexei Aravin & Dimos Gaidatzis & Sébastien Pfeffer & Mariana Lagos-Quintana & Pablo Landgraf & Nicola Iovino & Patricia Morris & Michael J. Brownstein & Satomi Kuramochi-Miyagawa & Toru Nakano & Minc, 2006. "A novel class of small RNAs bind to MILI protein in mouse testes," Nature, Nature, vol. 442(7099), pages 203-207, July.
    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. Birgit Stallmeyer & Clara Bühlmann & Rytis Stakaitis & Ann-Kristin Dicke & Farah Ghieh & Luisa Meier & Ansgar Zoch & David MacKenzie MacLeod & Johanna Steingröver & Özlem Okutman & Daniela Fietz & Adr, 2024. "Inherited defects of piRNA biogenesis cause transposon de-repression, impaired spermatogenesis, and human male infertility," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Yu H. Sun & Ruoqiao Huiyi Wang & Khai Du & Jiang Zhu & Jihong Zheng & Li Huitong Xie & Amanda A. Pereira & Chao Zhang & Emiliano P. Ricci & Xin Zhiguo Li, 2021. "Coupled protein synthesis and ribosome-guided piRNA processing on mRNAs," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Liina Nagirnaja & Alexandra M. Lopes & Wu-Lin Charng & Brian Miller & Rytis Stakaitis & Ieva Golubickaite & Alexandra Stendahl & Tianpengcheng Luan & Corinna Friedrich & Eisa Mahyari & Eloise Fadial &, 2022. "Diverse monogenic subforms of human spermatogenic failure," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Ariane Lismer & Sarah Kimmins, 2023. "Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    5. Xiaolong Lv & Wen Xiao & Yana Lai & Zhaozhen Zhang & Hongdao Zhang & Chen Qiu & Li Hou & Qin Chen & Duanduan Wang & Yun Gao & Yuanyuan Song & Xinjia Shui & Qinghua Chen & Ruixin Qin & Shuang Liang & W, 2023. "The non-redundant functions of PIWI family proteins in gametogenesis in golden hamsters," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Huan Wei & Jie Gao & Di-Hang Lin & Ruirong Geng & Jiaoyang Liao & Tian-Yu Huang & Guanyi Shang & Jiongjie Jing & Zong-Wei Fan & Duo Pan & Zi-Qi Yin & Tianming Li & Xinyu Liu & Shuang Zhao & Chen Chen , 2024. "piRNA loading triggers MIWI translocation from the intermitochondrial cement to chromatoid body during mouse spermatogenesis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Wenjun Chen & Jordan S. Brown & Tao He & Wei-Sheng Wu & Shikui Tu & Zhiping Weng & Donglei Zhang & Heng-Chi Lee, 2022. "GLH/VASA helicases promote germ granule formation to ensure the fidelity of piRNA-mediated transcriptome surveillance," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Hejin Lai & Ning Feng & Qiwei Zhai, 2023. "Discovery of the major 15–30 nt mammalian small RNAs, their biogenesis and function," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Shihui Chen & Carolyn M. Phillips, 2024. "HRDE-2 drives small RNA specificity for the nuclear Argonaute protein HRDE-1," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Maxim V. Zagoskin & Jianbin Wang & Ashley T. Neff & Giovana M. B. Veronezi & Richard E. Davis, 2022. "Small RNA pathways in the nematode Ascaris in the absence of piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    11. Gangming Zhang & Chunwei Zheng & Yue-he Ding & Craig Mello, 2024. "Casein kinase II promotes piRNA production through direct phosphorylation of USTC component TOFU-4," Nature Communications, Nature, vol. 15(1), pages 1-11, 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_s41467-022-29787-3. 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.