IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26233-8.html
   My bibliography  Save this article

Coupled protein synthesis and ribosome-guided piRNA processing on mRNAs

Author

Listed:
  • Yu H. Sun

    (University of Rochester Medical Center)

  • Ruoqiao Huiyi Wang

    (University of Rochester Medical Center)

  • Khai Du

    (University of Rochester Medical Center)

  • Jiang Zhu

    (University of Rochester Medical Center)

  • Jihong Zheng

    (Tongji University)

  • Li Huitong Xie

    (University of Rochester Medical Center)

  • Amanda A. Pereira

    (University of Rochester Medical Center)

  • Chao Zhang

    (Tongji University)

  • Emiliano P. Ricci

    (Université de Lyon, ENSL, UCBL, INSERM, CNRS, LBMC)

  • Xin Zhiguo Li

    (University of Rochester Medical Center)

Abstract

PIWI-interacting small RNAs (piRNAs) protect the germline genome and are essential for fertility. piRNAs originate from transposable element (TE) RNAs, long non-coding RNAs, or 3´ untranslated regions (3´UTRs) of protein-coding messenger genes, with the last being the least characterized of the three piRNA classes. Here, we demonstrate that the precursors of 3´UTR piRNAs are full-length mRNAs and that post-termination 80S ribosomes guide piRNA production on 3´UTRs in mice and chickens. At the pachytene stage, when other co-translational RNA surveillance pathways are sequestered, piRNA biogenesis degrades mRNAs right after pioneer rounds of translation and fine-tunes protein production from mRNAs. Although 3´UTR piRNA precursor mRNAs code for distinct proteins in mice and chickens, they all harbor embedded TEs and produce piRNAs that cleave TEs. Altogether, we discover a function of the piRNA pathway in fine-tuning protein production and reveal a conserved piRNA biogenesis mechanism that recognizes translating RNAs in amniotes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26233-8
    DOI: 10.1038/s41467-021-26233-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26233-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-021-26233-8?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. 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.
    2. Jonathan Bohlen & Liza Harbrecht & Saioa Blanco & Katharina Clemm von Hohenberg & Kai Fenzl & Günter Kramer & Bernd Bukau & Aurelio A. Teleman, 2020. "DENR promotes translation reinitiation via ribosome recycling to drive expression of oncogenes including ATF4," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    3. 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.
    4. Peter Refsing Andersen & Laszlo Tirian & Milica Vunjak & Julius Brennecke, 2017. "A heterochromatin-dependent transcription machinery drives piRNA expression," Nature, Nature, vol. 549(7670), pages 54-59, September.
    5. Yu H. Sun & Anqi Wang & Chi Song & Goutham Shankar & Rajesh K. Srivastava & Kin Fai Au & Xin Zhiguo Li, 2021. "Single-molecule long-read sequencing reveals a conserved intact long RNA profile in sperm," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. Christina Ernst & Duncan T. Odom & Claudia Kutter, 2017. "The emergence of piRNAs against transposon invasion to preserve mammalian genome integrity," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    7. Kuniaki Saito & Sachi Inagaki & Toutai Mituyama & Yoshinori Kawamura & Yukiteru Ono & Eri Sakota & Hazuki Kotani & Kiyoshi Asai & Haruhiko Siomi & Mikiko C. Siomi, 2009. "A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila," Nature, Nature, vol. 461(7268), pages 1296-1299, October.
    8. 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.
    9. David J. Young & Sezen Meydan & Nicholas R. Guydosh, 2021. "40S ribosome profiling reveals distinct roles for Tma20/Tma22 (MCT-1/DENR) and Tma64 (eIF2D) in 40S subunit recycling," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    10. Andrew Grimson & Mansi Srivastava & Bryony Fahey & Ben J. Woodcroft & H. Rosaria Chiang & Nicole King & Bernard M. Degnan & Daniel S. Rokhsar & David P. Bartel, 2008. "Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals," Nature, Nature, vol. 455(7217), pages 1193-1197, October.
    11. Mary E. Dickinson & Ann M. Flenniken & Xiao Ji & Lydia Teboul & Michael D. Wong & Jacqueline K. White & Terrence F. Meehan & Wolfgang J. Weninger & Henrik Westerberg & Hibret Adissu & Candice N. Baker, 2016. "High-throughput discovery of novel developmental phenotypes," Nature, Nature, vol. 537(7621), pages 508-514, September.
    12. 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.
    13. Deqiang Ding & Jiali Liu & Uros Midic & Yingjie Wu & Kunzhe Dong & Ashley Melnick & Keith E. Latham & Chen Chen, 2018. "TDRD5 binds piRNA precursors and selectively enhances pachytene piRNA processing in mice," Nature Communications, Nature, vol. 9(1), pages 1-13, 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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. Asmundur Oddsson & Patrick Sulem & Gardar Sveinbjornsson & Gudny A. Arnadottir & Valgerdur Steinthorsdottir & Gisli H. Halldorsson & Bjarni A. Atlason & Gudjon R. Oskarsson & Hannes Helgason & Henriet, 2023. "Deficit of homozygosity among 1.52 million individuals and genetic causes of recessive lethality," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Dafne Ibarra-Morales & Michael Rauer & Piergiuseppe Quarato & Leily Rabbani & Fides Zenk & Mariana Schulte-Sasse & Francesco Cardamone & Alejandro Gomez-Auli & Germano Cecere & Nicola Iovino, 2021. "Histone variant H2A.Z regulates zygotic genome activation," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    7. Katharina Clemm von Hohenberg & Sandra Müller & Sibylle Schleich & Matthias Meister & Jonathan Bohlen & Thomas G. Hofmann & Aurelio A. Teleman, 2022. "Cyclin B/CDK1 and Cyclin A/CDK2 phosphorylate DENR to promote mitotic protein translation and faithful cell division," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Shunya Kaneko & Keita Miyoshi & Kotaro Tomuro & Makoto Terauchi & Ryoya Tanaka & Shu Kondo & Naoki Tani & Kei-Ichiro Ishiguro & Atsushi Toyoda & Azusa Kamikouchi & Hideki Noguchi & Shintaro Iwasaki & , 2024. "Mettl1-dependent m7G tRNA modification is essential for maintaining spermatogenesis and fertility in Drosophila melanogaster," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Danial Pourjafar-Dehkordi & Martin Zacharias, 2021. "Binding-induced functional-domain motions in the Argonaute characterized by adaptive advanced sampling," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-16, November.
    10. Yong Geun Jeon & Hahn Nahmgoong & Jiyoung Oh & Dabin Lee & Dong Wook Kim & Jane Eunsoo Kim & Ye Young Kim & Yul Ji & Ji Seul Han & Sung Min Kim & Jee Hyung Sohn & Won Taek Lee & Sun Won Kim & Jeu Park, 2024. "Ubiquitin ligase RNF20 coordinates sequential adipose thermogenesis with brown and beige fat-specific substrates," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Mary P. LaPierre & Katherine Lawler & Svenja Godbersen & I. Sadaf Farooqi & Markus Stoffel, 2022. "MicroRNA-7 regulates melanocortin circuits involved in mammalian energy homeostasis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Nora-Guadalupe P. Ramirez & Jeon Lee & Yue Zheng & Lianbo Li & Bryce Dennis & Didi Chen & Ashwini Challa & Vicente Planelles & Kenneth D. Westover & Neal M. Alto & Iván D’Orso, 2022. "ADAP1 promotes latent HIV-1 reactivation by selectively tuning KRAS–ERK–AP-1 T cell signaling-transcriptional axis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Myoung Keun Lee & John R Shaffer & Elizabeth J Leslie & Ekaterina Orlova & Jenna C Carlson & Eleanor Feingold & Mary L Marazita & Seth M Weinberg, 2017. "Genome-wide association study of facial morphology reveals novel associations with FREM1 and PARK2," PLOS ONE, Public Library of Science, vol. 12(4), pages 1-13, April.
    14. Joel T. Rämö & Tuomo Kiiskinen & Richard Seist & Kristi Krebs & Masahiro Kanai & Juha Karjalainen & Mitja Kurki & Eija Hämäläinen & Paavo Häppölä & Aki S. Havulinna & Heidi Hautakangas & Reedik Mägi &, 2023. "Genome-wide screen of otosclerosis in population biobanks: 27 loci and shared associations with skeletal structure," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Ramona Weber & Leon Kleemann & Insa Hirschberg & Min-Yi Chung & Eugene Valkov & Cátia Igreja, 2022. "DAP5 enables main ORF translation on mRNAs with structured and uORF-containing 5′ leaders," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Suzanne Vogelezang & Jonathan P Bradfield & Tarunveer S Ahluwalia & John A Curtin & Timo A Lakka & Niels Grarup & Markus Scholz & Peter J van der Most & Claire Monnereau & Evie Stergiakouli & Anni Hei, 2020. "Novel loci for childhood body mass index and shared heritability with adult cardiometabolic traits," PLOS Genetics, Public Library of Science, vol. 16(10), pages 1-26, October.
    17. Peter T. A. Linders & Eveline C. F. Gerretsen & Angel Ashikov & Mari-Anne Vals & Rinse Boer & Natalia H. Revelo & Richard Arts & Melissa Baerenfaenger & Fokje Zijlstra & Karin Huijben & Kimiyo Raymond, 2021. "Congenital disorder of glycosylation caused by starting site-specific variant in syntaxin-5," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    18. Sen Zhao & Hengqiang Zhao & Lina Zhao & Xi Cheng & Zhifa Zheng & Mengfan Wu & Wen Wen & Shengru Wang & Zixiang Zhou & Haibo Xie & Dengfeng Ruan & Qing Li & Xinquan Liu & Chengzhu Ou & Guozhuang Li & Z, 2024. "Unraveling the genetic architecture of congenital vertebral malformation with reference to the developing spine," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    19. William J. Young & Jeffrey Haessler & Jan-Walter Benjamins & Linda Repetto & Jie Yao & Aaron Isaacs & Andrew R. Harper & Julia Ramirez & Sophie Garnier & Stefan Duijvenboden & Antoine R. Baldassari & , 2023. "Genetic architecture of spatial electrical biomarkers for cardiac arrhythmia and relationship with cardiovascular disease," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Bethany N. Radford & Xiang Zhao & Tali Glazer & Malcolm Eaton & Danielle Blackwell & Shuhiba Mohammad & Lucas Daniel Lo Vercio & Jay Devine & Tali Shalom-Barak & Benedikt Hallgrimsson & James C. Cross, 2023. "Defects in placental syncytiotrophoblast cells are a common cause of developmental heart disease," 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:12:y:2021:i:1:d:10.1038_s41467-021-26233-8. 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.