IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-59656-8.html
   My bibliography  Save this article

H/ACA snR30 snoRNP guides independent 18S rRNA subdomain formation

Author

Listed:
  • Paulina Fischer

    (Heidelberg University)

  • Matthias Thoms

    (University of Munich)

  • Benjamin Lau

    (Heidelberg University
    European Molecular Biology Laboratory (EMBL))

  • Timo Denk

    (University of Munich)

  • Maria Kuvshinova

    (Heidelberg University)

  • Otto Berninghausen

    (University of Munich)

  • Dirk Flemming

    (Heidelberg University)

  • Ed Hurt

    (Heidelberg University)

  • Roland Beckmann

    (University of Munich)

Abstract

Ribosome biogenesis follows a cascade of pre-rRNA folding and processing steps, coordinated with ribosomal protein incorporation. Nucleolar 90S pre-ribosomes are well-described stable intermediates, composed of pre-18S rRNA, ribosomal S-proteins, U3 snoRNA, and ~70 assembly factors. However, how numerous snoRNAs control pre-rRNA modification and folding during early maturation events remains unclear. We identify snR30 (human U17), the only essential H/ACA snoRNA in yeast, which binds with Cbf5-Gar1-Nop10-Nhp2 to a pre-18S rRNA subdomain containing platform helices and ES6 of the 40S central domain. Integration into the 90S is blocked by RNA hybridization with snR30. The snoRNP complex coordinates the recruitment of early assembly factors Krr1-Utp23-Kri1 and ribosomal proteins uS11-uS15, enabling isolated subdomain assembly. Krr1-dependent release of snR30 culminates in integration of the platform into the 90S. Our study reveals the essential role of snR30 in chaperoning central domain formation as a discrete assembly unit externalized from the pre-ribosomal core.

Suggested Citation

  • Paulina Fischer & Matthias Thoms & Benjamin Lau & Timo Denk & Maria Kuvshinova & Otto Berninghausen & Dirk Flemming & Ed Hurt & Roland Beckmann, 2025. "H/ACA snR30 snoRNP guides independent 18S rRNA subdomain formation," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-59656-8
    DOI: 10.1038/s41467-025-59656-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-59656-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-59656-8?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. Mirjam Hunziker & Jonas Barandun & Elisabeth Petfalski & Dongyan Tan & Clémentine Delan-Forino & Kelly R. Molloy & Kelly H. Kim & Hywel Dunn-Davies & Yi Shi & Malik Chaker-Margot & Brian T. Chait & Th, 2016. "UtpA and UtpB chaperone nascent pre-ribosomal RNA and U3 snoRNA to initiate eukaryotic ribosome assembly," Nature Communications, Nature, vol. 7(1), pages 1-10, November.
    2. Shan Wu & Beril Tutuncuoglu & Kaige Yan & Hailey Brown & Yixiao Zhang & Dan Tan & Michael Gamalinda & Yi Yuan & Zhifei Li & Jelena Jakovljevic & Chengying Ma & Jianlin Lei & Meng-Qiu Dong & John L. Wo, 2016. "Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes," Nature, Nature, vol. 534(7605), pages 133-137, June.
    3. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    4. Baocheng Liu & Yao He & Yaqiang Wang & He Song & Z. Hong Zhou & Juli Feigon, 2022. "Structure of active human telomerase with telomere shelterin protein TPP1," Nature, Nature, vol. 604(7906), pages 578-583, April.
    5. Miriam Sturm & Jingdong Cheng & Jochen Baßler & Roland Beckmann & Ed Hurt, 2017. "Interdependent action of KH domain proteins Krr1 and Dim2 drive the 40S platform assembly," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    6. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    7. George E. Ghanim & Adam J. Fountain & Anne-Marie M. Roon & Ramya Rangan & Rhiju Das & Kathleen Collins & Thi Hoang Duong Nguyen, 2021. "Structure of human telomerase holoenzyme with bound telomeric DNA," Nature, Nature, vol. 593(7859), pages 449-453, May.
    8. Ling Li & Keqiong Ye, 2006. "Crystal structure of an H/ACA box ribonucleoprotein particle," Nature, Nature, vol. 443(7109), pages 302-307, September.
    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. George E. Ghanim & Zala Sekne & Sebastian Balch & Anne-Marie M. van Roon & Thi Hoang Duong Nguyen, 2024. "2.7 Å cryo-EM structure of human telomerase H/ACA ribonucleoprotein," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. KeHuan K. Edmonds & Max E. Wilkinson & Daniel Strebinger & Hongyu Chen & Blake Lash & Clarissa C. Schaefer & Shiyou Zhu & Dangliang Liu & Shai Zilberzwige-Tal & Alim Ladha & Michelle L. Walsh & Chris , 2025. "Structure and biochemistry-guided engineering of an all-RNA system for DNA insertion with R2 retrotransposons," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    3. Sharmishtha Musalgaonkar & James N. Yelland & Ruta Chitale & Shilpa Rao & Hakan Ozadam & David W. Taylor & Can Cenik & Arlen W. Johnson, 2025. "The assembly factor Reh1 is released from the ribosome during its initial round of translation," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    4. Kamil Sekulski & Victor Emmanuel Cruz & Christine S. Weirich & Jan P. Erzberger, 2023. "rRNA methylation by Spb1 regulates the GTPase activity of Nog2 during 60S ribosomal subunit assembly," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. Ye Yuan & Lei Chen & Kexu Song & Miaomiao Cheng & Ling Fang & Lingfei Kong & Lanlan Yu & Ruonan Wang & Zhendong Fu & Minmin Sun & Qian Wang & Chengjun Cui & Haojue Wang & Jiuyang He & Xiaonan Wang & Y, 2024. "Stable peptide-assembled nanozyme mimicking dual antifungal actions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Ivica Odorčić & Mohamed Belal Hamed & Sam Lismont & Lucía Chávez-Gutiérrez & Rouslan G. Efremov, 2024. "Apo and Aβ46-bound γ-secretase structures provide insights into amyloid-β processing by the APH-1B isoform," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Pantelis Livanos & Choy Kriechbaum & Sophia Remers & Arvid Herrmann & Sabine Müller, 2025. "Kinesin-12 POK2 polarization is a prerequisite for a fully functional division site and aids cell plate positioning," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    8. Surabhi Kokane & Ashutosh Gulati & Pascal F. Meier & Rei Matsuoka & Tanadet Pipatpolkai & Giuseppe Albano & Tin Manh Ho & Lucie Delemotte & Daniel Fuster & David Drew, 2025. "PIP2-mediated oligomerization of the endosomal sodium/proton exchanger NHE9," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    9. Justin Riper & Arleth O. Martinez-Claros & Lie Wang & Hannah E. Schneiderman & Sweta Maheshwari & Monica C. Pillon, 2025. "CryoEM structure of the SLFN14 endoribonuclease reveals insight into RNA binding and cleavage," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    10. Stella Vitt & Simone Prinz & Martin Eisinger & Ulrich Ermler & Wolfgang Buckel, 2022. "Purification and structural characterization of the Na+-translocating ferredoxin: NAD+ reductase (Rnf) complex of Clostridium tetanomorphum," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Pierre Azoulay & Joshua Krieger & Abhishek Nagaraj, 2024. "Old Moats for New Models: Openness, Control, and Competition in Generative Artificial Intelligence," NBER Chapters, in: Entrepreneurship and Innovation Policy and the Economy, volume 4, pages 7-46, National Bureau of Economic Research, Inc.
    12. Riya Shah & Thomas C. Panagiotou & Gregory B. Cole & Trevor F. Moraes & Brigitte D. Lavoie & Christopher A. McCulloch & Andrew Wilde, 2024. "The DIAPH3 linker specifies a β-actin network that maintains RhoA and Myosin-II at the cytokinetic furrow," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Yashan Yang & Qianqian Shao & Mingcheng Guo & Lin Han & Xinyue Zhao & Aohan Wang & Xiangyun Li & Bo Wang & Ji-An Pan & Zhenguo Chen & Andrei Fokine & Lei Sun & Qianglin Fang, 2024. "Capsid structure of bacteriophage ΦKZ provides insights into assembly and stabilization of jumbo phages," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    14. Xin Yong & Guowen Jia & Qin Yang & Chunzhuang Zhou & Sitao Zhang & Huaqing Deng & Daniel D. Billadeau & Zhaoming Su & Da Jia, 2025. "Cryo-EM structure of the BLOC-3 complex provides insights into the pathogenesis of Hermansky-Pudlak syndrome," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    15. Bret M. Boyd & Ian James & Kevin P. Johnson & Robert B. Weiss & Sarah E. Bush & Dale H. Clayton & Colin Dale, 2024. "Stochasticity, determinism, and contingency shape genome evolution of endosymbiotic bacteria," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    16. Jun-Yu Si & Yuan-Mei Chen & Ye-Hui Sun & Meng-Xue Gu & Mei-Ling Huang & Lu-Lu Shi & Xiao Yu & Xiao Yang & Qing Xiong & Cheng-Bao Ma & Peng Liu & Zheng-Li Shi & Huan Yan, 2024. "Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Deyun Qiu & Jinxin V. Pei & James E. O. Rosling & Vandana Thathy & Dongdi Li & Yi Xue & John D. Tanner & Jocelyn Sietsma Penington & Yi Tong Vincent Aw & Jessica Yi Han Aw & Guoyue Xu & Abhai K. Tripa, 2022. "A G358S mutation in the Plasmodium falciparum Na+ pump PfATP4 confers clinically-relevant resistance to cipargamin," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    18. Shuo-Shuo Liu & Tian-Xia Jiang & Fan Bu & Ji-Lan Zhao & Guang-Fei Wang & Guo-Heng Yang & Jie-Yan Kong & Yun-Fan Qie & Pei Wen & Li-Bin Fan & Ning-Ning Li & Ning Gao & Xiao-Bo Qiu, 2024. "Molecular mechanisms underlying the BIRC6-mediated regulation of apoptosis and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Ahrum Son & Hyunsoo Kim & Jolene K. Diedrich & Casimir Bamberger & Daniel B. McClatchy & Stuart A. Lipton & John R. Yates, 2024. "Using in vivo intact structure for system-wide quantitative analysis of changes in proteins," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    20. Weizhu Huang & Nan Jin & Jia Guo & Cangsong Shen & Chanjuan Xu & Kun Xi & Léo Bonhomme & Robert B. Quast & Dan-Dan Shen & Jiao Qin & Yi-Ru Liu & Yuxuan Song & Yang Gao & Emmanuel Margeat & Philippe Ro, 2024. "Structural basis of orientated asymmetry in a mGlu heterodimer," Nature Communications, Nature, vol. 15(1), pages 1-15, 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:16:y:2025:i:1:d:10.1038_s41467-025-59656-8. 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.