IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31968-z.html
   My bibliography  Save this article

A comprehensive thermodynamic model for RNA binding by the Saccharomyces cerevisiae Pumilio protein PUF4

Author

Listed:
  • Christoph Sadée

    (Stanford University School of Medicine)

  • Lauren D. Hagler

    (Stanford University School of Medicine)

  • Winston R. Becker

    (Stanford University School of Medicine)

  • Inga Jarmoskaite

    (Stanford University School of Medicine
    Stanford University School of Medicine)

  • Pavanapuresan P. Vaidyanathan

    (Stanford University School of Medicine
    Protillion Biosciences)

  • Sarah K. Denny

    (Stanford University School of Medicine
    Scribe Therapeutics)

  • William J. Greenleaf

    (Stanford University School of Medicine
    Stanford University
    Chan Zuckerberg Biohub)

  • Daniel Herschlag

    (Stanford University School of Medicine
    Stanford University
    Stanford University)

Abstract

Genomic methods have been valuable for identifying RNA-binding proteins (RBPs) and the genes, pathways, and processes they regulate. Nevertheless, standard motif descriptions cannot be used to predict all RNA targets or test quantitative models for cellular interactions and regulation. We present a complete thermodynamic model for RNA binding to the S. cerevisiae Pumilio protein PUF4 derived from direct binding data for 6180 RNAs measured using the RNA on a massively parallel array (RNA-MaP) platform. The PUF4 model is highly similar to that of the related RBPs, human PUM2 and PUM1, with one marked exception: a single favorable site of base flipping for PUF4, such that PUF4 preferentially binds to a non-contiguous series of residues. These results are foundational for developing and testing cellular models of RNA-RBP interactions and function, for engineering RBPs, for understanding the biophysical nature of RBP binding and the evolutionary landscape of RNAs and RBPs.

Suggested Citation

  • Christoph Sadée & Lauren D. Hagler & Winston R. Becker & Inga Jarmoskaite & Pavanapuresan P. Vaidyanathan & Sarah K. Denny & William J. Greenleaf & Daniel Herschlag, 2022. "A comprehensive thermodynamic model for RNA binding by the Saccharomyces cerevisiae Pumilio protein PUF4," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31968-z
    DOI: 10.1038/s41467-022-31968-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31968-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31968-z?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. Beilin Zhang & Maria Gallegos & Alessandro Puoti & Eileen Durkin & Stanley Fields & Judith Kimble & Marvin P. Wickens, 1997. "A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line," Nature, Nature, vol. 390(6659), pages 477-484, December.
    2. Debashish Ray & Hilal Kazan & Kate B. Cook & Matthew T. Weirauch & Hamed S. Najafabadi & Xiao Li & Serge Gueroussov & Mihai Albu & Hong Zheng & Ally Yang & Hong Na & Manuel Irimia & Leah H. Matzat & R, 2013. "A compendium of RNA-binding motifs for decoding gene regulation," Nature, Nature, vol. 499(7457), pages 172-177, 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. Xuan Ye & Wen Yang & Soon Yi & Yanan Zhao & Gabriele Varani & Eckhard Jankowsky & Fan Yang, 2023. "Two distinct binding modes provide the RNA-binding protein RbFox with extraordinary sequence specificity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Miquel Anglada-Girotto & Ludovica Ciampi & Sophie Bonnal & Sarah A. Head & Samuel Miravet-Verde & Luis Serrano, 2024. "In silico RNA isoform screening to identify potential cancer driver exons with therapeutic applications," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Haili Shao & Jipeng Huang & Hui Wang & Guolei Wang & Xu Yang & Mei Cheng & Changjie Sun & Li Zou & Qin Yang & Dandan Zhang & Zhen Liu & Xuelong Jiang & Lei Shi & Peng Shi & Baowei Han & Baowei Jiao, 2024. "Fused in sarcoma (FUS) inhibits milk production efficiency in mammals," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Siddharth Sethi & David Zhang & Sebastian Guelfi & Zhongbo Chen & Sonia Garcia-Ruiz & Emmanuel O. Olagbaju & Mina Ryten & Harpreet Saini & Juan A. Botia, 2022. "Leveraging omic features with F3UTER enables identification of unannotated 3’UTRs for synaptic genes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Kenzui Taniue & Anzu Sugawara & Chao Zeng & Han Han & Xinyue Gao & Yuki Shimoura & Atsuko Nakanishi Ozeki & Rena Onoguchi-Mizutani & Masahide Seki & Yutaka Suzuki & Michiaki Hamada & Nobuyoshi Akimits, 2024. "The MTR4/hnRNPK complex surveils aberrant polyadenylated RNAs with multiple exons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Diane Lefaudeux & Supriya Sen & Kevin Jiang & Alexander Hoffmann, 2022. "Kinetics of mRNA nuclear export regulate innate immune response gene expression," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Aidan M. Fenix & Yuichiro Miyaoka & Alessandro Bertero & Steven M. Blue & Matthew J. Spindler & Kenneth K. B. Tan & Juan A. Perez-Bermejo & Amanda H. Chan & Steven J. Mayerl & Trieu D. Nguyen & Caitli, 2021. "Gain-of-function cardiomyopathic mutations in RBM20 rewire splicing regulation and re-distribute ribonucleoprotein granules within processing bodies," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    8. Chen Qiu & Zihan Zhang & Robert N. Wine & Zachary T. Campbell & Jun Zhang & Traci M. Tanaka Hall, 2023. "Intra- and inter-molecular regulation by intrinsically-disordered regions governs PUF protein RNA binding," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Ariel Madrigal & Tianyuan Lu & Larisa M. Soto & Hamed S. Najafabadi, 2024. "A unified model for interpretable latent embedding of multi-sample, multi-condition single-cell data," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Ulrike Zinnall & Miha Milek & Igor Minia & Carlos H. Vieira-Vieira & Simon Müller & Guido Mastrobuoni & Orsalia-Georgia Hazapis & Simone Giudice & David Schwefel & Nadine Bley & Franka Voigt & Jeffrey, 2022. "HDLBP binds ER-targeted mRNAs by multivalent interactions to promote protein synthesis of transmembrane and secreted proteins," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    11. Seungjae Lee & Yen-Chung Chen & Austin E. Gillen & J. Matthew Taliaferro & Bart Deplancke & Hongjie Li & Eric C. Lai, 2022. "Diverse cell-specific patterns of alternative polyadenylation in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Huijuan Feng & Xiang-Jun Lu & Suvrajit Maji & Linxi Liu & Dmytro Ustianenko & Noam D. Rudnick & Chaolin Zhang, 2024. "Structure-based prediction and characterization of photo-crosslinking in native protein–RNA complexes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    13. Deivid C. Rodrigues & Marat Mufteev & Kyoko E. Yuki & Ashrut Narula & Wei Wei & Alina Piekna & Jiajie Liu & Peter Pasceri & Olivia S. Rissland & Michael D. Wilson & James Ellis, 2023. "Buffering of transcription rate by mRNA half-life is a conserved feature of Rett syndrome models," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. Seisuke Yamashita & Kozo Tomita, 2023. "Mechanism of U6 snRNA oligouridylation by human TUT1," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    15. Komal Soni & Pravin Kumar Ankush Jagtap & Santiago Martínez-Lumbreras & Sophie Bonnal & Arie Geerlof & Ralf Stehle & Bernd Simon & Juan Valcárcel & Michael Sattler, 2023. "Structural basis for specific RNA recognition by the alternative splicing factor RBM5," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Rebeccah K. Stewart & Patrick Nguyen & Alain Laederach & Pelin C. Volkan & Jessica K. Sawyer & Donald T. Fox, 2024. "Orb2 enables rare-codon-enriched mRNA expression during Drosophila neuron differentiation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    17. Maya Ron & Igor Ulitsky, 2022. "Context-specific effects of sequence elements on subcellular localization of linear and circular RNAs," Nature Communications, Nature, vol. 13(1), pages 1-13, 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_s41467-022-31968-z. 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.