IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52707-6.html
   My bibliography  Save this article

Programmable editing of primary MicroRNA switches stem cell differentiation and improves tissue regeneration

Author

Listed:
  • Vu Anh Truong

    (National Tsing Hua University)

  • Yu-Han Chang

    (Chang Gung Memorial Hospital
    Chang Gung University)

  • Thuc Quyen Dang

    (National Tsing Hua University)

  • Yi Tu

    (National Taiwan University)

  • Jui Tu

    (National Taiwan University)

  • Chin-Wei Chang

    (National Tsing Hua University)

  • Yi-Hao Chang

    (National Tsing Hua University)

  • Guei-Sheung Liu

    (Royal Victorian Eye and Ear Hospital
    University of Melbourne
    University of Tasmania)

  • Yu-Chen Hu

    (National Tsing Hua University
    National Tsing Hua University)

Abstract

Programmable RNA editing is harnessed for modifying mRNA. Besides mRNA, miRNA also regulates numerous biological activities, but current RNA editors have yet to be exploited for miRNA manipulation. To engineer primary miRNA (pri-miRNA), the miRNA precursor, we present a customizable editor REPRESS (RNA Editing of Pri-miRNA for Efficient Suppression of miRNA) and characterize critical parameters. The optimized REPRESS is distinct from other mRNA editing tools in design rationale, hence enabling editing of pri-miRNAs that are not editable by other RNA editing systems. We edit various pri-miRNAs in different cells including adipose-derived stem cells (ASCs), hence attenuating mature miRNA levels without disturbing host gene expression. We further develop an improved REPRESS (iREPRESS) that enhances and prolongs pri-miR-21 editing for at least 10 days, with minimal perturbation of transcriptome and miRNAome. iREPRESS reprograms ASCs differentiation, promotes in vitro cartilage formation and augments calvarial bone regeneration in rats, thus implicating its potentials for engineering miRNA and applications such as stem cell reprogramming and tissue regeneration.

Suggested Citation

  • Vu Anh Truong & Yu-Han Chang & Thuc Quyen Dang & Yi Tu & Jui Tu & Chin-Wei Chang & Yi-Hao Chang & Guei-Sheung Liu & Yu-Chen Hu, 2024. "Programmable editing of primary MicroRNA switches stem cell differentiation and improves tissue regeneration," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52707-6
    DOI: 10.1038/s41467-024-52707-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52707-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-52707-6?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. Fatwa Adikusuma & Sandra Piltz & Mark A. Corbett & Michelle Turvey & Shaun R. McColl & Karla J. Helbig & Michael R. Beard & James Hughes & Richard T. Pomerantz & Paul Q. Thomas, 2018. "Large deletions induced by Cas9 cleavage," Nature, Nature, vol. 560(7717), pages 8-9, August.
    2. Feiyu Zhao & Tao Zhang & Xiaodi Sun & Xiyun Zhang & Letong Chen & Hejun Wang & Jinze Li & Peng Fan & Liangxue Lai & Tingting Sui & Zhanjun Li, 2023. "A strategy for Cas13 miniaturization based on the structure and AlphaFold," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Baiocchi, Giovanni, 2004. "Using Perl for Statistics: Data Processing and Statistical Computing," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 11(i01).
    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. Jun Huang & David Rowe & Pratima Subedi & Wei Zhang & Tyler Suelter & Barbara Valent & David E. Cook, 2022. "CRISPR-Cas12a induced DNA double-strand breaks are repaired by multiple pathways with different mutation profiles in Magnaporthe oryzae," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Martin Peterka & Nina Akrap & Songyuan Li & Sandra Wimberger & Pei-Pei Hsieh & Dmitrii Degtev & Burcu Bestas & Jack Barr & Stijn Plassche & Patricia Mendoza-Garcia & Saša Šviković & Grzegorz Sienski &, 2022. "Harnessing DSB repair to promote efficient homology-dependent and -independent prime editing," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    3. G. Cullot & J. Boutin & S. Fayet & F. Prat & J. Rosier & D. Cappellen & I. Lamrissi & P. Pennamen & J. Bouron & S. Amintas & C. Thibault & I. Moranvillier & E. Laharanne & J. P. Merlio & V. Guyonnet-D, 2023. "Cell cycle arrest and p53 prevent ON-target megabase-scale rearrangements induced by CRISPR-Cas9," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Jianhang Yin & Kailun Fang & Yanxia Gao & Liqiong Ou & Shaopeng Yuan & Changchang Xin & Weiwei Wu & Wei-wei Wu & Jiaxu Hong & Hui Yang & Jiazhi Hu, 2022. "Safeguarding genome integrity during gene-editing therapy in a mouse model of age-related macular degeneration," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    5. Burcu Bestas & Sandra Wimberger & Dmitrii Degtev & Alexandra Madsen & Antje K. Rottner & Fredrik Karlsson & Sergey Naumenko & Megan Callahan & Julia Liz Touza & Margherita Francescatto & Carl Ivar Möl, 2023. "A Type II-B Cas9 nuclease with minimized off-targets and reduced chromosomal translocations in vivo," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Stamatis Papathanasiou & Styliani Markoulaki & Logan J. Blaine & Mitchell L. Leibowitz & Cheng-Zhong Zhang & Rudolf Jaenisch & David Pellman, 2021. "Whole chromosome loss and genomic instability in mouse embryos after CRISPR-Cas9 genome editing," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
    7. Michael Kosicki & Felicity Allen & Frances Steward & Kärt Tomberg & Yangyang Pan & Allan Bradley, 2022. "Cas9-induced large deletions and small indels are controlled in a convergent fashion," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    8. Ju-Chan Park & Yun-Jeong Kim & Gue-Ho Hwang & Chan Young Kang & Sangsu Bae & Hyuk-Jin Cha, 2024. "Enhancing genome editing in hPSCs through dual inhibition of DNA damage response and repair pathways," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. Dan Liang & Aleksei Mikhalchenko & Hong Ma & Nuria Marti Gutierrez & Tailai Chen & Yeonmi Lee & Sang-Wook Park & Rebecca Tippner-Hedges & Amy Koski & Hayley Darby & Ying Li & Crystal Dyken & Han Zhao , 2023. "Limitations of gene editing assessments in human preimplantation embryos," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Jianli Tao & Qi Wang & Carlos Mendez-Dorantes & Kathleen H. Burns & Roberto Chiarle, 2022. "Frequency and mechanisms of LINE-1 retrotransposon insertions at CRISPR/Cas9 sites," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Jianhang Yin & Rusen Lu & Changchang Xin & Yuhong Wang & Xinyu Ling & Dong Li & Weiwei Zhang & Mengzhu Liu & Wutao Xie & Lingyun Kong & Wen Si & Ping Wei & Bingbing Xiao & Hsiang-Ying Lee & Tao Liu & , 2022. "Cas9 exo-endonuclease eliminates chromosomal translocations during genome editing," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. Sebald A. N. Verkuijl & Estela Gonzalez & Ming Li & Joshua X. D. Ang & Nikolay P. Kandul & Michelle A. E. Anderson & Omar S. Akbari & Michael B. Bonsall & Luke Alphey, 2022. "A CRISPR endonuclease gene drive reveals distinct mechanisms of inheritance bias," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    13. R L Bregman, 2009. "Preemptive expediting to improve project due date performance," Journal of the Operational Research Society, Palgrave Macmillan;The OR Society, vol. 60(1), pages 120-129, January.
    14. Jianli Tao & Daniel E. Bauer & Roberto Chiarle, 2023. "Assessing and advancing the safety of CRISPR-Cas tools: from DNA to RNA editing," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Bregman, Robert L., 2009. "A heuristic procedure for solving the dynamic probabilistic project expediting problem," European Journal of Operational Research, Elsevier, vol. 192(1), pages 125-137, January.
    16. Bert van de Kooij & Alex Kruswick & Haico van Attikum & Michael B. Yaffe, 2022. "Multi-pathway DNA-repair reporters reveal competition between end-joining, single-strand annealing and homologous recombination at Cas9-induced DNA double-strand breaks," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Giovanni Baiocchi, 2009. "PDL: an object-oriented programming environment for econometrics," Journal of Applied Econometrics, John Wiley & Sons, Ltd., vol. 24(5), pages 849-856.
    18. Giovanni Baiocchi, 2007. "Reproducible research in computational economics: guidelines, integrated approaches, and open source software," Computational Economics, Springer;Society for Computational Economics, vol. 30(1), pages 19-40, August.

    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:15:y:2024:i:1:d:10.1038_s41467-024-52707-6. 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.