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Programmable epigenome editing by transient delivery of CRISPR epigenome editor ribonucleoproteins

Author

Listed:
  • Da Xu

    (University of California)

  • Swen Besselink

    (University of California
    Radboud University)

  • Gokul N. Ramadoss

    (Gladstone Institutes)

  • Philip H. Dierks

    (Gladstone Institutes)

  • Justin P. Lubin

    (University of California)

  • Rithu K. Pattali

    (University of California)

  • Jinna I. Brim

    (University of California)

  • Anna E. Christenson

    (University of California)

  • Peter J. Colias

    (University of California)

  • Izaiah J. Ornelas

    (University of California)

  • Carolyn D. Nguyen

    (University of California)

  • Sarah E. Chasins

    (University of California
    Chan Zuckerberg Biohub San Francisco)

  • Bruce R. Conklin

    (Gladstone Institutes
    University of California
    University of California)

  • James K. Nuñez

    (University of California
    Chan Zuckerberg Biohub San Francisco)

Abstract

Programmable epigenome editors modify gene expression in mammalian cells by altering the local chromatin environment at target loci without inducing DNA breaks. However, the large size of CRISPR-based epigenome editors poses a challenge to their broad use in biomedical research and as future therapies. Here, we present Robust ENveloped Delivery of Epigenome-editor Ribonucleoproteins (RENDER) for transiently delivering programmable epigenetic repressors (CRISPRi, DNMT3A-3L-dCas9, CRISPRoff) and activator (TET1-dCas9) as ribonucleoprotein complexes into human cells to modulate gene expression. After rational engineering, we show that RENDER induces durable epigenetic silencing of endogenous genes across various human cell types, including primary T cells. Additionally, we apply RENDER to epigenetically repress endogenous genes in human stem cell-derived neurons, including the reduction of the neurodegenerative disease associated V337M-mutated Tau protein. Together, our RENDER platform advances the delivery of CRISPR-based epigenome editors into human cells, broadening the use of epigenome editing in fundamental research and therapeutic applications.

Suggested Citation

  • Da Xu & Swen Besselink & Gokul N. Ramadoss & Philip H. Dierks & Justin P. Lubin & Rithu K. Pattali & Jinna I. Brim & Anna E. Christenson & Peter J. Colias & Izaiah J. Ornelas & Carolyn D. Nguyen & Sar, 2025. "Programmable epigenome editing by transient delivery of CRISPR epigenome editor ribonucleoproteins," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-63167-x
    DOI: 10.1038/s41467-025-63167-x
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    References listed on IDEAS

    as
    1. Martino Alfredo Cappelluti & Valeria Mollica Poeta & Sara Valsoni & Piergiuseppe Quarato & Simone Merlin & Ivan Merelli & Angelo Lombardo, 2024. "Durable and efficient gene silencing in vivo by hit-and-run epigenome editing," Nature, Nature, vol. 627(8003), pages 416-423, March.
    2. 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.
    3. Philippe E. Mangeot & Valérie Risson & Floriane Fusil & Aline Marnef & Emilie Laurent & Juliana Blin & Virginie Mournetas & Emmanuelle Massouridès & Thibault J. M. Sohier & Antoine Corbin & Fabien Aub, 2019. "Genome editing in primary cells and in vivo using viral-derived Nanoblades loaded with Cas9-sgRNA ribonucleoproteins," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
    5. Grégoire Cullot & Julian Boutin & Jérôme Toutain & Florence Prat & Perrine Pennamen & Caroline Rooryck & Martin Teichmann & Emilie Rousseau & Isabelle Lamrissi-Garcia & Véronique Guyonnet-Duperat & Al, 2019. "CRISPR-Cas9 genome editing induces megabase-scale chromosomal truncations," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    6. Jennifer A. Doudna, 2020. "The promise and challenge of therapeutic genome editing," Nature, Nature, vol. 578(7794), pages 229-236, February.
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