Spatiotemporal, optogenetic control of gene expression in organoids.


Journal

Nature methods
ISSN: 1548-7105
Titre abrégé: Nat Methods
Pays: United States
ID NLM: 101215604

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 21 04 2023
accepted: 25 07 2023
medline: 26 10 2023
pubmed: 22 9 2023
entrez: 22 9 2023
Statut: ppublish

Résumé

Organoids derived from stem cells have become an increasingly important tool for studying human development and modeling disease. However, methods are still needed to control and study spatiotemporal patterns of gene expression in organoids. Here we combined optogenetics and gene perturbation technologies to activate or knock-down RNA of target genes in programmable spatiotemporal patterns. To illustrate the usefulness of our approach, we locally activated Sonic Hedgehog (SHH) signaling in an organoid model for human neurodevelopment. Spatial and single-cell transcriptomic analyses showed that this local induction was sufficient to generate stereotypically patterned organoids and revealed new insights into SHH's contribution to gene regulation in neurodevelopment. With this study, we propose optogenetic perturbations in combination with spatial transcriptomics as a powerful technology to reprogram and study cell fates and tissue patterning in organoids.

Identifiants

pubmed: 37735569
doi: 10.1038/s41592-023-01986-w
pii: 10.1038/s41592-023-01986-w
pmc: PMC10555836
doi:

Substances chimiques

Hedgehog Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1544-1552

Subventions

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : RA838/5-1
Organisme : European Molecular Biology Organization (EMBO)
ID : ALTF1235-206

Informations de copyright

© 2023. The Author(s).

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Auteurs

Ivano Legnini (I)

Laboratory for Systems Biology of Gene Regulatory Elements, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany. ivano.legnini@fht.org.
Human Technopole, Milan, Italy. ivano.legnini@fht.org.

Lisa Emmenegger (L)

Laboratory for Systems Biology of Gene Regulatory Elements, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Alessandra Zappulo (A)

Systems Biology of Neural Tissue Differentiation, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.
Human Technopole, Milan, Italy.

Agnieszka Rybak-Wolf (A)

Organoid Platform, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Ricardo Wurmus (R)

Bioinformatics and Omics Data Science, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Anna Oliveras Martinez (AO)

Systems Biology Imaging Platform, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Cledi Cerda Jara (CC)

Laboratory for Systems Biology of Gene Regulatory Elements, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Anastasiya Boltengagen (A)

Laboratory for Systems Biology of Gene Regulatory Elements, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Talé Hessler (T)

Laboratory for Systems Biology of Gene Regulatory Elements, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Guido Mastrobuoni (G)

Proteomic and Metabolomics Platform, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Stefan Kempa (S)

Proteomic and Metabolomics Platform, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Robert Zinzen (R)

Systems Biology of Neural Tissue Differentiation, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.
Systems Biology Imaging Platform, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.

Andrew Woehler (A)

Systems Biology Imaging Platform, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany.
Howard Hughes Medical Institute, Janelia Research Campus, Ashburn, VA, USA.

Nikolaus Rajewsky (N)

Laboratory for Systems Biology of Gene Regulatory Elements, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, Germany. rajewsky@mdc-berlin.de.
Charité-Universitätsmedizin, Berlin, Germany. rajewsky@mdc-berlin.de.
German Center for Cardiovascular Research (DZHK), Berlin, Germany. rajewsky@mdc-berlin.de.
NeuroCure Cluster of Excellence, Berlin, Germany. rajewsky@mdc-berlin.de.
National Center for Tumor Diseases (NCT), German Cancer Consortium (DKTK), Berlin, Germany. rajewsky@mdc-berlin.de.

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