Probing the Tumor Suppressor Function of BAP1 in CRISPR-Engineered Human Liver Organoids
Open accessAbstract
The deubiquitinating enzyme BAP1 is a tumor suppressor, among others involved in cholangiocarcinoma. BAP1 has many proposed molecular targets, while its Drosophila homolog is known to deubiquitinate histone H2AK119. We introduce BAP1 loss-of-function by CRISPR/Cas9 in normal human cholangiocyte organoids. We find that BAP1 controls the expression of junctional and cytoskeleton components by regulating chromatin accessibility. Consequently, we observe loss of multiple epithelial characteristics while motility increases. Importantly, restoring the catalytic activity of BAP1 in the nucleus rescues these cellular and molecular changes. We engineer human liver organoids to combine four common cholangiocarcinoma mutations (TP53, PTEN, SMAD4, and NF1). In this genetic background, BAP1 loss results in acquisition of malignant features upon xenotransplantation. Thus, control of epithelial identity through the regulation of chromatin accessibility appears to be a key aspect of BAP1's tumor suppressor function. Organoid technology combined with CRISPR/Cas9 provides an experimental platform for mechanistic studies of cancer gene function in a human context.
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Multiplexed gene-knockout by conventional CRISPR/Cas9-mediated NHEJ is very efficient and can be readily applied in organoids.
“Multiplexed gene-knockout by conventional CRISPR/Cas9-mediated NHEJ is very efficient and can be readily applied in organoids13,14,62.”
From One-step generation of tumor models by base editor multiplexing in adult stem cell-derived organoids (2023) · cites this paper as [62]
In “Generation of Cas9-gRNA plasmid, organoid electroporation and generation of KO lines” (page not provided), the paper describes co-injecting four or five Cas9-guide plasmids and says that, after TP53-mutant selection, the vast majority of organoids also carried mutations in the other targeted genes. This supports multiplex knockout in human liver organoids, but does not establish that NHEJ-mediated knockout itself is very efficient or readily applicable across organoids generally; the reported high efficiency is co-transfection in a selected population. (LLM, conf=0.85)
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Liu, S., Cheng, C., Zhu, L., Zhao, T., Wang, Z., Yi, X., Yan, F., Wang, X., Li, C., Cui, T., et al. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03865-3 · Cited by 26 · see citing works
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Nanoblades allow high-level genome editing in murine and human organoids
Tiroille, V., Krug, A., Bokobza, E., Kahi, M., Bulcaen, M., Ensinck, M. M., Geurts, M. H., Hendriks, D., Vermeulen, F., Larbret, F., et al. (2023) · Molecular Therapy - Nucleic Acids · doi:10.1016/j.omtn.2023.06.004 · Cited by 25 · see citing works
Self-citationAdvances in therapeutic application of CRISPR-Cas9
Sun, J., Wang, J., Zheng, D., & Hu, X. (2019) · Briefings in Functional Genomics · doi:10.1093/bfgp/elz031 · Cited by 25 · see citing works
Liver organoids: Current advances and future applications for hepatology
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Human Organoids as an Emerging Tool for Genome Screenings
Andreatta, F., Hendriks, D. F. G., & Artegiani, B. (2025) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-103023-122327 · Cited by 24 · see citing works
Self-citationOrganoids for Liver Stage Malaria Research
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Cholangiocarcinoma Disease Modelling Through Patients Derived Organoids
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Microenvironmental control of the ductular reaction: balancing repair and disease progression
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- Authors
- Artegiani, B., van Voorthuijsen, L., Lindeboom, R. G. H., Seinstra, D., Heo, I., Tapia, P., López-Iglesias, C., Postrach, D., Dayton, T., Oka, R., Hu, H., van Boxtel, R., van Es, J. H., Offerhaus, J., Peters, P. J., van Rheenen, J., Vermeulen, M., & Clevers, H.
- Affiliations
- Royal Netherlands Academy of Arts and Sciences (NL)
- Radboud University Nijmegen (NL)
- The Netherlands Cancer Institute (NL)
- Princess Máxima Center (NL)
- Shandong University (CN)
- Maastricht University (NL)
- Corresponding author
- Clevers, Hans
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2019-06
- Volume
- 24
- Issue
- 6
- Pages
- 927-943.e6
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- OpenAlex
- W2946448736
- Cited by
- 218
- References
- 84
- Citations by year
- 2026: 19 · 2025: 26 · 2024: 34 · 2023: 33 · 2022: 33 · 2021: 37 · 2020: 25 · 2019: 11
- FWCI
- 25.32
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- European Research Council
- Topics
- Health Sciences › Medicine › Surgery › Cholangiocarcinoma and Gallbladder Cancer Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hippo pathway signaling and YAP/TAZ
- Keywords
- BAP1, tumor suppressor, cholangiocarcinoma, liver organoids, cholangiocytes, chromatin accessibility, cell motility, deubiquitination, TP53, PTEN, SMAD4, neurofibromatosis type 1, xenotransplantation
- MeSH terms
- Loss of Function Mutation, Animals, Cells, Cultured, Chromatin, Cytoskeleton, Epithelial Cells, Female, Humans, Liver, Liver Neoplasms, Organoids, Transplantation, Heterologous, Mice, SCID, Cholangiocarcinoma, Tumor Suppressor Proteins, Ubiquitin Thiolesterase, Mice, Bioengineering, Carcinogenesis, Clustered Regularly Interspaced Short Palindromic Repeats
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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