High-throughput differentiation of human blood vessel organoids reveals overlapping and distinct functions of the cerebral cavernous malformation proteins Article Swipe
Dariush Skowronek
,
Robin A. Pilz
,
Valeriia V. Saenko
,
Lara Mellinger
,
Debora Singer
,
Silvia Ribback
,
Anja Weise
,
Kevin Claassen
,
Janine Büttner
,
Emily M Brockmann
,
Christian A. Hübner
,
Thiha Aung
,
Silke Haerteis
,
Sander Bekeschus
,
A Ekici
,
Ute Felbor
,
Matthias Rath
·
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1101/2024.12.04.626588
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1101/2024.12.04.626588
Cerebral cavernous malformations (CCMs) are clusters of thin-walled enlarged blood vessels in the central nervous system that are prone to recurrent hemorrhage and can occur in both sporadic and familial forms. The familial form results from loss-of-function variants in the CCM1 , CCM2 , or CCM3 gene. Despite a better understanding of CCM pathogenesis in recent years, it is still unclear why CCM3 mutations often lead to a more aggressive phenotype than CCM1 or CCM2 variants. By combining high-throughput differentiation of blood vessel organoids from human induced pluripotent stem cells (hiPSCs) with a CCM1 , CCM2 , or CCM3 knockout, single-cell RNA sequencing, and high-content imaging, we uncovered both shared and distinct functions of the CCM proteins. While there was a significant overlap of differentially expressed genes in fibroblasts across all three knockout conditions, inactivation of CCM1 , CCM2 , or CCM3 also led to specific gene expression patterns in neuronal, mesenchymal, and endothelial cell populations, respectively. Taking advantage of the different fluorescent labels of the hiPSCs, we could also visualize the abnormal expansion of CCM1 and CCM3 knockout cells when differentiated together with wild-type cells into mosaic blood vessel organoids. In contrast, CCM2 knockout cells showed even reduced proliferation. These observations may help to explain the less severe clinical course in individuals with a pathogenic variant in CCM2 and to decode the molecular and cellular heterogeneity in CCM disease. Finally, the ability to differentiate blood vessel organoids in a 96-well format will further facilitate their use in drug discovery and other biomedical research studies. STATEMENTS AND DECLARATIONS Conflicts of interest statement The authors declare no competing interests. The here described protocol for high-throughput organoid synthesis has been filed as a patent application at the European Patent Office (Process number: EP24213596.0) Author contribution statement MR, DSk, and UF designed the study. DSk, VS, LM, and RAP performed most of the functional experiments. SH and TA performed the CAM assays. SR performed the immunohistochemical stainings. SB, DSi, DSk, and VS performed the confocal microscopy and high-content imaging analyses. AE, CB, and EMB performed the scRNA sequencing analysis. AW and CAH performed and analyzed the karyotyping of the hiPSC clones. DSk, RAP, VS, KC, MR, and SB analyzed the data. DSk, VS, LM, and MR prepared figures. All authors contributed to the interpretation of the results. DSk, RAP, VS, and MR drafted the manuscript, and all authors contributed to writing. Ethics statement This study does not involve human participants or animal subjects. Availability of data and materials All relevant data are published within the paper and the supplementary files. ScRNA sequencing data can be accessed through the Gene Expression Omnibus (GEO) database (record number: GSE276497).
Related Topics
Concepts
Biology
Induced pluripotent stem cell
Phenotype
Organoid
Knockout mouse
Gene knockout
Cell biology
Gene
Embryonic stem cell
Cellular differentiation
Genetics
Metadata
- Type
- preprint
- Language
- en
- Landing Page
- https://doi.org/10.1101/2024.12.04.626588
- https://www.biorxiv.org/content/biorxiv/early/2024/12/05/2024.12.04.626588.full.pdf
- OA Status
- green
- References
- 69
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4405105574
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4405105574Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1101/2024.12.04.626588Digital Object Identifier
- Title
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High-throughput differentiation of human blood vessel organoids reveals overlapping and distinct functions of the cerebral cavernous malformation proteinsWork title
- Type
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preprintOpenAlex work type
- Language
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enPrimary language
- Publication year
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2024Year of publication
- Publication date
-
2024-12-05Full publication date if available
- Authors
-
Dariush Skowronek, Robin A. Pilz, Valeriia V. Saenko, Lara Mellinger, Debora Singer, Silvia Ribback, Anja Weise, Kevin Claassen, Janine Büttner, Emily M Brockmann, Christian A. Hübner, Thiha Aung, Silke Haerteis, Sander Bekeschus, A Ekici, Ute Felbor, Matthias RathList of authors in order
- Landing page
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https://doi.org/10.1101/2024.12.04.626588Publisher landing page
- PDF URL
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https://www.biorxiv.org/content/biorxiv/early/2024/12/05/2024.12.04.626588.full.pdfDirect link to full text PDF
- Open access
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YesWhether a free full text is available
- OA status
-
greenOpen access status per OpenAlex
- OA URL
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https://www.biorxiv.org/content/biorxiv/early/2024/12/05/2024.12.04.626588.full.pdfDirect OA link when available
- Concepts
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Biology, Induced pluripotent stem cell, Phenotype, Organoid, Knockout mouse, Gene knockout, Cell biology, Gene, Embryonic stem cell, Cellular differentiation, GeneticsTop concepts (fields/topics) attached by OpenAlex
- Cited by
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0Total citation count in OpenAlex
- References (count)
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69Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.mosaic | 188 |
| abstract_inverted_index.patent | 282 |
| abstract_inverted_index.recent | 56 |
| abstract_inverted_index.severe | 209 |
| abstract_inverted_index.shared | 110 |
| abstract_inverted_index.showed | 197 |
| abstract_inverted_index.study. | 301 |
| abstract_inverted_index.system | 16 |
| abstract_inverted_index.vessel | 83, 190, 237 |
| abstract_inverted_index.within | 421 |
| abstract_inverted_index.years, | 57 |
| abstract_inverted_index.(record | 441 |
| abstract_inverted_index.96-well | 241 |
| abstract_inverted_index.Despite | 48 |
| abstract_inverted_index.Omnibus | 438 |
| abstract_inverted_index.ability | 233 |
| abstract_inverted_index.assays. | 319 |
| abstract_inverted_index.authors | 264, 377, 395 |
| abstract_inverted_index.central | 14 |
| abstract_inverted_index.clones. | 358 |
| abstract_inverted_index.declare | 265 |
| abstract_inverted_index.drafted | 390 |
| abstract_inverted_index.explain | 206 |
| abstract_inverted_index.further | 244 |
| abstract_inverted_index.hiPSCs, | 167 |
| abstract_inverted_index.imaging | 336 |
| abstract_inverted_index.induced | 87 |
| abstract_inverted_index.involve | 405 |
| abstract_inverted_index.nervous | 15 |
| abstract_inverted_index.number: | 290, 442 |
| abstract_inverted_index.overlap | 123 |
| abstract_inverted_index.reduced | 199 |
| abstract_inverted_index.results | 35 |
| abstract_inverted_index.through | 434 |
| abstract_inverted_index.unclear | 61 |
| abstract_inverted_index.variant | 217 |
| abstract_inverted_index.vessels | 11 |
| abstract_inverted_index.(Process | 289 |
| abstract_inverted_index.(hiPSCs) | 91 |
| abstract_inverted_index.ABSTRACT | 0 |
| abstract_inverted_index.Cerebral | 1 |
| abstract_inverted_index.European | 286 |
| abstract_inverted_index.Finally, | 231 |
| abstract_inverted_index.abnormal | 173 |
| abstract_inverted_index.accessed | 433 |
| abstract_inverted_index.analyzed | 352, 366 |
| abstract_inverted_index.cellular | 226 |
| abstract_inverted_index.clinical | 210 |
| abstract_inverted_index.clusters | 6 |
| abstract_inverted_index.confocal | 332 |
| abstract_inverted_index.database | 440 |
| abstract_inverted_index.designed | 299 |
| abstract_inverted_index.disease. | 230 |
| abstract_inverted_index.distinct | 112 |
| abstract_inverted_index.enlarged | 9 |
| abstract_inverted_index.familial | 30, 33 |
| abstract_inverted_index.figures. | 375 |
| abstract_inverted_index.imaging, | 106 |
| abstract_inverted_index.interest | 261 |
| abstract_inverted_index.knockout | 133, 179, 195 |
| abstract_inverted_index.organoid | 275 |
| abstract_inverted_index.patterns | 149 |
| abstract_inverted_index.prepared | 374 |
| abstract_inverted_index.protocol | 272 |
| abstract_inverted_index.relevant | 417 |
| abstract_inverted_index.research | 254 |
| abstract_inverted_index.results. | 384 |
| abstract_inverted_index.specific | 146 |
| abstract_inverted_index.sporadic | 28 |
| abstract_inverted_index.studies. | 255 |
| abstract_inverted_index.together | 183 |
| abstract_inverted_index.variants | 38 |
| abstract_inverted_index.writing. | 398 |
| abstract_inverted_index.Conflicts | 259 |
| abstract_inverted_index.advantage | 159 |
| abstract_inverted_index.analyses. | 337 |
| abstract_inverted_index.analysis. | 346 |
| abstract_inverted_index.cavernous | 2 |
| abstract_inverted_index.combining | 78 |
| abstract_inverted_index.competing | 267 |
| abstract_inverted_index.contrast, | 193 |
| abstract_inverted_index.described | 271 |
| abstract_inverted_index.different | 162 |
| abstract_inverted_index.discovery | 250 |
| abstract_inverted_index.expansion | 174 |
| abstract_inverted_index.expressed | 126 |
| abstract_inverted_index.functions | 113 |
| abstract_inverted_index.knockout, | 100 |
| abstract_inverted_index.materials | 415 |
| abstract_inverted_index.molecular | 224 |
| abstract_inverted_index.mutations | 64 |
| abstract_inverted_index.neuronal, | 151 |
| abstract_inverted_index.organoids | 84, 238 |
| abstract_inverted_index.performed | 307, 316, 321, 330, 342, 350 |
| abstract_inverted_index.phenotype | 71 |
| abstract_inverted_index.proteins. | 117 |
| abstract_inverted_index.published | 420 |
| abstract_inverted_index.recurrent | 21 |
| abstract_inverted_index.statement | 262, 294, 400 |
| abstract_inverted_index.subjects. | 410 |
| abstract_inverted_index.synthesis | 276 |
| abstract_inverted_index.uncovered | 108 |
| abstract_inverted_index.variants. | 76 |
| abstract_inverted_index.visualize | 171 |
| abstract_inverted_index.wild-type | 185 |
| abstract_inverted_index.Expression | 437 |
| abstract_inverted_index.STATEMENTS | 256 |
| abstract_inverted_index.aggressive | 70 |
| abstract_inverted_index.biomedical | 253 |
| abstract_inverted_index.expression | 148 |
| abstract_inverted_index.facilitate | 245 |
| abstract_inverted_index.functional | 311 |
| abstract_inverted_index.hemorrhage | 22 |
| abstract_inverted_index.interests. | 268 |
| abstract_inverted_index.microscopy | 333 |
| abstract_inverted_index.organoids. | 191 |
| abstract_inverted_index.pathogenic | 216 |
| abstract_inverted_index.sequencing | 345, 429 |
| abstract_inverted_index.stainings. | 324 |
| abstract_inverted_index.GSE276497). | 443 |
| abstract_inverted_index.application | 283 |
| abstract_inverted_index.conditions, | 134 |
| abstract_inverted_index.contributed | 378, 396 |
| abstract_inverted_index.endothelial | 154 |
| abstract_inverted_index.fibroblasts | 129 |
| abstract_inverted_index.fluorescent | 163 |
| abstract_inverted_index.individuals | 213 |
| abstract_inverted_index.karyotyping | 354 |
| abstract_inverted_index.manuscript, | 392 |
| abstract_inverted_index.pluripotent | 88 |
| abstract_inverted_index.sequencing, | 103 |
| abstract_inverted_index.significant | 122 |
| abstract_inverted_index.single-cell | 101 |
| abstract_inverted_index.thin-walled | 8 |
| abstract_inverted_index.Availability | 411 |
| abstract_inverted_index.DECLARATIONS | 258 |
| abstract_inverted_index.contribution | 293 |
| abstract_inverted_index.experiments. | 312 |
| abstract_inverted_index.high-content | 105, 335 |
| abstract_inverted_index.inactivation | 135 |
| abstract_inverted_index.mesenchymal, | 152 |
| abstract_inverted_index.observations | 202 |
| abstract_inverted_index.participants | 407 |
| abstract_inverted_index.pathogenesis | 54 |
| abstract_inverted_index.populations, | 156 |
| abstract_inverted_index.EP24213596.0) | 291 |
| abstract_inverted_index.differentiate | 235 |
| abstract_inverted_index.heterogeneity | 227 |
| abstract_inverted_index.malformations | 3 |
| abstract_inverted_index.respectively. | 157 |
| abstract_inverted_index.supplementary | 426 |
| abstract_inverted_index.understanding | 51 |
| abstract_inverted_index.differentially | 125 |
| abstract_inverted_index.differentiated | 182 |
| abstract_inverted_index.interpretation | 381 |
| abstract_inverted_index.proliferation. | 200 |
| abstract_inverted_index.differentiation | 80 |
| abstract_inverted_index.high-throughput | 79, 274 |
| abstract_inverted_index.loss-of-function | 37 |
| abstract_inverted_index.immunohistochemical | 323 |
| cited_by_percentile_year | |
| corresponding_author_ids | https://openalex.org/A5029665921 |
| countries_distinct_count | 1 |
| institutions_distinct_count | 17 |
| corresponding_institution_ids | https://openalex.org/I2799318839, https://openalex.org/I36522303 |
| sustainable_development_goals[0].id | https://metadata.un.org/sdg/3 |
| sustainable_development_goals[0].score | 0.800000011920929 |
| sustainable_development_goals[0].display_name | Good health and well-being |
| citation_normalized_percentile.value | 0.39310124 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | False |