Coordinated inheritance of extrachromosomal DNA species in human cancer cells Article Swipe
King L. Hung
,
Matthew G. Jones
,
Ivy Tsz-Lo Wong
,
Joshua T. Lange
,
Jens Luebeck
,
Elisa Scanu
,
Britney Jiayu He
,
Lotte Brückner
,
Rui Li
,
Rocío Chamorro González
,
Rachel Schmargon
,
Jan R. Dörr
,
Julia A. Belk
,
Vineet Bafna
,
Benjamin Werner
,
Weini Huang
,
Anton G. Henssen
,
Paul S. Mischel
,
Howard Y. Chang
·
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1101/2023.07.18.549597
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1101/2023.07.18.549597
The chromosomal theory of inheritance has dominated human genetics, including cancer genetics. Genes on the same chromosome segregate together while genes on different chromosomes assort independently, providing a fundamental tenet of Mendelian inheritance. Extrachromosomal DNA (ecDNA) is a frequent event in cancer that drives oncogene amplification, dysregulated gene expression and intratumoral heterogeneity, including through random segregation during cell division. Distinct ecDNA sequences, herein termed ecDNA species, can co-exist to facilitate intermolecular cooperation in cancer cells. However, how multiple ecDNA species within a tumor cell are assorted and maintained across somatic cell generations to drive cancer cell evolution is not known. Here we show that cooperative ecDNA species can be coordinately inherited through mitotic co-segregation. Imaging and single-cell analyses show that multiple ecDNAs encoding distinct oncogenes co-occur and are correlated in copy number in human cancer cells. EcDNA species are coordinately segregated asymmetrically during mitosis, resulting in daughter cells with simultaneous copy number gains in multiple ecDNA species prior to any selection. Computational modeling reveals the quantitative principles of ecDNA co-segregation and co-selection, predicting their observed distributions in cancer cells. Finally, we show that coordinated inheritance of ecDNAs enables co-amplification of specialized ecDNAs containing only enhancer elements and guides therapeutic strategies to jointly deplete cooperating ecDNA oncogenes. Coordinated inheritance of ecDNAs confers stability to oncogene cooperation and novel gene regulatory circuits, allowing winning combinations of epigenetic states to be transmitted across cell generations.
Related Topics
Concepts
Extrachromosomal DNA
Inheritance (genetic algorithm)
Biology
DNA
Genetics
Evolutionary biology
Computational biology
Gene
Plasmid
Metadata
- Type
- preprint
- Language
- en
- Landing Page
- https://doi.org/10.1101/2023.07.18.549597
- https://www.biorxiv.org/content/biorxiv/early/2023/07/19/2023.07.18.549597.full.pdf
- OA Status
- green
- Cited By
- 4
- References
- 60
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4384821015
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4384821015Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1101/2023.07.18.549597Digital Object Identifier
- Title
-
Coordinated inheritance of extrachromosomal DNA species in human cancer cellsWork title
- Type
-
preprintOpenAlex work type
- Language
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enPrimary language
- Publication year
-
2023Year of publication
- Publication date
-
2023-07-19Full publication date if available
- Authors
-
King L. Hung, Matthew G. Jones, Ivy Tsz-Lo Wong, Joshua T. Lange, Jens Luebeck, Elisa Scanu, Britney Jiayu He, Lotte Brückner, Rui Li, Rocío Chamorro González, Rachel Schmargon, Jan R. Dörr, Julia A. Belk, Vineet Bafna, Benjamin Werner, Weini Huang, Anton G. Henssen, Paul S. Mischel, Howard Y. ChangList of authors in order
- Landing page
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https://doi.org/10.1101/2023.07.18.549597Publisher landing page
- PDF URL
-
https://www.biorxiv.org/content/biorxiv/early/2023/07/19/2023.07.18.549597.full.pdfDirect link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
greenOpen access status per OpenAlex
- OA URL
-
https://www.biorxiv.org/content/biorxiv/early/2023/07/19/2023.07.18.549597.full.pdfDirect OA link when available
- Concepts
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Extrachromosomal DNA, Inheritance (genetic algorithm), Biology, DNA, Genetics, Evolutionary biology, Computational biology, Gene, PlasmidTop concepts (fields/topics) attached by OpenAlex
- Cited by
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4Total citation count in OpenAlex
- Citations by year (recent)
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2025: 1, 2024: 3Per-year citation counts (last 5 years)
- References (count)
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60Number of works referenced by this work
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10Other works algorithmically related by OpenAlex
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