DNA demethylation triggers cell free DNA release in colorectal cancer cells Article Swipe
Valeria Pessei
,
Marco Macagno
,
Elisa Mariella
,
Noemi Congiusta
,
Vittorio Battaglieri
,
Paolo Battuello
,
Marco Viviani
,
Giulia Gionfriddo
,
Simona Lamba
,
Annalisa Lorenzato
,
Daniele Oddo
,
Fariha Idrees
,
Alessandro Cavaliere
,
Alice Bartolini
,
Simonetta Guarrera
,
Michael Linnebacher
,
Laura Monteonofrio
,
Luca Cardone
,
Michèle Milella
,
Andrea Bertotti
,
Silvia Soddu
,
Elena Grassi
,
Giovanni Crisafulli
,
Alberto Bardelli
,
Ludovic Barault
,
Federica Di Nicolantonio
·
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1186/s13073-024-01386-5
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1186/s13073-024-01386-5
Background Liquid biopsy based on cell-free DNA (cfDNA) analysis holds significant promise as a minimally invasive approach for the diagnosis, genotyping, and monitoring of solid malignancies. Human tumors release cfDNA in the bloodstream through a combination of events, including cell death, active and passive release. However, the precise mechanisms leading to cfDNA shedding remain to be characterized. Addressing this question in patients is confounded by several factors, such as tumor burden extent, anatomical and vasculature barriers, and release of nucleic acids from normal cells. In this work, we exploited cancer models to dissect basic mechanisms of DNA release. Methods We measured cell loss ratio, doubling time, and cfDNA release in the supernatant of a colorectal cancer (CRC) cell line collection ( N = 76) representative of the molecular subtypes previously identified in cancer patients. Association analyses between quantitative parameters of cfDNA release, cell proliferation, and molecular features were evaluated. Functional experiments were performed to test the impact of modulating DNA methylation on cfDNA release. Results Higher levels of supernatant cfDNA were significantly associated with slower cell cycling and increased cell death. In addition, a higher cfDNA shedding was found in non-CpG Island Methylator Phenotype (CIMP) models. These results indicate a positive correlation between lower methylation and increased cfDNA levels. To explore this further, we exploited methylation microarrays to identify a subset of probes significantly associated with cfDNA shedding and derive a methylation signature capable of discriminating high from low cfDNA releasers. We applied this signature to an independent set of 176 CRC cell lines and patient derived organoids to select 14 models predicted to be low or high releasers. The methylation profile successfully predicted the amount of cfDNA released in the supernatant. At the functional level, genetic ablation of DNA methyl-transferases increased chromatin accessibility and DNA fragmentation, leading to increased cfDNA release in isogenic CRC cell lines. Furthermore, in vitro treatment of five low releaser CRC cells with a demethylating agent was able to induce a significant increase in cfDNA shedding. Conclusions Methylation status of cancer cell lines contributes to the variability of cfDNA shedding in vitro. Changes in methylation pattern are associated with cfDNA release levels and might be exploited to increase sensitivity of liquid biopsy assays.
Related Topics
Concepts
DNA
Colorectal cancer
Human genetics
DNA demethylation
Cell-free fetal DNA
Computational biology
Biology
Cancer research
Medicine
Cell biology
Molecular biology
Cancer
Chemistry
Genetics
DNA methylation
Gene
Gene expression
Pregnancy
Prenatal diagnosis
Fetus
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1186/s13073-024-01386-5
- OA Status
- gold
- Cited By
- 4
- References
- 93
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4403261583
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
-
https://openalex.org/W4403261583Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1186/s13073-024-01386-5Digital Object Identifier
- Title
-
DNA demethylation triggers cell free DNA release in colorectal cancer cellsWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2024Year of publication
- Publication date
-
2024-10-09Full publication date if available
- Authors
-
Valeria Pessei, Marco Macagno, Elisa Mariella, Noemi Congiusta, Vittorio Battaglieri, Paolo Battuello, Marco Viviani, Giulia Gionfriddo, Simona Lamba, Annalisa Lorenzato, Daniele Oddo, Fariha Idrees, Alessandro Cavaliere, Alice Bartolini, Simonetta Guarrera, Michael Linnebacher, Laura Monteonofrio, Luca Cardone, Michèle Milella, Andrea Bertotti, Silvia Soddu, Elena Grassi, Giovanni Crisafulli, Alberto Bardelli, Ludovic Barault, Federica Di NicolantonioList of authors in order
- Landing page
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https://doi.org/10.1186/s13073-024-01386-5Publisher landing page
- Open access
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YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
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https://doi.org/10.1186/s13073-024-01386-5Direct OA link when available
- Concepts
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DNA, Colorectal cancer, Human genetics, DNA demethylation, Cell-free fetal DNA, Computational biology, Biology, Cancer research, Medicine, Cell biology, Molecular biology, Cancer, Chemistry, Genetics, DNA methylation, Gene, Gene expression, Pregnancy, Prenatal diagnosis, FetusTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
4Total citation count in OpenAlex
- Citations by year (recent)
-
2025: 4Per-year citation counts (last 5 years)
- References (count)
-
93Number of works referenced by this work
- Related works (count)
-
10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.patients | 62 |
| abstract_inverted_index.positive | 201 |
| abstract_inverted_index.question | 60 |
| abstract_inverted_index.release, | 142 |
| abstract_inverted_index.release. | 45, 98, 164 |
| abstract_inverted_index.released | 279 |
| abstract_inverted_index.releaser | 315 |
| abstract_inverted_index.shedding | 53, 187, 228, 345 |
| abstract_inverted_index.subtypes | 129 |
| abstract_inverted_index.Phenotype | 194 |
| abstract_inverted_index.addition, | 183 |
| abstract_inverted_index.barriers, | 76 |
| abstract_inverted_index.cell-free | 6 |
| abstract_inverted_index.chromatin | 293 |
| abstract_inverted_index.exploited | 89, 215, 361 |
| abstract_inverted_index.including | 39 |
| abstract_inverted_index.increased | 179, 207, 292, 300 |
| abstract_inverted_index.minimally | 15 |
| abstract_inverted_index.molecular | 128, 146 |
| abstract_inverted_index.organoids | 258 |
| abstract_inverted_index.patients. | 134 |
| abstract_inverted_index.performed | 153 |
| abstract_inverted_index.predicted | 263, 274 |
| abstract_inverted_index.shedding. | 331 |
| abstract_inverted_index.signature | 233, 245 |
| abstract_inverted_index.treatment | 311 |
| abstract_inverted_index.Addressing | 58 |
| abstract_inverted_index.Background | 1 |
| abstract_inverted_index.Functional | 150 |
| abstract_inverted_index.Methylator | 193 |
| abstract_inverted_index.anatomical | 73 |
| abstract_inverted_index.associated | 173, 225, 353 |
| abstract_inverted_index.collection | 120 |
| abstract_inverted_index.colorectal | 115 |
| abstract_inverted_index.confounded | 64 |
| abstract_inverted_index.diagnosis, | 20 |
| abstract_inverted_index.evaluated. | 149 |
| abstract_inverted_index.functional | 285 |
| abstract_inverted_index.identified | 131 |
| abstract_inverted_index.mechanisms | 49, 95 |
| abstract_inverted_index.modulating | 159 |
| abstract_inverted_index.monitoring | 23 |
| abstract_inverted_index.parameters | 139 |
| abstract_inverted_index.previously | 130 |
| abstract_inverted_index.releasers. | 241, 269 |
| abstract_inverted_index.Association | 135 |
| abstract_inverted_index.Conclusions | 332 |
| abstract_inverted_index.Methylation | 333 |
| abstract_inverted_index.bloodstream | 33 |
| abstract_inverted_index.combination | 36 |
| abstract_inverted_index.contributes | 339 |
| abstract_inverted_index.correlation | 202 |
| abstract_inverted_index.experiments | 151 |
| abstract_inverted_index.genotyping, | 21 |
| abstract_inverted_index.independent | 248 |
| abstract_inverted_index.methylation | 161, 205, 216, 232, 271, 350 |
| abstract_inverted_index.microarrays | 217 |
| abstract_inverted_index.sensitivity | 364 |
| abstract_inverted_index.significant | 11, 327 |
| abstract_inverted_index.supernatant | 112, 169 |
| abstract_inverted_index.variability | 342 |
| abstract_inverted_index.vasculature | 75 |
| abstract_inverted_index.Furthermore, | 308 |
| abstract_inverted_index.quantitative | 138 |
| abstract_inverted_index.successfully | 273 |
| abstract_inverted_index.supernatant. | 282 |
| abstract_inverted_index.accessibility | 294 |
| abstract_inverted_index.demethylating | 320 |
| abstract_inverted_index.malignancies. | 26 |
| abstract_inverted_index.significantly | 172, 224 |
| abstract_inverted_index.characterized. | 57 |
| abstract_inverted_index.discriminating | 236 |
| abstract_inverted_index.fragmentation, | 297 |
| abstract_inverted_index.proliferation, | 144 |
| abstract_inverted_index.representative | 125 |
| abstract_inverted_index.methyl-transferases | 291 |
| cited_by_percentile_year.max | 98 |
| cited_by_percentile_year.min | 97 |
| countries_distinct_count | 1 |
| institutions_distinct_count | 26 |
| sustainable_development_goals[0].id | https://metadata.un.org/sdg/3 |
| sustainable_development_goals[0].score | 0.8600000143051147 |
| sustainable_development_goals[0].display_name | Good health and well-being |
| citation_normalized_percentile.value | 0.81127778 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | False |