Shared enhancer gene regulatory networks between wound and oncogenic programs
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Abstract
Abstract Wound response programs are often activated during neoplastic growth in tumors. In both wound repair and tumor growth, cells respond to acute stress and balance the activation of multiple programs including apoptosis, proliferation, and cell migration. Central to those responses are the activation of the JNK/MAPK and JAK/STAT signaling pathways. Yet, to what extent these signaling cascades interact at the cis -regulatory level, and how they orchestrate different regulatory and phenotypic responses is still unclear. Here, we aim to characterize the regulatory states that emerge and cooperate in the wound response, using the Drosophila melanogaster wing disc as a model system, and compare these with cancer cell states induced by ras V12 scrib -/- in the eye disc. We used single-cell multiome profiling to derive enhancer Gene Regulatory Networks (eGRNs) by integrating chromatin accessibility and gene expression signals. We identify a “proliferative” eGRN, active in the majority of wounded cells and controlled by AP-1 and STAT. In a smaller, but distinct population of wound cells, a “senescent” eGRN is activated and driven by C/EBP-like transcription factors (Irbp18, Xrp1, Slow border, and Vrille) and Scalloped. In tumor cells on the other hand, both eGRN signatures are simultaneously active within the same cell. Our single-cell multiome and eGRNs resource offers an in-depth characterisation of the senescence markers, together with a new perspective on the shared gene regulatory programs acting during wound response and oncogenesis.
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Previously ectopic upregulation of a network of transcription factors (Upd, JAK-STAT, AP-1, Myc, Ftz, Ets, Irbp18, Xrp1, Slow border, and Vrille) promotes growth and invasiveness of RasV12,scrib- tumours.
“Previously ectopic upregulation of a network of transcription factors e.g., Upd, JAK-STAT, AP-1, Myc, Ftz, Ets, Irbp18, Xrp1, Slow border, and Vrille were reported to promote the growth and invasiveness of the Ras V12 ,scrib -tumours (53-57).”
From A Tumour-Specific Molecular Network Promotes Tumour Growth in <i>Drosophila</i> by Enforcing a JNK-YKI Feedforward Loop (2023) · cites this paper as [53]
The Results section (“Shared regulatory programs between wound response and cancer”; page not provided) reports AP-1 and Stat92E signatures in rasV12scrib-/- tumors and says the tumor cells appear to activate proliferative and senescence programs. The paper also identifies Irbp18, Xrp1, Slbo and Vrille in the senescent network. These observations do not establish that ectopic upregulation of the listed factors promotes tumor growth or invasiveness, and the passage does not substantiate the full list. (LLM, conf=0.87)
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Self-citationRasV12; scrib−/− Tumors: A Cooperative Oncogenesis Model Fueled by Tumor/Host Interactions
Dillard, C., Reis, J. G. T., & Rusten, T. E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168873 · Cited by 34 · see citing works
Crawling wounded: molecular genetic insights into wound healing from Drosophila larvae
Tsai, C.-R., Wang, Y., & Galko, M. J. (2018) · The International Journal of Developmental Biology · doi:10.1387/ijdb.180085mg · Cited by 30 · see citing works
Dichtel-Danjoy, M.-L., Caldeira, J., & Casares, F. (2009) · Development · doi:10.1242/dev.032854 · Cited by 29 · see citing works
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The cytolinker Pigs is a direct target and a negative regulator of Notch signalling
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Control of Cell Growth and Proliferation by the Tribbles Pseudokinase: Lessons from Drosophila
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Drosophila Imaginal Discs as a Model of Epithelial Wound Repair and Regeneration
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Identification and Functional Analysis of Healing Regulators in Drosophila
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vib-singlecell-nf/vsn-pipelines: v0.14.0
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Chromatin remodelling and retrotransposons activities during regeneration in Drosophila
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Critical genetic program for Drosophila imaginal disc regeneration revealed by single-cell analysisPreprint
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Mutual repression between JNK/AP-1 and JAK/STAT stratifies cell behaviors during tissue regenerationPreprint
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Self-citation
Flagged first, then by citations
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Sorted by citations
Waghmare, I., Gangwani, K., Rai, A., Singh, A., & Kango-Singh, M. (2023) · doi:10.1101/2023.10.18.561369 · Cited by 1 · see citing works
- Authors
- Floc'hlay, S., Balaji, R., Stanković, D., Christiaens, V. M., Bravo González-Blas, C., De Winter, S., Hulselmans, G. J., De Waegeneer, M., Quan, X., Koldere, D., Atkins, M., Halder, G., Uhlirova, M., Classen, A.-K., & Aerts, S.
- Affiliations
- VIB Center for Brain & Disease Research
- University of Freiburg (DE)
- University of Cologne (DE)
- VIB-KU Leuven Center for Brain & Disease Research (BE)
- Sam Houston State University (US)
- VIB-KU Leuven Center for Cancer Biology (BE)
- Institute for Genetics Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne
- Corresponding author
- Classen, Anne-Kathrin
- Aerts, Stein
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2023-05-03
- Volume
- 12
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC10238094
- OpenAlex
- W4367835324
- Cited by
- 27
- References
- 111
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 7 · 2023: 3
- FWCI
- 2.41
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Lirias (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- European Research Council (724226_cisCONTROL)
- Fonds Wetenschappelijk Onderzoek (G0C0417N, G094121N)
- Deutsche Forschungsgemeinschaft (EXC 2189 CIBSS, CL490/3-1, EXC 2030)
- KU Leuven (C14/18/092)
- Boehringer Ingelheim Foundation (Plus3 Programme)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- wounding response, carcinogenesis, chromatin accessibility, JNK signaling, JAK/STAT signaling, AP-1, senescence, Scalloped, Drosophila wing disc, eye disc, RasV12, SCRIB, cell proliferation
- MeSH terms
- Animals, Chromatin, DNA-Binding Proteins, Drosophila melanogaster, Neoplasms, Transcription Factors, Drosophila Proteins, Gene Regulatory Networks
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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