Targeting the Senescence-Overriding Cooperative Activity of Structurally Unrelated H3K9 Demethylases in Melanoma
Open accessAbstract
Oncogene-induced senescence, e.g., in melanocytic nevi, terminates the expansion of pre-malignant cells via transcriptional silencing of proliferation-related genes due to decoration of their promoters with repressive trimethylated histone H3 lysine 9 (H3K9) marks. We show here that structurally distinct H3K9-active demethylases-the lysine-specific demethylase-1 (LSD1) and several Jumonji C domain-containing moieties (such as JMJD2C)-disable senescence and permit Ras/Braf-evoked transformation. In mouse and zebrafish models, enforced LSD1 or JMJD2C expression promoted Braf-V600E-driven melanomagenesis. A large subset of established melanoma cell lines and primary human melanoma samples presented with a collective upregulation of related and unrelated H3K9 demethylase activities, whose targeted inhibition restored senescence, even in Braf inhibitor-resistant melanomas, evoked secondary immune effects and controlled tumor growth in vivo.
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Cells lacking functional p53 or overexpressing JMJD2c fail to enter VIS and lack a SASP after SARS-CoV-2 infection.
“in vitro experiments showed that cells that lack functional p53 or overexpress the H3K9me3 demethylase JMJD2c46,50 — which therefore cannot enter senescence in response to pro-senescent oncogenes such as Ras-G12V or Braf-V600E46,51 — also failed to enter VIS and lacked a SASP upon infection with SARS-CoV-2 (ref.28).”
From COVID-19 and cellular senescence (2023) · cites this paper as [50]
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Epigenetic regulation of stem cells in lung cancer oncogenesis and therapy resistance
Wu, J., Feng, J., Zhang, Q., He, Y., Xu, C. S., Wang, C., & Li, W. (2023) · Frontiers in Genetics · doi:10.3389/fgene.2023.1120815 · Cited by 11 · see citing works
Role of non-coding RNAs and exosomal non-coding RNAs in vasculitis: A narrative review
Tang, X., Guo, J., Feng, Q., & Rezaei, M. J. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.129658 · Cited by 11 · see citing works
Malignant melanoma: Underlying epigenetic mechanisms
Kaliyadan, F., Sabit, H., & Menezes, R. G. (2020) · Indian Journal of Dermatology Venereology and Leprology · doi:10.4103/ijdvl.ijdvl_791_19 · Cited by 11 · see citing works
- Authors
- Yu, Y., Schleich, K., Yue, B., Ji, S., Lohneis, P., Kemper, K., Silvis, M. R., Qutob, N., van Rooijen, E., Werner-Klein, M., Li, L., Dhawan, D., Meierjohann, S., Reimann, M., Elkahloun, A., Treitschke, S., Dörken, B., Speck, C., Mallette, F. A., Zon, L. I., Holmen, S. L., Peeper, D. S., Samuels, Y., Schmitt, C. A., & Lee, S.
- Affiliations
- Max Delbrück Center (DE)
- Humboldt-Universität zu Berlin (DE)
- The Netherlands Cancer Institute (NL)
- University of Utah (US)
- Weizmann Institute of Science (IL)
- University of Würzburg (DE)
- National Human Genome Research Institute (US)
- Fraunhofer Institute for Toxicology and Experimental Medicine (DE)
- MRC London Institute of Medical Sciences (GB)
- Hôpital Maisonneuve-Rosemont (CA)
- Boston Children's Hospital (US)
- Corresponding author
- Schmitt, Clemens A.
- ORCID
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2018-02
- Volume
- 33
- Issue
- 2
- Pages
- 322-336.e8
- ISSN
- 1535-6108 (ISSN-L)
- PMC
- PMC5977991
- OpenAlex
- W2787203782
- Cited by
- 156
- References
- 71
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 19 · 2023: 15 · 2022: 18 · 2021: 31 · 2020: 31 · 2019: 13 · 2018: 8
- FWCI
- 7.38
- Type
- journal article
- Language
- en
- Update notices
- erratum (2018-04-09)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- PubMed Central (acceptedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
- Publikationsdatenbank der Fraunhofer-Gesellschaft (Fraunhofer-Gesellschaft) (submittedVersion)
- Fraunhofer-Publica (Fraunhofer-Gesellschaft) (submittedVersion)
- Spiral (Imperial College London) (submittedVersion, cc-by-nc-nd)
- Funders
- Deutsche Forschungsgemeinschaft
- German Cancer Consortium
- Wilhelm Sander Foundation (2015.016.1)
- NIH (CA103846)
- Ellison Foundation
- Chinese Scholarship Council
- Berlin School of Integrative Oncology
- ERC (StG-335377)
- Canadian Institutes of Health Research (MOP-133442)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Melanoma and MAPK Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Keywords
- oncogene-induced senescence, LSD1, JMJD2C, melanoma, BRAF V600E mutation, melanomagenesis, histone demethylation, senescence reversal, BRAF inhibitor resistance, zebrafish model
- MeSH terms
- Animals, Histones, Humans, Lysine, Melanoma, Methylation, Mice, Nude, Promoter Regions, Genetic, Histone Demethylases, Jumonji Domain-Containing Histone Demethylases
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