Actionable cancer vulnerability due to translational arrest, p53 aggregation and ribosome biogenesis stress evoked by the disulfiram metabolite CuET
Open accessAbstract
Drug repurposing is a versatile strategy to improve current therapies. Disulfiram has long been used in the treatment of alcohol dependency and multiple clinical trials to evaluate its clinical value in oncology are ongoing. We have recently reported that the disulfiram metabolite diethyldithiocarbamate, when combined with copper (CuET), targets the NPL4 adapter of the p97VCP segregase to suppress the growth of a spectrum of cancer cell lines and xenograft models in vivo. CuET induces proteotoxic stress and genotoxic effects, however important issues concerning the full range of the CuET-evoked tumor cell phenotypes, their temporal order, and mechanistic basis have remained largely unexplored. Here, we have addressed these outstanding questions and show that in diverse human cancer cell models, CuET causes a very early translational arrest through the integrated stress response (ISR), later followed by features of nucleolar stress. Furthermore, we report that CuET entraps p53 in NPL4-rich aggregates leading to elevated p53 protein and its functional inhibition, consistent with the possibility of CuET-triggered cell death being p53-independent. Our transcriptomics profiling revealed activation of pro-survival adaptive pathways of ribosomal biogenesis (RiBi) and autophagy upon prolonged exposure to CuET, indicating potential feedback responses to CuET treatment. The latter concept was validated here by simultaneous pharmacological inhibition of RiBi and/or autophagy that further enhanced CuET’s tumor cytotoxicity, using both cell culture and zebrafish in vivo preclinical models. Overall, these findings expand the mechanistic repertoire of CuET’s anti-cancer activity, inform about the temporal order of responses and identify an unorthodox new mechanism of targeting p53. Our results are discussed in light of cancer-associated endogenous stresses as exploitable tumor vulnerabilities and may inspire future clinical applications of CuET in oncology, including combinatorial treatments and focus on potential advantages of using certain validated drug metabolites, rather than old, approved drugs with their, often complex, metabolic profiles.
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Transcriptomic profiling reveals pro-survival activation of ribosomal biogenesis and autophagy pathways during prolonged exposure, suggesting adaptive feedback responses.
“Transcriptomic profiling further reveals the pro-survival activation of ribosomal biogenesis (RiBi) and autophagy pathways during prolonged exposure, suggesting adaptive feedback responses.84”
From Off-label and repurposed use of disulfiram beyond alcohol dependence: A systematic review of clinical and preclinical evidence (2026) · cites this paper as [84]
Cu(DDC)2 sequesters p53 in NPL4-rich aggregates, elevating p53 levels while functionally inhibiting it, consistent with p53-independent cell death.
“Cu(DDC)2 sequesters p53 in NPL4-rich aggregates, elevating p53 levels while functionally inhibiting it, consistent with p53-independent cell death.84”
From Off-label and repurposed use of disulfiram beyond alcohol dependence: A systematic review of clinical and preclinical evidence (2026) · cites this paper as [84]
In diverse human cancer cell models, Cu(DDC)2 rapidly triggers integrated stress response-mediated translational arrest followed by nucleolar stress.
“In diverse human cancer cell models, Cu(DDC)2 rapidly triggers integrated stress response (ISR)–mediated translational arrest, followed by nucleolar stress.”
From Off-label and repurposed use of disulfiram beyond alcohol dependence: A systematic review of clinical and preclinical evidence (2026) · cites this paper as [84]
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Self-citation
- Authors
- Kanellis, D. C., Zisi, A., Skrott, Z., Lemmens, B., Espinoza, J. A., Kosar, M., Björkman, A., Li, X., Arampatzis, S., Bartkova, J., Andújar-Sánchez, M., Fernandez-Capetillo, O., Mistrik, M., Lindström, M. S., & Bartek, J.
- Affiliations
- Science for Life Laboratory (SE)
- Danish Cancer Society (DK)
- Corresponding author
- Kanellis, Dimitris C.
- ORCID
- Venue
- Cell Death & Differentiation
- Published
- 2023-05-04
- Volume
- 30
- Issue
- 7
- Pages
- 1666-1678
- ISSN
- 1350-9047 (ISSN-L)
- 1476-5403
- PMC
- PMC10307793
- OpenAlex
- W4372337602
- Cited by
- 27
- References
- 43
- Citations by year
- 2026: 15 · 2025: 7 · 2024: 4 · 2023: 1
- FWCI
- 3.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Cell Death and Differentiation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Cancerfonden (170176)
- Vetenskapsrådet (VR-MH 2014-46602-117891-30)
- Novo Nordisk Fonden (NNF20OC0060590)
- Danmarks Grundforskningsfond (DNRF 125)
- Dansk Kræftforsknings Fond (R204-A12617-B153)
- Det Frie Forskningsråd (1026-00241B)
- Grantová Agentura České Republiky (GACR 20-28685S)
- Topics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- diethyldithiocarbamate, drug repurposing, Npl4, integrated stress response, translational arrest, nucleolar stress, ribosome biogenesis, autophagy, proteotoxic stress, p53-independent cell death, tumor vulnerability, zebrafish xenograft
- MeSH terms
- Animals, Disulfiram, Humans, Neoplasms, Ribosomes, Zebrafish, Tumor Suppressor Protein p53, Cell Line, Tumor
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