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A new G-quadruplex-specific photosensitizer inducing genome instability in cancer cells by triggering oxidative DNA damage and impeding replication fork progression
Umeå University, Faculty of Medicine, Department of Medical Biochemistry and Biophysics.ORCID iD: 0000-0002-7815-4494
Univ Angers, CNRS, MOLTECH-ANJOU, France.
Univ Angers, CNRS, MOLTECH-ANJOU, France.
Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
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2023 (English)In: Nucleic Acids Research, ISSN 0305-1048, E-ISSN 1362-4962, Vol. 51, no 12, p. 6264-6285Article in journal (Refereed) Published
Abstract [en]

Photodynamic therapy (PDT) ideally relies on the administration, selective accumulation and photoactivation of a photosensitizer (PS) into diseased tissues. In this context, we report a new heavy-atom-free fluorescent G-quadruplex (G4) DNA-binding PS, named DBI. We reveal by fluorescence microscopy that DBI preferentially localizes in intraluminal vesicles (ILVs), precursors of exosomes, which are key components of cancer cell proliferation. Moreover, purified exosomal DNA was recognized by a G4-specific antibody, thus highlighting the presence of such G4-forming sequences in the vesicles. Despite the absence of fluorescence signal from DBI in nuclei, light-irradiated DBI-treated cells generated reactive oxygen species (ROS), triggering a 3-fold increase of nuclear G4 foci, slowing fork progression and elevated levels of both DNA base damage, 8-oxoguanine, and double-stranded DNA breaks. Consequently, DBI was found to exert significant phototoxic effects (at nanomolar scale) toward cancer cell lines and tumor organoids. Furthermore, in vivo testing reveals that photoactivation of DBI induces not only G4 formation and DNA damage but also apoptosis in zebrafish, specifically in the area where DBI had accumulated. Collectively, this approach shows significant promise for image-guided PDT.

Place, publisher, year, edition, pages
Oxford University Press, 2023. Vol. 51, no 12, p. 6264-6285
National Category
Biochemistry Molecular Biology Cell and Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-212227DOI: 10.1093/nar/gkad365ISI: 000988008500001PubMedID: 37191066Scopus ID: 2-s2.0-85164253573OAI: oai:DiVA.org:umu-212227DiVA, id: diva2:1783438
Funder
Swedish Cancer Society, 22 2380 PjSwedish Research Council, VR-MH 2021–02468Knut and Alice Wallenberg Foundation, KAW 2021-0173Swedish Cancer Society, 21 0302 PT 01 HWenner-Gren Foundations, UPD2020-0097Swedish Cancer Society, 20 0827 PjFCancerforskningsfonden i Norrland, LP 22-2312Cancerforskningsfonden i Norrland, LP20 1024 2257Cancerforskningsfonden i Norrland, LP 21–2298Swedish Research Council, 2017-01531Swedish Society of Medicine, SLS-890521Region Västerbotten, RV-930167Sjöberg FoundationKnut and Alice Wallenberg Foundation, KAW 2015.0114Marianne and Marcus Wallenberg Foundation, MMW 2020.0189Swedish Cancer Society, 20 1339 PjFAvailable from: 2023-07-21 Created: 2023-07-21 Last updated: 2025-10-23Bibliographically approved
In thesis
1. Tumour progression and photodynamic therapy in a zebrafish model of rhabdomyosarcoma
Open this publication in new window or tab >>Tumour progression and photodynamic therapy in a zebrafish model of rhabdomyosarcoma
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Rhabdomyosarcoma (RMS) is the most common pediatric soft-tissue cancer, which primarily develops in muscle tissue during childhood. Despite advances in treatment, outcomes for many patients remain poor. This thesis aims to investigate RMS progression and regression in different genetic contexts, using zebrafish RMS models to evaluate a novel molecule as a potential RMS treatment.

Pax3 and Pax7 transcription factors play important roles in fusion-positive RMS. However, their role in fusion-negative RMS remains less clear. Therefore, we aimed to examine how the lack of Pax3 and Pax7 influences fusion-negative RMS formation and progression.

In the first study, we investigated the role of Pax3 in RAS-driven, fusion-negative RMS. Using pax3a-/-;pax3b-/- double mutant zebrafish, we found that the RAS/MAPK signalling pathway was downregulated in the mutants compared to controls, correlating with a delay in tumour progression. These findings suggest that, in fusion-negative RMS, Pax3 also contributes to tumour development by modulating oncogenic signalling. 

In the second study, we aimed to explore the role of Pax7 in fusion-negative RMS, using a pax7-deficient zebrafish model. Our RNA-seq and lipidomics analyses showed downregulation of mitochondrial-related genes, decreased cardiolipin levels, and altered microtubule dynamics in pax7a-/-;pax7b-/- mutants compared to healthy wild-type fish. We also showed lower mitochondria labelling in pax7a-/-;pax7b-/- tumours compared to wild-type tumours. These findings indicate that Pax7 plays an important role in maintaining mitochondrial membrane integrity and function in healthy and tumourigenic conditions.

In the last part of the thesis, we aimed to evaluate the feasibility of photodynamic therapy using a novel photosensitizer for cancer treatment.

In the third study we designed and synthesized a heavy-atom-free light-inducible compound called dibenzothioxanthene imide (DBI), which binds to G-quadruplex (G4) DNA. Upon targeted photoactivation of DBI, it produced reactive oxygen species and caused DNA damage in human cancer cells and healthy zebrafish embryos. 

Complementing this, the last study explored the potential of photodynamic therapy using the photosensitizer DBI for treating RMS in zebrafish models. Treatment with light-activated DBI resulted in targeted apoptosis and tumour regression, compared to control treatments. In addition, RMS tissue was more affected by photoactivated DBI than healthy tissue, likely due to the higher accumulation of G4 structures in tumours compared to healthy regions.

Together, these findings uncover new roles of Pax3 and Pax7 in RMS biology using zebrafish models and highlight the therapeutic potential of G4-targeted photodynamic therapy for RMS.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2025. p. 60
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2384
Keywords
rhabdomyosarcoma, zebrafish, photodynamic therapy, G-quadruplex, cancer, Pax3, Pax7
National Category
Basic Cancer Research
Identifiers
urn:nbn:se:umu:diva-245793 (URN)978-91-8070-816-6 (ISBN)978-91-8070-815-9 (ISBN)
Public defence
2025-11-20, BIO.E.203 - Aula Biologica, Biologihuset, Umeå, 09:00 (English)
Opponent
Supervisors
Available from: 2025-10-30 Created: 2025-10-23 Last updated: 2025-10-29Bibliographically approved

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Deiana, MarcoKahsay, AbrahaPatel, Ankit KumarSengupta, PallabiObi, IkennaRodriguez-Marquez, EvaÖhlund, Danielvon Hofsten, JonasSabouri, Nasim

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Deiana, MarcoKahsay, AbrahaPatel, Ankit KumarSengupta, PallabiObi, IkennaRodriguez-Marquez, EvaÖhlund, Danielvon Hofsten, JonasSabouri, Nasim
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Department of Medical Biochemistry and BiophysicsDepartment of Integrative Medical Biology (IMB)Wallenberg Centre for Molecular Medicine at Umeå University (WCMM)Oncology
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