Characterizing the mutational burden, DNA methylation landscape, and proteome of germ cell tumor-related somatic-type malignancies to identify the tissue-of-origin, mechanisms of therapy resistance, and druggable targets.


Journal

British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 12 01 2023
accepted: 04 09 2023
revised: 22 08 2023
pubmed: 20 9 2023
medline: 20 9 2023
entrez: 19 9 2023
Statut: ppublish

Résumé

Germ cell tumors (GCT) might undergo transformation into a somatic-type malignancy (STM), resulting in a cell fate switch to tumors usually found in somatic tissues, such as rhabdomyosarcomas or adenocarcinomas. STM is associated with a poor prognosis, but the molecular and epigenetic mechanisms triggering STM are still enigmatic, the tissue-of-origin is under debate and biomarkers are lacking. To address these questions, we characterized a unique cohort of STM tissues on mutational, epigenetic and protein level using modern and high-throughput methods like TSO assays, 850k DNA methylation arrays and mass spectrometry. For the first time, we show that based on DNA methylation and proteome data carcinoma-related STM more closely resemble yolk-sac tumors, while sarcoma-related STM resemble teratoma. STM harbor mutations in FGF signaling factors (FGF6/23, FGFR1/4) highlighting the corresponding pathway as a therapeutic target. Furthermore, STM utilize signaling pathways, like AKT, FGF, MAPK, and WNT to mediate molecular functions coping with oxidative stress, toxin transport, DNA helicase activity, apoptosis and the cell cycle. Collectively, these data might explain the high therapy resistance of STM. Finally, we identified putative novel biomarkers secreted by STM, like EFEMP1, MIF, and DNA methylation at specific CpG dinucleotides.

Sections du résumé

BACKGROUND BACKGROUND
Germ cell tumors (GCT) might undergo transformation into a somatic-type malignancy (STM), resulting in a cell fate switch to tumors usually found in somatic tissues, such as rhabdomyosarcomas or adenocarcinomas. STM is associated with a poor prognosis, but the molecular and epigenetic mechanisms triggering STM are still enigmatic, the tissue-of-origin is under debate and biomarkers are lacking.
METHODS METHODS
To address these questions, we characterized a unique cohort of STM tissues on mutational, epigenetic and protein level using modern and high-throughput methods like TSO assays, 850k DNA methylation arrays and mass spectrometry.
RESULTS AND CONCLUSIONS CONCLUSIONS
For the first time, we show that based on DNA methylation and proteome data carcinoma-related STM more closely resemble yolk-sac tumors, while sarcoma-related STM resemble teratoma. STM harbor mutations in FGF signaling factors (FGF6/23, FGFR1/4) highlighting the corresponding pathway as a therapeutic target. Furthermore, STM utilize signaling pathways, like AKT, FGF, MAPK, and WNT to mediate molecular functions coping with oxidative stress, toxin transport, DNA helicase activity, apoptosis and the cell cycle. Collectively, these data might explain the high therapy resistance of STM. Finally, we identified putative novel biomarkers secreted by STM, like EFEMP1, MIF, and DNA methylation at specific CpG dinucleotides.

Identifiants

pubmed: 37726478
doi: 10.1038/s41416-023-02425-5
pii: 10.1038/s41416-023-02425-5
pmc: PMC10645790
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1580-1589

Subventions

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : NE 1861/8-1
Organisme : Wilhelm Sander-Stiftung (Wilhelm Sander Foundation)
ID : 2016.042.1 /.2 /.3

Informations de copyright

© 2023. The Author(s).

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Auteurs

Felix Bremmer (F)

Institute of Pathology, University Medical Center Goettingen, Goettingen, Germany.

Pailin Pongratanakul (P)

Department of Urology, Urological Research Laboratory, Translational UroOncology, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Margaretha Skowron (M)

Department of Urology, Urological Research Laboratory, Translational UroOncology, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Yue Che (Y)

Department of Urology, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Annika Richter (A)

Institute of Pathology, University Medical Center Goettingen, Goettingen, Germany.

Stefan Küffer (S)

Institute of Pathology, University Medical Center Goettingen, Goettingen, Germany.

Kirsten Reuter-Jessen (K)

Institute of Pathology, University Medical Center Goettingen, Goettingen, Germany.

Hanibal Bohnenberger (H)

Institute of Pathology, University Medical Center Goettingen, Goettingen, Germany.

Stella Pauls (S)

Molecular Proteomics Laboratory (MPL), Biological and Medical Research Centre (BMFZ), Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Catena Kresbach (C)

Institute of Neuropathology, University Hospital Hamburg-Eppendorf, Hamburg, Germany.

Ulrich Schüller (U)

Institute of Neuropathology, University Hospital Hamburg-Eppendorf, Hamburg, Germany.

Kai Stühler (K)

Molecular Proteomics Laboratory (MPL), Biological and Medical Research Centre (BMFZ), Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Philipp Ströbel (P)

Institute of Pathology, University Medical Center Goettingen, Goettingen, Germany.

Peter Albers (P)

Department of Urology, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Daniel Nettersheim (D)

Department of Urology, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany. Daniel.Nettersheim@med.uni-duesseldorf.de.

Classifications MeSH