UV-radiation and MC1R germline mutations are risk factors for the development of conventional and spitzoid melanomas in children and adolescents.

Exome sequencing MC1R Paediatric melanoma Rare paediatric tumours Tumour-normal sequencing UV-radiation

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 19 05 2023
revised: 24 08 2023
accepted: 30 08 2023
pubmed: 17 9 2023
medline: 17 9 2023
entrez: 16 9 2023
Statut: ppublish

Résumé

Genomic characterisation has led to an improved understanding of adult melanoma. However, the aetiology of melanoma in children is still unclear and identifying the correct diagnosis and therapeutic strategies remains challenging. Exome sequencing of matched tumour-normal pairs from 26 paediatric patients was performed to study the mutational spectrum of melanomas. The cohort was grouped into different categories: spitzoid melanoma (SM), conventional melanoma (CM), and other melanomas (OT). In all patients with CM (n = 10) germline variants associated with melanoma were found in low to moderate melanoma risk genes: in 8 patients MC1R variants, in 2 patients variants in MITF, PTEN and BRCA2. Somatic BRAF mutations were detected in 60% of CMs, homozygous deletions of CDKN2A in 20%, TERTp mutations in 30%. In the SM group (n = 12), 5 patients carried at least one MC1R variant; somatic BRAF mutations were detected in 8.3%, fusions in 25% of the cases. No SM showed a homozygous CDKN2A deletion nor a TERTp mutation. In 81.8% of the CM/SM cases the UV damage signatures SBS7 and/or DBS1 were detected. The patient with melanoma arising in giant congenital nevus (CNM) demonstrated the characteristic NRAS Q61K mutation. UV-radiation and MC1R germline variants are risk factors in the development of conventional and spitzoid paediatric melanomas. Paediatric CMs share genomic similarities with adult CMs while the SMs differ genetically from the CM group. Consistent genetic characterization of all paediatric melanomas will potentially lead to better subtype differentiation, treatment, and prevention in the future. Found in Acknowledgement.

Sections du résumé

BACKGROUND BACKGROUND
Genomic characterisation has led to an improved understanding of adult melanoma. However, the aetiology of melanoma in children is still unclear and identifying the correct diagnosis and therapeutic strategies remains challenging.
METHODS METHODS
Exome sequencing of matched tumour-normal pairs from 26 paediatric patients was performed to study the mutational spectrum of melanomas. The cohort was grouped into different categories: spitzoid melanoma (SM), conventional melanoma (CM), and other melanomas (OT).
FINDINGS RESULTS
In all patients with CM (n = 10) germline variants associated with melanoma were found in low to moderate melanoma risk genes: in 8 patients MC1R variants, in 2 patients variants in MITF, PTEN and BRCA2. Somatic BRAF mutations were detected in 60% of CMs, homozygous deletions of CDKN2A in 20%, TERTp mutations in 30%. In the SM group (n = 12), 5 patients carried at least one MC1R variant; somatic BRAF mutations were detected in 8.3%, fusions in 25% of the cases. No SM showed a homozygous CDKN2A deletion nor a TERTp mutation. In 81.8% of the CM/SM cases the UV damage signatures SBS7 and/or DBS1 were detected. The patient with melanoma arising in giant congenital nevus (CNM) demonstrated the characteristic NRAS Q61K mutation.
INTERPRETATION CONCLUSIONS
UV-radiation and MC1R germline variants are risk factors in the development of conventional and spitzoid paediatric melanomas. Paediatric CMs share genomic similarities with adult CMs while the SMs differ genetically from the CM group. Consistent genetic characterization of all paediatric melanomas will potentially lead to better subtype differentiation, treatment, and prevention in the future.
FUNDING BACKGROUND
Found in Acknowledgement.

Identifiants

pubmed: 37716236
pii: S2352-3964(23)00363-8
doi: 10.1016/j.ebiom.2023.104797
pmc: PMC10511785
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104797

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests Outside of submitted work: IBB: Institutional grant from Biontech. O.R. and C.Sc.: grants: Deutsche Forschungsgemeinschaft (DFG), Deutsche Krebshilfe (DKH), European Union (EU), grants to the institution from Illumina and BMS Stiftung Immunonkologie. U.L.S: grants: MSD; support for attending meeting and/or travel: Sun Pharma, Pierre Fabre; participation on a Data Safety Monitoring Board or Advisory Board: MSD, Novartis, Sun Pharma, Almirall, Roche, Sanofi; ADO board member. T.E.: Consulting fees: Bristol-Myers Squibb, MSD, Novartis, Almirall, Hermal, CureVac, Immunocore, Sanofi. S.O.: grants: DFG, Deutsche Luft und Raumfahrt Gesellschaft (DLR), European Union (EU), Bundesministerium für Bildung und Forschung (BMBF), Deutsche Krebshilfe, Bundesministerium für Arbeit und Soziales (BMSA); presentation: Illumina; support for attending meeting and/or travel: Oxford Nanopore Technologies. S.F.: grants: NeraCare, Skyline Dx, Biontech,; speakers honoraria: Kyowa Kirin, Recordati, Takeda Pharmaceuticals.

Auteurs

Alexandra Liebmann (A)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Jakob Admard (J)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Sorin Armeanu-Ebinger (S)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Hannah Wild (H)

Paediatric Hematology and Oncology, University Children's Hospital Tübingen, Tübingen, Germany.

Michael Abele (M)

Paediatric Hematology and Oncology, University Children's Hospital Tübingen, Tübingen, Germany.

Axel Gschwind (A)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Olga Seibel-Kelemen (O)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Christian Seitz (C)

Paediatric Hematology and Oncology, University Children's Hospital Tübingen, Tübingen, Germany.

Irina Bonzheim (I)

Institute of Pathology and Neuropathology, University Hospital Tübingen, Tübingen, Germany.

Olaf Riess (O)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

German Demidov (G)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Marc Sturm (M)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Malou Schadeck (M)

SYNLAB MVZ Human Genetics Freiburg GmbH, Freiburg, Germany.

Michaela Pogoda (M)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany; NGS Competence Center Tübingen, Tübingen, Germany.

Ewa Bien (E)

Department of Paediatrics, Hematology, Oncology, Medical University of Gdansk, Poland.

Malgorzata Krawczyk (M)

Department of Paediatrics, Hematology, Oncology, Medical University of Gdansk, Poland.

Eva Jüttner (E)

Department of Pathology, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Schleswig-Holstein, Germany.

Thomas Mentzel (T)

Dermatohistopathology Friedrichshafen, Friedrichshafen, Germany.

Maja Cesen (M)

Department of Paediatric Haematology and Oncology, University Hospital Ljubljana, Ljubljana, Slovenia.

Elke Pfaff (E)

Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.

Michal Kunc (M)

Department of Pathomorphology, Medical University of Gdansk, Poland.

Stephan Forchhammer (S)

Department of Dermatology, Center for Dermatooncology, University Hospital Tübingen, Tübingen, Germany.

Andrea Forschner (A)

Department of Dermatology, Center for Dermatooncology, University Hospital Tübingen, Tübingen, Germany.

Ulrike Leiter-Stöppke (U)

Department of Dermatology, Center for Dermatooncology, University Hospital Tübingen, Tübingen, Germany.

Thomas K Eigentler (TK)

Department of Dermatology, Venereology and Allergology, Charite Universitätsmedizin Berlin, Berlin, Germany.

Dominik T Schneider (DT)

Clinic of Paediatrics, Dortmund Municipal Hospital, Dortmund, Germany.

Christopher Schroeder (C)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Stephan Ossowski (S)

Institute of Medical Genetics and Applied Genomics, University Hospital Tübingen, Tübingen, Germany.

Ines B Brecht (IB)

Paediatric Hematology and Oncology, University Children's Hospital Tübingen, Tübingen, Germany. Electronic address: ines.brecht@med.uni-tuebingen.de.

Classifications MeSH