Oncotarget

Research Papers:

Full in-frame exon 3 skipping of BRCA2 confers high risk of breast and/or ovarian cancer

Sandrine M. Caputo _, Mélanie Léone, Francesca Damiola, Asa Ehlen, Aura Carreira, Pascaline Gaidrat, Alexandra Martins, Rita D. Brandão, Ana Peixoto, Ana Vega, Claude Houdayer, Capucine Delnatte, Myriam Bronner, Danièle Muller, Laurent Castera, Marine Guillaud-Bataille, Inge Søkilde, Nancy Uhrhammer, Sophie Demontety, Hélène Tubeuf, Gaïa Castelain, French COVAR group collaborators, Uffe Birk Jensen, Ambre Petitalot, Sophie Krieger, Cédrick Lefol, Virginie Moncoutier, Nadia Boutry-Kryza, Henriette Roed Nielsen, Olga Sinilnikova, Dominique Stoppa-Lyonnet, Amanda B. Spurdle, Manuel R. Teixeira, Florence Coulet, Mads Thomassen and Etienne Rouleau

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Oncotarget. 2018; 9:17334-17348. https://doi.org/10.18632/oncotarget.24671

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Abstract

Sandrine M. Caputo1, Mélanie Léone2,*, Francesca Damiola3,*, Asa Ehlen4,5,*, Aura Carreira4,5, Pascaline Gaidrat6, Alexandra Martins6, Rita D. Brandão7, Ana Peixoto8, Ana Vega8, Claude Houdayer1,10, Capucine Delnatte11, Myriam Bronner12, Danièle Muller13, Laurent Castera14, Marine Guillaud-Bataille15, Inge Søkilde16, Nancy Uhrhammer17, Sophie Demontety1, Hélène Tubeuf6,24, Gaïa Castelain6, French COVAR group collaborators, Uffe Birk Jensen18, Ambre Petitalot1, Sophie Krieger14, Cédrick Lefol1, Virginie Moncoutier1, Nadia Boutry-Kryza2, Henriette Roed Nielsen19, Olga Sinilnikova2,**, Dominique Stoppa-Lyonnet1,10, Amanda B. Spurdle20, Manuel R. Teixeira8,21,*, Florence Coulet22,*, Mads Thomassen23,* and Etienne Rouleau1,*

1Institut Curie, Service de Génétique, Paris, France

2Unité Mixte de Génétique Constitutionnelle des Cancers Fréquents, Hospices Civils de Lyon/Centre Léon Bérard, Lyon, France

3Centre Léon Bérard, Lyon, France

4Institut Curie, PSL Research University, CNRS UMR3348, Orsay, France

5Université Paris Sud, Université Paris-Saclay, CNRS UMR3348, Orsay, France

6Inserm-U1245, UNIROUEN, Normandie University, Normandy Centre for Genomic and Personalized Medicine, Rouen, France

7Maastricht University, Maastricht, Netherlands

8Department of Genetics, Portuguese Oncology Institute, Porto, Portugal

9Fundación Pública Galega de Medicina Xenómica-SERGAS, Grupo de Medicina Xenómica-USC, CIBERER, IDIS, Santiago de Compostela, Spain

10Université Paris Descartes, Paris, France

11Service de Génétique médicale, CHU Nantes, Nantes, France

12Service de Génétique, CHU Nancy Brabois, Nancy, France

13Laboratoire d’Oncogénétique, Centre Paul Strauss, Strasbourg, France

14Laboratoire de biologie et de génétique du cancer, CLCC François Baclesse, INSERM 1079 Centre Normand de Génomique et de Médecine Personnalisée, Caen, France

15Institut Gustave Roussy, Villejuif, France

16Section of Molecular Diagnostics, Department of Clinical Biochemistry, Aalborg University Hospital, Aalborg, Denmark

17Laboratoire de Biologie Médicale, CLCC Jean Perrin, Clermont-Ferrand, France

18Department of Clinical Genetics, Aarhus University Hospital, Aarhus, Denmark

19Department of Clinical Genetics, Vejle Hospital, Odense, Denmark

20Genetics and Comp utational Biology Division, QIMR Berghofer Medical Research Institute, Herston, Brisbane, Australia

21Institute of Biomedical Sciences, University of Porto, Porto, Portugal

22Laboratoire d’Oncogénétique et d’Angiogénétique Moléculaire, Groupe Hospitalier Pitié-Salpêtrière, Paris, France

23Department of Clinical Genetics, Odense University Hospital, Odense, Denmark

24Interactive Biosoftware, Rouen, France

*These authors have contributed equally to this work

**Deceased

Members of the French COVAR group collaborators are listed in the Appendix

Correspondence to:

Sandrine M. Caputo, email: [email protected]

Keywords: BRCA2 exon3; PALB2; variants; RNA splicing defects; splice donor site

Received: September 07, 2017    Accepted: February 24, 2018    Published: April 03, 2018

ABSTRACT

Germline pathogenic variants in the BRCA2 gene are associated with a cumulative high risk of breast/ovarian cancer. Several BRCA2 variants result in complete loss of the exon-3 at the transcript level. The pathogenicity of these variants and the functional impact of loss of exon 3 have yet to be established.

As a collaboration of the COVAR clinical trial group (France), and the ENIGMA consortium for investigating breast cancer gene variants, this study evaluated 8 BRCA2 variants resulting in complete deletion of exon 3. Clinical information for 39 families was gathered from Portugal, France, Denmark and Sweden. Multifactorial likelihood analyses were conducted using information from 293 patients, for 7 out of the 8 variants (including 6 intronic). For all variants combined the likelihood ratio in favor of causality was 4.39*1025. These results provide convincing evidence for the pathogenicity of all examined variants that lead to a total exon 3 skipping, and suggest that other variants that result in complete loss of exon 3 at the molecular level could be associated with a high risk of cancer comparable to that associated with classical pathogenic variants in BRCA1 or BRCA2 gene. In addition, our functional study shows, for the first time, that deletion of exon 3 impairs the ability of cells to survive upon Mitomycin-C treatment, supporting lack of function for the altered BRCA2 protein in these cells.

Finally, this study demonstrates that any variant leading to expression of only BRCA2 delta-exon 3 will be associated with an increased risk of breast and ovarian cancer.


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