A de novo germline pathogenic BRCA1 variant identified following an osteosarcoma pangenomic molecular analysis.

de novo BRCA1 Osteosarcoma Tumor sequencing Whole genome

Journal

Familial cancer
ISSN: 1573-7292
Titre abrégé: Fam Cancer
Pays: Netherlands
ID NLM: 100898211

Informations de publication

Date de publication:
19 May 2024
Historique:
received: 21 01 2024
accepted: 17 04 2024
medline: 20 5 2024
pubmed: 20 5 2024
entrez: 19 5 2024
Statut: aheadofprint

Résumé

De novo germline pathogenic variants (gPV) of the BReast CAncer 1 (BRCA1) gene are very rare. Only a few have been described up to date, usually in patients with a history of ovarian or breast cancer. Here, we report the first case of an incidental de novo BRCA1 germline pathogenic variant which was identified within the framework of the Plan France Médecine Génomique (PFMG) 2025 French national tumor sequencing program. The proband was a 29-year-old man diagnosed with metastatic osteosarcoma. Tumor whole exome sequencing identified a BRCA1 c.3756_3759del p.(Ser1253Argfs*10) pathogenic variant without loss-of-heterozygosity. A low genomic instability score and the absence of single base substitution signatures of homologous recombination deficiency suggested that the BRCA1 variant was not driver in the osteosarcoma tumorigenesis. Germline whole genome sequencing asserted the germline nature of this variant, with a 36% allele frequency, suggesting a mosaicism caused by a post-zygotic mutational event. The proband's family (parents and siblings) were not carriers of this variant confirming the de novo occurrence. Tumor sequencing programs like the French PFMG 2025 have been implemented worldwide and may help identify new gPV, including de novo variants.

Identifiants

pubmed: 38763984
doi: 10.1007/s10689-024-00393-0
pii: 10.1007/s10689-024-00393-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Maxwell KN, Domchek SM, Nathanson KL, Robson ME (2016) Population frequency of germline BRCA1/2 mutations. J Clin Oncol 34:4183–4185
doi: 10.1200/JCO.2016.67.0554 pubmed: 27551127
Li S, Silvestri V, Leslie G, Rebbeck TR, Neuhausen SL, Hopper JL, Nielsen HR, Lee A, Yang X, McGuffog L, Parsons MT, Andrulis IL, Arnold N, Belotti M, Borg Å, Buecher B, Buys SS, Caputo SM, Chung WK, Colas C, Colonna SV, Cook J, Daly MB, de la Hoya M, de Pauw A, Delhomelle H, Eason J, Engel C, Evans DG, Faust U, Fehm TN, Fostira F, Fountzilas G, Frone M, Garcia-Barberan V, Garre P, Gauthier-Villars M, Gehrig A, Glendon G, Goldgar DE, Golmard L, Greene MH, Hahnen E, Hamann U, Hanson H, Hassan T, Hentschel J, Horvath J, Izatt L, Janavicius R, Jiao Y, John EM, Karlan BY, Kim S-W, Konstantopoulou I, Kwong A, Laugé A, Lee JW, Lesueur F, Mebirouk N, Meindl A, Mouret-Fourme E, Musgrave H, Ngeow Yuen Yie J, Niederacher D, Park SK, Pedersen IS, Ramser J, Ramus SJ, Rantala J, Rashid MU, Reichl F, Ritter J, Rump A, Santamariña M, Saule C, Schmidt G, Schmutzler RK, Senter L, Shariff S, Singer CF, Southey MC, Stoppa-Lyonnet D, Sutter C, Tan Y, Teo SH, Terry MB, Thomassen M, Tischkowitz M, Toland AE, Torres D, Vega A, Wagner SA, Wang-Gohrke S, Wappenschmidt B, Weber BHF, Yannoukakos D, Spurdle AB, Easton DF, Chenevix-Trench G, Ottini L, Antoniou AC (2022) Cancer risks associated with BRCA1 and BRCA2 pathogenic variants. J Clin Oncol 40(14):1529–1541
doi: 10.1200/JCO.21.02112 pubmed: 35077220 pmcid: 9084432
Tlemsani C, Pasmant E, Boudou-Rouquette P, Bellesoeur A, Even J, Larousserie F, Reyes C, Gentien D, Alexandre J, Vidaud M, Anract P, Leroy K, Goldwasser F (2018) BRCA2 loss-of-function and high sensitivity to cisplatin-based chemotherapy in a patient with a pleomorphic soft tissue sarcoma: effect of genomic medicine. Am J Med Sci 356:404–407
doi: 10.1016/j.amjms.2018.04.015 pubmed: 30041945
Ballinger ML, Goode DL, Ray-Coquard I, James PA, Mitchell G, Niedermayr E, Puri A, Schiffman JD, Dite GS, Cipponi A, Maki RG, Brohl AS, Myklebost O, Stratford EW, Lorenz S, Ahn S-M, Ahn J-H, Kim JE, Shanley S, Beshay V, Randall RL, Judson I, Seddon B, Campbell IG, Young M-A, Sarin R, Blay J-Y, O’Donoghue SI, Thomas DM, International Sarcoma Kindred Study (2016) Monogenic and polygenic determinants of sarcoma risk: an international genetic study. Lancet Oncol 17:1261–71
doi: 10.1016/S1470-2045(16)30147-4 pubmed: 27498913
Golmard L, Delnatte C, Laugé A, Moncoutier V, Lefol C, Abidallah K, Tenreiro H, Copigny F, Giraudeau M, Guy C, Barbaroux C, Amorim G, Briaux A, Guibert V, Tarabeux J, Caputo S, Collet A, Gesta P, Ingster O, Stern M-H, Rouleau E, de Pauw A, Gauthier-Villars M, Buecher B, Bézieau S, Stoppa-Lyonnet D, Houdayer C (2016) Breast and ovarian cancer predisposition due to de novo BRCA1 and BRCA2 mutations. Oncogene 35:1324–1327
doi: 10.1038/onc.2015.181 pubmed: 26028024
Tesoriero A, Andersen C, Southey M, Somers G, McKay M, Armes J, McCredie M, Giles G, Hopper JL, Venter D (1999) De novo BRCA1 mutation in a patient with breast cancer and an inherited BRCA2 mutation. Am J Hum Genet 65:567–569
doi: 10.1086/302503 pubmed: 10417300 pmcid: 1377956
Edwards E, Yearwood C, Sillibourne J, Baralle D, Eccles D (2009) Identification of a de novo BRCA1 mutation in a woman with early onset bilateral breast cancer. Fam Cancer 8:479–482
doi: 10.1007/s10689-009-9270-8 pubmed: 19629752
Friedman E, Efrat N, Soussan-Gutman L, Dvir A, Kaplan Y, Ekstein T, Nykamp K, Powers M, Rabideau M, Sorenson J, Topper S (2015) Low-level constitutional mosaicism of a de novo BRCA1 gene mutation. Br J Cancer 112:765–768
doi: 10.1038/bjc.2015.14 pubmed: 25633036 pmcid: 4333503
Kwong A, Ng EKO, Tang EYH, Wong CLP, Law FBF, Leung CPH, Chan A, Cheung MT, To MY, Ma ESK, West DW, Ford JM (2011) A novel de novo BRCA1 mutation in a Chinese woman with early onset breast cancer. Fam Cancer 10:233–237
doi: 10.1007/s10689-011-9429-y pubmed: 21404118 pmcid: 3100488
Garcia-Casado Z, Romero I, Fernandez-Serra A, Rubio L, Llopis F, Garcia A, Llombart P, Lopez-Guerrero JA (2011) A de novo complete BRCA1 gene deletion identified in a Spanish woman with early bilateral breast cancer. BMC Med Genet 12:134
doi: 10.1186/1471-2350-12-134 pubmed: 21989022 pmcid: 3207938
De Leeneer K, Coene I, Crombez B, Simkens J, Van den Broecke R, Bols A, Stragier B, Vanhoutte I, De Paepe A, Poppe B, Claes K (2012) Prevalence of BRCA1/2 mutations in sporadic breast/ovarian cancer patients and identification of a novel de novo BRCA1 mutation in a patient diagnosed with late onset breast and ovarian cancer: implications for genetic testing. Breast Cancer Res Treat 132:87–95
doi: 10.1007/s10549-011-1544-9 pubmed: 21553119
Delon I, Taylor A, Molenda A, Drummond J, Oakhill K, Girling A, Liu H, Whittaker J, Treacy R, Tischkowitz M (2013) A germline mosaic BRCA1 exon deletion in a woman with bilateral basal-like breast cancer. Clin Genet 84:297–299
doi: 10.1111/cge.12057 pubmed: 23216102
Scherz A, Stoll S, Rothlisberger B, Rabaglio M (2023) A new de novo BRCA1 mutation in a young breast cancer patient: a case report. Appl Clin Genet 16:83–87
doi: 10.2147/TACG.S405120 pubmed: 37197323 pmcid: 10184889
Veltman JA, Brunner HG (2012) De novo mutations in human genetic disease. Nat Rev Genet 13:565–575
doi: 10.1038/nrg3241 pubmed: 22805709
RESERVED IU-AR. Orphanet: Li Fraumeni syndrome. https://www.orpha.net/consor/cgi-bin/OC_Exp.php?lng=EN&Expert=524. Accessed 2 Aug 2023
Kumar-Sinha C, Chinnaiyan AM (2018) Precision oncology in the age of integrative genomics. Nat Biotechnol 36:46–60
doi: 10.1038/nbt.4017 pubmed: 29319699 pmcid: 6364676
Malone ER, Oliva M, Sabatini PJB, Stockley TL, Siu LL (2020) Molecular profiling for precision cancer therapies. Genome Med 12:8
doi: 10.1186/s13073-019-0703-1 pubmed: 31937368 pmcid: 6961404
Niu B, Ye K, Zhang Q, Lu C, Xie M, McLellan MD, Wendl MC, Ding L (2014) MSIsensor: microsatellite instability detection using paired tumor-normal sequence data. Bioinformatics 30:1015–1016
doi: 10.1093/bioinformatics/btt755 pubmed: 24371154
Ray-Coquard I, Pautier P, Pignata S, Pérol D, González-Martín A, Berger R, Fujiwara K, Vergote I, Colombo N, Mäenpää J, Selle F, Sehouli J, Lorusso D, Guerra Alía EM, Reinthaller A, Nagao S, Lefeuvre-Plesse C, Canzler U, Scambia G, Lortholary A, Marmé F, Combe P, de Gregorio N, Rodrigues M, Buderath P, Dubot C, Burges A, You B, Pujade-Lauraine E, Harter P (2019) Olaparib plus bevacizumab as first-line maintenance in ovarian cancer. N Engl J Med 381:2416–2428
doi: 10.1056/NEJMoa1911361 pubmed: 31851799
Alexandrov LB, Kim J, Haradhvala NJ, Huang MN, Tian Ng AW, Wu Y, Boot A, Covington KR, Gordenin DA, Bergstrom EN, Islam SMA, Lopez-Bigas N, Klimczak LJ, McPherson JR, Morganella S, Sabarinathan R, Wheeler DA, Mustonen V, Getz G, Rozen SG, Stratton MR (2020) The repertoire of mutational signatures in human cancer. Nature 578:94–101
doi: 10.1038/s41586-020-1943-3 pubmed: 32025018 pmcid: 7054213
Rebbeck TR, Friebel TM, Friedman E, Hamann U, Huo D, Kwong A, Olah E, Olopade OI, Solano AR, Teo S-H, Thomassen M, Weitzel JN, Chan T, Couch FJ, Goldgar DE, Kruse TA, Palmero EI, Park SK, Torres D, van Rensburg EJ, McGuffog L, Parsons MT, Leslie G, Aalfs CM, Abugattas J, Adlard J, Agata S, Aittomäki K, Andrews L, Andrulis IL, Arason A, Arnold N, Arun BK, Asseryanis E, Auerbach L, Azzollini J, Balmaña J, Barile M, Barkardottir RB, Barrowdale D, Benitez J, Berger A, Berger R, Blanco AM, Blazer KR, Blok MJ, Bonadona V, Bonanni B, Bradbury AR, Brewer C, Buecher B, Buys SS, Caldes T, Caliebe A, Caligo MA, Campbell I, Caputo S, Chiquette J, Chung WK, Claes KBM, Collée JM, Cook J, Davidson R, de la Hoya M, De Leeneer K, de Pauw A, Delnatte C, Diez O, Ding YC, Ditsch N, Domchek SM, Dorfling CM, Velazquez C, Dworniczak B, Eason J, Easton DF, Eeles R, Ehrencrona H, Ejlertsen B, Engel C, Engert S, Evans DG, Faivre L, Feliubadaló L, Ferrer SF, Foretova L, Fowler J, Frost D, Galvão HCR, Ganz PA, Garber J, Gauthier-Villars M, Gehrig A, Gerdes A-M, Gesta P, Giannini G, Giraud S, Glendon G, Godwin AK, Greene MH, Gronwald J, Gutierrez-Barrera A, Hahnen E, Hauke J, Henderson A, Hentschel J, Hogervorst FBL, Honisch E, Imyanitov EN, Isaacs C, Izatt L, Izquierdo A, Jakubowska A, James P, Janavicius R, Jensen UB, John EM, Joseph V, Kaczmarek K, Karlan BY, Kast K, Kim S-W, Konstantopoulou I, Korach J, Laitman Y, Lasa A, Lasset C, Lázaro C, Lee A, Lee MH, Lester J, Lesueur F, Liljegren A, Lindor NM, Longy M, Loud JT, Lu KH, Lubinski J, Machackova E, Manoukian S, Mari V, Martínez-Bouzas C, Matrai Z, Mebirouk N, Meijers-Heijboer HEJ, Meindl A, Mensenkamp AR, Mickys U, Miller A, Montagna M, Moysich KB, Mulligan AM, Musinsky J, Neuhausen SL, Nevanlinna H, Ngeow J, Nguyen HP, Niederacher D, Nielsen HR, Nielsen FC, Nussbaum RL, Offit K, Öfverholm A, Ong K, Osorio A, Papi L, Papp J, Pasini B, Pedersen IS, Peixoto A, Peruga N, Peterlongo P, Pohl E, Pradhan N, Prajzendanc K, Prieur F, Pujol P, Radice P, Ramus SJ, Rantala J, Rashid MU, Rhiem K, Robson M, Rodriguez GC, Rogers MT, Rudaitis V, Schmidt AY, Schmutzler RK, Senter L, Shah PD, Sharma P, Side LE, Simard J, Singer CF, Skytte A-B, Slavin TP, Snape K, Sobol H, Southey M, Steele L, Steinemann D, Sukiennicki G, Sutter C, Szabo CI, Tan YY, Teixeira MR, Terry MB, Teulé A, Thomas A, Thull DL, Tischkowitz M, Tognazzo S, Toland AE, Topka S, Trainer AH, Tung N, van Asperen CJ, van der Hout AH, van der Kolk LE, van der Luijt RB, Van Heetvelde M, Varesco L, Varon-Mateeva R, Vega A, Villarreal-Garza C, von Wachenfeldt A, Walker L, Wang-Gohrke S, Wappenschmidt B, Weber BHF, Yannoukakos D, Yoon S-Y, Zanzottera C, Zidan J, Zorn KK, Hutten Selkirk CG, Hulick PJ, Chenevix-Trench G, Spurdle AB, Antoniou AC, Nathanson KL (2018) Mutational spectrum in a worldwide study of 29,700 families with BRCA1 or BRCA2 mutations. Hum Mutat 39:593–620
doi: 10.1002/humu.23406 pubmed: 29446198 pmcid: 5903938
Raymond VM, Gray SW, Roychowdhury S, Joffe S, Chinnaiyan AM, Parsons DW, Plon SE, Clinical Sequencing Exploratory Research Consortium Tumor Working Group (2016) Germline findings in tumor-only sequencing: points to consider for clinicians and laboratories. J Natl Cancer Inst 108:djv351
doi: 10.1093/jnci/djv351 pubmed: 26590952
Slavin TP, Banks KC, Chudova D, Oxnard GR, Odegaard JI, Nagy RJ, Tsang KWK, Neuhausen SL, Gray SW, Cristofanilli M, Rodriguez AA, Bardia A, Leyland-Jones B, Janicek MF, Lilly M, Sonpavde G, Lee CE, Lanman RB, Meric-Bernstam F, Kurzrock R, Weitzel JN (2018) Identification of incidental germline mutations in patients with advanced solid tumors who underwent cell-free circulating tumor DNA sequencing. J Clin Oncol 36:JCO1800328
doi: 10.1200/JCO.18.00328 pubmed: 30339520
Huang K-L, Mashl RJ, Wu Y, Ritter DI, Wang J, Oh C, Paczkowska M, Reynolds S, Wyczalkowski MA, Oak N, Scott AD, Krassowski M, Cherniack AD, Houlahan KE, Jayasinghe R, Wang L-B, Zhou DC, Liu D, Cao S, Kim YW, Koire A, McMichael JF, Hucthagowder V, Kim T-B, Hahn A, Wang C, McLellan MD, Al-Mulla F, Johnson KJ, Cancer Genome Atlas Research Network, Lichtarge O, Boutros PC, Raphael B, Lazar AJ, Zhang W, Wendl MC, Govindan R, Jain S, Wheeler D, Kulkarni S, Dipersio JF, Reimand J, Meric-Bernstam F, Chen K, Shmulevich I, Plon SE, Chen F, Ding L (2018) Pathogenic germline variants in 10,389 adult cancers. Cell 173:355-370.e14
doi: 10.1016/j.cell.2018.03.039 pubmed: 29625052 pmcid: 5949147

Auteurs

Adrien Mouren (A)

Department of Medical Oncology, Cochin Hospital, Paris Cancer Institute CARPEM, Université Paris Cité, APHP.Centre, Paris, France.

Albain Chansavang (A)

Department of Molecular Genetics, Fédération de Génétique et Médecine Génomique, Cochin Hospital, Université Paris Cité, APHP.Centre, Paris, France.
Institut Cochin, INSERM U1016, CNRS UMR8104, Université Paris Cité, CARPEM, Paris, France.

Nadim Hamzaoui (N)

Department of Molecular Genetics, Fédération de Génétique et Médecine Génomique, Cochin Hospital, Université Paris Cité, APHP.Centre, Paris, France.
Institut Cochin, INSERM U1016, CNRS UMR8104, Université Paris Cité, CARPEM, Paris, France.

Arunya Srikaran (A)

Department of Medical Oncology, Cochin Hospital, Paris Cancer Institute CARPEM, Université Paris Cité, APHP.Centre, Paris, France.

Pierre Laurent-Puig (P)

Institut du Cancer Paris Carpem, AP-HP, Genomic Medicine of Tumors and Cancers Department, Fédération de Génétique et Médecine Génomique, Université Paris Cité, APHP.Centre, Paris, France.
Centre de Recherche des Cordeliers, INSERM, CNRS SNC 5096, Université Paris Cité, Paris, France.

Laetitia Marisa (L)

Multi-Site Medical Biology Laboratory SeqOIA, Paris, France.

Sixtine De Percin (S)

Department of Medical Oncology, Cochin Hospital, Paris Cancer Institute CARPEM, Université Paris Cité, APHP.Centre, Paris, France.

Audrey Lupo (A)

Department of Pathology, Cochin Hospital, Paris Cancer Institute CARPEM, Université Paris Cité, APHP.Centre, Paris, France.

Frédérique Larousserie (F)

Department of Pathology, Cochin Hospital, Paris Cancer Institute CARPEM, Université Paris Cité, APHP.Centre, Paris, France.

Hélène Blons (H)

Institut du Cancer Paris Carpem, AP-HP, Genomic Medicine of Tumors and Cancers Department, Fédération de Génétique et Médecine Génomique, Université Paris Cité, APHP.Centre, Paris, France.
Centre de Recherche des Cordeliers, INSERM, CNRS SNC 5096, Université Paris Cité, Paris, France.

Anais L'Haridon (A)

Multi-Site Medical Biology Laboratory SeqOIA, Paris, France.

Nelly Burnichon (N)

Institut du Cancer Paris Carpem, AP-HP, Genomic Medicine of Tumors and Cancers Department, Fédération de Génétique et Médecine Génomique, Université Paris Cité, APHP.Centre, Paris, France.

Eric Pasmant (E)

Department of Molecular Genetics, Fédération de Génétique et Médecine Génomique, Cochin Hospital, Université Paris Cité, APHP.Centre, Paris, France.
Institut Cochin, INSERM U1016, CNRS UMR8104, Université Paris Cité, CARPEM, Paris, France.

Camille Tlemsani (C)

Department of Medical Oncology, Cochin Hospital, Paris Cancer Institute CARPEM, Université Paris Cité, APHP.Centre, Paris, France. camille.tlemsani@aphp.fr.
Institut Cochin, INSERM U1016, CNRS UMR8104, Université Paris Cité, CARPEM, Paris, France. camille.tlemsani@aphp.fr.

Classifications MeSH