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Breast Cancer Research and Treatment

, Volume 154, Issue 3, pp 463–471 | Cite as

Mutation analysis of PALB2 gene in French breast cancer families

  • Francesca Damiola
  • Inès Schultz
  • Laure Barjhoux
  • Valérie Sornin
  • Marie-Gabrielle Dondon
  • Séverine Eon-Marchais
  • Morgane Marcou
  • The GENESIS Study Investigators
  • Olivier Caron
  • Marion Gauthier-Villars
  • Antoine de Pauw
  • Elisabeth Luporsi
  • Pascaline Berthet
  • Capucine Delnatte
  • Valérie Bonadona
  • Christine Maugard
  • Pascal Pujol
  • Christine Lasset
  • Michel Longy
  • Yves-Jean Bignon
  • Jean-Pierre Fricker
  • Nadine Andrieu
  • Olga M. Sinilnikova
  • Dominique Stoppa-Lyonnet
  • Sylvie Mazoyer
  • Danièle Muller
Preclinical study

Abstract

Several population-based and family-based studies have demonstrated that germline mutations of the PALB2 gene (Partner and Localizer of BRCA2) are associated with an increased risk of breast cancer. Distinct mutation frequencies and spectrums have been described depending on the population studied. Here we describe the first complete PALB2 coding sequence screening in the French population. We screened the complete coding sequence and intron–exon boundaries of PALB2, using the EMMA technique, to assess the contribution of pathogenic mutations in a set of 835 familial breast cancer cases and 662 unrelated controls from the French national study GENESIS and the Paul Strauss Cancer Centre, all previously tested negative for BRCA1 and BRCA2 pathogenic mutations. Our analysis revealed the presence of four novel deleterious mutations: c.1186insT, c.1857delT and c.2850delC in three cases, c.3418dupT in one control. In addition, we identified two in-frame insertion/deletion, 19 missense substitutions (two of them predicted as pathogenic), 9 synonymous variants, 28 variants located in introns and 2 in UTRs, as well as frequent variants. Truncating PALB2 mutations were found in 0.36 % of familial breast cancer cases, a frequency lower than the one detected in comparable studies in other populations (0.73–3.40 %). This suggests a small but significant contribution of PALB2 mutations to the breast cancer susceptibility in the French population.

Keywords

PALB2 Familial breast cancer Germline mutations Genetic testing 

Notes

Acknowledgments

Financial support for GENESIS was provided by the Ligue Nationale contre le Cancer (3 grants: PRE05/DSL, PRE07/DSL, PRE11/NA), the French National Institute of Cancer (Grant INCa No b2008-029/LL-LC) and the comprehensive cancer center SiRIC (Site de Recherche Intégrée sur le Cancer: Grant INCa-DGOS-4654). We wish to thank the genetic epidemiology platform (the PIGE, Plateforme d’Investigation en Génétique et Epidémiologie: S. Eon-Marchais, M. Marcou, D. Le Gal, L. Toulemonde, J. Beauvallet, N. Mebirouk, E. Cavaciuti, A. Fescia), the biological resource center (C. Verny-Pierre, L. Barjhoux, V. Sornin) and all the GENESIS collaborating cancer clinics (Clinique Sainte Catherine, Avignon: H. Dreyfus; Hôpital Saint Jacques, Besançon: M-A. Collonge-Rame; Institut Bergonié, Bordeaux: M. Longy, A. Floquet, E. Barouk-Simonet; CHU, Brest: S. Audebert; Centre François Baclesse, Caen: P. Berthet; Hôpital Dieu, Chambéry: S. Fert-Ferrer; Centre Jean Perrin, Clermont-Ferrand: Y-J. Bignon; Hôpital Pasteur, Colmar: J-M. Limacher; Hôpital d’Enfants CHU—Centre Georges François Leclerc, Dijon: L. Faivre-Olivier; CHU, Fort de France: O. Bera; CHU Albert Michallon, Grenoble: D. Leroux; Hôpital Flaubert, Le Havre: V. Layet; Centre Oscar Lambret, Lille: P. Vennin†, C. Adenis; Hôpital Jeanne de Flandre, Lille: S. Lejeune-Dumoulin, S. Manouvier-Hanu; CHRU Dupuytren, Limoges: L. Venat-Bouvet; Centre Léon Bérard, Lyon: C. Lasset, V. Bonadona; Hôpital Edouard Herriot, Lyon: S. Giraud; Institut Paoli-Calmettes, Marseille: F. Eisinger, L. Huiart; Centre Val d’Aurelle—Paul Lamarque, Montpellier: I. Coupier; CHU Arnaud de Villeneuve, Montpellier: I. Coupier, P. Pujol; Centre René Gauducheau, Nantes: C. Delnatte; Centre Catherine de Sienne, Nantes: A. Lortholary; Centre Antoine Lacassagne, Nice: M. Frénay, V. Mari; Hôpital Caremeau, Nîmes: J. Chiesa; Réseau Oncogénétique Poitou Charente, Niort: P. Gesta; Institut Curie, Paris: D. Stoppa-Lyonnet, M. Gauthier-Villars, B. Buecher, A. de Pauw, C. Abadie, M. Belotti; Hôpital Saint-Louis, Paris: O. Cohen-Haguenauer; Centre Viggo-Petersen, Paris: F. Cornélis; Hôpital Tenon, Paris: A. Fajac; GH Pitié Salpétrière et Hôpital Beaujon, Paris: C. Colas, F. Soubrier, P. Hammel, A. Fajac; Institut Jean Godinot, Reims: C. Pennet, T. D. Nguyen; Polyclinique Courlancy, Reims: L. Demange†, C. Pennet; Centre Eugène Marquis, Rennes: C. Dugast; Centre Henri Becquerel, Rouen: A. Chevrier, T. Frebourg, J. Tinat, I. Tennevet, A. Rossi; Hôpital René Huguenin/Institut Curie, Saint Cloud: C. Noguès, L. Demange†, E. Mouret-Fourme; CHU, Saint-Etienne: F. Prieur; Centre Paul Strauss, Strasbourg: J-P. Fricker, H. Nehme-Schuster; Hôpital Civil, Strasbourg, C. Maugard; Institut Claudius Regaud, Toulouse: L. Gladieff, V. Feillel; Hôpital Bretonneau, Tours: I. Mortemousque; Centre Alexis Vautrin, Vandoeuvre-les-Nancy: E. Luporsi; Hôpital de Bravois, Vandoeuvre-les-Nancy: P. Jonveaux; Gustave Roussy, Villejuif: A. Chompret†, O. Caron).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interest.

Supplementary material

10549_2015_3625_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1239 kb)

References

  1. 1.
    Delaloge S, Caron O, Feunteun J (2015) Effect of PALB2 status on breast cancer precision medicine. Lancet 16(6):598–600CrossRefPubMedGoogle Scholar
  2. 2.
    Guenard F, Pedneault CS, Ouellette G, Labrie Y, Simard J, Durocher F (2010) Evaluation of the contribution of the three breast cancer susceptibility genes CHEK2, STK11, and PALB2 in non-BRCA1/2 French Canadian families with high risk of breast cancer. Genet Test Mol Biomark 14(4):515–526CrossRefGoogle Scholar
  3. 3.
    McInerney NM, Miller N, Rowan A, Colleran G, Barclay E, Curran C, Kerin MJ, Tomlinson IP, Sawyer E (2010) Evaluation of variants in the CHEK2, BRIP1 and PALB2 genes in an Irish breast cancer cohort. Breast Cancer Res Treat 121(1):203–210CrossRefPubMedGoogle Scholar
  4. 4.
    Gunnarsson H, Arason A, Gillanders EM, Agnarsson BA, Johannesdottir G, Johannsson OT, Barkardottir RB (2008) Evidence against PALB2 involvement in Icelandic breast cancer susceptibility. J Negat Results Biomed 7:5PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Rahman N, Seal S, Thompson D, Kelly P, Renwick A, Elliott A, Reid S, Spanova K, Barfoot R, Chagtai T et al (2007) PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat Genet 39(2):165–167PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Erkko H, Dowty JG, Nikkila J, Syrjakoski K, Mannermaa A, Pylkas K, Southey MC, Holli K, Kallioniemi A, Jukkola-Vuorinen A et al (2008) Penetrance analysis of the PALB2 c.1592delT founder mutation. Clin Cancer Res 14(14):4667–4671CrossRefPubMedGoogle Scholar
  7. 7.
    Southey MC, Teo ZL, Dowty JG, Odefrey FA, Park DJ, Tischkowitz M, Sabbaghian N, Apicella C, Byrnes GB, Winship I et al (2010) A PALB2 mutation associated with high risk of breast cancer. Breast Cancer Res 12(6):R109PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    Antoniou AC, Casadei S, Heikkinen T, Barrowdale D, Pylkas K, Roberts J, Lee A, Subramanian D, De Leeneer K, Fostira F et al (2014) Breast-cancer risk in families with mutations in PALB2. NEngl J Med 371(6):497–506CrossRefGoogle Scholar
  9. 9.
    Nguyen-Dumont T, Hammet F, Mahmoodi M, Tsimiklis H, Teo ZL, Li R, Pope BJ, Terry MB, Buys SS, Daly M et al (2015) Mutation screening of PALB2 in clinically ascertained families from the Breast Cancer Family Registry. Breast Cancer Res Treat 149(2):547–554CrossRefPubMedGoogle Scholar
  10. 10.
    Hellebrand H, Sutter C, Honisch E, Gross E, Wappenschmidt B, Schem C, Deissler H, Ditsch N, Gress V, Kiechle M et al (2011) Germline mutations in the PALB2 gene are population specific and occur with low frequencies in familial breast cancer. Hum Mutat 32(6):E2176–E2188CrossRefPubMedGoogle Scholar
  11. 11.
    Fernandes PH, Saam J, Peterson J, Hughes E, Kaldate R, Cummings S, Theisen A, Chen S, Trost J, Roa BB (2014) Comprehensive sequencing of PALB2 in patients with breast cancer suggests PALB2 mutations explain a subset of hereditary breast cancer. Cancer 120(7):963–967CrossRefPubMedGoogle Scholar
  12. 12.
    Teo ZL, Park DJ, Provenzano E, Chatfield CA, Odefrey FA, Nguyen-Dumont T, Dowty JG, Hopper JL, Winship I, Goldgar DE et al (2013) Prevalence of PALB2 mutations in Australasian multiple-case breast cancer families. Breast Cancer Res 15(1):R17PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Casadei S, Norquist BM, Walsh T, Stray S, Mandell JB, Lee MK, Stamatoyannopoulos JA, King MC (2011) Contribution of inherited mutations in the BRCA2-interacting protein PALB2 to familial breast cancer. Cancer Res 71(6):2222–2229PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Bogdanova N, Sokolenko AP, Iyevleva AG, Abysheva SN, Blaut M, Bremer M, Christiansen H, Rave-Frank M, Dork T, Imyanitov EN (2011) PALB2 mutations in German and Russian patients with bilateral breast cancer. Breast Cancer Res Treat 126(2):545–550PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Phuah SY, Lee SY, Kang P, Kang IN, Yoon SY, Thong MK, Hartman M, Sng JH, Yip CH, Taib NA et al (2013) Prevalence of PALB2 mutations in breast cancer patients in multi-ethnic Asian population in Malaysia and Singapore. PLoS One 8(8):e73638PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Catucci I, Peterlongo P, Ciceri S, Colombo M, Pasquini G, Barile M, Bonanni B, Verderio P, Pizzamiglio S, Foglia C et al (2014) PALB2 sequencing in Italian familial breast cancer cases reveals a high-risk mutation recurrent in the province of Bergamo. Genet Med 16(9):688–694CrossRefPubMedGoogle Scholar
  17. 17.
    Cao AY, Huang J, Hu Z, Li WF, Ma ZL, Tang LL, Zhang B, Su FX, Zhou J, Di GH et al (2009) The prevalence of PALB2 germline mutations in BRCA1/BRCA2 negative Chinese women with early onset breast cancer or affected relatives. Breast Cancer Res Treat 114(3):457–462CrossRefPubMedGoogle Scholar
  18. 18.
    Dansonka-Mieszkowska A, Kluska A, Moes J, Dabrowska M, Nowakowska D, Niwinska A, Derlatka P, Cendrowski K, Kupryjanczyk J (2010) A novel germline PALB2 deletion in Polish breast and ovarian cancer patients. BMC Med Genet 11:20PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Foulkes WD, Ghadirian P, Akbari MR, Hamel N, Giroux S, Sabbaghian N, Darnel A, Royer R, Poll A, Fafard E et al (2007) Identification of a novel truncating PALB2 mutation and analysis of its contribution to early-onset breast cancer in French-Canadian women. Breast Cancer Res 9(6):R83PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Weber J, Looten R, Houdayer C, Stoppa-Lyonnet D, Viovy JL (2006) Improving sensitivity of electrophoretic heteroduplex analysis using nucleosides as additives: application to the breast cancer predisposition gene BRCA2. Electrophoresis 27(8):1444–1452CrossRefPubMedGoogle Scholar
  21. 21.
    Caux-Moncoutier V, Castera L, Tirapo C, Michaux D, Remon MA, Lauge A, Rouleau E, De Pauw A, Buecher B, Gauthier-Villars M et al (2011) EMMA, a cost- and time-effective diagnostic method for simultaneous detection of point mutations and large-scale genomic rearrangements: application to BRCA1 and BRCA2 in 1525 patients. Hum Mutat 32(3):325–334CrossRefPubMedGoogle Scholar
  22. 22.
  23. 23.
    Ng PC, Henikoff S (2003) SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 31(13):3812–3814PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
  25. 25.
    Tavtigian SV, Deffenbaugh AM, Yin L, Judkins T, Scholl T, Samollow PB, de Silva D, Zharkikh A, Thomas A (2006) Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 43(4):295–305PubMedCentralCrossRefPubMedGoogle Scholar
  26. 26.
  27. 27.
    Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7(4):248–249PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Shapiro MB, Senapathy P (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15(17):7155–7174PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Yeo G, Burge CB (2004) Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 11(2–3):377–394CrossRefPubMedGoogle Scholar
  30. 30.
    Reese MG, Eeckman FH, Kulp D, Haussler D (1997) Improved splice site detection in Genie. J Comput Biol 4(3):311–323CrossRefPubMedGoogle Scholar
  31. 31.
    Pertea M, Lin X, Salzberg SL (2001) GeneSplicer: a new computational method for splice site prediction. Nucleic Acids Res 29(5):1185–1190PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, Beroud C (2009) Human splicing finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 37(9):e67PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Houdayer C, Caux-Moncoutier V, Krieger S, Barrois M, Bonnet F, Bourdon V, Bronner M, Buisson M, Coulet F, Gaildrat P et al (2012) Guidelines for splicing analysis in molecular diagnosis derived from a set of 327 combined in silico/in vitro studies on BRCA1 and BRCA2 variants. Hum Mutat 33(8):1228–1238CrossRefPubMedGoogle Scholar
  34. 34.
    Blanco A, de la Hoya M, Osorio A, Diez O, Miramar MD, Infante M, Martinez-Bouzas C, Torres A, Lasa A, Llort G et al (2013) Analysis of PALB2 gene in BRCA1/BRCA2 negative Spanish hereditary breast/ovarian cancer families with pancreatic cancer cases. PLoS One 8(7):e67538PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Hofstatter EW, Domchek SM, Miron A, Garber J, Wang M, Componeschi K, Boghossian L, Miron PL, Nathanson KL, Tung N (2011) PALB2 mutations in familial breast and pancreatic cancer. Fam Cancer 10(2):225–231CrossRefPubMedGoogle Scholar
  36. 36.
    Tischkowitz M, Capanu M, Sabbaghian N, Li L, Liang X, Vallee MP, Tavtigian SV, Concannon P, Foulkes WD, Bernstein L et al (2012) Rare germline mutations in PALB2 and breast cancer risk: a population-based study. Hum Mutat 33(4):674–680PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Wong-Brown MW, Avery-Kiejda KA, Bowden NA, Scott RJ (2013) Low prevalence of germline PALB2 mutations in Australian triple-negative breast cancer. Int J Cancer 134(2):301–305CrossRefPubMedGoogle Scholar
  38. 38.
    Xia B, Sheng Q, Nakanishi K, Ohashi A, Wu J, Christ N, Liu X, Jasin M, Couch FJ, Livingston DM (2006) Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol Cell 22(6):719–729CrossRefPubMedGoogle Scholar
  39. 39.
    Zhang F, Ma J, Wu J, Ye L, Cai H, Xia B, Yu X (2009) PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr Biol 19(6):524–529PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Ruiz-Echevarria MJ, Gonzalez CI, Peltz SW (1998) Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J 17(2):575–589PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Reid S, Schindler D, Hanenberg H, Barker K, Hanks S, Kalb R, Neveling K, Kelly P, Seal S, Freund M et al (2007) Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat Genet 39(2):162–164CrossRefPubMedGoogle Scholar
  42. 42.
    Peterlongo P, Catucci I, Pasquini G, Verderio P, Peissel B, Barile M, Varesco L, Riboni M, Fortuzzi S, Manoukian S et al (2011) PALB2 germline mutations in familial breast cancer cases with personal and family history of pancreatic cancer. Breast Cancer Res Treat 126(3):825–828CrossRefPubMedGoogle Scholar
  43. 43.
    Erkko H, Xia B, Nikkila J, Schleutker J, Syrjakoski K, Mannermaa A, Kallioniemi A, Pylkas K, Karppinen SM, Rapakko K et al (2007) A recurrent mutation in PALB2 in Finnish cancer families. Nature 446(7133):316–319CrossRefPubMedGoogle Scholar
  44. 44.
    Ding YC, Steele L, Chu LH, Kelley K, Davis H, John EM, Tomlinson GE, Neuhausen SL (2011) Germline mutations in PALB2 in African-American breast cancer cases. Breast Cancer Res Treat 126(1):227–230PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    de Chalon Sauty, Teo Z, Park DJ, Odefrey FA, Hopper JL, Southey MC (2010) Are PALB2 mutations associated with increased risk of male breast cancer? Breast Cancer Res Treat 121(1):253–255CrossRefGoogle Scholar
  46. 46.
    Jones S, Hruban RH, Kamiyama M, Borges M, Zhang X, Parsons DW, Lin JC, Palmisano E, Brune K, Jaffee EM et al (2009) Exomic sequencing identifies PALB2 as a pancreatic cancer susceptibility gene. Science 324(5924):217PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Tavtigian SV, Chenevix-Trench G (2015) Growing recognition of the role for rare missense substitutions in breast cancer susceptibility. Biomark Med 8(4):589–603CrossRefGoogle Scholar
  48. 48.
    Tischkowitz M, Sabbaghian N, Ray AM, Lange EM, Foulkes WD, Cooney KA (2008) Analysis of the gene coding for the BRCA2-interacting protein PALB2 in hereditary prostate cancer. Prostate 68(6):675–678PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Zheng Y, Zhang J, Niu Q, Huo D, Olopade OI (2012) Novel germline PALB2 truncating mutations in African American breast cancer patients. Cancer 118(5):1362–1370PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Papi L, Putignano AL, Congregati C, Piaceri I, Zanna I, Sera F, Morrone D, Genuardi M, Palli D (2010) A PALB2 germline mutation associated with hereditary breast cancer in Italy. Fam Cancer 9(2):181–185CrossRefPubMedGoogle Scholar
  51. 51.
    Balia C, Sensi E, Lombardi G, Roncella M, Bevilacqua G, Caligo MA (2010) PALB2: a novel inactivating mutation in a Italian breast cancer family. Fam Cancer 9(4):531–536CrossRefPubMedGoogle Scholar
  52. 52.
    Blanco A, de la Hoya M, Balmana J, Ramony Cajal T, Teule A, Miramar MD, Esteban E, Infante M, Benitez J, Torres A et al (2012) Detection of a large rearrangement in PALB2 in Spanish breast cancer families with male breast cancer. Breast Cancer Res Treat 132(1):307–315CrossRefPubMedGoogle Scholar
  53. 53.
    Bodian DL, McCutcheon JN, Kothiyal P, Huddleston KC, Iyer RK, Vockley JG, Niederhuber JE (2014) Germline variation in cancer-susceptibility genes in a healthy, ancestrally diverse cohort: implications for individual genome sequencing. PLoS One 9(4):e94554PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Garcia MJ, Fernandez V, Osorio A, Barroso A, Llort G, Lazaro C, Blanco I, Caldes T, de la Hoya M, Ramon YCT et al (2009) Analysis of FANCB and FANCN/PALB2 fanconi anemia genes in BRCA1/2-negative Spanish breast cancer families. Breast Cancer Res Treat 113(3):545–551CrossRefPubMedGoogle Scholar
  55. 55.
    Kuusisto KM, Bebel A, Vihinen M, Schleutker J, Sallinen SL (2011) Screening for BRCA1, BRCA2, CHEK2, PALB2, BRIP1, RAD50, and CDH1 mutations in high-risk Finnish BRCA1/2-founder mutation-negative breast and/or ovarian cancer individuals. Breast Cancer Res 13(1):R20PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Prokofyeva D, Bogdanova N, Bermisheva M, Zinnatullina G, Hillemanns P, Khusnutdinova E, Dork T (2012) Rare occurrence of PALB2 mutations in ovarian cancer patients from the Volga-Ural region. Clin Genet 82(1):100–101CrossRefPubMedGoogle Scholar
  57. 57.
    Wong MW, Nordfors C, Mossman D, Pecenpetelovska G, Avery-Kiejda KA, Talseth-Palmer B, Bowden NA, Scott RJ (2011) BRIP1, PALB2, and RAD51C mutation analysis reveals their relative importance as genetic susceptibility factors for breast cancer. Breast Cancer Res Treat 127(3):853–859CrossRefPubMedGoogle Scholar
  58. 58.
    Catucci I, Milgrom R, Kushnir A, Laitman Y, Paluch-Shimon S, Volorio S, Ficarazzi F, Bernard L, Radice P, Friedman E et al (2012) Germline mutations in BRIP1 and PALB2 in Jewish high cancer risk families. Fam Cancer 11(3):483–491CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Francesca Damiola
    • 1
  • Inès Schultz
    • 2
  • Laure Barjhoux
    • 1
  • Valérie Sornin
    • 1
  • Marie-Gabrielle Dondon
    • 3
    • 4
    • 5
  • Séverine Eon-Marchais
    • 3
    • 4
    • 5
  • Morgane Marcou
    • 3
    • 4
    • 5
  • The GENESIS Study Investigators
  • Olivier Caron
    • 6
  • Marion Gauthier-Villars
    • 7
  • Antoine de Pauw
    • 7
  • Elisabeth Luporsi
    • 8
  • Pascaline Berthet
    • 9
  • Capucine Delnatte
    • 10
  • Valérie Bonadona
    • 11
    • 12
    • 13
  • Christine Maugard
    • 14
  • Pascal Pujol
    • 15
    • 16
  • Christine Lasset
    • 11
    • 12
    • 13
  • Michel Longy
    • 17
  • Yves-Jean Bignon
    • 18
  • Jean-Pierre Fricker
    • 2
  • Nadine Andrieu
    • 3
    • 4
    • 5
  • Olga M. Sinilnikova
    • 1
    • 19
  • Dominique Stoppa-Lyonnet
    • 7
    • 20
    • 21
  • Sylvie Mazoyer
    • 1
  • Danièle Muller
    • 2
  1. 1.“Genetics of Breast Cancer” Team, Cancer Research Centre of LyonCNRS UMR5286/Inserm U1052/Université Lyon 1, Centre Léon BérardLyonFrance
  2. 2.Unité d’Oncologie GénétiqueCentre Paul StraussStrasbourgFrance
  3. 3.INSERM, U900ParisFrance
  4. 4.Institut CurieParisFrance
  5. 5.Mines ParisTechFontainebleauFrance
  6. 6.Service d’Oncologie GénétiqueInstitut de Cancérologie Gustave RoussyVillejuifFrance
  7. 7.Service de GénétiqueInstitut CurieParisFrance
  8. 8.Unité d’OncogénétiqueICL Alexis VautrinVandœuvre-lès-NancyFrance
  9. 9.Unité de Pathologie GynécologiqueCentre François BaclesseCaenFrance
  10. 10.Service Oncologie MédicaleCentre René GauducheauNantes Saint HerblainFrance
  11. 11.Université Claude Bernard Lyon 1VilleurbanneFrance
  12. 12.CNRS UMR 5558LyonFrance
  13. 13.Unité de Prévention et Epidémiologie GénétiqueCentre Léon BérardLyonFrance
  14. 14.Service d’Oncologie, UF6948Hôpital CivilStrasbourgFrance
  15. 15.Service de Génétique Médicale et OncogénétiqueHôpital Arnaud de Villeneuve, CHU MontpellierMontpellierFrance
  16. 16.INSERM U896, CRCM Val d’AurelMontpellierFrance
  17. 17.Institut BergoniéBordeauxFrance
  18. 18.Centre Jean-PerrinClermont-FerrandFrance
  19. 19.Unité Mixte de Génétique Constitutionnelle des Cancers Fréquents, Hospices Civils de LyonCentre Léon BérardLyonFrance
  20. 20.Inserm, U830ParisFrance
  21. 21.Université Paris-DescartesParisFrance

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