Variations in the NBN/NBS1 gene and the risk of breast cancer in non-BRCA1/2 French Canadian families with high risk of breast cancer

BMC Cancer

Volumn 9, Issue , 2009, Pages

  Desjardins, Sylvie ^a   Beauparlant, Joly Chrales ^a   Labrie, Yvan ^a   Ouellette, Geneviève ^a   Durocher, Francine ^a   Bessette, Paul ^b   Chiquette, Jocelyne ^c   Laframboise, Rachel ^c   Lépine, Jean ^d   Lespérance, Bernard ^e   Pichette, Roxane ^e   Plante, Marie ^c   Simard, Jacques ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

^c LAVAL UNIVERSITY   (Canada)

^d Centre Hospitalier Regional de Rimouski   (Canada)

^e HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BRCA1 PROTEIN; BRCA2 PROTEIN; HISTONE GAMMA H2AX; HISTONE H2AX; LUCIFERASE; NIBRIN; TRYPSIN; UNCLASSIFIED DRUG; VALINE; CELL CYCLE PROTEIN; NBN PROTEIN, HUMAN; NUCLEAR PROTEIN;

ARTICLE; BREAST CANCER; CANADA; CANCER CELL CULTURE; CANCER RISK; CANCER SUSCEPTIBILITY; COHORT ANALYSIS; COMPUTER MODEL; CONSENSUS SEQUENCE; CONTROLLED STUDY; FAMILY STUDY; FRANCE; GENE CONSTRUCT; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE SEQUENCE; GENETIC VARIABILITY; HIGH RISK POPULATION; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; REPORTER GENE; ALTERNATIVE RNA SPLICING; BIOSYNTHESIS; BREAST TUMOR; CASE CONTROL STUDY; ETHNOLOGY; FEMALE; GENETIC PREDISPOSITION; GENETICS; HAPLOIDY; HELA CELL; OVARY TUMOR; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

ALTERNATIVE SPLICING; BREAST NEOPLASMS; CANADA; CASE-CONTROL STUDIES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; FEMALE; FRANCE; GENE DELETION; GENES, BRCA1; GENES, BRCA2; GENES, REPORTER; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; HAPLOIDY; HELA CELLS; HUMANS; LUCIFERASES; NUCLEAR PROTEINS; OVARIAN NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 67650090387     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-9-181     Document Type: Article

References (55)

1. Stratton MR Rahman N The emerging landscape of breast cancer susceptibility Nat Genet 2008, 40(1):17- 22 10.1038/ng.2007.53 18163131
2. Williams RS Williams JS Tainer JA Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template Biochem Cell Biol 2007, 85(4):509-520 10.1139/O07-069 17713585
3. Durocher F Guénard F Desjardins S Ouellette G Labrie Y Inherited susceptibility to breast cancer: Accomplishments and challenges Molecular genetics of cancer Kerala: Research Signpost Sinnett D 2005, 9-93
4. Seemanova E An increased risk for malignant neoplasms in heterozygotes for a syndrome of microcephaly, normal intelligence, growth retardation, remarkable facies, immunodeficiency and chromosomal instability Mutat Res 1990, 238(3):321-324 2342514
5. Howlett NG Scuric Z D'Andrea AD Schiestl RH Impaired DNA double strand break repair in cells from Nijmegen breakage syndrome patients DNA Repair (Amst) 2006, 5(2):251-257 10.1016/j.dnarep.2005.10.004 16309973
6. Bogdanova N Feshchenko S Schurmann P Waltes R Wieland B Hillemanns P Rogov YI Dammann O Bremer M Karstens JH et al Nijmegen Breakage Syndrome mutations and risk of breast cancer Int J Cancer 2008, 122(4):802-806 10.1002/ijc.23168 17957789
7. Heikkinen K Rapakko K Karppinen SM Erkko H Knuutila S Lundan T Mannermaa A Borresen-Dale AL Borg A Barkardottir RB et al RAD50 and NBS1 are breast cancer susceptibility genes associated with genomic instability Carcinogenesis 2006, 27(8);1593-1599 10.1093/carcin/bgi360 16474176
8. Hsu HM Wang HC Chen ST Hsu GC Shen CY Yu JC Breast cancer risk is associated with the genes encoding the DNA double-strand break repair Mre11/Rad50/Nbs1 complex Cancer Epidemiol Biomarkers Prev 2007, 16(10):2024-2032 10.1158/1055-9965.EPI-07-0116 17932350
9. Nowak J Mosor M Ziolkowska I Wierzbicka M Pernak-Schwarz M Przyborska M Roznowski K Plawski A Slomski R Januszkiewicz D Heterozygous carriers of the I171V mutation of the NBS1 gene have a significantly increased risk of solid malignant tumours Eur J Cancer 2008, 44(4):627-630 10.1016/ j.ejca.2008.01.006 18280732
10. Roznowski K Januszkiewicz-Lewandowska D Mosor M Pernak M Litwiniuk M Nowak J I171V germline mutation in the NBS1 gene significantly increases risk of breast cancer Breast Cancer Res Treat 2008, 110(2):343-348 10.1007/s10549-007-9734-1 17899368
11. Seemanova E Jarolim P Seeman P Varon R Digweed M Swift M Sperling K Cancer risk of heterozygotes with the NBN founder mutation J Natl Cancer Inst 2007, 99(24);1875-1880 10.1093/jnci/djm251 18073374
12. Forsti A Angelini S Festa F Sanyal S Zhang Z Grzybowska E Pamula J Pekala W Zientek H Hemminki K et al Single nucleotide polymorphisms in breast cancer Oncol Rep 2004, 11(4):917-922 15010895
13. Millikan RC Player JS Decotret AR Tse CK Keku T Polymorphisms in DNA repair genes, medical exposure to ionizing radiation, and breast cancer risk Cancer Epidemiol Biomarkers Prev 2005, 14(10):2326-2334 10.1158/ 1055-9965.EPI-05-0186 16214912
14. Dumon-Jones V Frappart PO Tong WM Sajithlal G Hulla W Schmid G Herceg Z Digweed M Wang ZQ Nbn heterozygosity renders mice susceptible to tumor formation and ionizing radiation-induced tumorigenesis Cancer Res 2003, 63(21):7263-7269 14612522
15. Stumm M Neubauer S Keindorff S Wegner RD Wieacker P Sauer R High frequency of spontaneous translocations revealed by FISH in cells from patients with the cancer-prone syndromes ataxia telangiectasia and Nijmegen breakage syndrome Cytogenet Cell Genet 2001, 92(3-4):186-191 10.1159/000056900 11435685
16. Tanzanella C Antoccia A Spadoni E di Masi A Pecile V Demori E Varon R Marseglia GL Tiepolo L Maraschio P Chromosome instability and nibrin protein variants in NBS heterozygotes Eur J Hum Genet 2003, 11(4):297-303 10.1038/sj.ejhg.5200962 12708449
17. Neubauer S Arutyunyan R Stumm M Dork T Bendix R Bremer M Varon R Sauer R E Radiosensitivity of ataxia telangiectasia and Nijmegen breakage syndrome homozygotes and heterozygotes as determined by three-color FISH chromosome painting Radiat Res 2002, 157(3):312-321 10.1667/ 0033-7587(2002)157[0312:ROATAN]2.0.CO;2 11839094
18. Ferguson DO Alt FW DNA double strand break repair and chromosomal translocation: Lessons from animal models Oncogene 2001, 20(40):5572-5579 10.1038/sj.onc.1204767 11607810
19. Pierce AJ Stark JM Araujo FD Moynahan ME Berwick M Jasin M Double-strand breaks and tumorigenesis Trends Cell Biol 2001, 11(11):S52-59 10.1016/ S0962-8924(01)02149-3 11684443
20. Fodde R Smits R Cancer biology. A matter of dosage Science 2002, 298(5594):761-763 10.1126/science.1077707 12399571
21. Simard J Dumont M Moisan AM Gaborieau V Malouin H Durocher F Chiquette J Plante M Avard D Bessette P et al Evaluation of BRCA1 and BRCA2 mutation prevalence, risk prediction models and a multistep testing approach in French-Canadian families with high risk of breast and ovarian cancer J Med Genet 2007, 44(2):107 -21 10.1136/jmg.2006.044388 16905680
22. Durocher F Labrie Y Soucy P Sinilnikova O Labuda D Bessette P Chiquette J Laframboise R Lepine J Lesperance B et al Mutation analysis and characterization of ATR sequence variants in breast cancer cases from high-risk French Canadian breast/ovarian cancer families BMC Cancer 2006, 6:230 1599749 17010193 10.1186/1471-2407-6-230
23. Cartegni L Wang J Zhu Z Zhang MQ Krainer AR ESEfinder: A web resource to identify exonic splicing enhancers Nucleic Acids Res 2003, 31(13):3568-3571 169022 12824367 10.1093/nar/gkg616
24. Reese MG Eeckman FH Kulp D Haussler D Improved splice site detection in Genie J Comput Biol 1997, 4(3):311-323 10.1089/cmb.1997.4.311 9278062
25. Shapiro MB Senapathy P RNA splice junctions of different classes of eukaryotes: Sequence statistics and functional implications in gene expression Nucleic Acids Res 1987, 15(17):7155-7174 306199 3658675 10.1093/nar/15.17.7155
26. Guenard F Labrie Y Ouellette G Joly Beauparlant C Simard J Durocher F Mutational analysis of the breast cancer susceptibility gene BRIP1/BACH1/ FANCJ in high-risk non-BRCA1/BRCA2 breast cancer families J Hum Genet 2008, 53(7):579-591 10.1007/s10038-008-0285-z 18414782
27. Purcell S Daly MJ Sham PC WHAP: Haplotype-based association analysis Bioinformatics 2007, 23(2):255-256 10.1093/bioinformatics/btl580 17118959
28. Ivanga M Labrie Y Calvo E Belleau P Martel C Pelletier G Morissette J Labrie F Durocher F Fine temporal analysis of DHT transcriptional modulation of the ATM/Gadd45g signaling pathways in the mouse uterus Mol Reprod Dev 2009, 76(3):278-288 10.1002/mrd.20949 18671277
29. Takai K Sakamoto S Sakai T Yasunaga J Komatsu K Matsuoka M A potential link between alternative splicing of the NBS1 gene and DNA damage/ environmental stress Radiat Res 2008, 170(1):33-40 10.1667/RR1191.1 18582154
30. Varon R Dutrannoy V Weikert G Tanzarella C Antoccia A Stockl L Spadoni E Kruger LA di Masi A Sperling K et al Mild Nijmegen breakage syndrome phenotype due to alternative splicing Hum Mol Genet 2006, 15(5):679-689 10.1093/hmg/ddi482 16415040
31. Cheung VG Ewens WJ Heterozygous carriers of Nijmegen Breakage Syndrome have a distinct gene expression phenotype Genome Res 2006, 16(8):973-979 1524869 16809669 10.1101/gr.5320706
32. Someya M Sakata K Tauchi H Matsumoto Y Nakamura A Komatsu K Hareyama M Association of ionizing radiation-induced foci of NBS1 with chromosomal instability and breast cancer susceptibility Radiat Res 2006, 166(4):575-582 10.1667/RR0638.1 17007554
33. Antoniou AC Easton DF Polygenic inheritance of breast cancer: Implications for design of association studies Genet Epidemiol 2003, 25(3):190-202 10.1002/gepi.10261 14557987
34. di Masi A Viganotti M Polticelli F Ascenzi P Tanzarella C Antoccia A The R215W mutation in NBS1 impairs gamma-H2AX binding and affects DNA repair: Molecular bases for the severe phenotype of 657del5/R215W Nijmegen breakage syndrome patients Biochem Biophys Res Commun 2008, 369(3):835-840 10.1016/j.bbrc.2008.02.129 18328813
35. Kobayashi J Tauchi H Sakamoto S Nakamura A Morishima K Matsuura S Kobayashi T Tamai K Tanimoto K Komatsu K NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain Curr Biol 2002, 12(21):1846-1851 10.1016/S0960-9822(02)01259-9 12419185
36. Varon R Reis A Henze G von Einsiedel HG Sperling K Seeger K Mutations in the Nijmegen Breakage Syndrome gene (NBS1) in childhood acute lymphoblastic leukemia (ALL) Cancer Res 2001, 61(9):3570-3572 11325820
37. Mosor M Ziolkowska I Pernak-Schwarz M Januszkiewicz-Lewandowska D Nowak J Association of the heterozygous germline I171V mutation of the NBS1 gene with childhood acute lymphoblastic leukemia Leukemia 2006, 20(8):1454-456 10.1038/sj.leu.2404285 16810201
38. Ziolkowska I Mosor M Wierzbicka M Rydzanicz M Pernak-Schwarz M Nowak J Increased risk of larynx cancer in heterozygous carriers of the I171V mutation of the NBS1 gene Cancer Sci 2007, 98(11):1701-1705 10.1111/ j.1349-7006.2007.00594.x 17894553
39. Shimada H Shimizu K Mimaki S Sakiyama T Mori T Shimasaki N Yokota J Nakachi K Ohta T Ohki M First case of aplastic anemia in a Japanese child with a homozygous missense mutation in the NBS1 gene (I171V) associated with genomic instability Hum Genet 2004, 115(5):372-376 10.1007/s00439-004-1155-1 15338273
40. Bogdanova N Schurmann P Waltes R Feshchenko S Zalutsky IV Bremer M Dork T NBS1 variant I171V and breast cancer risk Breast Cancer Res Treat 2008, 112(1):75-79 10.1007/s10549-007-9820-4 18049891
41. Seemanova E Sperling K Neitzel H Varon R Hadac J Butova O Schrock E Seeman P Digweed M Nijmegen breakage syndrome (NBS) with neurological abnormalities and without chromosomal instability J Med Genet 2006, 43(3):218-224 2563240 16033915 10.1136/jmg.2005.035287
42. Cerosaletti KM Morrison VA Sabath DE Willerford DM Concannon P Mutations and molecular variants of the NBS1 gene in non-Hodgkin lymphoma Genes Chromosomes Cancer 2002, 35(3):282-286 10.1002/gcc.10114 12353271
43. Hebbring SJ Fredriksson H White KA Maier C Ewing C McDonnell SK Jacobsen SJ Cerhan J Schaid DJ Ikonen T et al Role of the Nijmegen breakage syndrome 1 gene in familial and sporadic prostate cancer Cancer Epidemiol Biomarkers Prev 2006, 15(5):935-938 10.1158/ 1055-9965.EPI-05-0910 16702373
44. Figueroa JD Malats N Rothman N Real FX Silverman D Kogevinas M Chanock S Yeager M Welch R Dosemeci M et al Evaluation of genetic variation in the double-strand break repair pathway and bladder cancer risk Carcinogenesis 2007, 28(8):1788-1793 10.1093/carcin/bgm132 17557904
45. Thirumaran RK Bermejo JL Rudnai P Gurzau E Koppova K Goessler W Vahter M Leonardi GS Clemens F Fletcher T et al Single nucleotide polymorphisms in DNA repair genes and basal cell carcinoma of skin Carcinogenesis 2006, 27(8):1676-1681 10.1093/carcin/bgi381 16501254
46. Vineis P Manuguerra M Kavvoura FK Guarrera S Allione A Rosa F Di Gregorio A Polidoro S Saletta F Ioannidis JP et al A field synopsis on low-penetrance variants in DNA repair genes and cancer susceptibility J Natl Cancer Inst 2009, 101(1):24-36 19116388
47. Musak L Soucek P Vodickova L Naccarati A Halasova E Polakova V Slyskova J Susova S Buchancova J Smerhovsky Z et al Chromosomal aberrations in tire plant workers and interaction with polymorphisms of biotransformation and DNA repair genes Mutat Res 2008, 641(1-2):36-42 18394656
48. Du R An X Chen Y Qin J Functional analysis of the Myostatin gene promoter in sheep Sci China C Life Sci 2007, 50(5):648-654 10.1007/ s11427-007-0085-2 17879064
49. Guo RJ Suh ER Lynch JP The role of Cdx proteins in intestinal development and cancer Cancer Biol Ther 2004, 3(7):593-601 15136761
50. Mogal AP Meer van der R Crooke PS Abdulkadir SA Haploinsufficient prostate tumor suppression by Nkx3.1: A role for chromatin accessibility in dosage-sensitive gene regulation J Biol Chem 2007, 282(35):25790-25800 10.1074/jbc.M702438200 17602165
51. Morinaga T Yasuda H Hashimoto T Higashio K Tamaoki T A human alpha-fetoprotein enhancer-binding protein, ATBF1, contains four homeodomains and seventeen zinc fingers Mol Cell Biol 1991, 11(12):6041-6049 361769 1719379
52. Kaspar P Dvorakova M Kralova J Pajer P Kozmik Z Dvorak M Myb-interacting protein, ATBF1, represses transcriptional activity of Myb oncoprotein J Biol Chem 1999, 274(20):14422-14428 10.1074/jbc.274.20.14422 10318867
53. Miura Y Kataoka H Joh T Tada T Asai K Nakanishi M Okada N Okada H Susceptibility to killer T cells of gastric cancer cells enhanced by Mitomycin-C involves induction of ATBF1 and activation of p21 (Waf1/ Cip1) promoter Microbiol Immunol 2004, 48(2):137-145 14978340
54. Zhang Z Yamashita H Toyama T Sugiura H Ando Y Mita K Hamaguchi M Kawaguchi M Miura Y Iwase H ATBF1-a messenger RNA expression is correlated with better prognosis in breast cancer Clin Cancer Res 2005, 11(1):193-198 15671546
55. Sun X Zhou Y Otto KB Wang M Chen C Zhou W Subramanian K Vertino PM Dong JT Infrequent mutation of ATBF1 in human breast cancer J Cancer Res Clin Oncol 2007, 133(2):103-105 10.1007/s00432-006-0148-y 16932943