Heterozygous mutations in the PALB2 hereditary breast cancer predisposition gene impact on the three-dimensional nuclear organization of patient-derived cell lines

Genes Chromosomes and Cancer

Volumn 52, Issue 5, 2013, Pages 480-494

  Wark, Landon ^a   Novak, David ^a,b,c   Sabbaghian, Nelly ^b,c   Amrein, Lilian ^c   Jangamreddy, Jaganmohan R ^c,f   Cheang, Mary ^a   Pouchet, Carly ^b,c   Aloyz, Raquel ^b,c   Foulkes, William D ^b,c,d   Mai, Sabine ^a   Tischkowitz, Marc ^b,c,e  

^a UNIVERSITY OF MANITOBA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; MITOMYCIN;

ALLELE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CELL CULTURE; CANCER PATIENT; CELL ASSAY; CELL METABOLISM; CELL NUCLEUS; CENTROMERE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; FIBROBLAST CULTURE; FIRST DEGREE RELATIVE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE MUTATION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENOMIC INSTABILITY; HEREDITARY BREAST CANCER; HETEROZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOBLASTOID CELL LINE; MALE; PARTNER AND LOCALIZER OF BRCA2 GENE; PHENOTYPE; PRIORITY JOURNAL; SPECTRAL KARYOTYPING; STATISTICAL SIGNIFICANCE; TELOMERE;

ADOLESCENT; ADULT; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CASE-CONTROL STUDIES; CELL NUCLEUS; CELL SURVIVAL; CENTROMERE; CISPLATIN; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HEREDITARY BREAST AND OVARIAN CANCER SYNDROME; HETEROZYGOTE; HUMANS; KARYOTYPE; MALE; MIDDLE AGED; MITOMYCIN; NUCLEAR PROTEINS; TELOMERE; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 84875075153     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22045     Document Type: Article

References (44)

1. Auerbach AD, Wolman SR. 1976. Susceptibility of Fanconi's anaemia fibroblasts to chromosome damage by carcinogens. Nature 261: 494-496.
2. Ball SE, Gibson FM, Rizzo S, Tooze JA, Marsh JC, Gordon-Smith EC. 1998. Progressive telomere shortening in aplastic anemia. Blood 91: 3582-3592.
3. Callen E, Samper E, Ramirez MJ, Creus A, Marcos R, Ortega JJ, Olive T, Badell I, Blasco MA, Surralles J. 2002. Breaks at telomeres and TRF2-independent end fusions in Fanconi anemia. Hum Mol Genet 11: 439-444.
4. 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: 2222-2229.
5. Chang S, Khoo CM, Naylor ML, Maser RS, DePinho RA. 2003. Telomere-based crisis: Functional differences between telomerase activation and ALT in tumor progression. Genes Dev 17: 88-100.
6. Chin K, de Solorzano CO, Knowles D, Jones A, Chou W, Rodriguez EG, Kuo WL, Ljung BM, Chew K, Myambo K, Miranda M, Krig S, Garbe J, Stampfer M, Yaswen P, Gray JW, Lockett SJ. 2004. In situ analyses of genome instability in breast cancer. Nat Genet 36: 984-988.
7. De Vos WH, Hoebe RA, Joss GH, Haffmans W, Baatout S, Van Oostveldt P, Manders EM. 2009. Controlled light exposure microscopy reveals dynamic telomere microterritories throughout the cell cycle. Cytometry A 75: 428-439.
8. DePinho RA, Polyak K. 2004. Cancer chromosomes in crisis. Nat Genet 36: 932-934.
9. Djuzenova CS, Rothfuss A, Oppitz U, Speit G, Schindler D, Hoehn H, Flentje M. 2001. Response to X-irradiation of Fanconi anemia homozygous and heterozygous cells assessed by the single-cell gel electrophoresis (comet) assay. Lab Invest 81: 185-192.
10. Erkko H, Xia B, Nikkilä J, Schleutker J, Syrjäkoski K, Mannermaa A, Kallioniemi A, Pylkas K, Karppinen SM, Rapakko K, Miron A, Sheng Q, Li G, Mattila H, Bell DW, Haber DA, Grip M, Reiman M, Jukkola-Vuorinen A, Mustonen A, Kere J, Aaltonen LA, Kosma VM, Kataja V, Soini Y, Drapkin RI, Livingston DM, Winqvist R. 2007. A recurrent mutation in PALB2 in Finnish cancer families. Nature 446: 316-319.
11. Foulkes WD, Ghadirian P, Akbari MR, Hamel N, Giroux S, Sabbaghian N, Darnel A, Royer R, Poll A, Fafard E, Robidoux A, Martin G, Bismar TA, Tischkowitz M, Rousseau F, Narod SA. 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: R83.
12. Garcia MJ, Fernandez V, Osorio A, Barroso A, Llort G, Lazaro C, Blanco I, Caldes T, de la Hoya M, Ramon YCT, Alonso C, Tejada MI, San Roman C, Robles-Diaz L, Urioste M, Benitez J. 2009. Analysis of FANCB and FANCN/PALB2 fanconi anemia genes in BRCA1/2-negative Spanish breast cancer families. Breast Cancer Res Treat 113: 545-551.
13. Gisselsson D, Jonson T, Petersen A, Strombeck B, Dal Cin P, Hoglund M, Mitelman F, Mertens F, Mandahl N. 2001. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc Natl Acad Sci U S A 98: 12683-12688.
14. Guffei A, Lichtensztejn Z, Goncalves Dos Santos Silva A, Louis SF, Caporali A, Mai S. 2007. c-Myc-dependent formation of Robertsonian translocation chromosomes in mouse cells. Neoplasia 9: 578-588.
15. Guffei A, Sarkar R, Klewes L, Righolt C, Knecht H, Mai S. 2010. Dynamic chromosomal rearrangements in Hodgkin's lymphoma are due to ongoing three-dimensional nuclear remodeling and breakage-bridge-fusion cycles. Haematologica 95: 2038-2046.
16. Hanson H, Mathew CG, Docherty Z, Mackie Ogilvie C. 2001. Telomere shortening in Fanconi anaemia demonstrated by a direct FISH approach. Cytogenet Cell Genet 93: 203-206.
17. Kim SH, McQueen PG, Lichtman MK, Shevach EM, Parada LA, Misteli T. 2004. Spatial genome organization during T-cell differentiation. Cytogenet Genome Res 105: 292-301.
18. Lacoste S, Wiechec E, Dos Santos Silva AG, Guffei A, Williams G, Lowbeer M, Benedek K, Henriksson M, Klein G, Mai S. 2010. Chromosomal rearrangements after ex vivo Epstein-Barr virus (EBV) infection of human B cells. Oncogene 29: 503-515.
19. Leteurtre F, Li X, Guardiola P, Le Roux G, Sergere JC, Richard P, Carosella ED, Gluckman E. 1999. Accelerated telomere shortening and telomerase activation in Fanconi's anaemia. Br J Haematol 105: 883-893.
20. Louis SF, Vermolen BJ, Garini Y, Young IT, Guffei A, Lichtensztejn Z, Kuttler F, Chuang TC, Moshir S, Mougey V, Chuang AY, Kerr PD, Fest T, Boukamp P, Mai S. 2005. c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci U S A 102: 9613-9618.
21. Mai S. 2010. Initiation of telomere-mediated chromosomal rearrangements in cancer. J Cell Biochem 109: 1095-1102.
22. Mai S, Garini Y. 2005. Oncogenic remodeling of the three-dimensional organization of the interphase nucleus: c-Myc induces telomeric aggregates whose formation precedes chromosomal rearrangements. Cell Cycle 4: 1327-1331.
23. Mai S, Garini Y. 2006. The significance of telomeric aggregates in the interphase nuclei of tumor cells. J Cell Biochem 97: 904-915.
24. Mai S, Wiener F. 2002. The impact of p53 loss on murine plasmacytoma development. Chromosome Res 10: 239-251.
25. McClintock B. 1941. The Stability of Broken Ends of Chromosomes in Zea Mays. Genetics 26: 234-282.
26. Moynahan ME, Chiu JW, Koller BH, Jasin M. 1999. Brca1 controls homology-directed DNA repair. Mol Cell 4: 511-518.
27. Pakkanen S, Wahlfors T, Siltanen S, Patrikainen M, Matikainen MP, Tammela TL, Schleutker J. 2009. PALB2 variants in hereditary and unselected Finnish prostate cancer cases. J Negat Results Biomed 8: 12.
28. Patel KJ, Yu VP, Lee H, Corcoran A, Thistlethwaite FC, Evans MJ, Colledge WH, Friedman LS, Ponder BA, Venkitaraman AR. 1998. Involvement of Brca2 in DNA repair. Mol Cell 1: 347-357.
29. Pearson T, Jansen S, Havenga C, Stones DK, Joubert G. 2001. Fanconi anemia. A statistical evaluation of cytogenetic results obtained from South African families. Cancer Genet Cytogenet 126: 52-55.
30. Reid S, Schindler D, Hanenberg H, Barker K, Hanks S, Kalb R, Neveling K, Kelly P, Seal S, Freund M, Wurm M, Batish SD, Lach FP, Yetgin S, Neitzel H, Ariffin H, Tischkowitz M, Mathew CG, Auerbach AD, Rahman N. 2007. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat Genet 39: 162-164.
31. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Greider C, DePinho RA. 1999. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96: 701-712.
32. Sarkar R, Guffei A, Vermolen BJ, Garini Y, Mai S. 2007. Alterations of centromere positions in nuclei of immortalized and malignant mouse lymphocytes. Cytometry A 71: 386-392.
33. Schaefer LH, Schuster D, Herz H. 2001. Generalized approach for accelerated maximum likelihood based image restoration applied to three-dimensional fluorescence microscopy. J Microsc 204: 99-107.
34. Selvarajah S, Yoshimoto M, Park PC, Maire G, Paderova J, Bayani J, Lim G, Al-Romaih K, Squire JA, Zielenska M. 2006. The breakage-fusion-bridge (BFB) cycle as a mechanism for generating genetic heterogeneity in osteosarcoma. Chromosoma 115: 459-467.
35. Shah SP, Morin RD, Khattra J, Prentice L, Pugh T, Burleigh A, Delaney A, Gelmon K, Guliany R, Senz J, Steidl C, Holt RA, Jones S, Sun M, Leung G, Moore R, Severson T, Taylor GA, Teschendorff AE, Tse K, Turashvili G, Varhol R, Warren RL, Watson P, Zhao Y, Caldas C, Huntsman D, Hirst M, Marra MA, Aparicio S. 2009. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461: 809-813.
36. Stewenius Y, Gorunova L, Jonson T, Larsson N, Hoglund M, Mandahl N, Mertens F, Mitelman F, Gisselsson D. 2005. Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc Natl Acad Sci U S A 102: 5541-5546.
37. Sy SM, Huen MS, Chen J. 2009a. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci U S A 106: 7155-7160.
38. Sy SM, Huen MS, Zhu Y, Chen J. 2009b. PALB2 Regulates Recombinational Repair through Chromatin Association and Oligomerization. J Biol Chem 284: 18302-18310.
39. Tischkowitz M, Xia B. 2010. PALB2/FANCN: Recombining cancer and Fanconi anemia. Cancer Res 70: 7353-7359.
40. Tischkowitz M, Xia B, Sabbaghian N, Reis-Filho JS, Hamel N, Li G, van Beers EH, Li L, Khalil T, Quenneville LA, Omeroglu A, Poll A, Lepage P, Wong N, Nederlof PM, Ashworth A, Tonin PN, Narod SA, Livingston DM, Foulkes WD. 2007. Analysis of PALB2/FANCN-associated breast cancer families. Proc Natl Acad Sci U S A 104: 6788-6793.
41. Vermolen BJ, Garini Y, Mai S, Mougey V, Fest T, Chuang TC, Chuang AY, Wark L, Young IT. 2005. Characterizing the three-dimensional organization of telomeres. Cytometry A 67: 144-150.
42. 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: 719-729.
43. Xia B, Dorsman JC, Ameziane N, de Vries Y, Rooimans MA, Sheng Q, Pals G, Errami A, Gluckman E, Llera J, Wang W, Livingston DM, Joenje H, de Winter JP. 2007. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat Genet 39: 159-161.
44. Zhang F, Fan Q, Ren K, Andreassen PR. 2009. PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol Cancer Res 7: 1110-1118.