Functional deficiency of NBN, the Nijmegen breakage syndrome protein, in a p.R215W mutant breast cancer cell line

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Schröder Heurich, Bianca ^a   Bogdanova, Natalia ^a   Wieland, Britta ^a   Xie, Xiaoxi ^a   Noskowicz, Monika ^a   Park Simon, Tjoung Won ^a   Hillemanns, Peter ^a   Christiansen, Hans ^a   Dörk, Thilo ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Breast carcinoma; DNA damage repair; DNA double strand break repair disorder; Ionising radiation sensitivity; MRN complex

Indexed keywords

ATM PROTEIN; BRCA1 PROTEIN; GENOMIC DNA; HISTONE H2AX; NIBRIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; CELL CYCLE PROTEIN; HISTONE; NBN PROTEIN, HUMAN; NUCLEAR PROTEIN;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL LINE; CELL CYCLE PROGRESSION; COLONY FORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENETIC ANALYSIS; HCC1395 CELL LINE; HEMIZYGOSITY; HETEROZYGOSITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IRRADIATION; MISSENSE MUTATION; MUTANT; NBN GENE; PROTEIN DEFICIENCY; RADIOSENSITIVITY; SCREENING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; WILD TYPE; BREAST TUMOR; DNA REPAIR; DRUG SCREENING; FEMALE; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; RADIATION DOSE; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA MUTATIONAL ANALYSIS; DNA REPAIR; FEMALE; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; MUTATION; NUCLEAR PROTEINS; RADIATION TOLERANCE; TUMOR STEM CELL ASSAY;

EID: 84902072358     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-434     Document Type: Article

References (46)

1. Turnbull C, Rahman N. Genetic predisposition to breast cancer: past, present, and future. Annu Rev Genomics Hum Genet 2008, 9:321-345.
2. Ghoussaini M, Pharoah PD, Easton DF. Inherited genetic susceptibility to breast cancer: the beginning of the end or the end of the beginning?. Am J Pathol 2013, 183:1038-1051.
3. Bogdanova N, Helbig S, Dörk T. Hereditary breast cancer: ever more pieces to the polygenic puzzle. Hered Cancer Clin Pract 2013, 11:12.
4. Varon R, Vissinga C, Platzer M, Cerosaletti KM, Chrzanowska KH, Saar K, Beckmann G, Seemanová E, Cooper PR, Nowak NJ, Stumm M, Weemaes CM, Gatti RA, Wilson RK, Digweed M, Rosenthal A, Sperling K, Concannon P, Reis A. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 1998, 93:467-476.
5. Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates JR, Hays L, Morgan WF, Petrini JH. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 1998, 93:477-486.
6. Matsuura S, Tauchi H, Nakamura A, Kondo N, Sakamoto S, Endo S, Smeets D, Solder B, Belohradsky BH, Der Kaloustian VM, Oshimura M, Isomura M, Nakamura Y, Komatsu K. Positional cloning of the gene for Nijmegen breakage syndrome. Nat Genet 1998, 19:179-181.
7. Digweed M, Sperling K. Nijmegen breakage syndrome: clinical manifestation of defective response to DNA double-strand breaks. DNA Repair 2004, 3:1207-1217.
8. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005, 434:605-611.
9. Kobayashi J, 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, 12:1846-1851.
10. Becker E, Meyer V, Madaoui H, Guerois R. Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 2006, 22:1289-1292.
11. Lee JH, Xu B, Lee CH, Ahn JY, Song MS, Lee H, Canman CE, Lee JS, Kastan MB, Lim DS. Distinct functions of Nijmegen breakage syndrome in ataxia telangiectasia mutated-dependent responses to DNA damage. Mol Cancer Res 2003, 1:674-681.
12. Stracker TH, Petrini JH. The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 2011, 12:90-103.
13. Seemanová 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, 99:1875-1880.
14. Gorski B, Debniak T, Masojc B, Mierzejewski M, Medrek K, Cybulski C, Jakubowska A, Kurzawski G, Chosia M, Scott R, Lubinski J. Germline 657del5 mutation in the NBS1 gene in breast cancer patients. Int J Cancer 2003, 106:379-381.
15. Steffen J, Varon R, Mosor M, Maneva G, Maurer M, Stumm M, Nowakowska D, Rubach M, Kosakowska E, Ruka W, Nowecki Z, Rutkowski P, Demkow T, Sadowska M, Bidzinski M, Gawrychowski K, Sperling K. Increased cancer risk of heterozygotes with NBS1 germline mutations in Poland. Int J Cancer 2004, 111:67-71.
16. Buslov KG, Iyevleva AG, Chekmariova EV, Suspitsin EN, Togo AV, Kuligina ES, Sokolenko AP, Matsko DE, Turkevich EA, Lazareva YR, Chagunava OL, Bit-Sava EM, Semiglazov VF, Devilee P, Cornelisse C, Hanson KP, Imyanitov EN. NBS1 657del5 mutation may contribute only to a limited fraction of breast cancer cases in Russia. Int J Cancer 2005, 114:585-589.
17. Górski B, Cybulski C, Huzarski T, Byrski T, Gronwald J, Jakubowska A, Stawicka M, Gozdecka-Grodecka S, Szwiec M, Urbański K, Mituś J, Marczyk E, Dziuba J, Wandzel P, Surdyka D, Haus O, Janiszewska H, Debniak T, Tooczko-Grabarek A, Medrek K, Masojc B, Mierzejewski M, Kowalska E, Narod SA, Lubinski J. Breast cancer predisposing alleles in Poland. Breast Cancer Res Treat 2005, 92:19-24.
18. Steffen J, Nowakowska D, Niwinska A, Czapczak D, Kluska A, Piatkowska M, Wisniewska A, Paszko Z. Germline mutations 657del5 of the NBS1 gene contribute significantly to the incidence of breast cancer in Central Poland. Int J Cancer 2006, 119:470-472.
19. Bogdanova N, Feshchenko S, Schürmann P, Waltes R, Wieland B, Hillemanns P, Rogov YI, Dammann O, Bremer M, Karstens JH, Sohn C, Varon R, Dörk T. Nijmegen breakage syndrome mutations and risk of breast cancer. Int J Cancer 2008, 122:802-806.
20. Seemanova E, Seemanová E, Sperling K, Neitzel H, Varon R, Hadac J, Butova O, Schröck E, Seeman P, Digweed M. Nijmegen breakage syndrome (NBS) with neurological abnormalities and without chromosomal instability. J Med Genet 2006, 43:218-224.
21. 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, 369:835-840.
22. Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JKV, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE. The consensus coding sequences of human breast and colorectal cancers. Science 2006, 314:268-274.
23. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JKV, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Krishna Pant PV. The genomic landscapes of human breast and colorectal cancers. Science 2007, 318:1108-1113.
24. Stephens PJ, McBride DJ, Lin ML, Varela I, Pleasance ED, Simpson JT, Stebbings LA, Leroy C, Edkins S, Mudie LJ, Greenman CD, Jia M, Latimer C, Teague JW, Lau KW, Burton J, Quail MA, Swerdlow H, Churcher C, Natrajan R, Sieuwerts AM, Martens JWM, Silver DP, Langerød A, Russnes HEG, Foekens JA, Reis-Filho JS, van 't Veer L, Richardson AL, Børresen-Dale AL. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009, 462:1005-1010.
25. Sakamoto S, Iijima K, Mochizuki D, Nakamura K, Teshigawara K, Kobayashi J, Matsuura S, Tauchi H, Komatsu K. Homologous recombination repair is regulated by domains at the N- and C-terminus of NBS1 and is dissociated with ATM functions. Oncogene 2007, 26:6002-6009.
26. Nakamura K, Kato A, Kobayashi J, Yanagihara H, Sakamoto S, Oliveira DV, Shimada M, Tauchi H, Suzuki H, Tashiro S, Zou L, Komatsu K. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol Cell 2011, 41:515-528.
27. Krenzlin H, Demuth I, Salewsky B, Wessendorf P, Weidele K, Bürkle A, Digweed M. DNA damage in Nijmegen breakage syndrome cells leads to PARP hyperactivation and increased oxidative stress. PLoS Genet 2012, 8:e1002557.
28. Cerosaletti KM, Concannon P. Nibrin forkhead-associated domain and breast cancer C-terminal domain are both required for nuclear focus formation and phosphorylation. J Biol Chem 2003, 278:21944-21951.
29. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 2003, 22:5612-5621.
30. Yazdi PT, Wang Y, Zhao S, Patel N, Lee EY, Qin J. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev 2002, 16:571-582.
31. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 2004, 18:1423-1438.
32. Mendez G, Cilli D, Berardinelli F, Viganotti M, Ascenzi P, Tanzarella C, Antoccia A, di Masi A. Cleavage of the BRCT tandem domains of nibrin by the 657del5 mutation affects the DNA damage response less than the Arg215Trp mutation. IUBMB Life 2012, 64:853-861.
33. Hari FJ, Spycher C, Jungmichel S, Pavic L, Stucki M. A divalent FHA/BRCT-binding mechanism couples the MRE11-RAD50-NBS1 complex to damaged chromatin. EMBO Rep 2010, 11:387-392.
34. Antoccia A, Sakamoto S, Matsuura S, Tauchi H, Komatsu K. NBS1 prevents chromatid-type aberrations through ATM-dependent interactions with SMC1. Radiat Res 2008, 170:345-352.
35. Bork P, Hofmann K, Bucher P, Neuwald AF, Altschul SF, Koonin EV. A superfamily of conserved domains in DNA damage responsive cell cycle checkpoint proteins. FASEB J 1997, 11:68-76.
36. Callebaut I, Mornon JP. From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett 1997, 400:25-30.
37. Lowndes NF, Toh GW. DNA repair: the importance of phosphorylating histone H2AX. Curr Biol 2005, 15:R99-R102.
38. Mateju M, Kleiblova P, Kleibl Z, Janatova M, Soukupova J, Ticha I, Novotny J, Pohlreich P. Germline mutations 657del5 and 643C>T (R215W) in NBN are not likely to be associated with increased risk of breast cancer in Czech women. Breast Cancer Res Treat 2012, 133:809-811.
39. di Masi A, Antoccia A. NBS1 heterozygosity and cancer risk. Curr Genomics 2008, 9:275-281.
40. Xu J, Huo D, Chen Y, Nwachukwu C, Collins C, Rowell J, Slamon DJ, Olopade OI. CpG island methylation affects accessibility of the proximal BRCA1 promoter to transcription factors. Breast Cancer Res Treat 2010, 120:593-601.
41. Li D, Ilnytskyy Y, Kovalchuk A, Khachigian LM, Bronson RT, Wang B, Kovalchuk O. Crucial role for early growth response-1 in the transcriptional regulation of miR-20b in breast cancer. Oncotarget 2013, 4:1373-1387.
42. Abbott DW, Thompson ME, Robinson-Benion C, Tomlinson G, Jensen RA, Holt JT. BRCA1 expression restores radiation resistance in BRCA1-defective cancer cells through enhancement of transcription-coupled DNA repair. J Biol Chem 1999, 274:18808-18812.
43. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
44. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
45. McCabe N, Turner NC, Lord CJ, Kluzek K, Bialkowska A, Swift S, Giavara S, O'Connor MJ, Tutt AN, Zdzienicka MZ, Smith GC, Ashworth A. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res 2006, 66:8109-8115.
46. Oplustilova L, Wolanin K, Mistrik M, Korinkova G, Simkova D, Bouchal J, Lenobel R, Bartkova J, Lau A, O'Connor MJ, Lukas J, Bartek J. Evaluation of candidate biomarkers to predict cancer cell sensitivity or resistance to PARP-1 inhibitor treatment. Cell Cycle 2012, 11:3837-3850.