A rare polymorphic variant of NBS1 reduces DNA repair activity and elevates chromosomal instability

Cancer Research

Volumn 74, Issue 14, 2014, Pages 3707-3715

  Yamamoto, Yuki ^a,b   Miyamoto, Mamiko ^a   Tatsuda, Daisuke ^a,d   Kubo, Michiaki ^e   Nakagama, Hitoshi ^a   Nakamura, Yusuke ^c   Satoh, Hitoshi ^b   Matsuda, Koichi ^c   Watanabe, Toshiki ^b   Ohta, Tsutomu ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b Graduate School of Frontier Sciences   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d INSTITUTE OF MICROBIAL CHEMISTRY   (Japan)

^e INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MDC1 PROTEIN; MRE11 PROTEIN; NIBRIN; PROTEIN; RAD50 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BREAST CANCER; CANCER RISK; CELL CYCLE; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA REPAIR; FEMALE; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOSITY LOSS; HUMAN; JAPANESE (PEOPLE); MAJOR CLINICAL STUDY; NBS1 GENE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA INTERACTION; PROTEIN LOCALIZATION; SPECIES DIFFERENCE; WILD TYPE;

AMINO ACID SEQUENCE; BREAST NEOPLASMS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMOSOMAL INSTABILITY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; FEMALE; HUMANS; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; POLYMORPHISM, GENETIC; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TRANS-ACTIVATORS;

EID: 84904268074     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3037     Document Type: Article

References (34)

1. Weemaes CM, Hustinx TW, Scheres JM, van Munster PJ, Bakkeren JA, Taalman RD. A new chromosomal instability disorder: the Nijmegen breakage syndrome. Acta Paediatr Scand 1981;70:557-64. (Pubitemid 11078625)
2. Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates JR 3rd, et al. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 1998;93:477-86. (Pubitemid 28232091)
3. Desai-Mehta A, Cerosaletti KM, Concannon P. Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization. Mol Cell Biol 2001;21:2184-91. (Pubitemid 32479638)
4. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005;434:605-11. (Pubitemid 40488547)
5. You Z, Chahwan C, Bailis J, Hunter T, Russell P. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol Cell Biol 2005;25:5363-79. (Pubitemid 40853574)
6. Kobayashi J, Tauchi H, Sakamoto S, Nakamura A, Morishima K, Matsuura S, et al. NBS1 localizes to γ-H2AX foci through interaction with the FHA/BRCT domain. Curr Biol 2002;12:1846-51. (Pubitemid 35273905)
7. Chapman JR, Jackson SP. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep 2008;9:795-801.
8. Lloyd J, Chapman JR, Clapperton JA, Haire LF, Hartsuiker E, Li J, et al. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 2009;139:100-11.
9. 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; 61:3570-2. (Pubitemid 32694962)
10. Shimada H, Shimizu K, Mimaki S, Sakiyama T, Mori T, Shimasaki N, et al. 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;115:372-6. (Pubitemid 39341710)
11. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 1999;13:2633-8. (Pubitemid 29508550)
12. Sakamoto S, Iijima K, Mochizuki D, Nakamura K, Teshigawara K, Kobayashi J, et al. Homologous recombination repair is regulated by domains at the N- and C-terminus of NBS1 and is dissociated with ATM functions. Oncogene 2007;26:6002-9. (Pubitemid 47373808)
13. Ishida M, Miyamoto M, Naitoh S, Tatsuda D, Hasegawa T, Nemoto T, et al. The SYT-SSX fusion protein down-regulates the cell proliferation regulator COM1 in t(x;18) synovial sarcoma. Mol Cell Biol 2007; 27:1348-55. (Pubitemid 46239817)
14. Master RS, Zinkel M, Petrini JHJ. An alternative mode of translation permits production of a variant NBS1 protein from the common Nijmegenbreakage syndrome allele. Nat Genet 2001;27:417-21. (Pubitemid 32268423)
15. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly (ADP-ribose) polymerase. Nature 2005;434:913-7. (Pubitemid 40559005)
16. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917-21. (Pubitemid 40559006)
17. Jongmans W, Vuillaume M, Chrzanowska K, Smeets D, Sperling K, Hall J. Nijmegen breakage syndrome cells fail to induce the p53-mediated DNA damage response following exposure to ionizing radiation. Mol Cell Biol 1997;17:5016-22. (Pubitemid 27357600)
18. Goldberg M, Stucki M, Falck J, D'Amours D, Rahman D, Pappin D, et al. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 2003;421:952-6. (Pubitemid 36288027)
19. Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003;421:961-6. (Pubitemid 36288029)
20. Williams SR, Dodson EG, Limbo O, Yamada Y, Williams SJ, Guenther G, et al. Nbs1 Flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 2009;139:87-99.
21. Nimonkar AV, Genschel J, Kinoshita E, Polaczek P, Campbell JL, Wyman C, et al. BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev 2011;25:350-62.
22. Robison JG, Lu L, Dixon K, Bissler JJ. DNA lesion-specific co-localization of the Mre11/Rad50/Nbs1 (MRN) complex and replication protein A (RPA) to repair foci. J Biol Chem 2005;280:12927-34.
23. Sung P, Robberson DL. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 1995;82:453-61.
24. Schlegel BP, Jodelka FM, Nunez R. BRCA1 promotes induction of ssDNA by ionizing radiation. Cancer Res 2006;66:5181-9. (Pubitemid 43844941)
25. Mosor M, Zióøkowska 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;20:1454-6. (Pubitemid 44084066)
26. Rozonowski 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;110:343-8. (Pubitemid 351793889)
27. 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;98:1701-5. (Pubitemid 47487904)
28. Nowak J, Mosor M, Zióøkowska I, Wierzbicka M, Pernak-Schwarz M, Przyborska M, et al. Heterozygous carriers of the I171V mutation of the NBS1 gene have a significantly increased risk of solid malignant tumours. Eur J Cancer 2008;44:627-30.
29. Kanka C, Brozek I, Skalska B, Siemiatkowska A, Limon J. Germline NBS1 mutations in families with aggregation of breast and/or ovarian cancer from north-east Poland. Anticancer Res 2007;27:3015-8. (Pubitemid 47228039)
30. Bogdanova N, Schürmann P, Waltes R, Feshchenko S, Zalutsky IV, Bremer M, et al. NBS1 variant I171V and breast cancer risk. Breast Cancer Res Treat 2008;112:75-9.
31. Taylor GM, O'Brien HP, Greaves MF, Ravetto PF, Eden OB. Mutations in the Nijmegen breakage syndrome gene (NBS1) in childhood acute lymphoblastic leukemia. Cancer Res 2003;63:6563-4.
32. Demuth I, Frappart PO, Hildebrand G, Melchers A, Lobitz S, Stöckl L, et al. An inducible null mutant murine model of Nijmegen breakage syndrome proves the essential function of NBS1 in chromosomal stability and cell viability. Hum Mol Genet 2004;13:2385-97. (Pubitemid 39377843)
33. Chen L, Nievera CJ, Lee AY, Wu X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 2008;283:7713-20.
34. Gupta GP, Vanness K, Barlas A, Manova-Todorova KO, Wen YH, Petrini JHJ. The Mre11 complex suppresses oncogene-driven breast tumorigenesis and metastasis. Mol Cell 2013;52:353-65.