BRCA1185delAG tumors may acquire therapy resistance through expression of RING-less BRCA1

Journal of Clinical Investigation

Volumn 126, Issue 8, 2016, Pages 2903-2918

  Drost, Rinske ^a   Dhillon, Kiranjit K ^b   Van Der Gulden, Hanneke ^a   Van Der Heijden, Ingrid ^a   Brandsma, Inger ^c   Cruz, Cristina ^d   Chondronasiou, Dafni ^a   Castroviejo Bermejo, Marta ^d   Boon, Ute ^a   Schut, Eva ^a   Van Der Burg, Eline ^a   Wientjens, Ellen ^a   Pieterse, Mark ^a   Klijn, Christiaan ^a   Klarenbeek, Sjoerd ^a   Loayza Puch, Fabricio ^a   Elkon, Ran ^a   Van Deemter, Liesbeth ^a   Rottenberg, Sven ^a,e   Van De Ven, Marieke ^a   Dekkers, Dick H W ^c   Demmers, Jeroen A A ^c   Van Gent, Dik C ^c   Agami, Reuven ^a   Balmaña, Judith ^d   Serra, Violeta ^d   Taniguchi, Toshiyasu ^b   Bouwman, Peter ^a   Jonkers, Jos ^a   more..

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b Fred Hutchinson Cancer Research Center   (United States)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d VALL D HEBRON UNIVERSITY HOSPITAL   (Spain)

^e UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; BRCA1 PROTEIN; CISPLATIN; CYTOKERATIN 8; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH3; PROTEIN P53; RAD51 PROTEIN; ANTINEOPLASTIC AGENT; BRCA1 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHTHALAZINE DERIVATIVE; PIPERAZINE DERIVATIVE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; CANCER RESISTANCE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE RESPONSE; DNA REPAIR; EMBRYO; ENZYME INHIBITION; FEMALE; FRAMESHIFT MUTATION; GENE DOSAGE; GENE EXPRESSION; GENETICALLY ENGINEERED MOUSE STRAIN; GENOMIC INSTABILITY; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; MALE; MISMATCH REPAIR; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERTANT; RING FINGER MOTIF; TRANSLATION INITIATION; TREATMENT RESPONSE; TRIPLE NEGATIVE BREAST CANCER; ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; CROSS BREEDING; DNA DAMAGE; DRUG RESISTANCE; DRUG SCREENING; FOUNDER EFFECT; GENE DELETION; GENETIC ENGINEERING; GENETIC RECOMBINATION; GENETICS; MAMMARY NEOPLASMS, ANIMAL; METABOLISM; MUTATION;

ALLELES; ANIMALS; ANTINEOPLASTIC AGENTS; BRCA1 PROTEIN; BREAST NEOPLASMS; CISPLATIN; CROSSES, GENETIC; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; FOUNDER EFFECT; FRAMESHIFT MUTATION; GENE DELETION; GENETIC ENGINEERING; HUMANS; MALE; MAMMARY NEOPLASMS, ANIMAL; MICE; MUTATION; NEOPLASM TRANSPLANTATION; PHTHALAZINES; PIPERAZINES; POLY(ADP-RIBOSE) POLYMERASES; RECOMBINATION, GENETIC;

EID: 84987811629     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI70196     Document Type: Article

References (71)

1. DeSantis C, Siegel R, Bandi P, Jemal A. Breast cancer statistics, 2011. CA Cancer J Clin. 2011;61(6):409-418.
2. Rahman N, Stratton MR. The genetics of breast cancer susceptibility. Annu Rev Genet. 1998;32:95-121.
3. Smith TM, et al. Complete genomic sequence and analysis of 117 kb of human DNA containing the gene BRCA1. Genome Res. 1996;6(11):1029-1049.
4. Conti E, Izaurralde E. Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species. Curr Opin Cell Biol. 2005;17(3):316-325.
5. Lejeune F, Maquat LE. Mechanistic links between nonsense-mediated mRNA decay and premRNA splicing in mammalian cells. Curr Opin Cell Biol. 2005;17(3):309-315.
6. Phelan CM, et al. A low frequency of non-founder BRCA1 mutations in Ashkenazi Jewish breast-ovarian cancer families. Hum Mutat. 2002;20(5):352-357.
7. Struewing JP, et al. The carrier frequency of the BRCA1 185delAG mutation is approximately 1 percent in Ashkenazi Jewish individuals. Nat Genet. 1995;11(2):198-200.
8. Roa BB, Boyd AA, Volcik K, Richards CS. Ashkenazi Jewish population frequencies for common mutations in BRCA1 and BRCA2. Nat Genet. 1996;14(2):185-187.
9. Moslehi R, et al. BRCA1 and BRCA2 muta-tion analysis of 208 Ashkenazi Jewish women with ovarian cancer. Am J Hum Genet. 2000;66(4):1259-1272.
10. Frank TS, et al. Clinical characteristics of individuals with germline mutations in BRCA1 and BRCA2: analysis of 10,000 individuals. J Clin Oncol. 2002;20(6):1480-1490.
11. Levy-Lahad E, Friedman E. Cancer risks among BRCA1 and BRCA2 mutation carriers. Br J Cancer. 2007;96(1):11-15.
12. Venkitaraman AR. Cancer suppression by the chromosome custodians, BRCA1 and BRCA2. Science 2014;343(6178):1470-1475.
13. Prakash R, Zhang Y, Feng W, Jasin M. Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins. Cold Spring Harb Perspect Biol. 2015;7(4):a016600.
14. Bhattacharyya A, Ear US, Koller BH, Weichselbaum RR, Bishop DK. The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J Biol Chem. 2000;275(31):23899-23903.
15. Boyd J, et al. Clinicopathologic features of BRCAlinked and sporadic ovarian cancer. JAMA. 2000;283(17):2260-2265.
16. Ben David Y, et al. Effect of BRCA mutations on the length of survival in epithelial ovarian tumors. J Clin Oncol. 2002;20(2):463-466.
17. Foulkes WD. BRCA1 and BRCA2: chemosensitivity, treatment outcomes and prognosis. Fam Cancer. 2006;5(2):135-142.
18. Chetrit A, Hirsh-Yechezkel G, Ben-David Y, Lubin F, Friedman E, Sadetzki S. Effect of BRCA1/2 mutations on long-term survival of patients with invasive ovarian cancer: the national Israeli study of ovarian cancer. J Clin Oncol. 2008;26(1):20-25.
19. Byrski T, et al. Pathologic complete response rates in young women with BRCA1-positive breast cancers after neoadjuvant chemotherapy. J Clin Oncol. 2010;28(3):375-379.
20. Vollebergh MA, et al. An aCGH classifier derived from BRCA1-mutated breast cancer and benefit of high-dose platinum-based chemotherapy in HER2-negative breast cancer patients. Ann Oncol. 2011;22(7):1561-1570.
21. Bryant HE, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434(7035):913-917.
22. Farmer H, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434(7035):917-921.
23. Rottenberg S, et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci USA. 2008;105(44):17079-17084.
24. Audeh MW, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet. 2010;376(9737):245-251.
25. Fong PC, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med. 2009;361(2):123-134.
26. Fong PC, et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol. 2010;28(15):2512-2519.
27. Gelmon KA, et al. Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, openlabel, non-randomised study. Lancet Oncol. 2011;12(9):852-861.
28. Tutt A, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet. 2010;376(9737):235-244.
29. Ledermann J, et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 2014;15(8):852-861.
30. Tewari KS, Eskander RN, Monk BJ. Development of olaparib for BRCA-deficient recurrent epithelial ovarian cancer. Clin Cancer Res. 2015;21(17):3829-3835.
31. Huen MS, Sy SM, Chen J. BRCA1 and its toolbox for the maintenance of genome integrity. Nat Rev Mol Cell Biol. 2010;11(2):138-148.
32. Mallery DL, Vandenberg CJ, Hiom K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 2002;21(24):6755-6762.
33. Xia Y, Pao GM, Chen HW, Verma IM, Hunter T. Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J Biol Chem. 2003;278(7):5255-5263.
34. Morris JR, Solomon E. BRCA1 : BARD1 induces the formation of conjugated ubiquitin structures, dependent on K6 of ubiquitin, in cells during DNA replication and repair. Hum Mol Genet. 2004;13(8):807-817.
35. Shabbeer S, et al. BRCA1 targets G2/M cell cycle proteins for ubiquitination and proteasomal degradation. Oncogene. 2013;32(42):5005-5016.
36. Scully R, et al. BRCA1 is a component of the RNA polymerase II holoenzyme. Proc Natl Acad Sci USA. 1997;94(11):5605-5610.
37. Scully R, et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 1997;88(2):265-275.
38. Anderson SF, Schlegel BP, Nakajima T, Wolpin ES, Parvin JD. BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat Genet. 1998;19(3):254-256.
39. Bochar DA, et al. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell. 2000;102(2):257-265.
40. Yarden RI, Brody LC. BRCA1 interacts with components of the histone deacetylase complex. Proc Natl Acad Sci USA. 1999;96(9):4983-4988.
41. Patel KJ, Crossan GP, Hodskinson MR. "Ring-fencing" BRCA1 tumor suppressor activity. Cancer Cell. 2011;20(6):693-695.
42. Shakya R, et al. BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 2011;334(6055):525-528.
43. Drost R, et al. BRCA1 RING function is essential for tumor suppression but dispensable for therapy resistance. Cancer Cell. 2011;20(6):797-809.
44. Dekker M, Brouwers C, te Riele H. Targeted gene modification in mismatch-repair-deficient embryonic stem cells by single-stranded DNA oligonucleotides. Nucleic Acids Res. 2003;31(6):e27.
45. Dekker M, et al. Effective oligonucleotidemediated gene disruption in ES cells lacking the mismatch repair protein MSH3. Gene Ther. 2006;13(8):686-694.
46. Dekker M, et al. Transient suppression of MLH1 allows effective single-nucleotide substitution by single-stranded DNA oligonucleotides. Mutat Res. 2011;715(1-2):52-60.
47. Aarts M, Dekker M, de Vries S, van der Wal A, te Riele H. Generation of a mouse mutant by oligonucleotide-mediated gene modification in ES cells. Nucleic Acids Res. 2006;34(21):e147.
48. Liu X, et al. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basallike breast cancer. Proc Natl Acad Sci USA. 2007;104(29):12111-12116.
49. Lakhani SR, et al. The pathology of familial breast cancer: predictive value of immunohistochemical markers estrogen receptor, progesterone receptor, HER-2, and p53 in patients with mutations in BRCA1 and BRCA2. J Clin Oncol. 2002;20(9):2310-2318.
50. Tirkkonen M, et al. Distinct somatic genetic changes associated with tumor progression in carriers of BRCA1 and BRCA2 germ-line mutations. Cancer Res. 1997;57(7):1222-1227.
51. Holstege H, et al. Cross-species comparison of aCGH data from mouse and human BRCA1-and BRCA2-mutated breast cancers. BMC Cancer. 2010;10:455.
52. Klijn C, et al. Identification of cancer genes using a statistical framework for multiexperiment analysis of nondiscretized array CGH data. Nucleic Acids Res. 2008;36(2):e13.
53. de Ronde JJ, et al. KC-SMARTR: An R package for detection of statistically significant aberrations in multi-experiment aCGH data. BMC Res Notes. 2010;3:298.
54. Pajic M, et al. Tumor-initiating cells are not enriched in cisplatin-surviving BRCA1;p53-deficient mammary tumor cells in vivo. Cell Cycle. 2010;9(18):3780-3791.
55. Rottenberg S, et al. Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer. Proc Natl Acad Sci USA. 2007;104(29):12117-12122.
56. Silver DP, et al. Efficacy of neoadjuvant Cisplatin in triple-negative breast cancer. J Clin Oncol. 2010;28(7):1145-1153.
57. Edwards SL, et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature. 2008;451(7182):1111-1115.
58. Sakai W, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008;451(7182):1116-1120.
59. Swisher EM, Sakai W, Karlan BY, Wurz K, Urban N, Taniguchi T. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res. 2008;68(8):2581-2586.
60. Norquist B, et al. Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol. 2011;29(22):3008-3015.
61. Jaspers JE, et al. Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors. Cancer Discov. 2013;3(1):68-81.
62. Elstrodt F, et al. BRCA1 mutation analysis of 41 human breast cancer cell lines reveals three new deleterious mutants. Cancer Res. 2006;66(1):41-45.
63. Ingolia NT, Lareau LF, Weissman JS. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell. 2011;147(4):789-802.
64. Sotiropoulou PA, et al. BRCA1 deficiency in skin epidermis leads to selective loss of hair follicle stem cells and their progeny. Genes Dev. 2013;27(1):39-51.
65. Roche-Lestienne C, et al. Several types of mutations of the Abl gene can be found in chronic myeloid leukemia patients resistant to STI571, and they can pre-exist to the onset of treatment. Blood. 2002;100(3):1014-1018.
66. Buisson M, Anczukow O, Zetoune AB, Ware MD, Mazoyer S. The 185delAG mutation (c.68-69delAG) in the BRCA1 gene triggers translation reinitiation at a downstream AUG codon. Hum Mutat. 2006;27(10):1024-1029.
67. Perrin-Vidoz L, Sinilnikova OM, Stoppa-Lyonnet D, Lenoir GM, Mazoyer S. The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Hum Mol Genet. 2002;11(23):2805-2814.
68. Cong L, et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013;339(6121):819-823.
69. Bouwman P, et al. A high-throughput functional complementation assay for classification of BRCA1 missense variants. Cancer Discov. 2013;3(10):1142-1155.
70. Bouwman P, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol. 2010;17(6):688-695.
71. Stap J, et al. Induction of linear tracks of DNA double-strand breaks by alpha-particle irradiation of cells. Nat Methods. 2008;5(3):261-266.