BRCAness: A deeper insight into basal-like breast tumors

Annals of Oncology

Volumn 24, Issue SUPPL.B, 2013, Pages

  De Summa, S ^a   Pinto, R ^a   Sambiasi, D ^a   Petriella, D ^a   Paradiso, V ^a   Paradiso, A ^a   Tommasi, S ^a  

^a NATIONAL CANCER INSTITUTE GIOVANNI PAOLO II   (Italy)

Author keywords

APE1; Basal like; BRCAness; DNA repair; PARP inhibitors; Triple negative breast cancer

Indexed keywords

8 HYDROXY 2 METHYL 4(3H) QUINAZOLINONE; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; BRCA2 PROTEIN; BUPARLISIB; CARBOPLATIN; CISPLATIN; CYCLOPHOSPHAMIDE; DNA; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; E 330; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GEMCITABINE; INIPARIB; LYASE INHIBITOR; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; PACLITAXEL; PROTEIN APE1; RAD51 PROTEIN; RUCAPARIB; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VELIPARIB;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BASAL LIKE BREAST CANCER; BREAST CANCER; BREAST CARCINOGENESIS; COPY NUMBER VARIATION; DNA DAMAGE; DNA MICROARRAY; DNA REPAIR; DRUG EFFICACY; ENZYME INHIBITION; EPIGENETICS; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MOLECULARLY TARGETED THERAPY; MULTICENTER STUDY (TOPIC); NONHUMAN; OVERALL SURVIVAL; OXIDATIVE STRESS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER;

APE1; BASAL-LIKE; BRCANESS; DNA REPAIR; PARP INHIBITORS; TRIPLE-NEGATIVE BREAST CANCER;

BRCA1 PROTEIN; BRCA2 PROTEIN; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; FEMALE; HUMANS; MOLECULAR TARGETED THERAPY; POLY(ADP-RIBOSE) POLYMERASES; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84886298881     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdt306     Document Type: Article

References (101)

1. Prat A, Baselga J. The role of hormonal therapy in the management of hormonalreceptor- positive breast cancer with co-expression of HER2. Nat Clin Pract Oncol 2008; 5: 531-542.
2. Kaplan HG, Malmgren JA. Impact of triple negative phenotype on breast cancer prognosis. Breast J 2008; 14: 456-463.
3. Rakha EA, El-Sayed ME, Green AR et al. Biologic and clinical characteristics of breast cancer with single hormone receptor positive phenotype. J Clin Oncol 2007; 25: 4772-4778.
4. Azambuja E, Durbecq V, Rosa DD et al. HER-2 overexpression/amplification and its interaction with taxane-based therapy in breast cancer. Ann Oncol 2008; 19: 223-232.
5. Rakha EA, Chan S. Metastatic triple-negative breast cancer. Clin Oncol (R Coll Radiol) 2011; 23: 587-600.
6. Haffty BG, Yang Q, Reiss M et al. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol 2006; 24: 5652-5657.
7. Dent R, Trudeau M, Pritchard KI et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007; 13: 4429-4434.
8. Perou CM, Sorlie T, Eisen MB et al. Molecular portraits of human breast tumours. Nature 2000; 406: 747-752.
9. Sorlie T, Perou CM, Tibshirani R et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001; 98: 10869-10874.
10. Herschkowitz JI, Simin K, Weigman VJ et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007; 8: R76.
11. Millikan RC, Newman B, Tse CK et al. Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 2008; 109: 123-139.
12. Cheang MC, Chia SK, Voduc D. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 2009; 101: 736-750.
13. Niemeier LA, Dabbs DJ, Beriwal S et al. Androgen receptor in breast cancer: expression in estrogen receptor-positive tumors and in estrogen receptornegative tumors with apocrine differentiation. Mod Pathol 2010; 23: 205-212.
14. Foulkes WD, Stefansson IM, Chappuis PO et al. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J Natl Cancer Inst 2003; 95: 1482-1485.
15. Waddell N, Arnold J, Cocciardi S et al. Subtypes of familial breast tumours revealed by expression and copy number profiling. Breast Cancer Res Treat 2010; 123: 661-677.
16. Kreike B, van Kouwenhove M, Horlings H et al. Gene expression profiling and histopathological characterization of triple-negative/basal-like breast carcinomas. Breast Cancer Res 2007; 9: R65.
17. Al Tamimi DM, Shawarby MA, Ahmed A et al. Protein expression profile and prevalence pattern of the molecular classes of breast cancer-a Saudi population based study. BMC Cancer 2010; 10: 223.
18. Lehmann BD, Bauer JA, Chen X et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121: 2750-2767.
19. Bertucci F, Finetti P, Cervera N et al. How basal are triple-negative breast cancers? Int J Cancer 2008; 123: 236-240.
20. Venkitaraman AR. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 2002; 108: 171-182.
21. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer 2004; 4: 665-676.
22. Boulton SJ. Cellular functions of the BRCA tumour-suppressor proteins. Biochem Soc Trans 2006; 34: 633-645.
23. Hartman AR, Ford JM. BRCA1 induces DNA damage recognition factors and enhances nucleotide excision repair. Nat Genet 2002; 32: 180-184.
24. Greenberg RA, Sobhian B, Pathania S et al. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev 2006; 20: 34-46.
25. Paull TT, Cortez D, Bowers B et al. Direct DNA binding by Brca1. Proc Natl Acad Sci USA 2001; 98: 6086-6091.
26. Starita LM, Parvin JD. The multiple nuclear functions of BRCA1: transcription, ubiquitination and DNA repair. Curr Opin Cell Biol 2003; 15: 345-350.
27. Ye Q, Hu YF, Zhong H et al. BRCA1-induced large-scale chromatin unfolding and allele-specific effects of cancer-predisposing mutations. J Cell Biol 2001; 155: 911-921.
28. Wang Y, Cortez D, Yazdi P et al. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 2000; 14: 927-939.
29. Gowen LC, Avrutskaya AV, Latour AM et al. BRCA1 required for transcriptioncoupled repair of oxidative DNA damage. Science 1998; 281: 1009-1012.
30. Le Page F, Randrianarison V, Marot D et al. BRCA1 and BRCA2 are necessary for the transcription-coupled repair of the oxidative 8-oxoguanine lesion in human cells. Cancer Res 2000; 60: 5548-5552.
31. Cavalieri E, Rogan E. Catechol quinones of estrogens in the initiation of breast, prostate, and other human cancers: keynote lecture. Ann N Y Acad Sci 2006; 1089: 286-301.
32. Saha T, Rih JK, Roy R et al. Transcriptional regulation of the base excision repair pathway by BRCA1. J Biol Chem 2010; 285: 19092-19105.
33. Sotiriou C, Neo SY, McShane LM et al. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci USA 2003; 100: 10393-10398.
34. Nielsen TO, Hsu FD, Jensen K et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. ClinCancer Res 2004; 10: 5367-5374.
35. Savage K, Lambros MB, Robertson D et al. Caveolin 1 is overexpressed and amplified in a subset of basal-like and metaplastic breast carcinomas: a morphologic, ultrastructural, immunohistochemical, and in situ hybridization analysis. Clin Cancer Res 2007; 13: 90-101.
36. Kim MJ, Ro JY, Ahn SH et al. Clinicopathologic significance of the basal-like subtype of breast cancer: a comparison with hormone receptor and Her2/neuoverexpressing phenotypes. Hum Pathol 2006; 37: 1217-1226.
37. Foulkes WD, Brunet JS, Stefansson IM et al. The prognostic implication of the basal-like (cyclin E high/p27 low/p53+/glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res 2004; 64: 830-835.
38. Potemski P, Kusinska R, Watala C et al. Prognostic relevance of basal cytokeratin expression in operable breast cancer. Oncology 2005; 69: 478-485.
39. Rakha EA, Putti TC, Abd El-Rehim DM et al. Morphological and immunophenotypic analysis of breast carcinomas with basal and myoepithelial differentiation. J Pathol 2006; 208: 495-506.
40. Kusinska R, Potemski P, Jesionek-Kupnicka D et al. Immunohistochemical identification of basal-type cytokeratins in invasive ductal breast carcinoma- relation with grade, stage, estrogen receptor and HER2. Pol J Pathol 2005; 56: 107-110.
41. Charafe-Jauffret E, Monville F, Bertucci F et al. Moesin expression is a marker of basal breast carcinomas. Int J Cancer 2007; 121: 1779-1785.
42. Rodriguez-Pinilla SM, Sarrio D, Honrado E et al. Prognostic significance of basallike phenotype and fascin expression in node-negative invasive breast carcinomas. Clin Cancer Res 2006; 12: 1533-1539.
43. Pinilla SM, Honrado E, Hardisson D et al. Caveolin-1 expression is associated with a basal-like phenotype in sporadic and hereditary breast cancer. Breast Cancer Res Treat 2006; 99: 85-90.
44. Reis-Filho JS, Milanezi F, Paredes J et al. Novel and classic myoepithelial/stem cell markers in metaplastic carcinomas of the breast. Appl Immunohistochem Mol Morphol 2003; 11: 1-8.
45. Leibl S, Gogg-Kammerer M, Sommersacher A et al. Metaplastic breast carcinomas: are they of myoepithelial differentiation?: immunohistochemicalprofile of the sarcomatoid subtype using novel myoepithelial markers. Am J Surg Pathol 2005; 29: 347-353.
46. Manie E, Vincent-Salomon A, Lehmann-Che J et al. High frequency of TP53 mutation in BRCA1 and sporadic basal-like carcinomas but not in BRCA1 luminal breast tumors. Cancer Res 2009; 69: 663-671.
47. Jonsson G, Staaf J, Vallon-Christersson J et al. The retinoblastoma gene undergoes rearrangements in BRCA1-deficient basal-like breast cancer. Cancer Res 2012; 72: 4028-4036.
48. Kenemans P, Verstraeten RA, Verheijen RH. Oncogenic pathways in hereditary and sporadic breast cancer. Maturitas 2004; 49: 34-43.
49. Staff S, Isola J, Tanner M. Haplo-insufficiency of BRCA1 in sporadic breast cancer. Cancer Res 2003; 63: 4978-4983.
50. Catteau A, Harris WH, Xu CF et al. Methylation of the BRCA1 promoter region in sporadic breast and ovarian cancer: correlation with disease characteristics. Oncogene 1999; 18: 1957-1965.
51. Esteller M, Silva JM, Dominguez G et al. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J Natl Cancer Inst 2000; 92: 564-569.
52. Turner NC, Reis-Filho JS, Russell AM et al. BRCA1 Dysfunction in sporadic basal-like breast cancer. Oncogene 2007; 26: 2126-2132.
53. Ding L, Ellis MJ, Li S et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010; 464: 999-1005.
54. Adelaide J, Finetti P, Bekhouche I et al. Integrated profiling of basal and luminal breast cancers. Cancer Res 2007; 67: 11565-11575.
55. Haverty PM, Fridlyand J, Li L et al. High-resolution genomic and expression analyses of copy number alterations in breast tumors. Genes Chromosomes Cancer 2008; 47: 530-542.
56. Gewinner C, Wang ZC, Richardson A et al. Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell 2009; 16: 115-125.
57. Weigman VJ, Chao HH, Shabalin AA et al. Basal-like Breast cancer DNA copy number losses identify genes involved in genomic instability, response to therapy, and patient survival. Breast Cancer Res Treat 2012; 133: 865-880.
58. Holstege H, Joosse SA, van Oostrom CT et al. High incidence of proteintruncating TP53 mutations in BRCA1-related breast cancer. Cancer Res 2009; 69: 3625-3633.
59. Saal LH, Gruvberger-Saal SK, Persson C et al. Recurrent gross mutations of the PTEN tumor suppressor gene in breast cancers with deficient DSB repair. Nat Genet 2008; 40: 102-107.
60. Mendes-Pereira AM, Martin SA, Brough R et al. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol Med 2009; 1: 315-322.
61. Holstege H, Horlings HM, Velds A et al. BRCA1-mutated and basal-like breast cancers have similar aCGH profiles and a high incidence of protein truncating TP53 mutations. BMC Cancer 2010; 10: 654.
62. Brugarolas J, Jacks T. Double indemnity: p53, BRCA and cancer. p53 mutation partially rescues developmental arrest in Brca1 and Brca2 null mice, suggesting a role for familial breast cancer genes in DNA damage repair. Nat Med 1997; 3: 721-722.
63. Clarke RB, Howell A, Potten CS et al. Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res 1997; 57: 4987-4991.
64. Young SR, Pilarski RT, Donenberg T et al. The prevalence of BRCA1 mutations among young women with triple-negative breast cancer. BMC Cancer 2009; 9: 86.
65. Sabatier R, Adelaide J, Finetti P et al. BARD1 homozygous deletion, a possible alternative to BRCA1 mutation in basal breast cancer. Genes Chromosomes Cancer 2010; 49: 1143-1151.
66. Wu LC, Wang ZW, Tsan JT et al. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat Genet 1996; 14: 430-440.
67. Irminger-Finger I, Soriano JV, Vaudan G et al. In vitro repression of Brca1- associated RING domain gene, Bard1, induces phenotypic changes in mammary epithelial cells. J Cell Biol 1998; 143: 1329-1339.
68. Mallery DL, Vandenberg CJ, Hiom K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J 2002; 21: 6755-6762.
69. Chen A, Kleiman FE, Manley JL et al. Autoubiquitination of the BRCA1. BARD1 RING ubiquitin ligase. J Biol Chem 2002; 277: 22085-22092.
70. McCarthy EE, Celebi JT, Baer R et al. Loss of Bard1, the heterodimeric partner of the Brca1 tumor suppressor, results in early embryonic lethality and chromosomal instability. Mol Cell Biol 2003; 23: 5056-5063.
71. Wang W. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 2007; 8: 735-748.
72. Alli E, Sharma VB, Sunderesakumar P et al. Defective repair of oxidative DNA damage in triple-negative breast cancer confers sensitivity to inhibition of poly (ADP-ribose) polymerase. Cancer Res 2009; 69: 3589-3596.
73. Moskwa P, Buffa FM, Pan Y et al. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 2011; 41: 210-220.
74. Ossovskaya V, Koo IC, Kaldjian EP et al. Upregulation of poly (ADP-ribose) polymerase-1 (PARP1) in triple-negative breast cancer and other primary human tumor types. Genes Cancer 2010; 1: 812-821.
75. Domagala P, Huzarski T, Lubinski J et al. PARP-1 expression in breast cancer including BRCA1-associated, triple negative and basal-like tumors: possible implications for PARP-1 inhibitor therapy. Breast Cancer Res Treat 2011; 127: 861-869.
76. Poletto M, Loreto CD, Marasco D et al. Acetylation on critical lysine residues of apurinic/apyrimidinic endonuclease 1 (APE1) in triple negative breast cancers. Biochem Biophys Res Commun 2012; 424: 34-39.
77. Fantini D, Vascotto C, Marasco D et al. Critical lysine residues within the overlooked N-terminal domain of human APE1 regulate its biological functions. Nucleic Acids Res 2010; 38: 8239-8256.
78. Sultana R, McNeill DR, Abbotts R et al. Synthetic lethal targeting of DNA doublestrand break repair deficient cells by human apurinic/apyrimidinic endonuclease inhibitors. Int J Cancer 2012; 131: 2433-2444.
79. Glas M, Happold C, Rieger J et al. Long-term survival of patients with glioblastoma treated with radiotherapy and lomustine plus temozolomide. J Clin Oncol 2009; 27: 1257-1261.
80. Dunn J, Baborie A, Alam F et al. Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer 2009; 101: 124-131.
81. Busch C, Geisler J, Lillehaug JR et al. MGMT expression levels predict disease stabilisation, progression-free and overall survival in patients with advanced melanomas treated with DTIC. Eur J Cancer 2010; 46: 2127-2133.
82. Matsukura S, Miyazaki K, Yakushiji H et al. Expression and prognostic significance of O6-methylguanine-DNA methyltransferase in hepatocellular, gastric, and breast cancers. Ann Surg Oncol 2001; 8: 807-816.
83. Neto JC, Carvalho K, Olivieri E et al. Evaluation of O6-methylguanine-DNA methyltransferase by immunohistochemistry: best clinical and research practices. Pathol Res Pract 2011; 207: 492-497.
84. Fumagalli C, Pruneri G, Possanzini P et al. Methylation of O(6)-methylguanine- DNA methyltransferase (MGMT) promoter gene in triple-negative breast cancer patients. Breast Cancer Res Treat 2012; 134: 131-137.
85. de Murcia G, Huletsky A, Lamarre D et al. Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J Biol Chem 1986; 261: 7011-7017.
86. Dobzhansky T. Genetics of natural populations. Xiii. Recombination and variability in populations of Drosophila Pseudoobscura. Genetics 1946; 31: 269-290.
87. Lucchesi JC. Synthetic lethality and semi-lethality among functionally related mutants of Drosophila melanfgaster. Genetics 1968; 59: 37-44.
88. Tutt AN, Lord CJ, McCabe N et al. Exploiting the DNA repair defect in BRCA mutant cells in the design of new therapeutic strategies for cancer. Cold Spring Harb Symp Quant Biol 2005; 70: 139-148.
89. Tutt A, Robson M, Garber JE 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: 235-244.
90. Chuang HC, Kapuriya N, Kulp SK et al. Differential anti-proliferative activities of poly(ADP-ribose) polymerase (PARP) inhibitors in triple-negative breast cancer cells. Breast Cancer Res Treat 2012; 134: 649-659.
91. O'Shaughnessy J, Osborne C, Pippen JE et al. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med 2011; 364: 205-214.
92. O'Shaughnessy J, Schwartzberg LS, Danso MA et al. A randomized phase III study of iniparib (BSI-201) in combination with gemcitabine/carboplatin (G/C) in metastatic triple negative breast cancer (TNBC). J Clinic Oncol 2011; 29: 1007.
93. Sanofi-aventis reports top-line results from phase III study with iniparib (BSI-201) in metastatic triple-negative breast cancer. http://sanofi-aventis.mediaroom.com/ index.php?=43&item=310 (26 July 2012, date last accessed).
94. Barzilay G, Walker LJ, Robson CN et al. Site-directed mutagenesis of the human DNA repair enzyme HAP1: identification of residues important for AP endonuclease and RNase H activity. Nucleic Acids Res 1995; 23: 1544-1550.
95. Rouleau M, Patel A, Hendzel MJ et al. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 2010; 10: 293-301.
96. Underhill C, Toulmonde M, Bonnefoi H. A review of PARP inhibitors: from bench to bedside. Ann Oncol 2011; 22: 268-279.
97. Madhusudan S, Smart F, Shrimpton P et al. Isolation of a small molecule inhibitor of DNA base excision repair. Nucleic Acids Res 2005; 33: 4711-4724.
98. Mohammed MZ, Vyjayanti VN, Laughton CA et al. Development and evaluation of human AP endonuclease inhibitors in melanoma and glioma cell lines. Br J Cancer 2011; 104: 653-663.
99. Luo M, Kelley MR. Inhibition of the human apurinic/apyrimidinic endonuclease (APE1) repair activity and sensitization of breast cancer cells to DNA alkylating agents with lucanthone. Anticancer Res 2004; 24: 2127-2134.
100. Naidu MD, Mason JM, Pica RV et al. Radiation resistance in glioma cells determined by DNA damage repair activity of Ape1/Ref-1. J Radiat Res 2010; 51: 393-404.
101. Al-Safi RI, Odde S, Shabaik Y et al. Small-molecule inhibitors of APE1 DNA repair function: an overview. Curr Mol Pharmacol 2012; 5: 14-35.