DNA repair and damage pathways in breast cancer development and therapy

DNA Repair

Volumn 54, Issue , 2017, Pages 22-29

  Majidinia, Maryam ^a   Yousefi, Bahman ^b,c,d  

^a URMIA UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Breast cancer; Chemotherapy; DNA damage; DNA repair

Indexed keywords

ABELSON KINASE; ATM PROTEIN; ATR PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN E; CYCLINE; CYCLOPHOSPHAMIDE; DOCETAXEL; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIRUBICIN; ESTROGEN RECEPTOR; FANCONI ANEMIA GROUP D2 PROTEIN; HISTONE H2AX; PACLITAXEL; PROGESTERONE RECEPTOR; PROTEIN; PROTEIN MDM2; PROTEIN P53; PROTEIN RAD17; UNCLASSIFIED DRUG;

BASAL LIKE BREAST CANCER; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER HORMONE THERAPY; CANCER THERAPY; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA REPAIR; EXCISION REPAIR; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN EPIDERMAL GROWTH FACTOR RECEPTOR 2 POSITIVE BREAST CANCER; LUMINAL A BREAST CANCER; LUMINAL B BREAST CANCER; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR SUPPRESSOR GENE; ANIMAL; BREAST NEOPLASMS; FEMALE; GENETICS; METABOLISM;

ANIMALS; BREAST NEOPLASMS; DNA DAMAGE; DNA REPAIR; FEMALE; HUMANS;

EID: 85017687847     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2017.03.009     Document Type: Review

References (131)

1. [1] Pearl, L.H., Schierz, A.C., Ward, S.E., Al-Lazikani, B., Pearl, F.M., Therapeutic opportunities within the DNA damage response. Nat. Rev. Cancer 15:3 (2015), 166–180.
2. [2] Hosoya, N., Miyagawa, K., Targeting DNA damage response in cancer therapy. Cancer Sci. 105:4 (2014), 370–388.
3. [3] Tian, H., Gao, Z., Li, H., Zhang, B., Wang, G., Zhang, Q., et al. DNA damage response – a double-edged sword in cancer prevention and cancer therapy. Cancer Lett. 358:1 (2015), 8–16.
4. [4] di Fagagna, F.d.A., A direct role for small non-coding RNAs in DNA damage response. Trends Cell Biol. 24:3 (2014), 171–178.
5. [5] Hoeijmakers, J.H., DNA damage, aging, and cancer. N. Engl. J. Med. 361:15 (2009), 1475–1485.
6. [6] Ciriello, G., Miller, M.L., Aksoy, B.A., Senbabaoglu, Y., Schultz, N., Sander, C., Emerging landscape of oncogenic signatures across human cancers. Nat. Genet. 45:10 (2013), 1127–1133.
7. [7] Reinhardt, H.C., Jiang, H., Hemann, M.T., Yaffe, M.B., Exploiting synthetic lethal interactions for targeted cancer therapy. Cell Cycle 8:19 (2009), 3112–3119.
8. [8] Lam, S., Jimenez, C., Boven, E., Breast cancer classification by proteomic technologies: current state of knowledge. Cancer Treat. Rev. 40:1 (2014), 129–138.
9. [9] Vuong, D., Simpson, P.T., Green, B., Cummings, M.C., Lakhani, S.R., Molecular classification of breast cancer. Virchows Archiv. 465:1 (2014), 1–14.
10. [10] Majidinia, M., Yousefi, B., Breast tumor stroma: a driving force in the development of resistance to therapies. Chem. Biol. Drug Des.(January), 2017, 10.1111/cbdd.12893.
11. [11] Gonzalez-Angulo, A.M., Timms, K.M., Liu, S., Chen, H., Litton, J.K., Potter, J., et al. Incidence and outcome of BRCA mutations in unselected patients with triple receptor-negative breast cancer. Clin. Cancer Res. 17:5 (2011), 1082–1089.
12. [12] Walsh, T., Casadei, S., Coats, K.H., Swisher, E., Stray, S.M., Higgins, J., et al. Spectrum of mutations in BRCA1, BRCA2, CHEK2, and TP53 in families at high risk of breast cancer. JAMA 295:12 (2006), 1379–1388.
13. [13] Karimian, A., Ahmadi, Y., Yousefi, B., Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Rep. (Amst.) 42 (2016), 63–71.
14. [14] Prat, A., Perou, C.M., Deconstructing the molecular portraits of breast cancer. Mol. Oncol. 5:1 (2011), 5–23.
15. [15] Higgins, M.J., Baselga, J., Breast cancer in 2010: novel targets and therapies for a personalized approach. Nat. Rev. Clin. Oncol. 8:2 (2011), 65–66.
16. [16] Guler, G., Himmetoglu, C., Jimenez, R.E., Geyer, S.M., Wang, W.P., Costinean, S., et al. Aberrant expression of DNA damage response proteins is associated with breast cancer subtype and clinical features. Breast Cancer Res. Treat. 129:2 (2011), 421–432.
17. [17] Foulkes, W.D., Smith, I.E., Reis-Filho, J.S., Triple-negative breast cancer. N. Engl. J. Med. 363:20 (2010), 1938–1948.
18. [18] Hamidinia, M., Ghafourian Boroujerdnia, M., Talaiezadeh, A., Solgi, G., Roshani, R., Iranprast, S., Khodadadi, A., Increased P-35, EBI3 transcripts and other Treg markers in peripheral blood mononuclear cells of breast cancer patients with different clinical stages. Adv. Pharm. Bull. 5:2 (2015), 261–267.
19. [19] Duffy, M.J., O'Donovan, N., Crown, J., Use of molecular markers for predicting therapy response in cancer patients. Cancer Treat. Rev. 37:2 (2011), 151–159.
20. [20] Rao, X., Di Leva, G., Li, M., Fang, F., Devlin, C., Hartman-Frey, C., et al. MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways. Oncogene 30:9 (2011), 1082–1097.
21. [21] Carey, L., Winer, E., Viale, G., Cameron, D., Gianni, L., Triple-negative breast cancer: disease entity or title of convenience?. Nat. Rev. Clin. Oncol. 7:12 (2010), 683–692.
22. [22] Allred, D.C., Wu, Y., Mao, S., Nagtegaal, I.D., Lee, S., Perou, C.M., et al. Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin. Cancer Res. 14:2 (2008), 370–378.
23. [23] 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., 7(4), 2015, a016600.
24. [24] Jasin, M., Rothstein, R., Repair of strand breaks by homologous recombination. Cold Spring Harb. Perspect. Biol., 5(11), 2013, a012740.
25. [25] Aymard, F., Bugler, B., Schmidt, C.K., Guillou, E., Caron, P., Briois, S., et al. Transcriptionally active chromatin recruits homologous recombination at DNA double strand breaks. Nat. Struct. Mol. Biol., 21(4), 2014, 366.
26. [26] Maacke, H., Opitz, S., Jost, K., Hamdorf, W., Henning, W., Krüger, S., et al. Over-expression of wild-type Rad51 correlates with histological grading of invasive ductal breast cancer. Int. J. Cancer 88:6 (2000), 907–913.
27. [27] Kato, M., Yano, K.-I., Matsuo, F., Saito, H., Katagiri, T., Kurumizaka, H., et al. Identification of Rad51 alteration in patients with bilateral breast cancer. J. Hum. Genet. 45:3 (2000), 133–137.
28. [28] Gasparini, P., Lovat, F., Fassan, M., Casadei, L., Cascione, L., Jacob, N.K., et al. Protective role of miR-155 in breast cancer through RAD51 targeting impairs homologous recombination after irradiation. Proc. Natl. Acad. Sci. U. S. A. 111:12 (2014), 4536–4541.
29. [29] Yousefi, B., Samadi, N., Baradaran, B., Shafiei-Irannejad, V., Zarghami, N., Peroxisome proliferator-activated receptor ligands and their role in chronic myeloid leukemia: therapeutic strategies. Chem. Biol. Drug Des. 88 (2016), 17–25.
30. [30] Thomas, G., Jacobs, K.B., Kraft, P., Yeager, M., Wacholder, S., Cox, D.G., et al. A multistage genome-wide association study in breast cancer identifies two new risk alleles at 1p11. 2 and 14q24. 1 (RAD51L1). Nat. Genet. 41:5 (2009), 579–584.
31. [31] King, M.-C., Marks, J.H., Mandell, J.B., Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 302:5645 (2003), 643–646.
32. [32] Moynahan, M.E., Chiu, J.W., Koller, B.H., Jasin, M., Brca1 controls homology-directed DNA repair. Mol. Cell 4:4 (1999), 511–518.
33. [33] Gonzalez, R., Silva, J., Dominguez, G., Garcia, J., Martinez, G., Vargas, J., et al. Detection of loss of heterozygosity at RAD51, RAD52, RAD54 and BRCA1 and BRCA2 loci in breast cancer: pathological correlations. Br. J. Cancer, 81(3), 1999, 503.
34. [34] Buisson, R., Dion-Côté, A.-M., Coulombe, Y., Launay, H., Cai, H., Stasiak, A.Z., et al. Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination. Nat. Struct. Mol. Biol. 17:10 (2010), 1247–1254.
35. [35] Rahman, N., Seal, S., Thompson, D., Kelly, P., Renwick, A., Elliott, A., et al. PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat. Genet. 39:2 (2007), 165–167.
36. [36] Véquaud, E., Desplanques, G., Jézéquel, P., Juin, P., Barillé-Nion, S., Survivin contributes to DNA repair by homologous recombination in breast cancer cells. Breast Cancer Res. Treat. 155:1 (2016), 53–63.
37. [37] Zeidler, M., Varambally, S., Cao, Q., Chinnaiyan, A.M., Ferguson, D.O., Merajver, S.D., et al. The Polycomb group protein EZH2 impairs DNA repair in breast epithelial cells. Neoplasia 7:11 (2005), 1011–1019.
38. [38] Watkins, J., Weekes, D., Shah, V., Gazinska, P., Joshi, S., Sidhu, B., et al. Genomic complexity profiling reveals that HORMAD1 overexpression contributes to homologous recombination deficiency in triple-negative breast cancers. Cancer Discov. 5:5 (2015), 488–505.
39. [39] Levy-Lahad, E., Lahad, A., Eisenberg, S., Dagan, E., Paperna, T., Kasinetz, L., et al. A single nucleotide polymorphism in the RAD51 gene modifies cancer risk in BRCA2 but not BRCA1 carriers. Proc. Natl. Acad. Sci. U. S. A. 98:6 (2001), 3232–3236.
40. [40] Silva, S.N., Tomar, M., Paulo, C., Gomes, B.C., Azevedo, A.P., Teixeira, V., et al. Breast cancer risk and common single nucleotide polymorphisms in homologous recombination DNA repair pathway genes XRCC2, XRCC3, NBS1 and RAD51. Cancer Epidemiol. 34:1 (2010), 85–92.
41. [41] Krupa, R., Synowiec, E., Pawlowska, E., Morawiec, Z., Sobczuk, A., Zadrozny, M., et al. Polymorphism of the homologous recombination repair genes RAD51 and XRCC3 in breast cancer. Exp. Mol. Pathol. 87:1 (2009), 32–35.
42. [42] Rafii, S., O'Regan, P., Xinarianos, G., Azmy, I., Stephenson, T., Reed, M., et al. A potential role for the XRCC2 R188H polymorphic site in DNA-damage repair and breast cancer. Hum. Mol. Genet. 11:12 (2002), 1433–1438.
43. [43] Smith, T.R., Miller, M.S., Lohman, K., Lange, E.M., Case, L.D., Mohrenweiser, H.W., et al. Polymorphisms of XRCC1 and XRCC3 genes and susceptibility to breast cancer. Cancer Lett. 190:2 (2003), 183–190.
44. [44] Smolarz, B., Makowska, M., Samulak, D., Michalska, M.M., Mojs, E., Wilczak, M., et al. Association between single nucleotide polymorphisms (SNPs) of XRCC2 and XRCC3 homologous recombination repair genes and triple-negative breast cancer in Polish women. Clin. Exp. Med. 15:2 (2015), 151–157.
45. [45] Michalska, M.M., Samulak, D., Romanowicz, H., Smolarz, B., Single nucleotide polymorphisms (SNPs) of RAD51-G172T and XRCC2-41657C/T homologous recombination repair genes and the risk of triple-negative breast cancer in Polish women. Pathol. Oncol. Res. 21:4 (2015), 935–940.
46. [46] Davis, A.J., Chen, D.J., DNA double strand break repair via non-homologous end-joining. Transl. Cancer Res., 2(3), 2013, 130.
47. [47] Bétermier, M., Bertrand, P., Lopez, B.S., Is non-homologous end-joining really an inherently error-prone process?. PLoS Genet., 10(1), 2014, e1004086.
48. [48] Woodbine, L., Gennery, A.R., Jeggo, P.A., The clinical impact of deficiency in DNA non-homologous end-joining. DNA Rep. 16 (2014), 84–96.
49. [49] Bau, D.-T., Mau, Y.-C., Ding, S.-L., Wu, P.-E., Shen, C.-Y., DNA double-strand break repair capacity and risk of breast cancer. Carcinogenesis 28:8 (2007), 1726–1730.
50. [50] Fu, Y.-P., Yu, J.-C., Cheng, T.-C., Lou, M.A., Hsu, G.-C., Wu, C.-Y., et al. Breast Cancer Risk Associated with Genotypic Polymorphism of the Nonhomologous End-Joining Genes A Multigenic Study on Cancer Susceptibility. Cancer Res. 63:10 (2003), 2440–2446.
51. [51] Kuschel, B., Auranen, A., McBride, S., Novik, K.L., Antoniou, A., Lipscombe, J.M., et al. Variants in DNA double-strand break repair genes and breast cancer susceptibility. Hum. Mol. Genet. 11:12 (2002), 1399–1407.
52. [52] Willems, P., Claes, K., Baeyens, A., Vandersickel, V., Werbrouck, J., De Ruyck, K., et al. Polymorphisms in nonhomologous end-joining genes associated with breast cancer risk and chromosomal radiosensitivity. Genes Chromosom. Cancer 47:2 (2008), 137–148.
53. [53] Chiu, C.-F., Wang, H.-C., Wang, C.-H., Wang, C.-L., Lin, C.-C., Shen, C.-Y., et al. A new single nucleotide polymorphism in XRCC4 gene is associated with breast cancer susceptibility in Taiwanese patients. Anticancer Res. 28:1A (2008), 267–270.
54. [54] Bau, D.-T., Fu, Y.-P., Chen, S.-T., Cheng, T.-C., Yu, J.-C., Wu, P.-E., et al. Breast cancer risk and the DNA double-strand break end-joining capacity of nonhomologous end-joining genes are affected by BRCA1. Cancer Res. 64:14 (2004), 5013–5019.
55. [55] Krokan, H.E., Bjørås, M., Base excision repair. Cold Spring Harb. Perspect. Biol., 5(4), 2013, a012583.
56. [56] Wallace, S.S., Base excision repair: a critical player in many games. DNA Rep. 19 (2014), 14–26.
57. [57] Dufloth, R.M., Costa, S., Schmitt, F., Zeferino, L.C., DNA repair gene polymorphisms and susceptibility to familial breast cancer in a group of patients from Campinas, Brazil. Genet. Mol. Res. 4:4 (2005), 771–782.
58. [58] Hsu, M.-S., Yu, J.-C., Wang, H.-W., Chen, S.-T., Hsiung, C.-N., Ding S-l, et al. Synergistic effects of polymorphisms in DNA repair genes and endogenous estrogen exposure on female breast cancer risk. Ann. Surg. Oncol. 17:3 (2010), 760–771.
59. [59] Majidinia, M., Yousefi, B., Long non-coding RNAs in cancer drug resistance development. DNA Rep. (Amst.) 45 (2016), 25–33.
60. [60] Sangrajrang, S., Schmezer, P., Burkholder, I., Waas, P., Boffetta, P., Brennan, P., et al. Polymorphisms in three base excision repair genes and breast cancer risk in Thai women. Breast Cancer Res. Treat. 111:2 (2008), 279–288.
61. [61] Chacko, P., Rajan, B., Joseph, T., Mathew, B.S., Pillai, M.R., Polymorphisms in DNA repair gene XRCC1 and increased genetic susceptibility to breast cancer. Breast Cancer Res. Treat. 89:1 (2005), 15–21.
62. [62] Smith, T.R., Levine, E.A., Perrier, N.D., Miller, M.S., Freimanis, R.I., Lohman, K., et al. DNA-repair genetic polymorphisms and breast cancer risk. Cancer Epidemiol. Biomark. Prev. 12:11 (2003), 1200–1204.
63. [63] Sigurdson, A.J., Hauptmann, M., Chatterjee, N., Alexander, B.H., Doody, M.M., Rutter, J.L., et al. Kin-cohort estimates for familial breast cancer risk in relation to variants in DNA base excision repair, BRCA1 interacting and growth factor genes. BMC Cancer, 4(1), 2004, 1.
64. [64] Duell, E.J., Millikan, R.C., Pittman, G.S., Winkel, S., Lunn, R.M., Chiu-Kit, J.T., et al. Polymorphisms in the DNA repair gene XRCC1 and breast cancer. Cancer Epidemiol. Biomark. Prev. 10:3 (2001), 217–222.
65. [65] Försti, A., Angelini, S., Festa, F., Sanyal, S., Zhang, Z., Grzybowska, E., et al. Single nucleotide polymorphisms in breast cancer. Oncol. Rep. 11:4 (2004), 917–922.
66. [66] Karimaian, A., Majidinia, M., Bannazadeh Baghi, H., Yousefi, B., The crosstalk between Wnt/β-catenin signaling pathway with DNA damage response and oxidative stress: implications in cancer therapy. DNA Rep. (Amst.) 51 (2017), 14–19.
67. [67] Shen, J., Gammon, M.D., Terry, M.B., Wang, L., Wang, Q., Zhang, F., et al. Polymorphisms in XRCC1 modify the association between polycyclic aromatic hydrocarbon-DNA adducts, cigarette smoking, dietary antioxidants, and breast cancer risk. Cancer Epidemiol. Biomark. Prev. 14:2 (2005), 336–342.
68. [68] Han, J., Hankinson, S.E., De Vivo, I., Spiegelman, D., Tamimi, R.M., Mohrenweiser, H.W., et al. A prospective study of XRCC1 haplotypes and their interaction with plasma carotenoids on breast cancer risk. Cancer Res. 63:23 (2003), 8536–8541.
69. [69] Marteijn, J.A., Lans, H., Vermeulen, W., Hoeijmakers, J.H., Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell Biol. 15:7 (2014), 465–481.
70. [70] Reardon, J.T., Sancar, A., Nucleotide excision repair. Prog. Nucl. Acid Res. Mol. Biol. 79 (2005), 183–235.
71. [71] Latimer, J.J., Johnson, J.M., Kelly, C.M., Miles, T.D., Beaudry-Rodgers, K.A., Lalanne, N.A., et al. Nucleotide excision repair deficiency is intrinsic in sporadic stage I breast cancer. Proc. Natl. Acad. Sci. U. S. A. 107:50 (2010), 21725–21730.
72. [72] Synowiec, E., Stefanska, J., Morawiec, Z., Blasiak, J., Wozniak, K., Association between DNA damage, DNA repair genes variability and clinical characteristics in breast cancer patients. Mutat. Res./Fundam. Mol. Mech. Mutagen. 648:1 (2008), 65–72.
73. [73] Justenhoven, C., Hamann, U., Pesch, B., Harth, V., Rabstein, S., Baisch, C., et al. ERCC2 genotypes and a corresponding haplotype are linked with breast cancer risk in a German population. Cancer Epidemiol. Biomark. Prev. 13:12 (2004), 2059–2064.
74. [74] Terry, M.B., Gammon, M.D., Zhang, F.F., Eng, S.M., Sagiv, S.K., Paykin, A.B., et al. Polymorphism in the DNA repair gene XPD, polycyclic aromatic hydrocarbon-DNA adducts, cigarette smoking, and breast cancer risk. Cancer Epidemiol. Biomark. Prev. 13:12 (2004), 2053–2058.
75. [75] Rajaraman, P., Bhatti, P., Doody, M.M., Simon, S.L., Weinstock, R.M., Linet, M.S., et al. Nucleotide excision repair polymorphisms may modify ionizing radiation-related breast cancer risk in US radiologic technologists. Int. J. Cancer 123:11 (2008), 2713–2716.
76. [76] Mechanic, L.E., Millikan, R.C., Player, J., de Cotret, A.R., Winkel, S., Worley, K., et al. Polymorphisms in nucleotide excision repair genes, smoking and breast cancer in African Americans and whites: a population-based case–control study. Carcinogenesis 27:7 (2006), 1377–1385.
77. [77] Badalzadeh, R., Mohammadi, M., Yousefi, B., Farajnia, S., Najafi, M., Mohammadi, S., Involvement of glycogen synthase kinase-3β and oxidation status in the loss of cardioprotection by postconditioning in chronic diabetic male rats. Adv. Pharm. Bull. 5:3 (2015), 321–327.
78. [78] Wang, H., Wang, T., Guo, H., Zhu, G., Yang, S., Hu, Q., et al. Association analysis of ERCC5 gene polymorphisms with risk of breast cancer in Han women of northwest China. Breast Cancer 23:3 (2016), 479–485.
79. [79] Dietlein, F., Thelen, L., Reinhardt, H.C., Cancer-specific defects in DNA repair pathways as targets for personalized therapeutic approaches. Trends Genet. 30:8 (2014), 326–339.
80. [80] Modrich, P., Mismatch repair, genetic stability and cancer. Science, 266(5193), 1994, 1959.
81. [81] Murata, H., Khattar, N.H., Gu, L., Li, G.-M., Roles of mismatch repair proteins hMSH2 and hMLH1 in the development of sporadic breast cancer. Cancer Lett. 223:1 (2005), 143–150.
82. [82] Ford, B.N., Ruttan, C.C., Kyle, V.L., Brackley, M.E., Glickman, B.W., Identification of single nucleotide polymorphisms in human DNA repair genes. Carcinogenesis 21:11 (2000), 1977–1981.
83. [83] Hoeijmakers, J.H., Genome maintenance mechanisms for preventing cancer. Nature 411:6835 (2001), 366–374.
84. [84] Moinfar, F., Beham, A., Friedrich, G., Deutsch, A., Hrzenjak, A., Luschin, G., et al. Macro-environment of breast carcinoma: frequent genetic alterations in the normal appearing skins of patients with breast cancer. Modern Pathol. 21:5 (2008), 639–646.
85. [85] Benachenhou, N., Guiral, S., Gorska-Flipot, I., Labuda, D., Sinnett, D., Frequent loss of heterozygosity at the DNA mismatch-repair loci hMLH1 and hMSH3 in sporadic breast cancer. Br. J. Cancer, 79(7–8), 1999, 1012.
86. [86] Majidinia, M., Yousefi, B., DNA damage response regulation by microRNAs as a therapeutic target in cancer. DNA Rep., 2016.
87. [87] Falck, J., Coates, J., Jackson, S.P., Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:7033 (2005), 605–611.
88. [88] Zhou B-BS, Elledge, S.J., The DNA damage response: putting checkpoints in perspective. Nature 408:6811 (2000), 433–439.
89. [89] Yousefi, B., Rahmati, M., Ahmadi, Y., The roles of p53R2 in cancer progression based on the new function of mutant p53 and cytoplasmic p21. Life Sci. 99:1 (2014), 14–17.
90. [90] Green, L.J., Lin, S.-Y., DNA Damage Response and Breast Cancer: An Overview. 2012, INTECH Open Access Publisher.
91. [91] Guo, X., Yang, C., Qian, X., Lei, T., Li, Y., Shen, H., et al. Estrogen receptor α regulates ATM expression through miRNAs in breast cancer. Clin. Cancer Res. 19:18 (2013), 4994–5002.
92. [92] Song, L., Lin, C., Wu, Z., Gong, H., Zeng, Y., Wu, J., et al. miR-18a impairs DNA damage response through downregulation of ataxia telangiectasia mutated (ATM) kinase. PLoS ONE., 6(9), 2011, e25454.
93. [93] Tommiska, J., Bartkova, J., Heinonen, M., Hautala, L., Kilpivaara, O., Eerola, H., et al. The DNA damage signalling kinase ATM is aberrantly reduced or lost in BRCA1/BRCA2-deficient and ER/PR/ERBB2-triple-negative breast cancer. Oncogene 27:17 (2008), 2501–2506.
94. [94] Pedram, A., Razandi, M., Evinger, A.J., Lee, E., Levin, E.R., Estrogen inhibits ATR signaling to cell cycle checkpoints and DNA repair. Mol. Biol. Cell 20:14 (2009), 3374–3389.
95. [95] Kim, H.J., Min, A., Im, S.A., Jang, H., Lee, K.H., Lau, A., et al. Anti-tumor activity of the ATR inhibitor AZD6738 in HER2 positive breast cancer cells. Int. J. Cancer 140:1 (2017), 109–119.
96. [96] Medunjanin, S., Weinert, S., Schmeisser, A., Mayer, D., Braun-Dullaeus, R.C., Interaction of the double-strand break repair kinase DNA-PK and estrogen receptor-α. Mol. Biol. Cell 21:9 (2010), 1620–1628.
97. [97] Barba, M., Vici, P., Pizzuti, L., Di Lauro, L., Sergi, D., Di Benedetto, A., et al. Body mass index modifies the relationship between γ-H2AX, a DNA damage biomarker, and pathological complete response in triple-negative breast cancer. BMC Cancer, 17(1), 2017, 101.
98. [98] Partipilo, G., Simone, G., Scattone, A., Scarpi, E., Azzariti, A., Mangia, A., Expression of proteins involved in DNA damage response in familial and sporadic breast cancer patients. Int. J. Cancer 138:1 (2016), 110–120.
99. [99] Nolan, E., Vaillant, F., Branstetter, D., Pal, B., Giner, G., Whitehead, L., et al. RANK ligand as a potential target for breast cancer prevention in BRCA1-mutation carriers. Nat. Med. 22:8 (2016), 933–939.
100. [100] Aleskandarany, M., Caracappa, D., Nolan, C.C., Macmillan, R.D., Ellis, I.O., Rakha, E.A., et al. DNA damage response markers are differentially expressed in BRCA-mutated breast cancers. Breast Cancer Res. Treat. 150:1 (2015), 81–90.
101. [101] Jeffy, B.D., Hockings, J.K., Kemp, M.Q., Morgan, S.S., Hager, J.A., Beliakoff, J., et al. An estrogen receptor-α/p300 complex activates the BRCA-1 promoter at an AP-1 site that binds Jun/Fos transcription factors: repressive effects of p53 on BRCA-1 transcription. Neoplasia 7:9 (2005), 873–882.
102. [102] Yousefi, B., Darabi, M., Baradaran, B., Shekari Khaniani, M., Rahbani, M., Darabi, M., et al. Inhibition of MEK/ERK1/2 signaling affects the fatty acid composition of HepG2 human hepatic cell line. Bioimpacts 2:3 (2012), 145–150.
103. [103] Mansoori, B., Mohammadi, A., Goldar, S., Shanehbandi, D., Mohammadnejad, L., Baghbani, E., Kazemi, T., Kachalaki, S., Baradaran, B., Silencing of high mobility group isoform I-C (HMGI-C) enhances paclitaxel chemosensitivity in breast adenocarcinoma cells (MDA-MB-468). Adv. Pharm. Bull. 6:2 (2016), 171–177.
104. [104] Egawa, C., Miyoshi, Y., Taguchi, T., Tamaki, Y., Noguchi, S., Quantitative analysis of BRCA1 and BRCA2 mRNA expression in sporadic breast carcinomas and its relationship with clinicopathological characteristics. Jpn. J. Cancer Res. 92:6 (2001), 624–630.
105. [105] Yousefi, B., Samadi, N., Ahmadi, Y., Akt and p53R2, partners that dictate the progression and invasiveness of cancer. DNA Rep. 22 (2014), 24–29.
106. [106] Cybulski, C., Huzarski, T., Byrski, T., Gronwald, J., Dębniak, T., Jakubowska, A., et al. Estrogen receptor status in CHEK2-positive breast cancers: implications for chemoprevention. Clin. Genet. 75:1 (2009), 72–78.
107. [107] Weischer, M., Nordestgaard, B.G., Pharoah, P., Bolla, M.K., Nevanlinna, H., Van't Veer, L.J., et al. CHEK2* 1100delC heterozygosity in women with breast cancer associated with early death, breast cancer–specific death, and increased risk of a second breast cancer. J. Clin. Oncol. 30:35 (2012), 4308–4316.
108. [108] Alexander, A., Karakas, C., Chen, X., Carey, J.P., Yi, M., Bondy, M., et al. Cyclin E overexpression as a biomarker for combination treatment strategies in inflammatory breast cancer. Oncotarget, 2017.
109. [109] He, X., Zheng, Z., Song, T., Wei, C., Ma, H., Ma, Q., et al. c-Abl regulates estrogen receptor α transcription activity through its stabilization by phosphorylation. Oncogene 29:15 (2010), 2238–2251.
110. [110] Zhao, H., Ou-Yang, F., Chen, I.-F., Hou, M.-F., Yuan S-SF, Chang, H.-L., et al. Enhanced resistance to tamoxifen by the c-ABL proto-oncogene in breast cancer. Neoplasia 12:3 (2010), 214–223.
111. [111] van der Groep, P., Hoelzel, M., Buerger, H., Joenje, H., de Winter, J.P., van Diest, P.J., Loss of expression of FANCD2 protein in sporadic and hereditary breast cancer. Breast Cancer Res. Treat. 107:1 (2008), 41–47.
112. [112] Saji, S., Okumura, N., Eguchi, H., Nakashima, S., Suzuki, A., Toi, M., et al. MDM2 enhances the function of estrogen receptor α in human breast cancer cells. Biochem. Biophys. Res. Commun. 281:1 (2001), 259–265.
113. [113] Brekman, A., Singh, K.E., Polotskaia, A., Kundu, N., Bargonetti, J., A p53-independent role of Mdm2 in estrogen-mediated activation of breast cancer cell proliferation. Breast Cancer Res., 13(1), 2011, 1.
114. [114] Duong, V., Boulle, N., Daujat, S., Chauvet, J., Bonnet, S., Neel, H., et al. Differential regulation of estrogen receptor α turnover and transactivation by Mdm2 and stress-inducing agents. Cancer Res. 67:11 (2007), 5513–5521.
115. [115] Rahmati-Yamchi, M., Zarghami, N., Nozad Charoudeh, H., Ahmadi, Y., Baradaran, B., Khalaj-Kondori, M., Milani, M., Akbarzadeh, A., Shaker, M., Pourhassan-Moghaddam, M., Clofarabine has apoptotic effect on T47D breast cancer cell line via P53R2 gene expression. Adv. Pharm. Bull. 5:4 (2015), 471–476.
116. [116] Maeda, T., Nakanishi, Y., Hirotani, Y., Fuchinoue, F., Enomoto, K., Sakurai, K., et al. Immunohistochemical co-expression status of cytokeratin 5/6, androgen receptor, and p53 as prognostic factors of adjuvant chemotherapy for triple negative breast cancer. Med. Mol. Morphol. 49:1 (2016), 11–21.
117. [117] Miller, L.D., Smeds, J., George, J., Vega, V.B., Vergara, L., Ploner, A., et al. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc. Natl. Acad. Sci. U. S. A. 102:38 (2005), 13550–13555.
118. [118] Lewandowski, S.A., Thiery, J., Jalil, A., Leclercq, G., Szczylik, C., Chouaib, S., Opposite effects of estrogen receptors alpha and beta on MCF-7 sensitivity to the cytotoxic action of TNF and p53 activity. Oncogene 24:30 (2005), 4789–4798.
119. [119] Hurd, C., Khattree, N., Alban, P., Nag, K., Jhanwar, S.C., Dinda, S., et al. Hormonal regulation of the p53 tumor suppressor protein in T47D human breast carcinoma cell line. J. Biol. Chem. 270:48 (1995), 28507–28510.
120. [120] Hurd, C., Khattree, N., Dinda, S., Alban, P., Moudgil, V., Regulation of tumor suppressor proteins, p53 and retinoblastoma, by estrogen and antiestrogens in breast cancer cells. Oncogene, 15(8), 1997.
121. [121] Okumura, N., Saji, S., Eguchi, H., Hayashi Si, Saji, S., Nakashima, S., Estradiol stabilizes p53 protein in breast cancer cell line, MCF-7. Jpn. J. Cancer Res. 93:8 (2002), 867–873.
122. [122] Konduri, S.D., Medisetty, R., Liu, W., Kaipparettu, B.A., Srivastava, P., Brauch, H., et al. Mechanisms of estrogen receptor antagonism toward p53 and its implications in breast cancer therapeutic response and stem cell regulation. Proc. Natl. Acad. Sci. U. S. A. 107:34 (2010), 15081–15086.
123. [123] Bailey, S.T., Shin, H., Westerling, T., Liu, X.S., Brown, M., Estrogen receptor prevents p53-dependent apoptosis in breast cancer. Proc. Natl. Acad. Sci. U. S. A. 109:44 (2012), 18060–18065.
124. [124] Shirley, S.H., Rundhaug, J.E., Tian, J., Cullinan-Ammann, N., Lambertz, I., Conti, C.J., et al. Transcriptional regulation of estrogen receptor-α by p53 in human breast cancer cells. Cancer Res. 69:8 (2009), 3405–3414.
125. [125] Schultz-Norton, J.R., Gabisi, V.A., Ziegler, Y.S., McLeod, I.X., Yates, J.R., Nardulli, A.M., Interaction of estrogen receptor α with proliferating cell nuclear antigen. Nucl. Acids Res. 35:15 (2007), 5028–5038.
126. [126] Kataoka, A., Sadanaga, N., Mimori, K., Ueo, H., Barnard, G.F., Sugimachi, K., et al. Overexpression of HRad17 mRNA in human breast cancer: correlation with lymph node metastasis. Clin. Cancer Res. 7:9 (2001), 2815–2820.
127. [127] Rakha, E.A., Reis-Filho, J.S., Ellis, I.O., Basal-like breast cancer: a critical review. J. Clin. Oncol. 26:15 (2008), 2568–2581.
128. [128] Bertoli, G., Cava, C., Castiglioni, I., MicroRNAs: new biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast cancer. Theranostics, 5(10), 2015, 1122.
129. [129] Khongkow, P., Gomes, A., Gong, C., Man, E., Tsang, J.W., Zhao, F., et al. Paclitaxel targets FOXM1 to regulate KIF20A in mitotic catastrophe and breast cancer paclitaxel resistance. Oncogene 35:8 (2016), 990–1002.
130. [130] Karunarathna, U., Kongsema, M., Zona, S., Gong, C., Cabrera, E., Gomes, A., et al. OTUB1 inhibits the ubiquitination and degradation of FOXM1 in breast cancer and epirubicin resistance. Oncogene 35:11 (2016), 1433–1444.
131. [131] Asakawa, H., Koizumi, H., Koike, A., Takahashi, M., Wu, W., Iwase, H., et al. Prediction of breast cancer sensitivity to neoadjuvant chemotherapy based on status of DNA damage repair proteins. Breast Cancer Res., 12(2), 2010, 1.