RAD51 mediates resistance of cancer stem cells to PARP inhibition in triple-negative breast cancer

Clinical Cancer Research

Volumn 23, Issue 2, 2017, Pages 514-522

  Liu, Yajing ^a   Burness, Monika L ^a   Martin Trevino, Rachel ^a   Guy, Joey ^a   Bai, Shoumin ^b   Harouaka, Ramdane ^a   Brooks, Michael D ^a   Shang, Li ^a   Fox, Alex ^a   Luther, Tahra K ^a   Davis, April ^a   Baker, Trenton L ^a   Colacino, Justin ^a   Clouthier, Shawn G ^a   Shao, Zhi Ming ^c,d   Wicha, Max S ^a   Liu, Suling ^e  

^a UNIVERSITY OF MICHIGAN   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^d FUDAN UNIVERSITY   (China)

^e UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RAD51 PROTEIN; SHORT HAIRPIN RNA; BRCA1 PROTEIN; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARP1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER CELL LINE; CANCER INHIBITION; CANCER RESISTANCE; CANCER STEM CELL; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; FEMALE; GENE CONTROL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; TRIPLE NEGATIVE BREAST CANCER; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METASTASIS; PATHOLOGY; TUMOR CELL LINE; TUMOR RECURRENCE;

ANIMALS; BRCA1 PROTEIN; BRCA2 PROTEIN; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NEOPLASM METASTASIS; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; POLY (ADP-RIBOSE) POLYMERASE-1; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; RAD51 RECOMBINASE; TRIPLE NEGATIVE BREAST NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85010991016     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1348     Document Type: Article

References (35)

1. Mayer IA, Abramson VG, Lehmann BD, Pietenpol JA. New strategies for triple-negative breast cancer-deciphering the heterogeneity. Clin Cancer Res 2014;20:782-90.
2. 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.
3. 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.
4. Kortmann U, McAlpine JN, Xue H, Guan J, Ha G, Tully S, et al. Tumor growth inhibition by olaparib in BRCA2 germline-mutated patient-derived ovarian cancer tissue xenografts. Clin Cancer Res 2011;17:783-91.
5. Menear KA, Adcock C, Boulter R, Cockcroft XL, Copsey L, Cranston A, et al. 4-[3-(4-cyclopropanecarbonylpiperazine-1-carbonyl)-4-fluorobenzyl]-2H-phthalazin- 1-one: A novel bioavailable inhibitor of poly(ADP-ribose) polymerase-1. J Med Chem 2008;51:6581-91.
6. Evers B, Drost R, Schut E, de Bruin M, van der Burg E, Derksen PW, et al. Selective inhibition of BRCA2-deficient mammary tumor cell growth by AZD2281 and cisplatin. Clin Cancer Res 2008;14:3916-25.
7. Rottenberg S, Jaspers JE, Kersbergen A, van der Burg E, Nygren AO, Zander SA, 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 U S A 2008;105:17079-84.
8. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, 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;376:245-51.
9. Tutt A, Robson M, Garber JE, Domchek SM, Audeh MW, Weitzel JN, 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;376:235-44.
10. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009;69:1302-13.
11. Raderschall E, Stout K, Freier S, Suckow V, Schweiger S, Haaf T. Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res 2002;62:219-25.
12. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006;66:7843-8.
13. Mathews LA, Cabarcas SM, Hurt EM, Zhang X, Jaffee EM, Farrar WL. Increased expression of DNA repair genes in invasive human pancreatic cancer cells. Pancreas 2011;40:730-9.
14. Karimi-Busheri F, Rasouli-Nia A, Mackey JR, Weinfeld M. Senescence evasion by MCF-7 human breast tumor-initiating cells. Breast Cancer Res 2010;12:R31.
15. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-67.
16. Hu Y, Smyth G. ELDA: Extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 2009;347:70-8.
17. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009;361:123-34.
18. Sy SM, Huen MS, Chen J. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci U S A 2009;106:7155-60.
19. Yuan SSF, Lee SY, Chen G, Song MH, Tomlinson GE, Lee EYHP. BRCA2 is required for ionizing radiation-induced assembly of rad51 complex in vivo. Cancer Res 1999;59:3547-51.
20. 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;275:23899-903.
21. Deng L, Shang L, Bai S, Chen J, He X, Martin-Trevino R, et al. MicroRNA100 inhibits self-renewal of breast cancer stem-like cells and breast tumor development. Cancer Res 2014;74:6648-60.
22. Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011;8:511-24.
23. Elstrodt F, Hollestelle A, Nagel JH, Gorin M, Wasielewski M, van den Ouweland A, et al. BRCA1 mutation analysis of 41 human breast cancer cell lines reveals three new deleterious mutants. Cancer Res 2006;66:41-5.
24. Gilabert M, Launay S, Ginestier C, Bertucci F, Audebert S, Pophillat M, et al. Poly(ADP-Ribose) polymerase 1 (PARP1) overexpression in human breast cancer stem cells and resistance to olaparib. PLoS One 2014;9:e104302.
25. Martin RW, Orelli BJ, Yamazoe M, Minn AJ, Takeda S, Bishop DK. RAD51 up-regulation bypasses BRCA1 function and is a common feature of BRCA1-deficient breast tumors. Cancer Res 2007;67:9658-65.
26. Johnson N, Johnson SF, Yao W, Li YC, Choi YE, Bernhardy AJ, et al. Stabilization of mutant BRCA1 protein confers PARP inhibitor and platinum resistance. Proc Natl Acad Sci U S A 2013;110:17041-6.
27. Tichy ED, Pillai R, Deng L, Tischfield JA, Hexley P, Babcock GF, et al. The abundance of Rad51 protein in mouse embryonic stem cells is regulated at multiple levels. Stem Cell Res 2012;9:124-34.
28. Maynard S, Swistowska AM, Lee JW, Liu Y, Liu ST, Da Cruz AB, et al. Human embryonic stem cells have enhanced repair of multiple forms of DNA damage. Stem Cells 2008;26:2266-74.
29. Al-Assar O, Mantoni T, Lunardi S, Kingham G, Helleday T, Brunner TB. Breast cancer stem-like cells show dominant homologous recombination due to a larger S-G2 fraction. Cancer Biol Ther 2011;11:1028-35.
30. Su YJ, Tsai MS, Kuo YH, Chiu YF, Cheng CM, Lin ST, et al. Role of Rad51 down-regulation and extracellular signal-regulated kinases 1 and 2 inactivation in emodin and mitomycin C-induced synergistic cytotoxicity in human non-small-cell lung cancer cells. Mol Pharmacol 2010;77:633-43.
31. Bindra RS, Schaffer PJ, Meng A, Woo J, Maseide K, Roth ME, et al. Downregulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 2004;24:8504-18.
32. Wang Y, Huang JW, Calses P, Kemp CJ, Taniguchi T. MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition. Cancer Res 2012;72:4037-46.
33. Bianchi-Smiraglia A, Paesante S, Bakin AV. Integrin beta5 contributes to the tumorigenic potential of breast cancer cells through the Src-FAK and MEK-ERK signaling pathways. Oncogene 2012;32:3049-58.
34. Lin H, Dai T, Xiong H, Zhao X, Chen X, Yu C, et al. Unregulated miR-96 induces cell proliferation in human breast cancer by downregulating transcriptional factor FOXO3a. PLoS ONE 2010;5:e15797.
35. Chang CJ, Yang JY, Xia W, Chen CT, Xie X, Chao CH, et al. EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-betacatenin signaling. Cancer Cell 2011;19:86-100.