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News in the studies of multidrug resistance of breast cancer cells

https://doi.org/10.17650/2313-805X.2015.2.1.039-051

Abstract

Breast cancer (BC) is the most common cancer among women in Russia. One of the main treatment methods of BC is systemic chemotherapy. Multidrug resistance of tumor cells (MDR) is the important hindrance on the way to successful chemotherapy. The new data concerning molecular mechanisms of MDR will be presented in this review. The recent data concerning some new biological prognostic markers will be also discussed. There are data showing that transporters of ABC family (ABC transporters) influence tumor progression not only by MDR induction but also by the influence on the traits of malignancy in tumor cells. The results of the studies of ABC transporters, participation in the processes of accumulation of tumor stem cells under the influence of chemotherapy will be discussed. The problem of the participation of ABC transporters in the phenomenon of influence of PI3K/AKT/PTEN signal transduction pathway on the MDR regulation is discussed. The results of the studies of the role of microRNA deregulation in breast cancer drug resistance as well as studies of some epigenetic mechanisms of MDR regulation will be considered. Protein phosphatase 2A (PP2A, serine/threonine phosphatase), PTK7 (protein tyrosine kinase 7). fascin (an actin bundling cytoskeletal protein) multifunctional YB-1 protein will considered as new BC prognostic markers. The perspectives of MDR studies will be discussed as well.

About the Authors

A. A. Stavrovskaya
N.N. Blokhin Russian Cancer Research Center
Russian Federation
24 Kashirskoye Highway, Moscow, 115478, Russia


G. P. Guens
A. I. Evdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia
Russian Federation
Department of Oncology and Radiology, 20 Bldg. 1 Delegatskaya St., Moscow, 127473, Russia


References

1. Ставровская А.А. Клеточные механизмы множественной лекарственной устойчивости опухолевых клеток (обзор). Биохимия 2000;65(1):112–26. [Stavrovskaya A.A. Cellular mechanisms of multiple drug resistance of malignant cells (review). Biokhimiya = Biochemistry 2000;65(1):112–26. (In Russ.)].

2. Ставровская А.А., Генс Г.П. Некоторые новые аспекты исследований множественной лекарственной устойчивости опухолевых клеток. Успехи молекулярной онкологии 2014;(1):5–11. [Stavrovskaya A.A., Guens G.P. Multidrug resistance of tumor cells: some new trends in research. Uspekhi molekulyarnoy onkologii = Advances in Molecular Oncology 2014;(1):5–11. (In Russ.)].

3. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP dependent transporters. Nat Rev Cancer 2002;2(1):48–58.

4. Dean M. ABC transporters, drug resistance, and cancer stem cells. J Mammary Gland Biol Neoplasia 2009;14(1):3–9.

5. Shen D.W., Goldenberg S., Pastan I., Gottesman M.M. Decreased accumulation of [14C] carboplatin in human cisplatin-resistant cells results from reduced energy-dependent uptake. J Cell Physiol 2000;183(1):108–16.

6. McDonnell A.M., Dang C.H. Basic review of the cytochrome p450 system. J Adv Pract Oncol 2013;4(4):263–8.

7. Salehan M.R., Morse H.R. DNA damage repair and tolerance: a role in chemotherapeutic drug resistance. Br J Biomed Sci 2013;70(1):31–40.

8. Lowe S.W., Ruley H.E., Jacks T., Housman D.E. p53-Dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993;74(6):957–67.

9. Davis N.M., Sokolosky M., Stadelman K. et al. Deregulation of the EGFR/PI3K/PTEN/Akt/mTORC1 pathway in breast cancer: possibilities for therapeutic intervention. Oncotarget 2014;5(13):4603–50.

10. Mulrane L., McGee S.F., Gallagher W.M., O,Connor D.P. miRNA dysregulation in breast cancer. Cancer Res 2013;73(22):6554–62.

11. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011;144(5):646–74.

12. Szakács G., Paterson J.K., Ludwig J.A. et al. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006;5(3):219–34.

13. Wind N.S., Holen I. Multidrug resistance in breast cancer: from in vitro models to clinical studies. Int J Breast Cancer 2011;2011:967419.

14. Chen Z.S., Tiwari A.K. Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J 2011;278(18):3226–45.

15. Hopper-Borge E., Chen Z.S., Shchaveleva I. et al. Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 2004;64(14):4927–30.

16. Kruh G.D., Guo Y., Hopper-Borge E. et al. ABCC10, ABCC11, and ABCC12. Pflugers Arch 2007;453(5):675–84.

17. Bera T.K., Iavarone C., Kumar V. et al. MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc Natl Acad Sci USA 2002;99(10):6997–7002.

18. Mao Q., Unadkat J.D. Role of the breast cancer resistance protein(ABCG2) in drug transport. AAPS J 2005;7(1):E118–33.

19. Jani M., Ambrus C., Magnan R. et al. Structure and function of BCRP, a broad specificity transporter of xenobiotics and endobiotics. Arch Toxicol 2014;88(6): 1205–48.

20. Noguchi K., Katayama K., Sugimoto Y. Human ABC transporter ABCG2/BCRP expression in chemoresistance: basic and clinical perspectives for molecular cancer therapeutics. Pharmgenomics Pers Med 2014;7:53–64.

21. Shukla S., Ohnuma S., Ambudkar S.V. Improving cancer chemotherapy with modulators of ABC drug transporters. Curr Drug Targets 2011;12(5):621–30.

22. Sosnik A. Reversal of multidrug resistance by the inhibition of ATP-binding cassette pumps employing “Generally Recognized As Safe” (GRAS) nanopharmaceuticals: A review. Adv Drug Deliv Rev 2013;65(13–14):1828–51.

23. Cheung L., Flemming C.L., Watt F. et al. High-throughput screening identifies Ceefourin 1 and Ceefourin 2 as highly selective inhibitors of multidrug resistance protein 4 (MRP4). Biochem Pharmacol 2014;91(1):97–108.

24. Schinkel A.H., Jonker J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 2003;55(1):3–29.

25. Kathawala R. J., Wang Y. J., Ashby C.R. Jr, Chen Z.S. Recent advances regarding the role of ABC subfamily C member 10 (ABCC10) in the efflux of antitumor drugs. Chin J Cancer 2014;33(5):223–30.

26. Honorat M., Mesnier A., Vendrell J. et al. ABCC11 expression is regulated by estrogen in MCF7 cells, correlated with estrogen receptor alpha expression in postmenopausal breast tumors and overexpressed in tamoxifen-resistant breast cancer cells. Endocr Relat Cancer 2008;15(1):125–38.

27. Sodani K., Patel A., Kathawala R. J., Chen Z.S. Multidrug resistance associated proteins in multidrug resistance. Chin J Cancer 2012;31(2):58–72.

28. Tsuruo T., Iida H., Tsukagoshi S., Sakurai Y. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res 1981;41(5):1967–72.

29. Slater L.M., Sweet P., Stupecky M., Gupta S. Cyclosporin A reverses vincristine and daunorubicin resistance in acute lymphatic leukemia in vitro. J Clin Invest 1986;77(4):1405–8.

30. Cornwell M.M., Pastan I., Gottesman M.M. Certain calcium channel blockers bind specifically to multidrug-resistant human KB carcinoma membrane vesicles and inhibit drug binding to P-glycoprotein. J Biol Chem 1987;262(5):2166–70.

31. Goldberg H., Ling V., Wong P.Y., Skorecki K. Reduced cyclosporin accumulation in multidrug-resistant cells. Biochem Biophys Res Commun 1988;152(2):552–8.

32. Falasca M., Linton K. J. Investigational ABC transporter inhibitors. Expert Opin Investig Drugs 2012;21(5):657–66.

33. Pusztai L., Wagner P., Ibrahim N. et al. Phase II study of tariquidar, a selective P-glycoprotein inhibitor, in patients with chemotherapy-resistant, advanced breast carcinoma. Cancer 2005;104(4):682–91.

34. Annereau J.P., Szakács G., Tucker C. J. et al. Analysis of ATP-binding cassette transporter expression in drug-selected cell lines by a microarray dedicated to multidrug resistance. Mol Pharmacol 2004;66(6):1397–405.

35. Szakács G., Annereau J.P., Lababidi S. et al. Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells. Cancer Cell 2004;6(2):129–37.

36. Gillet J.P., Efferth T., Steinbach D. et al. Microarray-based detection of multidrug resistance in human tumor cells by expression profiling of ATP-binding cassette transporter genes. Cancer Res 2004;64(24):8987–93.

37. Fletcher J.I., Haber M., Henderson M. J., Norris M.D. ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 2010;10(2):147–56.

38. Piñeiro R., Maffucci T., Falasca M. The putative cannabinoid receptor GPR55 defines a novel autocrine loop in cancer cell proliferation. Oncogene 2011;30(2):142–52.

39. Reid G., Wielinga P., Zelcer N. et al. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Natl Acad Sci USA 2003;100(16):9244–9.

40. Leier I., Jedlitschky G., Buchholz U. et al. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 1994;269(45):27807–10.

41. Peaston A.E., Gardaneh M., Franco A.V.et al. MRP1 gene expression level regulates the death and differentiation response of neuroblastoma cells. Br J Cancer 2001;85(10):1564–71.

42. Robbiani D.F., Finch R.A., Jäger D. et al. The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC) – dependent mobilization of dendritic cells to lymph nodes. Cell 2000;103(5):757–68.

43. Randolph G. J., Beaulieu S., Pope M. et al. A physiologic function for p-glycoprotein (MDR-1) during the migration of dendritic cells from skin via afferent lymphatic vessels. Proc Natl Acad Sci USA 1998;95(12):6924–9.

44. Miletti-González K.E., Chen S., Muthukumaran N. et al. The CD44 receptor interacts with P-glycoprotein to promote cell migration and invasion in cancer. Cancer Res 2005;65(15):6660–7.

45. Colone M., Calcabrini A., Toccacieli L. et al. The multidrug transporter P-glycoprotein: a mediator of melanoma invasion? J Invest Dermatol 2008;128(4):957–71.

46. Barakat S., Turcotte S., Demeule M. et al. Regulation of brain endothelial cells migration and angiogenesis by P-glycoprotein/ caveolin-1 interaction. Biochem Biophys Res Commun 2008;372(3):440–6.

47. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997;3(7):730–7.

48. Moitra K., Lou H., Dean M. Multidrug efflux pumps and cancer stem cells: insights into multidrug resistance and therapeutic development. Clin Pharmacol Ther 2011;89(4):491–502.

49. Barbet R., Peiffer I., Hutchins J.R. et al. Expression of the 49 human ATP binding cassette (ABC) genes in pluripotent embryonic stem cells and in early- and late-stage multipotent mesenchymal stem cells: possible role of ABC plasma membrane transporters in maintaining human stem cell pluripotency. Cell Cycle 2012;11(8):1611–20.

50. Patrawala L., Calhoun T., Schneider-Broussard R. et al. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2– cancer cells are similarly tumorigenic. Cancer Res 2005;65(4):6207–19.

51. Al-Hajj M., Wicha M.S., Benito-Hernandez А. et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100(7):3983–8.

52. Li X., Lewis M.T., Huang J. et al. Intrinsic resistance of tumorigenic breast cantherapeutic intervention. Oncotarget 2014;5(13):4603–50.

53. Park S., Shimizu C., Shimoyama T. et al. Gene expression profiling of ATP-binding cassette(ABC) transporters as a predictor of the pathologic response to neoadjuvant chemotherapy in breast cancer patients. Breast Cancer Res Treat 2006;99(1):9–17.

54. Calcagno A.M., Salcido C.D., Gillet J. et al. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. J Natl Cancer Inst 2010;102(21):1637–52.

55. Стромская Т.П., Рыбалкина Е.Ю., Круглов С.С. и др. Участие Р-гликопротеина в эволюции популяций клеток хронического миелолейкоза при воздействии иматиниба. Биохимия 2008;73(1):36–46. [Stromskaya T.P., Rybalkina E.Yu., Kruglov S.S. et al. Participation of Р-glycoprotein in evolution of chronic myelogenous leukemia cell pool under action of Imatinibа. Biokhimiya = Biochemistry 2008;73(1):36–46. (In Russ.)].

56. Guille A., Chaffanet M., Birnbaum D. Signaling pathway switch in breast cancer. Cancer Cell Int 2013;13(1):66.

57. Koboldt D.C., Fulton R.S., McLellan M. D. et al. Comprehensive molecular portraits of human breast tumours. Nature 2012;490(7418):61–70.

58. Shah S.P., Roth A., Goya R. et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012;486(7403):395–9.

59. Banerji S., Cibulskis K., Rangel-Escareno K. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 2012;486(7403):405–9.

60. Ellis M. J., Ding L., Shen D. et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 2012;486(7403):353–60.

61. VanderWeele D. J., Zhou R., Rudin C.M. Akt up-regulation increases resistance to microtubule-directed chemotherapeutic agents through mammalian target of rapamycin. Mol Cancer Ther 2004;3(12):1605–13.

62. Щербакова Е.А., Стромская Т.П., Рыбалкина Е.Ю., Ставровская А.А. Влияние повышения активности опухолевого супрессора PTEN на чувствительность малигнизированных клеток к химиотерапевтическим препаратам. Биологические мембраны 2007;24(2):143–50. [Shcherbakova E.A., Stromskaya T.P., Rybalkina E.Yu., Stavrovskaya A.A. Effect of increase in activity of tumour suppressor PTEN for sensibility of malignant cells to the chemotherapy drugs. Biologicheskie membrany = Biological Membranes 2007;24(2):143–50. (In Russ.)].

63. Burris H.A. 3rd. Overcoming acquired resistance to anticancer therapy: focus on the PI3K/AKT/mTOR pathway. Cancer Chemother Pharmacol 2013; 71(4):829–42.

64. McCubrey J. A., Steelman L.S., Chappell W.H. et al. Mutations and deregulation of Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascades which alter therapy response. Oncotarget 2012;3(9):954–87.

65. Knuefermann C., Lu Y., Liu B. et al. HER-2/PI-3K/Akt activation leads to a multidrug resistance in human breast adenocarcinoma cells. Oncogene 2003;22(21):3205–12.

66. Ma H., Cheng L., Hao K. et al. Reversal effect of ST6GAL 1 on multidrug resistance in human leukemia by regulating the PI3K/Akt pathway and the expression of P-gp and MRP1. PLoS One 2014;9(1):e85113.

67. Cidado J., Park B.H. Targeting the PI3K/Akt/mTOR pathway for breast cancer therapy. J Mammary Gland Biol Neoplasia 2012;17(3–4):205–16.

68. Lauring J., Park B.H., Wolff A.C. The phosphoinositide-3–kinase-Akt-mTOR pathway as a therapeutic target in breast cancer. J Natl Compr Canc Netw 2013;11(6):670–8.

69. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001;294(5543):862–4.

70. Melo S.A., Esteller M. Dysregulation of microRNAs in cancer: playing with fire. FEBS Lett 2011;585(13):2087–99.

71. Martin H.L., Smith L., Tomlinson D.C. Multidrug-resistant breast cancer: current perspectives. Breast Cancer (Dove Med Press) 2014;6:1–13.

72. Agarwal S., Hanna J., Sherman M.E. et al. Quantitative assessment of miR34a as an independent prognostic marker in breast cancer. Br J Cancer 2015;112(1):61–8.

73. Brown C.M., Reisfeld B., Mayeno A.N. Cytochromes P450: a structure-based summary of biotransformations using representative substrates. Drug Metab Rev 2008;40(1):1–100.

74. Gillet J.P., Gottesman M.M. Mechanisms of multidrug resistance in cancer. Methods Mol Biol 2010;596:47–76.

75. Benet L.Z. The drug transporter-metabolism alliance: uncovering and defining the interplay. Mol Pharm 2009;6(6):1631–43.

76. Edavana V.K., Penney R.B., Yao-Borengasser A. et al. Fulvestrant up regulates UGT1A4 and MRPs through ERα and c-Myb pathways: a possible primary drug disposition mechanism. Springerplus 2013;2:620.

77. Wang Y.M., Lin W., Chai S.C. et al. Piperine activates human pregnane X receptor to induce the expression of cytochrome P4503A4 and multidrug resistance protein 1. Toxicol Appl Pharmacol 2013;272(1): 96–107.

78. Копнин Б.П. Опухолевые супрессоры и мутаторные гены. В кн.: Канцерогенез. Под ред. Д.Г. Заридзе. М.: Медицина, 2004. С. 125–57. [Kopnin B.P. Tumour suppressors and mutator genes. In: Carcinogenesis. D.G. Zaridze (ed.). Moscow: Meditsina, 2004. Pp. 125–57. (In Russ.)].

79. Bertheau P., Lehmann-Che J., Varna M. et al. p53 in breast cancer subtypes and new insights into response to chemotherapy. Breast 2013;Suppl 2:S27–9.

80. Berger C.E., Qian Y., Liu G. et al. p53, a target of estrogen receptor (ER) α, modulates DNA damage-induced growth suppression in ER-positive breast cancer cells. J Biol Chem 2012;287(36):30117–27.

81. Berger C., Qian Y., Chen X. The p53- estrogen receptor loop in cancer. Curr Mol Med 2013;13(8):1229–40.

82. Dos Anjos Pultz B., da Luz F.A., de Faria P.R. et al. Far beyond the usual biomarkers in breast cancer: a review. J Cancer 2014;5(7):559–71.

83. Baldacchino S., Saliba C., Petroni V. et al. Deregulation of the phosphatase, PP2A is a common event in breast cancer, predicting sensitivity to FTY720. EPMA J 2014;5(1):3.

84. Katayama K., Yamaguchi M., Noguchi K., Sugimoto Y. Protein phosphatase complex PP5/PPP2R3C dephosphorylates P-glycoprotein/ABCB1 and down-regulates the expression and function. Cancer Lett 2014;345(1):124–31.

85. Perrotti D., Neviani P. Protein phosphatase 2A: a target for anticancer therapy. Lancet Oncol 2013;14(6):e229–38.

86. Ataseven B., Gunesch A., Eiermann W. et al. PTK7 as a potential prognostic and predictive marker of response to adjuvant chemotherapy in breast cancer patients, and resistance to anthracycline drugs. Onco Targets Ther 2014;7:1723–31.

87. Yang Y. Wnt signaling in development and disease. Cell Biosci 2012;2(1):14.

88. Peradziryi H., Kaplan N.A., Podleschny M. et al. PTK7/Otk interacts with Wnts and inhibits canonical Wnt signalling. EMBO J 2011;30(18):3729–40.

89. Васильев Ю.М., Гельфанд И.М. Взаимодействие нормальных и неопластических клеток со средой. М.: Наука, 1981. 820 с. [Vasilyev Yu.M., Gelfand I.M. Interaction between normal and neoplastic cells and environment. Moscow: Nauka, 1981. 820 p. (In Russ.)].

90. Yamashiro S., Yamakita Y., Ono S., Matsumura F. Fascin, an actinbundling protein, induces membrane protrusions and increases cell motility of epithelial cells. Mol Biol Cell 1998;9(5):993–1006.

91. Yoder B. J., Tso E., Skacel M. et al. The expression of fascin, an actin-bundling motility protein, correlates with hormone receptor negative breast cancer and a more aggressive linical course. Clin Cancer Res 2005;11(1):186–92.

92. Ghebeh H., Al-Khaldi S., Olabi S. et al. Fascin is involved in the chemotherapeutic resistance of breast cancer cells predominantly via the PI3K/Akt pathway. Br J Cancer 2014;111(8):1552–61.

93. Елисеева И.А., Ким Е.Р., Гурьянов С.Г. и др. Y-бокс-связывающий белок 1 (YB-1) и его функции. Успехи биологической химии 2011;51:65–132. [Eliseeva I.A., Kim E.R., Gur, yanov S. G. et al. Y-box-binding protein 1 (YB-1) and its functions. Uspekhi biologicheskoy khimii = Advances in Biological Chemistry 2011;51:65–132. (In Russ.)].

94. Скабкин М.А., Скабкина О.В., Овчинников Л.П. Мультифункциональные белки с доменом холодового шока в регуляции экспрессии генов. Успехи биологической химии 2004;44:3–51. [Skabkin M.A., Skabkina O.V., Ovchinnikov L.P. Multifunctional proteins with cold shock domain in regulation of gene expression. Uspekhi biologicheskoy khimii = Advances in Biological Chemistry 2004;44:3– 51. (In Russ.)].

95. Davicioni L.P., Triche T. J. E., Sorensen P.H. Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer Cell 2009;15(5):402–15.

96. Ohga T., Uchiumi T., Makino Y. et al. Direct involvement of the Y-box binding protein YB-1 in genotoxic stress-induced activation of the human multidrug resistance 1 gene. J Biol Chem 1998;273(11):5997–6000.

97. Stein U., Bergmann S., Scheffer G.L. et al. YB-1 facilitates basal and 5–fluorouracil-enducible expression of the human major vault protein (MVP) gene. Oncogene 2005;24(22):3606–18.

98. Jurchott K., Bergmann S., Stein U. et al. YB-1 as a cell cycle-regulated transcription factor facilitating cyclin A and cyclin B1 gene expression. J Biol Chem 2003;278(30):27988–96.

99. Kuwano M., Oda Y., Izumi H. et al. The role of nuclear Y-box binding protein 1 as a global marker in drug resistance. Mol Cancer Ther 2004;3(11):1485–92.

100. Matsumoto K., Bay B.H. Significance of the Y-box proteins in human cancers. J Mol Genet Med 2005;1(1):11–7.

101. Генс Г.П., Ставровская А.А. Белок YB-1 как фактор прогноза при раке молочной железы. Вестник РОНЦ им. Н.Н. Блохина РАМН 2010;21(1):3–10. [Guens G.P., Stavrovskaya A.A. Белок YB-1 как фактор прогноза при раке молочной железы. Vestnik RONC im. N.N. Protein YB-1 as forecast factor at breast cancer. Bulletin of N.N. Blokhin NN Blokhin Russian Cancer Research Center at RAMS 2010;21(1):3–10. (In Russ.)].

102. Stavrovskaya A., Stromskaya T., Rybalkina E. et al. YB-1 protein and multidrug resistance of tumor cells. Curr Signal Transduct Ther 2012;7(3):237–46.

103. Guens G.P., Moiseeva N.I., Ovsii O.G. et al. Marker-adjusted personalized chemotherapy of breast cancer. Global J Breast Cancer Res 2014;2:19–26.

104. Yang H., Liu Y., Bai F. et al. Tumor development is associated with decrease of TET gene expression and 5–methylcytosine hydroxylation. Oncogene 2013;32(5):663–9.

105. Lu H.G., Zhan W., Yan L. et al. TET1 partially mediates HDAC inhibitor-induced suppression of breast cancer invasion. Mol Med Rep 2014;10(5):2595–600.

106. Kastl L., Brown I., Schofield A.C. Altered DNA methylation is associated with docetaxel resistance in human breast cancer cells. Int J Oncol 2010;36(5):1235–41.

107. Jovanovic J., Rønneberg J.A., Tost J., Kristensen V. The epigenetics of breast cancer. Mol Oncol 2010;4(3):242–54.

108. Hartmann O., Spyratos F., Harbeck N. et al. DNA methylation markers predict outcome in node-positive, estrogen receptorpositive breast cancer with adjuvant anthracycline-based chemotherapy. Clin Cancer Res 2009;15(1):315–23.

109. Dejeux E., Rønneberg J.A., Solvang H. et al. DNA methylation profiling in doxorubicin treated primary locally advanced breast tumours identifies novel genes associated with survival and treatment response. Mol Cancer 2010;9:68.

110. Рыбалкина Е.Ю., Павлова Г.В., Ставровская А.А. Новое в исследовании глиобластом. Биологические мембраны 2014;31(6):1–13. [Rybalkina E.Yu., Pavlova G.V., Stavrovskaya A.A. News of glioblast research. Biologicheskie membrany = Biological Membranes 2014;31(6):1– 13. (In Russ.)].

111. Chae Y.K., Gonzalez-Angulo A.M. Implications of functional proteomics in breast cancer. Oncologist 2014;19(4):328–35.


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Stavrovskaya A.A., Guens G.P. News in the studies of multidrug resistance of breast cancer cells. Advances in Molecular Oncology. 2015;2(1):039-051. (In Russ.) https://doi.org/10.17650/2313-805X.2015.2.1.039-051

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