350 rub
Journal №12 for 2013 г.
Article in number:
The molecular mechanisms of hormonal resistance of breast cancer: the role of NF-kappaB and Snail1 signaling pathways
Keywords: breast cancer epithelial-mesenchymal transition Snail1 ERα estrogens NF-κ B
Authors:
A.M. Scherbakov - Ph.D., Senior Researcher, Federal State Budgetary Institution «The N.N. Blokhin Russian Cancer Research Center» of the Russian Academy of Medical Sciences, Moscow, Russian Federation
O.E. Andreeva - Junior Researcher, Federal State Budgetary Institution «The N.N. Blokhin Russian Cancer Research Center» of the Russian Academy of Medical Sciences, Moscow, Russian Federation
A.A. Sharapov - Laboratory Assistant, Federal State Budgetary Institution «The N.N. Blokhin Russian Cancer Research Center» of the Russian Academy of Medical Sciences, Moscow, Russian Federation
R.K. Tanoyan - Laboratory Assistant, Federal State Budgetary Institution «The N.N. Blokhin Russian Cancer Research Center» of the Russian Academy of Medical Sciences, Moscow, Russian Federation
Abstract:
The basic mechanisms of hormonal resistance were considered in the review; the molecular pathways responsible for the development of the tolerance of tumor to hormonal cytostatic drugs were analyzed. Two proteins, NF-κB и Snail1 and their roles in the development of hormonal resistance were discussed in detail. The important factors of the hormonal resistance are: 1) the increase of Snail1 expression, 2) the changes in NF-κB activity, 3) the coordinated negative action of NF-κB and Snail1 pathways on estrogen receptors machinery in breast cancer. Thus Snail1 and NF-κB may serve as perspective targets in the treatment of breast cancer, particularly the hormonal resistant tumors.
Pages: 42-52
References
  1. Yaghjyan L., Colditz G.A. Estrogens in the breast tissue: a systematic review // Cancer Causes Control. 2011. V. 22. № 4. P. 529-540.
  2. Stingl J. Estrogen and progesterone in normal mammary gland development and in cancer // Horm Cancer. 2011. V. 2. № 2. P. 85-90.
  3. Bershtejn L.M. Onkoe'ndokrinologiya. Tradiczii, sovremennost' i perspektivy'. SPb.: Nauka. 2004.
  4. Harris J.R. Diseases of the breast. Lippincott-Raven, Philadelphia: 1996.
  5. Parl F.F. Estrogens, estrogen receptor, and breast cancer. IOS Press, Amsterdam; Washington, DC. 2000.
  6. Ali S., Buluwela L., Coombes R.C. Antiestrogens and their therapeutic applications in breast cancer and other diseases // Annu. Rev. Med. 2011. V. 62. P. 217-232.
  7. Rao R.D., Cobleigh M.A. Adjuvant endocrine therapy for breast cancer // Oncology. 2012. V. 26. № 6. P. 541-547, 550, 552 passim.
  8. Cosman F., Lindsay R. Selective estrogen receptor modulators: clinical spectrum // Endocr. Rev. 1999. V. 20. № 3. P. 418-434.
  9. Mao C., Yang Z.Y., He B.F., Liu S., Zhou J.H., Luo R.C., Chen Q., Tang J.L. Toremifene versus tamoxifen for advanced breast cancer // Cochrane Database Syst Rev. 2012. V. 7. P. CD008926.
  10. Roop R.P., Ma C.X. Endocrine resistance in breast cancer: molecular pathways and rational development of targeted therapies // Future Oncol. 2012. V. 8. № 3. P. 273-292.
  11. Fox E.M., Arteaga C.L., Miller T.W. Abrogating endocrine resistance by targeting ERalpha and PI3K in breast cancer // Front Oncol. 2012. V. 2. P. 145.
  12. Ring A., Dowsett M. Mechanisms of tamoxifen resistance // Endocr Relat Cancer. 2004. V. 11. № 4. P. 643-658.
  13. Clarke R., Liu M.C., Bouker K.B., Gu Z., Lee R.Y., Zhu Y., Skaar T.C., Gomez B., O'Brien K., Wang Y., Hilakivi-Clarke L.A. Antiestrogen resistance in breast cancer and the role of estrogen receptor signaling // Oncogene. 2003. V. 22. № 47. P. 7316-7339.
  14. Bershtejn L.M., Santen R. Molekulyarny'e mexanizmy' rezistentnosti k tamoksifenu // Voprosy' onkologii. 2002. T. 48. № 1. S. 17-23.
  15. Krasil'nikov M.A. Sovremenny'e podxody' k izucheniyu mexanizma e'strogen-nezavisimogo rosta opuxolej molochnoj zhelezy' // Voprosy' onkologii. 2004. T. 50. № 4. S. 399-405.
  16. Henderson B.E., Ponder B.A.J., Ross R.K. Hormones, genes, and cancer. Oxford; New York. Oxford University Press. 2003.
  17. Mosselman S., Polman J., Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor // FEBS Lett. 1996. V. 392. № 1. P. 49-53.
  18. Walter P., Green S., Greene G., Krust A., Bornert J.M., Jeltsch J.M., Staub A., Jensen E., Scrace G., Waterfield M., et al. Cloning of the human estrogen receptor cDNA // Proc. Natl. Acad. Sci. USA. 1985. V. 82. № 23. P. 7889-7893.
  19. Strom A., Hartman J., Foster J.S., Kietz S., Wimalasena J., Gustafsson J.A. Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D // Proc. Natl. Acad. Sci. USA. 2004. V. 101. № 6. P. 1566-1571.
  20. Duan R., Porter W., Safe S. Estrogen-induced c-fos protooncogene expression in MCF-7 human breast cancer cells: role of estrogen receptor Sp1 complex formation // Endocrinology. 1998. V. 139. № 4. P. 1981-1990.
  21. Johnston S.R., Saccani-Jotti G., Smith I.E., Salter J., Newby J., Coppen M., Ebbs S.R., Dowsett M. Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifen-resistant human breast cancer // Cancer Res. 1995. V. 55. № 15. P. 3331-3338.
  22. Gutierrez M.C., Detre S., Johnston S., Mohsin S.K., Shou J., Allred D.C., Schiff R., Osborne C.K., Dowsett M. Molecular changes in tamoxifen-resistant breast cancer: relationship between estrogen receptor, HER-2, and p38 mitogen-activated protein kinase // J. Clin. Oncol. 2005. V. 23. № 11. P. 2469-2476.
  23. Bachleitner-Hofmann T., Pichler-Gebhard B., Rudas M., Gnant M., Taucher S., Kandioler D., Janschek E., Dubsky P., Roka S., Sporn E., Jakesz R. Pattern of hormone receptor status of secondary contralateral breast cancers in patients receiving adjuvant tamoxifen // Clin. Cancer Res. 2002. V. 8. № 11. P. 3427-3432.
  24. Brunner N., Boysen B., Jirus S., Skaar T.C., Holst-Hansen C., Lippman J., Frandsen T., Spang-Thomsen M., Fuqua S.A., Clarke R. MCF7/LCC9: an antiestrogen-resistant MCF-7 variant in which acquired resistance to the steroidal antiestrogen ICI 182,780 confers an early cross-resistance to the nonsteroidal antiestrogen tamoxifen // Cancer Res. 1997. V. 57. № 16. P. 3486-3493.
  25. Shherbakov A.M., Lobanova Ju.S., Shatskaya V.A., Onopchenko O.V., Gaspar'yan A.V., Gershtejn E.S., Krasil'nikov M.A. Sensibilizacziya kletok raka molochnoj zhelezy' MCF-7 k apoptoticheskomu dejstviyu e'stradiola // Byulleten' e'ksperimental'noj biologii i medicziny'. 2006. T. 141. № 3. S. 334-337.
  26. Bartella V., De Marco P., Malaguarnera R., Belfiore A., Maggiolini M. New advances on the functional cross-talk between insulin-like growth factor-I and estrogen signaling in cancer // Cell. Signal. 2012. V. 24. № 8. P. 1515-1521.
  27. Moore R., Faller D.V. SIRT1 represses estrogen-signaling, ligand-independent ERalpha-mediated transcription, and cell proliferation in estrogen-responsive breast cells // J. Endocrinol. 2012. V. 216. № 3. R. 273-285.
  28. Nicholson R.I., Hutcheson I.R., Harper M.E., Knowlden J.M., Barrow D., McClelland R.A., Jones H.E., Wakeling A.E., Gee J.M. Modulation of epidermal growth factor receptor in endocrine-resistant, oestrogen receptor-positive breast cancer // Endocr. Relat. Cancer. 2001. V. 8. № 3. P. 175-182.
  29. Gee J.M., Harper M.E., Hutcheson I.R., Madden T.A., Barrow D., Knowlden J.M., McClelland R.A., Jordan N., Wakeling A.E., Nicholson R.I. The antiepidermal growth factor receptor agent gefitinib (ZD1839/Iressa) improves antihormone response and prevents development of resistance in breast cancer in vitro // Endocrinology. 2003. V. 144. № 11. P. 5105-5117.
  30. Stoica G.E., Franke T.F., Wellstein A., Czubayko F., List H.J., Reiter R., Morgan E., Martin M.B., Stoica A. Estradiol rapidly activates Akt via the ErbB2 signaling pathway // Mol. Endocrinol. 2003. V. 17. № 5. P. 818-830.
  31. Zhou Y., Eppenberger-Castori S., Eppenberger U., Benz C.C. The NFkappaB pathway and endocrine-resistant breast cancer // Endocr. Relat. Cancer. 2005. V. 12 Suppl 1. № P. S37-46.
  32. Scherbakov A.M., Andreeva O.E., Shatskaya V.A., Krasil'nikov M.A. The relationships between snail1 and estrogen receptor signaling in breast cancer cells // Journal of cellular biochemistry. 2012. V. 113. № 6. P. 2147-2155.
  33. Hugo H.J., Kokkinos M.I., Blick T., Ackland M.L., Thompson E.W., Newgreen D.F. Defining the E-cadherin repressor interactome in epithelial-mesenchymal transition: the PMC42 model as a case study // Cells Tissues Organs. 2011. V. 193. № 1-2. P. 23-40.
  34. Berstein L.M., Zheng H., Yue W., Wang J.P., Lykkesfeldt A.E., Naftolin F., Harada H., Shanabrough M., Santen R.J. New approaches to the understanding of tamoxifen action and resistance // Endocr Relat Cancer. 2003. V. 10. № 2. P. 267-277.
  35. Santen R.J., Song R.X., Zhang Z., Kumar R., Jeng M.H., Masamura S., Yue W., Berstein L. Adaptive hypersensitivity to estrogen: mechanism for superiority of aromatase inhibitors over selective estrogen receptor modulators for breast cancer treatment and prevention // Endocr Relat Cancer. 2003. V. 10. № 2. P. 111-130.
  36. Scherbakov A.M., Lobanova Y.S., Shatskaya V.A., Onopchenko O.V., Gershtein E.S., Krasil'nikov M.A. Activation of mitogenic pathways and sensitization to estrogen-induced apoptosis: two independent characteristics of tamoxifen-resistant breast cancer cells - // Breast Cancer Res Treat. 2006. V. 100. № 1. P. 1-11.
  37. Jalava P., Kuopio T., Huovinen R., Laine J., Collan Y. Immunohistochemical staining of estrogen and progesterone receptors: aspects for evaluating positivity and defining the cutpoints // Anticancer Res. 2005. V. 25. № 3c. P. 2535-2542.
  38. Tamoxifen for early breast cancer: an overview of the randomised trials. Early Breast Cancer Trialists' Collaborative Group // Lancet. 1998. V. 351. № 9114. P. 1451-1467.
  39. Dotzlaw H., Leygue E., Watson P.H., Murphy L.C. Estrogen receptor-beta messenger RNA expression in human breast tumor biopsies: relationship to steroid receptor status and regulation by progestins // Cancer Res. 1999. V. 59. № 3. P. 529-532.
  40. Baselga J., Campone M., Piccart M., Burris H.A., 3rd, Rugo H.S., Sahmoud T., Noguchi S., Gnant M., Pritchard K.I., Lebrun F., Beck J.T., Ito Y., Yardley D., Deleu I., Perez A., Bachelot T., Vittori L., Xu Z., Mukhopadhyay P., Lebwohl D., Hortobagyi G.N. Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer // N. Engl. J. Med. 2012. V. 366. № 6. P. 520-529.
  41. Song R.X., Mor G., Naftolin F., McPherson R.A., Song J., Zhang Z., Yue W., Wang J., Santen R.J. Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17beta-estradiol // J. Natl. Cancer. Inst. 2001. V. 93. № 22. P. 1714-1723.
  42. Song R.X., Santen R.J. Apoptotic action of estrogen // Apoptosis. 2003. V. 8. № 1. P. 55-60.
  43. Lobanova Ju.S., Shherbakov A.M., Shatskaya V.A., Krasil'nikov M.A. E'strogen-zavisimy'j apoptoz v kletkax raka molochnoj zhelezy': rol' signal'nogo puti, reguliruemogo NF-kB // Bioximiya. 2007. T. 72. № 3. S. 392-401.
  44. Lobanova Y.S., Scherbakov A.M., Shatskaya V.A., Evteev V.A., Krasil'nikov M.A. NF-kappaB suppression provokes the sensitization of hormone-resistant breast cancer cells to estrogen apoptosis // Molecular and cellular biochemistry. 2009. V. 324. № 1-2. P. 65-71.
  45. Barron-Gonzalez A., Castro Romero I. Re-expression of estrogen receptor alpha using a tetracycline-regulated gene expression system induced estrogen-mediated growth inhibition of the MDA-MB-231 breast cancer cell line // Biochem. Cell. Biol. 2004. V. 82. № 2. P. 335-342.
  46. Jenkins J.K., Suwannaroj S., Elbourne K.B., Ndebele K., McMurray R.W. 17-beta-estradiol alters Jurkat lymphocyte cell cycling and induces apoptosis through suppression of Bcl-2 and cyclin A // Int Immunopharmacol. 2001. V. 1. № 11. P. 1897-1911.
  47. Jun D.Y., Park H.S., Kim J.S., Park W., Song B.H., Kim H.S., Taub D., Kim Y.H. 17alpha-Estradiol arrests cell cycle progression at G(2)/M and induces apoptotic cell death in human acute leukemia Jurkat T cells // Toxicol. Appl. Pharmacol. 2008.
  48. Seli E., Guzeloglu-Kayisli O., Kayisli U.A., Kizilay G., Arici A. Estrogen increases apoptosis in the arterial wall in a murine atherosclerosis model // Fertil Steril. 2007. V. 88. № 4 Suppl. P. 1190-1196.
  49. Jiang H.P., Teng R.Y., Wang Q., Zhang X., Wang H.H., Cao J., Teng L.S. Estrogen receptor alpha variant ERalpha46 mediates growth inhibition and apoptosis of human HT-29 colon adenocarcinoma cells in the presence of 17beta-oestradiol // Chin Med J (Engl). 2008. V. 121. № 11. P. 1025-1031.
  50. Song R.X., Zhang Z., Mor G., Santen R.J. Down-regulation of Bcl-2 enhances estrogen apoptotic action in long-term estradiol-depleted ER(+) breast cancer cells // Apoptosis. 2005. V. 10. № 3. P. 667-678.
  51. Liu H., Lee E.S., Gajdos C., Pearce S.T., Chen B., Osipo C., Loweth J., McKian K., De Los Reyes A., Wing L., Jordan V.C. Apoptotic action of 17beta-estradiol in raloxifene-resistant MCF-7 cells in vitro and in vivo // J. Natl. Cancer. Inst. 2003. V. 95. № 21. P. 1586-1597.
  52. Lewis J.S., Osipo C., Meeke K., Jordan V.C. Estrogen-induced apoptosis in a breast cancer model resistant to long-term estrogen withdrawal // J. Steroid. Biochem. Mol. Biol. 2005. V. 94. № 1-3. P. 131-141.
  53. Osipo C., Gajdos C., Cheng D., Jordan V.C. Reversal of tamoxifen resistant breast cancer by low dose estrogen therapy // J. Steroid. Biochem. Mol. Biol. 2005. V. 93. № 2-5. P. 249-256.
  54. Lonning P.E., Taylor P.D., Anker G., Iddon J., Wie L., Jorgensen L.M., Mella O., Howell A. High-dose estrogen treatment in postmenopausal breast cancer patients heavily exposed to endocrine therapy // Breast. Cancer. Res. Treat. 2001. V. 67. № 2. P. 111-116.
  55. Peethambaram P.P., Ingle J.N., Suman V.J., Hartmann L.C., Loprinzi C.L. Randomized trial of diethylstilbestrol vs. tamoxifen in postmenopausal women with metastatic breast cancer. An updated analysis // Breast. Cancer. Res. Treat. 1999. V. 54. № 2. P. 117-122.
  56. Osipo C., Gajdos C., Liu H., Chen B., Jordan V.C. Paradoxical action of fulvestrant in estradiol-induced regression of tamoxifen-stimulated breast cancer // J. Natl. Cancer. Inst. 2003. V. 95. № 21. P. 1597-1608.
  57. Osipo C., Liu H., Meeke K., Jordan V.C. The consequences of exhaustive antiestrogen therapy in breast cancer: estrogen-induced tumor cell death // Exp. Biol. Med. (Maywood). 2004. V. 229. № 8. P. 722-731.
  58. Van Laere S.J., Van der Auwera I., Van den Eynden G.G., van Dam P., Van Marck E.A., Vermeulen P.B., Dirix L.Y. NF-kappaB activation in inflammatory breast cancer is associated with oestrogen receptor downregulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation // Br. J. Cancer. 2007. V. 97. № 5. P. 659-669.
  59. Lobanova Ju.S., Shherbakov A.M., Shatskaya V.A., Krasil'nikov M.A. E'strogenzavisimy'j apoptoz v kletkax raka molochnoj zhelezy': rol' signal'nogo puti, reguliruemogo NF-κB // Bioximiya. 2007. T. 72. № 3. S. 392-401.
  60. Brasier A.R. The NF-kappaB regulatory network // Cardiovasc. Toxicol. 2006. V. 6. № 2. P. 111-130.
  61. Shostak K., Chariot A. NF-kappaB, stem cells and breast cancer: the links get stronger // Breast. cancer research.: BCR. 2011. V. 13. № 4. P. 214.
  62. Lan W., Petznick A., Heryati S., Rifada M., Tong L. Nuclear Factor-kappaB: central regulator in ocular surface inflammation and diseases // Ocul. Surf. 2012. V. 10. № 3. P. 137-148.
  63. Ling J., Kumar R. Crosstalk between NFkB and glucocorticoid signaling: a potential target of breast cancer therapy // Cancer letters. 2012. V. 322. № 2. P. 119-126.
  64. Evans M.J., Eckert A., Lai K., Adelman S.J., Harnish D.C. Reciprocal antagonism between estrogen receptor and NF-kappaB activity in vivo // Circ. Res. 2001. V. 89. № 9. P. 823-830.
  65. Sandholm J., Kauppila J.H., Pressey C., Tuomela J., Jukkola-Vuorinen A., Vaarala M., Johnson M.R., Harris K.W., Selander K.S. Estrogen receptor-alpha and sex steroid hormones regulate Toll-like receptor-9 expression and invasive function in human breast cancer cells // Breast cancer research and treatment. 2012. V. 132. № 2. P. 411-419.
  66. Biswas D.K., Singh S., Shi Q., Pardee A.B., Iglehart J.D. Crossroads of estrogen receptor and NF-kappaB signaling // Sci STKE. 2005. V. 2005. № 288. P. pe27.
  67. Harnish D.C., Scicchitano M.S., Adelman S.J., Lyttle C.R., Karathanasis S.K. The role of CBP in estrogen receptor cross-talk with nuclear factor-kappaB in HepG2 cells // Endocrinology. 2000. V. 141. № 9. P. 3403-3411.
  68. Wajant H., Pfizenmaier K., Scheurich P. Tumor necrosis factor signaling // Cell Death Differ. 2003. V. 10. № 1. P. 45-65.
  69. Singh S., Shi Q., Bailey S.T., Palczewski M.J., Pardee A.B., Iglehart J.D., Biswas D.K. Nuclear factor-kappaB activation: a molecular therapeutic target for estrogen receptor-negative and epidermal growth factor receptor family receptor-positive human breast cancer // Molecular cancer therapeutics. 2007. V. 6. № 7. P. 1973-1982.
  70. Cardoso F., Durbecq V., Laes J.F., Badran B., Lagneaux L., Bex F., Desmedt C., Willard-Gallo K., Ross J.S., Burny A., Piccart M., Sotiriou C. Bortezomib (PS-341, Velcade) increases the efficacy of trastuzumab (Herceptin) in HER-2-positive breast cancer cells in a synergistic manner // Molecular cancer therapeutics. 2006. V. 5. № 12. P. 3042-3051.
  71. Frasor J., Weaver A., Pradhan M., Dai Y., Miller L.D., Lin C.Y., Stanculescu A. Positive cross-talk between estrogen receptor and NF-kappaB in breast cancer // Cancer research. 2009. V. 69. № 23. P. 8918-8925.
  72. Scherbakov A.M., Lobanova Y.S., Andreeva O.E., Shatskaya V.A., Krasil'nikov M.A. Oestrogen treatment enhances the sensitivity of hormone-resistant breast cancer cells to doxorubicin // Bioscience reports. 2011. V. 31. № 2. P. 137-143.
  73. Li Y., Ahmed F., Ali S., Philip P.A., Kucuk O., Sarkar F.H. Inactivation of nuclear factor kappaB by soy isoflavone genistein contributes to increased apoptosis induced by chemotherapeutic agents in human cancer cells // Cancer research. 2005. V. 65. № 15. P. 6934-6942.
  74. Wu K., Bonavida B. The activated NF-kappaB-Snail-RKIP circuitry in cancer regulates both the metastatic cascade and resistance to apoptosis by cytotoxic drugs // Crit. Rev. Immunol. 2009. V. 29. № 3. P. 241-254.
  75. Acloque H., Adams M.S., Fishwick K., Bronner-Fraser M., Nieto M.A. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease // J. Clin. Invest. 2009. V. 119. № 6. P. 1438-1449.
  76. Zeisberg M., Neilson E.G. Biomarkers for epithelial-mesenchymal transitions // J Clin Invest. 2009. V. 119. № 6. P. 1429-1437.
  77. Nieto M.A. Epithelial-Mesenchymal Transitions in development and disease: old views and new perspectives // Int. J. Dev. Biol. 2008. V. N.
  78. De Wever O., Pauwels P., De Craene B., Sabbah M., Emami S., Redeuilh G., Gespach C., Bracke M., Berx G. Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front // Histochem. Cell. Biol. 2008. V. 130. № 3. P. 481-494.
  79. Alves C.C., Carneiro F., Hoefler H., Becker K.F. Role of the epithelial-mesenchymal transition regulator Slug in primary human cancers // Front Biosci. 2009. V. 14. P. 3035-3050.
  80. Becker K.F., Rosivatz E., Blechschmidt K., Kremmer E., Sarbia M., Hofler H. Analysis of the E-cadherin repressor Snail in primary human cancers // Cells. Tissues. Organs. 2007. V. 185. № 1-3. P. 204-212.
  81. Come C., Arnoux V., Bibeau F., Savagner P. Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression // J. Mammary Gland. Biol. Neoplasia. 2004. V. 9. № 2. P. 183-193.
  82. Blechschmidt K., Kremmer E., Hollweck R., Mylonas I., Hofler H., Kremer M., Becker K.F. The E-cadherin repressor snail plays a role in tumor progression of endometrioid adenocarcinomas // Diagn. Mol. Pathol. 2007. V. 16. № 4. P. 222-228.
  83. Park S.H., Cheung L.W., Wong A.S., Leung P.C. Estrogen regulates Snail and Slug in the down-regulation of E-cadherin and induces metastatic potential of ovarian cancer cells through estrogen receptor alpha // Mol. Endocrinol. 2008. V. 22. № 9. P. 2085-2098.
  84. Ye Y., Xiao Y., Wang W., Yearsley K., Gao J.X., Barsky S.H. ERalpha suppresses slug expression directly by transcriptional repression // Biochem. J. 2008. V. 416. № 2. P. 179-187.
  85. Dhasarathy A., Kajita M., Wade P.A. The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-alpha // Mol. Endocrinol. 2007. V. 21. № 12. P. 2907-2918.
  86. Fujita N., Jaye D.L., Kajita M., Geigerman C., Moreno C.S., Wade P.A. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer // Cell. 2003. V. 113. № 2. P. 207-219.
  87. Geradts J., de Herreros A.G., Su Z., Burchette J., Broadwater G., Bachelder R.E. Nuclear Snail1 and nuclear ZEB1 protein expression in invasive and intraductal human breast carcinomas // Human pathology. 2011. V. 42. № 8. P. 1125-1131.
  88. Andreeva O.E., Shcherbakov A.M., Shatskaia V.A., Krasil'nikov M.A. The role of transcription factor Snail1 in the regulation of hormonal sensitivity of in vitro cultured breast cancer cells // Voprosy. onkologii. 2012. V. 58. № 1. P. 71-76.
  89. Wu W.S., Heinrichs S., Xu D., Garrison S.P., Zambetti G.P., Adams J.M., Look A.T. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma // Cell. 2005. V. 123. № 4. P. 641-653.
  90. Maier P., Herskind C., Barzan D., Zeller W.J., Wenz F. SNAI2 as a novel radioprotector of normal tissue by gene transfer using a lentiviral bicistronic SIN vector // Radiat. Res. V. 173. № 5. P. 612-619.
  91. Escriva M., Peiro S., Herranz N., Villagrasa P., Dave N., Montserrat-Sentis B., Murray S.A., Franci C., Gridley T., Virtanen I., Garcia de Herreros A. Repression of PTEN phosphatase by Snail1 transcriptional factor during gamma radiation-induced apoptosis // Mol. Cell. Biol. 2008. V. 28. № 5. P. 1528-1540.