Effect of modulation of epithelial‑mesenchymal transition regulators Snail1 and Snail2 on cancer cell radiosensitivity by targeting of the cell cycle, cell apoptosis and cell migration/invasion (Review)
- Authors:
- Ganiou Assani
- Yunfeng Zhou
-
Affiliations: Department of Radiation and Medical Oncology, Zhongnan Hospital of Wuhan University, Wuhan, Hubei 430071, P.R. China - Published online on: October 29, 2018 https://doi.org/10.3892/ol.2018.9636
- Pages: 23-30
-
Copyright: © Assani et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: International Agency for Research on Cancer. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide. IARC CancerBase No.11.Globocan.iarc.fr. December. 12. 2013 | |
World Health Organization. Health Statistics and Information Systems. WHO Mortality. simpleDatabase.who.int/healthinfo/mortality_data/en/November 6–2014 | |
Ghoncheh M, Pournamdar Z and Salehiniya H: Incidence and mortality and epidemiology of breast cancer in the world. Asian Pac J Cancer Prev. 17:43–46. 2016. View Article : Google Scholar : PubMed/NCBI | |
Clifton K, Gutierrez-Barrera A, Ma J, Bassett R Jr, Litton J, Kuerer H, Moulder S, Albarracin C, Hortobagyi G and Arun B: Adjuvant versus neoadjuvant chemotherapy in triple-negative breast cancer patients with BRCA mutations. Breast Cancer Res Treat. 170:101–109. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lui F, Xu K, Yang H, Li Y, Liu J, Wang J and Guan Z: A novel approach to glioma therapy an oncolytic adenovirus with two specific promoters. Oncol Lett. 15:3362–3368. 2018.PubMed/NCBI | |
Bykov IM, Izhnina EV, Kochurova EV and Lapina NV: Radiation-associated changes in salivation of patients with cancer of maxillofacial region. Stomatologia (Mosk). 97:67–70. 2018.(In Russian). View Article : Google Scholar | |
Ochoa CE and Joseph RW: Nivolumab in renal cell carcinoma: Current trends and future perspectives. J Kidney Cancer VHL. 5:15–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
Delaney G, Jacob S, Featherstone C and Barton M: The role of radiotherapy in cancer treatment: Estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 104:1129–1137. 2005. View Article : Google Scholar : PubMed/NCBI | |
Delaney G, Jacob S and Barton M: Estimating the optimal external-beam radiotherapy utilization rate for genitourinary malignancies. Cancer. 103:462–473. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pedroza-Torres A, Campos-Parra AD, Millan-Catalan O, Loissell-Baltazar YA, Zamudio-Meza H, Cantú de León D, Montalvo-Esquivel G, Isla-Ortiz D, Herrera LA, Ángeles-Zaragoza Ó, et al: MicroRNA-125 modulates radioresistance through targeting p21 in cervical cancer. Oncol Rep. 39:1532–1540. 2018.PubMed/NCBI | |
Cox JD, Stetz J and Pajak TF: Toxicity criteria of the Radiation Therapy Oncology Group (RTOG) and the European Organization for Research and Treatment of Cancer (EORTC). Int J Radiat Oncol Biol Phys. 31:1341–1346. 1995. View Article : Google Scholar : PubMed/NCBI | |
Tetzlaff MT, Teh BS, Timme TL, Fujita T, Satoh T, Tabata K, Mai WY, Vlachaki MT, Amato RJ, Kadmon D, et al: Expanding the therapeutic index of radiation therapy by combining in situ gene therapy in the treatment of prostate cancer. Technol Cancer Res Treat. 5:23–36. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zheng X, Zhang Y, Liu Y, Fang L, Li L, Sun J, Pan Z, Xin W and Huang P: HIF-2α activated lncRNA NEAT1 promotes hepatocellular carcinoma cell invasion and metastasis by affecting the epithelial-mesenchymal transition. J Cell Biochem. 119:3247–3256. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yang F, Gu Y, Zhao Z, Huang J, Jiang WG and Cheng S: NHERF1 suppresses lung cancer cell migration by regulation of epithelial-mesenchymal transition. Anticancer Res. 37:4405–4414. 2017.PubMed/NCBI | |
Robson EJ, Khaled WT, Abell K and Watson CJ: Epithelial-to-mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines. Differentiation. 74:254–264. 2006. View Article : Google Scholar : PubMed/NCBI | |
Lovisa S, LeBleu VS, Tampe B, Sugimoto H, Vadnagara K, Carstens JL, Wu CC, Hagos Y, Burckhardt BC, Pentcheva-Hoang T, et al: Epithelial-to-mesenchymal transition induces cell cycle arrest and parenchymal damage in renal fibrosis. Nat Med. 21:998–1009. 2015. View Article : Google Scholar : PubMed/NCBI | |
Du B and Shim JS: Targeting Epithelial-Mesenchymal Transition (EMT) to Overcome Drug Resistance in Cancer. Molecules. 21(pii): E9652016. View Article : Google Scholar : PubMed/NCBI | |
Desai S, Barai A, Bukhari AB, De A and Sen S: α-Actinin-4 confers radioresistance coupled invasiveness in breast cancer cells through AKT pathway. Biochim Biophys Acta Mol Cell Res. 1865:196–208. 2018. View Article : Google Scholar : PubMed/NCBI | |
Martínez-Alvarez C, Blanco MJ, Pérez R, Rabadán MA, Aparicio M, Resel E, Martínez T and Nieto MA: Snail family members and cell survival in physiological and pathological cleft palates. Dev Biol. 265:207–218. 2004. View Article : Google Scholar : PubMed/NCBI | |
Côme C, Arnoux V, Bibeau F and Savagner P: Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression. J Mammary Gland Biol Neoplasia. 9:183–193. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY and Bapat SA: Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells. 27:2059–2068. 2009. View Article : Google Scholar : PubMed/NCBI | |
Thiery JP: Epithelial-mesenchymal transitions in tumor progression. Nat Rev Cancer. 2:442–454. 2002. View Article : Google Scholar : PubMed/NCBI | |
Savanger P: Leaving the neighbourhood: Molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays. 23:912–923. 2001. View Article : Google Scholar : PubMed/NCBI | |
Singh A and Settleman J: EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene. 29:4741–4751. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nieto MA: The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 3:155–166. 2002. View Article : Google Scholar : PubMed/NCBI | |
Bolós V, Peinado H, Pérez-Moreno MA, Fraga MF, Esteller M and Cano A: The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: A comparison with snail and E47 repressors. J Cell Sci. 116:499–511. 2003. View Article : Google Scholar : PubMed/NCBI | |
Storci G, Sansone P, Trere D, Tavolari S, Taffurelli M, Ceccarelli C, Guarnieri T, Paterini P, Pariali M, Montanaro L, et al: The basal-like breast carcinoma phenotype is regulated by SLUG gene expression. J Pathol. 214:25–37. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hajra KM, Chen DY and Fearon ER: The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 62:1613–1618. 2002.PubMed/NCBI | |
Zhou W, Lv R, Qi W, Wu D, Xu Y, Liu W, Mou Y and Wang L: Snail contributes to the maintenance of stem cell-like phenotype cells in human pancreatic cancer. PLoS One. 9:e874092014. View Article : Google Scholar : PubMed/NCBI | |
Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A and Weinberg RA: Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 117:927–939. 2004. View Article : Google Scholar : PubMed/NCBI | |
Guaita S, Puig I, Franci C, Garrido M, Dominguez D, Batlle E, Sancho E, Dedhar S, De Herreros AG and Baulida J: Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J Biol Chem. 277:39209–39216. 2002. View Article : Google Scholar : PubMed/NCBI | |
Perez-Moreno MA, Locascio A, Rodrigo I, Dhondt G, Portillo F, Nieto MA and Cano A: A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J Biol Chem. 276:27424–27431. 2001. View Article : Google Scholar : PubMed/NCBI | |
Nieto MA, Sargent MG, Wilkinson DG and Cooke J: Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science. 264:835–839. 1994. View Article : Google Scholar : PubMed/NCBI | |
Elloul S, Elstrand MB, Nesland JM, Tropé CG, Kvalheim G, Goldberg I, Reich R and Davidson B: Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer. 103:1631–1643. 2005. View Article : Google Scholar : PubMed/NCBI | |
Martin TA, Goyal A, Watkins G and Jiang WG: Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol. 12:488–496. 2005. View Article : Google Scholar : PubMed/NCBI | |
Côme C, Magnino F, Bibeau F, De Santa Barbara P, Becker KF, Theillet C and Savagner P: Snail and slug play distinct roles during breast carcinoma progression. Clin Cancer Res. 12:5395–5402. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hemavathy K, Ashraf SI and Ip YT: Snail/slug family of repressors: Slowly going into the fast lane of development and cancer. Gene. 257:1–12. 2000. View Article : Google Scholar : PubMed/NCBI | |
Cobaleda C, Perez-Caro M, Vicente-Dueñas C and Sánchez-García I: Function of the zinc-finger transcription factor SNAI2 in cancer and development. Annu Rev Genet. 41:41–61. 2007. View Article : Google Scholar : PubMed/NCBI | |
Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F and Nieto MA: The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol. 2:76–83. 2000. View Article : Google Scholar : PubMed/NCBI | |
Batlle E, Sancho E, Francí C, Domínguez D, Monfar M, Baulida J and García De Herreros A: The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2:84–89. 2000. View Article : Google Scholar : PubMed/NCBI | |
Ikenouchi J, Matsuda M, Furuse M and Tsukita S: Regulation of tight junctions during the epithelium-mesenchyme transition: Direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci. 116:1959–1967. 2003. View Article : Google Scholar : PubMed/NCBI | |
Tripathi MK, Misra S and Chaudhuri G: Negative regulation of the expressions of cytokeratins 8 and 19 by SLUG repressor protein in human breast cells. Biochem Biophys Res Commun. 329:508–515. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kurrey NK, K A and Bapat SA: Snail and slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol Oncol. 97:155–165. 2005. View Article : Google Scholar : PubMed/NCBI | |
Xu Z, Jiang Y, Steed H, Davidge S and Fu Y: TGFβ and EGF synergistically induce a more invasive phenotype of epithelial ovarian cancer cells. Biochem Biophys Res Commun. 401:376–381. 2010. View Article : Google Scholar : PubMed/NCBI | |
Peiró S, Escrivà M, Puig I, Barberà MJ, Dave N, Herranz N, Larriba MJ, Takkunen M, Francí C, Muñoz A, et al: Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic Acids Res. 34:2077–2084. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kumar B, Uppuladinne MV, Jani V, Sonavane U, Joshi RR and Bapat SA: Auto-regulation of Slug mediates its activity during epithelial to mesenchymal transition. Biochim Biophys Acta. 1849:1209–12018. 2015. View Article : Google Scholar : PubMed/NCBI | |
Peinado H, Olmeda D and Cano A: Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat Rev Cancer. 7:415–428. 2007. View Article : Google Scholar : PubMed/NCBI | |
Osorio LA, Farfán NM, Castellón EA and Contreras HR: SNAIL transcription factor increases the motility and invasive capacity of prostate cancer cells. Mol Med Rep. 13:778–786. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wu Z, Li X, Cai X, Huang C and Zheng M: miR-497 inhibits epithelial-mesenchymal transition in breast carcinoma by targeting Slug. Tumour Biol. 37:7939–7950. 2016. View Article : Google Scholar : PubMed/NCBI | |
Aletaha M, Mansoori B, Mohammadi A, Fazeli M and Baradaran B: The Effect of Snail1 Gene Silencing by siRNA in Metastatic Breast Cancer Cell Lines. Iran J Public Health. 46:659–670. 2017.PubMed/NCBI | |
Kajita M, McClinic KN and Wade PA: Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Mol Cell Biol. 24:7559–7566. 2004. View Article : Google Scholar : PubMed/NCBI | |
Franco DL, Mainez J, Vega S, Sancho P, Murillo MM, de Frutos CA, Del Castillo G, López-Blau C, Fabregat I and Nieto MA: Snail1 suppresses TGF-beta-induced apoptosis and is sufficient to trigger EMT in hepatocytes. J Cell Sci. 123:3467–3477. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wan Z, Pan H, Liu S, Zhu J, Qi W, Fu K, Zhao T and Liang J: Downregulation of SNAIL sensitizes hepatocellular carcinoma cells to TRAIL-induced apoptosis by regulating the NF-κB pathway. Oncol Rep. 33:1560–1566. 2015. View Article : Google Scholar : PubMed/NCBI | |
Olmeda D, Jordá M, Peinado H, Fabra A and Cano A: Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene. 26:1862–1874. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kim S, Yao J, Suyama K, Qian X, Qian BZ, Bandyopadhyay S, Loudig O, De Leon-Rodriguez C, Zhou ZN, Segall J, et al: Slug promotes survival during metastasis through suppression of Puma-mediated apoptosis. Cancer Res. 74:3695–3706. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Yue B, Yu X, Wang Z and Wang M: SLUG is activated by nuclear factor kappa B and confers human alveolar epithelial A549 cells resistance to tumor necrosis factor-alpha-induced apoptosis. World J Surg Oncol. 11:122013. View Article : Google Scholar : PubMed/NCBI | |
Mancini M, Petta S, Iacobucci I, Salvestrini V, Barbieri E and Santucci MA: Zinc-finger transcription factor slug contributes to the survival advantage of chronic myeloid leukemia cells. Cell Signal. 22:1247–1253. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhang K, Zhang S, Jiao X, Wang H, Zhang D, Niu Z, Shen Y, Lv L and Zhou Y: Slug regulates proliferation and invasiveness of esophageal adenocarcinoma cells in vitro and in vivo. Med Oncol. 28:1089–1100. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mezencev R, Matyunina lV, Jabbari N and McDonald JF: Snail-induced epithelial-to-mesenchymal transition of MCF-7 breast cancer cells: Systems analysis of molecular changes and their effect on radiation and drug sensitivity. BMC Cancer. 16:2362016. View Article : Google Scholar : PubMed/NCBI | |
Escrivà M, Peiró S, Herranz N, Villagrasa P, Dave N, Montserrat-Sentís B, Murray SA, Francí C, Gridley T, Virtanen I and García de Herreros A: Repression of PTEN phosphatase by Snail1 transcriptional factor during gamma radiation-induced apoptosis. Mol Cell Biol. 28:1528–1540. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zhang K, Jiao X, Liu X, Zhang B, Wang J, Wang Q, Tao Y and Zhang D: Knockdown of snail sensitizes pancreatic cancer cells to chemotherapeutic agents and irradiation. Int J Mol Sci. 11:4891–4892. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhang K, Zhang B, Lu Y, Sun C, Zhao W, Jiao X, Hu J, Mu P, Lu H and Zhou C: Slug inhibition upregulates radiation-induced PUMA activity leading to apoptosis in cholangiocarcinomas. Med Oncol. 28 (Suppl 1):S301–S309. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jiang F, Zhou L, Wei C, Zhao W and Yu D: Slug inhibition increases radiosensitivity of oral squamous cell carcinoma cells by upregulating PUMA. Int J Oncol. 49:709–719. 2016. View Article : Google Scholar : PubMed/NCBI | |
Inoue A, Seidel MG, Wu W, Kamizono S, Ferrando AA, Bronson RT, Iwasaki H, Akashi K, Morimoto A, Hitzler JK, et al: Slug, a highly conserved zinc finger transcriptional repressor, protects hematopoietic progenitor cells from radiation-induced apoptosis in vivo. Cancer Cell. 2:279–288. 2002. View Article : Google Scholar : PubMed/NCBI | |
Arienti C, Tesei A, Carloni S, Ulivi P, Romeo A, Ghigi G, Menghi E, Sarnelli A, Parisi E, Silvestrini R and Zoli W: SLUG silencing increases radiosensitivity of melanoma cells in vitro. Cell Oncol (Dordr). 36:131–139. 2013. View Article : Google Scholar : PubMed/NCBI | |
Vega S, Morales AV, Ocaña OH, Valdés F, Fabregat I and Nieto MA: Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18:1131–1143. 2004. View Article : Google Scholar : PubMed/NCBI | |
Mittal MK, Singh K, Misra S and Chaudhuri GJ: SLUG-induced elevation of D1 cyclin in breast cancer cells through the inhibition of its ubiquitination. Biol Chem. 286:469–479. 2011. View Article : Google Scholar | |
Sherr CJ: Mammalian G1 cyclins. Cell. 73:1059–1065. 1993. View Article : Google Scholar : PubMed/NCBI | |
Liu J, Uygur B, Zhang Z, Shao L, Romero D, Vary C, Ding Q and Wu WS: Slug inhibits proliferation of human prostate cancer cells via downregulation of cyclin D1 expression. Prostate. 70:1768–1777. 2010.PubMed/NCBI | |
Emadi Baygi M, Soheili ZS, Essmann F, Deezagi A, Engers R, Goering W and Schulz WA: Slug/SNAI2 regulates cell proliferation and invasiveness of metastatic prostate cancer cell lines. Tumour Biol. 31:297–307. 2010. View Article : Google Scholar : PubMed/NCBI | |
Biade S, Stobbe CC and Chapman JD: The intrinsic radiosensitivity of some human tumor cells throughout their cell cycles. Radiat Res. 147:416–421. 1997. View Article : Google Scholar : PubMed/NCBI | |
Pawlik TM and Keyomarsi K: Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 59:928–942. 2004. View Article : Google Scholar : PubMed/NCBI | |
Neal CL, Mckeithen D and Odero-Marah VA: Snail negatively regulates cell adhesion to extracellular matrix and integrin expression via the MAPK pathway in prostate cancer cells. Cell Adh Migr. 5:249–257. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jin H, Yu Y, Zhang T, Zhou X, Zhou J, Jia L, Wu Y, Zhou BP and Feng Y: Snail is critical for tumor growth and metastasis of ovarian carcinoma. Int J Cancer. 126:2102–2111. 2010.PubMed/NCBI | |
De Craene B, Gilbert B, Stove C, Bruyneel E, van Roy F and Berx G: The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res. 65:6237–6244. 2005. View Article : Google Scholar : PubMed/NCBI | |
Zhang A, Chen G, Meng L, Wang Q, Hu W, Xi L, Gao Q, Wang S, Zhou J, Xu G, Meng L and Ma D: Antisense-Snail transfer inhibits tumor metastasis by inducing E-cadherin expression. Anticancer Res. 28:621–628. 2008.PubMed/NCBI | |
Smith BN, Burton LJ, Henderson V, Randle DD, Morton DJ, Smith BA, Taliaferro-Smith L, Nagappan P, Yates C, Zayzafoon M, et al: Snail promotes epithelial mesenchymal transition in breast cancer cells in part via activation of nuclear ERK2. PLoS One. 9:e1049872014. View Article : Google Scholar : PubMed/NCBI | |
Qian J, Liu H, Chen W, Wen K, Lu W, Huang C and Fu Z: Knockdown of Slug by RNAi inhibits the proliferation and invasion of HCT116 colorectal cancer cells. Mol Med Rep. 8:1055–1059. 2013. View Article : Google Scholar : PubMed/NCBI | |
Gu A, Jie Y, Yao Q, Zhang Y and Mingyan E: Slug is associated with tumor metastasis and angiogenesis in ovarian cancer. Reprod Sci. 24:291–299. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhao X, Sun B, Sun D, Liu T, Che N, Gu Q, Dong X, Li R, Liu Y and Li J: Slug promotes hepatocellular cancer cell progression by increasing sox2 and nanog expression. Oncol Rep. 33:149–156. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yu Y, Li L, Zheng Z, Chen S, Chen E and Hu Y: Long non-coding RNA linc00261 suppresses gastric cancer progression via promoting Slug degradation. J Cell Mol Med. 21:955–967. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang YP, Wang MZ, Luo YR, Shen Y and Wei ZX: Lentivirus-mediated shRNA interference targeting SLUG inhibits lung cancer growth and metastasis. Asian Pac J Cancer Prev. 13:4947–4951. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sun Y, Song GD, Sun N, Chen JQ and Yang SS: Slug overexpression induces stemness and promotes hepatocellular carcinoma cell invasion and metastasis. Oncol Lett. 7:1936–1940. 2014. View Article : Google Scholar : PubMed/NCBI | |
Toiyama Y, Yasuda H, Saigusa S, Tanaka K, Inoue Y, Goel A and Kusunoki M: Increased expression of Slug and Vimentin as novel predictive biomarkers for lymph node metastasis and poor prognosis in colorectal cancer. Carcinogenesis. 34:2548–2557. 2013. View Article : Google Scholar : PubMed/NCBI | |
Bai JW, Chen MN, Wei XL, Li YC, Lin HY, Chen M, Li JW, Du CW, Man K and Zhang GJ: The zinc-finger transcriptional factor Slug transcriptionally downregulates ERα by recruiting lysine-specific demethylase 1 in human breast cancer. Oncogenesis. 6:e3302017. View Article : Google Scholar : PubMed/NCBI | |
Chen H, Zhu G, Li Y, Padia RN, Dong Z, Pan ZK, Liu K and Huang S: Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res. 69:9228–9235. 2009. View Article : Google Scholar : PubMed/NCBI | |
Liang YJ, Wang QY, Zhou CX, Yin QQ, He M, Yu XT, Cao DX, Chen GQ, He JR and Zhao Q: MiR-124 targets Slug to regulate epithelial-mesenchymal transition and metastasis of breast cancer. Carcinogenesis. 34:713–722. 2013. View Article : Google Scholar : PubMed/NCBI | |
Paquette B, Baptiste C, Therriault H, Arguin G, Plouffe B and Lemay R: In vitro irradiation of basement membrane enhances the invasiveness of breast cancer cells. Br J Cancer. 97:1505–1512. 2007. View Article : Google Scholar : PubMed/NCBI | |
Young AGH and Bennewith KL: Ionizing radiation enhances breast tumor cell migration in vitro. Radiat Res. 188:381–391. 2017. View Article : Google Scholar : PubMed/NCBI | |
Rodman SN, Spence JM, Ronnfeldt TJ, Zhu Y, Solst SR, O'Neill RA, Allen BG, Guan X, Spitz DR and Fath MA: Enhancement of radiation response in breast cancer stem cells by inhibition of thioredoxin- and glutathione-dependent metabolism. Radiat Res. 186:385–395. 2016. View Article : Google Scholar : PubMed/NCBI | |
Du XL, Jiang T, Wen ZQ, Gao R, Cui M and Wang F: Silencing of heat shock protein 70 expression enhances radiotherapy efficacy and inhibits cell invasion in endometrial cancer cell line. Croat Med J. 50:143–150. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yanamandra N, Kondraganti S, Srinivasula SM, Gujrati M, Olivero WC, Dinh DH and Rao JS: Activation of caspase-9 with irradiation inhibits invasion and angiogenesis in SNB19 human glioma cells. Oncogene. 23:2339–2344. 2004. View Article : Google Scholar : PubMed/NCBI |