EMT in cervical cancer: Its role in tumour progression and response to therapy

Cancer Letters

Volumn 356, Issue 2, 2015, Pages 321-331

  Qureshi, Rehana ^a   Arora, Himanshu ^b   Rizvi, M A ^a  

^a JAMIA MILLIA ISLAMIA CENTRAL UNIVERSITY   (India)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Cervical cancer; Epithelial Mesenchymal Transition; Mesenchymal transition (EMT); Oncogene; Therapeutics; Tumour suppressor

Indexed keywords

BIOLOGICAL MARKER; CARRIER PROTEINS AND BINDING PROTEINS; CELL PROTEIN; CITRATE SYNTHASE; CURCUMIN; CYTOSKELETON PROTEIN; EPHRIN RECEPTOR B2; FIBULIN 5; FLAVANOID; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; MICRORNA; MICRORNA 155; MICRORNA 361 5P; MORUSIN; NOGO B PROTEIN; ONCOPROTEIN; POTASSIUM CHLORIDE COTRANSPORTER 3; PROTEIN E6; PROTEIN E7; PROTEIN SAM68; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING ACIDIC COILED COIL PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT;

AEG 1 GENE; ANTINEOPLASTIC ACTIVITY; CANCER DIAGNOSIS; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RESISTANCE; CARCINOGENESIS; CELL HYPOXIA; DRUG MECHANISM; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; FUSED TOES HOMOLOG GENE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; LOW ENERGY RADIATION; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHORT SURVEY; TREATMENT RESPONSE; TUMOR GROWTH; UTERINE CERVIX CANCER; ANIMAL; CELL TRANSFORMATION; DISEASE COURSE; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; PATHOLOGY; SIGNAL TRANSDUCTION; UTERINE CERVICAL NEOPLASMS;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; SIGNAL TRANSDUCTION; UTERINE CERVICAL NEOPLASMS;

EID: 84919484112     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.09.021     Document Type: Review

References (166)

1. Samatov T.R., Tonevitsky A.G., Schumacher U. Epithelial-mesenchymal transition: focus on metastatic cascade, alternative splicing, non-coding RNAs and modulating compounds. Molecular cancer 2013, 12:107.
2. Kalluri R., Neilson E.G. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest 2003, 112:1776-1784.
3. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest 2009, 119:1420-1428.
4. Samavarchi-Tehrani P., Golipour A., David L., Sung H.K., Beyer T.A., Datti A., et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010, 7:64-77.
5. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
6. Lim J., Thiery J.P. Epithelial-mesenchymal transitions: insights from development. Development 2012, 139:3471-3486.
7. Zeisberg M., Kalluri R. Cellular mechanisms of tissue fibrosis. 1. Common and organ-specific mechanisms associated with tissue fibrosis. Am. J. Physiol. Cell Physiol 2013, 304:C216-C225.
8. Scheel C., Weinberg R.A. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin. Cancer Biol 2012, 22:396-403.
9. Huber M.A., Kraut N., Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol 2005, 17:548-558.
10. Lee J.M., Dedhar S., Kalluri R., Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol 2006, 172:973-981.
11. Tarin D., Thompson E.W., Newgreen D.F. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 2005, 65:5996-6000. discussion 6000-5991.
12. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2002, 2:442-454.
13. Tse J.C., Kalluri R. Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment. J. Cell. Biochem 2007, 101:816-829.
14. Polyak K., Weinberg R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 2009, 9:265-273.
15. Lamouille S., Xu J., Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol 2014, 15:178-196.
16. Lee M.Y., Chou C.Y., Tang M.J., Shen M.R. Epithelial-mesenchymal transition in cervical cancer: correlation with tumor progression, epidermal growth factor receptor overexpression, and snail up-regulation. Clin. Cancer Res 2008, 14:4743-4750.
17. Choo K.B., Huang C.J., Chen C.M., Han C.P., Au L.C. Jun-B oncogene aberrations in cervical cancer cell lines. Cancer Lett 1995, 93:249-253.
18. Ndubisi B., Sanz S., Lu L., Podczaski E., Benrubi G., Masood S. The prognostic value of HER-2/neu oncogene in cervical cancer. Ann. Clin. Lab. Sci 1997, 27:396-401.
19. Mehdi S.J., Alam M.S., Batra S., Rizvi M.M. Allelic loss of 6q25-27, the PARKIN tumor suppressor gene locus, in cervical carcinoma. Med. Oncol., 2011, 28:1520-1526.
20. Rizvi M.M., Alam M.S., Ali A., Mehdi S.J., Batra S., Mandal A.K. Aberrant promoter methylation and inactivation of PTEN gene in cervical carcinoma from Indian population. J. Cancer Res. Clin. Oncol 2011, 137:1255-1262.
21. Alam M.S., Ali A., Mehdi S.J., Alyasiri N.S., Kazim Z., Batra S., et al. HPV typing and its relation with apoptosis in cervical carcinoma from Indian population. Tumour Biol 2012, 33:17-22.
22. Rughooputh S., Manraj S., Eddoo R., Greenwell P. Expression of the c-myc oncogene and the presence of HPV 18: possible surrogate markers for cervical cancer?. Br. J. Biomed. Sci 2009, 66:74-78.
23. de Villiers E.M., Fauquet C., Broker T.R., Bernard H.U., zur Hausen H. Classification of papillomaviruses. Virology 2004, 324:17-27.
24. O'Connor T.E., West W.H., Marshall G.D., Orr D.W., Lewis M., Oldham R.K. Principles of biotherapy and its application to the treatment of disseminated renal cancer. Semin. Surg. Oncol 1988, 4:155-160.
25. Walboomers J.M., Jacobs M.V., Manos M.M., Bosch F.X., Kummer J.A., Shah K.V., et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol 1999, 189:12-19.
26. Cheng Y.M., Chou C.Y., Hsu Y.C., Chen M.J., Wing L.Y. The role of human papillomavirus type 16 E6/E7 oncoproteins in cervical epithelial-mesenchymal transition and carcinogenesis. Oncol. Lett 2012, 3:667-671.
27. Duffy C.L., Phillips S.L., Klingelhutz A.J. Microarray analysis identifies differentiation-associated genes regulated by human papillomavirus type 16 E6. Virology 2003, 314:196-205.
28. Kang D.C., Su Z.Z., Sarkar D., Emdad L., Volsky D.J., Fisher P.B. Cloning and characterization of HIV-1-inducible astrocyte elevated gene-1, AEG-1. Gene 2005, 353:8-15.
29. Yoo B.K., Emdad L., Su Z.Z., Villanueva A., Chiang D.Y., Mukhopadhyay N.D., et al. Astrocyte elevated gene-1 regulates hepatocellular carcinoma development and progression. J. Clin. Invest 2009, 119:465-477.
30. Yu C., Chen K., Zheng H., Guo X., Jia W., Li M., et al. Overexpression of astrocyte elevated gene-1 (AEG-1) is associated with esophageal squamous cell carcinoma (ESCC) progression and pathogenesis. Carcinogenesis 2009, 30:894-901.
31. Emdad L., Sarkar D., Su Z.Z., Randolph A., Boukerche H., Valerie K., et al. Activation of the nuclear factor kappaB pathway by astrocyte elevated gene-1: implications for tumor progression and metastasis. Cancer Res 2006, 66:1509-1516.
32. Long M., Dong K., Gao P., Wang X., Liu L., Yang S., et al. Overexpression of astrocyte-elevated gene-1 is associated with cervical carcinoma progression and angiogenesis. Oncol. Rep 2013, 30:1414-1422.
33. Liu X., Wang D., Liu H., Feng Y., Zhu T., Zhang L., et al. Knockdown of astrocyte elevated gene-1 (AEG-1) in cervical cancer cells decreases their invasiveness, epithelial to mesenchymal transition, and chemoresistance. Cell Cycle 2014, 13:1702-1707.
34. Ha G.H., Kim J.L., Breuer E.K. Transforming acidic coiled-coil proteins (TACCs) in human cancer. Cancer Lett 2013, 336:24-33.
35. Ha G.H., Kim J.L., Breuer E.K. TACC3 is essential for EGF-mediated EMT in cervical cancer. PLoS ONE 2013, 8:e70353.
36. Zhu K., Chen L., Han X., Wang J., Wang J. Short hairpin RNA targeting Twist1 suppresses cell proliferation and improves chemosensitivity to cisplatin in HeLa human cervical cancer cells. Oncol. Rep 2012, 27:1027-1034.
37. Yan S., Wang Y., Yang Q., Li X., Kong X., Zhang N., et al. Low-dose radiation-induced epithelial-mesenchymal transition through NF-kappaB in cervical cancer cells. Int. J. Oncol 2013, 42:1801-1806.
38. Lei C., Wang Y., Huang Y., Yu H., Huang Y., Wu L., et al. Up-regulated miR155 reverses the epithelial-mesenchymal transition induced by EGF and increases chemo-sensitivity to cisplatin in human Caski cervical cancer cells. PLoS ONE 2012, 7:e52310.
39. Lukong K.E., Richard S. Sam68, the KH domain-containing superSTAR. Biochim. Biophys. Acta 2003, 1653:73-86.
40. Lin Q., Taylor S.J., Shalloway D. Specificity and determinants of Sam68 RNA binding. Implications for the biological function of K homology domains. J. Biol. Chem 1997, 272:27274-27280.
41. Busa R., Paronetto M.P., Farini D., Pierantozzi E., Botti F., Angelini D.F., et al. The RNA-binding protein Sam68 contributes to proliferation and survival of human prostate cancer cells. Oncogene 2007, 26:4372-4382.
42. Song L., Wang L., Li Y., Xiong H., Wu J., Li J., et al. Sam68 up-regulation correlates with, and its down-regulation inhibits, proliferation and tumourigenicity of breast cancer cells. J. Pathol 2010, 222:227-237.
43. Zhang Z., Li J., Zheng H., Yu C., Chen J., Liu Z., et al. Expression and cytoplasmic localization of SAM68 is a significant and independent prognostic marker for renal cell carcinoma. Cancer Epidemiol. Biomarkers Prev 2009, 18:2685-2693.
44. Li Z., Yu C.P., Zhong Y., Liu T.J., Huang Q.D., Zhao X.H., et al. Sam68 expression and cytoplasmic localization is correlated with lymph node metastasis as well as prognosis in patients with early-stage cervical cancer. Ann. Oncol 2012, 23:638-646.
45. Cinghu S., Anandharaj A., Lee H.C., Yu J.R., Park W.Y. FTS (fused toes homolog) a novel oncoprotein involved in uterine cervical carcinogenesis and a potential diagnostic marker for cervical cancer. J. Cell. Physiol 2011, 226:1564-1572.
46. Muthusami S., Prabakaran D.S., Yu J.R., Park W.Y. EGF-induced expression of Fused Toes Homolog (FTS) facilitates epithelial-mesenchymal transition and promotes cell migration in ME180 cervical cancer cells. Cancer Lett 2014.
47. Liu C.Y., Chao T.K., Su P.H., Lee H.Y., Shih Y.L., Su H.Y., et al. Characterization of LMX-1A as a metastasis suppressor in cervical cancer. J. Pathol 2009, 219:222-231.
48. Chang B., Kim J., Jeong D., Jeong Y., Jeon S., Jung S.I., et al. Klotho inhibits the capacity of cell migration and invasion in cervical cancer. Oncol. Rep 2012, 28:1022-1028.
49. Li J., Zhou B.P. Activation of beta-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer 2011, 11:49.
50. Lin C.Y., Tsai P.H., Kandaswami C.C., Lee P.P., Huang C.J., Hwang J.J., et al. Matrix metalloproteinase-9 cooperates with transcription factor Snail to induce epithelial-mesenchymal transition. Cancer Sci 2011, 102:815-827.
51. Miao J.W., Liu L.J., Huang J. Interleukin-6-induced epithelial-mesenchymal transition through signal transducer and activator of transcription 3 in human cervical carcinoma. Int. J. Oncol 2014, 45:165-176.
52. Lin C.C., Cheng T.L., Tsai W.H., Tsai H.J., Hu K.H., Chang H.C., et al. Loss of the respiratory enzyme citrate synthase directly links the Warburg effect to tumor malignancy. Sci. Rep 2012, 2:785.
53. Hiramoto T., Oka T., Yoshihara K., Kubo C. Pyrogenic cytokines did not mediate a stress interview-induced hyperthermic response in a patient with psychogenic fever: a case report. Psychosom. Med 2009, 71:932-936.
54. Nakada M., Hayashi Y., Hamada J. Role of Eph/ephrin tyrosine kinase in malignant glioma. Neuro-Oncol 2011, 13:1163-1170.
55. Kullander K., Klein R. Mechanisms and functions of Eph and ephrin signalling. Nat. Rev. Mol. Cell Biol 2002, 3:475-486.
56. Nakada M., Niska J.A., Miyamori H., McDonough W.S., Wu J., Sato H., et al. The phosphorylation of EphB2 receptor regulates migration and invasion of human glioma cells. Cancer Res 2004, 64:3179-3185.
57. Nakada M., Niska J.A., Tran N.L., McDonough W.S., Berens M.E. EphB2/R-Ras signaling regulates glioma cell adhesion, growth, and invasion. Am. J. Pathol 2005, 167:565-576.
58. Gao Q., Liu W., Cai J., Li M., Gao Y., Lin W., et al. EphB2 promotes cervical cancer progression by inducing epithelial-mesenchymal transition. Hum. Pathol 2014, 45:372-381.
59. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
60. Mayer A., Hockel M., Schlischewsky N., Schmidberger H., Horn L.C., Vaupel P. Lacking hypoxia-mediated downregulation of E-cadherin in cancers of the uterine cervix. Br. J. Cancer 2013, 108:402-408.
61. Wilson W.R., Hay M.P. Targeting hypoxia in cancer therapy. Nat. Rev. Cancer 2011, 11:393-410.
62. Yang X., Li S., Li W., Chen J., Xiao X., Wang Y., et al. Inactivation of lysyl oxidase by beta-aminopropionitrile inhibits hypoxia-induced invasion and migration of cervical cancer cells. Oncol. Rep 2013, 29:541-548.
63. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
64. Burk U., Schubert J., Wellner U., Schmalhofer O., Vincan E., Spaderna S., et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008, 9:582-589.
65. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol 2008, 10:593-601.
66. Korpal M., Lee E.S., Hu G., Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem 2008, 283:14910-14914.
67. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008, 22:894-907.
68. Long M.J., Wu F.X., Li P., Liu M., Li X., Tang H. MicroRNA-10a targets CHL1 and promotes cell growth, migration and invasion in human cervical cancer cells. Cancer Lett 2012, 324:186-196.
69. Xu X.M., Wang X.B., Chen M.M., Liu T., Li Y.X., Jia W.H., et al. MicroRNA-19a and -19b regulate cervical carcinoma cell proliferation and invasion by targeting CUL5. Cancer Lett 2012, 322:148-158.
70. Wu X., Xi X., Yan Q., Zhang Z., Cai B., Lu W., et al. MicroRNA-361-5p facilitates cervical cancer progression through mediation of epithelial-to-mesenchymal transition. Med. Oncol 2013, 30:751.
71. Lee M.Y., Shen M.R. Epithelial-mesenchymal transition in cervical carcinoma. Am. J. Transl. Res 2012, 4:1-13.
72. Brabec V., Kasparkova J. Molecular aspects of resistance to antitumor platinum drugs. Drug Resist. Updat 2002, 5:147-161.
73. Djeu J.Y., Wei S. Clusterin and chemoresistance. Adv. Cancer Res 2009, 105:77-92.
74. Yamamoto N., Kinoshita T., Nohata N., Yoshino H., Itesako T., Fujimura L., et al. Tumor-suppressive microRNA-29a inhibits cancer cell migration and invasion via targeting HSP47 in cervical squamous cell carcinoma. Int. J. Oncol 2013, 43:1855-1863.
75. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 2007, 7:415-428.
76. Liao H., Duka T., Teng F.Y., Sun L., Bu W.Y., Ahmed S., et al. Nogo-66 and myelin-associated glycoprotein (MAG) inhibit the adhesion and migration of Nogo-66 receptor expressing human glioma cells. J. Neurochem 2004, 90:1156-1162.
77. Su Z., Cao L., Zhu Y., Liu X., Huang Z., Huang A., et al. Nogo enhances the adhesion of olfactory ensheathing cells and inhibits their migration. J. Cell Sci 2007, 120:1877-1887.
78. Miao R.Q., Gao Y., Harrison K.D., Prendergast J., Acevedo L.M., Yu J., et al. Identification of a receptor necessary for Nogo-B stimulated chemotaxis and morphogenesis of endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10997-11002.
79. Xiao W., Zhou S., Xu H., Li H., He G., Liu Y., et al. Nogo-B promotes the epithelial-mesenchymal transition in HeLa cervical cancer cells via Fibulin-5. Oncol. Rep 2013, 29:109-116.
80. Nakamura T., Lozano P.R., Ikeda Y., Iwanaga Y., Hinek A., Minamisawa S., et al. Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature 2002, 415:171-175.
81. Nakamura T., Ruiz-Lozano P., Lindner V., Yabe D., Taniwaki M., Furukawa Y., et al. DANCE, a novel secreted RGD protein expressed in developing, atherosclerotic, and balloon-injured arteries. J. Biol. Chem 1999, 274:22476-22483.
82. 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, 119:1438-1449.
83. Moustakas A., Heldin C.H. Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 2007, 98:1512-1520.
84. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr. Opin. Cell Biol 2004, 16:14-23.
85. Shagieva G.S., Domnina L.V., Chipysheva T.A., Ermilova V.D., Chaponnier C., Dugina V.B. Actin isoforms and reorganization of adhesion junctions in epithelial-to-mesenchymal transition of cervical carcinoma cells. Biochemistry (Mosc) 2012, 77:1266-1276.
86. Colomiere M., Ward A.C., Riley C., Trenerry M.K., Cameron-Smith D., Findlay J., et al. Cross talk of signals between EGFR and IL-6R through JAK2/STAT3 mediate epithelial-mesenchymal transition in ovarian carcinomas. Br. J. Cancer 2009, 100:134-144.
87. Sullivan N.J., Sasser A.K., Axel A.E., Vesuna F., Raman V., Ramirez N., et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009, 28:2940-2947.
88. Wang J., Ou J., Guo Y., Dai T., Li X., Liu J., et al. TBLR1 is a novel prognostic marker and promotes epithelial-mesenchymal transition in cervical cancer. Br. J. Cancer 2014, 111:112-124.
89. Lai H.C., Lin Y.W., Huang T.H., Yan P., Huang R.L., Wang H.C., et al. Identification of novel DNA methylation markers in cervical cancer. Int. J. Cancer 2008, 123:161-167.
90. Chung M.T., Sytwu H.K., Yan M.D., Shih Y.L., Chang C.C., Yu M.H., et al. Promoter methylation of SFRPs gene family in cervical cancer. Gynecol. Oncol 2009, 112:301-306.
91. Chung M.T., Lai H.C., Sytwu H.K., Yan M.D., Shih Y.L., Chang C.C., et al. SFRP1 and SFRP2 suppress the transformation and invasion abilities of cervical cancer cells through Wnt signal pathway. Gynecol. Oncol 2009, 112:646-653.
92. King G.D., Rosene D.L., Abraham C.R. Promoter methylation and age-related downregulation of Klotho in rhesus monkey. Age (Omaha) 2012, 34:1405-1419.
93. Lee J., Jeong D.J., Kim J., Lee S., Park J.H., Chang B., et al. The anti-aging gene KLOTHO is a novel target for epigenetic silencing in human cervical carcinoma. Mol. Cancer 2010, 9:109.
94. Pan J., Zhong J., Gan L.H., Chen S.J., Jin H.C., Wang X., et al. Klotho, an anti-senescence related gene, is frequently inactivated through promoter hypermethylation in colorectal cancer. Tumour Biol 2011, 32:729-735.
95. Wang L., Wang X., Wang X., Jie P., Lu H., Zhang S., et al. Klotho is silenced through promoter hypermethylation in gastric cancer. Am J. Cancer Res 2011, 1:111-119.
96. Liu H., Fergusson M.M., Castilho R.M., Liu J., Cao L., Chen J., et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science 2007, 317:803-806.
97. Gergely F., Karlsson C., Still I., Cowell J., Kilmartin J., Raff J.W. The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc. Natl Acad. Sci. U.S.A. 2000, 97:14352-14357.
98. O'Brien L.L., Albee A.J., Liu L., Tao W., Dobrzyn P., Lizarraga S.B., et al. The Xenopus TACC homologue, maskin, functions in mitotic spindle assembly. Mol. Biol. Cell 2005, 16:2836-2847.
99. Gergely F., Draviam V.M., Raff J.W. The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 2003, 17:336-341.
100. Lee M.J., Gergely F., Jeffers K., Peak-Chew S.Y., Raff J.W. Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat. Cell Biol 2001, 3:643-649.
101. Sadek C.M., Pelto-Huikko M., Tujague M., Steffensen K.R., Wennerholm M., Gustafsson J.A. TACC3 expression is tightly regulated during early differentiation. Gene Expr. Patterns 2003, 3:203-211.
102. Schneider L., Essmann F., Kletke A., Rio P., Hanenberg H., Wetzel W., et al. The transforming acidic coiled coil 3 protein is essential for spindle-dependent chromosome alignment and mitotic survival. J. Biol. Chem 2007, 282:29273-29283.
103. Piekorz R.P., Hoffmeyer A., Duntsch C.D., McKay C., Nakajima H., Sexl V., et al. The centrosomal protein TACC3 is essential for hematopoietic stem cell function and genetically interfaces with p53-regulated apoptosis. EMBO J. 2002, 21.
104. Ha G.H., Park J.S., Breuer E.K. TACC3 promotes epithelial-mesenchymal transition (EMT) through the activation of PI3K/Akt and ERK signaling pathways. Cancer Lett 2013, 332:63-73.
105. Shen M.R., Chou C.Y., Hsu K.F., Hsu Y.M., Chiu W.T., Tang M.J., et al. KCl cotransport is an important modulator of human cervical cancer growth and invasion. J. Biol. Chem 2003, 278:39941-39950.
106. Hsu Y.M., Chen Y.F., Chou C.Y., Tang M.J., Chen J.H., Wilkins R.J., et al. KCl cotransporter-3 down-regulates E-cadherin/beta-catenin complex to promote epithelial-mesenchymal transition. Cancer Res 2007, 67:11064-11073.
107. Behrens J. Cadherins and catenins: role in signal transduction and tumor progression. Cancer Metastasis Rev 1999, 18:15-30.
108. Schiffman M., Wentzensen N., Wacholder S., Kinney W., Gage J.C., Castle P.E. Human papillomavirus testing in the prevention of cervical cancer. J. Natl Cancer Inst 2011, 103:368-383.
109. Lamouille S., Derynck R. Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J. Cell Biol 2007, 178:437-451.
110. Zavadil J., Bottinger E.P. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005, 24:5764-5774.
111. Chopra V., Dinh T.V., Hannigan E.V. Circulating serum levels of cytokines and angiogenic factors in patients with cervical cancer. Cancer Invest 1998, 16:152-159.
112. Comerci J.T., Runowicz C.D., Flanders K.C., De Victoria C., Fields A.L., Kadish A.S., et al. Altered expression of transforming growth factor-beta 1 in cervical neoplasia as an early biomarker in carcinogenesis of the uterine cervix. Cancer 1996, 77:1107-1114.
113. Kloth J.N., Fleuren G.J., Oosting J., de Menezes R.X., Eilers P.H., Kenter G.G., et al. Substantial changes in gene expression of Wnt, MAPK and TNFalpha pathways induced by TGF-beta1 in cervical cancer cell lines. Carcinogenesis 2005, 26:1493-1502.
114. Yi J.Y., Hur K.C., Lee E., Jin Y.J., Arteaga C.L., Son Y.S. TGFbeta1 -mediated epithelial to mesenchymal transition is accompanied by invasion in the SiHa cell line. Eur. J. Cell Biol 2002, 81:457-468.
115. Bourboulia D., Stetler-Stevenson W.G. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion. Semin. Cancer Biol 2010, 20:161-168.
116. Katz B.Z. Adhesive interactions: the multi-task biochemical toolbox of cancer cells. Semin. Cancer Biol 2010, 20:125-127.
117. Orlichenko L.S., Radisky D.C. Matrix metalloproteinases stimulate epithelial-mesenchymal transition during tumor development. Clin. Exp. Metastasis 2008, 25:593-600.
118. Dhasarathy A., Phadke D., Mav D., Shah R.R., Wade P.A. The transcription factors Snail and Slug activate the transforming growth factor-beta signaling pathway in breast cancer. PLoS ONE 2011, 6:e26514.
119. Haslehurst A.M., Koti M., Dharsee M., Nuin P., Evans K., Geraci J., et al. EMT transcription factors snail and slug directly contribute to cisplatin resistance in ovarian cancer. BMC Cancer 2012, 12:91.
120. Kurrey N.K., Jalgaonkar S.P., Joglekar A.V., Ghanate A.D., Chaskar P.D., Doiphode R.Y., et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 2009, 27:2059-2068.
121. Kurrey N.K., K A., Bapat S.A. Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol. Oncol 2005, 97:155-165.
122. Mikami S., Katsube K., Oya M., Ishida M., Kosaka T., Mizuno R., et al. Expression of Snail and Slug in renal cell carcinoma: e-cadherin repressor Snail is associated with cancer invasion and prognosis. Lab. Invest 2011, 91:1443-1458.
123. Wu Y., Zhou B.P. Snail: more than EMT. Cell Adhes. Migr 2010, 4:199-203.
124. Drake J.M., Strohbehn G., Bair T.B., Moreland J.G., Henry M.D. ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells. Mol. Biol. Cell 2009, 20:2207-2217.
125. Hurt E.M., Saykally J.N., Anose B.M., Kalli K.R., Sanders M.M. Expression of the ZEB1 (deltaEF1) transcription factor in human: additional insights. Mol. Cell. Biochem 2008, 318:89-99.
126. Singh M., Spoelstra N.S., Jean A., Howe E., Torkko K.C., Clark H.R., et al. ZEB1 expression in type I vs type II endometrial cancers: a marker of aggressive disease. Modern Pathol 2008, 21:912-923.
127. Chen Z., Li S., Huang K., Zhang Q., Wang J., Li X., et al. The nuclear protein expression levels of SNAI1 and ZEB1 are involved in the progression and lymph node metastasis of cervical cancer via the epithelial-mesenchymal transition pathway. Hum. Pathol 2013, 44:2097-2105.
128. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
129. Li Y., Wang W., Wang W., Yang R., Wang T., Su T., et al. Correlation of TWIST2 up-regulation and epithelial-mesenchymal transition during tumorigenesis and progression of cervical carcinoma. Gynecol. Oncol 2012, 124:112-118.
130. Li Q.Q., Xu J.D., Wang W.J., Cao X.X., Chen Q., Tang F., et al. Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clin. Cancer Res 2009, 15:2657-2665.
131. Wang X., Ling M.T., Guan X.Y., Tsao S.W., Cheung H.W., Lee D.T., et al. Identification of a novel function of TWIST, a bHLH protein, in the development of acquired taxol resistance in human cancer cells. Oncogene 2004, 23:474-482.
132. Wang T., Li Y., Wang W., Tuerhanjiang A., Wu Z., Yang R., et al. Twist2, the key Twist isoform related to prognosis, promotes invasion of cervical cancer by inducing epithelial-mesenchymal transition and blocking senescence. Hum. Pathol 2014.
133. Shibata K., Kajiyama H., Ino K., Terauchi M., Yamamoto E., Nawa A., et al. Twist expression in patients with cervical cancer is associated with poor disease outcome. Ann. Oncol 2008, 19:81-85.
134. Honjo T. The shortest path from the surface to the nucleus: RBP-J kappa/Su(H) transcription factor. Genes Cells 1996, 1:1-9.
135. Veeraraghavalu K., Subbaiah V.K., Srivastava S., Chakrabarti O., Syal R., Krishna S. Complementation of human papillomavirus type 16 E6 and E7 by Jagged1-specific Notch1-phosphatidylinositol 3-kinase signaling involves pleiotropic oncogenic functions independent of CBF1;Su(H);Lag-1 activation. J. Virol 2005, 79:7889-7898.
136. Srivastava S., Ramdass B., Nagarajan S., Rehman M., Mukherjee G., Krishna S. Notch1 regulates the functional contribution of RhoC to cervical carcinoma progression. Br. J. Cancer 2010, 102:196-205.
137. Shimono Y., Zabala M., Cho R.W., Lobo N., Dalerba P., Qian D., et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009, 138:592-603.
138. Alison M.R., Lin W.R., Lim S.M., Nicholson L.J. Cancer stem cells: in the line of fire. Cancer Treat. Rev 2012, 38:589-598.
139. Liu X.F., Yang W.T., Xu R., Liu J.T., Zheng P.S. Cervical cancer cells with positive Sox2 expression exhibit the properties of cancer stem cells. PLoS ONE 2014, 9:e87092.
140. Chun K.H., Kosmeder J.W., Sun S., Pezzuto J.M., Lotan R., Hong W.K., et al. Effects of deguelin on the phosphatidylinositol 3-kinase/Akt pathway and apoptosis in premalignant human bronchial epithelial cells. J. Natl. Cancer Inst 2003, 95:291-302.
141. Hatcher H., Planalp R., Cho J., Torti F.M., Torti S.V. Curcumin: from ancient medicine to current clinical trials. Cell. Mol. Life Sci 2008, 65:1631-1652.
142. Chen C.L., Liu S.S., Ip S.M., Wong L.C., Ng T.Y., Ngan H.Y. E-cadherin expression is silenced by DNA methylation in cervical cancer cell lines and tumours. Eur. J. Cancer 2003, 39:517-523.
143. Shin D.Y., Lee W.S., Kim S.H., Kim M.J., Yun J.W., Lu J.N., et al. Anti-invasive activity of anthocyanins isolated from Vitis coignetiae in human hepatocarcinoma cells. J. Med. Food 2009, 12:967-972.
144. Shin D.Y., Ryu C.H., Lee W.S., Kim D.C., Kim S.H., Hah Y.S., et al. Induction of apoptosis and inhibition of invasion in human hepatoma cells by anthocyanins from meoru. Ann. N. Y. Acad. Sci 2009, 1171:137-148.
145. Shin D.Y., Lee W.S., Lu J.N., Kang M.H., Ryu C.H., Kim G.Y., et al. Induction of apoptosis in human colon cancer HCT-116 cells by anthocyanins through suppression of Akt and activation of p38-MAPK. Int. J. Oncol 2009, 35:1499-1504.
146. Aggarwal S., Ichikawa H., Takada Y., Sandur S.K., Shishodia S., Aggarwal B.B. Curcumin (diferuloylmethane) down-regulates expression of cell proliferation and antiapoptotic and metastatic gene products through suppression of IkappaBalpha kinase and Akt activation. Mol. Pharmacol 2006, 69:195-206.
147. Schmidt E.V. The role of c-myc in regulation of translation initiation. Oncogene 2004, 23:3217-3221.
148. Wu Y., Zhou B.P. TNF-alpha/NF-kappaB/Snail pathway in cancer cell migration and invasion. Br. J. Cancer 2010, 102:639-644.
149. Rangaswami H., Bulbule A., Kundu G.C. Nuclear factor-inducing kinase plays a crucial role in osteopontin-induced MAPK/IkappaBalpha kinase-dependent nuclear factor kappaB-mediated promatrix metalloproteinase-9 activation. J. Biol. Chem 2004, 279:38921-38935.
150. Lu J.N., Lee W.S., Yun J.W., Kim M.J., Kim H.J., Kim D.C., et al. Anthocyanins from Vitis coignetiae Pulliat inhibit cancer invasion and epithelial-mesenchymal transition, but these effects can be attenuated by tumor necrosis factor in human uterine cervical cancer HeLa cells. Evid. Based Complement. Alternat. Med 2013, 2013:503043.
151. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006, 66:9339-9344.
152. Gilbert C.A., Ross A.H. Cancer stem cells: cell culture, markers, and targets for new therapies. J. Cell. Biochem 2009, 108:1031-1038.
153. Hu Y., Fu L. Targeting cancer stem cells: a new therapy to cure cancer patients. Am. J. Cancer Res 2012, 2:340-356.
154. Dat N.T., Binh P.T., Quynh le T.P., Van Minh C., Huong H.T., Lee J.J. Cytotoxic prenylated flavonoids from Morus alba. Fitoterapia 2010, 81:1224-1227.
155. Lee J.C., Won S.J., Chao C.L., Wu F.L., Liu H.S., Ling P., et al. Morusin induces apoptosis and suppresses NF-kappaB activity in human colorectal cancer HT-29 cells. Biochem. Biophys. Res. Commun 2008, 372:236-242.
156. Wang L., Guo H., Yang L., Dong L., Lin C., Zhang J., et al. Morusin inhibits human cervical cancer stem cell growth and migration through attenuation of NF-kappaB activity and apoptosis induction. Mol. Cell. Biochem 2013, 379:7-18.
157. Noordhuis M.G., Fehrmann R.S., Wisman G.B., Nijhuis E.R., van Zanden J.J., Moerland P.D., et al. Involvement of the TGF-beta and beta-catenin pathways in pelvic lymph node metastasis in early-stage cervical cancer. Clin. Cancer Res 2011, 17:1317-1330.
158. Chen Y., Zhang L., Tian J., Fu X., Ren X., Hao Q. Significance of the absolute number and ratio of metastatic lymph nodes in predicting postoperative survival for the International Federation of Gynecology and Obstetrics stage IA2 to IIA cervical cancer. Int. J. Gynecol. Cancer 2013, 23:157-163.
159. Kodama J., Seki N., Masahiro S., Kusumoto T., Nakamura K., Hongo A., et al. Prognostic factors in stage IB-IIB cervical adenocarcinoma patients treated with radical hysterectomy and pelvic lymphadenectomy. J. Surg. Oncol 2010, 101:413-417.
160. Kersemaekers A.M., Fleuren G.J., Kenter G.G., Van den Broek L.J., Uljee S.M., Hermans J., et al. Oncogene alterations in carcinomas of the uterine cervix: overexpression of the epidermal growth factor receptor is associated with poor prognosis. Clin. Cancer Res 1999, 5:577-586.
161. Muthusami S., Prabakaran D.S., Yu J.R., Park W.Y. EGF-induced expression of Fused Toes Homolog (FTS) facilitates epithelial-mesenchymal transition and promotes cell migration in ME180 cervical cancer cells. Cancer Lett 2014, 351:252-259.
162. Parkin D.M., Bray F., Ferlay J., Pisani P. Estimating the world cancer burden: Globocan 2000. Int. J. Cancer 2001, 94:153-156.
163. Yim E.K., Tong S.Y., Ho E.M., Bae J.H., Um S.J., Park J.S. Anticancer effects on TACC3 by treatment of paclitaxel in HPV-18 positive cervical carcinoma cells. Oncol Rep 2009, 21:549-557.
164. Zhao W., Zhou Y., Xu H., Cheng Y., Kong B. Snail family proteins in cervical squamous carcinoma: expression and significance. Clinical and investigative medicine. Medecine clinique et experimentale 2013, 36:E223-E233.
165. Wang L., Guo H., Yang L., Dong L., Lin C., Zhang J., et al. Morusin inhibits human cervical cancer stem cell growth and migration through attenuation of NF-kappaB activity and apoptosis induction. Molecular and cellular biochemistry 2013, 379:7-18.
166. Rubinek T., et al. Epigenetic silencing of the tumor suppressor klotho in human breast cancer. Breast Cancer Res. Treat 2012, 133(2):649-657. 10.1007/s10549-011-1824-4.