LIM-homeobox transcription factor 1, alpha (LMX1A) inhibits tumourigenesis, epithelial-mesenchymal transition and stem-like properties of epithelial ovarian cancer

Gynecologic Oncology

Volumn 128, Issue 3, 2013, Pages 475-482

  Chao, Tai Kuang ^a   Yo, Yi Te ^a,b   Liao, Yu Ping ^b   Wang, Yu Chi ^a   Su, Po Hsuan ^b   Huang, Tien Shuo ^a   Lai, Hung Cheng ^a,b  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

Chemosensitivity; Epigenetic; Epithelial ovarian cancer; LMX1A; Methylation; Stem cell

Indexed keywords

CISPLATIN; EPIRUBICIN; GEMCITABINE; LIM HOMEOBOX TRANSCRIPTION FACTOR 1 ALPHA; PACLITAXEL; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RECURRENCE; CANCER STAGING; CANCER SURVIVAL; CARCINOGENESIS; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CHEMOSENSITIVITY; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; OVARY CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE MICROARRAY; TUMOR DIFFERENTIATION; TUMOR SPHEROID; XENOTRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DNA METHYLATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; LIM-HOMEODOMAIN PROTEINS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84873713034     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2012.12.018     Document Type: Article

References (62)

1. C.N. Landen Jr., M.J. Birrer, and A.K. Sood Early events in the pathogenesis of epithelial ovarian cancer J Clin Oncol 26 2008 995 1005
2. R.F. Ozols, M.A. Bookman, D.C. Connolly, M.B. Daly, A.K. Godwin, and R.J. Schilder Focus on epithelial ovarian cancer Cancer Cell 5 2004 19 24
3. J. Menczer, A. Chetrit, and S. Sadetzki Uterine metastases in ovarian carcinoma: frequency and survival in women who underwent hysterectomy J Gynecol Oncol 21 2010 191 195
4. B. Park, S. Park, T.J. Kim, S.H. Ma, B.G. Kim, and Y.M. Kim Epidemiological characteristics of ovarian cancer in Korea J Gynecol Oncol 21 2010 241 247
5. S.S. Buys, E. Partridge, A. Black, C.C. Johnson, L. Lamerato, and C. Isaacs Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial JAMA 305 2011 2295 2303
6. C.K. Lin, T.K. Chao, C.P. Yu, M.H. Yu, and J.S. Jin The expression of six biomarkers in the four most common ovarian cancers: correlation with clinicopathological parameters APMIS 117 2009 162 175
7. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, and M.J. Thun Cancer statistics, 2009 CA Cancer J Clin 59 2009 225 249
8. R.J. Kurman, and Ie M. Shih Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm Hum Pathol 42 2011 918 931
9. Integrated genomic analyses of ovarian carcinoma Nature 474 2011 609 615
10. Y. Lee, A. Miron, R. Drapkin, M.R. Nucci, F. Medeiros, and A. Saleemuddin A candidate precursor to serous carcinoma that originates in the distal fallopian tube J Pathol 211 2007 26 35
11. K. Levanon, C. Crum, and R. Drapkin New insights into the pathogenesis of serous ovarian cancer and its clinical impact J Clin Oncol 26 2008 5284 5293
12. J.M. Piek, P.J. van Diest, R.P. Zweemer, J.W. Jansen, R.J. Poort-Keesom, and F.H. Menko Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer J Pathol 195 2001 451 456
13. B. Davidson, R. Reich, C.G. Trope, T.L. Wang, and Ie M. Shih New determinates of disease progression and outcome in metastatic ovarian carcinoma Histol Histopathol 25 2010 1591 1609
14. D. Hanahan, and R.A. Weinberg The hallmarks of cancer Cell 100 2000 57 70
15. M. Zeisberg, and E.G. Neilson Biomarkers for epithelial-mesenchymal transitions J Clin Invest 119 2009 1429 1437
16. E. Lengyel Ovarian cancer development and metastasis Am J Pathol 177 2010 1053 1064
17. N. Ahmed, E.W. Thompson, and M.A. Quinn Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm J Cell Physiol 213 2007 581 588
18. K. Sundfeldt Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule Mol Cell Endocrinol 202 2003 89 96
19. S. Elloul, I. Silins, C.G. Trope, A. Benshushan, B. Davidson, and R. Reich Expression of E-cadherin transcriptional regulators in ovarian carcinoma Virchows Arch 449 2006 520 528
20. J.P. Thiery, and J.P. Sleeman Complex networks orchestrate epithelial-mesenchymal transitions Nat Rev Mol Cell Biol 7 2006 131 142
21. N. Auersperg, A.S. Wong, K.C. Choi, S.K. Kang, and P.C. Leung Ovarian surface epithelium: biology, endocrinology, and pathology Endocr Rev 22 2001 255 288
22. S. Okamoto, A. Okamoto, T. Nikaido, M. Saito, M. Takao, and N. Yanaihara Mesenchymal to epithelial transition in the human ovarian surface epithelium focusing on inclusion cysts Oncol Rep 21 2009 1209 1214
23. D. Vergara, B. Merlot, J.P. Lucot, P. Collinet, D. Vinatier, and I. Fournier Epithelial-mesenchymal transition in ovarian cancer Cancer Lett 291 2010 59 66
24. S. Floor, W.C. van Staveren, D. Larsimont, J.E. Dumont, and C. Maenhaut Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating- cancer stem cells: distinct, overlapping or same populations Oncogene 30 2011 4609 4621
25. H.Y. Su, H.C. Lai, Y.W. Lin, Y.C. Chou, C.Y. Liu, and M.H. Yu An epigenetic marker panel for screening and prognostic prediction of ovarian cancer Int J Cancer 124 2009 387 393
26. H.C. Lai, Y.W. Lin, T.H. Huang, P. Yan, R.L. Huang, and H.C. Wang Identification of novel DNA methylation markers in cervical cancer Int J Cancer 123 2008 161 167
27. C.Y. Liu, T.K. Chao, P.H. Su, H.Y. Lee, Y.L. Shih, and H.Y. Su Characterization of LMX-1A as a metastasis suppressor in cervical cancer J Pathol 219 2009 222 231
28. O. Hobert, and H. Westphal Functions of LIM-homeobox genes Trends Genet 16 2000 75 83
29. M.T. Chung, H.C. Lai, H.K. Sytwu, M.D. Yan, Y.L. Shih, and C.C. Chang SFRP1 and SFRP2 suppress the transformation and invasion abilities of cervical cancer cells through Wnt signal pathway Gynecol Oncol 112 2009 646 653
30. H.Y. Su, H.C. Lai, Y.W. Lin, C.Y. Liu, C.K. Chen, and Y.C. Chou Epigenetic silencing of SFRP5 is related to malignant phenotype and chemoresistance of ovarian cancer through Wnt signaling pathway Int J Cancer 127 2010 555 567
31. X. Zi, Y. Guo, A.R. Simoneau, C. Hope, J. Xie, and R.F. Holcombe Expression of Frzb/secreted Frizzled-related protein 3, a secreted Wnt antagonist, in human androgen-independent prostate cancer PC-3 cells suppresses tumor growth and cellular invasiveness Cancer Res 65 2005 9762 9770
32. D.G. Rosen, X. Huang, M.T. Deavers, A. Malpica, E.G. Silva, and J. Liu Validation of tissue microarray technology in ovarian carcinoma Mod Pathol 17 2004 790 797
33. Y.C. Wang, Y.T. Yo, H.Y. Lee, Y.P. Liao, T.K. Chao, and P.H. Su ALDH1-bright epithelial ovarian cancer cells are associated with CD44 expression, drug resistance, and poor clinical outcome Am J Pathol 180 2012 1159 1169
34. M. Dean, T. Fojo, and S. Bates Tumour stem cells and drug resistance Nat Rev Cancer 5 2005 275 284
35. W. Yue, F. Jiao, B. Liu, J. You, and Q. Zhou Enrichment and function research of large cell lung cancer stem cell-like cells Zhongguo Fei Ai Za Zhi 14 2011 484 491
36. L.G. Hudson, R. Zeineldin, and M.S. Stack Phenotypic plasticity of neoplastic ovarian epithelium: unique cadherin profiles in tumor progression Clin Exp Metastasis 25 2008 643 655
37. R.C. Bast Jr., B. Hennessy, and G.B. Mills The biology of ovarian cancer: new opportunities for translation Nat Rev Cancer 9 2009 415 428
38. M.F. Paz, S. Wei, J.C. Cigudosa, S. Rodriguez-Perales, M.A. Peinado, and T.H. Huang Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases Hum Mol Genet 12 2003 2209 2219
39. W. Dong, L. Feng, Y. Xie, H. Zhang, and Y. Wu Hypermethylation-mediated reduction of LMX1A expression in gastric cancer Cancer Sci 102 2011 361 366
40. H.C. Lai, Y.W. Lin, R.L. Huang, M.T. Chung, H.C. Wang, and Y.P. Liao Quantitative DNA methylation analysis detects cervical intraepithelial neoplasms type 3 and worse Cancer 116 2010 4266 4274
41. K. Sugimachi, S. Tanaka, T. Kameyama, K. Taguchi, S. Aishima, and M. Shimada Transcriptional repressor snail and progression of human hepatocellular carcinoma Clin Cancer Res 9 2003 2657 2664
42. S.J. Grille, A. Bellacosa, J. Upson, A.J. Klein-Szanto, F. van Roy, and W. Lee-Kwon The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines Cancer Res 63 2003 2172 2178
43. M.J. Blanco, G. Moreno-Bueno, D. Sarrio, A. Locascio, A. Cano, and J. Palacios Correlation of Snail expression with histological grade and lymph node status in breast carcinomas Oncogene 21 2002 3241 3246
44. K.M. Hajra, D.Y. Chen, and E.R. Fearon The SLUG zinc-finger protein represses E-cadherin in breast cancer Cancer Res 62 2002 1613 1618
45. J. Yoshida, A. Horiuchi, N. Kikuchi, A. Hayashi, R. Osada, and S. Ohira Changes in the expression of E-cadherin repressors, Snail, Slug, SIP1, and Twist, in the development and progression of ovarian carcinoma: the important role of Snail in ovarian tumorigenesis and progression Med Mol Morphol 42 2009 82 91
46. Y. Takeyama, M. Sato, M. Horio, T. Hase, K. Yoshida, and T. Yokoyama Knockdown of ZEB1, a master epithelial-to-mesenchymal transition (EMT) gene, suppresses anchorage-independent cell growth of lung cancer cells Cancer Lett 296 2010 216 224
47. S. Chung, A. Leung, B.S. Han, M.Y. Chang, J.I. Moon, and C.H. Kim Wnt1-lmx1a forms a novel autoregulatory loop and controls midbrain dopaminergic differentiation synergistically with the SHH-FoxA2 pathway Cell Stem Cell 5 2009 646 658
48. R.F. Ozols, B.N. Bundy, B.E. Greer, J.M. Fowler, D. Clarke-Pearson, and R.A. Burger Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study J Clin Oncol 21 2003 3194 3200
49. G. Ferrandina, G. Bonanno, L. Pierelli, A. Perillo, A. Procoli, and A. Mariotti Expression of CD133-1 and CD133-2 in ovarian cancer Int J Gynecol Cancer 18 2008 506 514
50. S.A. Bapat, A.M. Mali, C.B. Koppikar, and N.K. Kurrey Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer Cancer Res 65 2005 3025 3029
51. P.P. Szotek, R. Pieretti-Vanmarcke, P.T. Masiakos, D.M. Dinulescu, D. Connolly, and R. Foster Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness Proc Natl Acad Sci U S A 103 2006 11154 11159
52. T. Baba, P.A. Convery, N. Matsumura, R.S. Whitaker, E. Kondoh, and T. Perry Epigenetic regulation of CD133 and tumorigenicity of CD133 + ovarian cancer cells Oncogene 28 2009 209 218
53. S. Zhang, C. Balch, M.W. Chan, H.C. Lai, D. Matei, and J.M. Schilder Identification and characterization of ovarian cancer-initiating cells from primary human tumors Cancer Res 68 2008 4311 4320
54. P.C. Hermann, S.L. Huber, T. Herrler, A. Aicher, J.W. Ellwart, and M. Guba Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer Cell Stem Cell 1 2007 313 323
55. A. Biddle, and I.C. Mackenzie Cancer stem cells and EMT in carcinoma Cancer Metastasis Rev 31 2012 285 293
56. T. Brabletz, A. Jung, S. Spaderna, F. Hlubek, and T. Kirchner Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression Nat Rev Cancer 5 2005 744 749
57. A. Biddle, X. Liang, L. Gammon, B. Fazil, L.J. Harper, and H. Emich Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative Cancer Res 71 2011 5317 5326
58. J.J. Christiansen, and A.K. Rajasekaran Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis Cancer Res 66 2006 8319 8326
59. A. Sanchez-Danes, A. Consiglio, Y. Richaud, I. Rodriguez-Piza, B. Dehay, and M. Edel Efficient generation of A9 midbrain dopaminergic neurons by lentiviral delivery of LMX1A in human embryonic stem cells and induced pluripotent stem cells Hum Gene Ther 23 1 2012 56 69
60. M. Hall, and G. Rustin Recurrent ovarian cancer: when and how to treat Curr Oncol Rep 13 2011 459 471
61. R.Y. Zang, P. Harter, D.S. Chi, J. Sehouli, R. Jiang, and C.G. Trope Predictors of survival in patients with recurrent ovarian cancer undergoing secondary cytoreductive surgery based on the pooled analysis of an international collaborative cohort Br J Cancer 105 2011 890 896
62. W.J. Tian, D.S. Chi, J. Sehouli, C.G. Trope, R. Jiang, and A. Ayhan A risk model for secondary cytoreductive surgery in recurrent ovarian cancer: an evidence-based proposal for patient selection Ann Surg Oncol 19 2012 597 604