ZEB1 in pancreatic Cancer

Cancers

Volumn 2, Issue 3, 2010, Pages 1617-1628

  Wellner, Ulrich ^a   Brabletz, Thomas ^a   Keck, Tobias ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

EMT; MCSC; Pancreatic cancer; ZEB1

Indexed keywords

CISPLATIN; FLUOROURACIL; GEMCITABINE; K RAS PROTEIN; MICRORNA; MICRORNA 200; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN;

BIOLOGICAL ACTIVITY; CANCER INVASION; CANCER RESISTANCE; CANCER STEM CELL; CELL DIFFERENTIATION; DISTANT METASTASIS; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; LOCAL METASTASIS; MULTIDRUG RESISTANCE; NEGATIVE FEEDBACK; NONHUMAN; PANCREAS CANCER; PROTEIN RNA BINDING; REVIEW; STRUCTURE ACTIVITY RELATION; TISSUE DISTRIBUTION;

EID: 79952261223     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers2031617     Document Type: Review

References (59)

1. Kalluri, R.; Weinberg, R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119, 1420-1428.
2. Polyak, K.; Weinberg, R.A. Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits. Nat. Rev. 2009, 9, 265-273.
3. Greenburg, G.; Hay, E.D. Epithelia suspended in collagen gels can lose polarity and express characteristics of migrating mesenchymal cells. J. Cell Biol. 1982, 95, 333-339.
4. Hay, E.D. An overview of epithelio-mesenchymal transformation. Acta Anatomica 1995, 154, 8-20.
5. Thiery, J.P.; Acloque, H.; Huang, R.Y.; Nieto, M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139, 871-890.
6. Thiery, J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. 2002, 2, 442-454.
7. Remacle, J.E.; Kraft, H.; Lerchner, W.; Wuytens, G.; Collart, C.; Verschueren, K.; Smith, J.C.; Huylebroeck, D. New mode of DNA binding of multi-zinc finger transcription factors: Deltaef1 family members bind with two hands to two target sites. EMBO J. 1999, 18, 5073-5084.
8. Long, J.; Zuo, D.; Park, M. Pc2-mediated sumoylation of smad-interacting protein 1 attenuates transcriptional repression of e-cadherin. J. Biol. Chem. 2005, 280, 35477-35489.
9. Postigo, A.A. Opposing functions of zeb proteins in the regulation of the tgfbeta/bmp signaling pathway. EMBO J. 2003, 22, 2443-2452.
10. van Grunsven, L.A.; Michiels, C.; Van de Putte, T.; Nelles, L.; Wuytens, G.; Verschueren, K.; Huylebroeck, D. Interaction between smad-interacting protein-1 and the corepressor c-terminal binding protein is dispensable for transcriptional repression of e-cadherin. J. Biol. Chem. 2003, 278, 26135-26145.
11. Papadopoulou, V.; Postigo, A.; Sanchez-Tillo, E.; Porter, A.C.; Wagner, S.D. Zeb1 and ctbp form a repressive complex at a distal promoter element of the bcl6 locus. Biochem. J. 2010, 427, 541-550.
12. Wang, J.; Lee, S.; Teh, C.E.; Bunting, K.; Ma, L.; Shannon, M.F. The transcription repressor, zeb1, cooperates with ctbp2 and hdac1 to suppress il-2 gene activation in t cells. Int. Immun. 2009, 21, 227-235.
13. Zhao, L.J.; Kuppuswamy, M.; Vijayalingam, S.; Chinnadurai, G. Interaction of zeb and histone deacetylase with the pldls-binding cleft region of monomeric c-terminal binding protein 2. BMC Mol. Biol. 2009, 10, 89.
14. Furusawa, T.; Moribe, H.; Kondoh, H.; Higashi, Y. Identification of ctbp1 and ctbp2 as corepressors of zinc finger-homeodomain factor deltaef1. Mol. Cell. Biol. 1999, 19, 8581-8590.
15. Shi, Y.; Sawada, J.; Sui, G.; Affar el, B.; Whetstine, J.R.; Lan, F.; Ogawa, H.; Luke, M.P.; Nakatani, Y.; Shi, Y. Coordinated histone modifications mediated by a ctbp co-repressor complex. Nature 2003, 422, 735-738.
16. Sanchez-Tillo, E.; Lazaro, A.; Torrent, R.; Cuatrecasas, M.; Vaquero, E.C.; Castells, A.; Engel, P.; Postigo, A. Zeb1 represses e-cadherin and induces an emt by recruiting the swi/snf chromatinremodeling protein brg1. Oncogene 2010, 29, 3490-3500.
17. Darling, D.S.; Stearman, R.P.; Qi, Y.; Qiu, M.S.; Feller, J.P. Expression of zfhep/deltaef1 protein in palate, neural progenitors, and differentiated neurons. Gene Expr. Patterns 2003, 3, 709-717.
18. Takagi, T.; Moribe, H.; Kondoh, H.; Higashi, Y. Deltaef1, a zinc finger and homeodomain transcription factor, is required for skeleton patterning in multiple lineages. Development (Cambridge, England) 1998, 125, 21-31.
19. Murray, D.; Precht, P.; Balakir, R.; Horton, W.E. Jr. The transcription factor deltaef1 is inversely expressed with type ii collagen mrna and can repress col2a1 promoter activity in transfected chondrocytes. J. Biol. Chem. 2000, 275, 3610-3618.
20. Terraz, C.; Toman, D.; Delauche, M.; Ronco, P.; Rossert, J. Delta ef1 binds to a far upstream sequence of the mouse pro-alpha 1(i) collagen gene and represses its expression in osteoblasts. J. Biol. Chem. 2001, 276, 37011-37019.
21. Brabletz, T.; Jung, A.; Hlubek, F.; Lohberg, C.; Meiler, J.; Suchy, U.; Kirchner, T. Negative regulation of cd4 expression in t cells by the transcriptional repressor zeb. Int. Immun. 1999, 11, 1701-1708.
22. Miyoshi, T.; Maruhashi, M.; Van De Putte, T.; Kondoh, H.; Huylebroeck, D.; Higashi, Y. Complementary expression pattern of zfhx1 genes sip1 and deltaef1 in the mouse embryo and their genetic interaction revealed by compound mutants. Dev. Dyn. 2006, 235, 1941-1952.
23. Grooteclaes, M.L.; Frisch, S.M. Evidence for a function of ctbp in epithelial gene regulation and anoikis. Oncogene 2000, 19, 3823-3828.
24. Eger, A.; Aigner, K.; Sonderegger, S.; Dampier, B.; Oehler, S.; Schreiber, M.; Berx, G.; Cano, A.; Beug, H.; Foisner, R. Deltaef1 is a transcriptional repressor of e-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005, 24, 2375-2385.
25. Guaita, S.; Puig, I.; Franci, C.; Garrido, M.; Dominguez, D.; Batlle, E.; Sancho, E.; Dedhar, S.; De Herreros, A.G.; Baulida, J. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by muc1 repression and zeb1 expression. J. Biol. Chem. 2002, 277, 39209-39216.
26. Wellner, U.; Schubert, J.; Burk, U.C.; Schmalhofer, O.; Zhu, F.; Sonntag, A.; Waldvogel, B.; Vannier, C.; Darling, D.; zur Hausen, A.; Brunton, V.G.; Morton, J.; Sansom, O.; Schuler, J.; Stemmler, M.P.; Herzberger, C.; Hopt, U.; Keck, T.; Brabletz, S.; Brabletz, T. The emt-activator zeb1 promotes tumorigenicity by repressing stemness-inhibiting micrornas. Nat. Cell Biol. 2009, 11, 1487-1495.
27. Reinhold, W.C.; Reimers, M.A.; Lorenzi, P.; Ho, J.; Shankavaram, U.T.; Ziegler, M.S.; Bussey, K.J.; Nishizuka, S.; Ikediobi, O.; Pommier, Y.G.; Weinstein, J.N. Multifactorial regulation of e-cadherin expression: An integrative study. Mol. Cancer Ther. 2010, 9, 1-16.
28. Aigner, K.; Dampier, B.; Descovich, L.; Mikula, M.; Sultan, A.; Schreiber, M.; Mikulits, W.; Brabletz, T.; Strand, D.; Obrist, P.; Sommergruber, W.; Schweifer, N.; Wernitznig, A.; Beug, H.; Foisner, R.; Eger, A. The transcription factor zeb1 (deltaef1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007, 26, 6979-6988.
29. Hurteau, G.J.; Carlson, J.A.; Spivack, S.D.; Brock, G.J. Overexpression of the microrna hsa-mir-200c leads to reduced expression of transcription factor 8 and increased expression of e-cadherin. Cancer Res. 2007, 67, 7972-7976.
30. Hurteau, G.J.; Carlson, J.A.; Roos, E.; Brock, G.J. Stable expression of mir-200c alone is sufficient to regulate tcf8 (zeb1) and restore e-cadherin expression. Cell Cycle (Georgetown, Tex) 2009, 8, 2064-2069.
31. Burk, U.; Schubert, J.; Wellner, U.; Schmalhofer, O.; Vincan, E.; Spaderna, S.; Brabletz, T. 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.
32. Bracken, C.P.; Gregory, P.A.; Kolesnikoff, N.; Bert, A.G.; Wang, J.; Shannon, M.F.; Goodall, G.J. A double-negative feedback loop between zeb1-sip1 and the microrna-200 family regulates epithelial-mesenchymal transition. Cancer Res. 2008, 68, 7846-7854.
33. Gregory, P.A.; Bert, A.G.; Paterson, E.L.; Barry, S.C.; Tsykin, A.; Farshid, G.; Vadas, M.A.; Khew-Goodall, Y.; Goodall, G.J. The mir-200 family and mir-205 regulate epithelial to mesenchymal transition by targeting zeb1 and sip1. Nat. Cell Biol. 2008, 10, 593-601.
34. 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.
35. Spaderna, S.; Schmalhofer, O.; Wahlbuhl, M.; Dimmler, A.; Bauer, K.; Sultan, A.; Hlubek, F.; Jung, A.; Strand, D.; Eger, A.; Kirchner, T.; Behrens, J.; Brabletz, T. The transcriptional repressor zeb1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 2008, 68, 537-544.
36. Liu, Y.; El-Naggar, S.; Darling, D.S.; Higashi, Y.; Dean, D.C. Zeb1 links epithelial-mesenchymal transition and cellular senescence. Development (Cambridge, England) 2008, 135, 579-588.
37. Spaderna, S.; Schmalhofer, O.; Hlubek, F.; Berx, G.; Eger, A.; Merkel, S.; Jung, A.; Kirchner, T.; Brabletz, T. A transient, emt-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 2006, 131, 830-840.
38. Singh, M.; Spoelstra, N.S.; Jean, A.; Howe, E.; Torkko, K.C.; Clark, H.R.; Darling, D.S.; Shroyer, K.R.; Horwitz, K.B.; Broaddus, R.R.; Richer, J.K. Zeb1 expression in type i vs type ii endometrial cancers: A marker of aggressive disease. Mod. Pathol. 2008, 21, 912-923.
39. Spoelstra, N.S.; Manning, N.G.; Higashi, Y.; Darling, D.; Singh, M.; Shroyer, K.R.; Broaddus, R.R.; Horwitz, K.B.; Richer, J.K. The transcription factor zeb1 is aberrantly expressed in aggressive uterine cancers. Cancer Res. 2006, 66, 3893-3902.
40. Dohadwala, M.; Yang, S.C.; Luo, J.; Sharma, S.; Batra, R.K.; Huang, M.; Lin, Y.; Goodglick, L.; Krysan, K.; Fishbein, M.C.; Hong, L.; Lai, C.; Cameron, R.B.; Gemmill, R.M.; Drabkin, H.A.; Dubinett, S.M. Cyclooxygenase-2-dependent regulation of e-cadherin: Prostaglandin e(2) induces transcriptional repressors zeb1 and snail in non-small cell lung cancer. Cancer Res. 2006, 66, 5338-5345.
41. Graham, T.R.; Zhau, H.E.; Odero-Marah, V.A.; Osunkoya, A.O.; Kimbro, K.S.; Tighiouart, M.; Liu, T.; Simons, J.W.; O'Regan, R.M. Insulin-like growth factor-i-dependent up-regulation of zeb1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res. 2008, 68, 2479-2488.
42. Arumugam, T.; Ramachandran, V.; Fournier, K.F.; Wang, H.; Marquis, L.; Abbruzzese, J.L.; Gallick, G.E.; Logsdon, C.D.; McConkey, D.J.; Choi, W. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009, 69, 5820-5828.
43. Kent, O.A.; Mullendore, M.; Wentzel, E.A.; Lopez-Romero, P.; Tan, A.C.; Alvarez, H.; West, K.; Ochs, M.F.; Hidalgo, M.; Arking, D.E.; Maitra, A.; Mendell, J.T. A resource for analysis of microrna expression and function in pancreatic ductal adenocarcinoma cells. Cancer Biol. Ther. 2009, 8, 2013-2024.
44. Yu, J.; Ohuchida, K.; Mizumoto, K.; Sato, N.; Kayashima, T.; Fujita, H.; Nakata, K.; Tanaka, M. Microrna, hsa-mir-200c, is an independent prognostic factor in pancreatic cancer and its upregulation inhibits pancreatic cancer invasion but increases cell proliferation. Mol. Cancer 2010, 9, 169.
45. Brabletz, T.; Jung, A.; Spaderna, S.; Hlubek, F.; Kirchner, T. Opinion: Migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat. Rev. 2005, 5, 744-749.
46. Mani, S.A.; Guo, W.; Liao, M.J.; Eaton, E.N.; Ayyanan, A.; Zhou, A.Y.; Brooks, M.; Reinhard, F.; Zhang, C.C.; Shipitsin, M.; Campbell, L.L.; Polyak, K.; Brisken, C.; Yang, J.; Weinberg, R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133, 704-715.
47. Shimono, Y.; Zabala, M.; Cho, R.W.; Lobo, N.; Dalerba, P.; Qian, D.; Diehn, M.; Liu, H.; Panula, S.P.; Chiao, E.; Dirbas, F.M.; Somlo, G.; Pera, R.A.; Lao, K.; Clarke, M.F. Downregulation of mirna-200c links breast cancer stem cells with normal stem cells. Cell 2009, 138, 592-603.
48. Peter, M.E. Let-7 and mir-200 micrornas: Guardians against pluripotency and cancer progression. Cell Cycle (Georgetown, Tex) 2009, 8, 843-852.
49. Li, R.; Liang, J.; Ni, S.; Zhou, T.; Qing, X.; Li, H.; He, W.; Chen, J.; Li, F.; Zhuang, Q.; Qin, B.; Xu, J.; Li, W.; Yang, J.; Gan, Y.; Qin, D.; Feng, S.; Song, H.; Yang, D.; Zhang, B.; Zeng, L.; Lai, L.; Esteban, M.A.; Pei, D. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010, 7, 51-63.
50. Samavarchi-Tehrani, P.; Golipour, A.; David, L.; Sung, H.K.; Beyer, T.A.; Datti, A.; Woltjen, K.; Nagy, A.; Wrana, J.L. Functional genomics reveals a bmp-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010, 7, 64-77.
51. Singh, A.; Greninger, P.; Rhodes, D.; Koopman, L.; Violette, S.; Bardeesy, N.; Settleman, J. A gene expression signature associated with "K-ras addiction" Reveals regulators of emt and tumor cell survival. Cancer Cell 2009, 15, 489-500.
52. Buck, E.; Eyzaguirre, A.; Barr, S.; Thompson, S.; Sennello, R.; Young, D.; Iwata, K.K.; Gibson, N.W.; Cagnoni, P.; Haley, J.D. Loss of homotypic cell adhesion by epithelial-mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition. Mol. Cancer Ther. 2007, 6, 532-541.
53. Barr, S.; Thomson, S.; Buck, E.; Russo, S.; Petti, F.; Sujka-Kwok, I.; Eyzaguirre, A.; Rosenfeld- Franklin, M.; Gibson, N.W.; Miglarese, M.; Epstein, D.; Iwata, K.K.; Haley, J.D. Bypassing cellular egf receptor dependence through epithelial-to-mesenchymal-like transitions. Clin. Exp. Metast. 2008, 25, 685-693.
54. Wang, F.; Sloss, C.; Zhang, X.; Lee, S.W.; Cusack, J.C. Membrane-bound heparin-binding epidermal growth factor like growth factor regulates e-cadherin expression in pancreatic carcinoma cells. Cancer Res. 2007, 67, 8486-8493.
55. Wang, Z.; Li, Y.; Kong, D.; Banerjee, S.; Ahmad, A.; Azmi, A.S.; Ali, S.; Abbruzzese, J.L.; Gallick, G.E.; Sarkar, F.H. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res. 2009, 69, 2400-2407.
56. Shah, A.N.; Summy, J.M.; Zhang, J.; Park, S.I.; Parikh, N.U.; Gallick, G.E. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann. Surg. Oncol. 2007, 14, 3629-3637.
57. Cochrane, D.R.; Howe, E.N.; Spoelstra, N.S.; Richer, J.K. Loss of mir-200c: A marker of aggressiveness and chemoresistance in female reproductive cancers. J. Oncol. 2010, 2010, 821717.
58. Sharma, S.V.; Lee, D.Y.; Li, B.; Quinlan, M.P.; Takahashi, F.; Maheswaran, S.; McDermott, U.; Azizian, N.; Zou, L.; Fischbach, M.A.; Wong, K.K.; Brandstetter, K.; Wittner, B.; Ramaswamy, S.; Classon, M.; Settleman, J. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141, 69-80.
59. Vrba, L.; Jensen, T.J.; Garbe, J.C.; Heimark, R.L.; Cress, A.E.; Dickinson, S.; Stampfer, M.R.; Futscher, B.W. Role for DNA methylation in the regulation of mir-200c and mir-141 expression in normal and cancer cells. PloS One 2010, 5, e8697.