ZEB1 mediates drug resistance and EMT in p300-deficient CRC

Journal of Cancer

Volumn 8, Issue 8, 2017, Pages 1453-1459

  Lazarova, Darina ^a   Bordonaro, Michael ^a  

^a Janet Weis Children s Hospital   (United States)

Author keywords

Colorectal cancer; Epithelial to mesenchymal transition; Histone deactylase inhibitors; p300; Wnt; Wnt signaling; ZEB1

Indexed keywords

BUTYRIC ACID; E1A ASSOCIATED P300 PROTEIN; HISTONE ACETYLTRANSFERASE; TRANSCRIPTION FACTOR ZEB1; WNT PROTEIN;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CROSS RESISTANCE; DIETARY FIBER; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; INTRACELLULAR SIGNALING; PHENOTYPE; PROTEIN EXPRESSION; REPRESSOR GENE; WNT SIGNALING PATHWAY;

EID: 85019833224     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.18762     Document Type: Article

References (87)

1. Lazarova DL, Bordonaro M, Carbone R, et al. Linear relationship between WNT activity levels and apoptosis in colorectal carcinoma cells exposed to butyrate. Internat J Cancer. 2004; 110:523-31.
2. Bordonaro M, Lazarova DL, Sartorelli AC. The activation of beta-catenin by WNT signaling mediates the effects of histone deacetylase inhibitors. Exp Cell Res. 2007; 313:1652-66.
3. Chiaro C, Lazarova DL, Bordonaro M. Tcf3 and cell cycle factors contribute to butyrate resistance in colorectal cancer cells. Biochem Biophys Res Commun. 2012; 428:121-6.
4. Richter M, Jurek D, Wrba F, et al. Cells obtained from colorectal microadenomas mirror early premalignant growth patterns in vitro. Euro J Cancer. 2002; 38:1937-45.
5. Kautenberger T, Beyer-Sehlmeyer G, Festag G, et al. The gut fermentation product butyrate, a chemopreventive agent, suppresses glutathione S-transferase theta (hGSTT1) and cell growth more in human colon adenoma cells (LT97) than tumor (HT29) cells. J Cancer Res Clin Oncol. 2005; 131:692-700.
6. Bingham SA, Day NE, Luben R, et al. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet. 2003; 361:1496-501.
7. Peters U, Sinha R, Chaterjee N, et al. Dietary fibre and colorectal adenoma in a colorectal cancer early detection programme. Lancet. 2003; 361:1491-5.
8. Bingham SA, Norat T, Moskal A, et al. Is the association with fiber from foods in colorectal cancer confounded by folate intake? Cancer Epid Biom Prev. 2005; 14:1552-6.
9. Cummings JH, Pomare EW, Branch WJ, et al. Short chain fatty acids in human large intestine, portal, hepatic, and venous blood. Gut. 1987; 28:1221-7.
10. Belcheva A, Irrazabal T, Robertson SJ, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014; 158: 288-99.
11. Heerdt BG, Houston MA, Augenlicht LH. Potentiation by specific short-chain fatty acids of differentiation and apoptosis in human colonic carcinoma cell lines. Cancer Res. 1994; 54:3288-94.
12. Hague A, Elder DJ, Hicks DJ, et al. Apoptosis in colorectal tumor cells: induction by the short chain fatty acids butyrate, propionate and acetate and by the bile salt deoxycholate. Internat J Cancer. 1995; 60:400-6.
13. Medina V, Young GP, Edmonds B, et al. Induction of caspase-3 protease activity and apoptosis by butyrate and another inhibitor of histone deacetylase: dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res. 1997; 57:3697-707.
14. Marks PA, Dokmanovic M. Histone deacetylase inhibitors: discovery and development as anticancer agents. Expert Opin Investig Drugs. 2005; 12:1497-511.
15. Lin HY, Chen CS, Lin SP, et al. Targeting histone deacetylase in cancer therapy. Med Res Rev. 2006; 26:397-413.
16. Bordonaro M, Mariadason JM, Aslam F, et al. Butyrate-induced apoptotic cascade in colonic carcinoma cells: modulation of the beta-catenin-Tcf pathway and concordance with effects of sulindac and trichostatin A but not curcumin. Cell Growth Differ. 1999; 10:713-20.
17. Li VSW, Ng SS, Boersema PJ, et al. WNT signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell. 2012; 149:1245-56.
18. Cook D, Fry M, Hughes K, et al. Wingless inactivates glycogen synthase kinase-3 via an intracellular signaling pathway which involves a protein kinase C. EMBO J. 1996; 15:4526-36.
19. Rubinfeld B, Souza B, Albert I, et al. Association of the APC gene product with β-catenin. Science. 1993; 262:1731-4.
20. Su LK, Vogelstein B, Kinzler KW. Association of the APC tumor suppresser protein with catenins. Science. 1993; 262:1734-7.
21. Munemitsu S, Albert I, Souza B, et al. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci USA. 1995; 92:3046-50.
22. Behrens J, Von Kries JP, Kuhl M, et al. Functional interaction of β-catenin with the transcriptional factor LEF-1. Nature. 1996; 381:638-42.
23. Molenaar M, Van De Wetering M, Osterwegel M. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell. 1996; 86:391-9.
24. Korinek V, Barker N, Morin PJ, et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 1997; 275:1774-7.
25. Morin J, Sparks AB, Korinek V, et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science. 1997; 275:1777-90.
26. Bienz M, Clevers H. Linking colorectal cancer to WNT signaling. Cell. 2000; 103:311-20.
27. Emami KH, Nguyen C, Ma H, et al. A small molecule inhibitor of β-catenin/CREB-binding protein transcription. Proc Natl Acad Sci USA. 2004; 101:12681-7.
28. McMillan M, Kahn M. Investigating WNT signaling: a chemogenomic safari. Drug Disc Today. 2005; 10:1467-74.
29. Teo JL, Ma H, Nguyen C, et al. Specific inhibition of CBP/β-catenin interaction rescues defects in neuronal differentiation caused by presenilin-1 mutation. Proc Natl Acad Sci USA. 2005; 102:12171-6.
30. Ma H, Nguyen C, Lee KS, et al. Differential roles for the coactivators CBP and p300 on TCF/β-catenin-mediated survivin gene expression. Oncogene. 2005; 24:3619-31.
31. Miyabayashi T, Teo JL, Yamamoto M, et al. WNT/β-catenin/CBP signaling maintains long-term murine stem cell pluripotency. Proc Natl Acad Sci USA. 2007; 104:5668-73.
32. Teo JL, Kahn M. The WNT signaling pathway in cellular proliferation and differentiation: a tale of two coactivators. Adv Drug Delivery Rev. 2010; 62:1149-55.
33. Iyer NG, Ozdag H, Caldas C. p300/CBP and cancer. Oncogene. 2004; 23: 4225-31.
34. Hecht A, Vleminckx K, Stemmler MP, et al. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J. 2000; 19:1829-50.
35. Bryan EJ, Jokubaitis VJ, Chamberlain NL, et al. Mutation analysis of EP300 in colon, breast and ovarian carcinomas. Int J Cancer. 2002; 102: 137-141.
36. Levy L, Wei Y, Labalette C, et al. Acetylation of beta-catenin by p300 regulates beta-catenin-Tcf4 interaction. Mol Cell Biol. 2004; 24:3404-14.
37. Takahashi-Yanaga F, Kahn M. Targeting WNT signaling: can we safely eradicate cancer stem cells? Clin Cancer Res. 2010; 16:3153-62.
38. Lazarova DL, Chiaro C, Wong T, et al. CBP activity mediates effects of the histone deacetylase inhibitor butyrate on WNT activity and apoptosis in colon cancer cells. J. Cancer. 2013; 4: 480-90.
39. Lazarova DL, Wong T, Chiaro C, et al. p300 influences butyrate-mediated WNT hyperactivation in colorectal cancer cells. J. Cancer. 2013; 4: 491-501.
40. Lazarova DL, Lee A, Wong T, et al. Modulation of Wnt Activity and cell physiology by butyrate in LT97 microadenoma cells. J. Cancer. 2014; 5: 203-13.
41. Bordonaro M, Lazarova DL. CBP, p300, butyrate, and Wnt signaling in colorectal cancer. World J Gastroenterology. 2015; 21: 8138-48.
42. Bordonaro M, Drago E, Atamna W, et al. Comprehensive suppression of all apoptosis-induced proliferation pathways as a proposed approach to colorectal cancer prevention and therapy. PLoS One. 2014; 9:e115068
43. Krubasik D, Iyer NG, English WR, et al. Absence of p300 induces cellular phenotype changes characteristic of epithelial to mesenchyme transition. Br J Cancer. 2006; 94: 1326-32.
44. Sanches-Tillo E, Siles L, de Barrios O, et al. Expanding roles of ZEB factors in tumorigenesis and tumor progression. Am J Cancer. 2012; 2: 897-912.
45. Postigo AA. Opposing functions of ZEB proteins in the regulation of the TGFβ/BMP signaling pathway. EMBO J. 2003; 22: 2243-52.
46. Mizuguchi Y, Specht S, Lunz III JG, et al. Cooperation of p300 and PCAF in the control of microRNA 200c/141 transcription and epithelial characteristics. PLoS One. 2012; 7: e32449.
47. Sanchez-Tillo E, Lazaro A, Torrent R, et al. ZEB1 represses E-cadherin and induces EMT by recruiting the SWI/SNF chromatin-remodeling protein BRG1. Oncogene. 2010; 29: 3490-500.
48. Sanchez-Tillo E, de Barrios O, Siles L, et al. β-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc Natl Acad Sci USA. 2011; 108: 19204-9
49. Sanchez-Tillo E, de Barrios O, Siles L, et al. ZEB1 promotes invasiveness of colorectal carcinoma cells through the opposing regulation of uPA and PAI-1. Clin Cancer Res. 2013; 19: 1071-81.
50. Sanchez-Tillo E, de Barrios O, Valls E, et al. ZEB1 and TCF4 reciprocally modulate their transcriptional activities to regulate Wnt target gene expression. Oncogene. 2015; 34: 5760-70.
51. Pena C, Garcia JM, Garcia V, et al. The expression levels of the transcriptional regulators p300 and CtBP modulate the correlations between SNAIL, ZEB1, E-cadherin and vitamin D receptor in human colon carcinomas. Int J Cancer. 2006; 119: 2098-104.
52. Aigner K, Dampier B, Descovich L, et al. The transcription factor ZEB1 (dEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene. 2007; 26: 6978-88.
53. Moheimani F, Roth HM, Cross J, et al. Disruption of β-catenin/CBP signaling inhibits human airway epithelial-mesenchymal transition and repair. Int J Biochem & Cell Biol. 2015; 68: 59-69.
54. Martincorena I, Campbell PJ. Somatic mutation in cancer and normal cells. Science. 2015; 349: 1482-8.
55. Buck E, Eyzaguirre A, Barr S, et al. Loss of homotypic cell adhesion by epithelial-mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition. Mol Cancer Ther. 2007; 6:532-41.
56. Ono H, Imoto I, Kozaki K, et al. SIX1 promotes epithelial-mesenchymal transition in colorectal cancer through ZEB1 activation. Oncogene. 2012; 31:4923-34.
57. Hu Z, Wang J. Histone deacetylase inhibitor induces the expression of select epithelial genes in mouse utricle sensory epithelia-derived progenitor cells. Cell Reprogram. 2014; 16:266-75.
58. Qin Y, Tang B, Hu CJ, et al. A hTERT/ZEB1 complex directly regulates E-cadherin to promote epithelial to mesenchymal transition (EMT) in colorectal cancer. Oncotarget. 2015; 7: 351-61.
59. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010; 29: 4741-51.
60. Zaravinos A. The regulatory role of microRNAs in EMT and cancer. J Oncol. 2015; :articleID865806.
61. Jolly MK, Jia D, Boareto M, et al. Coupling the modules of EMT and stemness: A tunable 'stemness window' model. Oncotarget. 2015; 6: 25161-74.
62. Roca H, Hernadez J, Weidner S, et al. Transcription Factors OVOL1 and OVOL2 Induce the Mesenchymal to Epithelial Transition in Human Cancer. PLoS One. 2013; DOI: 10.1371/journal.pone.007633.
63. Ring A, Kim Y-M, Khan M. Wnt/catenin signaling in adult stem cell physiology and disease. Stem Cell Rev. 2014; 10: 512-25
64. Sellerio AL, Ciusani E, Ben-Moshe NB, et al. Overshoot during phenotypic switching of cancer cell populations. Sci Rep. 2015; 5: 15464.
65. Medema JP, Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature. 2011; 474:318-26.
66. Lopez de Silanes I, Olmo N, Turnay J, et al. Acquisition of resistance to butyrate enhances survival after stress and induces malignancy of human colon carcinoma cells. Cancer Res. 2004; 64: 4593-4600.
67. Gill RK, Dudeja PK. A novel fact to consider for the effects of butyrate on its target cells. Focus on "The short-chain fatty acid butyrate is a substrate of breast cancer resistance protein." Am J Physiol Cell Physiol. 2011; 301: C93-9.
68. Goncalves P, Gregorio I, Martel F. The short-chain fatty acid butyrate is a substrate of breast cancer resistance protein. Am J Physiol Cell Physiol. 2011; 301: C983-94.
69. Shi J, Jiang X, Yu Z, et al. ZNRF3 contributes to the growth of lung carcinoma via inhibiting Wnt/b-catenin pathway an is regulated by miR-93. Tumour Biol. 2016; 37: 3051-7.
70. Serpa J, Caiado F, Carvalho T, et al. Butyrate-rich microenvironment is a relevant selection factor for metabolically adapted tumor cells. J Biol Chem. 2010; 285:39211-23.
71. Kim AY, Kwak JH, Je NK, et al. Epithelial-mesenchymal transition is associated with acquired resistance to 5-flurouracil in HT-29 colon cancer cells. Toxicol Res. 2015; 31: 151-6
72. Lazarova DL, Bordonaro M. Extreme fluctuations in Wnt/beta-catenin signaling as an approach for colon cancer prevention and therapy. Advanced Studies in Biology. 2012; 4: 351-62.
73. Bordonaro M, Tewari S, Cicco CE, et al. A switch from canonical to noncanonical Wnt signaling mediates drug resistance in colon cancer cells. PLoS One. 2011;6:e27308. doi: 10.1371/journal.pone.0027308.
74. Lazarova DL, Bordonaro M, Sartorelli AC. Transcriptional regulation of the vitamin D3 receptor by ZEB. Cell Growth Diff. 2001; 12: 319-6.
75. Ji M, Lee EJ, Kim KB, et al. HDAC inhibitors induce epithelial-mesenchymal transition in colon carcinoma cells. Oncol Rep. 2015; 33:2299-308.
76. Kikuchi M, Yamashita K, Waraya M, et al. Epigenetic regulation of ZEB1-RAB25/ESRP1 axis plays a critical role in phenylbutyrate treatment-resistant breast cancer. Oncotarget. 2016; 7: 1741-53.
77. Higuchi Y, Nguyen C, Yasuda SY, et al. Specific direct small Molecule p300/β-catenin antagonists maintain stem cell potency. Curr Mol Pharmacol. 2016; 9: 272-9.
78. Sakamoto T, Kobayashi S, Yamada D, et al. A histone deacetylase inhibitor suppresses epithelial-mesenchymal transition and attenuates chemoresistance in biliary tract cancer. PLoS One. 2016; 11: e0145985.
79. Burk U, Schubert J, Wellner U, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008; 9:581-588.
80. Su J, Zhang A, Shi Z, et al. MicroRNA-200a suppresses the Wnt/β-catenin signaling pathway by interacting with β-catenin. Int J Oncol. 2012; 40: 1162-70.
81. Ghahhari NM, Babahah S. Interplay between microRNAs and WNT/β-catenin signaling pathway regulates epithelial-mesenchymal transition in cancer. Euro J Cancer. 2015; 51: 1638-49.
82. Wellner U, Schubert J, Burk UC, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 2009; 11:1487-95.
83. de Barrios O, Gyorffy B, Fernández-Aceñero MJ, et al. ZEB1-induced tumourigenesis requires senescence inhibition via activation of DKK1/mutant p53/Mdm2/CtBP and repression of macroH2A1. Gut. 2017; 66: 666-82.
84. Spaderna S, Schmalhofer O, Wahlbuhl M, et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 2008; 68:537-44.
85. Jägle S, Dertmann A, Schrempp M, et al. ZEB1 is neither sufficient nor required for epithelial-mesenchymal transition in LS174T colorectal cancer cells. Biochem Biophys Res Commun. 2017; 48:1226-1232.
86. Muto Y, Suzuki K, Kato T, et al. Heterogeneous expression of zinc-finger E-box-binding homeobox 1 plays a pivotal role in metastasis via regulation of miR-200c in epithelial-mesenchymal transition. Int J Oncol. 2016; 49:1057-67.
87. Du J, Sun B, Zhao X, et al. Hypoxia promotes vasculogenic mimicry formation by inducing epithelial-mesenchymal transition in ovarian carcinoma. Gynecol Oncol. 2014; 133:575-83.