ZEB1-induced tumourigenesis requires senescence inhibition via activation of DKK1/mutant p53/Mdm2/CtBP and repression of macroH2A1

Gut

Volumn 66, Issue 4, 2017, Pages 666-682

  De Barrios, Oriol ^a   Gyorffy, Balázs ^b   Fernández Aceñero, María Jesús ^c,d   Sánchez Tilló, Ester ^a   Sánchez Moral, Lidia ^a   Siles, Laura ^a   Esteve Arenys, Anna ^a   Roué, Gaël ^a   Casal, José I ^e   Darling, Douglas S ^f   Castells, Antoni ^g,h   Postigo, Antonio ^a,h,i,j  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c HOSPITAL UNIVERSITARIO FUNDACIÓN JIMÉNEZ DÍAZ   (Spain)

^d HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^e CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^f UNIVERSITY OF LOUISVILLE   (United States)

^g HOSPITAL CLÍNIC   (Spain)

^h INSTITUTO DE SALUD CARLOS III   (Spain)

ⁱ UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

^j INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARBOXYTERMINAL BINDING PROTEIN; DICKKOPF 1 PROTEIN; HISTONE H2A; PROTEIN MDM2; PROTEIN P53; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; ALCOHOL DEHYDROGENASE; C-TERMINAL BINDING PROTEIN; DKK1 PROTEIN, MOUSE; DNA BINDING PROTEIN; HISTONE; MACROH2A HISTONE; MDM2 PROTEIN, MOUSE; SIGNAL PEPTIDE; ZEB1 PROTEIN, HUMAN; ZEB1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PROGNOSIS; CARCINOGENESIS; CELL VIABILITY; COLORECTAL CARCINOMA; CONTROLLED STUDY; DISEASE ASSOCIATION; DKK1 GENE; GENE CONTROL; GENE EXPRESSION ASSAY; H2AFY GENE; HETEROCHROMATIN; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENESCENCE; SURVIVAL ANALYSIS; TRANSGENE; TUMOR XENOGRAFT; ZEB1 GENE; ANIMAL; CELL AGING; CELL SURVIVAL; COLON TUMOR; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; SURVIVAL RATE; TRANSGENIC MOUSE; TUMOR CELL LINE; UPREGULATION; WNT SIGNALING PATHWAY; XENOGRAFT;

ALCOHOL OXIDOREDUCTASES; ANIMALS; CARCINOGENESIS; CELL AGING; CELL LINE, TUMOR; CELL SURVIVAL; COLONIC NEOPLASMS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HISTONES; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, TRANSGENIC; MUTATION; PROTO-ONCOGENE PROTEINS C-MDM2; SURVIVAL RATE; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; WNT SIGNALING PATHWAY; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 85006968681     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2015-310838     Document Type: Article

References (58)

1. Clevers H, Nusse R. Wnt/β-catenin signaling and Disease. Cell 2012;149:1192-205.
2. Saini S, Majid S, Dahiya R. The complex roles of Wnt antagonists in RCC. Nat Rev Urol 2011;8:690-9.
3. Chamorro MN, Schwartz DR, Vonica A, et al. FGF-20 and DKK1 are transcriptional targets of β-catenin and FGF-20 is implicated in cancer and development. EMBO J 2005;24:73-84.
4. Menezes ME, Devine DJ, Shevde LA, et al. Dickkopf1: a tumor suppressor or metastasis promoter? Int J Cancer 2012;130:1477-83.
5. Pérez-Mancera PA, Young AR, Narita M. Inside and out: the activities of senescence in cancer. Nat Rev Cancer. 2014;14:547-58.
6. Zhang R, Poustovoitov MV, Ye X, et al. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev Cell 2005;8:19-30.
7. Zhang R, Chen W, Adams PD. Molecular dissection of formation of senescence-associated heterochromatin foci. Mol Cell Biol 2007;27:2343-58.
8. Di Micco R, Sulli G, Dobreva M, et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat Cell Biol 2011;13:292-302.
9. Ye X, Zerlanko B, Kennedy A, et al. Downregulation of Wnt signaling is a trigger for formation of facultative heterochromatin and onset of cell senescence in primary human cells. Mol Cell 2007;27:183-96.
10. Sánchez-Tilló E, Liu Y, de Barrios O, et al. EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell Mol Life Sci 2012;69:3429-56.
11. Postigo AA, Dean DC. ZEB represses transcription through interaction with the corepressor CtBP. Proc Natl Acad Sci USA 1999;96:6683-8.
12. Postigo A, Depp JL, Taylor JJ, et al. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. EMBO J 2003;22:2453-62.
13. Postigo AA. Opposing functions of ZEB proteins in the regulation of the TGFβ/BMP signaling pathway. EMBO J 2003;22:2443-52.
14. 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.
15. Sánchez-Tilló 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.
16. Hill L, Browne G, Tulchinsky E. ZEB/miR-200 feedback loop: at the crossroads of signal transduction in cancer. Int J Cancer. 2013;132:745-54.
17. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014;15:178-96.
18. Smith JJ, Deane NG, Wu F, et al. Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 2010;138:958-68.
19. Freeman TJ, Smith JJ, Chen X, et al. Smad4-mediated signaling inhibits intestinal neoplasia by inhibiting expression of β-catenin. Gastroenterology 2013;142:562-571.e2.
20. Voloshanenko O, Erdmann G, Dubash TD, et al. Wnt secretion is required to maintain high levels of Wnt activity in colon cancer cells. Nat Commun 2013;4:2610.
21. Karamariti E, Margariti A, Winkler B, et al. Smooth muscle cells differentiated from reprogrammed embryonic lung fibroblasts through DKK3 signaling are potent for tissue engineering of vascular grafts. Circ Res 2013;112:1433-43.
22. Yue W, Sun Q, Dacic S, et al. Downregulation of Dkk3 activates β-catenin/TCF-4 signaling in lung cancer. Carcinogenesis 2008;29:84-92.
23. Postigo AA, Dean DC. Differential expression and function of members of the zfh-1 family of zinc finger/homeodomain repressors. Proc Natl Acad Sci USA 2000;97:6391-6.
24. Takagi T, Moribe H, Kondoh H, et al. δEF1, a zinc finger and homeodomain transcription factor, is required for skeleton patterning in multiple lineages. Development 1998;125:21-31.
25. Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995;92:93363-9367.
26. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, et al. Protocols to detect senescence-associated beta-galactosidase (SA-βgal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc 2009;4:1798-806.
27. Fregoso OI, Das S, Akerman M, et al. Splicing-factor oncoprotein SRSF1 stabilizes p53 via RPL5 and induces cellular senescence. Mol Cell 2013;50:56-66.
28. Salsman J, Pinder J, Tse B, et al. The translation initiation factor 3 subunit eIF3K interacts with PML and associates with PML nuclear bodies. Exp Cell Res 2013;319:2554-65.
29. Tachibana M, Sugimoto K, Nozaki M, et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 2002;16:1779-91.
30. Bruno T, De Nicola F, Iezzi S, et al. Che-1 phosphorylation by ATM/ATR and Chk2 kinases activates p53 transcription and the G2/M checkpoint. Cancer Cell 2006;10:473-86.
31. Liu Y, Sánchez-Tilló E, Lu X, et al. The ZEB1 transcription factor acts in a negative feedback loop with miR200 downstream of Ras and Rb1 to regulate Bmi1 expression. J Biol Chem 2014;289:4116-25.
32. Vardabasso C, Hasson D, Ratnakumar K, et al. Histone variants: emerging players in cancer biology. Cell Mol Life Sci 2013;71:379-404.
33. Siles L, Sánchez-Tilló E, Lim JW, et al. ZEB1 imposes a temporary stage-dependent inhibition of muscle gene expression and differentiation via CtBP-mediated transcriptional repression. Mol Cell Biol 2013;33:1368-82.
34. Di LJ, Byun JS, Wong MM, et al. Genome-wide profiles of CtBP link metabolism with genome stability and epithelial reprogramming in breast cancer. Nat Commun 2013;4:1449.
35. Wade M, Li YC, Wahl GM. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat Rev Cancer 2013;13:83-96.
36. Gu L, Findley HW, Zhou M. MDM2 induces NF-κB/p65 expression transcriptionally through Sp1-binding sites: a novel, p53-independent role of MDM2 in doxorubicin resistance in acute lymphoblastic leukemia. Blood 2002;99:3367-75.
37. Wienken M, Dickmanns A, Nemajerova A, et al. MDM2 associates with Polycomb Repressor Complex 2 and enhances stemness-promoting chromatin modifications independent of p53. Mol Cell 2016;61:68-83.
38. Rufini A, Tucci P, Celardo I, et al. Senescence and aging: the critical roles of p53. Oncogene 2013;32:5129-43.
39. Efeyan A, Ortega-Molina A, Velasco-Miguel S, et al. Induction of p53-dependent senescence by the MDM2 antagonist nutlin-3a in mouse cells of fibroblast origin. Cancer Res 2007;67:7350-7.
40. Mirnezami AH, Campbell SJ, Darley M, et al. Hdm2 recruits a hypoxia-sensitive corepressor to negatively regulate p53-dependent transcription. Curr Biol 2003;13:1234-9.
41. Morton JP, Timpson P, Karim SA, et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc Natl Acad Sci USA 2010;107:246-51.
42. Muller PA, Vousden KH. Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell 2014;25:304-17.
43. Freed-Pastor WA, Prives C. Mutant p53: one name, many proteins. Genes Dev 2012;26:1268-86.
44. Willis A, Jung EJ, Wakefield T, et al. Mutant p53 exerts a dominant negative effect by preventing wild-type p53 from binding to the promoter of its target genes. Oncogene. 2004;23:2330-8.
45. Chan WM, Mak MC, Fung TK, et al. Ubiquitination of p53 at multiple sites in the DNA-binding domain. Mol Cancer Res 2006;4:15-25.
46. Zhang S, Zhou L, Hong B, et al. Small-molecule NSC59984 restores p53 pathway signaling and antitumor effects against colorectal cancer via p73 activation and degradation of mutant p53. Cancer Res 2015;75:3842-52.
47. Chang CJ, Chao CH, Xia W, et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol 2011;13:317-23.
48. Spaderna S, Schmalhofer O, Hlubek F, et al. A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 2006;131:830-40.
49. Suram A, Kaplunov J, Patel PL, et al. Oncogene-induced telomere dysfunction enforces cellular senescence in human cancer precursor lesions. EMBO J 2012;31:2839-51.
50. Neufert C, Becker C, Neurath MF. An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protocol 2007;2:1998-2004.
51. Hall CL, Daignault SD, Shah RB, et al. Dickkopf-1 expression increases early in prostate cancer development and decreases during progression from primary tumor to metastasis. Prostate 2008;68:1396-404.
52. De Sousa E Melo F, Colak S, Buikhuisen J, et al. Methylation of cancer-stem-cell-associated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell 2008;9:476-85.
53. Shi Y, Sawada JI, Sui G, et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 2003;422:735-8.
54. Kim TW, Kim HJ, Lee C, et al. Identification of replicative senescence-associated genes in human umbilical vein endothelial cells by annealing control primer system. Exp Gerontol 2008;43:286-95.
55. Lyros O, Rafiee P, Nie L, et al. Dickkopf-1, the Wnt antagonist, is induced by acidic pH and mediates epithelial cellular senescence in human reflux esophagitis. Am J Physiol Gastrointest Liver Physiol 2014;306:G557-74.
56. Ozturk N, Erdal E, Mumcuoglu M, et al. Reprogramming of replicative senescence in hepatocellular carcinoma-derived cells. Proc Natl Acad Sci USA 2006;103:2178-83.
57. Caramel J, Papadogeorgakis E, Hill L, et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell 2013;24:466-80.
58. Nardella C, Clohessy JG, Alimonti A, et al. Pro-senescence therapy for cancer treatment. Nat Rev Cancer 2011;11:503-11.