β-Catenin/Tcf-4 Inhibition After Progastrin Targeting Reduces Growth and Drives Differentiation of Intestinal Tumors

Gastroenterology

Volumn 133, Issue 5, 2007, Pages 1554-1568

  Pannequin, Julie ^a   Delaunay, Nathalie ^a   Buchert, Michael ^a   Surrel, Fanny ^b   Bourgaux, Jean François ^c   Ryan, Joanne ^a   Boireau, Stéphanie ^a   Coelho, Jessica ^a   Pélegrin, André ^d   Singh, Pomila ^e   Shulkes, Arthur ^f   Yim, Mildred ^f   Baldwin, Graham S ^f   Pignodel, Christine ^c   Lambeau, Gérard ^b   Jay, Philippe ^a   Joubert, Dominique ^a   Hollande, Frédéric ^a  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b CNRS   (France)

^c NÎMES UNIVERSITY HOSPITAL   (France)

^d INSERM   (France)

^e University of Texas Medical Branch School of Medicine   (United States)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GASTRIN; GLYCINE; INTEGRIN LINKED KINASE; PROGASTRIN; RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 4; UNCLASSIFIED DRUG;

ADENOMA; AMIDATION; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL LINEAGE; CLINICAL ASSESSMENT; COLON MUCOSA; COLON POLYPOSIS; COLORECTAL CANCER; COLORECTAL TUMOR; CONTROLLED STUDY; CORRELATION FUNCTION; DOWN REGULATION; DRUG ACTIVITY; DRUG INHIBITION; GENE; GENE ACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GOBLET CELL; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INTESTINE TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TUMOR CELL; TUMOR DIFFERENTIATION; TUMOR GROWTH; TUMOR VOLUME;

ADENOMA; ADENOMATOUS POLYPOSIS COLI; ANIMALS; APOPTOSIS; BETA CATENIN; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; GASTRINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, APC; HUMANS; MICE; MICE, NUDE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN PRECURSORS; RANDOM ALLOCATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSPLANTATION, HETEROLOGOUS;

EID: 35748959029     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2007.08.023     Document Type: Article

References (45)

1. Lallemand-Breitenbach V., Zhu J., Kogan S., et al. Opinion: how patients have benefited from mouse models of acute promyelocytic leukaemia. Nat Rev Cancer 5 (2005) 821-827
2. Wang Z.Y., and Chen Z. Differentiation and apoptosis induction therapy in acute promyelocytic leukaemia. Lancet Oncol 1 (2000) 101-106
3. Coelho S.M., Vaisman M., and Carvalho D.P. Tumour re-differentiation effect of retinoic acid: a novel therapeutic approach for advanced thyroid cancer. Curr Pharm Des 11 (2005) 2525-2531
4. Radtke F., and Clevers H. Self-renewal and cancer of the gut: two sides of a coin. Science 307 (2005) 1904-1909
5. van Es J.H., and Clevers H. Notch and Wnt inhibitors as potential new drugs for intestinal neoplastic disease. Trends Mol Med 11 (2005) 496-502
6. Fre S., Huyghe M., Mourikis P., et al. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435 (2005) 964-968
7. van Es J.H., van Gijn M.E., Riccio O., et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435 (2005) 959-963
8. Jain M., Arvanitis C., Chu K., et al. Sustained loss of a neoplastic phenotype by brief inactivation of MYC. Science 297 (2002) 102-104
9. van de Wetering M., Sancho E., Verweij C., et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111 (2002) 241-250
10. Lepourcelet M., Chen Y.-N.P., France D.S., et al. Small-molecule antagonists of the oncogenic Tcf/[beta]-catenin protein complex. Cancer Cell 5 (2004) 91-102
11. Chakladar A., Dubeykovskiy A., Wojtukiewicz L.J., et al. Synergistic activation of the murine gastrin promoter by oncogenic Ras and beta-catenin involves SMAD recruitment. Biochem Biophys Res Commun 336 (2005) 190-196
12. Koh T.J., Bulitta C.J., Fleming J.V., et al. Gastrin is a target of the beta-catenin/TCF-4 growth-signaling pathway in a model of intestinal polyposis. J Clin Invest 106 (2000) 533-539
13. Janssen K.P., Alberici P., Fsihi H., et al. APC and oncogenic KRAS are synergistic in enhancing Wnt signaling in intestinal tumor formation and progression. Gastroenterology 131 (2006) 1096-1109
14. Hollande F., Imdahl A., Mantamadiotis T., et al. Glycine-extended gastrin acts as an autocrine growth factor in a nontransformed colon cell line. Gastroenterology 113 (1997) 1576-1588
15. Hollande F., Lee D.J., Choquet A., et al. Adherens junctions and tight junctions are regulated via different pathways by progastrin in epithelial cells. J Cell Sci 116 (2003) 1187-1197
16. Seva C., Dickinson C.J., and Yamada T. Growth-promoting effects of glycine-extended progastrin. Science 265 (1994) 410-412
17. Ottewell P.D., Varro A., Dockray G.J., et al. COOH-terminal 26-amino acid residues of progastrin are sufficient for stimulation of mitosis in murine colonic epithelium in vivo. Am J Physiol 288 (2005) G541-G549
18. Singh P., Velasco M., Given R., et al. Mice overexpressing progastrin are predisposed for developing aberrant colonic crypt foci in response to AOM. Am J Physiol 278 (2000) G390-G399
19. Hollande F., Shulkes A., and Baldwin G.S. Signaling the junctions in gut epithelium. Sci STKE 2005 (2005) pe13
20. Ciccotosto G.D., McLeish A., Hardy K.J., et al. Expression, processing, and secretion of gastrin in patients with colorectal carcinoma. Gastroenterology 109 (1995) 1142-1153
21. Konturek P.C., Bielanski W., Konturek S.J., et al. Progastrin and cyclooxygenase-2 in colorectal cancer. Dig Dis Sci 47 (2002) 1984-1991
22. Siddheshwar R.K., Gray J.C., and Kelly S.B. Plasma levels of progastrin but not amidated gastrin or glycine extended gastrin are elevated in patients with colorectal carcinoma. Gut 48 (2001) 47-52
23. Van Solinge W.W., Nielsen F.C., Friis-Hansen L., et al. Expression but incomplete maturation of progastrin in colorectal carcinomas. Gastroenterology 104 (1993) 1099-1107
24. Fodde R., Smits R., and Clevers H. APC, signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer 1 (2001) 55-67
25. Gottardi C.J., and Gumbiner B.M. Role for ICAT in beta-catenin-dependent nuclear signaling and cadherin functions. Am J Physiol 286 (2004) C747-C756
26. Blache P., van de Wetering M., Duluc I., et al. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 166 (2004) 37-47
27. Pear W.S., Nolan G.P., Scott M.L., et al. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci U S A 90 (1993) 8392-8396
28. Judge A.D., Sood V., Shaw J.R., et al. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat Biotechnol 23 (2005) 457-462
29. Marques J.T., Devosse T., Wang D., et al. A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat Biotechnol 24 (2006) 559-565
30. Colnot S., Niwa-Kawakita M., Hamard G., et al. Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab Invest 84 (2004) 1619-1630
31. Morin P.J., Sparks A.B., Korinek V., et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275 (1997) 1787-1790
32. Korinek V., Barker N., Morin P.J., et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275 (1997) 1784-1787
33. Tago K., Nakamura T., Nishita M., et al. Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev 14 (2000) 1741-1749
34. Sekiya T., Nakamura T., Kazuki Y., et al. Overexpression of Icat induces G(2) arrest and cell death in tumor cell mutants for adenomatous polyposis coli, beta-catenin, or Axin. Cancer Res 62 (2002) 3322-3326
35. Cobb S., Wood T., Ceci J., et al. Intestinal expression of mutant and wild-type progastrin significantly increases colon carcinogenesis in response to azoxymethane in transgenic mice. Cancer 100 (2004) 1311-1323
36. Daniels D.L., and Weis W.I. ICAT inhibits beta-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol Cell 10 (2002) 573-584
37. Ferrand A., Bertrand C., Portolan G., et al. Signaling pathways associated with colonic mucosa hyperproliferation in mice overexpressing gastrin precursors. Cancer Res 65 (2005) 2770-2777
38. Delcommenne M., Tan C., Gray V., et al. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc Natl Acad Sci U S A 95 (1998) 11211-11216
39. Mulrooney J., Foley K., Vineberg S., et al. Phosphorylation of the beta1 integrin cytoplasmic domain: toward an understanding of function and mechanism. Exp Cell Res 258 (2000) 332-341
40. Chung J.H., and Eng C. Nuclear-cytoplasmic partitioning of phosphatase and tensin homologue deleted on chromosome 10 (PTEN) differentially regulates the cell cycle and apoptosis. Cancer Res 65 (2005) 8096-8100
41. Lian Z., and Di Cristofano A. Class reunion: PTEN joins the nuclear crew. Oncogene 24 (2005) 7394-7400
42. Tan C., Costello P., Sanghera J., et al. Inhibition of integrin linked kinase (ILK) suppresses beta-catenin-Lef/Tcf-dependent transcription and expression of the E-cadherin repressor, snail, in APC-/- human colon carcinoma cells. Oncogene 20 (2001) 133-140
43. Koh T.J., Dockray G.J., Varro A., et al. Overexpression of glycine-extended gastrin in transgenic mice results in increased colonic proliferation. J Clin Invest 103 (1999) 1119-1126
44. Wang T.C., Koh T.J., Varro A., et al. Processing and proliferative effects of human progastrin in transgenic mice. J Clin Invest 98 (1996) 1918-1929
45. Potten C.S. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 353 (1998) 821-830