The microenvironment controls CDX2 homeobox gene expression in colorectal cancer cells

American Journal of Pathology

Volumn 170, Issue 2, 2007, Pages 733-744

  Benahmed, Fairouz ^a   Gross, Isabelle ^a   Guenot, Dominique ^a   Jehan, Frédéric ^a   Martin, Elisabeth ^a   Domon Dell, Claire ^a   Brabletz, Thomas ^b   Kedinger, Michèle ^a   Freund, Jean Noël ^a   Duluc, Isabelle ^a  

^a INSERM   (France)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR CDX2; CDX2 PROTEIN, HUMAN; CDX2 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; COLORECTAL CANCER; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; HETEROTOPIC TRANSPLANTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; SKIN FIBROBLAST; ADULT; ANIMAL; BIOSYNTHESIS; CANCER INVASION; CANCER TRANSPLANTATION; CECUM; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; MOUSE; NUDE MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ADULT; ANIMALS; CECUM; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; PROMOTER REGIONS (GENETICS); RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS;

EID: 33947536361     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.060696     Document Type: Article

References (34)

1. Diep CB, Kleivi K, Ribeiro FR, Teixeira MR, Lindgjaerde OC, Lothe RA: The order of genetic events associated with colorectal cancer progression inferred from meta-analysis of copy number changes. Genes Chromosom Cancer 2006, 45:31-41
2. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T: Migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 2005, 5:744-749
3. Brabletz T, Spaderna S, Kolb J, Hlubek F, Faller G, Bruns CJ, Jung A, Nentwich J, Duluc I, Domon-Dell C, Kirchner T, Freund JN: Down-regulation of the homeodomain factor cdx2 in colorectal cancer by collagen type I: an active role for the tumor environment in malignant tumor progression. Cancer Res 2004, 64:6973-6977
4. Beck F, Chawengsaksophak K, Waring P, Playford RJ, Furness JB: Reprogramming of intestinal differentiation and intercalary regeneration in cdx2 mutant mice. Proc Natl Acad Sci USA 1999, 96:7318-7323
5. Mutoh H, Hakamata Y, Sato K, Eda A, Yanaka I, Honda S, Osawa H, Kaneko Y, Sugano K: Conversion of gastric mucosa to intestinal metaplasia in Cdx2-expressing transgenic mice. Biochem Biophys Res Commun 2002, 294:470-479
6. Silberg DG, Sullivan J, Kang E, Swain GP, Moffett J, Sund NJ, Sackett SD, Kaestner KH: Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology 2002, 122:689-696
7. Tamai Y, Nakajima R, Ishikawa T, Takaku K, Seldin MF, Taketo MM: Colonic hamartoma development by anomalous duplication in Cdx2 knockout mice. Cancer Res 1999, 59:2965-2970
8. Lorentz O, Duluc I, De Arcangelis A, Simon-Assmann P, Kedinger M, Freund JN: Key role of the Cdx2 homeobox gene in extracellular matrix-mediated intestinal cell differentiation. J Cell Biol 1997, 139:1553-1565
9. Suh E, Traber PG: An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol 1996, 16:619-625
10. Aoki K, Tamai Y, Horiike S, Oshima M, Taketo MM: Colonic polyposis caused by mTOR-mediated chromosomal instability in Apc(+/Delta716) Cdx2(+/-) compound mutant mice. Nat Genet 2003, 35:323-330
11. Bonhomme C, Duluc I, Martin E, Chawengsaksophak K, Chenard MP, Kedinger M, Beck F, Freund JN, Domon-Dell C: The Cdx2 homeobox gene has a tumour suppressor function in the distal colon in addition to a homeotic role during gut development. Gut 2003, 52:1465-1471
12. Ee HC, Erler T, Bhathal PS, Young GP, James RJ: Cdx-2 homeodomain protein expression in human and rat colorectal adenoma and carcinoma. Am J Pathol 1995, 147:586-592
13. Hinoi T, Tani M, Lucas PC, Caca K, Dunn RL, Macri E, Loda M, Appelman HD, Cho KR, Fearon R: Loss of CDX2 expression and microsatellite instability are prominent features of large cell minimally differentiated carcinomas of the colon. Am J Pathol 2001, 159:2239-2248
14. Subtil C, Guérin E, Schneider A, Chenard MP, Martin E, Domon-Dell C, Duluc I, Brabletz T, Kedinger M, Duclos B, Gaub MP, Freund JN: Frequent rearrangements and amplification of the CDX2 homeobox gene in human sporadic colorectal cancers with chromosomal instability. Cancer Lett (in press)
15. Hinoi T, Loda M, Fearon ER: Silencing of CDX2 expression in colon cancer via a dominant repression pathway. J Biol Chem 2003, 278:44608-44616
16. Yagi OK, Akiyama Y, Yuasa Y: Genomic structure and alterations of homeobox gene CDX2 in colorectal carcinomas. Br J Cancer 1999, 79:440-444
17. Duluc I, Lorentz O, Fritsch C, Leberquier C, Kedinger M, Freund JN: Changing intestinal connective tissue interactions alters homeobox gene expression in epithelial cells. J Cell Sci 1997, 110:1317-1324
18. Choudhury A, Moniaux N, Ulrich AB, Schmied BM, Standop J, Pour PM, Gendler SJ, Hollingsworth MA, Aubert JP, Batra SK: MUC4 mucin expression in human pancreatic tumours is affected by organ environment: the possible role of TGFbeta2. Br J Cancer 2004, 90:657-664
19. Guenot D, Guerin E, Aguillon-Romain S, Pencreach E, Schneider A, Neuville A, Chenard MP, Duluc I, du Manoir S, Brigand C, Oudet P, Kedinger M, Gaub MP: Primary tumour genetic alterations and intratumoral heterogeneity are maintained in xenografts of human colon cancers showing chromosome instability. J Pathol 2006, 208:643-652
20. Plateroti M, Rubin DC, Duluc I, Singh R, Foltzer-Jourdainne C, Freund JN, Kedinger M: Subepithelial fibroblast cell lines from different levels of gut axis display regional characteristics. Am J Physiol 1998, 274:G945-G954
21. Hsieh JJ, Henkel T, Salmon P, Robey E, Peterson MG, Hayward SD: Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol Cell Biol 1996, 16:952-959
22. Tani S, Kurooka H, Aoki T, Hashimoto N, Honjo T: The N- and C-terminal regions of RBP-J interact with the ankyrin repeats of Notch1 RAMIC to activate transcription. Nucleic Acids Res 2001, 29:1373-1380
23. Gross I, Lhermitte B, Domon-Dell C, Duluc I, Martin E, Gaiddon C, Kedinger M, Freund JN: Phosphorylation of the homeotic tumor suppressor Cdx2 mediates its ubiquitin-dependent proteasome degradation. Oncogene 2005, 24:7955-7963
24. Lorentz O, Cadoret A, Duluc I, Capeau J, Gespach C, Cherqui G, Freund JN: Downregulation of the colon tumour-suppressor homeobox gene Cdx-2 by oncogenic ras. Oncogene 1999, 18:87-92
25. Blache P, van de Wetering M, Duluc I, Domon C, Berta P, Freund JN, Clevers H, Jay P: SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 2004, 166:37-47
26. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S: Notch signals control the fate of immature progenitor cells in the intestine. Nature 2005, 435:964-968
27. van Es JH, van Gijn ME, Riccio O, van den BM, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H: Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005, 435:959-963
28. Mesquita P, Jonckheere N, Almeida R, Ducourouble MP, Serpa J, Silva E, Pigny P, Silva FS, Reis C, Silberg D, Van Seuningen I, David L: Human MUC2 mucin gene is transcriptionally regulated by cdx homeodomain proteins in gastrointestinal carcinoma cell lines. J Biol Chem 2003, 278:51549-51556
29. Yamamoto H, Bai YQ, Yuasa Y: Homeodomain protein CDX2 regulates goblet-specific MUC2 gene expression. Biochem Biophys Res Commun 2003, 300:813-818
30. Le Brigand K, Russell R, Moreilhon C, Rouillard JM, Jost B, Amiot F, Magnone V, Bole-Feysot C, Rostagno P, Virolle V, Defamie V, Dessen P, Williams G, Lyons P, Rios G, Mari B, Gulari E, Kastner P, Gidrol X, Freeman TC, Barbry P: An open-access long oligonucleotide microarray resource for analysis of the human and mouse transcriptomes. Nucleic Acids Res 2006, 34: (in press)
31. Balda MS, Matter K: The tight junction protein ZO-1 and an interacting transcription factor regulate ErbB-2 expression. EMBO J 2000, 19:2024-2033
32. Uesaka T, Kageyama N, Watanabe H: Identifying target genes regulated downstream of cdx2 by microarray analysis. J Mol Biol 2004, 337:647-660
33. Kim S, Domon-Dell C, Wang Q, Chung DH, Di Cristofano A, Pandolfi PP, Freund JN, Evers BM: PTEN and TNF-α regulation of the intestinal-specific Cdx-2 homeobox gene through a PI3K, PKB/Akt, and NF-kappaB-dependent pathway. Gastroenterology 2002, 123:1163-1178
34. Turck N, Gross I, Gendry P, Stutzmann J, Freund JN, Kedinger M, Simon-Assmann P, Launay JF: Laminin isoforms: biological roles and effects on the intracellular distribution of nuclear proteins in intestinal epithelial cells. Exp Cell Res 2005, 303:494-503