Control of intestinal promoter activity of the cellular migratory regulator gene ELMO3 by CDX2 and SP1

Journal of Cellular Biochemistry

Volumn 109, Issue 6, 2010, Pages 1118-1128

  Coskun, Mehmet ^a   Boyd, Mette ^a   Olsen, Jørgen ^a   Troelsen, Jesper T ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

CDX2; ELMO3; Intestine; Migration; SP1

Indexed keywords

ELMO PROTEIN; GENOMIC DNA; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN; RAC PROTEIN; TRANSCRIPTION FACTOR CDX2; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CANCER CELL; CELL MIGRATION; CELL SPECIFICITY; CELL STRAIN CACO 2; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MICROARRAY; ELMO3 GENE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; INTESTINE VILLUS; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CACO-2 CELLS; CHROMATIN IMMUNOPRECIPITATION; CYTOSKELETAL PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HELA CELLS; HOMEODOMAIN PROTEINS; HT29 CELLS; HUMANS; INTESTINES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SP1 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 77951755076     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22490     Document Type: Article

References (54)

1. Abdelrahim M, Safe S. 2005. Cyclooxygenase-2 inhibitors decrease vascular endothelial growth factor expression in colon cancer cells by enhanced degradation of Sp1 and Sp4 proteins. Mol Pharmacol 68:317-329. (Pubitemid 41058295)
2. Abdelrahim M, Smith R III, Burghardt R, Safe S. 2004. Role of Sp proteins in regulation of vascular endothelial growth factor expression and proliferation of pancreatic cancer cells. Cancer Res 64:6740-6749. (Pubitemid 39297937)
3. Abdelrahim M, Baker CH, Abbruzzese JL, Sheikh-Hamad D, Liu S, Cho SD, Yoon K, Safe S. 2007. Regulation of vascular endothelial growth factor receptor-1 expression by specificity proteins 1, 3 and 4 in pancreatic cancer cells. Cancer Res 67:3286-3294. (Pubitemid 46724867)
4. Bonhomme C, Duluc I, Martin E, Chawengsaksophak K, Chenard MP, Kedinger M, Beck F, Freund JN, Domon-Dell C. 2003. The Cdx2 homeobox gene has a tumour suppressor function in the distal colon in addition to a homeotic role during gut development. Gut 52:1465-1471. (Pubitemid 37176727)
5. Boudreau F, Zhu Y, Traber PG. 2001. Sucrase-isomaltase gene transcription requires the hepatocyte nuclear factor-1 (HNF-1) regulatory element and is regulated by the ratio of HNF-1 alpha to HNF-1 beta. J Biol Chem 276:32122-32128. (Pubitemid 37384873)
6. Boukamel R, Freund JN. 1994. The cis-element CE-LPH1 of the rat intestinal lactase gene promoter interacts in vitro with several nuclear factors present in endodermal tissues. FEBS Lett 353:108-112. (Pubitemid 24312554)
7. Bowzard JB, Cheng D, Peng J, Kahn RA. 2007. ELMOD2 is an Arl2 GTPase-activating protein that also acts on Arfs. J Biol Chem 282:17568-17580. (Pubitemid 47100320)
8. Boyd M, Bressendorff S, Moller J, Olsen J, Troelsen JT. 2009. Mapping of HNF4alpha target genes in intestinal epithelial cells. BMC Gastroenterol 9:68.
9. 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. 2004. 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 64:6973-6977. (Pubitemid 39331007)
10. Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. 1997. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386:84-87. (Pubitemid 27130925)
11. Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F. 2004. Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 101:7641-7645. (Pubitemid 38658082)
12. Cheng H, Leblond CP. 1974. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am J Anat 141:537-561.
13. Chintharlapalli S, Papineni S, Abdelrahim M, Abudayyeh A, Jutooru I, Chadalapaka G, Wu F, Mertens-Talcott S, Vanderlaag K, Cho SD, Smith R III, Safe S. 2009. Oncogenic microRNA-27a is a target for anticancer agent methyl 2-cyano-3,11-dioxo-18beta-olean-1,12-dien-30-oate in colon cancer cells. Int J Cancer 125:1965-1974.
14. Choi BJ, Kim CJ, Cho YG, Song JH, Kim SY, Nam SW, Lee SH, Yoo NJ, Lee JY, Park WS. 2006. Altered expression of CDX2 in colorectal cancers. APMIS 114:50-54. (Pubitemid 43356834)
15. Duprey P, Chowdhury K, Dressler GR, Balling R, Simon D, Guenet JL, Gruss P. 1988. A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev 2: 1647-1654.
16. Fang R, Olds LC, Santiago NA, Sibley E. 2001. GATA family transcription factors activate lactase gene promoter in intestinal Caco-2 cells. AmJ Physiol Gastrointest Liver Physiol 280:G58-G67. (Pubitemid 32466875)
17. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B. 2001. Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 15:2069-2082. (Pubitemid 32762051)
18. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S. 2005. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435:964-968. (Pubitemid 40896323)
19. Freund JN, Domon-Dell C, Kedinger M, Duluc I. 1998. The Cdx-1 and Cdx-2 homeobox genes in the intestine. Biochem Cell Biol 76:957-969. (Pubitemid 29450564)
20. Gao N, White P, Kaestner KH. 2009. Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev Cell 16:588-599.
21. German MS, Wang J, Chadwick RB, Rutter WJ. 1992. Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: Building a functional insulin minienhancer complex. Genes Dev 6:2165-2176.
22. Grimsley CM, Kinchen JM, Tosello-Trampont AC, Brugnera E, Haney LB, Lu M, Chen Q, Klingele D, Hengartner MO, Ravichandran KS. 2004. Dock180 and ELMO1 proteins cooperate to promote evolutionarily conserved Rac-dependent cell migration. J Biol Chem 279:6087-6097. (Pubitemid 38220641)
23. Grimsley CM, Lu M, Haney LB, Kinchen JM, Ravichandran KS. 2006. Characterization of a novel interaction between ELMO1 and ERM proteins. J Biol Chem 281:5928-5937. (Pubitemid 43847693)
24. Grinstein E, Jundt F, Weinert I, Wernet P, Royer HD. 2002. Sp1 as G1 cell cycle phase specific transcription factor in epithelial cells. Oncogene 21:1485-1492. (Pubitemid 34226135)
25. Gross I, Duluc I, Benameur T, Calon A, Martin E, Brabletz T, Kedinger M, Domon-Dell C, Freund JN. 2008. The intestine-specific homeobox gene Cdx2 decreases mobility and antagonizes dissemination of colon cancer cells. Oncogene 27:107-115.
26. Gumienny TL, Brugnera E, Tosello-Trampont AC, Kinchen JM, Haney LB, Nishiwaki K, Walk SF, Nemergut ME, Macara IG, Francis R, Schedl T, Qin Y, Van Aelst L, Hengartner MO, Ravichandran KS. 2001. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107:27-41. (Pubitemid 32972035)
27. Hagen G, Muller S, Beato M, Suske G. 1994. Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J 13:3843-3851. (Pubitemid 24275030)
28. Hardwick JC, Van Den Brink GR, Bleuming SA, Ballester I, Van Den Brande JM, Keller JJ, Offerhaus GJ, Van Deventer SJ, Peppelenbosch MP. 2004. Bone morphogenetic protein 2 is expressed by, and acts upon, mature epithelial cells in the colon. Gastroenterology 126:111-121. (Pubitemid 38040729)
29. Heath JP. 1996. Epithelial cell migration in the intestine. Cell Biol Int 20:139-146.
30. Higgins KJ, Abdelrahim M, Liu S, Yoon K, Safe S. 2006. Regulation of vascular endothelial growth factor receptor-2 expression in pancreatic cancer cells by Sp proteins. Biochem Biophys Res Commun 345:292-301. (Pubitemid 44269283)
31. Hinoi T, GesinaG,AkyolA, Kuick R, Hanash S, Giordano TJ,Gruber SB, Fearon ER. 2005. CDX2-regulated expression of iron transport protein hephaestin in intestinal and colonic epithelium. Gastroenterology 128:946-961. (Pubitemid 40523546)
32. Kaimaktchiev V, Terracciano L, Tornillo L, Spichtin H, Stoios D, Bundi M, Korcheva V, Mirlacher M, Loda M, Sauter G, Corless CL. 2004. The homeobox intestinal differentiation factor CDX2 is selectively expressed in gastrointestinal adenocarcinomas. Mod Pathol 17:1392-1399. (Pubitemid 39472995)
33. Kajiwara M, Terada T, Asaka J, Ogasawara K, Katsura T, Ogawa O, Fukatsu A, Doi T, Inui K. 2007. Critical roles of Sp1 in gene expression of human and rat H+/organic cation antiporter MATE1. Am J Physiol Renal Physiol 293:F1564-F1570. (Pubitemid 350085992)
34. Katoh H, Negishi M. 2003. RhoG activates Rac1 by direct interaction with the Dock180-binding protein Elmo. Nature 424:461-464. (Pubitemid 36917498)
35. Komander D, Patel M, Laurin M, Fradet N, Pelletier A, Barford D, Cote JF. 2008. An alpha-helical extension of the ELMO1 pleckstrin homology domain mediates direct interaction to DOCK180 and is critical in Rac signaling. Mol Biol Cell 19:4837-4851.
36. Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Munch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S, Wingender E. 2003. TRANSFAC: Transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31:374-378. (Pubitemid 36150406)
37. Modica S, Morgano A, Salvatore L, Petruzzelli M, Vanier MT, Valanzano R, Esposito DL, Palasciano G, Duluc I, Freund JN, Mariani-Costantini R, Moschetta A. 2009. Expression and localisation of insulin receptor substrate 2 in normal intestine and colorectal tumours. Regulation by intestinespecific transcription factor CDX2. Gut 58:1250-1259.
38. Nishida H, Suzuki T, Kondo S, Miura H, Fujimura Y, Hayashizaki Y. 2006. Histone H3 acetylated at lysine 9 in promoter is associated with low nucleosome density in the vicinity of transcription start site in human cell. Chromosome Res 14:203-211.
39. Odom DT, Zizlsperger N, Gordon DB, Bell GW, Rinaldi NJ, Murray HL, Volkert TL, Schreiber J, Rolfe PA, Gifford DK, Fraenkel E, Bell GI, Young RA. 2004. Control of pancreas and liver gene expression by HNF transcription factors. Science 303:1378-1381. (Pubitemid 38269432)
40. Olsen J, Kirkeby LT, Brorsson MM, Dabelsteen S, Troelsen JT, Bordoy R, Fenger K, Larsson LI, Simon-Assmann P. 2003. Converging signals synergistically activate the LAMC2 promoter and lead to accumulation of the laminin gamma 2 chain in human colon carcinoma cells. Biochem J 371:211-221. (Pubitemid 36458096)
41. Pinto D, Gregorieff A, Begthel H, Clevers H. 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev 17:1709-1713. (Pubitemid 36870334)
42. Rao JN, Li J, Li L, Bass BL, Wang JY. 1999. Differentiated intestinal epithelial cells exhibit increased migration through polyamines and myosin II. Am J Physiol 277:G1149-G1158. (Pubitemid 30046016)
43. Rings EH, Boudreau F, Taylor JK, Moffett J, Suh ER, Traber PG. 2001. Phosphorylation of the serine 60 residue within the Cdx2 activation domain mediates its transactivation capacity. Gastroenterology 121:1437-1450. (Pubitemid 33140461)
44. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386.
45. Schjoldager KT, Maltesen HR, Balmer S, Lund LR, Claesson MH, Sjostrom H, Troelsen JT, Olsen J. 2008. Cellular cross talk in the small intestinal mucosa: Postnatal lymphocytic immigration elicits a specific epithelial transcriptional response. Am J Physiol Gastrointest Liver Physiol 294:G1335-G1343.
46. Shimakura J, Terada T, Katsura T, Inui K. 2005. Characterization of the human peptide transporter PEPT1 promoter: Sp1 functions as a basal transcriptional regulator of human PEPT1. Am J Physiol Gastrointest Liver Physiol 289:G471-G477. (Pubitemid 41216384)
47. Shimakura J, Terada T, Shimada Y, Katsura T, Inui K. 2006. The transcription factor Cdx2 regulates the intestine-specific expression of human peptide transporter 1 through functional interaction with Sp1. Biochem Pharmacol 71:1581-1588.
48. Silberg DG, Swain GP, Suh ER, Traber PG. 2000. Cdx1 and cdx2 expression during intestinal development. Gastroenterology 119:961-971.
49. Stegmann A, Hansen M, Wang Y, Larsen JB, Lund LR, Ritie L, Nicholson JK, Quistorff B, Simon-Assmann P, Troelsen JT, Olsen J. 2006. Metabolome, transcriptome, and bioinformatic cis-element analyses point to HNF-4 as a central regulator of gene expression during enterocyte differentiation. Physiol Genomics 27:141-155. (Pubitemid 46705407)
50. Troelsen JT, Mitchelmore C, Spodsberg N, Jensen AM, Noren O, Sjostrom H. 1997. Regulation of lactase-phlorizin hydrolase gene expression by the caudal-related homoeodomain protein Cdx-2. Biochem J 322(Pt 3): 833-838. (Pubitemid 27135632)
51. Uesaka T, Kageyama N, Watanabe H. 2004. Identifying target genes regulated downstream of Cdx2 by microarray analysis. J Mol Biol 337:647-660. (Pubitemid 38331980)
52. Vivanco I, Sawyers CL. 2002. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2:489-501. (Pubitemid 37328931)
53. Wierstra I. 2008. Sp1: Emerging roles - Beyond constitutive activation of TATA-less housekeeping genes. Biochem Biophys Res Commun 372:1-13.
54. Zhou Z, Caron E, Hartwieg E, Hall A, Horvitz HR. 2001. The C. elegans pH domain protein CED-12 regulates cytoskeletal reorganization via a Rho/Rac GTPase signaling pathway. Dev Cell 1:477-489. (Pubitemid 33586100)