A key role for E-cadherin in intestinal homeostasis and paneth cell maturation

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Schneider, Marlon R ^a   Dahlhoff, Maik ^a   Horst, David ^a,d   Hirschi, Benjamin ^b   Trülzsch, Konrad ^a   Müller Höcker, Josef ^a   Vogelmann, Roger ^c   Allgäuer, Michael ^c   Gerhard, Markus ^c   Steininger, Sylvia ^c   Wolf, Eckhard ^a   Kolligs, Frank T ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UVOMORULIN; CADHERIN; CELL CYCLE PROTEIN; FZR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; BLOODY DIARRHEA; CELL DIFFERENTIATION; CELL JUNCTION; CELL MATURATION; CELL MIGRATION; COLON MUCOSA; CONTROLLED STUDY; CRYPT CELL; DESMOSOME; DISEASE DURATION; GENE FUNCTION; GENE INACTIVATION; GENE LOCATION; GOBLET CELL; INNATE IMMUNITY; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PANETH CELL; PROTEIN DEPLETION; SMALL INTESTINE MUCOSA; TISSUE DISTRIBUTION; ANIMAL; BIOSYNTHESIS; CELL DEATH; COLON; CROHN DISEASE; CYTOLOGY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; HOMOZYGOTE; METABOLISM; PHYSIOLOGY; SMALL INTESTINE; TRANSGENIC MOUSE;

BACTERIA (MICROORGANISMS); MUS;

ANIMALS; CADHERINS; CELL CYCLE PROTEINS; CELL DEATH; COLON; CROHN DISEASE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GOBLET CELLS; HOMEOSTASIS; HOMOZYGOTE; INTESTINE, SMALL; MICE; MICE, TRANSGENIC; PANETH CELLS;

EID: 78650775249     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014325     Document Type: Article

References (54)

1. Meddings J (2008) The significance of the gut barrier in disease. Gut 57: 438-440.
2. Barker N, Clevers H (2007) Tracking down the stem cells of the intestine: strategies to identify adult stem cells. Gastroenterology 133: 1755-1760.
3. Scoville DH, Sato T, He XC, Li L (2008) Current view: intestinal stem cells and signaling. Gastroenterology 134: 849-864.
4. Laukoetter MG, Nava P, Nusrat A (2008) Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol 14: 401-407.
5. Kottke MD, Delva E, Kowalczyk AP (2006) The desmosome: cell science lessons from human diseases. J Cell Sci 119: 797-806.
6. Halbleib JM, Nelson WJ (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-3214.
7. Larue L, Ohsugi M, Hirchenhain J, Kemler R (1994) E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci U S A 91: 8263-8267.
8. Jankowski JA, Bedford FK, Boulton RA, Cruickshank N, Hall C, et al. (1998) Alterations in classical cadherins associated with progression in ulcerative and Crohn's colitis. Lab Invest 78: 1155-1167.
9. Gassler N, Rohr C, Schneider A, Kartenbeck J, Bach A, et al. (2001) Inflammatory bowel disease is associated with changes of enterocytic junctions. Am J Physiol Gastrointest Liver Physiol 281: G216-G228.
10. Kucharzik T, Walsh SV, Chen J, Parkos CA, Nusrat A (2001) Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol 159: 2001-2009.
11. Bruewer M, Samarin S, Nusrat A (2006) Inflammatory bowel disease and the apical junctional complex. Ann N Y Acad Sci 1072: 242-252.
12. Muise AM, Walters TD, Glowacka WK, Griffiths AM, Ngan BY, et al. (2009) Polymorphisms in E-cadherin (CDH1) result in a mis-localized cytoplasmic protein that is associated with Crohn's Disease. Gut 58(8): 1121-1127.
13. Smits R, Ruiz P, Diaz-Cano S, Luz A, Jagmohan-Changur S, et al. (2000) Ecadherin and adenomatous polyposis coli mutations are synergistic in intestinal tumor initiation in mice. Gastroenterology 119: 1045-1053.
14. Hermiston ML, Gordon JI (1995) Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270: 1203-1207.
15. Smalley-Freed WG, Efimov A, Burnett PE, Short SP, Davis MA, et al. (2010) p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J Clin Invest 120: 1824-1835.
16. Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R (2002) E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev 115: 53-62.
17. el Marjou F, Janssen KP, Chang BH, Li M, Hindie V, et al. (2004) Tissuespecific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39: 186-193.
18. Loessner H, Endmann A, Leschner S, Westphal K, Rohde M, et al. (2007) Remote control of tumour-targeted Salmonella enterica serovar Typhimurium by the use of L-arabinose as inducer of bacterial gene expression in vivo. Cell Microbiol 9: 1529-1537.
19. Oellerich MF, Jacobi CA, Freund S, Niedung K, Bach A, et al. (2007) Yersinia enterocolitica infection of mice reveals clonal invasion and abscess formation. Infect Immun 75: 3802-3811.
20. Moolenbeek C, Ruitenberg EJ (1981) The ''Swiss roll'': a simple technique for histological studies of the rodent intestine. Lab Anim 15: 57-59.
21. Gregorieff A, Grosschedl R, Clevers H (2004) Hindgut defects and transformation of the gastro-intestinal tract in Tcf4(2/2)/Tcf1(2/2) embryos. EMBO J 23: 1825-1833.
22. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, et al. (2002) Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111: 251-263.
23. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, et al. (2004) Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18: 1385-1390.
24. Salzman NH, Ghosh D, Huttner KM, Paterson Y, Bevins CL (2003) Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 422: 522-526.
25. Porter EM, Bevins CL, Ghosh D, Ganz T (2002) The multifaceted Paneth cell. Cell Mol Life Sci 59: 156-170.
26. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, et al. (2005) Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7: 381-386.
27. 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.
28. Mori-Akiyama Y, van den Borm M, van Es JH, Hamilton SR, Adams HP, et al. (2007) SOX9 is required for the differentiation of paneth cells in the intestinal epithelium. Gastroenterology 133: 539-546.
29. Bastide P, Darido C, Pannequin J, Kist R, Robine S, et al. (2007) Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J Cell Biol 178: 635-648.
30. Varnat F, Heggeler BB, Grisel P, Boucard N, Corthesy-Theulaz I, et al. (2006) PPARbeta/delta regulates paneth cell differentiation via controlling the hedgehog signaling pathway. Gastroenterology 131: 538-553.
31. Ireland H, Kemp R, Houghton C, Howard L, Clarke AR, et al. (2004) Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology 126: 1236-1246.
32. Fevr T, Robine S, Louvard D, Huelsken J (2007) Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol 27: 7551-7559.
33. Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY (2001) Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294: 2155-2158.
34. Shroyer NF, Helmrath MA, Wang VY, Antalffy B, Henning SJ, et al. (2007) Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132: 2478-2488.
35. Lee CS, Perreault N, Brestelli JE, Kaestner KH (2002) Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev 16: 1488-1497.
36. Jenny M, Uhl C, Roche C, Duluc I, Guillermin V, et al. (2002) Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J 21: 6338-6347.
37. Stappenbeck TS, Gordon JI (2000) Rac1 mutations produce aberrant epithelial differentiation in the developing and adult mouse small intestine. Development 127: 2629-2642.
38. Braga VM (2002) Cell-cell adhesion and signalling. Curr Opin Cell Biol 14: 546-556.
39. Young P, Boussadia O, Halfter H, Grose R, Berger P, et al. (2003) E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles. EMBO J 22: 5723-5733.
40. Tinkle CL, Lechler T, Pasolli HA, Fuchs E (2004) Conditional targeting of Ecadherin in skin: insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci U S A 101: 552-557.
41. Tunggal JA, Helfrich I, Schmitz A, Schwarz H, Gunzel D, et al. (2005) Ecadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J 24: 1146-1156.
42. Gumbiner B, Stevenson B, Grimaldi A (1988) The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol 107: 1575-1587.
43. Fouquet S, Lugo-Martinez VH, Faussat AM, Renaud F, Cardot P, et al. (2004) Early loss of E-cadherin from cell-cell contacts is involved in the onset of Anoikis in enterocytes. J Biol Chem 279: 43061-43069.
44. Hermiston ML, Gordon JI (1995) In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J Cell Biol 129: 489-506.
45. Williams EJ, Furness J, Walsh FS, Doherty P (1994) Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and Ncadherin. Neuron 13: 583-594.
46. Suyama K, Shapiro I, Guttman M, Hazan RB (2002) A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2: 301-314.
47. Hermiston ML, Wong MH, Gordon JI (1996) Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev 10: 985-996.
48. Wu S, Lim KC, Huang J, Saidi RF, Sears CL (1998) Bacteroides fragilis enterotoxin cleaves the zonula adherens protein, E-cadherin. Proc Natl Acad Sci U S A 95: 14979-14984.
49. Chambers FG, Koshy SS, Saidi RF, Clark DP, Moore RD, et al. (1997) Bacteroides fragilis toxin exhibits polar activity on monolayers of human intestinal epithelial cells (T84 cells) in vitro. Infect Immun 65: 3561-3570.
50. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H (2005) Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 43: 3380-3389.
51. Keighley MR, Eastwood D, Ambrose NS, Allan RN, Burdon DW (1982) Incidence and microbiology of abdominal and pelvic abscess in Crohn's disease. Gastroenterology 83: 1271-1275.
52. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, et al. (2005) Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc Natl Acad Sci U S A 102: 18129-18134.
53. Zbar AP, Simopoulos C, Karayiannakis AJ (2004) Cadherins: an integral role in inflammatory bowel disease and mucosal restitution. J Gastroenterol 39: 413-421.
54. Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.