TFF3 and EGF induce different migration patterns of intestinal epithelial cells in vitro and trigger increased internalization of E-cadherin

Cellular Physiology and Biochemistry

Volumn 20, Issue 5, 2007, Pages 329-346

  Dürer, Uwe ^a   Hartig, Roland ^a   Bang, Susanne ^b   Thim, Lars ^b   Hoffmann, Werner ^a,c  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b NOVO NORDISK A S   (Denmark)

^c UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

Author keywords

Adherens junction; Cell migration; Cell cell contact; E cadherin; EGF; Epithelial repair; Epithelial mesenchymal transition; Restitution; TFF domain; Time lapse video microscopy; Trefoil factor

Indexed keywords

EPIDERMAL GROWTH FACTOR; TREFOIL FACTOR FAMILY 3; TREFOIL PEPTIDE; UNCLASSIFIED DRUG; UVOMORULIN;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL STRUCTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; FIBROBLAST; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; INTESTINE EPITHELIUM CELL; MICROSCOPY; MORPHOMETRICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SCRATCH WOUND ASSAY;

LOTUS;

EID: 34548361215     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000107519     Document Type: Article

References (78)

1. Suemori S, Lynch-Devaney K, Podolsky DK: Identification and characterization of rat intestinal trefoil factor: tissue- and cell-specific member of the trefoil protein family. Proc Natl Acad Sci USA 1991;88:11017-11021.
2. Hauser F, Poulsom R, Chinery R, Rogers LA, Hanby AM, Wright NA, Hoffmann W: hP1.B, a human P-domain peptide homologous with rat intestinal trefoil factor, is expressed also in the ulcer-associated cell lineage and the uterus. Proc Natl Acad Sci USA 1993;90:6961-6965.
3. Madsen J, Nielsen O, Tornoe I, Thim L, Holmskov U: Tissue localization of human trefoil factor 1, 2 and 3. J. Histochem. Cytochem 2007;55:505-513.
4. Kouznetsova I, Kalinski T, Peitz U, Mönkemüller KE, Kalbacher H, Vieth M, Meyer F, Roessner A, Malfertheiner P, Lippert H, Hoffmann W: Localization of TFF3 peptide in human esophageal submucosal glands and gastric cardia: differentiation of two types of gastric pit cells along the rostro-caudal axis. Cell Tissue Res 2007;328:365-374.
5. Wong WM, Poulsom R, Wright NA: Trefoil peptides. Gut 1999;44:890-895.
6. Hoffmann W, Jagla W, Wiede A. Molecular medicine of TFF-peptides: from gut to brain. Histol Histopathol 2001;16:319-334.
7. Hoffmann W: TFF (trefoil factor family) peptides. In: Kastin AJ (ed): Handbook of Biologically Active Peptides. San Diego, Elsevier, 2006, pp 1147-1154.
8. Paulsen FP, Berry MS: Mucins and TFF peptides of the tear film and lacrimal apparatus. Prog Histochem Cytochem 2006;41:1-53.
9. Jackerott M, Lee YC, Mollgard K, Kofod H, Jensen J, Rohleder S, Neubauer N, Gaarn LW, Lykke J, Dodge R, Dalgaard LT, Sostrup B, Jensen DB, Thim L, Nexo E, Thams P, Bisgaard HC, Nielsen JH: Trefoil factors are expressed in human and rat endocrine pancreas: differential regulation by growth hormone. Endocrinology 2006;147:5752-5759.
10. Hinz M, Schwegler H, Chwieralski CE, Laube G, Linke R, Pohle W, Hoffmann W: Trefoil factor family (TFF) expression in the mouse brain and pituitary: changes in the developing cerebellum. Peptides 2004;25:827-832.
11. Wong WM, Playford RJ, Wright NA: Peptide gene expression in gastrointestinal mucosal ulceration: ordered sequence or redundancy? Gut 2000;46:286-292.
12. Hoffmann W, Jagla W: Cell type specific expression of secretory TFF peptides: colocalization with mucins and synthesis in the brain. Int Rev Cytol 2002;213:147-181.
13. Emami S, Rodrigues S, Rodrigue CM, Le Floch N, Rivat C, Attoub S, Bruyneel E, Gespach C: Trefoil factor family (TFF) peptides and cancer progression. Peptides 2004;25:885-898.
14. Regalo G, Wright NA, Machado JC: Trefoil factors: from ulceration to neoplasia. Cell Mol Life Sci 2005;62:2910-2915.
15. Yio X, Zhang JY, Babyatsky M, Chen A, Lin J, Fan QX, Werther JL, Itzkowitz S: Trefoil factor family-3 is associated with aggressive behaviour of colon cancer cells. Clin Exp Metastasis 2005;22:157-165.
16. Wright NA: Aspects of the biology of regeneration and repair in the human gastrointestinal tract. Phil Trans R Soc Lond 1998;B 353:925-933.
17. Zhang BH, Yu HG, Sheng ZX, Luo HS, Yu JP: The therapeutic effect of recombinant human trefoil factor 3 on hypoxia-induced necrotizing enterocolitis in immature rat. Regul Peptides 2003;116:53-60.
18. Beck PL, Wong JF, Li Y, Swaminathan S, Xavier RJ, Devaney KL, Podolsky DK: Chemotherapy- and radiotherapy-induced intestinal damage is regulated by intestinal trefoil factor. Gastroenterology 2004;126:796-808.
19. Vandenbroucke K, Hans W, van Huysse J, Neirynck S, Demetter P, Remaut E, Rottiers P, Steidler L: Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology 2004;127:502-513.
20. Poulsen SS, Kissow H, Hare K, Hartmann B, Thim L: Luminal and parenteral TFF2 and TFF3 dimer and monomer in two models of experimental colitis in the rat. Regul Peptides 2005;126:163-171.
21. Taupin D, Podolsky DK: Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 2003;4:721-732.
22. Playford RJ: Peptides and gastrointestinal mucosal integrity. Gut 1995;37:595-597.
23. Playford RJ, Ghosh S: Cytokines and growth factor modulators in intestinal inflammation and repair. J Pathol 2005;205:417-425.
24. Lacy ER: Epithelial restitution in the gastrointestinal tract. J Clin Gastroenterol 1988;10(Suppl. 1):S72-S77.
25. Hoffmann W: TFF-triggered signals promoting restitution of mucous epithelia. Cell Mol Life Sci 2005;62:2932-2938.
26. Emami S, Le Flock N, Bruyneel L, Thim L, May F, Westley B, Rio MC, Mareel M, Gespach C: Induction of scattering and cellular invasion by trefoil peptides in src-and RhoA-transformed kidney and colonic epithelial cells. FASEB J 2001;15:351-361.
27. Rodrigues S, Attoub S, Hguyen QD, Bruyneel E, Rodrigue CM, Westley BR, May FEB, Thim L, Mareel M, Emami S, Gespach C: Selective abrogation of the proinvasive activity of the trefoil peptides pS2 and spasmolytic polypeptide by disruption of the EGF receptor signaling pathways in kidney and colonic cancer cells. Oncogene 2003;22:4488-4497.
28. Liu D, El-Hariry I, Karayiannakis AJ, Wilding J, Chinery R, Kmiot W, McCrea PD, Gullick WJ, Pignatelli M: Phosphorylation of ß-catenin and epidermal growth factor receptor by intestinal trefoil factor. Lab Invest 1997;77:557-563.
29. Efstathiou, JA, Noda, M, Rowan, A, Dixon, C, Chinery, R, Jawhari, A, Hattori, T, Wright, NA, Bodmer, WF, Pignatelli, M: Intestinal trefoil factor controls the expression of the adenomatous polyposis coli-catenin and the E-cadherincatenin complexes in human colon carcinoma cells. Proc Natl Acad Sci USA 1998;95:3122-3127.
30. Meyer zum Büschenfelde D, Hoschützky H, Tauber R, Huber O: Molecular mechanisms involved in TFF3 peptide-mediated modulation of the E-cadherin/catenin cell adhesion complex. Peptides 2004;25:873-883.
31. Chan, VYW, Chan MWY, Leung WK, Leung PS, Sung JJY, Chan, FKL: Intestinal trefoil factor promotes invasion in non-tumorigenic Rat-2 fibroblast cell. Regul Peptides 2005;127:87-94.
32. Meyer zum Büschenfelde D, Tauber R, Huber O: TFF3-peptide increases transepithelial resistance in epithelial cells by modulating claudin-1 and -2 expression. Peptides 2006;27:3383-3390.
33. Dignass A, Lynch-Devaney K, Kindon H, Thim L, Podolsky DK: Trefoil peptides promote epithelial migration through a transforming growth factor ß-independent pathway. J Clin Invest 1994;94:376-383.
34. Kinoshita T, Taupin, DR, Itoh H, Podolsky, DK: Distinct pathways of cell migration and antiapoptotic response to epithelial injury: structure-function analysis of human intestinal trefoil factor. Mol Cell Biol 2000;20:4680-4690.
35. Chwieralski CE, Schnurra I, Thim L, Hoffmann W: Epidermal growth factor and trefoil factor family 2 synergistically trigger chemotaxis on BEAS-2B cells via different signaling cascades. Am J Respir Cell Mol Biol 2004;31:528-537.
36. Cho SY, Klemke RL: Extracellular-regulated kinase activation and CAS/Crk coupling regulate cell migration and suppress apoptosis during invasion of the extracellular matrix. J Cell Biol 2000;149;223-236.
37. Taupin DR, Kinoshita K, Podolsky, DK: Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc Natl Acad Sci USA 2000;97:799-804.
38. Chen, YH, Lu, Y, De Plaen, IG, Wang, LY, Tan, XD: Transcription factor NF-κB signals antianoikic function of trefoil factor 3 on intestinal epithelial cells. Biochem Biophys Res Commun 2000;274:576-582.
39. Chan MWY, Chan VYW, Leung WK, Chan KK, To KF, Sung JJY, Chan FKL: Anti-sense trefoil factor family-3 (intestinal trefoil factor) inhibits cell growth and induces chemosensitivity to adriamycin in human gastric cancer cells. Life Sci 2005;76:2581-2592.
40. Wang H, Tong Y, Fang M, Ru B: High-level expression of human TFF3 in Escherichia coli. Peptides 2005; 26:1213-1218.
41. Goodlad RA, Wright NA: Epidermal growth factor and transforming growth factor-α actions on the gut. Eur J Gastroenterol Hepatol 1995;7:928-932.
42. Barnard JA, Beachamp RD, Russell WE, Dubios RN, Coffey RJ: Epidermal growth factor-related peptides and their relevance to gastrointestinal pathophysiology. Gastroenterology 1995;108:564-580.
43. Andl CD, Mizushima T, Nakagawa H, Oyama K, Harada H, Chruma K, Herlyn M, Rustgi AK: Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. J Biol Chem 2003;278:1824-1830.
44. Oertel M, Graness A, Thim L, Bühling F, Kalbacher H, Hoffmann W: Trefoil factor family-peptides promote migration of human bronchial epithelial cells: synergistic effect with epidermal growth factor. Am J Respir Cell Mol Biol 2001;25:418-424.
45. Chinery R, Playford RJ: Combined intestinal trefoil factor and epidermal growth factor is prophylactic against indomethacin-induced gastric damage in the rat. Clin Sci 1995;88:401-403.
46. FitzGerald AJ, Pu M, Marchbank T, Westley BR, May FEB, Boyle J, Yadollahi-Farsani M, Ghosh S, Playford RJ: Synergistic effects of systemic trefoil factor family 1 (TFF1) peptide and epidermal growth factor in a rat model of colitis. Peptides 2004;25:793-801.
47. McCormack SA, Viar MJ, Johnson LR: Migration of IEC-6 cells: a model for mucosal healing. Am J Physiol 1992;263:G426-G435.
48. Quaroni A, Isselbacher KJ: Cytotoxic effects and metabolism of benzo(a)pyrene and 7,12-dimethylbenz(a)anthracene in duodenal and ileal epithelial cell cultures. J Natl Cancer Inst 1981;67:1353-1362.
49. Garner CM, Hubbold LM, Chakraborti PR: Mycoplasma detection in cell cultures: a comparison of four methods. Br J Biomed Sci 2000;57:295-301.
50. Thim L, Wöldike HF, Nielsen PF, Christensen M, Lynch-Devaney K, Podolsky DK: Characterization of human and rat intestinal trefoil factor produced in yeast. Biochemistry 1995;34:4757-4764.
51. Bedner E, Li X, Gorczyca W, Melamed MR, Darzynkiewicz Z: Analysis of apoptosis by laser scanning cytometry. Cytometry 1999;35:181-195.
52. Holubec H, Payne CM, Bernstein H, Dvorakova K, Bernstein C, Waltmire CN, Warneke JA, Garewal H: Assessment of apoptosis by immunhistochemical markers compared to cellular morphology in ex vivo-stressed colonic mucosa. J Histochem Cytochem 2005;53:229-235.
53. Porter AG, Jänicke RU: Emerging roles of caspase-3 in apoptosis. Cell Death Diff 1999;6:99-104.
54. Van Diest PJ, Baak JP, Matze-Cok P: Reproducibility of mitosis counting in 2.469 breast cancer specimens: results from the multicenter morphometric mammary carcinoma project. Hum Pathol 1992;23:603-607.
55. Grünert S, Jechlinger M, Beug H: Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat Rev Mol Cell Biol 2003;4:657-665.
56. Hay ED: The mesenchymal cell, its role in the embryo, and the remarkable signalling mechanisms that create it. Dev Dynam 2005;233:706-720.
57. Savagner P: Leaving the neighbourhood: molecular mechanisms involved during epithelial-mesenchymal transition. BioEssays 2001;23:912-923.
58. Lee JM, Dedhar S, Kalluri R, Thompson EW: The epithelial-mesenchymal transition: new insights in signalling, development, and disease. J Cell Biol 2006;172:973-981.
59. Birchmeier W: Cell adhesion and signal transduction in cancer. EMBO Report 2005;6:413-417.
60. Rokutan K, Sakai A, Teramoto F, Kido Y, Shizuka F, Kishi K: Epidermal growth factor-induced mitogen signals in cultured intestinal epithelial cells. J Gastroenterol 1994;29:59-62.
61. Tetreault MP, Chailler P, Rivard N, Menard D: Differential growth factor induction and modulation of human gastric epithelial regeneration. Exp Cell Res 2005;306:285-297.
62. 2+ ion medium. J Cell Biol 1991;113:881-892.
63. Le TL, Yap AS, Stow JL: Recycling of Ecadherin: a potential mechanism for regulating cadherin dynamics. J Cell Biol 1999;146:219-232.
64. Janda E, Nevolo M, Lehmann K, Downward J, Beug H, Grieco M: Raf plus TGFßdependent EMT is initiated by endocytosis and lysosomal degradation of Ecadherin. Oncogene 2006;25:7117-7130.
65. Palacios, F, Tushir JS, Fujita Y, D'Souza-Schorey C: Lysosomal targeting of Ecadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol 2005;25:389-402.
66. Khew-Goodall Y, Wadham C: A perspective on regulation of cell-cell adhesion and epithelial-mesenchymal transition: known and novel. Cell Tissue Organs 2005;179:81-86.
67. Fujita Y, Krause G, Scheffner M, Zechner D, Molina Leddy HE, Behrens J, Sommer T, Birchmeier W: Hakai, a c-Cbl-like protein, ubiquitinates and induced endocytosis of the E-cadherin complex. Nat Cell Biol 2002;4:222-231.
68. Palacios F, Price L, Schweitzer J, Collard JG, D'Souza-Schorey C: An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J 2001;20:4973-4986.
69. Hanby AM, Chinery R, Poulsom R, Playford RJ, Pignatelli M: Downregulation of E-cadherin in the reparative epithelium of the human gastrointestinal tract. Am J Pathol 1996;148:723-729.
70. Miller JR, McClay DR: Characterization of the role of cadherin in regulating cell adhesion during sea urchin development. Dev Biol 1997;192:323-339.
71. Pece S, Gutkind JS: E-cadherin and hakai: signalling, remodelling or destruction? Nat Cell Biol 2002;4:E72-E74.
72. Karayiannakis AJ, Syrigos KN, Efstathiou J, Valizadeh A, Noda M, Playford RJ, Kmiot W, Pignatelli M: Expression of catenins and E-cadherin during epithelial restitution in inflammatory bowel disease. J Pathol 1998;185:413-418.
73. Jones MC, Caswell PT, Norman JC: Endocytic recycling pathways: emerging regulators of cell migration. Curr Opin Cell Biol 2006;18:549-557.
74. Balzac F, Avolio M, Degani S, Kaverina I, Torti M, Silengo L, Small JV, Retta SF: E-cadherin endocytosis regulates the activity of Rap1: a traffic light GTPase at the crossroads between cadherin and integrin function. J Cell Sci 2005;118:4765-4783.
75. Bos JL, de Bruyn K, Enserink J, Kuiperij B, Rangarajan S, Rehmann H, Riedl J, de Rooij J, van Mansfeld F, Zwartkruis F: The role of Rap 1 in integrin-mediated cell adhesion. Biochem Soc Trans 2003;31:83-86.
76. Graness A, Chwieralski CE, Reinhold D, Thim L, Hoffmann W: Protein kinase C and ERK activation are required for TFF-peptide-stimulated bronchial epithelial cell migration and tumor necrosis factor-α-induced interleukin-6 (IL-6) and IL-8 secretion. J Biol Chem 2002;277:18440-18446.
77. Barth AIM, Näthke IS, Nelson WJ: Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signalling pathways. Curr Opin Cell Biol 1997;9:683-690.
78. Wright NA, Pike C, Elia G: Induction of a novel epidermal growth factor-secreting cell lineage by mucosal ulceration in human gastrointestinal stem cells. Nature 1990;343:82-85.