45
Views
154
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Distinct Pathways of Cell Migration and Antiapoptotic Response to Epithelial Injury: Structure-Function Analysis of Human Intestinal Trefoil Factor

, , &
Pages 4680-4690 | Received 22 Oct 1999, Accepted 23 Mar 2000, Published online: 28 Mar 2023

REFERENCES

  • Alison, M. R., Chinery, R., Poulsom, R., Ashwood, P., Longcroft, J. M., and Wright, N. A.. 1995. Experimental ulceration leads to sequential expression of spasmolytic polypeptide, intestinal trefoil factor, epidermal growth factor, and transforming growth factor alpha mRNAs in rat stomach. J. Pathol. 175:405–414
  • Babyatsky, M. W., deBeaumont, M., Thim, L., and Podolsky, D. K.. 1996. Oral trefoil peptide protect against ethanol- and indomethacin-induced gastric injury in rats. Gastroenterology 105:1323–1332
  • Carr, M., Bauer, C. J., Gradwell, M. J., and Feeney, J.. 1994. Solution structure of a trefoil-motif-containing cell growth factor, porcine spasmolytic protein. Proc. Natl. Acad. Sci. USA 91:2206–2210
  • Chen, P., Xie, H., Sekar, M., Gupta, K., and Wells, A.. 1994. Epidermal growth factor protects epithelial cells against Fas-induced apoptosis. J. Biol. Chem. 274:17612–17618
  • Chinery, R., and Cox, H. M.. 1995. Immunoprecipitation and characterization of a binding protein specific for the peptide, intestinal trefoil factor. Peptides 16:749–755
  • Chung, D. C., Brand, S. J., and Tillotson, L. G.. 1995. Mutually exclusive interactions between factors binding to adjacent Sp1 and AT-rich elements regulate gastrin gene transcription in insulinoma cells. J. Biol. Chem. 270:8829–8836
  • Ciacci, C., Lind, S. E., and Podolsky, D. K.. 1993. Transforming growth factor beta regulation of migration in wounded rat intestinal epithelial monolayers. Gastroenterology 105:93–101
  • Dieckgraefe, B. K., Stenson, W. F., and Alpers, D. H.. 1996. Gastrointestinal epithelial response to injury. Curr. Opin. Gastroenterol. 12:109–114
  • Dignass, A. U., Lynch-Devaney, K., Kindon, H., Thim, L., and Podolsky, D. K.. 1994. Trefoil peptides promote epithelial migration through a TGF-β independent pathway. J. Clin. Investig. 94:376–383
  • Dignass, A. U., Lynch-Devaney, K., and Podolsky, D. K.. 1994. Hepatocyte growth factor/scatter factor modulate intestinal epithelial cell proliferation and migration. Biochem. Biophys. Res. Commun. 202:701–709
  • Dignass, A. U., and Podolsky, D. K.. 1993. Cytokine modulation of intestinal epithelial cell restitution: central role of transforming growth factor-β. Gastroenterology 105:1323–1332
  • Dignass, A. U., Tsunekawa, S., and Podolsky, D. K.. 1994. Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology 106:1254–1262
  • Efstathiou, J. A., Noda, M., Rowan, A., Dixon, C., Chinery, R., Jawhari, A., Hattori, T., Wright, N. A., Bodmer, W. F., and Pignatelli, M.. 1998. Intestinal trefoil factor controls the expression of the adenomatous polyposis coli-catenin and the E-cadherin-catenin complexes in human colon carcinoma cells. Proc. Natl. Acad. Sci. USA 95:3122–3127
  • Gibson, S., Tu, S., Oyer, R., Anderson, S. M., and Johnson, G. L.. 1999. Epidermal growth factor protects epithelial cells against Fas-induced apoptosis. J. Biol. Chem. 274:17612–17618
  • Gilmore, A. P., and Romer, L. H.. 1996. Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol. Cell. Biol. 7:1209–1224
  • Jørgensen, K. H., Thim, L., and Jacobsen, H. E.. 1982. Pancreatic spasmolytic polypeptide (PSP). I. Preparation and initial chemical characterization of a new polypeptide from porcine pancreas. Regul. Pept. 3:207–219
  • Kanai, M., and Podolsky, D. K.. 1997. Intestinal trefoil factor induces inactivation of extracellular signal-related protein kinases in intestinal epithelial cells. Proc. Natl. Acad. Sci. USA 95:178–182
  • Kennedy, S. G., Wagner, A. J., Conzen, S. D., Jordan, J., Bellacosa, A., Tsichlis, P. N., and Hay, N.. 1997. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes. Dev. 11:701–713
  • Khwaja, A., Lehmann, K., Marte, B. M., and Downward, J.. 1998. Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J. Biol. Chem. 273:18793–18801
  • Kindon, H., Pothoulakis, C., Thim, L., Lynch-Devaney, K., and Podolsky, D. K.. 1995. Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein. Gastroenterology 109:516–523
  • Klemke, R. L., Cai, S., Giannini, A. L., Gallagher, P. J., deLanerolle, P., and Cheresh, D. A.. 1997. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137:481–492
  • Liu, D., El-Hariry, I., Karayiannakis, A. J., Wilding, J., Chinery, R., Kmiot, W., McCrea, P. D., Gullick, W. J., and Pignatelli, M.. 1997. Phosphorylation of β-catenin and epidermal growth factor receptor by intestinal growth factor. Lab. Investig. 77:557–563
  • Lunn, C. A., Kathju, S., Wallace, B. J., Kushner, S. R., and Pigiet, V.. 1984. Amplification and purification of plasmid-encoded thioredoxin from Escherichia coli K12. J. Biol. Chem. 259:10469–10474
  • Marchbank, T., Westley, B. R., May, F. E. B., Calman, D. P., and Playford, R. J.. 1998. Dimerization of human pS2 (TFF1) plays a key role in its protective/healing effects. J. Pathol. 185:153–158
  • Mashimo, H., Wu, D.-C., Podolsky, D. K., and Fishman, M. C.. 1996. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 274:262–265
  • Menard, D., and Pothier, P.. 1991. Radioautographic localization of epidermal growth factor receptors in human fetal gut. Gastroenterology 101:640–649
  • Moro, L., Venturino, M., Bozzo, C., Silengo, L., Altruda, F., Beguinot, L., Tarone, G., and Defilippi, P.. 1998. Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO. J. 17:6622–6633
  • Nguyen, D. H., Catling, A. D., Webb, D. J., Sankovie, M., Walker, L. A., Somlyo, A. V., Weber, M. J., and Gonias, S. L.. 1999. Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J. Cell Biol. 146:149–164
  • Nisson, P. E., Rashtchain, A., and Watkins, P. C.. 1991. Rapid and efficient cloning of Alu-PCR products using uracil DNA glycosylase. PCR Methods Appl. 1:120–123
  • Nusrat, A., Delp, C., and Madara, J. L.. 1992. Intestinal epithelial restitution: characterization of a cell culture model and mapping of cytoskeletal elements in migrating cells. J. Clin. Investig. 89:1501–1511
  • Nusrat, A., Parkos, C., Bacarra, A., Godowski, P., Delp-Archer, C., Rosen, C., and Madara, J.. 1994. Hepatocyte growth factor/scatter factor effects on epithelial cells: regulation of intercellular junctions in transformed and nontransformed cell lines, basolateral polarization of c-met receptor in transformed and natural intestinal epithelia, and induction of rapid wound repair in a transformed model epithelium. J. Clin. Investig. 93:2056–2065
  • Playford, R. J., Marchbank, T., Calnan, D. P., Calam, J., Royston, P., Batten, J. J., and Hansen, H. F.. 1995. Epidermal growth factor is digested to smaller, less active forms in acidic gastric juice. Gastroenterology 108:92–101
  • Podolsky, D. K., Lynch-Devaney, K., Stow, J. L., Oates, P., Murgue, B., deBeaumont, M., Sands, B. E., and Mahida, Y. R.. 1993. Identification of human intestinal trefoil factor: goblet cell-specific expression of a peptide targeted for apical secretion. J. Biol. Chem. 268:6694–6702
  • Polshakov, V. I., Frenkiel, T. A., Westley, B., Chadwick, M., May, F., Carr, M. D., and Feeney, J.. 1995. NMR-based structural studies of the pNR-2/pS2 single domain trefoil peptide. Similarities to porcine spasmolytic peptide and evidence for a monomeric structure. Eur. J. Biochem. 233:847–855
  • Polshakov, V. I., Williams, M. A., Gargaro, A. R., Frenkiel, T. A., Westley, B. R., Chadwick, M. P., May, F. E., and Feeney, J.. 1997. High-resolution solution structure of human pNR-2/pS2: a single trefoil motif protein. J. Mol. Biol. 267:418–432
  • Poulsom, R., and Wright, N. A.. 1993. Trefoil peptides: a newly recognized family of epithelial mucin-associated molecules. Am. J. Physiol. 272:G1540–G1549
  • Rashtchian, A., Thornton, C. G., and Heidecker, G.. 1992. A novel method for site-directed mutagenesis using PCR and uracil DNA glycosylase. PCR Methods Appl. 2:124–130
  • Reyland, M. E., Anderson, S. M., Matassa, A. A., Barzen, K. A., and Quissell, D. O.. 1999. Protein kinase C δ is essential for etoposide-induced apoptosis in salivary gland acinar cells. J. Biol. Chem. 274:19115–19123
  • Rodriguez-Viciana, P., Warne, P. H., Khwaja, A., Marte, B. M., Pappin, D., Das, P., Waterfield, M. D., Ridley, A., and Downward, J.. 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of actin cytoskeleton by Ras. Cell 89:457–467
  • Sands, B. E., and Podolsky, D. K.. 1996. The trefoil peptide family. Annu. Rev. Physiol. 58:253–273
  • Santos, M. F., McCormack, S. A., Guo, Z., Okolicany, J., Zheng, Y., Johnson, L. R., and Tigyi, G.. 1997. Rho proteins play a critical role in cell migration during the early phase of mucosal restitution. J. Clin. Investig. 100:216–225
  • Schlaepfer, D. D., Jones, K. C., and Hunter, T.. 1998. Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol. Cell. Biol. 18:2571–2585
  • Suarez-Quian, C. A., and Byers, S. W.. 1993. Redistribution of epidermal growth factor receptor as a function of cell density, cell-cell adhesion and calcium in human (A-431) cells. Tissue Cell 25:1–17
  • Takaishi, K., Kikuchi, A., Kuroda, S., Kotani, K., Sasaki, T., and Takai, Y.. 1993. Involvement of rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in cell motility. Mol. Cell. Biol. 13:72–79
  • Tan, X.-D., Hsueh, W., Chang, H., Wei, K.-R., and Gonzalez-Crussi, F.. 1997. Characterization of a putative receptor for intestinal trefoil factor in rat small intestine: identification by in situ binding and ligand blotting. Biochem. Biophys. Res. Commun. 237:673–677
  • Taupin, D. R., and Podolsky, D. K.. 1999. Mitogen-activated protein kinase activation regulates intestinal epithelial differentiation. Gastroenterology 116:1072–1080
  • Taupin, D. R., Wu, D. C., Jeon, W. K., Devaney, K., Wang, T. C., and Podolsky, D. K.. 1999. The trefoil gene family are coordinately expressed immediate-early genes: EGF receptor-and MAP kinase-dependent interregulation. J. Clin. Investig. 103:R31–R38
  • Taupin, D. R., Kinoshita, K., and Podolsky, D. K.. 2000. Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc. Natl. Acad. Sci. USA 97:799–804
  • Thim, L.. 1989. A new family of growth factor-like peptides. 'Trefoil' disulfide loop structures as a common feature in breast cancer associated peptide (pS2), pancreatic spasmolytic polypeptide (PSP), and frog skin peptides (spasmolysins). FEBS. Lett. 250:85–90
  • Thim, L., Thomsen, J., Christensen, M., and Jørgensen, K. H.. 1985. The amino acid sequence of pancreatic spasmolytic polypeptide. Biochim. Biophys. Acta 827:410–418
  • Thim, L., Wöldike, H. F., Nielsen, P. F., Christensen, M., Lynch-Devaney, K., and Podolsky, D. K.. 1995. Characterization of human and rat intestinal trefoil factor produced in yeast. Biochemistry 34:4757–4764
  • Tran, C. P., Cook, G. A., Yeomans, N. D., Thim, L., and Giraud, A. S.. 1999. Trefoil peptide TFF2 (spasmolytic polypeptide) potently accelerates healing and reduces inflammation in a rat model of colitis. Gut 44:636–642
  • Wagner, M., Cao, T., Lopez, M. E., Hope, C., van Nostrand, K., Kobrin, M. S., Fan, H. U., Buchler, M. W., and Korc, M.. 1996. Expression of a truncated EGF receptor is associated with inhibition of pancreatic cell growth and enhanced sensitivity to cisplatinum. Int. J. Cancer 68:782–787
  • Walker, F., Kato, A., Gonez, L. J., Hibbs, M. L., Pouliot, N., Levitzki, A., and Burgess, A. W.. 1998. Activation of Ras/Mitogen-activated protein kinase pathway by kinase-defective epidermal growth factor receptors results in cell survival but not proliferation. Mol. Cell. Biol. 18:7192–7204
  • Westermark, K., Westermark, B., Karlsson, F. A., and Ericson, L. E.. 1986. Location of epidermal growth factor receptors on porcine thyroid follicle cells and receptor regulation by thyrotropin. Endocrinology 118:1040–1046
  • Wright, N. A., Hoffmann, W., Otto, W. R., Rio, M. C., and Thim, L.. 1997. Rolling in the clover: trefoil factor family (TFF)-domain peptides, cell migration and cancer. FEBS Lett. 408:121–123
  • Wright, N. A., Poulsom, R., Stamp, G., Vannorden, S., Saffaf, C., Elia, G., Ahnen, D., Jeffery, R., Longcroft, J., Pike, C., Rio, M. C., and Chambon, P.. 1993. Trefoil peptide gene expression in gastrointestinal epithelial cells in inflammatory bowel disease. Gastroenterology 104:12–20
  • Yoshimura, S., Banno, Y., Nakashima, S., Takenaka, K., Sakai, H., Nishimura, Y., Sakai, N., Shimizu, S., Eguchi, Y., Tsujimoto, Y., and Nozawa, Y.. 1998. Ceramide formation leads to caspase-3 activation during hypoxic PC12 cell death. J. Biol. Chem. 273:6921–6927
  • Zeigler, M. E., Chi, Y., Schmidt, T., and Varani, J.. 1999. Role of ERK and JNK pathways in regulating cell motility and matrix metalloproteinase 9 production in growth factor-stimulated human epidermal keratinocytes. J. Cell. Physiol. 180:271–284

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.