Intestinal trefoil factor activates the PI3K/Akt signaling pathway to protect gastric mucosal epithelium from damage

International Journal of Oncology

Volumn 45, Issue 3, 2014, Pages 1123-1132

  Sun, Zhaorui ^a   Liu, Hongmei ^a   Yang, Zhizhou ^a   Shao, Danbing ^a   Zhang, Wei ^a   Ren, Yi ^a   Sun, Baodi ^a   Lin, Jinfeng ^a   Xu, Min ^a   Nie, Shinan ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

Integrity; Intestinal trefoil factor; Mucosal epithelium; PI3K Akt signaling pathway

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CHOLECYSTOKININ OCTAPEPTIDE; INTESTINAL TREFOIL FACTOR; LIPOPOLYSACCHARIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TIGHT JUNCTION PROTEIN; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; MORPHOLINE DERIVATIVE; PEPTIDE; TREFOIL FACTOR;

APOPTOSIS; ARTICLE; CELL DAMAGE; CELL MEMBRANE; CELL MIGRATION; CELL MIGRATION ASSAY; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CELL VIABILITY ASSAY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; EPITHELIUM CELL; IN VITRO STUDY; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STOMACH EPITHELIUM; STOMACH MUCOSA; STOMACH PROTECTION; TIGHT JUNCTION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL MOTION; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; PATHOLOGY;

CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CHROMONES; EPITHELIAL CELLS; GASTRIC MUCOSA; HUMANS; LIPOPOLYSACCHARIDES; MORPHOLINES; PEPTIDES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84904395898     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2527     Document Type: Article

References (40)

1. Podolsky DK: Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense. Am J Physiol 277: G495-G499, 1999.
2. Wright NA: Aspects of the biology of regeneration and repair in the human gastrointestinal tract. Philos Trans R Soc Lond B Biol Sci 353: 925-933, 1998.
3. Podolsky DK: Healing the epithelium: solving the problem from two sides. J Gastroenterol 32: 122-126, 1997.
4. Santos MF, McCormack SA, Guo Z, et al: Rho proteins play a critical role in cell migration during the early phase of mucosal restitution. J Clin Invest 100: 216-225, 1997. (Pubitemid 27311260)
5. Dieckgraefe BK, Santoro SA and Alpers DH: Immunolocalization of alpha-integrin subunits and extracellular matrix components during human colonic organogenesis. Gastroenterology 110: 58-71, 1996.
6. Wright NA, Hoffmann W, Otto WR, Rio MC and Thim L: Rolling in the clover: trefoil factor family (TFF)-domain peptides, cell migration and cancer. FEBS Lett 408: 121-123, 1997. (Pubitemid 27226779)
7. Taupin D and Podolsky DK: Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 4: 721-732, 2003. (Pubitemid 37082187)
8. Dignass A, Lynch-Devaney K, Kindon H, Thim L and Podolsky DK: Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. J Clin Invest 94: 376-383, 1994. (Pubitemid 24218114)
9. Potten CS, Merritt A, Hickman J, Hall P and Faranda A: Characterization of radiation-induced apoptosis in the small intestine and its biological implications. Int J Radiat Biol 65: 71-78, 1994. (Pubitemid 24063532)
10. Babyatsky MW, deBeaumont M, Thim L and Podolsky DK: Oral trefoil peptides protect against ethanol- and indomethacin-induced gastric injury in rats. Gastroenterology 110: 489-497, 1996. (Pubitemid 26043882)
11. Sun Y, Zhu Y, Wang L, Mao X, Peng X and Peng Y: Recombinant adenovirus-mediated intestinal trefoil factor gene therapy for burn-induced intestinal mucosal injury. PLoS One 8: e62429, 2013.
12. Cantley LC: The phosphoinositide 3-kinase pathway. Science 296: 1655-1657, 2002.
13. Li Q and Zhu GD: Targeting serine/threonine protein kinase B/Akt and cell-cycle checkpoint kinases for treating cancer. Curr Top Med Chem 2: 939-971, 2002.
14. Bao S, Wang Y, Sweeney P, et al: Keratinocyte growth factor induces Akt kinase activity and inhibits Fas-mediated apoptosis in A549 lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 288: L36-L42, 2005. (Pubitemid 40023884)
15. Baus-Loncar M and Giraud AS: Multiple regulatory pathways for trefoil factor (TFF) genes. Cell Mol Life Sci 62: 2921-2931, 2005. (Pubitemid 43004745)
16. Sun Z, Wang Y, Gong X, Su H and Han X: Secretion of rat tracheal epithelial cells induces mesenchymal stem cells to differentiate into epithelial cells. Cell Biol Int 36: 169-175, 2012.
17. Storesund T, Hayashi K, Kolltveit KM, Bryne M and Schenck K: Salivary trefoil factor 3 enhances migration of oral keratinocytes. Eur J Oral Sci 116: 135-140, 2008.
18. Yee DS, Tang Y, Li X, et al: The Wnt inhibitory factor 1 restoration in prostate cancer cells was associated with reduced tumor growth, decreased capacity of cell migration and invasion and a reversal of epithelial to mesenchymal transition. Mol Cancer 9: 162, 2010.
19. Madsen J, Nielsen O, Tornoe I, Thim L and Holmskov U: Tissue localization of human trefoil factors 1, 2, and 3. J Histochem Cytochem 55: 505-513, 2007. (Pubitemid 46668632)
20. Kouznetsova I, Peitz U, Vieth M, et al: A gradient of TFF3 (trefoil factor family 3) peptide synthesis within the normal human gastric mucosa. Cell Tissue Res 316: 155-165, 2004. (Pubitemid 38658536)
21. Durer U, Hartig R, Bang S, Thim L and Hoffmann W: TFF3 and EGF induce different migration patterns of intestinal epithelial cells in vitro and trigger increased internalization of E-cadherin. Cell Physiol Biochem 20: 329-346, 2007. (Pubitemid 47340596)
22. Podolsky DK: Mechanisms of regulatory peptide action in the gastrointestinal tract: trefoil peptides. J Gastroenterol 35 (Suppl 12): 69-74, 2000.
23. Lin N, Xu LF and Sun M: The protective effect of trefoil factor 3 on the intestinal tight junction barrier is mediated by toll-like receptor 2 via a PI3K/Akt dependent mechanism. Biochem Biophys Res Commun 440: 143-149, 2013.
24. Zheng Q, Gao J, Li H, et al: Trefoil factor 3 peptide regulates migration via a Twist-dependent pathway in gastric cell. Biochem Biophys Res Commun 438: 6-12, 2013.
25. Qu Y, Yang Y, Ma D and Xiao W: Increased trefoil factor 3 levels in the serum of patients with three major histological subtypes of lung cancer. Oncol Rep 27: 1277-1283, 2012.
26. Hernandez C, Santamatilde E, McCreath KJ, et al: Induction of trefoil factor (TFF)1, TFF2 and TFF3 by hypoxia is mediated by hypoxia inducible factor-1: implications for gastric mucosal healing. Br J Pharmacol 156: 262-272, 2009.
27. Liu D, el-Hariry I, Karayiannakis AJ, et al: Phosphorylation of beta-catenin and epidermal growth factor receptor by intestinal trefoil factor. Lab Invest 77: 557-563, 1997. (Pubitemid 28018775)
28. Gibson S, Tu S, Oyer R, Anderson SM and Johnson GL: Epidermal growth factor protects epithelial cells against Fas-induced apoptosis. Requirement for Akt activation. J Biol Chem 274: 17612-17618, 1999.
29. Moro L, Venturino M, Bozzo C, et al: Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesiondependent cell survival. EMBO J 17: 6622-6632, 1998. (Pubitemid 28521796)
30. Walker F, Kato A, Gonez LJ, et al: Activation of the 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, 1998. (Pubitemid 28533039)
31. Graness A, Chwieralski CE, Reinhold D, Thim L and Hoffmann W: Protein kinase C and ERK activation are required for TFF-peptide-stimulated bronchial epithelial cell migration and tumor necrosis factor-alpha-induced interleukin-6 (IL-6) and IL-8 secretion. J Biol Chem 277: 18440-18446, 2002. (Pubitemid 34952390)
32. Shi HS, Zhu WL, Liu JF, et al: PI3K/Akt signaling pathway in the basolateral amygdala mediates the rapid antidepressant-like effects of trefoil factor 3. Neuropsychopharmacology 37: 2671-2683, 2012.
33. Astle MV, Ooms LM, Cole AR, et al: Identification of a prolinerich inositol polyphosphate 5-phosphatase (PIPP)* collapsin response mediator protein 2 (CRMP2) complex that regulates neurite elongation. J Biol Chem 286: 23407-23418, 2011.
34. Chan CB, Liu X, Pradoldej S, et al: Phosphoinositide 3-kinase enhancer regulates neuronal dendritogenesis and survival in neocortex. J Neurosci 31: 8083-8092, 2011.
35. Nedachi T, Kawai T, Matsuwaki T, Yamanouchi K and Nishihara M: Progranulin enhances neural progenitor cell proliferation through glycogen synthase kinase 3beta phosphorylation. Neuroscience 185: 106-115, 2011.
36. Pugazhenthi S, Nesterova A, Sable C, et al: Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem 275: 10761-10766, 2000. (Pubitemid 30212704)
37. Mashimo H, Wu DC, Podolsky DK and Fishman MC: Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 274: 262-265, 1996. (Pubitemid 26353206)
38. Kindon H, Pothoulakis C, Thim L, Lynch-Devaney K and Podolsky DK: Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein. Gastroenterology 109: 516-523, 1995.
39. Taupin DR, Kinoshita K and Podolsky DK: Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc Natl Acad Sci USA 97: 799-804, 2000. (Pubitemid 30070390)
40. Playford RJ, Marchbank T, Goodlad RA, Chinery RA, Poulsom R and Hanby AM: Transgenic mice that overexpress the human trefoil peptide pS2 have an increased resistance to intestinal damage. Proc Natl Acad Sci USA 93: 2137-2142, 1996. (Pubitemid 26079894)