Interferon-γ-induced increases in intestinal epithelial macromolecular permeability requires the Src kinase Fyn

Laboratory Investigation

Volumn 91, Issue 5, 2011, Pages 764-777

  Smyth, David ^a   Phan, Van ^a   Wang, Arthur ^a   McKay, Derek M ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

bacterial translocation; barrier function; PI3K

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; HORSERADISH PEROXIDASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN GAB2; PROTEIN KINASE B; PROTEIN KINASE FYN; PROTEIN P85; PROTEIN P85ALPHA; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; STAT5 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; MEMBRANE PERMEABILITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SRC HOMOLOGY DOMAIN;

BASE SEQUENCE; CELL LINE, TRANSFORMED; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTERFERON-GAMMA; INTESTINAL MUCOSA; JANUS KINASES; PERMEABILITY; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FYN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR;

EID: 79955542476     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2010.208     Document Type: Article

References (48)

1. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009;9:799-809.
2. Uhlig HH, Powrie F. Mouse models of intestinal inflammation as tools to understand the pathogenesis of inflammatory bowel disease. Eur J Immunol 2009;39:2021-2026.
3. Mankertz J, Schulzke JD. Altered permeability in inflammatory bowel disease: pathophysiology and clinical implications. Curr Opin Gastroenterol 2007;23:379-383. (Pubitemid 46878948)
4. Camoglio L, Te Velde AA, Tigges AJ, et al. Altered expression of interferon-g and interleukin-4 in inflammatory bowel disease. Inflamm Bowel Dis 1998;4:285-290. (Pubitemid 128699868)
5. Beaurepaire C, Smyth D, McKay DM. Interferon-g regulation of intestinal epithelial permeability. J Interferon Cytokine Res 2009;23: 133-143.
6. Bruewer M, Utech M, Ivanov AI, et al. Interferon-g induces internalization of epithelial tight junction proteins via a macropinocytosis- like process. FASEB J 2005;19:923-929.
7. Youakim A, Ahdieh M. Interferon-g decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am J Physiol Gastrointestin Physiol 1999;276:G1279-G1288. (Pubitemid 29251928)
8. Wang F, Graham WV, Wang Y, et al. Interferon-g and tumor necrosis factor-a synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 2005;166:409-419. (Pubitemid 40189038)
9. Clark E, Hoare C, Tanianis-Hughes J, et al. Interferon-g induces translocation of commensal Escherichia coli across gut epithelial cells via a lipid raft-mediated process. Gastroenterology 2005;128: 1258-1267. (Pubitemid 40712177)
10. McKay DM, Watson JL, Wang A, et al. Phosphatidylinositol 30-kinase is a critical mediator of interferon-g-induced increases in enteric epithelial permeability. J Pharm Exp Ther 2007;320:1013-1022. (Pubitemid 46294056)
11. Stark GR, Kerr IM, Williams BR, et al. How cells respond to interferons. Annu Rev Biochem 1998;67:227-264. (Pubitemid 28411130)
12. Scharl M, Paul G, Barrett KE, et al. AMP-activated protein kinase mediates the interferon-g-induced decrease in intestinal epithelial barrier function. J Biol Chem 2009;284:27952-27963.
13. Nguyen H, Ramana CV, Bayes J, et al. Roles of phosphatidylinositol 3- kinase in interferon-gamma-dependent phosphorylation of STAT1 on serine 727 and activation of gene expression. J Biol Chem 2001;276:33361-33368.
14. Brown MT, Cooper JA. Regulation, substrates and functions of src. Biochim Biophys Acta 1996;1287:121-149. (Pubitemid 26189191)
15. Hayakawa F, Naoe T. SFK-STAT pathway: an alternative and important way to malignancies. Ann NY Acad Sci 2006;1086:213-222. (Pubitemid 47084370)
16. Jin W, Yun C, Jeong J, et al. c-Src is required for tropomyosin receptor kinase C (TrkC)-induced activation of the phosphatidylinositol 3-kinase (PI3K)-AKT pathway. J Biol Chem 2008;283:1391-1400.
17. Xing J, Zhang Z, Mao H, et al. Src regulates cell cycle protein expression and renal epithelial cell proliferation via PI3K/Akt signaling-dependent and -independent mechanisms. Am J Physiol Renal Physiol 2008; 295:F145-F152.
18. Uribe JM, McCole DF, Barrett KE. Interferon-g activates EGF receptor and increases TGF-a in T84 cells: implications for chloride secretion. Am J Physiol Gastrointest Liver Physiol 2002;283:G923-G931. (Pubitemid 35033935)
19. Saksena S, Gill RK, Tyagi S, et al. Role of Fyn and PI3K in H2O2-induced inhibition of apical Cl-/OH- exchange activity in human intestinal epithelial cells. Biochem J 2008;416:99-108.
20. Chappell AE, Bunz M, Smoll E, et al. Hydrogen peroxide inhibits Ca2+- dependent chloride secretion across colonic epithelial cells via distinct kinase signaling pathways and ion transport proteins. FASEB J 2008;22:2023-2036. (Pubitemid 351811478)
21. Watson JL, Ansari S, Cameron H, et al. Green tea polyphenol (-)- epigallocatechin gallate blocks epithelial barrier dysfunction provoked by IFN-g but not by IL-4. Am J Physiol Gastrointest Liver Physiol 2004;287:G954-G961. (Pubitemid 39423686)
22. Hanke JH, Gardner JP, Dow RL, et al. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynTdependent T cell activation. J Biol Chem 1996;271:695-701.
23. Brickell PM. The p60c-src family of protein-tyrosine kinases: structure, regulation, and function. Crit Rev Oncog 1992;3:401-446.
24. Santos SC, Lacronique V, Bouchaert I, et al. Constitutively active STAT5 variants induce growth and survival of hematopoietic cells through a PI 3-kinase/Akt dependent pathway. Oncogene 2001;20:2080-2090. (Pubitemid 32424002)
25. Nyga R, Pecquet C, Harir N, et al. Activated STAT5 proteins induce activation of the PI 3-kinase/Akt and Ras/MAPK pathways via the Gab2 scaffolding adapter. Biochem J 2005;390:359-366. (Pubitemid 41192263)
26. Karnitz LM, Sutor SL, Abraham RT. The Src-family kinase, Fyn, regulates the activation of phosphatidylinositol 3-kinase in an interleukin 2-responsive T cell line. J Exp Med 1994;179:1799-1808. (Pubitemid 24155661)
27. Madara JL, Stafford J. Interferon-g directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 1989;83: 724-727. (Pubitemid 19061198)
28. Ito R, Shin-Ya M, Kishida T, et al. Interferon-g is causatively involved in experimental inflammatory bowel disease in mice. Clin Exp Immunol 2006;146:330-338. (Pubitemid 44581349)
29. Utech M, Ivanov AI, Samarin SN, et al. Mechanism of IFN-g-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 2005;16:5040-5052. (Pubitemid 41416480)
30. Bach EA, Aguet M, Schreiber RD. The IFN-g receptor: a paradigm for cytokine receptor signaling. Annu Rev Immunol 1997;15:563-591. (Pubitemid 27169292)
31. Ramana CV, Gil MP, Schreiber RD, et al. Stat1-dependent and - independent pathways in IFN-g-dependent signaling. Trends Immunol 2002;23:96-101. (Pubitemid 34310151)
32. McKay DM, Botelho F, Ceponis PJ, et al. Superantigen immune stimulation activates epithelial STAT-1 and PI3-K: PI3-K regulation of permeability. Am J Physiol Gastrointest Liver Physiol 2000;279: G1094-G1103.
33. Meinke A, Barahmand-Pour F, Wohrl S, et al. Activation of different Stat5 isoforms contributes to cell-type-restricted signaling in response to interferons. Mol Cell Biol 1996;16:6937-6944. (Pubitemid 26389753)
34. Woldman I, Varinou L, Ramsauer K, et al. The Stat1 binding motif of the interferon-g receptor is sufficient to mediate Stat5 activation and its repression by SOCS3. J Biol Chem 2001;276:45722-45728.
35. Sarmay G, Angyal A, Kertesz A, et al. The multiple function of Grb2 associated binder (Gab) adaptor/scaffolding protein in immune cell signaling. Immunol Lett 2006;104:76-82. (Pubitemid 43330712)
36. Bennett HL, Brummer T, Jeanes A, et al. Gab2 and Src co-operate in human mammary epithelial cells to promote growth factor independence and disruption of acinar morphogenesis. Oncogene 2008;27:2693-2704. (Pubitemid 351581464)
37. Riggins RB, Thomas KS, Ta HQ, et al. Physical and functional interactions between Cas and c-Src induce tamoxifen resistance of breast cancer cells through pathways involving epidermal growth factor receptor and signal transducer and activator of transcription 5b. Cancer Res 2006;66:7007-7015. (Pubitemid 44197676)
38. Fox EM, Bernaciak TM, Wen J, et al. Signal transducer and activator of transcription 5b, c-Src, and epidermal growth factor receptor signaling play integral roles in estrogen-stimulated proliferation of estrogen receptor-positive breast cancer cells. Mol Endocrinol 2008;22:1781-1796.
39. Silva CM. Role of STATs as downstream signal transducers in Src family kinase-mediated tumorigenesis. Oncogene 2004;23:8017-8023. (Pubitemid 39468859)
40. Huveneers S, Danen EH. Adhesion signaling-crosstalk between integrins, Src and Rho. J Cell Sci 2009;122:1059-1069.
41. Sousa S, Cabanes D, Bougneres L, et al. Src, cortactin and Arp2/3 complex are required for E-cadherin-mediated internalization of Listeria into cells. Cell Microbiol 2007;9:2629-2643. (Pubitemid 47500515)
42. Elias BC, Suzuki T, Seth A, et al. Phosphorylation of Tyr-398 and Tyr-402 in occludin prevents its interaction with ZO-1 and destabilizes its assembly at the tight junctions. J Biol Chem 2009; 284:1559-1569.
43. Kale G, Naren AP, Sheth P, et al. Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2, and ZO-3. Biochem Biophys Res Commun 2003;302:324-329. (Pubitemid 36397924)
44. Castano J, Solanas G, Casagolda D, et al. Specific phosphorylation of p120-catenin regulatory domain differently modulates its binding to RhoA. Mol Cell Biol 2007;27:1745-1757.
45. Piedra J, Miravet S, Castano J, et al. p120 Catenin-associated Fer and Fyn tyrosine kinases regulate b-catenin Tyr-142 phosphorylation and b-catenin-a-catenin interaction. Mol Cell Biol 2003;23: 2287-2297. (Pubitemid 36351012)
46. Phillips N, Hayward RD, Koronakis V. Phosphorylation of the enteropathogenic E coli receptor by the Src-family kinase c-Fyn triggers actin pedestal formation. Nat Cell Biol 2004;6:618-625. (Pubitemid 38960919)
47. Hayward RD, Hume PJ, Humphreys D, et al. Clustering transfers the translocated Escherichia coli receptor into lipid rafts to stimulate reversible activation of c-Fyn. Cell Microbiol 2009;11:433-441.
48. Dorman SE, Holland SM. Interferon-g and interleukin-12 pathway defects and human disease. Cytokine Growth Factor Rev 2000;11: 321-333.