Protein phosphatase 2A plays a role in hydrogen peroxide-induced disruption of tight junctions in Caco-2 cell monolayers

Biochemical Journal

Volumn 421, Issue 1, 2009, Pages 59-70

  Sheth, Parimal ^a   Samak, Geetha ^a   Shull, J Andrew ^a   Seth, Ankur ^a   Rao, Radhakrishna K ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Barrier function; C Src; Cell cell adhesion; Epithelium; Occludin; Phospho threonine

Indexed keywords

BARRIER FUNCTION; C-SRC; CELL-CELL ADHESION; EPITHELIUM; OCCLUDIN; PHOSPHO-THREONINE;

ACID RESISTANCE; ADHESION; AMINO ACIDS; CAPILLARITY; CELL ADHESION; CELL MEMBRANES; ELECTRIC RESISTANCE; HYDROGEN PEROXIDE; LIVING SYSTEMS STUDIES; MONOLAYERS; OXIDATION; PHOSPHORYLATION; PLANTS (BOTANY); SYSTEM THEORY;

HYDROGEN;

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; FOSTRIECIN; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; INULIN; OCCLUDIN; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN ZO1; THREONINE; TYROSINE; MEMBRANE PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN SUBUNIT; SMALL INTERFERING RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DISRUPTION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME PURIFICATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TIGHT JUNCTION; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; RNA INTERFERENCE;

CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYDROGEN PEROXIDE; MEMBRANE PROTEINS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; PROTEIN PHOSPHATASE 2; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA, SMALL INTERFERING; THREONINE; TIGHT JUNCTIONS;

EID: 67650306418     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081951     Document Type: Article

References (33)

1. Hollander, D., Vadheim, C. M., Brettholz, E., Petersen, G. M., Delahunty, T. and Rotter, J. I. (1986) Increased intestinal permeability in patients with Crohn's disease and their relatives. A possible etiologic factor. Ann. Intern. Med. 105, 883-885
2. Lee, D. B., Huang, E. and Ward, H. J. (2006) Tight junction biology and kidney dysfunction. Am. J. Physiol. Renal Physiol. 290, F20-F34
3. Budinger, G. R. and Sznajder, J. I. (2006) The alveolar-epithelial barrier: A target for potential therapy. Clin. Chest Med. 27, 655-669
4. Turner, J. R. (2006) Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am. J. Pathol. 169, 1901-1909
5. Utech, M., Bruwer, M. and Nusrat, A. (2006) Tight junctions and cell-cell interactions. Methods Mol. Biol. 341, 185-195
6. Rao, R. (2008) Oxidative stress-induced disruption of epithelial and endothelial tight junctions. Front. Biosci. 13, 7210-7226
7. Rao, R. K., Baker, R. D., Baker, S. S., Gupta, A. and Holycross, M. (1997) Oxidant-induced disruption of intestinal epithelial barrier function: Role of protein tyrosine phosphorylation. Am. J. Physiol. 273, G812-G823
8. Tsukita, S. and Furuse, M. (1999) Occludin and claudins in tight-junction strands: Leading or supporting players? Trends Cell Biol. 9, 268-273
9. Ikenouchi, J., Furuse, M., Furuse, K., Sasaki, H. and Tsukita, S. (2005) Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J. Cell Biol. 171, 939-945
10. Martin-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., Panzeri, C., Stoppacciaro, A., Ruco, L., Villa, A. et al. (1998) Junctional adhesion molecule, a novel member of the immunoglobulin super family that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142, 117-127
11. Atkinson, K. J. and Rao, R. K. (2001) Role of protein tyrosine phosphorylation in acetaldehyde-induced disruption of epithelial tight junctions. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G1280-G1288
12. Basuroy, S., Sheth, P., Kuppuswamy, D., Balasubramanian, S., Ray, R. M. and Rao, R. K. (2003) Expression of kinase-inactive c-Src delays oxidative stress-induced disassembly and accelerates calcium-mediated reassembly of tight junctions in the Caco-2 cell monolayer. J. Biol. Chem. 278, 11916-11924
13. Chen, Y. H., Lu, Q., Goodenough, D. A. and Jeansonne, B. (2002) Non-receptor tyrosine kinase c-Yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Mol. Biol. Cell 13, 1227-1237
14. Denker, B. M., Saha, C., Khawaja, S. and Nigam, S. K. (1996) Involvement of a heterotrimeric G protein α subunit in tight junction biogenesis. J. Biol. Chem. 271, 25750-25753
15. Nusrat, A., Giry, M., Turner, J. R., Colgan, S. P., Parkos, C. A., Carnes, D., Lemichez, E., Boquet, P. and Madara, J. L. (1995) Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc. Natl. Acad. Sci. U.S.A. 92, 10629-10633
16. Rao, R. K., Basuroy, S., Rao, V. U., Karnaky, Jr, K. J. and Gupta, A. (2002) Tyrosine phosphorylation and dissociation of occludin-Z0-1 and E-cadherin-β-catenin complexes from the cytoskeleton by oxidative stress. Biochem. J. 368, 471-481
17. Rao, R. K., Li, L., Baker, R. D., Baker, S. S. and Gupta, A. (2000) Glutathione oxidation and PTPase inhibition by hydrogen peroxide in Caco-2 cell monolayer. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G332-G340
18. --sensitive G proteins in the function of T84 epithelial cells: Transport and barrier effects. Am. J. Physiol. 272, C794-C803
19. Stuart, R. O. and Nigam, S. K. (1995) Regulated assembly of tight junctions by protein kinase C. Proc. Natl. Acad. Sci. U.S.A. 92, 6072-6076
20. Walsh, S. V., Hopkins, A. M., Chen, J., Narumiya, S., Parkos, C. A. and Nusrat, A. (2001) Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology 121, 566-579
21. Basuroy, S., Seth, A., Elias, B., Naren, A. P. and Rao, R. (2006) MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem. J. 393, 69-77
22. Sheth, P., Basuroy, S., Li, C., Naren, A. P. and Rao, R. K. (2003) Role of phosphatidylinositol 3-kinase in oxidative stress-induced disruption of tight junctions. J. Biol. Chem. 278, 49239-49245
23. Kale, G., Naren, A. P., Sheth, P. and Rao, R. K. (2003) Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2, and ZO-3. Biochem. Biophys. Res. Commun. 302, 324-329
24. Sakakibara, A., Furuse, M., Saitou, M., Ando-Akatsuka, Y. and Tsukita, S. (1997) Possible involvement of phosphorylation of occludin in tight junction formation. J. Cell Biol. 137, 1393-1401
25. Wong, V. (1997) Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am. J. Physiol. 273 C1859-C1867
26. Andreeva, A. Y., Krause, E., Muller, E. C., Blasig, I. E. and Utepbergenov, D. I. (2001) Protein kinase C regulates the phosphorylation and cellular localization of occludin. J. Biol. Chem. 276, 38480-38486
27. Clarke, H., Soler, A. P. and Mullin, J. M. (2000) Protein kinase C activation leads to dephosphorylation of occludin and tight junction permeability increase in LLC-PK1 epithelial cell sheets. J. Cell Sci. 113, 3187-3196
28. Simonovic, I., Rosenberg, J., Koutsouris, A. and Hecht, G. (2000) Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol. 2, 305-315
29. Suzuki, T., Elias, B. C., Seth, A., Shen, L., Turner, J. R., Giorgianni, F., Desiderio, D., Guntaka, R. and Rao, R. (2009) PKCη regulates occludin phosphorylation and epithelial tight junction integrity. Proc. Natl. Acad. Sci. U.S.A. 106, 61-66
30. Nunbhakdi-Craig, V., Machleidt, T., Ogris, E., Bellotto, D., White, 3rd, C.L. and Sontag, E. (2002) Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J. Cell Biol. 158, 967-978
31. Seth, A., Sheth, P., Elias, B. C. and Rao, R. (2007) Protein phosphatases 2A and 1 interact with occludin and negatively regulate the assembly of tight junctions in the CACO-2 cell monolayer. J. Biol. Chem. 282, 11487-11498
32. Favre, B., Turowski, P. and Hemmings, B. A. (1997) Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem. 272, 13856-13863
33. Elias, B. C., Suzuki, T., Seth, A., Giorgianni, F., Kale, G., Shen, L., Turner, J. R., Naren, A., Desiderio, D. M. and Rao, R. (2009) 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. 284, 1559-1569