Phosphorylation of zona occludens-2 by protein kinase Cε regulates its nuclear exportation

Molecular Biology of the Cell

Volumn 20, Issue 18, 2009, Pages 4120-4129

  Chamorro, David ^a   Alarcón, Lourdes ^a   Ponce, Arturo ^a   Tapia, Rocio ^a   González Aguilar, Héctor ^b   Robles Flores, Martha ^b   Mejía Castillo, Teresa ^a   Segovia, José ^a   Bandala, Yamir ^a   Juaristi, Eusebio ^a   González Mariscal, Lorenza ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; MUTANT PROTEIN; PROTEIN ANTIBODY; PROTEIN KINASE C EPSILON; SERINE; UNCLASSIFIED DRUG; ZONA OCCLUDENS 2 PROTEIN; ZONA OCCLUDENS 2 PROTEIN ANTIBODY;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIUM CELL; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; TIGHT JUNCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL MEMBRANE; CELL NUCLEUS; DOGS; EPITHELIAL CELLS; FATTY ACIDS, UNSATURATED; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MUTANT PROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN KINASE C-EPSILON; PROTEIN KINASE INHIBITORS; TIME FACTORS; TRANSFECTION;

EID: 70350221818     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-11-1129     Document Type: Article

References (23)

1. Avila-Flores, A., Rendon-Huerta, E., Moreno, J., Islas, S., Betanzos, A., Robles-Flores, M., and Gonzalez-Mariscal, L. (2001). Tight-junction protein zonula occludens 2 is a target of phosphorylation by protein kinase C. Biochem. J. 360, 295-304. (Pubitemid 33151324)
2. Brandman, R., Disatnik, M. H., Churchill, E., and Mochly-Rosen, D. (2007). Peptides derived from the C2 domain of protein kinase C epsilon (epsilon PKC) modulate epsilon PKC activity and identify potential protein-protein interaction surfaces. J. Biol. Chem. 282, 4113-4123.
3. Dodane, V., and Kachar, B. (1996). Identification of isoforms of G proteins and PKC that colocalize with tight junctions. J. Membr. Biol. 149, 199-209.
4. Gonzalez-Mariscal, L., Betanzos, A., and Avila-Flores, A. (2000a). MAGUK proteins: structure and role in the tight junction. Semin. Cell Dev. Biol. 11, 315-324.
5. Gonzalez-Mariscal, L., Chavez, d. R., and Cereijido, M. (1985). Tight junction formation in cultured epithelial cells (MDCK). J. Membr. Biol. 86, 113-125.
6. Gonzalez-Mariscal, L., Namorado, M. C., Martin, D., Luna, J., Alarcon, L., Islas, S., Valencia, L., Muriel, P., Ponce, L., and Reyes, J. L. (2000b). Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int. 57, 2386-2402. (Pubitemid 30340737)
7. Gonzalez-Mariscal, L., Ponce, A., Alarcon, L., and Jaramillo, B. E. (2006). The tight junction protein ZO-2 has several functional nuclear export signals. Exp. Cell Res. 312, 3323-3335.
8. Gumbiner, B., Lowenkopf, T., and Apatira, D. (1991). Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA 88, 3460-3464.
9. Islas, S., Vega, J., Ponce, L., and Gonzalez-Mariscal, L. (2002). Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Exp. Cell Res. 274, 138-148.
10. Itoh, M., Furuse, M., Morita, K., Kubota, K., Saitou, M., and Tsukita, S. (1999a). Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J. Cell Biol. 147, 1351-1363. (Pubitemid 30012818)
11. Itoh, M., Morita, K., and Tsukita, S. (1999b). Characterization of ZO-2 as a MAGUK family member associated with tight as well as adherens junctions with a binding affinity to occludin and alpha catenin. J. Biol. Chem. 274, 5981-5986.
12. Jaramillo, B. E., Ponce, A., Moreno, J., Betanzos, A., Huerta, M., Lopez-Bayghen, E., and Gonzalez-Mariscal, L. (2004). Characterization of the tight junction protein ZO-2 localized at the nucleus of epithelial cells. Exp. Cell Res. 297, 247-258.
13. Johnson, J. A., Gray, M. O., Chen, C. H., and Mochly-Rosen, D. (1996). A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J. Biol. Chem. 271, 24962-24966.
14. Kudo, N., Wolff, B., Sekimoto, T., Schreiner, E. P., Yoneda, Y., Yanagida, M., Horinouchi, S., and Yoshida, M. (1998). Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242, 540-547.
15. Makowske, M., and Rosen, O. M. (1989). Complete activation of protein kinase C by an antipeptide antibody directed against the pseudosubstrate prototope. J. Biol. Chem. 264, 16155-16159.
16. Mattagajasingh, S. N., Huang, S. C., Hartenstein, J. S., and Benz, E. J., Jr. (2000). Characterization of the interaction between protein 4.1R and ZO-2. A possible link between the tight junction and the actin cytoskeleton. J. Biol. Chem. 275, 30573-30585.
17. Metais, J. Y., Navarro, C., Santoni, M. J., Audebert, S., and Borg, J. P. (2005). hScrib interacts with ZO-2 at the cell-cell junctions of epithelial cells. FEBS Lett. 579, 3725-3730. (Pubitemid 40897716)
18. Robles-Flores, M., Rendon-Huerta, E., Gonzalez-Aguilar, H., Mendoza-Hernandez, G., Islas, S., Mendoza, V., Ponce-Castaneda, M. V., Gonzalez-Mariscal, L., and Lopez-Casillas, F. (2002). p32 (gC1qBP) is a general protein kinase C (PKC)-binding protein; interaction and cellular localization of P32-PKC complexes in ray hepatocytes. J. Biol. Chem. 277, 5247-5255.
19. Shoshani, L., Contreras, R. G., Roldan, M. L., Moreno, J., Lazaro, A., Balda, M. S., Matter, K., and Cereijido, M. (2005). The polarized expression of Na+,K+-ATPase in epithelia depends on the association between beta-subunits located in neighboring cells. Mol. Biol. Cell 16, 1071-1081.
20. Song, J. C., Hanson, C. M., Tsai, V., Farokhzad, O. C., Lotz, M., and Matthews, J. B. (2001). Regulation of epithelial transport and barrier function by distinct protein kinase C isoforms. Am. J. Physiol. Cell Physiol. 281, C649-C661.
21. Tapia, R., Huerta, M., Islas, S., Avila-Flores, A., Lopez-Bayghen, E., Weiske, J., Huber, O., and Gonzalez-Mariscal, L. (2009). Zona occludens-2 inhibits cyclin D1 expression and cell proliferation and exhibits changes in localization along the cell cycle. Mol. Biol. Cell 20, 1102-1117.
22. Traweger, A., Fuchs, R., Krizbai, I. A., Weiger, T. M., Bauer, H. C., and Bauer, H. (2003). The tight junction protein ZO-2 localizes to the nucleus and interacts with the heterogeneous nuclear ribonucleoprotein scaffold attachment factor-B. J. Biol. Chem. 278, 2692-2700.
23. Wittchen, E. S., Haskins, J., and Stevenson, B. R. (1999). Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J. Biol. Chem. 274, 35179-35185.