Gα12 regulates protein interactions within the MDCK cell tight junction and inhibits tight-junction assembly

Journal of Cell Science

Volumn 121, Issue 6, 2008, Pages 814-824

  Sabath, Ernesto ^a   Negoro, Hideyuki ^a   Beaudry, Sarah ^a   Paniagua, Manuel ^a   Angelow, Susanne ^b   Shah, Jagesh ^a   Grammatikakis, Nicholas ^c   Yu, Alan S L ^b   Denker, Bradley M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

Author keywords

Epithelial cells; G proteins; G12; Kidney; Tight junctions

Indexed keywords

CLAUDIN 1; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT 12; HEAT SHOCK PROTEIN 90; OCCLUDIN; PROTEIN ZO1; RAC PROTEIN; RHO FACTOR; STEROID RECEPTOR COACTIVATOR 1; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PHOSPHOPROTEIN; PROTEIN KINASE P60; TYROSINE; ZONULA OCCLUDENS 1 PROTEIN; ZONULA OCCLUDENS 2 PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; KIDNEY EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ANIMAL; CELL LINE; CHEMISTRY; DOG; DRUG ANTAGONISM; ENZYMOLOGY; EPITHELIUM CELL; GENETICS; METABOLISM; MUTATION;

ANIMALS; CELL LINE; CELL MEMBRANE PERMEABILITY; DOGS; EPITHELIAL CELLS; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HSP90 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MUTATION; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS PP60(C-SRC); SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; TYROSINE;

EID: 42549148464     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.014878     Document Type: Article

References (58)

1. Balda, M. S., Gonzalez-Mariscal, L., Macias-Silva, M., Torres-Marquez, M. E., Garcia Sainz, J. A. and Cereijido, M. (1991). Assembly and sealing of tight junctions: possible participaton of G-proteins, phospholipase C, protein kina C and calmodulin. J. Membr. Biol. 122, 193-202.
2. 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.
3. Blumer, J. B., Chandler, L. J. and Lanier, S. M. (2002). Expression analysis and subcellular distribution of the two G-protein regulators AGS3 and LGN indicate distinct functionality. Localization of LGN to the midbody during cytokinesis. J. Biol. Chem. 277, 15897-15903.
4. Busconi, L., Guan, J. and Denker, B. M. (2000). Degradation of heterotrimeric Gαo subunits via the proteosome pathway is induced by the hsp9O-specific compound geldanamycin. J. Biol. Chem. 275, 1565-1569.
5. Cereijido, M., Robbins, E. S., Dolan, W. J., Rotunno, C. A. and Sabatini, D. D. (1978). Polarized monolayers formed by epithelial cells on a permeable and tran lucent support. J. Cell Biol. 77, 853-880.
6. Cereijido, M., Gonzalez-Mariscal, L., Conreras, R. G., Gallardo, J.M., Garcia-Villegas, R. and Valdes, J. (1993). The making of a tight junction. J. Cell Sci. Suppl. 17, 127-132.
7. Collares-Buzato, C. B., Jepson, M. A., Simmons, N. L. and Hirst, B. H. (1998). Increased tyrosine phosphorylation causes redistribution of adherens junction and tight junction proteins and perturbs paracellular barrier function in MDCK epithelia. Eur. J. Cell Biol. 76, 85-92.
8. de Almeida, J. B., Holtzman, E. J., Peters, P. Ercolani, L., Ausiello, D. A. and Stow, J. L. (1994). Targeting of chimeric Gαi proteins to specific membrane domain. J. Cell Sci. 107, 507-515.
9. Denker, B. M. and Nigam, S. K. (1998). Molecular structure and assembly of the tight junction. Am. J. Physiol. 274, 171-179.
10. Denker, B. M., Saha, C., Eliawaja, S. and Nigam, S. K. (1996). Involvement of a haterotrimeric G protein α subunit in tight junction biogenesis. J. Biol. Chem. 271, 25750-25753.
11. Diamond, J. M. and Wright, E. M. (1969). Biological membranes: The physical basis of ion and nonelectrolyte selectivity. Annu. Rev. Physiol. 31, 581-646.
12. 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.
13. D'Souza, T., Agarwal, R. and Morin, P. J. (2005). Phosphorylation of claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells. J. Biol. Chem. 280, 26233-26240.
14. Ercolani, L., Stow, J. L., Boyle, J. F., Holtzman, E. J., Lin, H., Grove, J. R. and Ausiello, D. A. (1990). Membrane localization of the pertussis toxin-sensitive G-protein subunits αi2 and αi3 and expression of a metatlothionein- αi2 fusion gene in LLC-PK1 cells. Proc. Natl. Acad. Sci. USA 87, 4635-4639 [published erratum appears in Proc. Natl. Acad. Sci. USA 87, 7344].
15. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K. and Tsukita, S. (1998). Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141, 1539-1550.
16. Grammatikakis, N., Vultur, A., Ramana, C. V., Siganou, A., Schweinfest, C. W., Watson, D. K. and Raptis, L. (2002). The role of Hsp90N, a new member of the Hsp9O family, in signal transduction and neoplastic transformation. J. Biol. Chem. 277, 8312-8320.
17. Hamilton, S. E. and Nathanson, N. M. (1997). Differential localization of G proteins, Gαo and Gαil, -2, and -3 in polarized epithelial MDCK cells. Biochem. Biophys. Res. Commun. 234, 1-7.
18. 2+-sensing receptor couples to Gα12/13 to activate phospholipase D in Madin-Darby canine kidney cells. Am. J. Physiol. Cell Physiol. 286, C22-C30.
19. Jacob, C., Yang, P. C., Darmoul, D., Amadesi, S., Saito, T., Cottrell, G. S., Coelho, A. M., Singh, P., Grady, E. F., Perdue, M. et al. (2005). Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and β-arrestins. J. Biol. Chem. 280, 31936-31948.
20. Jiang, Y., Ma, W., Wan, Y., Kozasa, T., Hattori, S. and Huang, X. Y. (1998). The G protein Gα12 stimulates Bruton's tyrosine kinase and a rasGAP through a conserved PH/BM domain. Nature 395, 808-913.
21. Kimizuka, H. and Koketsu, K. (1964). Ion transport through cell membrane. J. Theor. Biol. 6, 290-305.
22. Lee, D. B., Huang, E. and Ward, H. J. (2006). Tight junction biology and kidney dysfunction. Am. J. Physiol. Renal Physiol. 290, F20-F34.
23. Lu, T. S., Chen, H. W., Huang, M. H., Wang, S. J. and Yang, R. C. (2004). Heat shock treatment protects osmotic stress-induced dysfunction of the blood-brain barrier through preservation of tight junction proteins. Cell Stress Chaperones 9, 369-377.
24. Ma, Y. C., Huang, J., Ali, S., Lowry, W. and Huang, X. Y. (2000). Src tyrosine kinase is a novel direct effector of G proteins. Cell 102, 635-646.
25. Matter, K. and Balda, M. S. (2003). Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 4, 225-236.
26. McNell, E., Capaldo, C. T. and Macara, I. G. (2006). Zonula occludens-1 function in the assembly of tight junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 17, 1922-1932.
27. Meyer, T. N, ScheslngerC,YeJ, Denker, B. M. and Nigam, S. K. (2001). Reassembly of the tight junction after oxidative stress depends on tyrosine kinase activity. J. Biol. Chem. 276, 22048-22055.
28. Meyer, T. N., Schwesinger, C. and Denker, B. M. (2002). Zonula occludens-1 is a scaffolding protein for signaling molecules. Gα12 directly binds to the Src homology 3 domain and regulates paracellular permeability in epithelial cells. J. Biol. Chem. 277, 24855-24858.
29. Meyer, T. N., Hunt, J., Schwesinger, C. and Deuker, B. M. (2003). Ga12 regulates epihelial cell junctions through Src tyrosine kinases. Am. J. Physiol. Cell Physiol. 285, C1281-C1293.
30. Nagao, M., Kazhro, Y. and Itoh, H. (1999). The Src family tyrosine kinase is involved in Rho-dependent activation of c-Jun N-terminal kinase by Gα12. Oncogene 18, 4425-4434.
31. Neer, E. J. (1995). Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80, 249-257.
32. Nusrat, A., Turner, J. R. and Madara, J. L. (2000). Molecular physiology and pathophysiology of tight junctions. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G851-G857.
33. Phimplikar, S. W. and Simons, K. (1993). Role of heterotrimeric G proteins in polarized membrane transport. J. Cell Sci. Suppl. 17, 27-32.
34. Postma, F. R., Hengeveld, T., Alblas, J. Giepmans, B. N., Zondag, G. C., Jalink, K. and Moolenaar, W. H. (1998). Acute loss of cell-cell communication caused by G protein-coupled receptors: a critical role for c-Src. J. Cell Biol. 140, 1199-1209.
35. Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W. and Pearl, L. H. (1997). Identification and structural characterization of the ATP/ADP-binding site in the Hsp9O molecular chaperone. Cell 90, 65-75.
36. Riobo, N. A. and Manning, D. R. (2005). Receptors coupled to heteretrimeric G proteins of the G12 family. Trends Pharmacol. Sci. 26, 146-154.
37. Rodriguez-Boulan, E. and Nelson, W. J. (1989). Morphogenesis of the polarized epithelial cell phenotype. Science 245, 718-725.
38. Saba, C., Nigam, S. K. and Denker, B. M. (1998). Involvement of Gαi2 in the maintenance and biogenesis of epithelial cell tight junctions. J. Biol. Chem. 273, 21629-21633.
39. Saba, C., Nigam, S. K. and Denker, B. M. (2001). Expanding role of G proteins in tight junction regulation: Gα(s) stimulates TJ assembly. Biochem. Biophys. Res. Commun. 285, 250-256.
40. Salton, M., Fujimoto, K. Doi, Y., Itoh, M., Fujimoto, T., Furuse, M., Takano, H., Noda, T. and Tsukita, S. (1998). Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J. Cell Biol. 141, 397-408.
41. Schulze, C., Smales, C., Rubbin, L. L. and Staddon, J. M. (1997). Lysophosphatidic acid increases tight junction permeability in cultured brain endothelial cells. J. Neurochem. 68, 991-1000.
42. Shigh, A. B. and Harris, R. C. (2004). Epidermal growth factor receptor activation differentially regulates claudin expression and enhances transepithelial resistance in Madin-Darby canine kidney cells. J. Biol. Chem. 279, 3543-3552.
43. Sinha, D., Wang, Z., Price, V. R., Schwartz, J. H. and Lieberthal, W. (2003). Chemical anoxia of tubular cells induces activation of c-Src and its translocation to the zonula adherens. Am. J. Physiol. Renal Physiol. 284, F488-F497.
44. Stow, J. L., de Almeida, J. B., Narula, N., Holtzman, E. J., Ercolani, L. and Ausiello, D. A. (1991). A heterotrimeric G protein, Gαi3, on Golgi membranes regulates the secretion of a heparan salfate proteoglycan in LLC-PK1 epithelial cells. J. Cell Biol. 114, 1113-1124.
45. Takeda, H. and Tsukita, S. (1995). Effects of tyrosine phosphorylation on tight junctions in temperature-sensitive v-src-transfected MDCK cells. Cell Struct. Funct. 20, 387-393.
46. Tsapara, A., Matter, K. and Balda, M. S. (2006). The heat shock protein Apg-2 binds to the tight junction protein ZO-1 and regulates transcriptional activity of ZONAB. Mol. Biol. Cell 17, 1322-1330.
47. Tsukamoto, T. and Nigam, S. K. (1999). Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. Am. J. Physiol. 276, F737-F750.
48. Tsukita, S., Furuse, M. and Itoh, M. (2001). Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293.
49. Vaisimnaite, R., Kozasa, T. and Voyno-Yasenetskaya, T. A. (2001). Interaction between the Gα subunit of heterotrimeric G(12) protein and Hsp9O is required for Gα12 signaling. J. Biol. Chem. 276, 46088-46093.
50. Van Itallie, C., Rahner, C. and Anderson, J. M. (2001). Regulated expression of claudin-4 decreases paracallular conductance through a selective decrease in sodium permeability. J. Clin. Invest. 107, 1319-1327.
51. Waheed, A. A. and Jones, T. L. (2002). Hsp90 interactions and acylation target the G protein G12 but not Gα13 to lipid rafts. J. Biol. Chem. 277, 32409-32412.
52. Whitesell, L. and Lindquist, S. L. (2005). HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5, 761-772.
53. Xu, Y. and Lindquist, S. (1993). Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. USA 90, 7074-7078.
54. Xu, Y., Singer, M. A. and Lindquist, S. (1999). Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90. Proc. Natl. Acad. Sci. USA 96, 109-114.
55. Yamaguchi, Y., Katoh, H., Mori, K. and Negishi, M. (2002). Gα12 and Gα13 interact with Ser/Thr protein phosphatase type 5 and stimulate its phosphatase activity. Curr. Biol. 12, 1353-1358.
56. Yamaguchi, Y., Katoh, H. and Negishi, M. (2003). N-terminal short sequences of a subunits of the G12 family determine selective coupling to receptors. J. Biol. Chem. 278, 14936-14939.
57. Yanamadala, V., Negoro, H., Gunaratman, L., Kong, T. and Denker, B. M. (2007). Gα12 stimulates apoptosis in epithelial cells through JNK1-mediated Bc1-2 degradation and up-regulation of IκBα. J. Biol. Chem. 282, 24352-24363.
58. Yu, A. S., Erick, A. H., Lencer, W. I. and Schneeberger, E. E. (2003). Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J. Biol. Chem. 278, 17350-17359.