Rho/Rho-associated kinase-II signaling mediates disassembly of epithelial apical junctions

Molecular Biology of the Cell

Volumn 18, Issue 9, 2007, Pages 3429-3439

  Samarin, Stanislav N ^a   Ivanov, Andrei I ^a   Flatau, Gilles ^b   Parkos, Charles A ^a   Nusrat, Asma ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; F ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN KINASE; MYOSIN PHOSPHATASE; PHOSPHATASE; RHO ASSOCIATED KINASE I; RHO ASSOCIATED KINASE II; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR H1; RHO KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APICAL JUNCTIONAL COMPLEX; ARTICLE; CALCIUM DEPLETION; CELL CULTURE; CELL JUNCTION; CULTURE MEDIUM; ENZYME ACTIVATION; EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

CALCIUM; CELL LINE; ENZYME ACTIVATION; EPITHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INTERCELLULAR JUNCTIONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; MYOSIN-LIGHT-CHAIN KINASE; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RHO GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 34548491399     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-04-0315     Document Type: Article

References (67)

1. Adelstein, R. S. (1982). Calmodulin and the regulation of the actin-myosin interaction in smooth muscle and nonmuscle cells. Cell 30, 349-350.
2. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
3. Aullo, P., Giry, M., Olsnes, S., Popoff, M. R., Kocks, C., and Boquet, P. (1993). A chimeric toxin to study the role of the 21 kDa GTP binding protein rho in the control of actin microfilament assembly. EMBO J. 12, 921-931.
4. Benais-Pont, G., Punn, A., Flores-Maldonado, C., Eckert, J., Raposo, G., Fleming, T. P., Cereijido, M., Balda, M. S., and Matter, K. (2003). Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability. J. Cell Biol. 160, 729-740.
5. Birukov, K. G., Csortos, C., Marzilli, L., Dudek, S., Ma, S. F., Bresnick, A. R., Verin, A. D., Cotter, R. J., and Garcia, J. G. (2001). Differential regulation of alternatively spliced endothelial cell myosin light chain kinase isoforms by p60(Src). J. Biol. Chem. 276, 8567-8573.
6. Birukova, A. A., Adyshev, D., Gorshkov, B., Bokoch, G. M., Birukov, K. G., and Verin, A. A. (2006). GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am. J. Physiol. 290, L540-L548.
7. Bogatcheva, N. V., Adyshev, D., Mambetsariev, B., Moldobaeva, N., and Verin, A. D. (2007). Involvement of microtubules, p38, and Rho kinases pathway in 2-methoxyestradiol-induced lung vascular barrier dysfunction. Am. J. Physiol. 292, L487-499.
8. Bresnick, A. R. (1999). Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11, 26-33.
9. Bruewer, M., Hopkins, A. M., Hobert, M. E., Nusrat, A., and Madara, J. L. (2004). RhoA, Rac1, and Cdc42 exert distinct effects on epithelial barrier via selective structural and biochemical modulation of junctional proteins and F-actin. Am. J. Physiol. 287, C327-C335.
10. Cordenonsi, M., D'Atri, F., Hammar, E., Parry, D. A., Kendrick-Jones, J., Shore, D., and Citi, S. (1999). Cingulin contains globular and coiled-coil domains and interacts with ZO-1, ZO-2, ZO-3, and myosin. J. Cell Biol. 147, 1569-1582.
11. Cramer, L. P., Briggs, L. J., and Dawe, H. R. (2002). Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells. Cell Motil. Cytoskeleton 51, 27-38.
12. de Rooij, J., Kerstens, A., Danuser, G., Schwartz, M. A., and Waterman-Storer, C. M. (2005). Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell Biol. 171, 153-164.
13. Gonzalez-Mariscal, L., Chavez de Ramirez, B., and Cereijido, M. (1985). Tight junction formation in cultured epithelial cells (MDCK). J. Membr. Biol. 86, 113-125.
14. Grunert, S., Jechlinger, M., and Beug, H. (2003). Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat. Rev. Mol. Cell Biol. 4, 657-665.
15. Hart, M. J., Sharma, S., elMasry, N., Qiu, R. G., McCabe, P., Polakis, P., and Bollag, G. (1996). Identification of a novel guanine nucleotide exchange factor for the Rho GTPase. J. Biol. Chem. 271, 25452-25458.
16. Hecht, G., Pestic, L., Nikcevic, G., Koutsouris, A., Tripuraneni, J., Lorimer, D. D., Nowak, G., Guerriero, V., Jr., Elson, E. L., and Lanerolle, P. D. (1996). Expression of the catalytic domain of myosin light chain kinase increases paracellular permeability. Am. J. Physiol. 271, C1678-C1684.
17. Hecht, G., Pothoulakis, C., LaMont, J. T., and Madara, J. L. (1988). Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J. Clin. Invest. 82, 1516-1524.
18. Hopkins, A. M., Walsh, S. V., Verkade, P., Boquet, P., and Nusrat, A. (2003). Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J. Cell Sci. 116, 725-742.
19. Ivanov, A. I., Hunt, D., Utech, M., Nusrat, A., and Parkos, C. A. (2005). Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol. Biol. Cell 16, 2636-2650.
20. Ivanov, A. I., McCall, I. C., Babbin, B., Samarin, S. N., Nusrat, A., and Parkos, C. A. (2006). Microtubules regulate disassembly of epithelial apical junctions. BMC Cell Biol. 7, 12.
21. Ivanov, A. I., McCall, I. C., Parkos, C. A., and Nusrat, A. (2004a). Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol. Biol. Cell 15, 2639-2651.
22. Ivanov, A. I., Nusrat, A., and Parkos, C. A. (2004b). Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell 15, 176-188.
23. Jou, T. S., Schneeberger, E. E., and Nelson, W. J. (1998). Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases. J. Cell Biol. 142, 101-115.
24. Katoh, K., Kano, Y., Amano, M., Kaibuchi, K., and Fujiwara, K. (2001). Stress fiber organization regulated by MLCK and Rho-kinase in cultured human fibroblasts. Am. J. Physiol. 280, C1669-C1679.
25. Kimura, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
26. Koch, A. W., Manzur, K. L., and Shan, W. (2004). Structure-based models of cadherin-mediated cell adhesion: the evolution continues. Cell Mol. Life Sci. 61, 1884-1895.
27. Krendel, M., Zenke, F. T., and Bokoch, G. M. (2002). Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4, 294-301.
28. Le Bivic, A., Real, F. X., and Rodriguez-Boulan, E. (1989). Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line. Proc. Natl. Acad. Sci. USA 86, 9313-9317.
29. Lecuit, T. (2005). Adhesion remodeling underlying tissue morphogenesis. Trends Cell Biol. 15, 34-42.
30. Leung, T., Chen, X. Q., Manser, E., and Lim, L. (1996). The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16, 5313-5327.
31. Leung, T., Manser, E., Tan, L., and Lim, L. (1995). A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270, 29051-29054.
32. Lui, W. Y., and Lee, W. M. (2006). Regulation of junction dynamics in the testis-transcriptional and post-translational regulations of cell junction proteins. Mol. Cell. Endocrinol. 250, 25-35.
33. Ma, T. Y., Tran, D., Hoa, N., Nguyen, D., Merryfield, M., and Tarnawski, A. (2000). Mechanism of extracellular calcium regulation of intestinal epithelial tight junction permeability: role of cytoskeletal involvement. Microsc. Res. Tech. 51, 156-168.
34. Matsui, T., Amano, M., Yamamoto, T., Chihara, K., Nakafuku, M., Ito, M., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J. 15, 2208-2216.
35. Matsumura, F. (2005). Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15, 371-377.
36. Matter, K., and Balda, M. S. (2003). Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 4, 225-236.
37. Mege, R. M., Gavard, J., and Lambert, M. (2006). Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 18, 541-548.
38. Miyake, Y., Inoue, N., Nishimura, K., Kinoshita, N., Hosoya, H., and Yonemura, S. (2006). Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation. Exp. Cell Res. 312, 1637-1650.
39. Morel, N. M., Petruzzo, P. P., Hechtman, H. B., and Shepro, D. (1990). Inflammatory agonists that increase microvascular permeability in vivo stimulate cultured pulmonary microvessel endothelial cell contraction. Inflammation 14, 571-583.
40. Noren, N. K., Niessen, C. M., Gumbiner, B. M., and Burridge, K. (2001). Cadherin engagement regulates Rho family GTPases. J. Biol. Chem. 276, 33305-33308.
41. 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. USA 92, 10629-10633.
42. Ren, Y., Li, R., Zheng, Y., and Busch, H. (1998). Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J. Biol. Chem. 273, 34954-34960.
43. Riento, K., and Ridley, A. J. (2003). Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4, 446-456.
44. Sahai, E., and Marshall, C. J. (2002). ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat. Cell Biol. 4, 408-415.
45. Saitoh, M., Naka, M., and Hidaka, H. (1986). The modulatory role of myosin light chain phosphorylation in human platelet activation. Biochem. Biophys Res. Commun. 140, 280-287.
46. Sandig, M., Voura, E. B., Kalnins, V. I., and Siu, C. H. (1997). Role of cadherins in the transendothelial migration of melanoma cells in culture. Cell Motil. Cytoskeleton 38, 351-364.
47. Sasaki, Y., Suzuki, M., and Hidaka, H. (2002). The novel and specific Rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoqumoline)sulfonyl]- homopiperazine as a probing molecule for Rho-kinase-involved pathway. Pharmacol. Ther. 93, 225-232.
48. Schmidt, A., and Hall, A. (2002). Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16, 1587-1609.
49. Shen, L., Black, E. D., Witkowski, E. D., Lencer, W. I., Guerriero, V., Schneeberger, E. E., and Turner, J. R. (2006). Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J. Cell Sci. 119, 2095-2106.
50. Shewan, A. M., Maddugoda, M., Kraemer, A., Stehbens, S. J., Verma, S., Kovacs, E. M., and Yap, A. S. (2005). Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531-4542.
51. Siliciano, J. D., and Goodenough, D. A. (1988). Localization of the tight junction protein, ZO-1, is modulated by extracellular calcium and cell-cell contact in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 107, 2389-2399.
52. Spitz, J., Yuhan, R., Koutsouris, A., Blatt, C., Alverdy, J., and Hecht, G. (1995). Enteropathogenic Escherichia coli adherence to intestinal epithelial monolayers diminishes barrier function. Am. J. Physiol. 268, G374-G379.
53. Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H., and Takai, Y. (1997). Regulation of cell-cell adhesion by rac and rho small G proteins in MDCK cells. J. Cell Biol. 139, 1047-1059.
54. Tan, J. L., Ravid, S., and Spudich, J. A. (1992). Control of nonmuscle myosins by phosphorylation. Annu. Rev. Biochem. 61, 721-759.
55. Tokman, M. G., Porter, R. A., and Williams, C. L. (1997). Regulation of cadherin-mediated adhesion by the small GTP-binding protein Rho in small cell lung carcinoma cells. Cancer Res. 57, 1785-1793.
56. Totsukawa, G., Yamakita, Y., Yamashiro, S., Hartshorne, D. J., Sasaki, Y., and Matsumura, F. (2000). Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797-806.
57. Tsukita, S., Furuse, M., and Itoh, M. (2001). Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293.
58. Turner, J. R. (2000). 'Putting the squeeze' on the tight junction: understanding cytoskeletal regulation. Semin. Cell Dev. Biol. 11, 301-308.
59. Turner, J. R., Rill, B. K., Carlson, S. L., Carnes, D., Kerner, R., Mrsny, R. J., and Madara, J. L. (1997). Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am. J. Physiol. 273, C1378-C1385.
60. Uehata, M. et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
61. Utech, M., Ivanov, A. I., Samarin, S. N., Bruewer, M., Turner, J. R., Mrsny, R. J., Parkos, C. A., and Nusrat, A. (2005). Mechanism of IFN-{gamma}-induced endocytosis of tight junction proteins: myosin ii-dependent vacuolarization of the apical plasma membrane. Mol. Biol. Cell 16, 5040-5052.
62. 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.
63. Xu, H., Dawson, R., Crane, I. J., and Liversidge, J. (2005). Leukocyte diapedesis in vivo induces transient loss of tight junction protein at the blood-retina barrier. Invest Ophthalmol. Vis. Sci. 46, 2487-2494.
64. Yap, A. S., Brieher, W. M., and Gumbiner, B. M. (1997). Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell Dev. Biol. 13, 119-146.
65. Yoneda, A., Multhaupt, H. A., and Couchman, J. R. (2005). The Rho kinases I and II regulate different aspects of myosin II activity. J. Cell Biol. 170, 443-453.
66. Zhang, J., Betson, M., Erasmus, J., Zeikos, K., Bailly, M., Cramer, L. P., and Braga, V. M. (2005). Actin at cell-cell junctions is composed of two dynamic and functional populations. J. Cell Sci. 118, 5549-5562.
67. Zolotarevsky, Y., Hecht, G., Koutsouris, A., Gonzalez, D. E., Quan, C., Tom, J., Mrsny, R. J., and Turner, J. R. (2002). A membrane-permeant peptide that inhibits MLC kinase restores barrier function in in vitro models of intestinal disease. Gastroenterology 123, 163-172.