Tricellulin regulates junctional tension of epithelial cells at tricellular contacts through Cdc42

Journal of Cell Science

Volumn 127, Issue 19, 2014, Pages 4201-4212

  Oda, Yukako ^a   Otani, Tetsuhisa ^b   Ikenouchi, Junichi ^c,d   Furuse, Mikio ^a,e,f  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^f GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

Cdc42; Cell cell junction; Epithelial cell; F actin; MARVELD2; Tricellulin; Tuba

Indexed keywords

F ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN IIB; PROTEIN CDC42; PROTEIN ZO1; TRICELLULIN; TUBA PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BREAST EPITHELIUM; CACO 2 CELL LINE; CELL JUNCTION; EPITHELIUM CELL; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NICK END LABELING; PHENOTYPE; PROTEIN BINDING; RNA INTERFERENCE; GENETICS; METABOLISM;

DERRIS TRIFOLIATA;

CACO-2 CELLS; CDC42 GTP-BINDING PROTEIN; EPITHELIAL CELLS; HUMANS; MARVEL DOMAIN CONTAINING 2 PROTEIN;

EID: 84910023987     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.150607     Document Type: Article

References (50)

1. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
2. Bi, F., Debreceni, B., Zhu, K., Salani, B., Eva, A. and Zheng, Y. (2001). Autoinhibition mechanism of proto-Dbl. Mol. Cell. Biol. 21, 1463-1474.
3. Blankenship, J. T., Backovic, S. T., Sanny, J. S., Weitz, O. and Zallen, J. A. (2006). Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11, 459-470.
4. Cavey, M. and Lecuit, T. (2009). Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb. Perspect. Biol. 1, a002998.
5. Chen, Z., Guo, L., Sprang, S. R. and Sternweis, P. C. (2011). Modulation of a GEF switch: autoinhibition of the intrinsic guanine nucleotide exchange activity of p115-RhoGEF. Protein Sci. 20, 107-117.
6. Cunningham, K. E. and Turner, J. R. (2012). Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann. N. Y. Acad. Sci. 1258, 34-42.
7. Fanning, A. S., Van Itallie, C. M. and Anderson, J. M. (2012). Zonula occludens-1 and-2 regulate apical cell structure and the zonula adherens cytoskeleton in polarized epithelia. Mol. Biol. Cell 23, 577-590.
8. Farquhar, M. G. and Palade, G. E. (1963). Junctional complexes in various epithelia. J. Cell Biol. 17, 375-412.
9. Feller, S. M., Ren, R., Hanafusa, H. and Baltimore, D. (1994). SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Abl. Trends Biochem. Sci. 19, 453-458.
10. Fernandez-Gonzalez, R., Simoes, S. M., Röper, J. C., Eaton, S. and Zallen, J. A. (2009). Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 17, 736-743.
11. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
12. Higashi, T., Tokuda, S., Kitajiri, S., Masuda, S., Nakamura, H., Oda, Y. and Furuse, M. (2013). Analysis of the 'angulin' proteins LSR, ILDR1 and ILDR2-tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. J. Cell Sci. 126, 966-977.
13. Hogan, C., Dupré-Crochet, S., Norman, M., Kajita, M., Zimmermann, C., Pelling, A. E., Piddini, E., Baena-López, L. A., Vincent, J. P., Itoh, Y. et al. (2009). Characterization of the interface between normal and transformed epithelial cells. Nat. Cell Biol. 11, 460-467.
14. Honda, H. (1983). Geometricalmodels for cells in tissues. Int. Rev. Cytol. 81, 191-248.
15. Honda, H., Ogita, Y., Higuchi, S. and Kani, K. (1982). Cell movements in a living mammalian tissue: long-term observation of individual cells in wounded corneal endothelia of cats. J. Morphol. 174, 25-39.
16. Honda, H., Dan-Sohkawa, M. and Watanabe, K. (1984). Geometrical analysis of cells becoming organized into a tensile sheet, the blastular wall, in the starfish. Differentiation 25, 16-22.
17. Ikenouchi, J., Furuse, M., Furuse, K., Sasaki, H., Tsukita, S. and Tsukita, S. (2005). Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J. Cell Biol. 171, 939-945.
18. Ikenouchi, J., Sasaki, H., Tsukita, S., Furuse, M. and Tsukita, S. (2008). Loss of occludin affects tricellular localization of tricellulin. Mol. Biol. Cell 19, 4687-4693.
19. Ishiuchi, T. and Takeichi, M. (2011). Willin and Par3 cooperatively regulate epithelial apical constriction through aPKC-mediated ROCK phosphorylation. Nat. Cell Biol. 13, 860-866.
20. Itoh, M., Yonemura, S., Nagafuchi, A., Tsukita, S. and Tsukita, S. (1991). A 220-kD undercoat-constitutive protein: its specific localization at cadherin-based cellcell adhesion sites. J. Cell Biol. 115, 1449-1462.
21. Ivanov, A. I., Parkos, C. A. and Nusrat, A. (2010). Cytoskeletal regulation of epithelial barrier function during inflammation. Am. J. Pathol. 177, 512-524.
22. Jaffe, A. B. and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269.
23. Kubo, A., Nagao, K., Yokouchi, M., Sasaki, H. and Amagai, M. (2009). External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J. Exp. Med. 206, 2937-2946.
24. Lecuit, T. and Lenne, P. F. (2007). Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633-644.
25. Lecuit, T., Lenne, P. F. and Munro, E. (2011). Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 27, 157-184.
26. Machesky, L. M., Mullins, R. D., Higgs, H. N., Kaiser, D. A., Blanchoin, L., May, R. C., Hall, M. E. and Pollard, T. D. (1999). Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 96, 3739-3744.
27. Masuda, S., Oda, Y., Sasaki, H., Ikenouchi, J., Higashi, T., Akashi, M., Nishi, E. and Furuse, M. (2011). LSR defines cell corners for tricellular tight junction formation in epithelial cells. J. Cell Sci. 124, 548-555.
28. Mitin, N., Betts, L., Yohe, M. E., Der, C. J., Sondek, J. and Rossman, K. L. (2007). Release of autoinhibition of ASEF by APC leads to CDC42 activation and tumor suppression. Nat. Struct. Mol. Biol. 14, 814-823.
29. Nagafuchi, A. and Tsukita, S. (1994). The loss of the expression of alpha catenin, the 102 kD cadherin associated protein, in central nervous tissues during development. Dev. Growth Differ. 36, 59-71.
30. Nakajima, H. and Tanoue, T. (2011). Lulu2 regulates the circumferential actomyosin tensile system in epithelial cells through p114RhoGEF. J. Cell Biol. 195, 245-261.
31. Nayak, G., Lee, S. I., Yousaf, R., Edelmann, S. E., Trincot, C., Van Itallie, C. M., Sinha, G. P., Rafeeq, M., Jones, S. M., Belyantseva, I. A. et al. (2013). Tricellulin deficiency affects tight junction architecture and cochlear hair cells. J. Clin. Invest. 123, 4036-4049.
32. Nishimura, T. and Takeichi, M. (2008). Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493-1502.
33. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
34. Otani, T., Ichii, T., Aono, S. and Takeichi, M. (2006). Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J. Cell Biol. 175, 135-146.
35. Raleigh, D. R., Marchiando, A. M., Zhang, Y., Shen, L., Sasaki, H., Wang, Y., Long, M. and Turner, J. R. (2010). Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol. Biol. Cell 21, 1200-1213.
36. Riazuddin, S., Ahmed, Z. M., Fanning, A. S., Lagziel, A., Kitajiri, S., Ramzan, K., Khan, S. N., Chattaraj, P., Friedman, P. L., Anderson, J. M. et al. (2006). Tricellulin is a tight-junction protein necessary for hearing. Am. J. Hum. Genet. 79, 1040-1051.
37. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T. and Kirschner, M. W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
38. Salazar, M. A., Kwiatkowski, A. V., Pellegrini, L., Cestra, G., Butler, M. H., Rossman, K. L., Serna, D. M., Sondek, J., Gertler, F. B. and De Camilli, P. (2003). Tuba, a novel protein containing bin/amphiphysin/Rvs and Dbl homology domains, links dynamin to regulation of the actin cytoskeleton. J. Biol. Chem. 278, 49031-49043.
39. Schlüter, H., Moll, I., Wolburg, H. and Franke, W. W. (2007). The different structures containing tight junction proteins in epidermal and other stratified epithelial cells, including squamous cell metaplasia. Eur. J. Cell Biol. 86, 645-655.
40. Shum, W. W., Da Silva, N., McKee, M., Smith, P. J., Brown, D. and Breton, S. (2008). Transepithelial projections from basal cells are luminal sensors in pseudostratified epithelia. Cell 135, 1108-1117.
41. Smutny, M., Cox, H. L., Leerberg, J. M., Kovacs, E. M., Conti, M. A., Ferguson, C., Hamilton, N. A., Parton, R. G., Adelstein, R. S. and Yap, A. S. (2010). Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat. Cell Biol. 12, 696-702.
42. Sondermann, H., Soisson, S. M., Boykevisch, S., Yang, S. S., Bar-Sagi, D. and Kuriyan, J. (2004). Structural analysis of autoinhibition in the Ras activator Son of sevenless. Cell 119, 393-405.
43. Steed, E., Rodrigues, N. T., Balda, M. S. and Matter, K. (2009). Identification of MarvelD3 as a tight junction-associated transmembrane protein of the occludin family. BMC Cell Biol. 10, 95.
44. Terry, S. J., Zihni, C., Elbediwy, A., Vitiello, E., Leefa Chong San, I. V., Balda, M. S. and Matter, K. (2011). Spatially restricted activation of RhoA signalling at epithelial junctions by p114RhoGEF drives junction formation and morphogenesis. Nat. Cell Biol. 13, 159-166.
45. Vichas, A. and Zallen, J. A. (2011). Translating cell polarity into tissue elongation. Semin. Cell Dev. Biol. 22, 858-864.
46. Watanabe, T., Hosoya, H. and Yonemura, S. (2007). Regulation of myosin II dynamics by phosphorylation and dephosphorylation of its light chain in epithelial cells. Mol. Biol. Cell 18, 605-616.
47. Yamada, S. and Nelson, W. J. (2007). Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 178, 517-527.
48. Yonemura, S. (2011). Cadherin-actin interactions at adherens junctions. Curr. Opin. Cell Biol. 23, 515-522.
49. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A. and Shibata, M. (2010). alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542.
50. Yu, B., Martins, I. R., Li, P., Amarasinghe, G. K., Umetani, J., Fernandez-Zapico, M. E., Billadeau, D. D., Machius, M., Tomchick, D. R. and Rosen, M. K. (2010). Structural and energetic mechanisms of cooperative autoinhibition and activation of Vav1. Cell 140, 246-256.