Thrombomodulin is an ezrin-interacting protein that controls epithelial morphology and promotes collective cell migration

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3440-3452

  Hsu, Yun Yan ^a   Shi, Guey Yueh ^a   Kuo, Cheng Hsiang ^a   Liu, Shu Lin ^a   Wu, Ching Ming ^a   Ma, Chih Yuan ^a   Lin, Feng Yi ^a   Yang, Hsi Yuan ^b   Wu, Hua Lin ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Cell cell adhesion; Keratinocyte; Neoepidermis; Wound healing

Indexed keywords

EPIDERMAL GROWTH FACTOR; EZRIN; THROMBOMODULIN;

ACTIN FILAMENT; ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA INTERFERENCE; WOUND HEALING;

ACTINS; ANIMALS; BINDING SITES; CELL ADHESION; CELL LINE; CELL MOVEMENT; CYTOSKELETAL PROTEINS; EPIDERMAL GROWTH FACTOR; EPIDERMIS; HUMANS; MICE; PROTEIN STRUCTURE, TERTIARY; THROMBOMODULIN; WOUND HEALING;

MUS;

EID: 84864741032     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-204917     Document Type: Article

References (41)

1. Perez-Moreno, M., Jamora, C., and Fuchs, E. (2003) Sticky business: orchestrating cellular signals at adherens junctions. Cell 112, 535-548 (Pubitemid 36263085)
2. Harris, T. J., and Tepass, U. (2010) Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11, 502-514
3. Giepmans, B. N., and van Ijzendoorn, S. C. (2009) Epithelial cell-cell junctions and plasma membrane domains. Biochim. Biophys. Acta 1788, 820-831
4. Suzuki, K., Kusumoto, H., Deyashiki, Y., Nishioka, J., Maruyama, I., Zushi, M., Kawahara, S., Honda, G., Yamamoto, S., and Horiguchi, S. (1987) Structure and expression of human thrombomodulin, a thrombin receptor on endothelium acting as a cofactor for protein C activation. EMBO J. 6, 1891-1897
5. Maruyama, I., Bell, C. E., and Majerus, P. W. (1985) Thrombomodulin is found on endothelium of arteries, veins, capillaries, and lymphatics, and on syncytiotrophoblast of human placenta. J. Cell Biol. 101, 363-371 (Pubitemid 15239110)
6. Raife, T. J., Lager, D. J., Madison, K. C., Piette, W. W., Howard, E. J., Sturm, M. T., Chen, Y., and Lentz, S. R. (1994) Thrombomodulin expression by human keratinocytes. Induction of cofactor activity during epidermal differentiation. J. Clin. Invest. 93, 1846-1851
7. Healy, A. M., Rayburn, H. B., Rosenberg, R. D., and Weiler, H. (1995) Absence of the blood-clotting regulator thrombomodulin causes embryonic lethality in mice before development of a functional cardiovascular system. Proc. Natl. Acad. Sci. U. S. A. 92, 850-854
8. Suehiro, T., Shimada, M., Matsumata, T., Taketomi, A., Yamamoto, K., and Sugimachi, K. (1995) Thrombomodulin inhibits intrahepatic spread in human hepatocellular carcinoma. Hepatology 21, 1285-1290
9. Tezuka, Y., Yonezawa, S., Maruyama, I., Matsushita, Y., Shimizu, T., Obama, H., Sagara, M., Shirao, K., Kusano, C., Natsugoe, S., Yoshinaka, H., Baba, M., Fukumoto, T., Aikou, T., and Sato, E. (1995) Expression of thrombomodulin in esophageal squamous cell carcinoma and its relationship to lymph node metastasis. Cancer Res. 55, 4196-4200
10. Ogawa, H., Yonezawa, S., Maruyama, I., Matsushita, Y., Tezuka, Y., Toyoyama, H., Yanagi, M., Matsumoto, H., Nishijima, H., Shimotakahara, T., Aikou, T., and Sato, E. (2000) Expression of thrombomodulin in squamous cell carcinoma of the lung: its relationship to lymph node metastasis and prognosis of the patients. Cancer Lett. 149, 95-103 (Pubitemid 30100565)
11. Huang, H. C., Shi, G. Y., Jiang, S. J., Shi, C. S., Wu, C. M., Yang, H. Y., and Wu, H. L. (2003) Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain. J. Biol. Chem. 278, 46750-46759
12. Kao, Y. C., Wu, L. W., Shi, C. S., Chu, C. H., Huang, C. W., Kuo, C. P., Sheu, H. M., Shi, G. Y., and Wu, H. L. (2010) Downregulation of thrombomodulin, a novel target of Snail, induces tumorigenesis through epithelial-mesenchymal transition. Mol. Cell. Biol. 30, 4767-4785
13. Tsukita, S., and Yonemura, S. (1999) Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J. Biol. Chem. 274, 34507-34510 (Pubitemid 129509480)
14. Bretscher, A., Edwards, K., and Fehon, R. G. (2002) ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599
15. Tsukita, S., and Hieda, Y. (1989) A new 82-kD barbed end-capping protein (radixin) localized in the cell-to-cell adherens junction: purification and characterization. J. Cell Biol. 108, 2369-2382 (Pubitemid 19168926)
16. Yonemura, S., Nagafuchi, A., Sato, N., and Tsukita, S. (1993) Concentration of an integral membrane protein, CD43 (leukosialin, sialophorin), in the cleavage furrow through the interaction of its cytoplasmic domain with actin-based cytoskeletons. J. Cell Biol. 120, 437-449 (Pubitemid 23040082)
17. Tsukita, S., Oishi, K., Sato, N., Sagara, J., and Kawai, A. (1994) ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126, 391-401 (Pubitemid 24226255)
18. Heiska, L., Alfthan, K., Gronholm, M., Vilja, P., Vaheri, A., and Carpen, O. (1998) Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2). Regulation by phosphatidylinositol 4, 5-bisphosphate. J. Biol. Chem. 273, 21893-21900 (Pubitemid 28405367)
19. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., and Tsukita, S. (1998) Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J. Cell Biol. 140, 885-895 (Pubitemid 28141226)
20. Turunen, O., Wahlstrom, T., and Vaheri, A. (1994) Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126, 1445-1453 (Pubitemid 24284609)
21. Gary, R., and Bretscher, A. (1995) Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell 6, 1061-1075
22. Magendantz, M., Henry, M. D., Lander, A., and Solomon, F. (1995) Interdomain interactions of radixin in vitro. J. Biol. Chem. 270, 25324-25327
23. Fievet, B. T., Gautreau, A., Roy, C., Del Maestro, L., Mangeat, P., Louvard, D., and Arpin, M. (2004) Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164, 653-659 (Pubitemid 38282949)
24. Legg, J. W., and Isacke, C. M. (1998) Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr. Biol. 8, 705-708 (Pubitemid 28286278)
25. Bretscher, A. (1989) Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes induced in A-431 cells by epidermal growth factor. J. Cell Biol. 108, 921-930
26. Krieg, J., and Hunter, T. (1992) Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J. Biol. Chem. 267, 19258-19265
27. Friedl, P., and Gilmour, D. (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457
28. Ilina, O., and Friedl, P. (2009) Mechanisms of collective cell migration at a glance. J. Cell Sci. 122, 3203-3208
29. Schafer, M., and Werner, S. (2008) Cancer as an overhealing wound: an old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9, 628-638
30. Shaw, T. J., and Martin, P. (2009) Wound repair at a glance. J. Cell Sci. 122, 3209-3213
31. Peterson, J. J., Rayburn, H. B., Lager, D. J., Raife, T. J., Kealey, G. P., Rosenberg, R. D., and Lentz, S. R. (1999) Expression of thrombomodulin and consequences of thrombomodulin deficiency during healing of cutaneous wounds. Am. J. Pathol. 155, 1569-1575
32. Amieva, M. R., and Furthmayr, H. (1995) Subcellular localization of moesin in dynamic filopodia, retraction fibers, and other structures involved in substrate exploration, attachment, and cell-cell contacts. Exp. Cell Res. 219, 180-196
33. Yonemura, S., and Tsukita, S. (1999) Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins. J. Cell Biol. 145, 1497-1509 (Pubitemid 29310006)
34. Lien, W. H., Klezovitch, O., and Vasioukhin, V. (2006) Cadherin-catenin proteins in vertebrate development. Curr. Opin. Cell Biol. 18, 499-506 (Pubitemid 44349063)
35. Takai, Y., Miyoshi, J., Ikeda, W., and Ogita, H. (2008) Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat. Rev. Mol. Cell Biol. 9, 603-615 (Pubitemid 352032927)
36. Tanaka, Y., Nakanishi, H., Kakunaga, S., Okabe, N., Kawakatsu, T., Shimizu, K., and Takai, Y. (2003) Role of nectin in formation of E-cadherin-based adherens junctions in keratinocytes: analysis with the N-cadherin dominant negative mutant. Mol. Biol. Cell 14, 1597-1609 (Pubitemid 36547425)
37. Speck, O., Hughes, S. C., Noren, N. K., Kulikauskas, R. M., and Fehon, R. G. (2003) Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87 (Pubitemid 36077089)
38. Vasioukhin, V., Bauer, C., Yin, M., and Fuchs, E. (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100, 209-219 (Pubitemid 30064909)
39. Orian-Rousseau, V., Chen, L., Sleeman, J. P., Herrlich, P., and Ponta, H. (2002) CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev. 16, 3074-3086 (Pubitemid 35424194)
40. Federici, C., Brambilla, D., Lozupone, F., Matarrese, P., de Milito, A., Lugini, L., Iessi, E., Cecchetti, S., Marino, M., Perdicchio, M., Logozzi, M., Spada, M., Malorni, W., and Fais, S. (2009) Pleiotropic function of ezrin in human metastatic melanomas. Int. J. Cancer 124, 2804-2812
41. Lara-Pezzi, E., Serrador, J. M., Montoya, M. C., Zamora, D., Yanez-Mo, M., Carretero, M., Furthmayr, H., Sanchez-Madrid, F., and Lopez-Cabrera, M. (2001) The hepatitis B virus X protein (HBx) induces a migratory phenotype in a CD44-dependent manner: possible role of HBx in invasion and metastasis. Hepatology 33, 1270-1281 (Pubitemid 32378227)