Thrombin induces rapid disassembly of claudin-5 from the tight junction of endothelial cells

Experimental Cell Research

Volumn 315, Issue 17, 2009, Pages 2879-2887

  Kondo, Nobuyuki ^a,b   Ogawa, Minetaro ^c   Wada, Hiromi ^b   Nishikawa, Shin Ichi ^a  

^a RIKEN   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Cell cell junction; Claudin 5; Embryonic stem cells; Endothelial cells; PAR1; Thrombin

Indexed keywords

CLAUDIN 5; HISTAMINE; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN A;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TIGHT JUNCTION;

EID: 70349445278     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.07.031     Document Type: Article

References (42)

1. Bazzoni G., and Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84 (2004) 869-901
2. Tsukita S., Furuse M., and Itoh M. Multifunctional strands in tight junctions. Nat. Rev., Mol. Cell Biol. 2 (2001) 285-293
3. Dejana E., Bazzoni G., and Lampugnani M.G. Vascular endothelial (VE)-cadherin: only an intercellular glue?. Exp. Cell Res. 252 (1999) 13-19
4. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251 (1991) 1451-1455
5. Lampugnani M.G., Resnati M., Raiteri M., Pigott R., Pisacane A., Houen G., Ruco L.P., and Dejana E. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118 (1992) 1511-1522
6. Corada M., Mariotti M., Thurston G., Smith K., Kunkel R., Brockhaus M., Lampugnani M.G., Martin-Padura I., Stoppacciaro A., Ruco L., McDonald D.M., Ward P.A., and Dejana E. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9815-9820
7. Corada M., Zanetta L., Orsenigo F., Breviario F., Lampugnani M.G., Bernasconi S., Liao F., Hicklin D.J., Bohlen P., and Dejana E. A monoclonal antibody to vascular endothelial-cadherin inhibits tumor angiogenesis without side effects on endothelial permeability. Blood 100 (2002) 905-911
8. Morita K., Sasaki H., Furuse M., and Tsukita S. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J. Cell Biol. 147 (1999) 185-194
9. Fontijn R.D., Rohlena J., van Marle J., Pannekoek H., and Horrevoets A.J. Limited contribution of claudin-5-dependent tight junction strands to endothelial barrier function. Eur. J. Cell Biol. 85 (2006) 1131-1144
10. Nitta T., Hata M., Gotoh S., Seo Y., Sasaki H., Hashimoto N., Furuse M., and Tsukita S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 161 (2003) 653-660
11. Roberts W.G., and Palade G.E. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J. Cell Sci. 108 Pt. 6 (1995) 2369-2379
12. Esser S., Lampugnani M.G., Corada M., Dejana E., and Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111 Pt. 13 (1998) 1853-1865
13. Malik A.B., and Fenton II J.W. Thrombin-mediated increase in vascular endothelial permeability. Semin. Thromb. Hemost. 18 (1992) 193-199
14. Cirino G., Cicala C., Bucci M.R., Sorrentino L., Maraganore J.M., and Stone S.R. Thrombin functions as an inflammatory mediator through activation of its receptor. J. Exp. Med. 183 (1996) 821-827
15. Andriopoulou P., Navarro P., Zanetti A., Lampugnani M.G., and Dejana E. Histamine induces tyrosine phosphorylation of endothelial cell-to-cell adherens junctions. Arterioscler. Thromb. Vasc. Biol. 19 (1999) 2286-2297
16. Rabiet M.J., Plantier J.L., Rival Y., Genoux Y., Lampugnani M.G., and Dejana E. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler. Thromb. Vasc. Biol. 16 (1996) 488-496
17. Kataoka H., Takakura N., Nishikawa S., Tsuchida K., Kodama H., Kunisada T., Risau W., Kita T., and Nishikawa S.I. Expressions of PDGF receptor alpha, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev. Growth Differ. 39 (1997) 729-740
18. Nishikawa S. Embryonic stem cells as a source of hematopoietic and vascular endothelial cells in vitro. J. Allergy Clin. Immunol. 100 (1997) S102-104
19. Nishikawa S.I., Nishikawa S., Hirashima M., Matsuyoshi N., and Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK1 + VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 125 (1998) 1747-1757
20. Yamashita J., Itoh H., Hirashima M., Ogawa M., Nishikawa S., Yurugi T., Naito M., and Nakao K. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408 (2000) 92-96
21. Hirashima M., Kataoka H., Nishikawa S., and Matsuyoshi N. Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 93 (1999) 1253-1263
22. Robertson E., Bradley A., Kuehn M., and Evans M. Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature 323 (1986) 445-448
23. Ogawa M., Kizumoto M., Nishikawa S., Fujimoto T., Kodama H., and Nishikawa S.I. Expression of alpha4-integrin defines the earliest precursor of hematopoietic cell lineage diverged from endothelial cells. Blood 93 (1999) 1168-1177
24. Kodama H., Nose M., Niida S., and Nishikawa S. Involvement of the c-kit receptor in the adhesion of hematopoietic stem cells to stromal cells. Exp. Hematol. 22 (1994) 979-984
25. Matsuyoshi N., Toda K., Horiguchi Y., Tanaka T., Nakagawa S., Takeichi M., and Imamura S. In vivo evidence of the critical role of cadherin-5 in murine vascular integrity. Proc. Assoc. Am. Physicians 109 (1997) 362-371
26. Itoh M., Yonemura S., Nagafuchi A., and Tsukita S. A 220-kD undercoat-constitutive protein: its specific localization at cadherin-based cell-cell adhesion sites. J. Cell Biol. 115 (1991) 1449-1462
27. Matsumura K., Hirashima M., Ogawa M., Kubo H., Hisatsune H., Kondo N., Nishikawa S., and Chiba T. Modulation of VEGFR-2-mediated endothelial-cell activity by VEGF-C/VEGFR-3. Blood 101 (2003) 1367-1374
28. Hirai H., Ogawa M., Suzuki N., Yamamoto M., Breier G., Mazda O., Imanishi J., and Nishikawa S. Hemogenic and nonhemogenic endothelium can be distinguished by the activity of fetal liver kinase (Flk)-1 promoter/enhancer during mouse embryogenesis. Blood 101 (2003) 886-893
29. Kataoka H., Hamilton J.R., McKemy D.D., Camerer E., Zheng Y.W., Cheng A., Griffin C., and Coughlin S.R. Protease-activated receptors 1 and 4 mediate thrombin signaling in endothelial cells. Blood 102 (2003) 3224-3231
30. Vu T.K., Hung D.T., Wheaton V.I., and Coughlin S.R. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64 (1991) 1057-1068
31. Coughlin S.R. How the protease thrombin talks to cells. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11023-11027
32. Vittet D., Prandini M.H., Berthier R., Schweitzer A., Martin-Sisteron H., Uzan G., and Dejana E. Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88 (1996) 3424-3431
33. Dejana E., Corada M., and Lampugnani M.G. Endothelial cell-to-cell junctions. FASEB J. 9 (1995) 910-918
34. Nishikawa S.I., Hirashima M., Nishikawa S., and Ogawa M. Cell biology of vascular endothelial cells. Ann. N.Y. Acad. Sci. 947 (2001) 35-40 discussion 41
35. Ehringer W.D., Edwards M.J., and Miller F.N. Mechanisms of alpha-thrombin, histamine, and bradykinin induced endothelial permeability. J. Cell Physiol. 167 (1996) 562-569
36. Konstantoulaki M., Kouklis P., and Malik A.B. Protein kinase C modifications of VE-cadherin, p120, and beta-catenin contribute to endothelial barrier dysregulation induced by thrombin. Am. J. Physiol., Lung Cell Mol. Physiol. 285 (2003) L434-442
37. Coughlin S.R. Thrombin signalling and protease-activated receptors. Nature 407 (2000) 258-264
38. Harhaj N.S., Barber A.J., and Antonetti D.A. Platelet-derived growth factor mediates tight junction redistribution and increases permeability in MDCK cells. J. Cell Physiol. 193 (2002) 349-364
39. Itoh M., Sasaki H., Furuse M., Ozaki H., Kita T., and Tsukita S. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J. Cell Biol. 154 (2001) 491-497
40. Connolly A.J., Ishihara H., Kahn M.L., Farese Jr. R.V., and Coughlin S.R. Role of the thrombin receptor in development and evidence for a second receptor. Nature 381 (1996) 516-519
41. Griffin C.T., Srinivasan Y., Zheng Y.W., Huang W., and Coughlin S.R. A role for thrombin receptor signaling in endothelial cells during embryonic development. Science 293 (2001) 1666-1670
42. Trejo J., Hammes S.R., and Coughlin S.R. Termination of signaling by protease-activated receptor-1 is linked to lysosomal sorting. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 13698-13702