Enhanced interaction between focal adhesion and adherens junction proteins: Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement

Xiaoguang Sun; Yasushi Shikata; Lichun Wang; Kazuyoshi Ohmori; Naoko Watanabe; Jun Wada; Kenichi Shikata; Konstantin G. Birukov; Hirofumi Makino; Jeffrey R. Jacobson; Steven M. Dudek; Joe G.N. Garcia

doi:10.1016/j.mvr.2008.12.004

Enhanced interaction between focal adhesion and adherens junction proteins: Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement

Xiaoguang Sun, Yasushi Shikata, Lichun Wang, Kazuyoshi Ohmori, Naoko Watanabe, Jun Wada, Kenichi Shikata, Konstantin G. Birukov, Hirofumi Makino, Jeffrey R. Jacobson, Steven M. Dudek, Joe G.N. Garcia

Research output: Contribution to journal › Article › peer-review

78 Scopus citations

Abstract

Sphingosine 1-phosphate (S1P) is an important vascular barrier regulatory agonist which enhances the junctional integrity of human lung endothelial cell monolayers. We have now demonstrated that S1P induced cortical actin ring formation and redistribution of focal adhesion kinase (FAK) and paxillin to the cell periphery suggesting the critical role of cell-cell adhesion in endothelial barrier enhancement. Co-immunoprecipitation studies revealed increased association of VE-cadherin with FAK and paxillin in S1P-challenged human pulmonary artery endothelial cell (HPAEC) monolayers. Furthermore, S1P-induced enhancement of VE-cadherin interaction with α-catenin and β-catenin was associated with the increased formation of FAK-β-catenin protein complexes. Depletion of β-catenin (siRNA) resulted in loss of S1P-mediated VE-cadherin association with FAK and paxillin rearrangement. Furthermore, transendothelial electrical resistance (an index of barrier function) demonstrated that β-catenin siRNA significantly attenuated S1P-induced barrier enhancement. These results demonstrate a mechanism of S1P-induced endothelial barrier enhancement via β-catenin-linked adherens junction and focal adhesion interaction.

Original language	English (US)
Pages (from-to)	304-313
Number of pages	10
Journal	Microvascular Research
Volume	77
Issue number	3
DOIs	https://doi.org/10.1016/j.mvr.2008.12.004
State	Published - May 2009
Externally published	Yes

Keywords

Adherens junction
Endothelial
F-actin
Focal adhesion
Focal adhesion kinase
Paxillin
Sphingosine 1-phosphate
VE-cadherin
α-catenin
β-catenin

ASJC Scopus subject areas

Biochemistry
Cardiology and Cardiovascular Medicine
Cell Biology

Access to Document

10.1016/j.mvr.2008.12.004

Cite this

Sun, X., Shikata, Y., Wang, L., Ohmori, K., Watanabe, N., Wada, J., Shikata, K., Birukov, K. G., Makino, H., Jacobson, J. R., Dudek, S. M., & Garcia, J. G. N. (2009). Enhanced interaction between focal adhesion and adherens junction proteins: Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement. Microvascular Research, 77(3), 304-313. https://doi.org/10.1016/j.mvr.2008.12.004

Sun, X, Shikata, Y, Wang, L, Ohmori, K, Watanabe, N, Wada, J, Shikata, K, Birukov, KG, Makino, H, Jacobson, JR, Dudek, SM & Garcia, JGN 2009, 'Enhanced interaction between focal adhesion and adherens junction proteins: Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement', Microvascular Research, vol. 77, no. 3, pp. 304-313. https://doi.org/10.1016/j.mvr.2008.12.004

@article{3a26cc71646e474782bc806b1ca77c10,

title = "Enhanced interaction between focal adhesion and adherens junction proteins: Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement",

abstract = "Sphingosine 1-phosphate (S1P) is an important vascular barrier regulatory agonist which enhances the junctional integrity of human lung endothelial cell monolayers. We have now demonstrated that S1P induced cortical actin ring formation and redistribution of focal adhesion kinase (FAK) and paxillin to the cell periphery suggesting the critical role of cell-cell adhesion in endothelial barrier enhancement. Co-immunoprecipitation studies revealed increased association of VE-cadherin with FAK and paxillin in S1P-challenged human pulmonary artery endothelial cell (HPAEC) monolayers. Furthermore, S1P-induced enhancement of VE-cadherin interaction with α-catenin and β-catenin was associated with the increased formation of FAK-β-catenin protein complexes. Depletion of β-catenin (siRNA) resulted in loss of S1P-mediated VE-cadherin association with FAK and paxillin rearrangement. Furthermore, transendothelial electrical resistance (an index of barrier function) demonstrated that β-catenin siRNA significantly attenuated S1P-induced barrier enhancement. These results demonstrate a mechanism of S1P-induced endothelial barrier enhancement via β-catenin-linked adherens junction and focal adhesion interaction.",

keywords = "Adherens junction, Endothelial, F-actin, Focal adhesion, Focal adhesion kinase, Paxillin, Sphingosine 1-phosphate, VE-cadherin, α-catenin, β-catenin",

author = "Xiaoguang Sun and Yasushi Shikata and Lichun Wang and Kazuyoshi Ohmori and Naoko Watanabe and Jun Wada and Kenichi Shikata and Birukov, {Konstantin G.} and Hirofumi Makino and Jacobson, {Jeffrey R.} and Dudek, {Steven M.} and Garcia, {Joe G.N.}",

note = "Funding Information: This study was supported in part by NIH NHLBI grants HL076259, HL075349 and HL58064 (JGNG), MEXT (Japan, YS), HL088144 (SMD), HL077134 (JRJ) and GM07019 (XS).",

year = "2009",

month = may,

doi = "10.1016/j.mvr.2008.12.004",

language = "English (US)",

volume = "77",

pages = "304--313",

journal = "Microvascular Research",

issn = "0026-2862",

publisher = "Academic Press Inc.",

number = "3",

}

TY - JOUR

T1 - Enhanced interaction between focal adhesion and adherens junction proteins

T2 - Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement

AU - Sun, Xiaoguang

AU - Shikata, Yasushi

AU - Wang, Lichun

AU - Ohmori, Kazuyoshi

AU - Watanabe, Naoko

AU - Wada, Jun

AU - Shikata, Kenichi

AU - Birukov, Konstantin G.

AU - Makino, Hirofumi

AU - Jacobson, Jeffrey R.

AU - Dudek, Steven M.

AU - Garcia, Joe G.N.

N1 - Funding Information: This study was supported in part by NIH NHLBI grants HL076259, HL075349 and HL58064 (JGNG), MEXT (Japan, YS), HL088144 (SMD), HL077134 (JRJ) and GM07019 (XS).

PY - 2009/5

Y1 - 2009/5

N2 - Sphingosine 1-phosphate (S1P) is an important vascular barrier regulatory agonist which enhances the junctional integrity of human lung endothelial cell monolayers. We have now demonstrated that S1P induced cortical actin ring formation and redistribution of focal adhesion kinase (FAK) and paxillin to the cell periphery suggesting the critical role of cell-cell adhesion in endothelial barrier enhancement. Co-immunoprecipitation studies revealed increased association of VE-cadherin with FAK and paxillin in S1P-challenged human pulmonary artery endothelial cell (HPAEC) monolayers. Furthermore, S1P-induced enhancement of VE-cadherin interaction with α-catenin and β-catenin was associated with the increased formation of FAK-β-catenin protein complexes. Depletion of β-catenin (siRNA) resulted in loss of S1P-mediated VE-cadherin association with FAK and paxillin rearrangement. Furthermore, transendothelial electrical resistance (an index of barrier function) demonstrated that β-catenin siRNA significantly attenuated S1P-induced barrier enhancement. These results demonstrate a mechanism of S1P-induced endothelial barrier enhancement via β-catenin-linked adherens junction and focal adhesion interaction.

AB - Sphingosine 1-phosphate (S1P) is an important vascular barrier regulatory agonist which enhances the junctional integrity of human lung endothelial cell monolayers. We have now demonstrated that S1P induced cortical actin ring formation and redistribution of focal adhesion kinase (FAK) and paxillin to the cell periphery suggesting the critical role of cell-cell adhesion in endothelial barrier enhancement. Co-immunoprecipitation studies revealed increased association of VE-cadherin with FAK and paxillin in S1P-challenged human pulmonary artery endothelial cell (HPAEC) monolayers. Furthermore, S1P-induced enhancement of VE-cadherin interaction with α-catenin and β-catenin was associated with the increased formation of FAK-β-catenin protein complexes. Depletion of β-catenin (siRNA) resulted in loss of S1P-mediated VE-cadherin association with FAK and paxillin rearrangement. Furthermore, transendothelial electrical resistance (an index of barrier function) demonstrated that β-catenin siRNA significantly attenuated S1P-induced barrier enhancement. These results demonstrate a mechanism of S1P-induced endothelial barrier enhancement via β-catenin-linked adherens junction and focal adhesion interaction.

KW - Adherens junction

KW - Endothelial

KW - F-actin

KW - Focal adhesion

KW - Focal adhesion kinase

KW - Paxillin

KW - Sphingosine 1-phosphate

KW - VE-cadherin

KW - α-catenin

KW - β-catenin

UR - http://www.scopus.com/inward/record.url?scp=64049110683&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=64049110683&partnerID=8YFLogxK

U2 - 10.1016/j.mvr.2008.12.004

DO - 10.1016/j.mvr.2008.12.004

M3 - Article

C2 - 19323978

AN - SCOPUS:64049110683

SN - 0026-2862

VL - 77

SP - 304

EP - 313

JO - Microvascular Research

JF - Microvascular Research

IS - 3

ER -

Enhanced interaction between focal adhesion and adherens junction proteins: Involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this