R-Ras interacts with filamin a to maintain endothelial barrier function

The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R‐Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa�...

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Published in:	Journal of cellular physiology Vol. 226; no. 9; pp. 2287 - 2296
Main Authors:	Griffiths, G.S., Grundl, M., Allen III, J.S., Matter, M.L.
Format:	Journal Article
Language:	English
Published:	Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.09.2011
Subjects:	Cadherins - metabolism Capillary Permeability Contractile Proteins - metabolism Coronary Vessels - cytology Cytoskeleton - metabolism Endothelial Cells - cytology Endothelial Cells - metabolism Filamins Gene Knockdown Techniques Humans Microfilament Proteins - metabolism Phosphorylation Phosphoserine - metabolism Protein Binding Protein Transport Proto-Oncogene Proteins pp60(c-src) - metabolism ras Proteins - metabolism RNA, Small Interfering - metabolism
ISSN:	0021-9541, 1097-4652, 1097-4652
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Abstract	The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R‐Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa's association with R‐Ras affects endothelial barrier function. We report that in endothelial cells endogenous R‐Ras interacts with endogenous FLNa as determined by co‐immunoprecipitations and pulldowns with the FLNa‐GST fusion protein repeats 1–10. Deletion of FLNa repeat 3 (FLNaΔ3) abrogated this interaction. In these cells FLNa and R‐Ras co‐localize at the plasma membrane. Knockdown of R‐Ras and/or FLNa by siRNA promotes vascular permeability, as determined by TransEndothelial Electrical Resistance and FITC‐dextran transwell assays. Re‐expression of FLNa restored endothelial barrier function in cells lacking FLNa whereas re‐expression of FLNaΔ3 did not. Immunostaining for VE‐Cadherin in cells with knocked down R‐Ras and FLNa demonstrated a disorganization of VE‐Cadherin at adherens junctions. Loss of R‐Ras and FLNa or blocking R‐Ras function via GGTI‐2133, a selective R‐Ras inhibitor, induced vascular permeability and increased phosphorylation of VE‐Cadherin (Y731) and Src (Y416). Expression of dominant negative R‐Ras promoted vascular permeability that was blocked by the Src inhibitor PP2. These findings demonstrate that maintaining endothelial barrier function is dependent upon active R‐Ras and association between R‐Ras and FLNa and that loss of this interaction promotes VE‐Cadherin phosphorylation and changes in downstream effectors that lead to endothelial leakiness. J. Cell. Physiol. 226: 2287–2296, 2011. © 2010 Wiley‐Liss, Inc.
AbstractList	The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R‐Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa's association with R‐Ras affects endothelial barrier function. We report that in endothelial cells endogenous R‐Ras interacts with endogenous FLNa as determined by co‐immunoprecipitations and pulldowns with the FLNa‐GST fusion protein repeats 1–10. Deletion of FLNa repeat 3 (FLNaΔ3) abrogated this interaction. In these cells FLNa and R‐Ras co‐localize at the plasma membrane. Knockdown of R‐Ras and/or FLNa by siRNA promotes vascular permeability, as determined by TransEndothelial Electrical Resistance and FITC‐dextran transwell assays. Re‐expression of FLNa restored endothelial barrier function in cells lacking FLNa whereas re‐expression of FLNaΔ3 did not. Immunostaining for VE‐Cadherin in cells with knocked down R‐Ras and FLNa demonstrated a disorganization of VE‐Cadherin at adherens junctions. Loss of R‐Ras and FLNa or blocking R‐Ras function via GGTI‐2133, a selective R‐Ras inhibitor, induced vascular permeability and increased phosphorylation of VE‐Cadherin (Y731) and Src (Y416). Expression of dominant negative R‐Ras promoted vascular permeability that was blocked by the Src inhibitor PP2. These findings demonstrate that maintaining endothelial barrier function is dependent upon active R‐Ras and association between R‐Ras and FLNa and that loss of this interaction promotes VE‐Cadherin phosphorylation and changes in downstream effectors that lead to endothelial leakiness. J. Cell. Physiol. 226: 2287–2296, 2011. © 2010 Wiley‐Liss, Inc. The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R-Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa’s association with R-Ras affects endothelial barrier function. We report that in endothelial cells endogenous R-Ras interacts with endogenous FLNa as determined by co-immunoprecipitations and pulldowns with the FLNa-GST fusion protein repeats 1–10. Deletion of FLNa repeat 3 (FLNa 3) abrogated this interaction. In these cells FLNa and R-Ras co-localize at the plasma membrane. Knockdown of R-Ras and/or FLNa by siRNA promotes vascular permeability, as determined by TransEndothelial Electrical Resistance and FITC-dextran transwell assays. Re-expression of FLNa restored endothelial barrier function in cells lacking FLNa whereas re-expression of FLNaΔ3 did not. Immunostaining for VE-Cadherin in cells with knocked down R-Ras and FLNa demonstrated a disorganization of VE-Cadherin at adherens junctions. Loss of R-Ras and FLNa or blocking R-Ras function via GGTI-2133, a selective R-Ras inhibitor, induced vascular permeability and increased phosphorylation of VE-Cadherin (Y731) and Src (Y416). Expression of dominant negative R-Ras promoted vascular permeability that was blocked by the Src inhibitor PP2. These findings demonstrate that maintaining endothelial barrier function is dependent upon active R-Ras and association between R-Ras and FLNa and that loss of this interaction promotes VE-Cadherin phosphorylation and changes in downstream effectors that lead to endothelial leakiness. The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R-Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa's association with R-Ras affects endothelial barrier function. We report that in endothelial cells endogenous R-Ras interacts with endogenous FLNa as determined by co-immunoprecipitations and pulldowns with the FLNa-GST fusion protein repeats 1-10. Deletion of FLNa repeat 3 (FLNaΔ3) abrogated this interaction. In these cells FLNa and R-Ras co-localize at the plasma membrane. Knockdown of R-Ras and/or FLNa by siRNA promotes vascular permeability, as determined by TransEndothelial Electrical Resistance and FITC-dextran transwell assays. Re-expression of FLNa restored endothelial barrier function in cells lacking FLNa whereas re-expression of FLNaΔ3 did not. Immunostaining for VE-Cadherin in cells with knocked down R-Ras and FLNa demonstrated a disorganization of VE-Cadherin at adherens junctions. Loss of R-Ras and FLNa or blocking R-Ras function via GGTI-2133, a selective R-Ras inhibitor, induced vascular permeability and increased phosphorylation of VE-Cadherin (Y731) and Src (Y416). Expression of dominant negative R-Ras promoted vascular permeability that was blocked by the Src inhibitor PP2. These findings demonstrate that maintaining endothelial barrier function is dependent upon active R-Ras and association between R-Ras and FLNa and that loss of this interaction promotes VE-Cadherin phosphorylation and changes in downstream effectors that lead to endothelial leakiness. The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R-Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa's association with R-Ras affects endothelial barrier function. We report that in endothelial cells endogenous R-Ras interacts with endogenous FLNa as determined by co-immunoprecipitations and pulldowns with the FLNa-GST fusion protein repeats 1-10. Deletion of FLNa repeat 3 (FLNaΔ3) abrogated this interaction. In these cells FLNa and R-Ras co-localize at the plasma membrane. Knockdown of R-Ras and/or FLNa by siRNA promotes vascular permeability, as determined by TransEndothelial Electrical Resistance and FITC-dextran transwell assays. Re-expression of FLNa restored endothelial barrier function in cells lacking FLNa whereas re-expression of FLNaΔ3 did not. Immunostaining for VE-Cadherin in cells with knocked down R-Ras and FLNa demonstrated a disorganization of VE-Cadherin at adherens junctions. Loss of R-Ras and FLNa or blocking R-Ras function via GGTI-2133, a selective R-Ras inhibitor, induced vascular permeability and increased phosphorylation of VE-Cadherin (Y731) and Src (Y416). Expression of dominant negative R-Ras promoted vascular permeability that was blocked by the Src inhibitor PP2. These findings demonstrate that maintaining endothelial barrier function is dependent upon active R-Ras and association between R-Ras and FLNa and that loss of this interaction promotes VE-Cadherin phosphorylation and changes in downstream effectors that lead to endothelial leakiness.The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase R-Ras and repeat 3 of Filamin A (FLNa). Loss of FLNa has been linked to increased vascular permeability. We sought to determine whether FLNa's association with R-Ras affects endothelial barrier function. We report that in endothelial cells endogenous R-Ras interacts with endogenous FLNa as determined by co-immunoprecipitations and pulldowns with the FLNa-GST fusion protein repeats 1-10. Deletion of FLNa repeat 3 (FLNaΔ3) abrogated this interaction. In these cells FLNa and R-Ras co-localize at the plasma membrane. Knockdown of R-Ras and/or FLNa by siRNA promotes vascular permeability, as determined by TransEndothelial Electrical Resistance and FITC-dextran transwell assays. Re-expression of FLNa restored endothelial barrier function in cells lacking FLNa whereas re-expression of FLNaΔ3 did not. Immunostaining for VE-Cadherin in cells with knocked down R-Ras and FLNa demonstrated a disorganization of VE-Cadherin at adherens junctions. Loss of R-Ras and FLNa or blocking R-Ras function via GGTI-2133, a selective R-Ras inhibitor, induced vascular permeability and increased phosphorylation of VE-Cadherin (Y731) and Src (Y416). Expression of dominant negative R-Ras promoted vascular permeability that was blocked by the Src inhibitor PP2. These findings demonstrate that maintaining endothelial barrier function is dependent upon active R-Ras and association between R-Ras and FLNa and that loss of this interaction promotes VE-Cadherin phosphorylation and changes in downstream effectors that lead to endothelial leakiness.
Author	Grundl, M. Matter, M.L. Griffiths, G.S. Allen III, J.S.
AuthorAffiliation	1 Cardiovascular Research Center and the Department of Cell and Molecular Biology, John A. Burns School of Medicine, University of Hawaii at Manoa, 651 Ilalo Street, Honolulu, HI 96813, USA 2 School of Mechanical Engineering, University of Hawaii at Manoa, 2540 Dole Street, Honolulu HI 96822
AuthorAffiliation_xml	– name: 2 School of Mechanical Engineering, University of Hawaii at Manoa, 2540 Dole Street, Honolulu HI 96822 – name: 1 Cardiovascular Research Center and the Department of Cell and Molecular Biology, John A. Burns School of Medicine, University of Hawaii at Manoa, 651 Ilalo Street, Honolulu, HI 96813, USA
Author_xml	– sequence: 1 givenname: G.S. surname: Griffiths fullname: Griffiths, G.S. organization: Department of Cell and Molecular Biology, Cardiovascular Research Center and the John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu, Hawaii – sequence: 2 givenname: M. surname: Grundl fullname: Grundl, M. organization: Department of Cell and Molecular Biology, Cardiovascular Research Center and the John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu, Hawaii – sequence: 3 givenname: J.S. surname: Allen III fullname: Allen III, J.S. organization: School of Mechanical Engineering, University of Hawaii at Manoa, Honolulu Hawaii – sequence: 4 givenname: M.L. surname: Matter fullname: Matter, M.L. email: matter@hawaii.edu organization: Department of Cell and Molecular Biology, Cardiovascular Research Center and the John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu, Hawaii
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Dejana E, Orsenigo F, Lampugnani MG. 2008. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 121: 2115-2122. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, Aepfelbacher M. 1998. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem 273: 21867-21874. Gavard J. 2009. Breaking the VE-cadherin bonds. FEBS Lett 583: 1-6. Cukier IH, Li Y, Lee JM. 2007. Cyclin B1/Cdk1 binds and phosphorylates Filamin A and regulates its ability to cross-link actin. FEBS Lett 581: 1661-1672. Sun J, Ohkanda J, Coppola D, Yin H, Kothare M, Busciglio B, Hamilton AD, Sebti SM. 2003. Geranylgeranyltransferase I inhibitor GGTI-2154 induces breast carcinoma apoptosis and tumor regression in H-Ras transgenic mice. Cancer Res 63: 8922-8929. Tinsley JH, Hunter FA, Childs EW. 2009. PKC and MLCK-Dependent, Cytokine-Induced Rat Coronary Endothelial Dysfunction. J Surg Res 152: 76-83. Takaya A, Kamio T, Masuda M, Mochizuki N, Sawa H, Sato M, Nagashima K, Mizutani A, Matsuno A, Kiyokawa E, Matsuda M. 2007. R-Ras regulates exocytosis by Rgl2/Rlf-mediated activation of RalA on endosomes. Mol Biol Cell 18: 1850-1860. Schiestl RH, Gietz RD. 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16: 339-346. Schulz B, Pruessmeyer J, Maretzky T, Ludwig A, Blobel CP, Saftig P, Reiss K. 2008. ADAM10 regulates endothelial permeability and T-Cell transmigration by proteolysis of vascular endothelial cadherin. Circ Res 102: 1192-1201. Serban D, Leng J, Cheresh D. 2008. H-ras regulates angiogenesis and vascular permeability by activation of distinct downstream effectors. Circ Res 102: 1350-1358. Matter ML, Zhang Z, Nordstedt C, Ruoslahti E. 1998. The alpha5beta1 integrin mediates elimination of amyloid-beta peptide and protects against apoptosis. J Cell Biol 141: 1019-1030. Dejana E, Tournier-Lasserve E, Weinstein BM. 2009. The control of vascular integrity by endothelial cell junctions: Molecular basis and pathological implications. Dev Cell 16: 209-221. Zhou X, Boren J, Akyurek LM. 2007. Filamins in cardiovascular development 1. Trends Cardiovasc Med 17: 222-229. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232. Seye CI, Yu N, Gonzalez FA, Erb L, Weisman GA. 2004. The P2Y2 nucleotide receptor mediates vascular cell adhesion molecule-1 expression through interaction with VEGF receptor-2 (KDR/Flk-1). J Biol Chem 279: 35679-35686. Groeneveld AB. 2002. Vascular pharmacology of acute lung injury and acute respiratory distress syndrome. Vascul Pharmacol 39: 247-256. Vaidyanathan H, Opoku-Ansah J, Pastorino S, Renganathan H, Matter ML, Ramos JW. 2007. ERK MAP kinase is targeted to RSK2 by the phosphoprotein PEA-15 1. Proc Natl Acad Sci USA 104: 19837-19842. Ha CH, Bennett AM, Jin ZG. 2008. A novel role of vascular endothelial cadherin in modulating c-Src activation and downstream signaling of vascular endothelial growth factor. J Biol Chem 283: 7261-7270. Holly SP, Larson MK, Parise LV. 2005. The unique N-terminus of R-ras is required for Rac activation and precise regulation of cell migration 1. Mol Biol Cell 16: 2458-2469. Caraglia M, Budillon A, Tagliaferri P, Marra M, Abbruzzese A, Caponigro F. 2005. Isoprenylation of intracellular proteins as a new target for the therapy of human neoplasms: Preclinical and clinical implications. Curr Drug Targets 6: 301-323. Borbiev T, Verin AD, Shi S, Liu F, Garcia JG. 2001. Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II. Am J Physiol Lung Cell Mol Physiol 280: L983-L990. 2007; 17 2002; 39 2007; 18 2007; 104 2009; 1788 2007; 101 2007; 127 2010; 207 2001; 280 2002; 157 1995; 34 2007; 581 2005; 437 2000; 275 2009; 152 2008; 102 2008; 121 2008; 283 1998; 273 2010; 22 2007; 115 2005; 280 2003; 306 2004; 279 2008; 28 2009; 583 2009; 221 2003; 4 2006; 29 1996; 85 2005; 6 2001; 3 2006; 281 2005; 16 2001; 12 1989; 16 2010; 5 1990; 111 2003; 63 2009; 16 2005; 11 2008; 294 2001; 114 2006; 224 2006; 103 2003; 23 1998; 141 2003; 284 e_1_2_6_51_1 e_1_2_6_53_1 e_1_2_6_32_1 e_1_2_6_30_1 e_1_2_6_19_1 e_1_2_6_13_1 e_1_2_6_36_1 e_1_2_6_11_1 e_1_2_6_34_1 e_1_2_6_17_1 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_20_1 e_1_2_6_41_1 e_1_2_6_5_1 e_1_2_6_7_1 e_1_2_6_24_1 e_1_2_6_49_1 e_1_2_6_3_1 e_1_2_6_22_1 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_47_1 e_1_2_6_52_1 e_1_2_6_10_1 e_1_2_6_31_1 e_1_2_6_50_1 Sun J (e_1_2_6_43_1) 2003; 63 Kusama T (e_1_2_6_26_1) 2006; 29 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_42_1 e_1_2_6_21_1 e_1_2_6_40_1 Cole AL (e_1_2_6_9_1) 2003; 23 e_1_2_6_8_1 e_1_2_6_4_1 e_1_2_6_6_1 e_1_2_6_25_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_29_1 e_1_2_6_44_1 e_1_2_6_27_1 e_1_2_6_46_1
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Snippet	The molecular mechanisms regulating vascular barrier integrity remain incompletely elucidated. We have previously reported an association between the GTPase...
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SubjectTerms	Cadherins - metabolism Capillary Permeability Contractile Proteins - metabolism Coronary Vessels - cytology Cytoskeleton - metabolism Endothelial Cells - cytology Endothelial Cells - metabolism Filamins Gene Knockdown Techniques Humans Microfilament Proteins - metabolism Phosphorylation Phosphoserine - metabolism Protein Binding Protein Transport Proto-Oncogene Proteins pp60(c-src) - metabolism ras Proteins - metabolism RNA, Small Interfering - metabolism
Title	R-Ras interacts with filamin a to maintain endothelial barrier function
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