Sac-1004, a novel vascular leakage blocker, enhances endothelial barrier through the cAMP/Rac/cortactin pathway

Biochemical and Biophysical Research Communications

Volumn 435, Issue 3, 2013, Pages 420-427

  Maharjan, Sony ^a   Kim, Kyeojin ^b   Agrawal, Vijayendra ^a   Choi, Hyun Jung ^a   Kim, Nam Jung ^b   Kim, Young Myeong ^c   Suh, Young Ger ^b   Kwon, Young Guen ^a  

^a Yonsei University   (South Korea)

^b Seoul National University   (South Korea)

^c Kangwon National University   (South Korea)

Author keywords

Cortactin; Endothelial cells; Rac; Sac 1004; Vascular permeability; VEGF

Indexed keywords

2',3' DIDEOXYADENOSINE; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; 4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; ACTIN; CORTACTIN; CYCLIC AMP; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; HISTAMINE; RAC PROTEIN; SAC 1004; THROMBIN; UNCLASSIFIED DRUG; VASCULAR TARGETING AGENT; VASCULOTROPIN;

ARTICLE; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; DRUG INHIBITION; DRUG MECHANISM; DRUG STRUCTURE; ENDOTHELIAL BARRIER; ENDOTHELIAL HYPERPERMEABILITY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOPRECIPITATION; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING;

CAPILLARY PERMEABILITY; CELLS, CULTURED; CORTACTIN; CYCLIC AMP; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; PREGNENOLONE; RAC GTP-BINDING PROTEINS; SAPONINS; SIGNAL TRANSDUCTION;

EID: 84878981742     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.04.104     Document Type: Article

References (34)

1. Mehta D., Malik A.B. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 2006, 86:279-367.
2. Vestweber D., Winderlich M., Cagna G., Nottebaum A.F. Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol. 2009, 19:8-15.
3. Barber A.J. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27:283-290.
4. Maniatis N.A., Kotanidou A., Catravas J.D., Orfanos S.E. Endothelial pathomechanisms in acute lung injury. Vasc. Pharmacol. 2008, 49:119-133.
5. Lusis A.J. Atherosclerosis. Nature 2000, 407:233-241.
6. Vandenbroucke E., Mehta D., Minshall R., Malik A.B. Regulation of endothelial junctional permeability. Ann. N. Y. Acad. Sci. 2008, 1123:134-145.
7. Bazzoni G., Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 2004, 84:869-901.
8. Birukova A.A., Zagranichnaya T., Fu P., Alekseeva E., Chen W., Jacobson J.R., Birukov K.G. Prostaglandins PGE(2) and PGI(2) promote endothelial barrier enhancement via PKA- and Epac1/Rap1-dependent Rac activation. Exp. Cell Res. 2007, 313:2504-2520.
9. Liu F., Verin A.D., Borbiev T., Garcia J.G. Role of cAMP-dependent protein kinase A activity in endothelial cell cytoskeleton rearrangement. Am. J. Physiol. Lung Cell. Mol. Physiol. 2001, 280:L1309-1317.
10. Spindler V., Schlegel N., Waschke J. Role of GTPases in control of microvascular permeability. Cardiovasc. Res. 2010, 87:243-253.
11. Baumer Y., Spindler V., Werthmann R.C., Bunemann M., Waschke J. Role of Rac 1 and cAMP in endothelial barrier stabilization and thrombin-induced barrier breakdown. J. Cell. Physiol. 2009, 220:716-726.
12. Dejana E., Tournier-Lasserve E., Weinstein B.M. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev. Cell 2009, 16:209-221.
13. Furst R., Bubik M.F., Bihari P., Mayer B.A., Khandoga A.G., Hoffmann F., Rehberg M., Krombach F., Zahler S., Vollmar A.M. Atrial natriuretic peptide protects against histamine-induced endothelial barrier dysfunction in vivo. Mol. Pharmacol. 2008, 74:1-8.
14. Bubik M.F., Willer E.A., Bihari P., Jurgenliemk G., Ammer H., Krombach F., Zahler S., Vollmar A.M., Furst R. A novel approach to prevent endothelial hyperpermeability: the Crataegus extract WS(R) 1442 targets the cAMP/Rap1 pathway. J. Mol. Cell. Cardiol. 2012, 52:196-205.
15. Birukova A.A., Zebda N., Fu P., Poroyko V., Cokic I., Birukov K.G. Association between adherens junctions and tight junctions via Rap1 promotes barrier protective effects of oxidized phospholipids. J. Cell. Physiol. 2011, 226:2052-2062.
16. Komarova Y., Malik A.B. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu. Rev. Physiol. 2010, 72:463-493.
17. Maharjan S., Lee S., Agrawal V., Choi H.J., Maeng Y.S., Kim K., Kim N.J., Suh Y.G., Kwon Y.G. Sac-0601 prevents retinal vascular leakage in a mouse model of diabetic retinopathy. Eur. J. Pharmacol. 2011, 657:35-40.
18. Hou W.H., Liu I.H., Tsai C.C., Johnson F.E., Huang S.S., Huang J.S. CRSBP-1/LYVE-1 ligands disrupt lymphatic intercellular adhesion by inducing tyrosine phosphorylation and internalization of VE-cadherin. J. Cell Sci. 2011, 124:1231-1244.
19. Jacobson J.R., Dudek S.M., Singleton P.A., Kolosova I.A., Verin A.D., Garcia J.G. Endothelial cell barrier enhancement by ATP is mediated by the small GTPase Rac and cortactin. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L289-295.
20. Birukova A.A., Alekseeva E., Mikaelyan A., Birukov K.G. HGF attenuates thrombin-induced endothelial permeability by Tiam1-mediated activation of the Rac pathway and by Tiam1/Rac-dependent inhibition of the Rho pathway. FASEB J. 2007, 21:2776-2786.
21. Dejana E., Orsenigo F., Lampugnani M.G. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell. Sci. 2008, 121:2115-2122.
22. Andriopoulou P., Navarro P., Zanetti A., Lampugnani M.G., Dejana E. Histamine induces tyrosine phosphorylation of endothelial cell-to-cell adherens junctions. Arterioscler. Thromb. Vasc. Biol. 1999, 19:2286-2297.
23. Gavard J., Gutkind J.S. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 2006, 8:1223-1234.
24. Lin M.T., Yen M.L., Lin C.Y., Kuo M.L. Inhibition of vascular endothelial growth factor-induced angiogenesis by resveratrol through interruption of Src-dependent vascular endothelial cadherin tyrosine phosphorylation. Mol. Pharmacol. 2003, 64:1029-1036.
25. Pyun B.J., Choi S., Lee Y., Kim T.W., Min J.K., Kim Y., Kim B.D., Kim J.H., Kim T.Y., Kim Y.M., Kwon Y.G. Capsiate, a nonpungent capsaicin-like compound, inhibits angiogenesis and vascular permeability via a direct inhibition of Src kinase activity. Cancer Res. 2008, 68:227-235.
26. Sandoval K.E., Witt K.A. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol. Dis. 2008, 32:200-219.
27. Kaur C., Foulds W.S., Ling E.A. Blood-retinal barrier in hypoxic ischaemic conditions: basic concepts, clinical features and management. Prog. Retin. Eye Res. 2008, 27:622-647.
28. Birukova A.A., Tian Y., Dubrovskyi O., Zebda N., Sarich N., Tian X., Wang Y., Birukov K.G. VE-cadherin trans-interactions modulate Rac activation and enhancement of lung endothelial barrier by iloprost. J. Cell. Physiol. 2012, 227:3405-3416.
29. Prasain N., Stevens T. The actin cytoskeleton in endothelial cell phenotypes. Microvasc. Res. 2009, 77:53-63.
30. Suttorp N., Weber U., Welsch T., Schudt C. Role of phosphodiesterases in the regulation of endothelial permeability in vitro. J. Clin. Invest. 1993, 91:1421-1428.
31. Sheldon R., Moy A., Lindsley K., Shasby S., Shasby D.M. Role of myosin light-chain phosphorylation in endothelial cell retraction. Am. J. Physiol. 1993, 265:L606-L612.
32. Fu B.M., Shen S., Chen B. Structural mechanisms in the abolishment of VEGF-induced microvascular hyperpermeability by cAMP. J. Biomech. Eng. 2006, 128:317-328.
33. Weis S.M., Cheresh D.A. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 2005, 437:497-504.
34. Kumar P., Shen Q., Pivetti C.D., Lee E.S., Wu M.H., Yuan S.Y. Molecular mechanisms of endothelial hyperpermeability: implications in inflammation. Expert Rev. Mol. Med. 2009, 11:e19.