A role for VEGFR2 activation in endothelial responses caused by barrier disruptive OxPAPC concentrations

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Birukova, Anna A ^a   Lee, Sangderk ^b   Starosta, Vitaliy ^a   Wu, Tinghuai ^a   Ho, Tiffany ^b   Kim, Jin ^b   Berliner, Judith A ^b   Birukov, Konstantin G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYL 2 ARACHIDONOYL SN GLYCERO 3 PHOSPHATIDYLCHOLINE; ACTIN; ADVANCED OXIDATION PROTEIN PRODUCT; MYOSIN LIGHT CHAIN; PHALLOIDIN; RHO FACTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2; YTTRIUM; CADHERIN; LEUKOCYTE ANTIGEN; OXIDIZED L ALPHA 1 PALMITOYL 2 ARACHIDONOYL SN GLYCERO 3 PHOSPHORYLCHOLINE; OXIDIZED-L-ALPHA-1-PALMITOYL-2-ARACHIDONOYL-SN-GLYCERO-3-PHOSPHORYLCHOLINE; PHOSPHATIDYLCHOLINE; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

AORTA; ARTERY ENDOTHELIUM; ARTICLE; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; DOSE RESPONSE; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LUNG CIRCULATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PULMONARY ARTERY; SIGNAL TRANSDUCTION; STRESS FIBER; SYSTEMIC CIRCULATION; TRANSENDOTHELIAL ELECTRIC RESISTANCE; WESTERN BLOTTING; ACTIN FILAMENT; CYTOLOGY; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; IMPEDANCE; INTRACELLULAR SPACE; METABOLISM; PROTEIN TRANSPORT;

ACTIN CYTOSKELETON; ANTIGENS, CD; AORTA; CADHERINS; CELL MEMBRANE PERMEABILITY; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; INTRACELLULAR SPACE; MYOSIN LIGHT CHAINS; PHOSPHATIDYLCHOLINES; PROTEIN TRANSPORT; PULMONARY ARTERY; RAC GTP-BINDING PROTEINS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; STRESS FIBERS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84856408598     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030957     Document Type: Article

References (56)

1. Berliner JA, Gharavi NM, (2008) Endothelial cell regulation by phospholipid oxidation products. Free Radic Biol Med 45: 119-123.
2. Bochkov VN, Oskolkova OV, Birukov KG, Levonen AL, Binder CJ, et al. (2010) Generation and biological activities of oxidized phospholipids. Antioxid Redox Signal 12: 1009-1059.
3. Gargalovic PS, Gharavi NM, Clark MJ, Pagnon J, Yang WP, et al. (2006) The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 26: 2490-2496.
4. Zimman A, Chen SS, Komisopoulou E, Titz B, Martinez-Pinna R, et al. (2010) Activation of aortic endothelial cells by oxidized phospholipids: a phosphoproteomic analysis. J Proteome Res 9: 2812-2824.
5. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, et al. (2008) Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235-249.
6. Ma Z, Li J, Yang L, Mu Y, Xie W, et al. (2004) Inhibition of LPS- and CpG DNA-induced TNF-alpha response by oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol 286: L808-816.
7. Nonas S, Birukova AA, Fu P, Xing J, Chatchavalvanich S, et al. (2008) Oxidized phospholipids reduce ventilator-induced vascular leak and inflammation in vivo. Crit Care 12: R27.
8. Nonas SA, Miller I, Kawkitinarong K, Chatchavalvanich S, Gorshkova I, et al. (2006) Oxidized phospholipids reduce vascular leak and inflammation in rat model of acute lung injury. Am J Respir Crit Care Med 173: 1130-1138.
9. Birukova AA, Malyukova I, Poroyko V, Birukov KG, (2007) Paxillin- {beta}-catenin interactions are involved in Rac/Cdc42-mediated endothelial barrier-protective response to oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol 293: L199-211.
10. Birukova AA, Zebda N, Fu P, Poroyko V, Cokic I, et al. (2011) Association between adherens junctions and tight junctions via Rap1 promotes barrier protective effects of oxidized phospholipids. J Cell Physiol 226: 2052-2062.
11. Birukov KG, Bochkov VN, Birukova AA, Kawkitinarong K, Rios A, et al. (2004) Epoxycyclopentenone-containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res 95: 892-901.
12. Birukova AA, Fu P, Chatchavalvanich S, Burdette D, Oskolkova O, et al. (2007) Polar head groups are important for barrier protective effects of oxidized phospholipids on pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 292: L924-935.
13. DeMaio L, Rouhanizadeh M, Reddy S, Sevanian A, Hwang J, et al. (2006) Oxidized phospholipids mediate occludin expression and phosphorylation in vascular endothelial cells. Am J Physiol Heart Circ Physiol 290: H674-683.
14. Zimman A, Mouillesseaux KP, Le T, Gharavi NM, Ryvkin A, et al. (2007) Vascular endothelial growth factor receptor 2 plays a role in the activation of aortic endothelial cells by oxidized phospholipids. Arterioscler Thromb Vasc Biol 27: 332-338.
15. Medford AR, Millar AB, (2006) Vascular endothelial growth factor (VEGF) in acute lung injury (ALI) and acute respiratory distress syndrome (ARDS): paradox or paradigm? Thorax 61: 621-626.
16. Sun H, Breslin JW, Zhu J, Yuan SY, Wu MH, (2006) Rho and ROCK signaling in VEGF-induced microvascular endothelial hyperpermeability. Microcirculation 13: 237-247.
17. Beckers CM, van Hinsbergh VW, van Nieuw Amerongen GP, (2010) Driving Rho GTPase activity in endothelial cells regulates barrier integrity. Thromb Haemost 103: 40-55.
18. Subbanagounder G, Leitinger N, Schwenke DC, Wong JW, Lee H, et al. (2000) Determinants of bioactivity of oxidized phospholipids. Specific oxidized fatty acyl groups at the sn-2 position. Arterioscler Thromb Vasc Biol 20: 2248-2254.
19. Breslin JW, Pappas PJ, Cerveira JJ, Hobson RW 2nd, Duran WN, (2003) VEGF increases endothelial permeability by separate signaling pathways involving ERK-1/2 and nitric oxide. Am J Physiol Heart Circ Physiol 284: H92-H100.
20. Kaner RJ, Ladetto JV, Singh R, Fukuda N, Matthay MA, et al. (2000) Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema. Am J Respir Cell Mol Biol 22: 657-664.
21. Gavard J, Gutkind JS, (2006) VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8: 1223-1234.
22. Mirzapoiazova T, Kolosova I, Usatyuk PV, Natarajan V, Verin AD, (2006) Diverse effects of vascular endothelial growth factor on human pulmonary endothelial barrier and migration. Am J Physiol Lung Cell Mol Physiol 291: L718-724.
23. Birukova AA, Moldobaeva N, Xing J, Birukov KG, (2008) Magnitude-dependent effects of cyclic stretch on HGF- and VEGF-induced pulmonary endothelial remodeling and barrier regulation. Am J Physiol Lung Cell Mol Physiol 295: L612-623.
24. Dudek SM, Garcia JG, (2001) Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91: 1487-1500.
25. Birukova AA, Smurova K, Birukov KG, Kaibuchi K, Garcia JGN, et al. (2004) Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 67: 64-77.
26. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, et al. (1998) Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem 273: 21867-21874.
27. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW, (2000) Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res 87: 335-340.
28. van Nieuw Amerongen GP, Koolwijk P, Versteilen A, van Hinsbergh VW, (2003) Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler Thromb Vasc Biol 23: 211-217.
29. Starosta V, Wu T, Zimman A, Pham D, Tian X, et al. (2011) Differential Regulation of Endothelial Cell Permeability by High and low Doses of OxPAPC. Am J Respir Cell Mol Biol Oct 13. [Epub ahead of print].
30. Lee S, Gharavi NM, Honda H, Chang I, Kim B, et al. (2009) A role for NADPH oxidase 4 in the activation of vascular endothelial cells by oxidized phospholipids. Free Radic Biol Med 47: 145-151.
31. Chen W, Pendyala S, Natarajan V, Garcia JG, Jacobson JR, (2008) Endothelial cell barrier protection by simvastatin: GTPase regulation and NADPH oxidase inhibition. Am J Physiol Lung Cell Mol Physiol 295: L575-583.
32. Fu P, Birukov KG, (2009) Oxidized phospholipids in control of inflammation and endothelial barrier. Transl Res 153: 166-176.
33. Bochkov VN, Kadl A, Huber J, Gruber F, Binder BR, et al. (2002) Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature 419: 77-81.
34. Podrez EA, Byzova TV, Febbraio M, Salomon RG, Ma Y, et al. (2007) Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat Med 13: 1086-1095.
35. Hammad LA, Wu G, Saleh MM, Klouckova I, Dobrolecki LE, et al. (2009) Elevated levels of hydroxylated phosphocholine lipids in the blood serum of breast cancer patients. Rapid Commun Mass Spectrom 23: 863-876.
36. Oskolkova OV, Afonyushkin T, Preinerstorfer B, Bicker W, von Schlieffen E, et al. (2010) Oxidized Phospholipids Are More Potent Antagonists of Lipopolysaccharide than Inducers of Inflammation. J Immunol 185: 7706-7712.
37. Watson AD, Leitinger N, Navab M, Faull KF, Horkko S, et al. (1997) Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem 272: 13597-13607.
38. Birukova AA, Chatchavalvanich S, Oskolkova O, Bochkov VN, Birukov KG, (2007) Signaling pathways involved in OxPAPC-induced pulmonary endothelial barrier protection. Microvasc Res 73: 173-181.
39. Birukova AA, Malyukova I, Mikaelyan A, Fu P, Birukov KG, (2007) Tiam1 and betaPIX mediate Rac-dependent endothelial barrier protective response to oxidized phospholipids. J Cell Physiol 211: 608-617.
40. Birukova AA, Zebda N, Cokic I, Fu P, Wu T, et al. (2011) p190RhoGAP mediates protective effects of oxidized phospholipids in the models of ventilator-induced lung injury. Exp Cell Res 317: 859-872.
41. Leitinger N, Tyner TR, Oslund L, Rizza C, Subbanagounder G, et al. (1999) Structurally similar oxidized phospholipids differentially regulate endothelial binding of monocytes and neutrophils. Proc Natl Acad Sci U S A 96: 12010-12015.
42. Birukov KG, Leitinger N, Bochkov VN, Garcia JG, (2004) Signal transduction pathways activated in human pulmonary endothelial cells by OxPAPC, a bioactive component of oxidized lipoproteins. Microvasc Res 67: 18-28.
43. Zeng H, Zhao D, Mukhopadhyay D, (2002) KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/11-mediated activation of a small GTPase RhoA. J Biol Chem 277: 46791-46798.
44. Potter MD, Barbero S, Cheresh DA, (2005) Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem 280: 31906-31912.
45. Cole AL, Subbanagounder G, Mukhopadhyay S, Berliner JA, Vora DK, (2003) Oxidized phospholipid-induced endothelial cell/monocyte interaction is mediated by a cAMP-dependent R-Ras/PI3-kinase pathway. Arterioscler Thromb Vasc Biol 23: 1384-1390.
46. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, et al. (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. Embo J 15: 510-519.
47. Qiao J, Huang F, Lum H, (2003) PKA inhibits RhoA activation: a protection mechanism against endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 284: L972-980.
48. Busca R, Bertolotto C, Abbe P, Englaro W, Ishizaki T, et al. (1998) Inhibition of Rho is required for cAMP-induced melanoma cell differentiation. Mol Biol Cell 9: 1367-1378.
49. Petrovan RJ, Kaplan CD, Reisfeld RA, Curtiss LK, (2007) DNA vaccination against VEGF receptor 2 reduces atherosclerosis in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol 27: 1095-1100.
50. Yeh M, Leitinger N, de Martin R, Onai N, Matsushima K, et al. (2001) Increased transcription of IL-8 in endothelial cells is differentially regulated by TNF-alpha and oxidized phospholipids. Arterioscler Thromb Vasc Biol 21: 1585-1591.
51. Birukova AA, Chatchavalvanich S, Rios A, Kawkitinarong K, Garcia JG, et al. (2006) Differential regulation of pulmonary endothelial monolayer integrity by varying degrees of cyclic stretch. Am J Pathol 168: 1749-1761.
52. Birukova AA, Smurova K, Birukov KG, Usatyuk P, Liu F, et al. (2004) Microtubule disassembly induces cytoskeletal remodeling and lung vascular barrier dysfunction: Role of Rho-dependent mechanisms. J Cell Physiol 201: 55-70.
53. Birukova AA, Birukov KG, Smurova K, Adyshev DM, Kaibuchi K, et al. (2004) Novel role of microtubules in thrombin-induced endothelial barrier dysfunction. FASEB J 18: 1879-1890.
54. Birukova AA, Adyshev D, Gorshkov B, Bokoch GM, Birukov KG, et al. (2006) GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 290: L540-548.
55. Shikata Y, Birukov KG, Birukova AA, Verin AD, Garcia JG, (2003) Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J 17: 2240-2249.
56. Shikata Y, Rios A, Kawkitinarong K, DePaola N, Garcia JG, et al. (2005) Differential effects of shear stress and cyclic stretch on focal adhesion remodeling, site-specific FAK phosphorylation, and small GTPases in human lung endothelial cells. Exp Cell Res 304: 40-49.