Therapeutic Strategies to Limit Lung Endothelial Cell Permeability

The Pulmonary Endothelium: Function in health and disease

Volumn , Issue , 2009, Pages 337-354

  Wolfson, Rachel K ^a   Lang, Gabriel ^a   Jacobson, Jeff ^a   Garcia, Joe G N ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Acute (inflammatory) lung injury (ALI); Intracellular signaling pathways and EC edemagenic agents; Methylnaltrexone (MNTX) peripherally restricted mu opioid receptor (mOP R) antagonist; Oxidized phospholipids; Receptor mediated barrier protection role of RAC GTPase; S1P; Simvastatin mediated thrombin inhibition; Sphingolipid from sphingosine phosphorylation; Therapeutic strategies limiting lung endothelial cell permeability; Vascular endothelium primary cellular target in physiologic derangement

Indexed keywords

EID: 84864771059     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470747490.ch21     Document Type: Chapter

References (107)

1. Garcia, J.G., Liu, F., Verin, A.D. et al. (2001) Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. The Journal of Clinical Investigation, 108, 689-701.
2. Singleton, P.A., Dudek, S.M., Ma, S.F., and Garcia, J.G. (2006) Transactivation of sphingosine 1-phosphate receptors is essential for vascular barrier regulation. Novel role for hyaluronan and CD44 receptor family. The Journal of Biological Chemistry, 281, 34381-93.
3. Dudek, S.M. and Garcia, J.G. (2001) Cytoskele-tal regulation of pulmonary vascular permeability. Journal of Applied Physiology, 91, 1487-500.
4. Romer, L.H., Birukov, K.G., and Garcia, J.G. (2006) Focal adhesions: paradigm for a signaling nexus. Circulation Research, 98, 606-16.
5. 2+ signaling in the regulation of endothelial permeability. Vascular Pharmacology, 39, 173-85.
6. Garcia, J.G., Schaphorst, K.L., Shi, S. et al. (1997) Mechanisms of ionomycin-induced endothelial cell barrier dysfunction. American Journal of Physiology: Lung Cellular and Molecular Physiology, 273, L172-84.
7. Borbiev, T., Verin, A.D., Shi, S. et al. (2001) Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II. American Journal of Physiology: Lung Cellular and Molecular Physiology, 280, L983-90.
8. Borbiev, T., Verin, A.D., Birukova, A. et al. (2003) Role of CaM kinase II and ERK activation in thrombin-induced endothelial cell barrier dysfunction. American Journal of Physiology: Lung Cellular and Molecular Physiology, 285, L43-L54.
9. Cai, H., Liu, D., and Garcia, J.G. (2008) CaM kinase II-dependent pathophysiological signalling in endothelial cells. Cardiovascular Research, 77, 30-34.
10. Garcia, J.G., Lazar, V., Gilbert-McClain, L.I. et al. (1997) Myosin light chain kinase in endothelium: molecular cloning and regulation. American Journal of Respiratory Cell and Molecular Biology, 16, 489-94.
11. Garcia, J.G., Verin, A.D., Herenyiova, M., and English, D. (1998) Adherent neutrophils activate endothelial myosin light chain kinase: role in transendothelial migration. Journal of Applied Physiology, 84, 1817-21.
12. 2+/calmodulin-dependent phosphatase 2B in thrombin-induced endothelial cell contractile responses. American Journal of Physiology: Lung Cellular and Molecular Physiology, 275, L788-99.
13. Wang, P., Verin, A.D., Birukova, A. et al. (2001) Mechanisms of sodium fluoride-induced endothelial cell barrier dysfunction: role of MLC phosphorylation. American Journal ofPhysiology: Lung Cellular and Molecular Physiology, 281, L1472-83.
14. Verin, A.D., Csortos, C., Durbin, S.D. et al. (2000) Characterization of the protein phosphatase 1 catalytic subunit in endothelium: involvement in contractile responses. Journal of Cellular Biochemistry, 79, 113-25.
15. Verin, A.D., Wang, P., and Garcia, J.G. (2000) Immunochemical characterization of myosin-specific phosphatase 1 regulatory subunits in bovine endothelium. Journal of Cellular Biochemistry, 76, 489-98.
16. α2-linked Rho kinase activity. American Journal ofRespiratory Cell and Molecular Biology, 24, 711-19.
17. Birukova, A.A., Smurova, K., Birukov, K.G. et al. (2004) Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvascular Research, 67, 64-77.
18. Verin, A.D., Patterson, C.E., Day, M.A., and Garcia, J.G. (1995) Regulation of endothelial cell gap formation and barrier function by myosin-associated phosphatase activities. American Journal of Physiology: Lung Cellular and Molecular Physiology, 269, L99-108.
19. Csortos, C., Kolosova, I., and Verin, A.D. (2007) Regulation of vascular endothelial cell barrier function and cytoskeleton structure by protein phosphatases of the PPP family. American Journal of Physiology: Lung Cellular and Molecular Physiology, 293, L843-54.
20. Kawkitinarong, K., Linz-McGillem, L., Birukov, K.G., and Garcia, J.G. (2004) Differential regulation of human lung epithelial and endothelial barrier function by thrombin. American Journal of Respiratory Cell and Molecular Biology, 31, 517-27.
21. src. American Journal of Physiology: Lung Cellular and Molecular Physiology, 276, L989-98.
22. Garcia, J.G., Davis, H.W., and Patterson, C.E. (1995) Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. Journal of Cellular Physiology, 163, 510-22.
23. Petrache, I., Birukov, K., Zaiman, A.L. et al. (2003) Caspase-dependent cleavage of myosin light chain kinase (MLCK) is involved in TNF-alpha-mediated bovine pulmonary endothelial cell apoptosis. The FASEB Journal, 17, 407-16.
24. Wainwright, M.S., Rossi, J., Schavocky, J. et al. (2003) Protein kinase involved in lung injury susceptibility: evidence from enzyme isoform genetic knockout and in vivo inhibitor treatment. Proceedings of the National Academy of Sciences of the United States of America, 100, 6233-38.
25. Behanna, H.A., Watterson, D.M., and Ranaivo, H.R. (2006) Development of a novel bioavailable inhibitor of the calmodulin-regulated protein kinase MLCK: a lead compound that attenuates vascular leak. Biochimica et Biophysica Acta, 1763, 1266-74.
26. Rossi, J.L., Velentza, A.V., Steinhorn, D.M. et al. (2007) MLCK210 gene knockout or kinase inhibition preserves lung function following endotoxin-induced lung injury in mice. American Journal of Physiology: Lung Cellular and Molecular Physiology, 292, L1327-34.
27. Verin, A.D., Liu, F., Bogatcheva, N. et al. (2000) Role of ras-dependent ERK activation in phorbol ester-induced endothelial cell barrier dysfunction. American Journal of Physiology: Lung Cellular and Molecular Physiology, 279, L360-70.
28. Ikebe, M., Hartshorne, D.J., and Elzinga, M. (1986) Identification, phosphorylation, and dephosphorylation of a second site for myosin light chain kinase on the 20,000-dalton light chain of smooth muscle myosin. The Journal ofBiological Chemistry, 261, 36-39.
29. Ikebe, M., Hartshorne, D.J., and Elzinga, M. (1987) Phosphorylation of the 20,000-dalton light chain of smooth muscle myosin by the calcium-activated, phospholipid-dependent protein kinase. Phosphorylation sites and effects of phosphorylation. The Journal of Biological Chemistry, 262, 9569-73.
30. Bogatcheva, N.V., Verin, A.D., Wang, P. et al. (2003) Phorbol esters increase MLC phosphorylation and actin remodeling in bovine lung endothelium without increased contraction. American Journal of Physiology: Lung Cellular and Molecular Physiology, 285, L415-26.
31. Tinsley, J.H., Teasdale, N.R., and Yuan, S.Y. (2004) Involvement of PKCdelta and PKD in pulmonary microvascular endothelial cell hyperpermeability. American Journal of Physiology: Cell Physiology, 286, C105-11.
32. Stasek, J.E. Jr., Patterson, C.E., and Garcia, J.G. (1992) Protein kinase C phosphorylates caldesmon77 and vimentin and enhances albumin permeability across cultured bovine pulmonary artery endothelial cell monolayers. Journal of Cellular Physiology, 153, 62-75.
33. Bogatcheva, N.V., Birukova, A., Borbiev, T. et al. (2006) Caldesmon is a cytoskeletal target for PKC in endothelium. Journal of Cellular Biochemistry, 99, 1593-605.
34. Mirzapoiazova, T., Kolosova, I.A., Romer, L. et al. (2005) The role of caldesmon in the regulation of endothelial cytoskeleton and migration. Journal of Cellular Physiology, 203, 520-28.
35. Lynch, J.J., Ferro, T.J., Blumenstock, F.A. et al. (1990) Increased endothelial albumin permeability mediated by protein kinase C activation. The Journal of Clinical Investigation, 85, 1991-98.
36. Siflinger-Birnboim, A., Goligorsky, M.S., Del Vecchio, P.J., and Malik, A.B. (1992) Activation of protein kinase C pathway contributes to hydrogen peroxide-induced increase in endothelial permeability. Laboratory Investigation, 67, 24-30.
37. Hammerschmidt, S., Vogel, T., Jockel, S. et al. (2007) Protein kinase C inhibition attenuates hypochlorite-induced acute lung injury. Respiratory Medicine, 101, 1205-11.
38. Chiang, E.T., Persaud-Sawin, D.A., Kulkarni, S. et al. (2006) Bluetongue virus and double-stranded RNA increase human vascular permeability: role of p38 MAPK. Journal of Clinical Immunology, 26, 406-16.
39. Guay, J., Lambert, H., Gingras-Breton, G. et al. (1997) Regulation of actin filament dynamics by p38 MAP kinase-mediated phosphorylation of heat shock protein 27. Journal of Cell Science, 110, 357-68.
40. Borbiev, T., Birukova, A., Liu, F. et al. (2004) p38 MAP kinase-dependent regulation of endothelial cell permeability. American Journal ofPhysiology: Lung Cellular and Molecular Physiology, 287, L911-18.
41. Garcia, J.G., Wang, P., Schaphorst, K.L. et al. (2002) Critical involvement of p38 MAP kinase in pertussis toxin-induced cytoskeletal reorganization and lung permeability. The FASEB Journal, 16, 1064-76.
42. Birukova, A.A., Birukov, K.G., Gorshkov, B. et al. (2005) MAP kinases in lung endothelial permeability induced by microtubule disassembly. American Journal of Physiology: Lung Cellular and Molecular Physiology, 289, L75-L84.
43. Stelzner, T.J., Weil, J.V., and O'Brien, R.F. (1989) Role of cyclic adenosine monophosphate in the induction of endothelial barrier properties. Journal of Cellular Physiology, 139, 157-66.
44. Patterson, C.E., Lum, H., Schaphorst, K.L. et al. (2000) Regulation of endothelial barrier function by the cAMP-dependent protein kinase. Endothelium, 7, 287-308.
45. Liu, F., Verin, A.D., Borbiev, T., and Garcia, J.G. (2001) Role of cAMP-dependent protein kinase A activity in endothelial cell cytoskeleton rearrangement. American Journal of Physiology: Lung Cellular and Molecular Physiology, 280, L1309-17.
46. Birukova, A.A., Liu, F., Garcia, J.G., and Verin, A.D. (2004) Protein kinase A attenuates endothelial cell barrier dysfunction induced by microtubule disassembly. American Journal of Physiology: Lung Cellular and Molecular Physiology, 287, L86-L93.
47. Liu, F., Schaphorst, K.L., Verin, A.D. et al. (2002) Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. The FASEB Journal, 16, 950-62.
48. Jacobson, J.R., Dudek, S.M., Birukov, K.G. et al. (2004) Cytoskeletal activation and altered gene expression in endothelial barrier regulation by simvastatin. American Journal ofRespiratory Cell and Molecular Biology, 30, 662-70.
49. Finigan, J.H., Dudek, S.M., Singleton, P.A. et al. (2005) Activated protein C mediates novel lung endothelial barrier enhancement: role of sphin-gosine 1-phosphate receptor transactivation. The Journal of Biological Chemistry, 280, 17286-93.
50. Jacobson, J.R., Dudek, S.M., Singleton, P.A. et al. (2006) Endothelial cell barrier enhancement by ATP is mediated by the small GTPase Rac and cor-tactin. American Journal ofPhysiology: Lung Cellular and Molecular Physiology, 291, L289-95.
51. Birukov, K.G., Bochkov, V.N., Birukova, A.A. et al. (2004) Epoxycyclopentenone-containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circulation Research, 95, 892-901.
52. Broman, M.T., Mehta, D., and Malik, A.B. (2007) Cdc42 regulates the restoration of endothelial adherens junctions and permeability. Trends in Cardiovascular Medicine, 17, 151-56.
53. Dudek, S.M., Jacobson, J.R., Chiang, E.T. et al. (2004) Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cor-tactin and myosin light chain kinase. The Journal of Biological Chemistry, 279, 24692-700.
54. Birukova, A.A., Zagranichnaya, T., Fu, P. et al. (2007) Prostaglandins PGE2 and PG12 promote endothelial barrier enhancement via PKA-and Epac1/Rap1-dependent Rac activation. Experimental Cell Research, 313, 2504-20.
55. Dudek, S.M., Birukov, K.G., Zhan, X., and Garcia, J.G. (2002) Novel interaction of cortactin with endothelial cell myosin light chain kinase. Biochemical and Biophysical Research Communications, 298, 511-19.
56. Morales-Ruiz, M., Fulton, D., Sowa, G. et al. (2000) Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circulation Research, 86, 892-96.
57. Miyahara, T., Hamanaka, K., Weber, D.S. et al. (2007) Phosphoinositide 3-kinase, Src, and Akt modulate acute ventilation-induced vascular permeability increases in mouse lungs. American Journal of Physiology: Lung Cellular and Molecular Physiology, 293, L11-21.
58. McVerry, B.J. and Garcia, J.G. (2005) In vitro and in vivo modulation of vascular barrier integrity by sphingosine 1-phosphate: mechanistic insights. Cellular Signalling, 17, 131-39.
59. English, D., Welch, Z., Kovala, A.T. et al. (2000) Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and an-giogenesis. The FASEB Journal, 14, 2255-65.
60. Gimbrone, M.A. Jr., Aster, R.H., Cotran, R.S. et al. (1969) Preservation of vascular integrity in organs perfused in vitro with a platelet-rich medium. Nature, 222, 33-36.
61. Schaphorst, K.L., Chiang, E., Jacobs, K.N. et al. (2003) Role of sphingosine-1 phosphate in the enhancement of endothelial barrier integrity by platelet-released products. American Journal of Physiology: Lung Cellular and Molecular Physiology, 285, L258-67.
62. English, D., Kovala, A.T., Welch, Z. et al. (1999) Induction of endothelial cell chemotaxis by sphin-gosine 1-phosphate and stabilization of endothelial monolayer barrier function by lysophosphatidic acid, potential mediators of hematopoietic angio-genesis. Journal of Hematotherapy and Stem Cell Research, 8, 627-34.
63. McVerry, B.J. and Garcia, J.G. (2004) Endothelial cell barrier regulation by sphingosine 1-phosphate. Journal of Cellular Biochemistry, 92, 1075-85.
64. 2+ mediates rac activation and adherens junction assembly in endothelial cells. The Journal of Biological Chemistry, 280, 17320-28.
65. Guo, Y., Singleton, P.A., Rowshan, A. et al. (2007) Quantitative proteomics analysis of human endothelial cell membrane rafts: evidence of MARCKS and MRP regulation in the sphingosine 1-phosphate-induced barrier enhancement. Molecular and Cellular Proteomics, 6, 689-96.
66. Arce, F.T., Whitlock, J.L., Birukova, A.A. et al. (2008) Regulation of the micromechanical properties of pulmonary endothelium by S1P and thrombin: role of cortactin. Biophysical Journal, 95, 886-94.
67. Weed, S.A. and Parsons, J.T. (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene, 20, 6418-34.
68. Shikata, Y., Birukov, K.G., and Garcia, J.G. (2003) S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. Journal of Applied Physiology, 94, 1193-203.
69. Peng, X., Hassoun, P.M., Sammani, S. et al. (2004) Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. American Journal of Respiratory and Critical Care Medicine, 169, 1245-51.
70. McVerry, B.J., Peng, X., Hassoun, P.M. et al. (2004) Sphingosine 1-phosphate reduces vascular leak in murine and canine models of acute lung injury. American Journal ofRespiratory and Critical Care Medicine, 170, 987-93.
71. Moreno-Vinasco, L., Jacobson, J.R., Bonde, P. et al. (2008) Attenuation of ischemia-reperfusion lung injury by sphingosine 1-phosphate in rodents. Journal of Organ Dysfunction, 4, 106-14.
72. Gon, Y., Wood, M.R., Kiosses, W.B. et al. (2005) S1P3 receptor-induced reorganization of epithelial tight junctions compromises lung barrier integrity and is potentiated by TNF. Proceedings of the National Academy of Sciences of the United States of America, 102, 9270-75.
73. Forrest, M., Sun, S.Y., Hajdu, R. et al. (2004) Immune cell regulation and cardiovascular effects of sphingosine 1-phosphate receptor agonists in rodents are mediated via distinct receptor subtypes. The Journal of Pharmacology and Experimental Therapeutics, 309, 758-68.
74. Chiba, K. (2005) FTY720, a new class of im-munomodulator, inhibits lymphocyte egress from secondary lymphoid tissues and thymus by agonistic activity at sphingosine 1-phosphate receptors. Pharmacology and Therapeutics, 108, 308-19.
75. Tedesco-Silva, H., Szakaly, P., Shoker, A. et al. (2007) FTY720 versus mycophenolate mofetil in de novo renal transplantation: six-month results of a double-blind study. Transplantation, 84, 885-92.
76. Dudek, S.M., Camp, S.M., Chiang, E.T. et al. (2007) Pulmonary endothelial cell barrier enhancement by FTY720 does not require the S1P1 receptor. Cellular Signalling, 19, 1754-64.
77. van Nieuw Amerongen, G.P., Vermeer, M.A., Negre-Aminou, P. et al. (2000) Simvastatin improves disturbed endothelial barrier function. Circulation, 102, 2803-9.
78. Liappis, A.P., Kan, V.L., Rochester, C.G., and Simon, G.L. (2001) The effect of statins on mortality in patients with bacteremia. Clinical Infectious Diseases, 33, 1352-57.
79. Merx, M.W., Liehn, E.A., Janssens, U. et al. (2004) HMG-CoA reductase inhibitor simvastatin profoundly improves survival in a murine model of sepsis. Circulation, 109, 2560-65.
80. Merx, M.W., Liehn, E.A., Graf, J. et al. (2005) Statin treatment after onset of sepsis in a murine model improves survival. Circulation, 112, 117-24.
81. Schmidt, H., Hennen, R., Keller, A. et al. (2006) Association of statin therapy and increased survival in patients with multiple organ dysfunction syndrome. Intensive Care Medicine, 32, 1248-51.
82. Chen, W., Pendyala, S., Natarajan, V. et al. (2008) Endothelial cell barrier protection by simvastatin: GTPase regulation and NADPH oxidase inhibition. American Journal of Physiology: Lung Cellular and Molecular Physiology, 295, L575-83.
83. Jacobson, J.R., Barnard, J.W., Grigoryev, D.N. et al. (2005) Simvastatin attenuates vascular leak and inflammation in murine inflammatory lung injury. American Journal of Physiology: Lung Cellular and Molecular Physiology, 288, L1026-32.
84. Kolosova, I.A., Mirzapoiazova, T., Adyshev, D. et al. (2005) Signaling pathways involved in adenosine triphosphate-induced endothelial cell barrier enhancement. Circulation Research, 97, 115-24.
85. Schwiebert, L.M., Rice, W.C., Kudlow, B.A. et al. (2002) Extracellular ATP signaling and P2X nucleotide receptors in monolayers of primary human vascular endothelial cells. American Journal ofPhysiology: Cell Physiology, 282, C289-C301.
86. 2+]i. American Journal of Physiology, 276, H1892-901.
87. Noll, T., Schafer, M., Schavier-Schmitz, U., and Piper, H.M. (2000) ATP induces dephosphorylation of myosin light chain in endothelial cells. American Journal of Physiology: Cell Physiology, 279, C717-23.
88. Gunduz, D., Hirche, F., Hartel, F.V. et al. (2003) ATP antagonism of thrombin-induced endothelial barrier permeability. Cardiovascular Research, 59, 470-78.
89. Kolosova, I.A., Mirzapoiazova, T., Moreno-Vinasco, L. et al. (2008) Protective effect of purinergic agonist ATPgammaS against acute lung injury. American Journal of Physiology: Lung Cellular and Molecular Physiology, 294, L319-24.
90. Singleton, P.A., Salgia, R., Moreno-Vinasco, L. et al. (2007) CD44 regulates hepatocyte growth factor-mediated vascular integrity. Role of c-Met, Tiam1/Rac1, dynamin 2, and cortactin. The Journal of Biological Chemistry, 282, 30643-57.
91. Birukova, A.A., Alekseeva, E., Mikaelyan, A., and Birukov, K.G. (2007) HGF attenuates thrombin-induced endothelial permeability by Tiam1-mediated activation of the Rac pathway and by Tiam1/Rac-dependent inhibition of the Rho pathway. The FASEB Journal, 21, 2776-86.
92. Bernard, G.R., Vincent, J.L., Laterre, P.F. et al. (2001) Efficacy and safety of recombinant human activated protein C for severe sepsis. The New England Journal of Medicine, 344, 699-709.
93. Kalil, A.C., Coyle, S.M., Um, J.Y. et al. (2004) Effects of drotrecogin alfa (activated) in human endotoxemia. Shock, 21, 222-29.
94. Teke, Z., Sacar, M., Yenisey, C. et al. (2008) Activated protein C attenuates intestinal reperfusion-induced acute lung injury: an experimental study in a rat model. American Journal of Surgery, 195, 861-73.
95. Birukov, K.G., Leitinger, N., Bochkov, V.N., and Garcia, J.G. (2004) Signal transduction pathways activated in human pulmonary endothelial cells by OxPAPC, a bioactive component of oxidized lipoproteins. Microvascular Research, 67, 18-28.
96. Chabot, F., Mitchell, J.A., Gutteridge, J.M., and Evan's, T.W. (1998) Reactive oxygen species in acute lung injury. The European Respiratory Journal, 11, 745-57.
97. Birukova, A.A., Chatchavalvanich, S., Oskolkova, O. et al. (2007) Signaling pathways involved in OxPAPC-induced pulmonary endothelial barrier protection. Microvascular Research, 73, 173-81.
98. Nonas, S., Birukova, A.A., Fu, P. et al. (2008) Oxidized phospholipids reduce ventilator-induced vascular leak and inflammation in vivo. Critical Care, 12, R27.
99. Nonas, S., Miller, I., Kawkitinarong, K. et al. (2006) Oxidized phospholipids reduce vascular leak and inflammation in rat model of acute lung injury. American Journal of Respiratory and Critical Care Medicine, 173, 1130-38.
100. Birukova, A.A., Fu, P., Chatchavalvanich, S. et al. (2007) Polar head groups are important for barrier-protective effects of oxidized phospholipids on pulmonary endothelium. American Journal of Physiology: Lung Cellular and Molecular Physiology, 292, L924-35.
101. Birukova, A.A., Malyukova, I., Mikaelyan, A. et al. (2007) Tiam1 and betaPIX mediate Rac-dependent endothelial barrier protective response to oxidized phospholipids. Journal of Cellular Physiology, 211, 608-17.
102. Birukova, A.A., Malyukova, I., Poroyko, V., and Birukov, K.G. (2007) Paxillin-beta-catenin interactions are involved in Rac/Cdc42-mediated endothelial barrier-protective response to oxidized phospholipids. American Journal of Physiology: Lung Cellular and Molecular Physiology, 293, L199-211.
103. 2, and its mechanisms. Prostaglandins, 53, 279-89.
104. Farmer, P.J., Bernier, S.G., Lepage, A. et al. (2001) Permeability of endothelial monolayers to albumin is increased by bradykinin and inhibited by prostaglandins. American Journal ofPhys-iology: Lung Cellular and Molecular Physiology, 280, L732-38.
105. Singleton, P.A., Garcia, J.G., and Moss, J. (2008) Synergistic effects of methylnaltrexone with 5-fluorouracil and bevacizumab on inhibition of vascular endothelial growth factor-induced angiogenesis. Molecular Cancer Therapeutics, 7, 1669-79.
106. Liu, H.C., Anday, J.K., House, S.D., and Chang, S.L. (2004) Dual effects of morphine on permeability and apoptosis of vascular endothelial cells: morphine potentiates lipopolysaccharide-induced permeability and apoptosis of vascular endothelial cells. Journal of Neuroimmunology, 146, 13-21.
107. Singleton, P.A., Moreno-Vinasco, L., Sammani, S. et al. (2007) Attenuation of vascular permeability by methylnaltrexone: role of mOP-R and S1P3 transactivation. American Journal of Respiratory Cell and Molecular Biology, 37, 222-31.