Lung endothelial barrier protection by iloprost in the 2-hit models of ventilator-induced lung injury (VILI) involves inhibition of Rho signaling

Translational Research

Volumn 155, Issue 1, 2010, Pages 44-54

  Birukova, Anna A ^a   Fu, Panfeng ^a   Xing, Junjie ^a   Cokic, Ivan ^a   Birukov, Konstantin G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EVANS BLUE; GUANOSINE TRIPHOSPHATASE; ILOPROST; MYOSIN LIGHT CHAIN; PHOSPHATASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; THROMBIN; THROMBIN RECEPTOR ACTIVATING PEPTIDE 6;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; BLOOD CLOTTING; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DISEASE MODEL; DRUG EFFECT; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INFLAMMATION; LUNG ENDOTHELIUM; LUNG INJURY; LUNG LAVAGE; LUNG PARENCHYMA; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; SIGNAL TRANSDUCTION; STRETCHING; TIDAL VOLUME; VENTILATOR INDUCED LUNG INJURY;

EID: 71049174151     PISSN: 19315244     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.trsl.2009.09.002     Document Type: Article

References (60)

1. Slutsky A.S., and Tremblay L.N. Multiple system organ failure. Is mechanical ventilation a contributing factor?. Am J Respir Crit Care Med 157 (1998) 1721-1725
2. Dos Santos C.C., and Slutsky A.S. Invited review: mechanisms of ventilator-induced lung injury: a perspective. J Appl Physiol 89 (2000) 1645-1655
3. Uhlig S. Ventilation-induced lung injury and mechanotransduction: stretching it too far?. Am J Physiol Lung Cell Mol Physiol 282 (2002) L892-L896
4. Oeckler R.A., and Hubmayr R.D. Ventilator-associated lung injury: a search for better therapeutic targets. Eur Respir J 30 (2007) 1216-1226
5. Schultz M.J., Haitsma J.J., Zhang H., and Slutsky A.S. Pulmonary coagulopathy as a new target in therapeutic studies of acute lung injury or pneumonia-a review. Crit Care Med 34 (2006) 871-877
6. Russell J.A. Management of sepsis. N Engl J Med 355 (2006) 1699-1713
7. Ware L.B., Camerer E., Welty-Wolf K., Schultz M.J., and Matthay M.A. Bench to bedside: targeting coagulation and fibrinolysis in acute lung injury. Am J Physiol Lung Cell Mol Physiol 291 (2006) L307-L311
8. Narimanbekov I.O., and Rozycki H.J. Effect of IL-1 blockade on inflammatory manifestations of acute ventilator-induced lung injury in a rabbit model. Exp Lung Res 21 (1995) 239-254
9. Pugin J., Dunn I., Jolliet P., et al. Activation of human macrophages by mechanical ventilation in vitro. Am J Physiol 275 (1998) L1040-L1050
10. Vlahakis N.E., Schroeder M.A., Limper A.H., and Hubmayr R.D. Stretch induces cytokine release by alveolar epithelial cells in vitro. Am J Physiol 277 (1999) L167-L173
11. Birukova A.A., Chatchavalvanich S., Rios A., Kawkitinarong K., Garcia J.G., and Birukov K.G. Differential regulation of pulmonary endothelial monolayer integrity by varying degrees of cyclic stretch. Am J Pathol 168 (2006) 1749-1761
12. Birukova A.A., Moldobaeva N., Xing J., and Birukov K.G. 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 (2008) L612-L623
13. Shikata Y., Rios A., Kawkitinarong K., DePaola N., Garcia J.G., and Birukov K.G. 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 (2005) 40-49
14. Nonas S., Birukova A.A., Fu P., et al. Oxidized phospholipids reduce ventilator-induced vascular leak and inflammation in vivo. Crit Care 12 (2008) R27
15. Nonas S., Miller I., Kawkitinarong K., et al. Oxidized phospholipids reduce vascular leak and inflammation in rat model of acute lung injury. Am J Respir Crit Care Med 173 (2006) 1130-1138
16. Tasaka S., Koh H., Yamada W., et al. Attenuation of endotoxin-induced acute lung injury by the Rho-associated kinase inhibitor, Y-27632. Am J Respir Cell Mol Biol 32 (2005) 504-510
17. Howard L.S., and Morrell N.W. New therapeutic agents for pulmonary vascular disease. Paediatr Respir Rev 6 (2005) 285-291
18. Ueno Y., Koike H., Annoh S., and Nishio S. Anti-inflammatory effects of beraprost sodium, a stable analogue of PGI2, and its mechanisms. Prostaglandins 53 (1997) 279-289
19. Birukova A.A., Zagranichnaya T., Alekseeva E., et al. Prostaglandins PGE2 and PGI2 promote endothelial barrier enhancement via PKA- and Epac1/Rap1-dependent Rac activation. Exp Cell Res 313 (2007) 2504-2520
20. Fukuhara S., Sakurai A., Sano H., et al. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol 25 (2005) 136-146
21. Kooistra M.R., Corada M., Dejana E., and Bos J.L. Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett 579 (2005) 4966-4972
22. Birukova A.A., Fu P., Chatchavalvanich S., et al. Polar head groups are important for barrier protective effects of oxidized phospholipids on pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 292 (2007) L924-L935
23. Fu P., Birukova A.A., Xing J., et al. Amifostine reduces lung vascular permeability via suppression of inflammatory signalling. Eur Respir J 33 (2009) 612-624
24. Moitra J., Sammani S., and Garcia J.G. Re-evaluation of Evans Blue dye as a marker of albumin clearance in murine models of acute lung injury. Transl Res 150 (2007) 253-265
25. Birukov K.G., Jacobson J.R., Flores A.A., et al. Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol Lung Cell Mol Physiol 285 (2003) L785-L797
26. Tschumperlin D.J., Oswari J., and Margulies A.S. Deformation-induced injury of alveolar epithelial cells. Effect of frequency, duration, and amplitude. Am J Respir Crit Care Med 162 (2000) 357-362
27. Tschumperlin D.J., and Margulies S.S. Alveolar epithelial surface area-volume relationship in isolated rat lungs. J Appl Physiol 86 (1999) 2026-2033
28. Birukov K.G., Bochkov V.N., Birukova A.A., et al. Epoxycyclopentenone-containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res 95 (2004) 892-901
29. Birukova A.A., Cokic I., Moldobaeva N., and Birukov K.G. Paxillin is involved in the differential regulation of endothelial barrier by HGF and VEGF. Am J Respir Cell Mol Biol 40 (2008) 99-107
30. Birukova A.A., Rios A., and Birukov K.G. Long-term cyclic stretch controls pulmonary endothelial permeability at translational and post-translational levels. Exp Cell Res 314 (2008) 3466-3477
31. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 342 (2000) 1301-1308
32. Matthay M.A., Bhattacharya S., Gaver D., et al. Ventilator-induced lung injury: in vivo and in vitro mechanisms. Am J Physiol Lung Cell Mol Physiol 283 (2002) L678-L682
33. Matthay M.A., Robriquet L., and Fang X. Alveolar epithelium: role in lung fluid balance and acute lung injury. Proc Am Thorac Soc 2 (2005) 206-213
34. Nieuwenhuizen L., de Groot P.G., Grutters J.C., and Biesma D.H. A review of pulmonary coagulopathy in acute lung injury, acute respiratory distress syndrome and pneumonia. Eur J Haematol 82 (2009) 413-425
35. Malik A.B., and Horgan M.J. Mechanisms of thrombin-induced lung vascular injury and edema. Am Rev Respir Dis 136 (1987) 467-470
36. Mehta D., and Malik A.B. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86 (2006) 279-367
37. Garcia J.G., Verin A.D., and Schaphorst K.L. Regulation of thrombin-mediated endothelial cell contraction and permeability. Semin Thromb Hemost 22 (1996) 309-315
38. Verin A.D., Cooke C., Herenyiova M., Patterson C.E., and Garcia J.G. Role of Ca2+/calmodulin-dependent phosphatase 2B in thrombin-induced endothelial cell contractile responses. Am J Physiol 275 (1998) L788-L799
39. Essler M., Amano M., Kruse H.J., Kaibuchi K., Weber P.C., and Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem 273 (1998) 21867-21874
40. Matute-Bello G., Frevert C.W., and Martin T.R. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 295 (2008) L379-L399
41. Katsumi A., Orr A.W., Tzima E., and Schwartz M.A. Integrins in mechanotransduction. J Biol Chem 279 (2004) 12001-12004
42. Geiger B., and Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 13 (2001) 584-592
43. Finigan J.H., Boueiz A., Wilkinson E., et al. Activated protein C protects against ventilator-induced pulmonary capillary leak. Am J Physiol Lung Cell Mol Physiol 296 (2009) L1002-L1011
44. Birukov K.G. Small GTPases in mechanosensitive regulation of endothelial barrier. Microvasc Res 77 (2009) 46-52
45. Parker J.C. Inhibitors of myosin light chain kinase and phosphodiesterase reduce ventilator-induced lung injury. J Appl Physiol 89 (2000) 2241-2248
46. Dudek S.M., and Garcia J.G. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91 (2001) 1487-1500
47. Kawkitinarong K., Linz-McGillem L., Birukov K.G., and Garcia J.G. Differential regulation of human lung epithelial and endothelial barrier function by thrombin. Am J Respir Cell Mol Biol 31 (2004) 517-527
48. McAuley D.F., Frank J.A., Fang X., and Matthay M.A. Clinically relevant concentrations of beta2-adrenergic agonists stimulate maximal cyclic adenosine monophosphate-dependent airspace fluid clearance and decrease pulmonary edema in experimental acid-induced lung injury. Crit Care Med 32 (2004) 1470-1476
49. Perlman M.B., Lo S.K., and Malik A.B. Effect of prostacyclin on pulmonary vascular response to thrombin in awake sheep. J Appl Physiol 60 (1986) 546-553
50. Dembinski R., Brackhahn W., Henzler D., et al. Cardiopulmonary effects of iloprost in experimental acute lung injury. Eur Respir J 25 (2005) 81-87
51. Wittwer T., Franke U.F., Ochs M., et al. Inhalative pre-treatment of donor lungs using the aerosolized prostacyclin analog iloprost ameliorates reperfusion injury. J Heart Lung Transplant 24 (2005) 1673-1679
52. Hucklenbruch C., Hinder F., Berger C., et al. Effects of inhaled aerosolized iloprost and inhaled NO on pulmonary circulation and edema formation in ovine lung injury. Shock 30 (2008) 75-80
53. Mei F.C., Qiao J., Tsygankova O.M., Meinkoth J.L., Quilliam L.A., and Cheng X. Differential signaling of cyclic AMP: opposing effects of exchange protein directly activated by cyclic AMP and cAMP-dependent protein kinase on protein kinase B activation. J Biol Chem 277 (2002) 11497-11504
54. Cullere X., Shaw S.K., Andersson L., Hirahashi J., Luscinskas F.W., and Mayadas T.N. Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 105 (2005) 1950-1955
55. Birukova A.A., Zagranichnaya T., Alekseeva E., Bokoch G.M., and Birukov K.G. Epac/Rap and PKA are novel mechanisms of ANP-induced Rac-mediated pulmonary endothelial barrier protection. J Cell Physiol 215 (2008) 715-724
56. Bos J.L. Epac proteins: multi-purpose cAMP targets. Trends Biochem Sci 31 (2006) 680-686
57. Qiao J., Huang F., and Lum H. PKA inhibits RhoA activation: a protection mechanism against endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 284 (2003) L972-L980
58. Lampugnani M.G., Giorgi M., Gaboli M., Dejana E., and Marchisio P.C. Endothelial cell motility, integrin receptor clustering, and microfilament organization are inhibited by agents that increase intracellular cAMP. Lab Invest 63 (1990) 521-531
59. Wong K.W., Mohammadi S., and Isberg R.R. Disruption of RhoGDI and RhoA regulation by a Rac1 specificity switch mutant. J Biol Chem 281 (2006) 40379-40388
60. Herbrand U., and Ahmadian M.R. p190-RhoGAP as an integral component of the Tiam1/Rac1-induced downregulation of Rho. Biol Chem 387 (2006) 311-317