Differential regulation of pulmonary endothelial monolayer integrity by varying degrees of cyclic stretch

American Journal of Pathology

Volumn 168, Issue 5, 2006, Pages 1749-1761

  Birukova, Anna A ^a   Chatchavalvanich, Santipongse ^a   Rios, Alexander ^a   Kawkitinarong, Kamon ^a   Garcia, Joe G N ^a   Birukov, Konstantin G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; RAC PROTEIN; RHO FACTOR; SMALL INTERFERING RNA;

ARTICLE; ARTIFICIAL VENTILATION; CELL CULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LUNG ARTERY; LUNG ENDOTHELIUM; LUNG INJURY; MONOLAYER CULTURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VENTILATOR INDUCED LUNG INJURY; WESTERN BLOTTING;

EID: 33646525704     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.050431     Document Type: Article

References (58)

1. Dos Santos CC, Slutsky AS: Invited review: mechanisms of ventilator-induced lung injury: a perspective. J Appl Physiol 2000, 89:1645-1655
2. Uhlig S: Ventilation-induced lung injury and mechanotransduction: stretching it too far? Am J Physiol 2002, 282:L892-L896
3. Narimanbekov IO, Rozycki HJ: Effect of IL-1 blockade on inflammatory manifestations of acute ventilator-induced lung injury in a rabbit model. Exp Lung Res 1995, 21:239-254
4. Pugin J, Dunn I, Jolliet P, Tassaux D, Magnenat JL, Nicod LP, Chevrolet JC: Activation of human macrophages by mechanical ventilation in vitro. Am J Physiol 1998, 275:L1040-L1050
5. Vlahakis NE, Schroeder MA, Limper AH, Hubmayr RD: Stretch induces cytokine release by alveolar epithelial cells in vitro. Am J Physiol 1999, 277:L167-L173
6. Matthay MA, Zimmerman GA, Esmon C, Bhattacharya J, Coller B, Doerschuk CM, Floros J, Gimbrone Jr MA, Hoffman E, Hubmayr RD, Leppert M, Matalon S, Munford R, Parsons P, Slutsky AS, Tracey KJ, Ward P, Gail DB, Harabin AL: Future research directions in acute lung injury: summary of a National Heart, Lung, and Blood Institute working group. Am J Respir Crit Care Med 2003, 167:1027-1035
7. Ingber DE: Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 1997, 59:575-599
8. Dudek SM, Garcia JG: Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 2001, 91:1487-1500
9. Garcia JG, Verin AD, Schaphorst KL: Regulation of thrombin-mediated endothelial cell contraction and permeability. Semin Thromb Hemost 1996, 22:309-315
10. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D: Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 2001, 108:689-701
11. Verin AD, Birukova A, Wang P, Liu F, Becker P, Birukov K, Garcia JG: Microtubule disassembly increases endothelial cell barrier dysfunction: role of MLC phosphorylation. Am J Physiol 2001, 281:L565-L574
12. Liu F, Schaphorst KL, Verin AD, Jacobs K, Birukova A, Day RM, Bogatcheva N, Bottaro DP, Garcia JG: Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. FASEB J 2002, 16:950-962
13. Shikata Y, Birukov KG, Garcia JG: S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK and paxillin. J Appl Physiol 2003, 94:1193-1203
14. Birukova AA, Smurova K, Birukov KG, Kaibuchi K, Garcia JGN, Verin AD: Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 2004, 67:64-77
15. van Nieuw Amerongen GP, Draijer R, Vermeer MA, van Hinsbergh VW: Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circ Res 1998, 83:1115-1123
16. Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ: Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 2001, 114:1343-1355
17. Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, Matsuura Y, Kaibuchi K: Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 1997, 275:1308-1311
18. Birukov KG, Bochkov VN, Birukova AA, Kawkitinarong K, Rios A, Leitner A, Verin AD, Bokoch GM, Leitinger N, Garcia JG: Epoxycyclopentenone-containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res 2004, 95:892-901
19. Birukov KG, Jacobson JR, Flores AA, Ye SQ, Birukova AA, Verin AD, Garcia JG: Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol 2003, 285:L785-L797
20. Shikata Y, Rios A, Kawkitinarong K, DePaola N, Garcia JG, Birukov KG: 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 2005, 304:40-49
21. Tzima E, del Pozo MA, Shattil SJ, Chien S, Schwartz MA: Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J 2001, 20:4639-4647
22. Katsumi A, Milanini J, Kiosses WB, del Pozo MA, Kaunas R, Chien S, Hahn KM, Schwartz MA: Effects of cell tension on the small GTPase Rac. J Cell Biol 2002, 158:153-164
23. Tzima E, Del Pozo MA, Kiosses WB, Mohamed SA, Li S, Chien S, Schwartz MA: Activation of Rad by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J 2002, 21:6791-6800
24. Birukova AA, Birukov KG, Smurova K, Adyshev DM, Kaibuchi K, Alieva I, Garcia JG, Verin AD: Novel role of microtubules in thrombin-induced endothelial barrier dysfunction. FASEB J 2004, 18:1879-1890
25. Birukova AA, Smurova K, Birukov KG, Usatyuk P, Liu F, Kaibuchi K, Ricks-Cord A, Natarajan V, Alieva I, Garcia JG, Verin AD: Microtubule disassembly induces cytoskeletal remodeling and lung vascular barrier dysfunction: role of Rho-dependent mechanisms. J Cell Physiol 2004, 201:55-70
26. Birukov KG, Leitinger N, Bochkov VN, Garcia JG: Signal transduction pathways activated in human pulmonary endothelial cells by Ox-PAPC, a bioactive component of oxidized lipoproteins. Microvasc Res 2004, 67:18-28
27. Shikata Y, Birukov KG, Birukova AA, Verin AD, Garcia JG: Involvement of site-specific FAK phosphorytation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J 2003, 17:2240-2249
28. Geng WD, Boskovic G, Fultz ME, Li C, Niles RM, Ohno S, Wright GL: Regulation of expression and activity of four PKC isozymes in confluent and mechanically stimulated UMR-108 osteoblastic cells. J Cell Physiol 2001, 189:216-228
29. Naruse K, Yamada T, Sai XR, Hamaguchi M, Sokabe M: Pp125FAK is required for stretch dependent morphological response of endothelial cells. Oncogene 1998, 17:455-463
30. Panetti TS: Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells. Biochim Biophys Acta 2002, 1582:190-196
31. Dudek SM, Jacobson JR, Chiang ET, Birukov KG, Wang P, Zhan X, Garcia JG: Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cortactin and myosin light chain kinase. J Biol Chem 2004, 279:24692-24700
32. Endo A, Nagashima K, Kurose H, Mochizuki S, Matsuda M, Mochizuki N: Sphingosine 1-phosphate induces membrane ruffling and increases motility of human umbilical vein endothelial cells via vascular endothelial growth factor receptor and CrkII. J Biol Chem 2002, 277:23747-23754
33. Birukov KG, Birukova AA, Dudek SM, Verin AD, Crow MT, Zhan X, DePaola N, Garcia JG: Shear stress-mediated cytoskeletal remodeling and cortactin translocation in pulmonary endothelial cells. Am J Respir Cell Mol Biol 2002, 26:453-464
34. Gao Y, Dickerson JB, Quo F, Zheng J, Zheng Y: Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 2004, 101:7618-7623
35. Tschumperlin DJ, Margulies SS: Alveolar epithelial surface area-volume relationship in isolated rat lungs. J Appl Physiol 1999, 86:2026-2033
36. Tschumperlin DJ, Margulies SS: Equibiaxial deformation-induced injury of alveolar epithelial cells in vitro. Am J Physiol 1998, 275:L1173-L1183
37. Tschumperlin DJ, Oswari J, Margulies AS: Deformation-induced injury of alveolar epithelial cells. Effect of frequency, duration, and amplitude. Am J Respir Crit Care Med 2000, 162:357-362
38. Vlahakis NE, Hubmayr RD: Invited review: plasma membrane stress failure in alveolar epithelial cells. J Appl Physiol 2000, 89:2490-2497
39. Matthay MA, Bhattacharya S, Gaver D, Ware LB, Lim LH, Syrkina O, Eyal F, Hubmayr R: Ventilator-induced lung injury: in vivo and in vitro mechanisms. Am J Physiol 2002, 283:L678-L682
40. Pugin J: Molecular mechanisms of lung cell activation induced by cyclic stretch. Crit Care Med 2003, 31:S200-S206
41. Ricard JD, Dreyfuss D, Saumon G: Ventilator-induced lung injury. Eur Respir J Suppl 2003, 42:2s-9s
42. McVerry BJ, Peng X, Hassoun PM, Sammani S, Simon BA, Garcia JG: Sphingosine 1-phosphate reduces vascular leak in murine and canine models of acute lung injury. Am J Respir Crit Care Med 2004, 170:987-993
43. Manser E, Loo TH, Koh CG, Zhao ZS, Chen XQ, Tan L, Tan I, Leung T, Lim L: PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol Cell 1998, 1:183-192
44. Hall A: Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514
45. Kouklis P, Konstantouiaki M, Vogel S, Broman M, Malik AB: Cdc42 regulates the restoration of endothelial barrier function. Circ Res 2004, 94:159-166
46. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW: Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res 2000, 87:335-340
47. Bishop AL, Hall A: Rho GTPases and their effector proteins. Biochem J 2000, 348:241-255
48. Bokoch GM: Biology of the p21-activated kinases. Annu Rev Biochem 2003, 72:743-781
49. Manser E: Small GTPases take the stage. Dev Cell 2002, 3:323-328
50. Turner CE, West KA, Brown MC: Paxillin-ARF GAP signaling and the cytoskeleton. Curr Opin Cell Biol 2001, 13:593-599
51. Uruno T, Liu J, Zhang P, Fan Y, Egile C, Li R, Mueller SC, Zhan X: Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 2001, 3:259-266
52. Pyne S, Pyne NJ: Sphingosine 1-phosphate signalling in mammalian cells. Biochem J 2000, 349:385-402
53. West KA, Zhang H, Brown MC, Nikolopoulos SN, Riedy MC, Horwitz AF, Turner CE: The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL). J Cell Biol 2001, 154:161-176
54. Zhao ZS, Manser E, Loo TH, Lim L: Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol 2000, 20:6354-6363
55. Brown MC, West KA, Turner CE: Paxillin-dependent paxillin kinase linker and p21-activated kinase localization to focal adhesions involves a multistep activation pathway. Mol Biol Cell 2002, 13:1550-1565
56. Manevich Y, Al-Mehdi A, Muzykantov V, Fisher AB: Oxidative burst and NO generation as initial response to ischemia in flow-adapted endothelial cells. Am J Physiol 2001, 280:H2126-H2135
57. Matsuzaki I, Chatterjee S, Debolt K, Manevich Y, Zhang Q, Fisher AB: Membrane depolarization and NADPH oxidase activation in aortic endothelium during ischemia reflect altered mechanotransduction. Am J Physiol 2005, 288:H336-H343
58. Zheng Y: Dbl family guanine nucleotide exchange factors. Trends Biochem Sci 2001, 26:724-732