Absence of integrin ανβ3 enhances vascular leak in mice by inhibiting endothelial cortical actin formation

American Journal of Respiratory and Critical Care Medicine

Volumn 185, Issue 1, 2012, Pages 58-66

  Su, George ^a   Atakilit, Amha ^a   Li, John T ^a   Wu, Nanyan ^a   Bhattacharya, Mallar ^a   Zhu, Jieling ^a   Shieh, Jennifer E ^a   Li, Elizabeth ^a   Chen, Robert ^a   Sun, Stephen ^a   Su, Cynthia P ^a   Sheppard, Dean ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acute lung injury; Integrin; Sepsis; Vascular endothelium

Indexed keywords

ACTIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; RAC1 PROTEIN; SPHINGOSINE 1 PHOSPHATE; VITRONECTIN RECEPTOR;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM; EPIFLUORESCENCE MICROSCOPY; FEMALE; IMMUNOCYTOCHEMISTRY; LUNG EDEMA; MOUSE; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; RECEPTOR AFFINITY; RECEPTOR BLOCKING; RECEPTOR SENSITIVITY; VASCULAR DISEASE; VASCULAR LEAK;

ACTINS; ACUTE LUNG INJURY; ANIMALS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; FEMALE; INTEGRIN ALPHAVBETA3; LYSOPHOSPHOLIPIDS; MICE; MICE, KNOCKOUT; PULMONARY EDEMA; SEPSIS; SIGNAL TRANSDUCTION; SPHINGOSINE; VASCULAR DISEASES;

EID: 84855294125     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201108-1381OC     Document Type: Article

References (56)

1. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med 2005;353:1685-1693. (Pubitemid 41464707)
2. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003;348:1546-1554. (Pubitemid 36437931)
3. Rubenfeld GD. Epidemiology of acute lung injury. Crit Care Med 2003;31:S276-S284. (Pubitemid 36458180)
4. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-1349. (Pubitemid 30408719)
5. Deng X, Wang X, Andersson R. Endothelial barrier resistance in multiple organs after septic and nonseptic challenges in the rat. J Appl Physiol 1995;78:2052-2061.
6. Groeneveld AB. Vascular pharmacology of acute lung injury and acute respiratory distress syndrome. Vascul Pharmacol 2002;39:247-256. (Pubitemid 37490750)
7. Mura M, dos Santos CC, Stewart D, Liu M. Vascular endothelial growth factor and related molecules in acute lung injury. J Appl Physiol 2004;97:1605-1617. (Pubitemid 39425973)
8. Garcia JG, Davis HW, Patterson CE. Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol 1995;163:510-522.
9. Lum H, Malik AB. Regulation of vascular endothelial barrier function. Am J Physiol 1994;267:L223-L241.
10. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 2001;91:1487-1500. (Pubitemid 32900340)
11. Lampugnani MG, Resnati M, Dejana E, Marchisio PC. The role of integrins in the maintenance of endothelial monolayer integrity. J Cell Biol 1991;112:479-490. (Pubitemid 21926002)
12. Eliceiri BP, Puente XS, Hood JD, Stupack DG, Schlaepfer DD, Huang XZ, Sheppard D, Cheresh DA. Src-mediated coupling of focal adhesion kinase to integrin alpha(v)beta5 in vascular endothelial growth factor signaling. J Cell Biol 2002;157:149-160.
13. Su G, Hodnett M, Wu N, Atakilit A, Kosinski C, Godzich M, Huang XZ, Kim JK, Frank JA, Matthay MA, et al. Integrin alphavbeta5 regulates lung vascular permeability and pulmonary endothelial barrier function. Am J Respir Cell Mol Biol 2007;36:377-386. (Pubitemid 46365289)
14. Luscinskas FW, Lawler J. Integrins as dynamic regulators of vascular function. FASEB J 1994;8:929-938. (Pubitemid 24286856)
15. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992;69:11-25.
16. Qiao RL, Yan W, Lum H, Malik AB. Arg-Gly-Asp peptide increases endothelial hydraulic conductivity: comparison with thrombin response. Am J Physiol 1995;269:C110-C117.
17. Wu MH, Ustinova E, Granger HJ. Integrin binding to fibronectin and vitronectin maintains the barrier function of isolated porcine coronary venules. J Physiol 2001;532:785-791. (Pubitemid 32427891)
18. Robinson SD, Reynolds LE, Wyder L, Hicklin DJ, Hodivala-Dilke KM. Beta3-integrin regulates vascular endothelial growth factor-A-dependent permeability. Arterioscler Thromb Vasc Biol 2004;24:2108-2114. (Pubitemid 39482438)
19. Reynolds AR, Reynolds LE, Nagel TE, Lively JC, Robinson SD, Hicklin DJ, Bodary SC, Hodivala-Dilke KM. Elevated Flk1 (vascular endothelial growth factor receptor 2) signaling mediates enhanced angiogenesis in beta3-integrin-deficient mice. Cancer Res 2004;64:8643-8650. (Pubitemid 39552078)
20. 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. (Pubitemid 38725337)
21. 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. (Pubitemid 32906197)
22. 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. (Pubitemid 39425695)
23. Peng X, Hassoun PM, Sammani S, McVerry BJ, Burne MJ, Rabb H, Pearse D, Tuder RM, Garcia JG. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med 2004;169:1245-1251. (Pubitemid 38680403)
24. Lee MJ, Van Brocklyn JR, Thangada S, Liu CH, Hand AR, Menzeleev R, Spiegel S, Hla T. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 1998;279:1552-1555. (Pubitemid 28217081)
25. Paik JH, Chae S, Lee MJ, Thangada S, Hla T. Sphingosine 1-phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alpha vbeta3- and beta1-containing integrins. J Biol Chem 2001;276:11830-11837.
26. Baluk P, Thurston G, Murphy TJ, Bunnett NW, McDonald DM. Neurogenic plasma leakage in mouse airways. Br J Pharmacol 1999;126:522-528. (Pubitemid 29057605)
27. Rittirsch D, Huber-Lang MS, Flierl MA, Ward PA. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc 2009;4:31-36.
28. Rojas M, Woods CR, Mora AL, Xu J, Brigham KL. Endotoxin-induced lung injury in mice: structural, functional, and biochemical responses. Am J Physiol Lung Cell Mol Physiol 2005;288:L333-L341. (Pubitemid 40105372)
29. Sepp NT, Li LJ, Lee KH, Brown EJ, Caughman SW, Lawley TJ, Swerlick RA. Basic fibroblast growth factor increases expression of the alpha v beta 3 integrin complex on human microvascular endothelial cells. J Invest Dermatol 1994;103:295-299. (Pubitemid 24329746)
30. Max R, Gerritsen RR, Nooijen PT, Goodman SL, Sutter A, Keilholz U, Ruiter DJ, De Waal RM. Immunohistochemical analysis of integrin alpha vbeta3 expression on tumor-associated vessels of human carcinomas. Int J Cancer 1997;71:320-324. (Pubitemid 27224290)
31. Singh B, Fu C, Bhattacharya J. Vascular expression of the alpha(v)beta (3)-integrin in lung and other organs. Am J Physiol Lung Cell Mol Physiol 2000;278:L217-L226. (Pubitemid 30104194)
32. Savill J, Dransfield I, Hogg N, Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 1990;343:170-173.
33. Jaganathan BG, Ruester B, Dressel L, Stein S, Grez M, Seifried E, Henschler R. Rho inhibition induces migration of mesenchymal stromal cells. Stem Cells 2007;25:1966-1974. (Pubitemid 47258174)
34. Garcia JG, Siflinger-Birnboim A, Bizios R, Del Vecchio PJ, Fenton JW II, Malik AB. Thrombin-induced increase in albumin permeability across the endothelium. J Cell Physiol 1986;128:96-104. (Pubitemid 16099466)
35. 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. (Pubitemid 30655976)
36. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999;4:915-924. (Pubitemid 30054898)
37. Clements RT, Minnear FL, Singer HA, Keller RS, Vincent PA. RhoA and Rho-kinase dependent and independent signals mediate TGF-beta-induced pulmonary endothelial cytoskeletal reorganization and permeability. Am J Physiol Lung Cell Mol Physiol 2005;288:L294-L306. (Pubitemid 40105368)
38. Camerer E, Regard JB, Cornelissen I, Srinivasan Y, Duong DN, Palmer D, Pham TH, Wong JS, Pappu R, Coughlin SR. Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. J Clin Invest 2009;119:1871-1879.
39. Tauseef M, Kini V, Knezevic N, Brannan M, Ramchandaran R, Fyrst H, Saba J, Vogel SM, Malik AB, Mehta D. Activation of sphingosine kinase-1 reverses the increase in lung vascular permeability through sphingosine-1-phosphate receptor signaling in endothelial cells. Circ Res 2008;103:1164-1172.
40. Singleton PA, Dudek SM, Chiang ET, Garcia JG. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB J 2005;19:1646-1656. (Pubitemid 41429522)
41. Shikata Y, Birukov KG, Birukova AA, Verin A, Garcia JG. Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J 2003;17:2240-2249. (Pubitemid 37509580)
42. Garcia JG, Verin AD, Schaphorst K, Siddiqui R, Patterson CE, Csortos C, Natarajan V. Regulation of endothelial cell myosin light chain kinase by Rho, cortactin, and p60(src). Am J Physiol 1999;276:L989-L998. (Pubitemid 29321177)
43. Humphries JD, Wang P, Streuli C, Geiger B, Humphries MJ, Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J Cell Biol 2007;179:1043-1057. (Pubitemid 350223497)
44. Liu F, Verin AD, Wang P, Day R, Wersto RP, Chrest FJ, English DK, Garcia JG. Differential regulation of sphingosine-1-phosphate- and VEGF-induced endothelial cell chemotaxis. Involvement of G(ialpha2)-linked Rho kinase activity. Am J Respir Cell Mol Biol 2001;24:711-719. (Pubitemid 32550593)
45. Watanabe S, Mukaida N, Ikeda N, Akiyama M, Harada A, Nakanishi I, Nariuchi H, Watanabe Y, Matsushima K. Prevention of endotoxin shock by an antibody against leukocyte integrin beta 2 through inhibiting production and action of TNF. Int Immunol 1995;7:1037-1046.
46. Price LS, Leng J, Schwartz MA, Bokoch GM. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell 1998;9:1863-1871. (Pubitemid 28337528)
47. del Pozo MA, Price LS, Alderson NB, Ren XD, Schwartz MA. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J 2000;19:2008-2014. (Pubitemid 30237576)
48. Del Pozo MA, Kiosses WB, Alderson NB, Meller N, Hahn KM, Schwartz MA. Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat Cell Biol 2002;4:232-239. (Pubitemid 34218197)
49. Stupack DG, Cheresh DA. ECM remodeling regulates angiogenesis: endothelial integrins look for new ligands. Sci STKE 2002;2002:PE7.
50. Ziegler WH, Liddington RC, Critchley DR. The structure and regulation of vinculin. Trends Cell Biol 2006;16:453-460. (Pubitemid 44293400)
51. Gingras AR, Vogel KP, Steinhoff HJ, Ziegler WH, Patel B, Emsley J, Critchley DR, Roberts GC, Barsukov IL. Structural and dynamic characterization of a vinculin binding site in the talin rod. Biochemistry 2006;45:1805-1817. (Pubitemid 43222124)
52. Papagrigoriou E, Gingras AR, Barsukov IL, Bate N, Fillingham IJ, Patel B, Frank R, Ziegler WH, Roberts GC, Critchley DR, et al. Activation of a vinculin-binding site in the talin rod involves rearrangement of a five-helix bundle. EMBO J 2004;23:2942-2951. (Pubitemid 39093589)
53. Gingras AR, Ziegler WH, Bobkov AA, Joyce MG, Fasci D, Himmel M, Rothemund S, Ritter A, Grossmann JG, Patel B, et al. Structural determinants of integrin binding to the talin rod. J Biol Chem 2009;284:8866-8876.
54. Hodivala-Dilke KM, McHugh KP, Tsakiris DA, Rayburn H, Crowley D, Ullman-Cullere M, Ross FP, Coller BS, Teitelbaum S, Hynes RO. Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 1999;103:229-238. (Pubitemid 29053141)
55. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, Huang X, Sheppard D, Hynes RO, Hodivala-Dilke KM. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat Med 2002;8:27-34. (Pubitemid 34101725)
56. Weis SM, Lindquist JN, Barnes LA, Lutu-Fuga KM, Cui J, Wood MR, Cheresh DA. Cooperation between VEGF and beta3 integrin during cardiac vascular development. Blood 2007;109:1962-1970. (Pubitemid 46348193)