Cigarette smoke causes lung vascular barrier dysfunction via oxidative stress-mediated inhibition of RhoA and focal adhesion kinase

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 301, Issue 6, 2011, Pages

  Lu, Qing ^a   Sakhatskyy, Pavlo ^a   Grinnell, Katie ^a   Ortiz, Julie Newton Melanie ^a   Wang, Yulian ^a   Sanchez Esteban, Juan ^a   Harrington, Elizabeth O ^a   Rounds, Sharon ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Acute lung injury; Adherens junctions; Endothelial permeability; Focal adhesion complexes; Lung edema

Indexed keywords

ACETYLCYSTEINE; CIGARETTE SMOKE; F ACTIN; FOCAL ADHESION KINASE; LIPOPOLYSACCHARIDE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL CULTURE; CELL JUNCTION; COW; DISEASE EXACERBATION; ENZYME ACTIVATION; ENZYME INHIBITION; FOCAL ADHESION; LUNG ALVEOLUS CELL; LUNG EDEMA; LUNG ENDOTHELIUM; LUNG FUNCTION; LUNG VASCULAR BARRIER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACETYLCYSTEINE; ACTINS; ADHERENS JUNCTIONS; ANIMALS; ANTIOXIDANTS; CATTLE; CELL LINE; ELECTRIC IMPEDANCE; ENZYME ACTIVATION; EPITHELIAL CELLS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; LIPOPOLYSACCHARIDES; LUNG; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PERMEABILITY; PRIMARY CELL CULTURE; PULMONARY EDEMA; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SMOKE; SMOKING; TOBACCO;

EID: 82855181152     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00178.2011     Document Type: Article

References (67)

1. Aghajanian A, Wittchen ES, Campbell SL, Burridge K. Direct activation of RhoA by reactive oxygen species requires a redox-sensitive motif.PLoS One 4: e8045, 2009.
2. Bazin M, Turcotte H, Lagace R, Boutet M. Cardiovascular effects of cigarette smoke in the rat. Aortic endothelial and myocardial capillary permeability in the rat. Rev Can Biol 40: 263-276, 1981.
3. Bernhard D, Csordas A, Henderson B, Rossmann A, Kind M, Wick G.Cigarette smoke metal-catalyzed protein oxidation leads to vascular endothelial cell contraction by depolymerization of microtubules. FASEB J 19: 1096-1107, 2005.
4. Bhavsar TM, Cerreta JM, Cantor JO. Short-term cigarette smoke exposure predisposes the lung to secondary injury. Lung 185: 227-233,2007.
5. Braga VM, Machesky LM, Hall A, Hotchin NA. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J Cell Biol 137: 1421-1431, 1997.
6. Burns AR, Hosford SP, Dunn LA, Walker DC, Hogg JC. Respiratory epithelial permeability after cigarette smoke exposure in guinea pigs. J Appl Physiol 66: 2109-2116, 1989.
7. Cai J, Niu X, Chen Y, Hu Q, Shi G, Wu H, Wang J, Yi J. Emodininduced generation of reactive oxygen species inhibits RhoA activation to sensitize gastric carcinoma cells to anoikis. Neoplasia 10: 41-51, 2008.
8. Calfee CS, Matthay MA, Eisner MD, Benowitz N, Call M, Pittet JF, Cohen MJ. Active and passive cigarette smoking and acute lung injury following severe blunt trauma. Am J Respir Crit Care Med 183: 1660-1665, 2011.
9. Conklin DJ, Haberzettl P, Prough RA, Bhatnagar A. Glutathione-Stransferase P protects against endothelial dysfunction induced by exposure to tobacco smoke. Am J Physiol Heart Circ Physiol 296: H1586-H1597, 2009.
10. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91: 1487-1500, 2001.
11. Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, Dragotto A, Gigli PM, Catinella S, Civelli M, Patacchini R. Alpha,betaunsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am J Respir Cell Mol Biol 37: 617-623, 2007.
12. Ferrer E, Peinado VI, Castaneda J, Prieto-Lloret J, Olea E, Gonzalez- Martin MC, Vega-Agapito MV, Diez M, Dominguez-Fandos D, Obeso A, Gonzalez C, Barbera JA. Effects of cigarette smoke and hypoxia on the pulmonary circulation in the guinea pig. Eur Respir J 38: 617-627,2011.
13. Ferro TN, Goslar PW, Romanovsky AA, Petersen SR. Smoking in trauma patients: the effects on the incidence of sepsis, respiratory failure, organ failure, and mortality. J Trauma 69: 308-312, 2010.
14. Fordjour AK, Harrington EO. PKCdelta influences p190 phosphorylation and activity: events independent of PKCdelta-mediated regulation of endothelial cell stress fiber and focal adhesion formation and barrier function. Biochim Biophys Acta 1790: 1179-1190, 2009.
15. Fu P, Birukova AA, Xing J, Sammani S, Murley JS, Garcia JG, Grdina DJ, Birukov KG. Amifostine reduces lung vascular permeability via suppression of inflammatory signalling. Eur Respir J 33: 612-624,2009.
16. Gajic O, Dabbagh O, Park PK, Adesanya A, Chang SY, Hou P, Anderson H 3rd, Hoth JJ, Mikkelsen ME, Gentile NT, Gong MN, Talmor D, Bajwa E, Watkins TR, Festic E, Yilmaz M, Iscimen R, Kaufman DA, Esper AM, Sadikot R, Douglas I, Sevransky J. Early identification of patients at risk of acute lung injury: evaluation of lung injury prediction score in a multicenter cohort study. Am J Respir Crit Care Med 183: 462-470, 2011.
17. Grinnell KL, Harrington EO. Interplay between FAK, PKCdelta, and p190RhoGAP in the regulation of endothelial barrier function. Microvasc Res April 22 [Epub ahead of print], 2011.
18. Guo M, Wu MH, Granger HJ, Yuan SY. Focal adhesion kinase in neutrophil-induced microvascular hyperpermeability. Microcirculation 12: 223-232, 2005.
19. Harrington EO, Shannon CJ, Morin N, Rowlett H, Murphy C, Lu Q. PKCdelta regulates endothelial basal barrier function through modulation of RhoA GTPase activity. Exp Cell Res 308: 407-421, 2005.
20. Heffner JE, Sahn SA. Salicylate-induced pulmonary edema. Clinical features and prognosis. Ann Intern Med 95: 405-409, 1981.
21. Henderson B, Csordas A, Backovic A, Kind M, Bernhard D, Wick G. Cigarette smoke is an endothelial stressor and leads to cell cycle arrest. Atherosclerosis 201: 298-305, 2008.
22. Heo J, Raines KW, Mocanu V, Campbell SL. Redox regulation of RhoA. Biochemistry 45: 14481-14489, 2006.
23. Holden WE, Maier JM, Malinow MR. Cigarette smoke extract increases albumin flux across pulmonary endothelium in vitro. J Appl Physiol 66:443-449, 1989.
24. Holinstat M, Knezevic N, Broman M, Samarel AM, Malik AB, Mehta D. Suppression of RhoA activity by focal adhesion kinase-induced activation of p190RhoGAP: role in regulation of endothelial permeability. J Biol Chem 281: 2296-2305, 2006.
25. Iizuka T, Ishii Y, Itoh K, Kiwamoto T, Kimura T, Matsuno Y, Morishima Y, Yamamoto M, Sekizawa K. Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema. Genes Cells 10: 1113-1125, 2005.
26. Iribarren C, Jacobs DR Jr, Sidney S, Gross MD, Eisner MD. Cigarette smoking, alcohol consumption, and risk of ARDS: a 15-year cohort study in a managed care setting. Chest 117: 163-168, 2000.
27. Knezevic N, Tauseef M, Thennes T, Mehta D. The G protein betagamma subunit mediates reannealing of adherens junctions to reverse endothelial permeability increase by thrombin. J Exp Med 206: 2761-2777, 2009.
28. Kosecik M, Erel O, Sevinc E, Selek S. Increased oxidative stress in children exposed to passive smoking. Int J Cardiol 100: 61-64, 2005.
29. Li R, Zhang B, Zheng Y. Structural determinants required for the interaction between Rho GTPase and the GTPase-activating domain of p190. J Biol Chem 272: 32830-32835, 1997.
30. Lim ST, Mikolon D, Stupack DG, Schlaepfer DD. FERM control of FAK function: implications for cancer therapy. Cell Cycle 7: 2306-2314,2008.
31. Lu Q, Harrington EO, Hai CM, Newton J, Garber M, Hirase T, Rounds S. Isoprenylcysteine carboxyl methyltransferase (ICMT) modulates endothelial monolayer permeability: involvement of RhoA carboxyl methylation. Circ Res 94: 306-315, 2004.
32. Lu Q, Harrington EO, Jackson H, Morin N, Shannon C, Rounds S. Transforming growth factor-beta1-induced endothelial barrier dysfunction involves Smad2-dependent p38 activation and subsequent RhoA activation.J Appl Physiol 101: 375-384, 2006.
33. Lu Q, Harrington EO, Newton J, Casserly B, Radin G, Warburton R, Zhou Y, Blackburn MR, Rounds S. Adenosine protected against pulmonary edema through transporter- and receptor A2-mediated endothelial barrier enhancement. Am J Physiol Lung Cell Mol Physiol 298: L755-L767, 2010.
34. Lu Q, Rounds S. Focal adhesion kinase and endothelial cell apoptosis. Microvasc Res May 19 [Epub ahead of print], 2011.
35. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction.Am J Physiol Cell Physiol 280: C719-C741, 2001.
36. MacNee W. Pulmonary and systemic oxidant/antioxidant imbalance in chronic obstructive pulmonary disease. Proc Am Thorac Soc 2: 50-60,2005.
37. Nimnual AS, Taylor LJ, Bar-Sagi D. Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5: 236-241, 2003.
38. Orosz Z, Csiszar A, Labinskyy N, Smith K, Kaminski PM, Ferdinandy P, Wolin MS, Rivera A, Ungvari Z. Cigarette smoke-induced proinflammatory alterations in the endothelial phenotype: role of NAD(P)H oxidase activation. Am J Physiol Heart Circ Physiol 292: H130-H139, 2007.
39. Ozaki K, Hori T, Ishibashi T, Nishio M, Aizawa Y. Effects of chronic cigarette smoking on endothelial function in young men. J Cardiol 56:307-313, 2010.
40. Peinado VI, Pizarro S, Barbera JA. Pulmonary vascular involvement in COPD. Chest 134: 808-814, 2008.
41. Pierrou S, Broberg P, O'Donnell RA, Pawlowski K, Virtala R, Lindqvist E, Richter A, Wilson SJ, Angco G, Moller S, Bergstrand H, Koopmann W, Wieslander E, Stromstedt PE, Holgate ST, Davies DE, Lund J, Djukanovic R. Expression of genes involved in oxidative stress responses in airway epithelial cells of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 175: 577-586, 2007.
42. Podowski M, Calvi CL, Cheadle C, Tuder RM, Biswals S, Neptune ER. Complex integration of matrix, oxidative stress, and apoptosis in genetic emphysema. Am J Pathol 175: 84-96, 2009.
43. Presson RG Jr, Brown MB, Fisher AJ, Sandoval RM, Dunn KW,Lorenz KS, Delp EJ, Salama P, Molitoris BA, Petrache I. Two-photon imaging within the murine thorax without respiratory and cardiac motion artifact. Am J Pathol 179: 75-82, 2011.
44. Qamar W, Sultana S. Polyphenols from Juglans regia L. (Walnut) kernel modulate cigarette smoke extract induced acute inflammation, oxidative stress and lung injury in Wistar rats. Hum Exp Toxicol 2010.
45. Quadri SK, Bhattacharya J. Resealing of endothelial junctions by focal adhesion kinase. Am J Physiol Lung Cell Mol Physiol 292: L334-L342,2007.
46. Rahman I, Kilty I. Antioxidant therapeutic targets in COPD. Curr Drug Targets 7: 707-720, 2006.
47. Rangasamy T, Misra V, Zhen L, Tankersley CG, Tuder RM, Biswal S. Cigarette smoke-induced emphysema in A/J mice is associated with pulmonary oxidative stress, apoptosis of lung cells, and global alterations in gene expression. Am J Physiol Lung Cell Mol Physiol 296: L888-L900,2009.
48. Richens TR, Linderman DJ, Horstmann SA, Lambert C, Xiao YQ, Keith RL, Boe DM, Morimoto K, Bowler RP, Day BJ, Janssen WJ, Henson PM, Vandivier RW. Cigarette smoke impairs clearance of apoptotic cells through oxidant-dependent activation of RhoA. Am J Respir Crit Care Med 179: 1011-1021, 2009.
49. Sanchez-Esteban J, Wang Y, Filardo EJ, Rubin LP, Ingber DE. Integrins beta1, alpha6, and alpha3 contribute to mechanical strain-induced differentiation of fetal lung type II epithelial cells via distinct mechanisms. Am J Physiol Lung Cell Mol Physiol 290: L343-L350, 2006.
50. Schaller MD. Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123: 1007-1013, 2010.
51. Schlegel N, Baumer Y, Drenckhahn D, Waschke J. Lipopolysaccharide-induced endothelial barrier breakdown is cyclic adenosine monophosphate dependent in vivo and in vitro. Crit Care Med 37: 1735-1743, 2009.
52. Schweitzer KS, Hatoum H, Brown MB, Gupta M, Justice MJ, Beteck B, Van Demark MJ, Gu Y, Presson RG Jr, Hubbard WC, Petrache I. Mechanisms of lung endothelial barrier disruption induced by cigarette smoke: role of oxidative stress and ceramides. Am J Physiol Lung Cell Mol Physiol. First published August 26, 2011; doi:10.1152/ajplung.00385.2010.
53. Sin DD, Anthonisen NR, Soriano JB, Agusti AG. Mortality in COPD: role of comorbidities. Eur Respir J 28: 1245-1257, 2006.
54. Siu ER, Wong EW, Mruk DD, Porto CS, Cheng CY. Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 106:9298-9303, 2009.
55. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev 81: 153-208, 2001.
56. Talukder MAH, Johnson WM, Varadharaj S, Lian J, Kearns PN, El-Mahdy MA, Liu X, Zweier JL. Chronic cigarette smoking causes hypertension, increased oxidative stress, impaired NO bioavailability,endothelial dysfunction, and cardiac remodeling in mice. Am J Physiol Heart Circ Physiol 300: H388-H396, 2011.
57. Taraseviciene-Stewart L, Voelkel NF. Molecular pathogenesis of emphysema. J Clin Invest 118: 394-402, 2008.
58. Tzima E. Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ Res 98: 176-185, 2006.
59. Usatyuk PV, Parinandi NL, Natarajan V. Redox regulation of 4-hydroxy-2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. J Biol Chem 281: 35554-35566, 2006.
60. Van Der Vaart H, Postma DS, Timens W, ten Hacken NHT. Acute effects of cigarette smoke on inflammation and oxidative stress: a review. Thorax 59: 713-721, 2004.
61. Witten ML, Lemen RJ, Quan SF, Sobonya RE, Magarelli JL, Bruck DC. Acute cigarette smoke exposure causes lung injury in rabbits treated with ibuprofen. Exp Lung Res 13: 113-126, 1987.
62. Wright JL, Churg A. Short-term exposure to cigarette smoke induces endothelial dysfunction in small intrapulmonary arteries: analysis using guinea pig precision cut lung slices. J Appl Physiol 104: 1462-1469, 2008.
63. Wu MH. Endothelial focal adhesions and barrier function. J Physiol 569:359-366, 2005.
64. Yanbaeva DG, Dentener MA, Creutzberg EC, Wesseling G, Wouters EFM. Systemic effects of smoking. Chest 131: 1557-1566, 2007.
65. Yao H, Rahman I. Current concepts on oxidative/carbonyl stress, inflammation and epigenetics in pathogenesis of chronic obstructive pulmonary disease. Toxicol Appl Pharmacol 254: 72-85, 2011.
66. Yoshida T, Mett I, Bhunia AK, Bowman J, Perez M, Zhang L, Gandjeva A, Zhen L, Chukwueke U, Mao T, Richter A, Brown E, Ashush H, Notkin N, Gelfand A, Thimmulappa RK, Rangasamy T, Sussan T, Cosgrove G, Mouded M, Shapiro SD, Petrache I, Biswal S, Feinstein E, Tuder RM. Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat Med 16: 767-773, 2011.
67. Zhao X, Peng X, Sun S, Park AY, Guan JL. Role of kinaseindependent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J Cell Biol 189: 955-965, 2011.