Effects of cigarette smoke on pulmonary endothelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 314, Issue 5, 2018, Pages L743-L756

  Lu, Qing ^a,b   Gottlieb, Eric ^b   Rounds, Sharon ^a,b  

^a PROVIDENCE VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

Acute respiratory distress syndrome; Cigarette smoke; Emphysema; Endothelial cells; Pulmonary hypertension

Indexed keywords

ANIMAL; CHEMICALLY INDUCED; DRUG EFFECT; HUMAN; PATHOLOGY; PULMONARY ARTERY; PULMONARY HYPERTENSION; SMOKING; VASCULAR ENDOTHELIUM;

ANIMALS; ENDOTHELIUM, VASCULAR; HUMANS; HYPERTENSION, PULMONARY; PULMONARY ARTERY; SMOKING;

EID: 85054775316     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/AJPLUNG.00373.2017     Document Type: Review

References (160)

1. Abadie Y, Bregeon F, Papazian L, Lange F, Chailley-Heu B, Thomas P, Duvaldestin P, Adnot S, Maitre B, Delclaux C. Decreased VEGF concentration in lung tissue and vascular injury during ARDS. Eur Respir J 25: 139 –146, 2005. doi:10.1183/09031936.04.00065504.
2. 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. doi:10.1371/journal.pone.0008045.
3. Agrawal A, Garg R, Sahu D, Kumar M. Study the association of chronic obstructive pulmonary disease with early endothelial dysfunction and its impact on cardiovascular system by estimating urinary albumin creatinine ratio. Lung India 34: 138 –143, 2017. doi:10.4103/0970-2113. 201299.
4. Aldonyte R, Hutchinson TE, Jin B, Brantly M, Block E, Patel J, Zhang J. Endothelial alpha-1-antitrypsin attenuates cigarette smoke induced apoptosis in vitro. COPD 5: 153–162, 2008. [Erratum in COPD 5: 405, 2008.] doi:10.1080/15412550802092936.
5. Alwis KU, deCastro BR, Morrow JC, Blount BC. Acrolein exposure in U.S. tobacco smokers and non-tobacco users: NHANES 2005-2006. Environ Health Perspect 123: 1302–1308, 2015. doi:10.1289/ehp. 1409251.
6. Arunachalam G, Yao H, Sundar IK, Caito S, Rahman I. SIRT1 regulates oxidant- and cigarette smoke-induced eNOS acetylation in endothelial cells: role of resveratrol. Biochem Biophys Res Commun 393: 66 –72, 2010. doi:10.1016/j.bbrc.2010.01.080.
7. Barberà JA. Mechanisms of development of chronic obstructive pulmonary disease-associated pulmonary hypertension. Pulm Circ 3: 160–164, 2013. doi:10.4103/2045-8932.109949.
8. Barberà JA, Peinado VI, Santos S, Ramirez J, Roca J, Rodriguez-Roisin R. Reduced expression of endothelial nitric oxide synthase in pulmonary arteries of smokers. Am J Respir Crit Care Med 164: 709–713, 2001. doi:10.1164/ajrccm.164.4.2101023.
9. Barbieri SS, Ruggiero L, Tremoli E, Weksler BB. Suppressing PTEN activity by tobacco smoke plus interleukin-1β modulates dissociation of VE-cadherin/β-catenin complexes in endothelium. Arterioscler Thromb Vasc Biol 28: 732–738, 2008. doi:10.1161/ATVBAHA.107.159434.
10. Barbieri SS, Weksler BB. Tobacco smoke cooperates with interleukin-1β to alter β-catenin trafficking in vascular endothelium resulting in increased permeability and induction of cyclooxygenase-2 expression in vitro and in vivo. FASEB J 21: 1831–1843, 2007. doi:10.1096/fj.06-7557com.
11. Barnoya J, Glantz SA. Cardiovascular effects of secondhand smoke: nearly as large as smoking. Circulation 111: 2684–2698, 2005. doi:10. 1161/CIRCULATIONAHA.104.492215.
12. Barrowcliffe MP, Jones JG. Pulmonary clearance of 99mTc-DTPA in the diagnosis and evolution of increased permeability pulmonary oedema. Anaesth Intensive Care 17: 422–432, 1989.
13. Bello S, Menéndez R, Antoni T, Reyes S, Zalacain R, Capelastegui A, Aspa J, Borderías L, Martin-Villasclaras JJ, Alfageme I, Rodríguez de Castro F, Rello J, Luis M, Ruiz-Manzano J. Tobacco smoking increases the risk for death from pneumococcal pneumonia. Chest 146: 1029 –1037, 2014. doi:10.1378/chest.13-2853.
14. 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. doi:10.1096/fj.04-3192com.
15. Birukova AA, Birukov KG, Smurova K, Adyshev D, Kaibuchi K, Alieva I, Garcia JG, Verin AD. Novel role of microtubules in thrombin-induced endothelial barrier dysfunction. FASEB J 18: 1879 –1890, 2004. doi:10.1096/fj.04-2328com.
16. Biswas P, Canosa S, Schoenfeld D, Schoenfeld J, Li P, Cheas LC, Zhang J, Cordova A, Sumpio B, Madri JA. PECAM-1 affects GSK-3β-mediated β-catenin phosphorylation and degradation. Am J Pathol 169: 314–324, 2006. doi:10.2353/ajpath.2006.051112.
17. Böhm F, Pernow J. The importance of endothelin-1 for vascular dysfunction in cardiovascular disease. Cardiovasc Res 76: 8–18, 2007. doi:10.1016/j.cardiores.2007.06.004.
18. Borgas D, Chambers E, Newton J, Ko J, Rivera S, Rounds S, Lu Q. Cigarette smoke disrupted lung endothelial barrier integrity and increased susceptibility to acute lung injury via histone deacetylase 6. Am J Respir Cell Mol Biol 54: 683–696, 2016. doi:10.1165/rcmb.2015-0149OC.
19. 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. doi:10.1083/jcb. 137.6.1421.
20. Brown SM, Wilson E, Presson AP, Zhang C, Dinglas VD, Greene T, Hopkins RO, Needham DM; National Institutes of Health NHLBI ARDS Network. Predictors of 6-month health utility outcomes in survivors of acute respiratory distress syndrome. Thorax 72: 311–317, 2017. doi:10.1136/thoraxjnl-2016-208560.
21. Burns AR, Hosford SP, Dunn LA, Walker DC, Hogg JC. Respiratory epithelial permeability after cigarette smoke exposure in guinea pigs. J Appl Physiol (1985) 66: 2109 –2116, 1989. doi:10.1152/jappl.1989.66.5. 2109.
22. Cai J, Niu X, Chen Y, Hu Q, Shi G, Wu H, Wang J, Yi J. Emodin-induced generation of reactive oxygen species inhibits RhoA activation to sensitize gastric carcinoma cells to anoikis. Neoplasia 10: 41–51, 2008. doi:10.1593/neo.07754.
23. Calfee CS, Delucchi K, Parsons PE, Thompson BT, Ware LB, Matthay MA; NHLBI ARDS Network. Subphenotypes in acute respiratory distress syndrome: latent class analysis of data from two randomised controlled trials. Lancet Respir Med 2: 611–620, 2014. doi:10. 1016/S2213-2600(14)70097-9.
24. Calfee CS, Matthay MA, Eisner MD, Benowitz N, Call M, Pittet JF, Cohen MJ. Active and passive cigarette smoking and acute lung injury after severe blunt trauma. Am J Respir Crit Care Med 183: 1660 –1665, 2011. doi:10.1164/rccm.201011-1802OC.
25. Chan ED, Kinney WH, Honda JR, Bishwakarma R, Gangavelli A, Mya J, Bai X, Ordway DJ. Tobacco exposure and susceptibility to tuberculosis: is there a smoking gun? Tuberculosis (Edinb) 94: 544 –550, 2014. doi:10.1016/j.tube.2014.08.010.
26. Chattopadhyay S, Fensterl V, Zhang Y, Veleeparambil M, Wetzel JL, Sen GC. Inhibition of viral pathogenesis and promotion of the septic shock response to bacterial infection by IRF-3 are regulated by the acetylation and phosphorylation of its coactivators. MBio 4: e00636-12, 2013. doi:10.1128/mBio.00636-12.
27. Chen HY, Li L, Fu ZJ. Histone deacetylase inhibitors trichostatin A and suberoylanilide hydroxamic acid attenuate ventilator-induced lung injury. Pharmazie 69: 55–59, 2014. doi:10.1691/ph.2014.3716.
28. Chun LF, Moazed F, Calfee CS, Matthay MA, Gotts JE. Pulmonary toxicity of e-cigarettes. Am J Physiol Lung Cell Mol Physiol 313: L193–L206, 2017. doi:10.1152/ajplung.00071.2017.
29. Demos-Davies KM, Ferguson BS, Cavasin MA, Mahaffey JH, Williams SM, Spiltoir JI, Schuetze KB, Horn TR, Chen B, Ferrara C, Scellini B, Piroddi N, Tesi C, Poggesi C, Jeong MY, McKinsey TA. HDAC6 contributes to pathological responses of heart and skeletal muscle to chronic angiotensin-II signaling. Am J Physiol Heart Circ Physiol 307: H252–H258, 2014. doi:10.1152/ajpheart.00149.2014.
30. Divo M. COPD, co-morbidities and health-related quality of life (HRQOL): more is less. COPD 10: 275–276, 2013. doi:10.3109/15412555.2013. 795409.
31. Drannik AG, Pouladi MA, Robbins CS, Goncharova SI, Kianpour S, Stämpfli MR. Impact of cigarette smoke on clearance and inflammation after Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 170: 1164–1171, 2004. doi:10.1164/rccm.200311-1521OC.
32. Duong-Quy S, Dao P, Hua-Huy T, Guilluy C, Pacaud P, Dinh-Xuan AT. Increased Rho-kinase expression and activity and pulmonary endothelial dysfunction in smokers with normal lung function. Eur Respir J 37: 349–355, 2011. doi:10.1183/09031936.00056610.
33. Fabbri LM, Beghé B, Agustí A. COPD and the solar system: introducing the chronic obstructive pulmonary disease comorbidome. Am J Respir Crit Care Med 186: 117–119, 2012. doi:10.1164/rccm.201205-0906ED.
34. Famous KR, Delucchi K, Ware LB, Kangelaris KN, Liu KD, Thompson BT, Calfee CS; ARDS Network. Acute respiratory distress syndrome subphenotypes respond differently to randomized fluid management strategy. Am J Respir Crit Care Med 195: 331–338, 2017. doi:10. 1164/rccm.201603-0645OC.
35. Ferrer E, Peinado VI, Díez M, Carrasco JL, Musri MM, Martínez A, Rodríguez-Roisin R, Barberà JA. Effects of cigarette smoke on endothelial function of pulmonary arteries in the guinea pig. Respir Res 10: 76, 2009. doi:10.1186/1465-9921-10-76.
36. 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. doi:10.1097/TA.0b013e3181e1761e.
37. Freixa X, Portillo K, Paré C, Garcia-Aymerich J, Gomez FP, Benet M, Roca J, Farrero E, Ferrer J, Fernandez-Palomeque C, Antó JM, Barberà JA; PAC-COPD Study Investigators. Echocardiographic abnormalities in patients with COPD at their first hospital admission. Eur Respir J 41: 784–791, 2013. doi:10.1183/09031936.00222511.
38. Fujita M, Kuwano K, Kunitake R, Hagimoto N, Miyazaki H, Kaneko Y, Kawasaki M, Maeyama T, Hara N. Endothelial cell apoptosis in lipopolysaccharide-induced lung injury in mice. Int Arch Allergy Immunol 117: 202–208, 1998. doi:10.1159/000024011.
39. Fukada M, Hanai A, Nakayama A, Suzuki T, Miyata N, Rodriguiz RM, Wetsel WC, Yao TP, Kawaguchi Y. Loss of deacetylation activity of Hdac6 affects emotional behavior in mice. PLoS One 7: e30924, 2012. doi:10.1371/journal.pone.0030924.
40. Gajic O, Dabbagh O, Park PK, Adesanya A, Chang SY, Hou P, Anderson H III, 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, Malinchoc M; U.S. Critical Illness and Injury Trials Group: Lung Injury Prevention Study Investigators (USCIITG-LIPS). 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. doi:10.1164/rccm.201004-0549OC.
41. García-Lucio J, Argemi G, Tura-Ceide O, Diez M, Paul T, Bonjoch C, Coll-Bonfill N, Blanco I, Barberà JA, Musri MM, Peinado VI. Gene expression profile of angiogenic factors in pulmonary arteries in COPD: relationship with vascular remodeling. Am J Physiol Lung Cell Mol Physiol 310: L583–L592, 2016. doi:10.1152/ajplung.00261.2015.
42. Gill SE, Rohan M, Mehta S. Role of pulmonary microvascular endothelial cell apoptosis in murine sepsis-induced lung injury in vivo. Respir Res 16: 109, 2015. doi:10.1186/s12931-015-0266-7.
43. Gill SE, Taneja R, Rohan M, Wang L, Mehta S. Pulmonary microvascular albumin leak is associated with endothelial cell death in murine sepsis-induced lung injury in vivo. PLoS One 9: e88501, 2014. doi:10. 1371/journal.pone.0088501.
44. Govindarajan N, Rao P, Burkhardt S, Sananbenesi F, Schlüter OM, Bradke F, Lu J, Fischer A. Reducing HDAC6 ameliorates cognitive deficits in a mouse model for Alzheimer’s disease. EMBO Mol Med 5: 52–63, 2013. doi:10.1002/emmm.201201923.
45. Green LA, Petrusca D, Rajashekhar G, Gianaris T, Schweitzer KS, Wang L, Justice MJ, Petrache I, Clauss M. Cigarette smoke-induced CXCR3 receptor up-regulation mediates endothelial apoptosis. Am J Respir Cell Mol Biol 47: 807–814, 2012. doi:10.1165/rcmb.2012-0132OC.
46. Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo H, Triantafillopoulos A, Whittaker K, Hoidal JR, Cosio MG. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am J Respir Crit Care Med 170: 974–980, 2004. doi:10.1164/rccm.200309-1270OC.
47. Guo M, Wu MH, Granger HJ, Yuan SY. Focal adhesion kinase in neutrophil-induced microvascular hyperpermeability. Microcirculation 12: 223–232, 2005. doi:10.1080/10739680590905251.
48. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci USA 100: 4389 –4394, 2003. doi:10.1073/pnas.0430973100.
49. Heijink IH, Pouwels SD, Leijendekker C, de Bruin HG, Zijlstra GJ, van der Vaart H, Ten Hacken NH, van Oosterhout AJ, Nawijn MC, van der Toorn M. Cigarette smoke induced damage-associated molecular pattern release from necrotic neutrophils triggers proinflammatory mediator release. Am J Respir Cell Mol Biol 52: 554–562, 2015. doi:10.1165/rcmb.2013-0505OC.
50. Hengstermann A, Müller T. Endoplasmic reticulum stress induced by aqueous extracts of cigarette smoke in 3T3 cells activates the unfolded-protein-response-dependent PERK pathway of cell survival. Free Radic Biol Med 44: 1097–1107, 2008. doi:10.1016/j.freeradbiomed.2007.12. 009.
51. Heo J, Raines KW, Mocanu V, Campbell SL. Redox regulation of RhoA. Biochemistry 45: 14481–14489, 2006. doi:10.1021/bi0610101.
52. Hirsch J, Chalkley RJ, Bentley T, Burlingame AL, Frank JA. Double impact of cigarette smoke and mechanical ventilation on the alveolar epithelial type II cell. Crit Care 18: R50, 2014. doi:10.1186/cc13795.
53. Holden WE, Maier JM, Malinow MR. Cigarette smoke extract increases albumin flux across pulmonary endothelium in vitro. J Appl Physiol (1985) 66: 443–449, 1989. doi:10.1152/jappl.1989.66.1.443.
54. 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. doi:10.1074/jbc. M511248200.
55. Hsieh SJ, Zhuo H, Benowitz NL, Thompson BT, Liu KD, Matthay MA, Calfee CS; National Heart, Lung, and Blood Institute Acute Respiratory Distress Syndrome Network; National Heart Lung and Blood Institute Acute Respiratory Distress Syndrome Network. Prevalence and impact of active and passive cigarette smoking in acute respiratory distress syndrome. Crit Care Med 42: 2058 –2068, 2014. doi:10.1097/CCM.0000000000000418.
56. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP. HDAC6 is a microtubule-associated deacetylase. Nature 417: 455–458, 2002. doi:10.1038/417455a.
57. Imai K, Mercer BA, Schulman LL, Sonett JR, D’Armiento JM. Correlation of lung surface area to apoptosis and proliferation in human emphysema. Eur Respir J 25: 250–258, 2005. doi:10.1183/09031936. 05.00023704.
58. 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. doi:10.1378/chest.117.1.163.
59. Jaimes EA, DeMaster EG, Tian RX, Raij L. Stable compounds of cigarette smoke induce endothelial superoxide anion production via NADPH oxidase activation. Arterioscler Thromb Vasc Biol 24: 1031–1036, 2004. doi:10.1161/01.ATV.0000127083.88549.58.
60. Jochems J, Boulden J, Lee BG, Blendy JA, Jarpe M, Mazitschek R, Van Duzer JH, Jones S, Berton O. Antidepressant-like properties of novel HDAC6-selective inhibitors with improved brain bioavailability. Neuropsychopharmacology 39: 389–400, 2014. doi:10.1038/npp.2013. 207.
61. Jones JG, Lawler P, Crawley JC, Minty BD, Hulands G, Veall N. Increased alveolar epithelial permeability in cigarette smokers. Lancet 315: 66–68, 1980. doi:10.1016/S0140-6736(80)90493-6.
62. Jorgensen E, Stinson A, Shan L, Yang J, Gietl D, Albino AP. Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 8: 229, 2008. doi:10.1186/1471-2407-8-229.
63. Kang MJ, Lee CG, Lee JY, Dela Cruz CS, Chen ZJ, Enelow R, Elias JA. Cigarette smoke selectively enhances viral PAMP- and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest 118: 2771–2784, 2008. doi:10.1172/JCI32709.
64. Kasahara Y, Tuder RM, Cool CD, Lynch DA, Flores SC, Voelkel NF. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. Am J Respir Crit Care Med 163: 737–744, 2001. doi:10. 1164/ajrccm.163.3.2002117.
65. Kawasaki M, Kuwano K, Hagimoto N, Matsuba T, Kunitake R, Tanaka T, Maeyama T, Hara N. Protection from lethal apoptosis in lipopolysaccharide-induced acute lung injury in mice by a caspase inhibitor. Am J Pathol 157: 597–603, 2000. doi:10.1016/S0002-9440(10) 64570-1.
66. Kelsen SG, Duan X, Ji R, Perez O, Liu C, Merali S. Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am J Respir Cell Mol Biol 38: 541–550, 2008. doi:10.1165/rcmb.2007-0221OC.
67. Kim BS, Serebreni L, Hamdan O, Wang L, Parniani A, Sussan T, Scott Stephens R, Boyer L, Damarla M, Hassoun PM, Damico R. Xanthine oxidoreductase is a critical mediator of cigarette smoke-induced endothelial cell DNA damage and apoptosis. Free Radic Biol Med 60: 336 –346, 2013. doi:10.1016/j.freeradbiomed.2013.01.023.
68. Kispert SE, Marentette JO, McHowat J. Enhanced breast cancer cell adherence to the lung endothelium via PAF acetylhydrolase inhibition: a potential mechanism for enhanced metastasis in smokers. Am J Physiol Cell Physiol 307: C951–C956, 2014. doi:10.1152/ajpcell.00218.2014.
69. Kitaguchi Y, Taraseviciene-Stewart L, Hanaoka M, Natarajan R, Kraskauskas D, Voelkel NF. Acrolein induces endoplasmic reticulum stress and causes airspace enlargement. PLoS One 7: e38038, 2012. doi:10.1371/journal.pone.0038038.
70. Knezevic N, Tauseef M, Thennes T, Mehta D. The G protein βγ subunit mediates reannealing of adherens junctions to reverse endothelial permeability increase by thrombin. J Exp Med 206: 2761–2777, 2009. doi:10.1084/jem.20090652.
71. Kratzer A, Chu HW, Salys J, Moumen Z, Leberl M, Bowler R, Cool C, Zamora M, Taraseviciene-Stewart L. Endothelial cell adhesion molecule CD146: implications for its role in the pathogenesis of COPD. J Pathol 230: 388–398, 2013. doi:10.1002/path.4197.
72. Kubo S, Kobayashi M, Masunaga Y, Ishii H, Hirano Y, Takahashi K, Shimizu Y. Cytokine and chemokine expression in cigarette smoke-induced lung injury in guinea pigs. Eur Respir J 26: 993–1001, 2005. doi:10.1183/09031936.05.00042405.
73. Lam HC, Cloonan SM, Bhashyam AR, Haspel JA, Singh A, Sathirapongsasuti JF, Cervo M, Yao H, Chung AL, Mizumura K, An CH, Shan B, Franks JM, Haley KJ, Owen CA, Tesfaigzi Y, Washko GR, Quackenbush J, Silverman EK, Rahman I, Kim HP, Mahmood A, Biswal SS, Ryter SW, Choi AM. Histone deacetylase 6-mediated selective autophagy regulates COPD-associated cilia dysfunction. J Clin Invest 123: 5212–5230, 2013. doi:10.1172/JCI69636.
74. Lehr HA, Frei B, Arfors KE. Vitamin C prevents cigarette smoke-induced leukocyte aggregation and adhesion to endothelium in vivo. Proc Natl Acad Sci USA 91: 7688 –7692, 1994. doi:10.1073/pnas.91.16. 7688.
75. Lehr HA, Kress E, Menger MD, Friedl HP, Hübner C, Arfors KE, Messmer K. Cigarette smoke elicits leukocyte adhesion to endothelium in hamsters: inhibition by CuZn-SOD. Free Radic Biol Med 14: 573–581, 1993. doi:10.1016/0891-5849(93)90138-K.
76. Li XY, Rahman I, Donaldson K, MacNee W. Mechanisms of cigarette smoke induced increased airspace permeability. Thorax 51: 465–471, 1996. doi:10.1136/thx.51.5.465.
77. Liu H, Ding L, Zhang Y, Ni S. Circulating endothelial microparticles involved in lung function decline in a rat exposed in cigarette smoke maybe from apoptotic pulmonary capillary endothelial cells. J Thorac Dis 6: 649–655, 2014. doi:10.3978/j.issn.2072-1439.2014.06.26.
78. Liu X, Liu Y, Huang X, Lin G, Xie C. Endothelial progenitor cell dysfunction in acute exacerbation of chronic obstructive pulmonary disease. Mol Med Rep 16: 5294–5302, 2017. doi:10.3892/mmr.2017. 7260.
79. Low B, Liang M, Fu J. p38 mitogen-activated protein kinase mediates sidestream cigarette smoke-induced endothelial permeability. J Pharmacol Sci 104: 225–231, 2007. doi:10.1254/jphs.FP0070385.
80. Lu Q, Mundy M, Chambers E, Lange T, Newton J, Borgas D, Yao H, Choudhary G, Basak R, Oldham M, Rounds S. Alda-1 protects against acrolein-induced acute lung injury and endothelial barrier dysfunction. Am J Respir Cell Mol Biol 57: 662–673, 2017. doi:10.1165/rcmb.2016-0342OC.
81. Lu Q, Rounds S. Focal adhesion kinase and endothelial cell apoptosis. Microvasc Res 83: 56–63, 2012. doi:10.1016/j.mvr.2011.05.003.
82. Lu Q, Sakhatskyy P, Grinnell K, Newton J, Ortiz M, Wang Y, Sanchez-Esteban J, Harrington EO, Rounds S. Cigarette smoke causes lung vascular barrier dysfunction via oxidative stress-mediated inhibition of RhoA and focal adhesion kinase. Am J Physiol Lung Cell Mol Physiol 301: L847–L857, 2011. doi:10.1152/ajplung.00178.2011.
83. Lu Q, Sakhatskyy P, Newton J, Shamirian P, Hsiao V, Curren S, Gabino Miranda GA, Pedroza M, Blackburn MR, Rounds S. Sustained adenosine exposure causes lung endothelial apoptosis: a possible contributor to cigarette smoke-induced endothelial apoptosis and lung injury. Am J Physiol Lung Cell Mol Physiol 304: L361–L370, 2013. doi:10.1152/ajplung.00161.2012.
84. Lugade AA, Bogner PN, Thatcher TH, Sime PJ, Phipps RP, Thanavala Y. Cigarette smoke exposure exacerbates lung inflammation and compromises immunity to bacterial infection. J Immunol 192: 5226–5235, 2014. doi:10.4049/jimmunol.1302584.
85. Marwick JA, Stevenson CS, Giddings J, MacNee W, Butler K, Rahman I, Kirkham PA. Cigarette smoke disrupts VEGF165-VEGFR-2 receptor signaling complex in rat lungs and patients with COPD: morphological impact of VEGFR-2 inhibition. Am J Physiol Lung Cell Mol Physiol 290: L897–L908, 2006. doi:10.1152/ajplung. 00116.2005.
86. Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, Horinouchi S, Yoshida M. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21: 6820–6831, 2002. doi:10.1093/emboj/cdf682.
87. Milara J, Ortiz JL, Juan G, Guijarro R, Almudever P, Martorell M, Morcillo EJ, Cortijo J. Cigarette smoke exposure up-regulates endothelin receptor B in human pulmonary artery endothelial cells: molecular and functional consequences. Br J Pharmacol 161: 1599–1615, 2010. doi:10.1111/j.1476-5381.2010.00979.x.
88. Mirzapoiazova T, Kolosova IA, Moreno L, Sammani S, Garcia JG, Verin AD. Suppression of endotoxin-induced inflammation by taxol. Eur Respir J 30: 429 –435, 2007. doi:10.1183/09031936.00154206.
89. Mizumura K, Cloonan SM, Nakahira K, Bhashyam AR, Cervo M, Kitada T, Glass K, Owen CA, Mahmood A, Washko GR, Hashimoto S, Ryter SW, Choi AM. Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J Clin Invest 124: 3987–4003, 2014. doi:10.1172/JCI74985.
90. Mizuno S, Yasuo M, Bogaard HJ, Kraskauskas D, Alhussaini A, Gomez-Arroyo J, Farkas D, Farkas L, Voelkel NF. Copper deficiency induced emphysema is associated with focal adhesion kinase inactivation. PLoS One 7: e30678, 2012. doi:10.1371/journal.pone.0030678.
91. Moazed F, Burnham EL, Vandivier RW, O’Kane CM, Shyamsundar M, Hamid U, Abbott J, Thickett DR, Matthay MA, McAuley DF, Calfee CS. Cigarette smokers have exaggerated alveolar barrier disruption in response to lipopolysaccharide inhalation. Thorax 71: 1130 –1136, 2016. doi:10.1136/thoraxjnl-2015-207886.
92. Nana-Sinkam SP, Lee JD, Sotto-Santiago S, Stearman RS, Keith RL, Choudhury Q, Cool C, Parr J, Moore MD, Bull TM, Voelkel NF, Geraci MW. Prostacyclin prevents pulmonary endothelial cell apoptosis induced by cigarette smoke. Am J Respir Crit Care Med 175: 676 –685, 2007. doi:10.1164/rccm.200605-724OC.
93. Ni YF, Wang J, Yan XL, Tian F, Zhao JB, Wang YJ, Jiang T. Histone deacetylase inhibitor, butyrate, attenuates lipopolysaccharide-induced acute lung injury in mice. Respir Res 11: 33, 2010. doi:10.1186/1465-9921-11-33.
94. 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. doi:10.1152/ajpheart.00599.2006.
95. Overbeek SA, Braber S, Henricks PA, Kleinjan M, Kamp VM, Georgiou NA, Garssen J, Kraneveld AD, Folkerts G. Cigarette smoke induces β2-integrin-dependent neutrophil migration across human endothelium. Respir Res 12: 75, 2011. doi:10.1186/1465-9921-12-75.
96. 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. doi:10.1016/j.jjcc.2010.07.003.
97. Panzer AR, Lynch SV, Langelier C, Christie JD, McCauley K, Nelson M, Cheung CK, Benowitz NL, Cohen MJ, Calfee CS. Lung microbiota is related to smoking status and to development of acute respiratory distress syndrome in critically ill trauma patients. Am J Respir Crit Care Med 197: 621–631, 2018. doi:10.1164/rccm.201702-0441OC.
98. Petrache I, Birukova A, Ramirez SI, Garcia JG, Verin AD. The role of the microtubules in tumor necrosis factor-α-induced endothelial cell permeability. Am J Respir Cell Mol Biol 28: 574–581, 2003. doi:10. 1165/rcmb.2002-0075OC.
99. Petrache I, Fijalkowska I, Medler TR, Skirball J, Cruz P, Zhen L, Petrache HI, Flotte TR, Tuder RM. α-1 antitrypsin inhibits caspase-3 activity, preventing lung endothelial cell apoptosis. Am J Pathol 169: 1155–1166, 2006. doi:10.2353/ajpath.2006.060058.
100. Petrache I, Natarajan V, Zhen L, Medler TR, Richter AT, Cho C, Hubbard WC, Berdyshev EV, Tuder RM. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat Med 11: 491–498, 2005. doi:10.1038/nm1238.
101. Petta V, Bakakos P, Tseliou E, Kostikas K, Simoes DC, Konstantellou E, Hillas G, Koulouris NG, Papiris S, Loukides S. Angiopoietins 1 and 2 in sputum supernatant of optimally treated asthmatics: the effect of smoking. Eur J Clin Invest 45: 56–62, 2015. doi:10.1111/eci.12379.
102. Phillips E, Wang TW, Husten CG, Corey CG, Apelberg BJ, Jamal A, Homa DM, King BA. Tobacco product use among adults: United States, 2015. MMWR Morb Mortal Wkly Rep 66: 1209 –1215, 2017. doi:10. 15585/mmwr.mm6644a2.
103. Pines H, Koutsky L, Buskin S. Cigarette smoking and mortality among HIV-infected individuals in Seattle, Washington (1996–2008). AIDS Behav 15: 243–251, 2011. doi:10.1007/s10461-010-9682-3.
104. Polverino F, Laucho-Contreras ME, Petersen H, Bijol V, Sholl LM, Choi ME, Divo M, Pinto-Plata V, Chetta A, Tesfaigzi Y, Celli BR, Owen CA. A pilot study linking endothelial injury in lungs and kidneys in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 195: 1464–1476, 2017. doi:10.1164/rccm.201609-1765OC.
105. Pouwels SD, Heijink IH, ten Hacken NH, Vandenabeele P, Krysko DV, Nawijn MC, van Oosterhout AJ. DAMPs activating innate and adaptive immune responses in COPD. Mucosal Immunol 7: 215–226, 2014. doi:10.1038/mi.2013.77.
106. Pouwels SD, Hesse L, Faiz A, Lubbers J, Bodha PK, Ten Hacken NH, van Oosterhout AJ, Nawijn MC, Heijink IH. Susceptibility for cigarette smoke-induced DAMP release and DAMP-induced inflammation in COPD. Am J Physiol Lung Cell Mol Physiol 311: L881–L892, 2016. doi:10.1152/ajplung.00135.2016.
107. Pouwels SD, Zijlstra GJ, van der Toorn M, Hesse L, Gras R, Ten Hacken NH, Krysko DV, Vandenabeele P, de Vries M, van Oosterhout AJ, Heijink IH, Nawijn MC. Cigarette smoke-induced necroptosis and DAMP release trigger neutrophilic airway inflammation in mice. Am J Physiol Lung Cell Mol Physiol 310: L377–L386, 2016. doi:10.1152/ajplung.00174.2015.
108. Quadri SK, Bhattacharya J. Resealing of endothelial junctions by focal adhesion kinase. Am J Physiol Lung Cell Mol Physiol 292: L334 –L342, 2007. doi:10.1152/ajplung.00228.2006.
109. Reddy KP, Parker RA, Losina E, Baggett TP, Paltiel AD, Rigotti NA, Weinstein MC, Freedberg KA, Walensky RP. Impact of cigarette smoking and smoking cessation on life expectancy among people with HIV: a US-based modeling study. J Infect Dis 214: 1672–1681, 2016. doi:10.1093/infdis/jiw430.
110. Saito S, Lasky JA, Guo W, Nguyen H, Mai A, Danchuk S, Sullivan DE, Shan B. Pharmacological inhibition of HDAC6 attenuates endothelial barrier dysfunction induced by thrombin. Biochem Biophys Res Commun 408: 630–634, 2011. doi:10.1016/j.bbrc.2011.04.075.
111. Sakhatskyy P, Gabino Miranda GA, Newton J, Lee CG, Choudhary G, Vang A, Rounds S, Lu Q. Cigarette smoke-induced lung endothelial apoptosis and emphysema are associated with impairment of FAK and eIF2α. Microvasc Res 94: 80–89, 2014. doi:10.1016/j.mvr.2014.05.003.
112. Sakhatskyy P, Wang Z, Borgas D, Lomas-Neira J, Chen Y, Ayala A, Rounds S, Lu Q. Double-hit mouse model of cigarette smoke priming for acute lung injury. Am J Physiol Lung Cell Mol Physiol 312: L56–L67, 2017. doi:10.1152/ajplung.00436.2016.
113. Santos S, Peinado VI, Ramírez J, Melgosa T, Roca J, Rodriguez-Roisin R, Barberà JA. Characterization of pulmonary vascular remodelling in smokers and patients with mild COPD. Eur Respir J 19: 632–638, 2002. doi:10.1183/09031936.02.00245902.
114. Schröder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 74: 739–789, 2005. doi:10.1146/annurev.biochem. 73.011303.074134.
115. Schweitzer KS, Chen SX, Law S, Van Demark M, Poirier C, Justice MJ, Hubbard WC, Kim ES, Lai X, Wang M, Kranz WD, Carroll CJ, Ray BD, Bittman R, Goodpaster J, Petrache I. Endothelial disruptive proinflammatory effects of nicotine and e-cigarette vapor exposures. Am J Physiol Lung Cell Mol Physiol 309: L175–L187, 2015. doi:10.1152/ajplung.00411.2014.
116. Schweitzer KS, Hatoum H, Brown MB, Gupta M, Justice MJ, Beteck B, Van Demark M, 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 301: L836 –L846, 2011. doi:10.1152/ajplung.00385.2010.
117. Serban KA, Rezania S, Petrusca DN, Poirier C, Cao D, Justice MJ, Patel M, Tsvetkova I, Kamocki K, Mikosz A, Schweitzer KS, Jacobson S, Cardoso A, Carlesso N, Hubbard WC, Kechris K, Dragnea B, Berdyshev EV, McClintock J, Petrache I. Structural and functional characterization of endothelial microparticles released by cigarette smoke. Sci Rep 6: 31596, 2016. doi:10.1038/srep31596.
118. Shankar-Hari M, McAuley DF. Acute respiratory distress syndrome phenotypes and identifying treatable traits. The dawn of personalized medicine for ARDS. Am J Respir Crit Care Med 195: 280–281, 2017. doi:10.1164/rccm.201608-1729ED.
119. Sharma J, Young DM, Marentette JO, Rastogi P, Turk J, McHowat J. Lung endothelial cell platelet-activating factor production and inflammatory cell adherence are increased in response to cigarette smoke component exposure. Am J Physiol Lung Cell Mol Physiol 302: L47–L55, 2012. doi:10.1152/ajplung.00179.2011.
120. Shen Y, Rattan V, Sultana C, Kalra VK. Cigarette smoke condensate-induced adhesion molecule expression and transendothelial migration of monocytes. Am J Physiol Heart Circ Physiol 270: H1624 –H1633, 1996. doi:10.1152/ajpheart.1996.270.5.H1624.
121. Sikka G, Pandey D, Bhuniya AK, Steppan J, Armstrong D, Santhanam L, Nyhan D, Berkowitz DE. Contribution of arginase activation to vascular dysfunction in cigarette smoking. Atherosclerosis 231: 91–94, 2013. doi:10.1016/j.atherosclerosis.2013.08.026.
122. 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. doi:10.1073/pnas.0813113106.
123. Stämpfli MR, Anderson GP. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9: 377–384, 2009. doi:10.1038/nri2530.
124. Strulovici-Barel Y, Staudt MR, Krause A, Gordon C, Tilley AE, Harvey BG, Kaner RJ, Hollmann C, Mezey JG, Bitter H, Pillai SG, Hilton H, Wolff G, Stevenson CS, Visvanathan S, Fine JS, Crystal RG. Persistence of circulating endothelial microparticles in COPD despite smoking cessation. Thorax 71: 1137–1144, 2016. doi:10.1136/thoraxjnl-2015-208274.
125. Su Y, Han W, Giraldo C, De Li Y, Block ER. Effect of cigarette smoke extract on nitric oxide synthase in pulmonary artery endothelial cells. Am J Respir Cell Mol Biol 19: 819–825, 1998. doi:10.1165/ajrcmb.19.5.3091.
126. Sun S, Sursal T, Adibnia Y, Zhao C, Zheng Y, Li H, Otterbein LE, Hauser CJ, Itagaki K. Mitochondrial DAMPs increase endothelial permeability through neutrophil dependent and independent pathways. PLoS One 8: e59989, 2013. doi:10.1371/journal.pone.0059989.
127. Takahashi T, Kobayashi S, Fujino N, Suzuki T, Ota C, He M, Yamada M, Suzuki S, Yanai M, Kurosawa S, Yamaya M, Kubo H. Increased circulating endothelial microparticles in COPD patients: a potential biomarker for COPD exacerbation susceptibility. Thorax 67: 1067–1074, 2012. doi:10.1136/thoraxjnl-2011-201395.
128. Tandon S, Batchelor A, Bullock R, Gascoigne A, Griffin M, Hayes N, Hing J, Shaw I, Warnell I, Baudouin SV. Peri-operative risk factors for acute lung injury after elective oesophagectomy. Br J Anaesth 86: 633–638, 2001. doi:10.1093/bja/86.5.633.
129. Taylor AE, Gaar KA Jr. Estimation of equivalent pore radii of pulmonary capillary and alveolar membranes. Am J Physiol 218: 1133–1140, 1970. doi:10.1152/ajplegacy.1970.218.4.1133.
130. Thomashow MA, Shimbo D, Parikh MA, Hoffman EA, Vogel-Claussen J, Hueper K, Fu J, Liu CY, Bluemke DA, Ventetuolo CE, Doyle MF, Barr RG. Endothelial microparticles in mild chronic obstructive pulmonary disease and emphysema. The Multi-Ethnic Study of Atherosclerosis Chronic Obstructive Pulmonary Disease study. Am J Respir Crit Care Med 188: 60–68, 2013. doi:10.1164/rccm.201209-1697OC.
131. Tuder RM, Wood K, Taraseviciene L, Flores SC, Voekel NF. Cigarette smoke extract decreases the expression of vascular endothelial growth factor by cultured cells and triggers apoptosis of pulmonary endothelial cells. Chest 117, Suppl 1: 241S–242S, 2000. doi:10.1378/chest.117.5_suppl_1.241S.
132. Tzima E. Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ Res 98: 176 –185, 2006. doi:10.1161/01.RES.0000200162.94463.d7.
133. United States. Department of Health and Human Services. The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General. Atlanta, GA: U.S. Dept. of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, 2014.
134. Usatyuk PV, Parinandi NL, Natarajan V. Redox regulation of 4-hy-droxy-2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. J Biol Chem 281: 35554–35566, 2006. doi:10.1074/jbc.M607305200.
135. Vandenbroucke E, Mehta D, Minshall R, Malik AB. Regulation of endothelial junctional permeability. Ann N Y Acad Sci 1123: 134–145, 2008. doi:10.1196/annals.1420.016.
136. 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 Lung Cell Mol Physiol 281: L565–L574, 2001. doi:10.1152/ajplung.2001.281.3.L565.
137. Voelkel NF. Cigarette smoke is an endothelial cell toxin. Am J Respir Crit Care Med 197: 274, 2018. doi:10.1164/rccm.201706-1123LE.
138. Wacharasint P, Fuengfoo P, Sukcharoen N, Rangsin R; THAI-SICU Trial Group. Smoking increased risk of ARDS in surgical critically ill patients: results from the multicenter THAI-SICU study (Abstract). Crit Care 19, Suppl 1: 238, 2015. doi:10.1186/cc14318.
139. Wagner K, Gröger M, McCook O, Scheuerle A, Asfar P, Stahl B, Huber-Lang M, Ignatius A, Jung B, Duechs M, Möller P, Georgieff M, Calzia E, Radermacher P, Wagner F. Blunt chest trauma in mice after cigarette smoke-exposure: effects of mechanical ventilation with 100% O2. PLoS One 10: e0132810, 2015. doi:10.1371/journal.pone.0132810.
140. Wagner L, Laczy B, Tamaskó M, Mazák I, Markó L, Molnár GA, Wagner Z, Mohás M, Cseh J, Fekete A, Wittmann I. Cigarette smoke-induced alterations in endothelial nitric oxide synthase phosphorylation: role of protein kinase C. Endothelium 14: 245–255, 2007. doi:10.1080/10623320701606707.
141. Wang B, Rao YH, Inoue M, Hao R, Lai CH, Chen D, McDonald SL, Choi MC, Wang Q, Shinohara ML, Yao TP. Microtubule acetylation amplifies p38 kinase signalling and anti-inflammatory IL-10 production. Nat Commun 5: 3479, 2014. doi:10.1038/ncomms4479.
142. Ward C, Thien F, Secombe J, Gollant S, Walters EH. Bronchoalveolar lavage fluid urea as a measure of pulmonary permeability in healthy smokers. Eur Respir J 15: 285–290, 2000. doi:10.1034/j.1399-3003. 2000.15b11.x.
143. Ware LB, Lee JW, Wickersham N, Nguyen J, Matthay MA, Calfee CS; California Transplant Donor Network. Donor smoking is associated with pulmonary edema, inflammation and epithelial dysfunction in ex vivo human donor lungs. Am J Transplant 14: 2295–2302, 2014. doi:10.1111/ajt.12853.
144. Ware LB, Zhao Z, Koyama T, May AK, Matthay MA, Lurmann FW, Balmes JR, Calfee CS. Long-term ozone exposure increases the risk of developing the acute respiratory distress syndrome. Am J Respir Crit Care Med 193: 1143–1150, 2016. doi:10.1164/rccm.201507-1418OC.
145. Wickenden JA, Clarke MC, Rossi AG, Rahman I, Faux SP, Donaldson K, MacNee W. Cigarette smoke prevents apoptosis through inhibition of caspase activation and induces necrosis. Am J Respir Cell Mol Biol 29: 562–570, 2003. doi:10.1165/rcmb.2002-0235OC.
146. Winkler R, Benz V, Clemenz M, Bloch M, Foryst-Ludwig A, Wardat S, Witte N, Trappiel M, Namsolleck P, Mai K, Spranger J, Matthias G, Roloff T, Truee O, Kappert K, Schupp M, Matthias P, Kintscher U. Histone deacetylase 6 (HDAC6) is an essential modifier of glucocorticoid-induced hepatic gluconeogenesis. Diabetes 61: 513–523, 2012. doi:10.2337/db11-0313.
147. Wong CM, Yang L, Chan KP, Chan WM, Song L, Lai HK, Thach TQ, Ho LM, Chan KH, Lam TH, Peiris JS. Cigarette smoking as a risk factor for influenza-associated mortality: evidence from an elderly cohort. Influenza Other Respi Viruses 7: 531–539, 2013. doi:10.1111/j. 1750-2659.2012.00411.x.
148. World Health Organization. Tobacco Fact Sheet [Online]. Geneva: WHO. http://www.who.int/mediacentre/factsheets/fs339/en/[March 2018].
149. Wright JL, Tai H, Churg A. Vasoactive mediators and pulmonary hypertension after cigarette smoke exposure in the guinea pig. J Appl Physiol (1985) 100: 672–678, 2006. doi:10.1152/japplphysiol.00274.2005.
150. Wright JL, Zhou S, Churg A. Pulmonary hypertension and vascular oxidative damage in cigarette smoke exposed eNOS-/- mice and human smokers. Inhal Toxicol 24: 732–740, 2012. doi:10.3109/08958378.2012. 715698.
151. Wu MH. Endothelial focal adhesions and barrier function. J Physiol 569: 359 –366, 2005. doi:10.1113/jphysiol.2005.096537.
152. Xiong Y, Zhao K, Wu J, Xu Z, Jin S, Zhang YQ. HDAC6 mutations rescue human tau-induced microtubule defects in Drosophila. Proc Natl Acad Sci USA 110: 4604–4609, 2013. doi:10.1073/pnas.1207586110.
153. Yao H, Rahman I. Role of histone deacetylase 2 in epigenetics and cellular senescence: implications in lung inflammaging and COPD. Am J Physiol Lung Cell Mol Physiol 303: L557–L566, 2012. doi:10.1152/ajplung.00175.2012.
154. Yildiz L, Akçay F, Kaynar H, Bakan N. Increased plasma endothelin-1 in heavy and light smokers. Clin Chem 42: 483–484, 1996.
155. Zhang L, Jin S, Wang C, Jiang R, Wan J. Histone deacetylase inhibitors attenuate acute lung injury during cecal ligation and puncture-induced polymicrobial sepsis. World J Surg 34: 1676–1683, 2010. doi:10.1007/s00268-010-0493-5.
156. Zhang Y, Kwon S, Yamaguchi T, Cubizolles F, Rousseaux S, Kneissel M, Cao C, Li N, Cheng HL, Chua K, Lombard D, Mizeracki A, Matthias G, Alt FW, Khochbin S, Matthias P. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol Cell Biol 28: 1688 –1701, 2008. doi:10.1128/MCB.01154-06.
157. Zhang Y, Li N, Caron C, Matthias G, Hess D, Khochbin S, Matthias P. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 22: 1168–1179, 2003. doi:10.1093/emboj/cdg115.
158. Zhao X, Peng X, Sun S, Park AY, Guan JL. Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J Cell Biol 189: 955–965, 2010. doi:10.1083/jcb.200912094.
159. Zhou Y, Mohsenin A, Morschl E, Young HW, Molina JG, Ma W, Sun CX, Martinez-Valdez H, Blackburn MR. Enhanced airway inflammation and remodeling in adenosine deaminase-deficient mice lacking the A2B adenosine receptor. J Immunol 182: 8037–8046, 2009. doi:10.4049/jimmunol.0900515.
160. Zhou Y, Murthy JN, Zeng D, Belardinelli L, Blackburn MR. Alterations in adenosine metabolism and signaling in patients with chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis. PLoS One 5: e9224, 2010. doi:10.1371/journal.pone.0009224.