The endothelium in acute lung injury/acute respiratory distress syndrome

Current Opinion in Critical Care

Volumn 14, Issue 1, 2008, Pages 22-30

  Maniatis, Nikolaos A ^a   Orfanos, Stylianos E ^a,b  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b NATIONAL AND KAPODISTRIAN UNIVERSITY OF ATHENS   (Greece)

Author keywords

ALI; ARDS; Endothelium; Lung

Indexed keywords

ACTIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CYTOSKELETON; HUMAN; INTENSIVE CARE; LUNG EDEMA; LUNG ENDOTHELIUM; NOCICEPTIVE STIMULATION; PATHOGENESIS; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANGIOPOIETINS; ANIMALS; CYTOSKELETON; ENDOTHELIUM, VASCULAR; HUMANS; PULMONARY EDEMA; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; RENIN-ANGIOTENSIN SYSTEM; RESPIRATORY DISTRESS SYNDROME, ADULT; SIGNAL TRANSDUCTION;

EID: 38149077303     PISSN: 10705295     EISSN: 15317072     Source Type: Journal    
DOI: 10.1097/MCC.0b013e3282f269b9     Document Type: Review

References (69)

1. Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 2007; 100:174-190. Comprehensively illustrated detailed review on endothelium heterogeneity.
2. Orfanos SE, Mavrommati I, Korovesi I, Roussos C. Pulmonary endothelium in acute lung injury: from basic science to the critically ill. Intensive Care Med 2004; 30:1702-1714.
3. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 2006; 86:279-367.
4. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 2001; 91:1487-1500.
5. Reutershan J, Stockton R, Zarbock A, et al. Blocking p21-activated kinase reduces lipopolysaccharide-induced acute lung injury by preventing polymorphonuclear leukocyte infiltration. Am J Respir Crit Care Med 2007; 175:1027-1035.
6. Rossi JL, Velentza AV, Steinhorn DM, et al. MLCK210 gene knockout or kinase inhibition preserves lung function following endotoxin-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2007; 292:L1327-L1334.
7. Ralay Ranaivo H, Carusio N, Wangensteen R, et al. Protection against endotoxic shock as a consequence of reduced nitrosative stress in MLCK210-null mice. Am J Pathol 2007; 170:439-446. This work provides evidence for a link between endothelial cell cytoskeletal remodeling and regulation of proinflammatory gene expression in ALI.
8. Bogatcheva NV, Adyshev D, Mambetsariev B, et al. Involvement of microtubules, p38, and Rho kinases pathway in 2-methoxyestradiol-induced lung vascular barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 2007; 292:L487-L499.
9. Mirzapoiazova T, Kolosova IA, Moreno L, et al. Suppression of endotoxin-induced inflammation by taxol. Eur Respir J 2007; 30:429-435.
10. Su G, Hodnett M, Wu N, et al. Integrin alphavbeta5 regulates lung vascular permeability and pulmonary endothelial barrier function. Am J Respir Cell Mol Biol 2007; 36:377-386.
11. Lu Q, Harrington EO, Jackson H, et al. Transforming growth factor-beta1-induced endothelial barrier dysfunction involves Smad2-dependent p38 activation and subsequent RhoA activation. J Appl Physiol 2006; 101: 375-384.
12. Georgieva GS, Kurata S, Ikeda S, et al. Nonischemic lung injury by mediators from unilateral ischemic reperfused lung: ameliorating effect of tumor necrosis factor-alpha-converting enzyme inhibitor. Shock 2007; 27:84-90. This work demonstrates remote organ effects of TNF-α secreted from lungs undergoing ischemia/reperfusion.
13. Angelini DJ, Hyun SW, Grigoryev DN, et al. TNF-alpha increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am J Physiol Lung Cell Mol Physiol 2006; 291:L1232-L1245. Novel mechanism of endothelial cell barrier disruption by TNF-α.
14. 2+ influx from the extracellular space in endothelial cells, which induces permeability increases in ALI.
15. 2+-mediated spread of inflammatory signals along adjacent endothelial cells interconnected via gap junctions, thus propagating inflammation in ALI.
16. Chatterjee A, Dimitropoulou C, Drakopanayiotakis F, et al. Heat shock protein 90 inhibitors prolong survival, attenuate inflammation and reduce lung injury in murine sepsis. Am J Respir Crit Care Med 2007; 176:667-675. Work showing the protective effect of HSP-90 inhibitors in sepsis/ALI, bearing potential clinical implications.
17. Kim KS, Rajagopal V, Gonsalves C, et al. A novel role of hypoxia-inducible factor in cobalt chloride- and hypoxia-mediated expression of IL-8 chemokine in human endothelial cells. J Immunol 2006; 177:7211-7224.
18. Yoshida K, Kondo R, Wang Q, Doerschuk CM. Neutrophil cytoskeletal rearrangements during capillary sequestration in bacterial pneumonia in rats. Am J Respir Crit Care Med 2006; 174:689-698.
19. Perkowski S, Scherpereel A, Murciano JC, et al. Dissociation between alveolar transmigration of neutrophils and lung injury in hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006; 291:L1050-L1058.
20. Gao XP, Zhu X, Fu J, et al. Blockade of class IA phosphoinositide 3-kinase in neutrophils prevents NADPH oxidase activation- and adhesion-dependent inflammation. J Biol Chem 2007; 282:6116-6125. This work characterizes a molecular pathway of ROS production by TNF-α stimulated PMNs with implications on endothelial permeability.
21. Kiefmann R, Heckel K, Schenkat S, et al. Role of p-selectin in platelet sequestration in pulmonary capillaries during endotoxemia. J Vasc Res 2006; 43:473-481.
22. 2 secreted by complexes of platelet-PMN is critical in inducing vascular permeability and inflammation.
23. Khan SY, Kelher MR, Heal JM, et al. Soluble CD40 ligand accumulates in stored blood components, primes neutrophils through CD40, and is a potential cofactor in the development of transfusion-related acute lung injury. Blood 2006; 108:2455-2462. Soluble CD40 ligand-activated PMNs induce endothelial alterations in transfusion-related acute lung injury.
24. Pero RS, Borchers MT, Spicher K, et al. Galphai2-mediated signaling events in the endothelium are involved in controlling leukocyte extravasation. Proc Natl Acad Sci U S A 2007; 104:4371-4376. Insight in endothelial cell signaling pathways that regulate PMN transmigration.
25. Orrington-Myers J, Gao X, Kouklis P, et al. Regulation of lung neutrophil recruitment by VE-cadherin. Am J Physiol Lung Cell Mol Physiol 2006; 291:L764-L771. Vascular endothelial cadherin signaling regulates NF-κB activation and adhesion molecule expression.
26. Abdulnour RE, Peng X, Finigan JH, et al. Mechanical stress activates xanthine oxidoreductase through MAP kinase-dependent pathways. Am J Physiol Lung Cell Mol Physiol 2006; 291:L345-L353.
27. Flaishon R, Szold O, Weinbroum AA. Acute lung injury following pancreas ischaemia-reperfusion: role of xanthine oxidase. Eur J Clin Invest 2006; 36:831-837.
28. 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 2006; 281:35554-35566.
29. Silliman CC, Curtis BR, Kopko PM, et al. Donor antibodies to HNA-3a implicated in TRALI reactions prime neutrophils and cause PMN-mediated damage to human pulmonary microvascular endothelial cells in a two-event in vitro model. Blood 2007; 109:1752-1755. Transfusion-related acute lung injury requires a 'two-hit' model of preexisting endothelial cell stimulation followed by oxidant-mediated endothelial cell toxicity from PMNs activated by antibodies in donor blood.
30. Gorbunov NV, Das DK, Goswami SK, et al. Spatial coordination of cell-adhesion molecules and redox cycling of iron in the microvascular inflammatory response to pulmonary injury. Antioxid Redox Signal 2007; 9:483-495.
31. Adhikari NK, Burns KE, Friedrich JO, et al. Effect of nitric oxide on oxygenation and mortality in acute lung injury: systematic review and meta-analysis. BMJ 2007; 334:757-758. Most recent metaanalysis arguing against the routine use of inhaled nitric oxide in ALI/ARDS due to lack of clinical outcome improvement and potential renal toxicity.
32. Ader F, Le Berre R, Lancel S, et al. Inhaled nitric oxide increases endothelial permeability in Pseudomonas aeruginosa pneumonia. Intensive Care Med 2007; 33:503-510.
33. Shelton JL, Wang L, Cepinskas G, et al. Inducible NO synthase (iNOS) in human neutrophils but not pulmonary microvascular endothelial cells (PMVEC) mediates septic protein leak in vitro. Microvasc Res 2007; 74:23-31.
34. Shields CJ, Delaney CP, Winter DC, et al. Induction of nitric oxide synthase is a key determinant of progression to pulmonary injury in experimental pancreatitis. Surg Infect (Larchmt) 2006; 7:501-511.
35. He X, Han B, Mura M, et al. Angiotensin-converting enzyme inhibitor captopril prevents oleic acid-induced severe acute lung injury in rats. Shock 2007; 28:106-111.
36. Jerng JS, Hsu YC, Wu HD, et al. Role of the renin-angiotensin system in ventilator-induced lung injury: an in vivo study in a rat model. Thorax 2007; 62:527-535. This article demonstrates increased levels of angiotensin II in a rat VILI model and lung protection by ACE inhibition.
37. Jerng JS, Yu CJ, Wang HC, et al. Polymorphism of the angiotensin-converting enzyme gene affects the outcome of acute respiratory distress syndrome. Crit Care Med 2006; 34:1001-1006. This work shows that ACE D allele carriers have increased ARDS mortality.
38. Orfanos SE, Kotanidou A, Glynos C, et al. Angiopoietin-2 is increased in severe sepsis: correlation with inflammatory mediators. Crit Care Med 2007; 35:199-206.
39. McCarter SD, Mei SH, Lai PF, et al. Cell-based angiopoietin-1 gene therapy for acute lung injury. Am J Respir Crit Care Med 2007; 175:1014-1026. Skin fibroblasts genetically engineered to secrete high levels of angiopoietin-1 can be incorporated in lung vessel walls and confer protection against ALI.
40. Parikh SM, Mammoto T, Schultz A, et al. Excess circulating angiopoietin-2 may contribute to pulmonary vascular leak in sepsis in humans. PLoS Med 2006; 3:e46:0356-0370.
41. Bhandari V, Choo-Wing R, Lee CG, et al. Hyperoxia causes angiopoietin-2-mediated acute lung injury and necrotic cell death. Nat Med 2006; 12:1287-1293. Toxic effects of hyperoxia on lung tissue are mediated by angiopoietin-2 secretion.
42. Daly C, Pasnikowski E, Burova E, et al. Angiopoietin-2 functions as an autocrine protective factor in stressed endothelial cells. Proc Natl Acad Sci U S A 2006; 103:15491-15496. Evidence for the novel protective properties of angiopoietin-2.
43. Zheng X, Li W, Song Y, et al. Nonhematopoietic EPCR regulates the coagulation and inflammatory responses during endotoxemia. J Thromb Haemost 2007; 5:1394-1400. Endothelial protein C receptors on endothelial cells and not hematopoietic cells protect mice from sepsis-induced mortality and ALI.
44. Maybauer MO, Maybauer DM, Fraser JF, et al. Recombinant human activated protein C improves pulmonary function in ovine acute lung injury resulting from smoke inhalation and sepsis. Crit Care Med 2006; 34:2432-2438.
45. Kotanidou A, Loutrari H, Papadomichelakis E, et al. Inhaled activated protein C attenuates lung injury induced by aerosolized endotoxin in mice. Vascul Pharmacol 2006; 45:134-140. This work shows the protective effect of APC topical administration in a model of direct ALI, by influencing endothelial cell-PMN interactions.
46. Slofstra SH, Groot AP, Maris NA, et al. Inhalation of activated protein C inhibits endotoxin-induced pulmonary inflammation in mice independent of neutrophil recruitment. Br J Pharmacol 2006; 149:740-746. This work offers evidence on the protective effect of topical administration of APC in a model of direct ALI via PMN-independent pathway(s).
47. Kendirli T, Ciftç E, Ince E, et al. Homozygous 23-bp insertion of endothelial protein C receptor gene in a child with fatal sepsis. Pediatr Hematol Oncol 2007; 24:199-204. A case reporting a mutation of the endothelial protein C receptor possibly associated with poor outcome.
48. Papaiahgari S, Yerrapureddy A, Hassoun PM, et al. EGFR-activated signaling and actin remodeling regulate cyclic stretch-induced NRF2-ARE activation. Am J Respir Cell Mol Biol 2007; 36:304-312.
49. Marzec JM, Christie JD, Reddy SP, et al. Functional polymorphisms in the transcription factor NRF2 in humans increase the risk of acute lung injury. FASEB J 2007; 21:2237-2246. Genetic polymorphism in the NRF2 promoter increases the risk of ALI in trauma patients.
50. Nowak K, Weih S, Metzger R, et al. Immunotargeting of catalase to lung endothelium via antiangiotensin-converting enzyme antibodies attenuates ischemia-reperfusion injury of the lung in vivo. Am J Physiol Lung Cell Mol Physiol 2007; 293:L162-L169. This work describes a novel approach to concentrate catalase on lung endothelial cells by conjugating it to antibodies against ACE.
51. McClintock DE, Ware LB, Eisner MD, et al. Higher urine nitric oxide is associated with improved outcomes in patients with acute lung injury. Am J Respir Crit Care Med 2007; 175:256-262. Unexpected finding that ALI patients with higher nitric oxide levels have better outcomes.
52. Garrean S, Gao XP, Brovkovych V, et al. Caveolin-1 regulates NF-kappaB activation and lung inflammatory response to sepsis induced by lipopolysaccharide. J Immunol 2006; 177:4853-4860. Excess eNOS-derived nitric oxide is protective in septic ALI in mice.
53. Yoshimura S, Nishimura Y, Nishiuma T, et al. Overexpression of nitric oxide synthase by the endothelium attenuates bleomycin-induced lung fibrosis and impairs MMP-9/TIMP-1 balance. Respirology 2006; 11:546-556. This work shows that transgenic endothelial cell-specific eNOS expression counteracts the effects of bleomycin.
54. Kaminski A, Kasch C, Zhang L, et al. Endothelial nitric oxide synthase mediates protective effects of hypoxic preconditioning in lungs. Respir Physiol Neurobiol 2007; 155:280-285.
55. •] offer information on the endothelial cell protective actions of carbon monoxide in hyperoxia.
56. •] offer information on the endothelial cell protective actions of carbon monoxide in hyperoxia.
57. •] offer information on the endothelial cell protective actions of carbon monoxide in hyperoxia.
58. Sun B, Sun H, Liu C, et al. Role of CO-releasing molecules liberated CO in attenuating leukocytes sequestration and inflammatory responses in the lung of thermally injured mice. J Surg Res 2007; 139:128-135. This work provides in-vivo evidence for the beneficial effect of carbon monoxide donors in ALI induced by burns.
59. Eckle T, Füllbier L, Wehrmann M, et al. Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J Immunol 2007; 178:8127-8137. Adenosine produced by enzymes CD39 and CD73 protects mice from ALI.
60. Heller AR, Rothermel J, Weigand MA, et al. Adenosine A1 and A2 receptor agonists reduce endotoxin-induced cellular energy depletion and oedema formation in the lung. Eur J Anaesthesiol 2007; 24:258-266.
61. Rivo J, Zeira E, Galun E, et al. Attenuation of reperfusion lung injury and apoptosis by A2A adenosine receptor activation is associated with modulation of Bcl-2 and Bax expression and activation of extracellular signal-regulated kinases. Shock 2007; 27:266-273.
62. Birukova AA, Zagranichnaya T, Fu P, Alekseeva E, et al. Prostaglandins PGE(2) and PGI(2) promote endothelial barrier enhancement via PKA and Epac1/Rap1-dependent Rac activation. Exp Cell Res 2007; 313:2504-2520.
63. Birukova AA, Malyukova I, Poroyko V, Birukov KG. Paxillin-beta-catenin interactions are involved in Rac/Cdc42-mediated endothelial barrier-protective response to oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol 2007; 293:L199-L211. Oxidized phospholipids are compounds which promote sealing of endothelial junctions and enhance the endothelial barrier tightness.
64. Birukova AA, 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 2007; 292:L924-L935.
65. Okazaki M, Kreisel F, Richardson SB, et al. Sphingosine 1-phosphate inhibits ischemia reperfusion injury following experimental lung transplantation. Am J Transplant 2007; 7:751-758.
66. Zhao YY, Gao XP, Zhao YD, et al. Endothelial cell-restricted disruption of FoxM1 impairs endothelial repair following LPS-induced vascular injury. J Clin Invest 2006; 116:2333-2343. Sepsis induces lung endothelial cell apoptosis; subsequent proliferation of surviving endothelial cells, dependent on transcription factor FoxM1, is essential to recovery from ALI.
67. Kunig AM, Balasubramaniam V, Markham NE, et al. Recombinant human VEGF treatment transiently increases lung edema but enhances lung structure after neonatal hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006; 291:L1068-L1078. Exogenous VEGF increases permeability but restores vascular development in neonatal hyperoxia.
68. Quadri SK, Bhattacharya J. Resealing of endothelial junctions by focal adhesion kinase. Am J Physiol Lung Cell Mol Physiol 2007; 292:L334-L342.
69. Kinniry P, Pick J, Stephens S, et al. KL4-surfactant prevents hyperoxic and LPS-induced lung injury in mice. Pediatr Pulmonol 2006; 41:916-928. Surfactant component KL(4) from epithelial cells protects endothelial cells in endotoxemic mice.