Angiopoietin-1 treatment reduces inflammation but does not prevent ventilator-induced lung injury

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Hegeman, Maria A ^a   Hennus, Marije P ^a   van Meurs, Matijs ^b   Cobelens, Pieter M ^a   Kavelaars, Annemieke ^a   Jansen, Nicolaas J ^a   Schultz, Marcus J ^c   van Vught, Adrianus J ^a   Molema, Grietje ^b   Heijnen, Cobi J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; INTERLEUKIN 1BETA; KERATINOCYTE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE B; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ARTIFICIAL VENTILATION; CAPILLARY PERMEABILITY; CELL INFILTRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG DOSE COMPARISON; GAS EXCHANGE; GRANULOCYTE; INFLAMMATORY INFILTRATE; LUNG EDEMA; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIDAL VOLUME; VENTILATOR INDUCED LUNG INJURY; ANIMAL; BLOOD GAS ANALYSIS; C57BL MOUSE; CYTOLOGY; HEMODYNAMICS; HUMAN; INFLAMMATION; KERATINOCYTE; LUNG INJURY; METABOLISM; PHOSPHORYLATION;

ANIMALIA; MUS;

ANGIOPOIETIN-1; ANIMALS; BLOOD GAS ANALYSIS; GRANULOCYTES; HEMODYNAMICS; HUMANS; INFLAMMATION; KERATINOCYTES; LUNG INJURY; MALE; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; RECEPTOR, TIE-2; VENTILATOR-INDUCED LUNG INJURY;

EID: 78650763375     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015653     Document Type: Article

References (43)

1. Dreyfuss D, Saumon G (1998) Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 157: 294-323.
2. Slutsky AS (1999) Lung injury caused by mechanical ventilation. Chest 116: 9S-15S.
3. Parker JC, Hernandez LA, Peevy KJ (1993) Mechanisms of ventilator-induced lung injury. Crit Care Med 21: 131-143.
4. Dreyfuss D, Basset G, Soler P, Saumon G (1985) Intermittent positive-pressure hyperventilation with high inflation pressures produces pulmonary microvascular injury in rats. Am Rev Respir Dis 132: 880-884.
5. Egan EA (1982) Lung inflation, lung solute permeability, and alveolar edema. J Appl Physiol 53: 121-125.
6. Parker JC, Townsley MI, Rippe B, Taylor AE, Thigpen J (1984) Increased microvascular permeability in dog lungs due to high peak airway pressures. J Appl Physiol 57: 1809-1816.
7. Tremblay LN, Slutsky AS (1998) Ventilator-induced injury: from barotrauma to biotrauma. Proc Assoc Am Physicians 110: 482-488.
8. Vreugdenhil HA, Heijnen CJ, Plotz FB, Zijlstra J, Jansen NJ, et al. (2004) Mechanical ventilation of healthy rats suppresses peripheral immune function. Eur Respir J 23: 122-128.
9. Pugin J (2003) Molecular mechanisms of lung cell activation induced by cyclic stretch. Crit Care Med 31: S200-S206.
10. Fiedler U, Augustin HG (2006) Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol 27: 552-558.
11. van der Heijden M, van Nieuw Amerongen GP, Chedamni S, van Hinsbergh VW, Groeneveld AB (2009) The angiopoietin-Tie2 system as a therapeutic target in sepsis and acute lung injury. Expert Opin Ther Targets 13: 39-53.
12. Fiedler U, Reiss Y, Scharpfenecker M, Grunow V, Koidl S, et al. (2006) Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation. Nat Med 12: 235-239.
13. Daly C, Pasnikowski E, Burova E, Wong V, Aldrich TH, et al. (2006) Angiopoietin-2 functions as an autocrine protective factor in stressed endothelial cells. Proc Natl Acad Sci U S A 103: 15491-15496.
14. Karmpaliotis D, Kosmidou I, Ingenito EP, Hong K, Malhotra A, et al. (2002) Angiogenic growth factors in the pathophysiology of a murine model of acute lung injury. Am J Physiol Lung Cell Mol Physiol 283: L585-L595.
15. Huang YQ, Sauthoff H, Herscovici P, Pipiya T, Cheng J, et al. (2008) Angiopoietin-1 increases survival and reduces the development of lung edema induced by endotoxin administration in a murine model of acute lung injury. Crit Care Med 36: 262-267.
16. McCarter SD, Mei SH, Lai PF, Zhang QW, Parker CH, et al. (2007) Cell-based angiopoietin-1 gene therapy for acute lung injury. Am J Respir Crit Care Med 175: 1014-1026.
17. Mei SH, McCarter SD, Deng Y, Parker CH, Liles WC, et al. (2007) Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med 4: e269.
18. Witzenbichler B, Westermann D, Knueppel S, Schultheiss HP, Tschope C (2005) Protective role of angiopoietin-1 in endotoxic shock. Circulation 111: 97-105.
19. van Meurs M, Kumpers P, Ligtenberg JJ, Meertens JH, Molema G, et al. (2009) Bench-to-bedside review: Angiopoietin signalling in critical illness-a future target? Crit Care 13: 207.
20. Wolthuis EK, Vlaar AP, Choi G, Roelofs JJ, Juffermans NP, et al. (2009) Mechanical ventilation using non-injurious ventilation settings causes lung injury in the absence of pre-existing lung injury in healthy mice. Crit Care 13: R1.
21. Simoes DC, Vassilakopoulos T, Toumpanakis D, Petrochilou K, Roussos C, et al. (2008) Angiopoietin-1 protects against airway inflammation and hyperreactivity in asthma. Am J Respir Crit Care Med 177: 1314-1321.
22. Hegeman MA, Hennus MP, Heijnen CJ, Specht PA, Lachmann B, et al. (2009) Ventilator-induced endothelial activation and inflammation in the lung and distal organs. Crit Care 13: R182.
23. Nijboer CH, Groenendaal F, Kavelaars A, Hagberg HH, van Bel F, et al. (2007) Gender-specific neuroprotection by 2-iminobiotin after hypoxia-ischemia in the neonatal rat via a nitric oxide independent pathway. J Cereb Blood Flow Metab 27: 282-292.
24. Hamanaka K, Jian MY, Weber DS, Alvarez DF, Townsley MI, et al. (2007) TRPV4 initiates the acute calcium-dependent permeability increase during ventilator-induced lung injury in isolated mouse lungs. Am J Physiol Lung Cell Mol Physiol 293: L923-L932.
25. Belperio JA, Keane MP, Burdick MD, Londhe V, Xue YY, et al. (2002) Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilatorinduced lung injury. J Clin Invest 110: 1703-1716.
26. Copland IB, Martinez F, Kavanagh BP, Engelberts D, McKerlie C, et al. (2004) High tidal volume ventilation causes different inflammatory responses in newborn versus adult lung. Am J Respir Crit Care Med 169: 739-748.
27. Haitsma JJ, Uhlig S, Verbrugge SJ, Goggel R, Poelma DL, et al. (2003) Injurious ventilation strategies cause systemic release of IL-6 and MIP-2 in rats in vivo. Clin Physiol Funct Imaging 23: 349-353.
28. Wilson MR, Choudhury S, Goddard ME, O'Dea KP, Nicholson AG, et al. (2003) High tidal volume upregulates intrapulmonary cytokines in an in vivo mouse model of ventilator-induced lung injury. J Appl Physiol 95: 1385-1393.
29. Wilson MR, Choudhury S, Takata M (2005) Pulmonary inflammation induced by high-stretch ventilation is mediated by tumor necrosis factor signaling in mice. Am J Physiol Lung Cell Mol Physiol 288: L599-L607.
30. Kim I, Kim HG, So JN, Kim JH, Kwak HJ, et al. (2000) Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 39-Kinase/ Akt signal transduction pathway. Circ Res 86: 24-29.
31. Papapetropoulos A, Fulton D, Mahboubi K, Kalb RG, O'Connor DS, et al. (2000) Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J Biol Chem 275: 9102-9105.
32. Kuebler WM, Uhlig U, Goldmann T, Schael G, Kerem A, et al. (2003) Stretch activates nitric oxide production in pulmonary vascular endothelial cells in situ. Am J Respir Crit Care Med 168: 1391-1398.
33. Uhlig U, Fehrenbach H, Lachmann RA, Goldmann T, Lachmann B, et al. (2004) Phosphoinositide 3-OH kinase inhibition prevents ventilation-induced lung cell activation. Am J Respir Crit Care Med 169: 201-208.
34. Daly C, Wong V, Burova E, Wei Y, Zabski S, et al. (2004) Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev 18: 1060-1071.
35. Bhatia M, Moochhala S (2004) Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J Pathol 202: 145-156.
36. Lemieux C, Maliba R, Favier J, Theoret JF, Merhi Y, et al. (2005) Angiopoietins can directly activate endothelial cells and neutrophils to promote proinflammatory responses. Blood 105: 1523-1530.
37. Murdoch C, Tazzyman S, Webster S, Lewis CE (2007) Expression of Tie-2 by human monocytes and their responses to angiopoietin-2. J Immunol 178: 7405-7411.
38. Lee KS, Park HS, Park SJ, Kim SR, Min KH, et al. (2005) A prodrug of cysteine, L-2-oxothiazolidine-4-carboxylic acid, regulates vascular permeability by reducing vascular endothelial growth factor expression in asthma. Mol Pharmacol 68: 1281-1290.
39. Nin N, Lorente JA, de Paula M, El Assar M, Vallejo S, et al. (2008) Rats surviving injurious mechanical ventilation show reversible pulmonary, vascular and inflammatory changes. Intensive Care Med 34: 948-956.
40. Thurston G, Suri C, Smith K, McClain J, Sato TN, et al. (1999) Leakageresistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 286: 2511-2514.
41. Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, et al. (2000) Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 6: 460-463.
42. Weppler A, Issekutz AC (2008) Alveolar epithelium down-modulates endotoxinbut not tumor necrosis factor alpha-induced activation of endothelium and selectively inhibits neutrophil transendothelial migration. Exp Lung Res 34: 425-453.
43. Wolthuis EK, Vlaar AP, Choi G, Roelofs JJ, Haitsma JJ, et al. (2009) Recombinant human soluble tumor necrosis factor-alpha receptor fusion protein partly attenuates ventilator-induced lung injury. Shock 31: 262-266.