Induction of cellular antioxidant defense by amifostine improves ventilator-induced lung injury

Critical Care Medicine

Volumn 39, Issue 12, 2011, Pages 2711-2721

  Fu, Panfeng ^a   Murley, Jeffrey S ^b   Grdina, David J ^b   Birukova, Anna A ^a   Birukov, Konstantin G ^a  

^a Department of Medicine   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

endothelium; reactive oxygen species; superoxide dismutase 2; ventilator induced lung injury

Indexed keywords

AMIFOSTINE; CATALASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; OXIDOREDUCTASE; SUPEROXIDE DISMUTASE; THROMBIN;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; ARTIFICIAL VENTILATION; C57BL 6 MOUSE; CELL CULTURE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG FUNCTION; LUNG LAVAGE; LUNG PARENCHYMA; MOUSE; NEWBORN INTENSIVE CARE NURSING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; TIDAL VOLUME; VENTILATOR INDUCED LUNG INJURY;

AMIFOSTINE; ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; ENDOTHELIUM; FREE RADICAL SCAVENGERS; INFLAMMATION; LUNG; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; VENTILATOR-INDUCED LUNG INJURY;

EID: 81855176160     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0b013e3182284a5f     Document Type: Article

References (71)

1. Rubenfeld GD, Caldwell E, Peabody E, et al: Incidence and outcomes of acute lung injury. N Engl J Med 2005; 353:1685-1693 (Pubitemid 41464707)
2. Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med 2000; 342: 1334-1349 (Pubitemid 30408719)
3. Ranieri VM, Suter PM, Tortorella C, et al: Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: A randomized controlled trial. JAMA 1999; 282:54-61 (Pubitemid 29318933)
4. Tremblay L, Valenza F, Ribeiro SP: Injurious ventilatory strategies increase cytokines and c-fos m-RNA expression in an isolated rat lung model. J Clin Invest 1997; 99:944-952 (Pubitemid 27123631)
5. Villar J, Flores C, Mendez-Alvarez S: Genetic susceptibility to acute lung injury. Crit Care Med 2003; 31(Suppl 4):S272-S275 (Pubitemid 36458179)
6. Nonas S, Birukova AA, Fu P, et al: Oxidized phospholipids reduce ventilator-induced vascular leak and inflammation in vivo. Crit Care 2008; 12:R27
7. Quinn DA, Moufarrej RK, Volokhov A, et al: Interactions of lung stretch, hyperoxia, and MIP-2 production in ventilator-induced lung injury. J Appl Physiol 2002; 93:517-525 (Pubitemid 34810213)
8. Finigan JH, Boueiz A, Wilkinson E, et al: Activated protein C protects against ventilator-induced pulmonary capillary leak. Am J Physiol Lung Cell Mol Physiol 2009; 296: L1002-L10011
9. Boueiz A, Hassoun PM: Regulation of endothelial barrier function by reactive oxygen and nitrogen species. Microvasc Res 2009; 77:26-34
10. Tasaka S, Amaya F, Hashimoto S, et al: Roles of oxidants and redox signaling in the pathogenesis of acute respiratory distress syndrome. Antioxid Redox Signal 2008; 10: 739-753 (Pubitemid 351225899)
11. Ali MH, Pearlstein DP, Mathieu CE, et al: Mitochondrial requirement for endothelial responses to cyclic strain: implications for mechanotransduction. Am J Physiol Lung Cell Mol Physiol 2004; 287:L486-L4896
12. Grote K, Flach I, Luchtefeld M, et al: Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidasederived reactive oxygen species. Circ Res 2003; 92:e80-e86
13. 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 (Pubitemid 44343709)
14. Chapman KE, Sinclair SE, Zhuang D, et al: Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 2005; 289:L834-L841 (Pubitemid 41504415)
15. Chess PR, Toia L, Finkelstein JN: Mechanical strain-induced proliferation and signaling in pulmonary epithelial H441 cells. Am J Physiol Lung Cell Mol Physiol 2000; 279: L43-L51 (Pubitemid 30619522)
16. 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 (Pubitemid 46365281)
17. Birukov KG: Cyclic stretch, reactive oxygen species and vascular remodeling. Antioxid Redox Signal 2009; 11:1651-1667
18. Comhair SA, Erzurum SC: Antioxidant responses to oxidant-mediated lung diseases. Am J Physiol Lung Cell Mol Physiol 2002; 283:L246-L255 (Pubitemid 34803980)
19. Comhair SA, Xu W, Ghosh S, et al: Superoxide dismutase inactivation in pathophysiology of asthmatic airway remodeling and reactivity. Am J Pathol 2005; 166:663-674 (Pubitemid 40315624)
20. Epperly MW, Epstein CJ, Travis EL, et al: Decreased pulmonary radiation resistance of manganese superoxide dismutase (MnSOD)-deficient mice is corrected by human manganese superoxide dismutase-plasmid/liposome (SOD2-PL) intratracheal gene therapy. Radiat Res 2000; 154:365-374
21. Asikainen TM, Huang TT, Taskinen E, et al: Increased sensitivity of homozygous Sod2 mutant mice to oxygen toxicity. Free Radic Biol Med 2002; 32:175-186 (Pubitemid 34127708)
22. Arita Y, Harkness SH, Kazzaz JA, et al: Mitochondrial localization of catalase provides optimal protection from H2O2-induced cell death in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006; 290:L978-L986 (Pubitemid 43725060)
23. Nowak K, Weih S, Metzger R, et al: Immunotargeting of catalase to lung endothelium via anti-angiotensin-converting enzyme antibodies attenuates ischemia-reperfusion injury of the lung in vivo. Am J Physiol Lung Cell Mol Physiol 2007; 293:L162-L119
24. Smoluk GD, Fahey RC, Calabro-Jones PM, et al: Radioprotection of cells in culture by WR-2721 and derivatives: Form of the drug responsible for protection. Cancer Res 1988; 48:3641-3647
25. Brizel DM, Wasserman TH, Henke M, et al: Phase III randomized trial of amifostine as a radioprotector in head and neck cancer. J Clin Oncol 2000; 18:3339-3345
26. Fu P, Birukova AA, Xing J, et al: Amifostine reduces lung vascular permeability via suppression of inflammatory signalling. Eur Respir J 2009; 33:612-624
27. Grdina DJ, Murley JS, Kataoka Y, et al: Amifostine induces antioxidant enzymatic activities in normal tissues and a transplantable tumor that can affect radiation response. Int J Radiat Oncol Biol Phys 2009; 73:886-896
28. Dragojevic-Simic VM, Dobric SL, Bokonjic DR, et al: Amifostine protection against doxorubicin cardiotoxicity in rats. Anticancer Drugs 2004; 15:169-178 (Pubitemid 38316751)
29. Birukova AA, Fu P, Xing J, et al: Rap1 mediates protective effects of iloprost against ventilator induced lung injury. J Appl Physiol 2009; 107:1900-1910
30. Birukova AA, Fu P, Xing J, et al: Mechanotransduction by GEF-H1 as a novel mechanism of ventilator-induced vascular endothelial permeability. Am J Physiol Lung Cell Mol Physiol 2010; 298:L837-L848
31. Singleton PA, Chatchavalvanich S, Fu P, et al: Akt-mediated transactivation of the S1P1 receptor in caveolin-enriched microdomains regulates endothelial barrier enhancement by oxidized phospholipids. Circ Res 2009; 104:978-986
32. Nonas SA, Miller I, Kawkitinarong K, et al: Oxidized phospholipids reduce vascular leak and inflammation in rat model of acute lung injury. Am J Respir Crit Care Med 2006; 173:1130-1138 (Pubitemid 43726894)
33. Birukova AA, Fu P, Xing J, et al: Lung endothelial barrier protection by iloprost in the 2-hit models of ventilator-induced lung injury (VILI) involves inhibition of Rho signaling. Transl Res 2010; 155:44-54
34. Moitra J, Sammani S, Garcia JG: Reevaluation of Evans Blue dye as a marker of albumin clearance in murine models of acute lung injury. Transl Res 2007; 150:253-265 (Pubitemid 47444609)
35. Birukov KG, Jacobson JR, Flores AA, et al: Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol Lung Cell Mol Physiol 2003; 285:L785-L797 (Pubitemid 37158824)
36. Birukova AA, Rios A, Birukov KG: Long-term cyclic stretch controls pulmonary endothelial permeability at translational and posttranslational levels. Exp Cell Res 2008; 314: 3466-3477
37. Birukova AA, Chatchavalvanich S, Rios A, et al: Differential regulation of pulmonary endothelial monolayer integrity by varying degrees of cyclic stretch. Am J Pathol 2006; 168:1749-1761
38. Birukova AA, Moldobaeva N, Xing J, et al: Magnitude-dependent effects of cyclic stretch on HGF-and VEGF-induced pulmonary endothelial remodeling and barrier regulation. Am J Physiol Lung Cell Mol Physiol 2008; 295:L612-L623
39. Reddy SP, Hassoun PM, Brower R: Redox imbalance and ventilator-induced lung injury. Antioxid Redox Signal 2007; 9:2003-2012 (Pubitemid 47628604)
40. Matthay MA, Zimmerman GA, Esmon C, et al: Future research directions in acute lung injury: Summary of a National Heart, Lung, and Blood Institute working group. Am J Respir Crit Care Med 2003; 167:1027-1035 (Pubitemid 36408170)
41. Ichimura H, Parthasarathi K, Quadri S, et al: Mechano-oxidative coupling by mitochondria induces proinflammatory responses in lung venular capillaries. J Clin Invest 2003; 111:691-699 (Pubitemid 36278587)
42. Ali MH, Mungai PT, Schumacker PT: Stretch-induced phosphorylation of focal adhesion kinase in endothelial cells: Role of mitochondrial oxidants. Am J Physiol Lung Cell Mol Physiol 2006; 291:L38-L45
43. Chandel NS, Budinger GR: The cellular basis for diverse responses to oxygen. Free Radic Biol Med 2007; 42:165-174 (Pubitemid 44970533)
44. Goldberg PL, MacNaughton DE, Clements RT, et al: p38 MAPK activation by TGF-beta1 increases MLC phosphorylation and endothelial monolayer permeability. Am J Physiol Lung Cell Mol Physiol 2002; 282:L146-L154 (Pubitemid 34654191)
45. Kevil CG, Oshima T, Alexander JS: The role of p38 MAP kinase in hydrogen peroxide mediated endothelial solute permeability. Endothelium 2001; 8:107-116 (Pubitemid 32821322)
46. Niwa K, Inanami O, Ohta T, et al: p38 MAPK and Ca2+ contribute to hydrogen peroxideinduced increase of permeability in vascular endothelial cells but ERK does not. Free Radic Res 2001; 35:519-527 (Pubitemid 33133588)
47. Shaw LM, Bonner HS, Schuchter L, et al: Pharmacokinetics of amifostine: Effects of dose and method of administration. Semin Oncol 1999; 26(Suppl 7):34-36 (Pubitemid 29246627)
48. Fan M, Ahmed KM, Coleman MC, et al: Nuclear factor-kappaB and manganese superoxide dismutase mediate adaptive radioresistance in low-dose irradiated mouse skin epithelial cells. Cancer Res 2007; 67: 3220-3228 (Pubitemid 46724860)
49. Murley JS, Kataoka Y, Hallahan DE, et al: Activation of NFkappaB and MnSOD gene expression by free radical scavengers in human microvascular endothelial cells. Free Radic Biol Med 2001; 30:1426-1439 (Pubitemid 32522958)
50. Murley JS, Kataoka Y, Weydert CJ, et al: Delayed cytoprotection after enhancement of Sod2 (MnSOD) gene expression in SA-NH mouse sarcoma cells exposed to WR-1065, the active metabolite of amifostine. Radiat Res 2002; 158:101-109 (Pubitemid 34728917)
51. Xu Y, Kiningham KK, Devalaraja MN, et al: An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factor-alpha and interleukin-1beta. DNA Cell Biol 1999; 18:709-722 (Pubitemid 29439223)
52. Kops GJ, Dansen TB, Polderman PE, et al: Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002; 419:316-321
53. Murley JS, Kataoka Y, Cao D, et al: Delayed radioprotection by NFkappaB-mediated induction of Sod2 (MnSOD) in SA-NH tumor cells after exposure to clinically used thiolcontaining drugs. Radiat Res 2004; 162: 536-546 (Pubitemid 39600542)
54. Matthews JR, Wakasugi N, Virelizier JL, et al: Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 1992; 20:3821-3830
55. Kataoka Y, Murley JS, Khodarev NN, et al: Activation of the nuclear transcription factor kappaB (NFkappaB) and differential gene expression in U87 glioma cells after exposure to the cytoprotector amifostine. Int J Radiat Oncol Biol Phys 2002; 53:180-189 (Pubitemid 34465823)
56. Grdina DJ, Kataoka Y, Murley JS, et al: Antimetastatic effectiveness of amifostine therapy following surgical removal of Sa-NH tumors in mice. Semin Oncol. 2002; 29 (Suppl 19):22-28 (Pubitemid 36173242)
57. Koukourakis MI, Giatromanolaki A, Chong W, et al: Amifostine induces anaerobic metabolism and hypoxia-inducible factor 1 alpha. Cancer Chemother Pharmacol 2004; 53:8-14 (Pubitemid 38161183)
58. Dedieu S, Canron X, Rezvani HR, et al: The cytoprotective drug amifostine modifies both expression and activity of the pro-angiogenic factor VEGF-A. BMC Med 2010; 8:19
59. Mura M, Han B, Andrade CF, et al: The early responses of VEGF and its receptors during acute lung injury: implication of VEGF in alveolar epithelial cell survival. Crit Care 2006; 10:R130
60. Karmpaliotis D, Kosmidou I, Ingenito EP, et al: Angiogenic growth factors in the pathophysiology of a murine model of acute lung injury. Am J Physiol Lung Cell Mol Physiol 2002; 283:L585-L595
61. Vlahakis NE, Hubmayr RD: Invited review: Plasma membrane stress failure in alveolar epithelial cells. J Appl Physiol 2000; 89: 2490-2496
62. Frank JA, Matthay MA: Science review: Mechanisms of ventilator-induced injury. Crit Care 2003; 7:233-241 (Pubitemid 36748885)
63. Schultz MJ, Haitsma JJ, Zhang H, et al: Pulmonary coagulopathy as a new target in therapeutic studies of acute lung injury or pneumonia-A review. Crit Care Med 2006; 34:871-877
64. Maniatis NA, Kotanidou A, Catravas JD, et al: Endothelial pathomechanisms in acute lung injury. Vascul Pharmacol 2008; 49:119-133
65. Yun JK, Anderson JM, Ziats NP: Cyclicstrain-induced endothelial cell expression of adhesion molecules and their roles in monocyte-endothelial interaction. J Biomed Mater Res 1999; 44:87-97
66. Cheng JJ, Wung BS, Chao YJ, Wang DL: Cyclic strain-induced reactive oxygen species involved in ICAM-1 gene induction in endothelial cells. Hypertension 1998; 31: 125-130 (Pubitemid 28124704)
67. Metzler SA, Pregonero CA, Butcher JT, et al: Cyclic strain regulates pro-inflammatory protein expression in porcine aortic valve endothelial cells. J Heart Valve Dis 2008; 17:571-577
68. Birukova AA, Burdette D, Moldobaeva N, et al: Rac GTPase is a hub for protein kinase A and Epac signaling in endothelial barrier protection by cAMP. Microvasc Res 2010; 79: 128-138
69. Waters CM: Reactive oxygen species in mechanotransduction. Am J Physiol Lung Cell Mol Physiol 2004; 287:L484-L485 (Pubitemid 39095902)
70. Birukov KG, Bochkov VN, Birukova AA, et al: Epoxycyclopentenone- containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res 2004; 95:892-901 (Pubitemid 39435004)
71. Kouklis P, Konstantoulaki M, Vogel S, et al: Cdc42 regulates the restoration of endothelial barrier function. Circ Res 2004; 94: 159-166 (Pubitemid 38197447)