Preconditioning by inhaled nitric oxide prevents hyperoxic and ischemia/reperfusion injury in rat lungs

Pulmonary Pharmacology and Therapeutics

Volumn 21, Issue 2, 2008, Pages 418-429

  Waldow, Thomas ^a   Witt, Wolfgang ^a   Ulmer, André ^a   Janke, Andreas ^a   Alexiou, Konstantin ^a   Matschke, Klaus ^a  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

Glycogen synthase kinase; Hyperoxia; Lung permeability; Mitogen activated protein kinases; Nitric oxide; Preconditioning; Protein kinase B

Indexed keywords

CYCLIC GMP; EVANS BLUE; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOPEROXIDASE; NITRIC OXIDE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL OXYGEN TENSION; ARTICLE; CELL INVASION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HYPEROXIA; ISCHEMIA; LEUKOCYTE; LUNG DISEASE; LUNG FUNCTION; LUNG ISCHEMIA; MALE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REPERFUSION INJURY; SPRAGUE DAWLEY RAT;

ADMINISTRATION, INHALATION; ANIMALS; CAPILLARY PERMEABILITY; CYCLIC GMP; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASES; HYPEROXIA; ISCHEMIA; ISCHEMIC PRECONDITIONING; LUNG; MALE; MAP KINASE SIGNALING SYSTEM; NITRIC OXIDE; PROTO-ONCOGENE PROTEINS C-AKT; PULMONARY GAS EXCHANGE; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

EID: 39749186606     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2007.10.005     Document Type: Article

References (69)

1. de Perrot M., Liu M., Waddell T.K., and Keshavjee S. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med 167 (2003) 490-511
2. Ng C.S.H., Wan S., Arifi A.A., and Yim A.P.C. Inflammatory response to pulmonary ischemia-reperfusion injury. Surg Today 36 (2006) 205-214
3. Seal J.B., and Gewertz B.L. Vascular dysfunction in ischemia-reperfusion injury. Ann Vasc Surg 19 (2005) 572-584
4. Lee P.J., and Choi A.M.K. Pathways of cell signaling in hyperoxia. Free Radic Biol Med 35 (2003) 341-350
5. Altemeier W.A., and Sinclair S.E. Hyperoxia in the intensive care unit: why more is not always better. Curr Opin Crit Care 13 (2007) 73-78
6. Ryter S.W., Kim H.P., Hoetzel A., Park J.W., Nakahira K., Wang X., et al. Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9 (2007) 49-89
7. Murry C.E., Jennings R.B., and Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74 (1986) 1124-1136
8. Pasupathy S., and Homer-Vanniasinkam S. Ischaemic preconditioning protects against ischaemia/reperfusion injury: emerging concepts. Eur J Vasc Endovasc Surg 29 (2005) 106-115
9. Downey J.M., Davis A.M., and Cohen M.V. Signaling pathways in ischemic preconditioning. Heart Fail Rev 12 (2007) 181-188
10. Cohen M.V., Yang X.M., and Downey J.M. Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies. Cardiovasc Res 70 (2006) 231-239
11. Fujino S., Nagahiro I., Triantafillou A.N., Boasquevisque C.H., Yano M., Cooper J.D., et al. Inhaled nitric oxide at the time of harvest early lung allograft function. Ann Thorac Surg 63 (1997) 1383-1390
12. Guery B., Neviere R., Viget N., Foucher C., Fialdes P., Wattel F., et al. Inhaled NO preadministration modulates local and remote ischemia-reperfusion organ injury in a rat model. J Appl Physiol 87 (1999) 47-53
13. Schütte H., Witzenrath M., Mayer K., Rosseau S., Seeger W., and Grimminger F. Short-term "preconditioning" with inhaled nitric oxide protects rabbit lungs against ischemia-reperfusion injury. Transplantation 72 (2001) 1363-1370
14. Gómez C.B., del Valle H.F., Bertolotti A., Negroni J.A., Cuniberti L., Martínez V., et al. Effects of short-term inhaled nitric oxide on interleukin-8 release after single-lung transplantation in pigs. J Heart Lung Transplant 24 (2005) 714-722
15. Jheon S., Lee Y.M., Sung S.W., Choh J.H., Kwon K.Y., Keum D.Y., et al. Pulmonary preservation effect of nitroglycerine in isolated rat lung reperfusion model. Transplant Proc 36 (2004) 1933-1935
16. Waldow T., Alexiou K., Witt W., Wagner F.M., Kappert U., Knaut M., et al. Protection of lung tissue against ischemia/reperfusion injury by preconditioning with inhaled nitric oxide in an in situ pig model of normothermic pulmonary ischemia. Nitric Oxide 10 (2004) 195-201
17. Waldow T., Alexiou K., Witt W., Wagner F.M., Gulielmos V., Matschke K., et al. Attenuation of reperfusion-induced systemic inflammation by preconditioning with nitric oxide in an in situ porcine model of normothermic lung ischemia. Chest 125 (2004) 2253-2259
18. Takano H., Tang X.L., Qiu Y., Guo Y., French B.A., and Bolli R. Nitric oxide donors induce late preconditioning against myocardial stunning and infarction in conscious rabbits via an antioxidant-sensitive mechanism. Circ Res 83 (1998) 73-84
19. Hill M., Takano H., Tang X.L., Kodani E., Shirk G., and Bolli R. Nitroglycerin induces late preconditioning against myocardial infarction in conscious rabbits despite development of nitrate tolerance. Circulation 104 (2001) 694-699
20. Hausen B., Muller P., Bahra M., Ramsamooj R., and Hewitt C.W. Donor pretreatment with intravenous prostacyclin versus inhaled nitric oxide in experimental lung transplantation. Transplantation 62 (1996) 1714-1719
21. Naidu B.V., Fraga C., Salzmann A.L., Szabo C., Verrier E.D., and Mulligan M.S. Critical role of reactive nitrogen species in lung ischemia-reperfusion injury. J Heart Lung Transplant 22 (2003) 784-793
22. Kao S.J., Peng T.C., Lee R.P., Hsu K., Chen C.F., Hung Y.K., et al. Nitric oxide mediates lung injury induced by ischemia-reperfusion in rats. J Biomed Sci 10 (2003) 58-64
23. Turan N.N., and Demiryürek A.T. Preconditioning effects of peroxynitrite in the rat lung. Pharmacol Res 54 (2006) 380-388
24. Schumacher J., Binkowski K., Dendorfer A., and Klotz K.F. Organ-specific extravasation of albumin-bound Evans blue during nonresuscitated hemorrhagic shock in rats. Shock 20 (2003) 565-568
25. Murakami S., Bacha E.A., Hervé P., Détruit H., Chapelier A.R., Dartevelle P.G., et al. Prevention of reperfusion injury by inhaled nitric oxide in lungs harvested from non-heart-beating donors. Ann Thorac Surg 62 (1996) 1632-1638
26. Waldow T., Witt W., Weber E., and Matschke K. Nitric oxide donor-induced persistent inhibition of cell adhesion protein expression and NFkappaB activation in endothelial cells. Nitric Oxide 15 (2006) 103-113
27. Miranda K.M., Espey M.G., and Wink D.A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5 (2001) 62-71
28. Ignarro L.J. Introduction and overview. In: Ignarro L.J. (Ed). Nitric oxide. Biology and pathobiology (2000), Academic Press, San Diego 3-19
29. Ichinose F., Roberts J.D., and Zapol W.M. Inhaled nitric oxide: a selective pulmonary vasodilator: current uses and therapeutic potential. Circulation 109 (2004) 3106-3111
30. Bloch K.D., Ichinose F., Roberts J.D., and Zapol W.M. Inhaled NO as a therapeutic agent. Cardiovasc Res 75 (2007) 339-348
31. Brueckl C., Kaestle S., Kerem A., Habazettl H., Krombach F., Kuppe H., et al. Hyperoxia-induced reactive oxygen species formation in pulmonary capillary endothelial cells in situ. Am J Respir Cell Mol Biol 34 (2006) 453-463
32. Zaher T.E., Miller E.J., Morrow D.M., Javdan M., and Mantell L.L. Hyperoxia-induced signal transduction pathways in pulmonary epithelial cells. Free Radic Biol Med 42 (2007) 897-908
33. Weinberger B., Laskin D.L., Heck D.E., and Laskin J.D. The toxicology of inhaled nitric oxide. Toxicol Sci 59 (2001) 5-16
34. Lorch S.A., Munson D., Lightfoot R.T., and Ischiropoulos H. Oxygen tension and inhaled nitric oxide modulate pulmonary levels of S-nitrosocysteine and 3-nitrotyrosine in rats. Padiatr Res 56 (2004) 345-352
35. Klotz L.O., Schroeder P., and Sies H. Peroxynitrite signaling: receptor tyrosine kinases and activation of stress-responsive pathways. Free Radic Biol Med 33 (2002) 737-743
36. Bove P.F., and van der Vliet A. Nitric oxide and reactive nitrogen species in airway epithelial signaling and inflammation. Free Radic Biol Med 41 (2006) 515-527
37. Pinsky D.J., Naka Y., Chowdhury N.C., Liao H., Oz M.C., Michler R.E., et al. The nitric oxide/cyclic GMP pathway in organ transplantation: critical role in successful lung preservation. Proc Natl Acad Sci USA 91 (1994) 12086-12090
38. Egan T.M., Hoffmann S.C., Sevala M., Sadoff J.D., and Schlidt S.A. Nitroglycerin reperfusion reduces ischemia-reperfusion injury in non-heart-beating donor lungs. J Heart Lung Transplant 25 (2006) 110-119
39. Naka Y., Roy D.K., Smerling A.J., Michler R.E., Smith C.R., Stern D.M., et al. Inhaled nitric oxide fails to confer the pulmonary protection provided by distal stimulation of the nitric oxide pathway at the level of cyclic guanosine monophosphate. J Thorac Cardiovasc Surg 110 (1995) 1434-1440
40. Chetham P.M., Sefton W.D., Bridges J.P., Stevens T., and McMurtry I.F. Inhaled nitric oxide pretreatment but not posttreatment attenuates ischemia-reperfusion-induced pulmonary microvascular leak. Anesthesiology 86 (1997) 895-902
41. Sandera P., Hillinger S., Stammberger U., Schoedon G., Zalunardo M., Weder W., et al. 8-Br-cyclic GMP given during reperfusion improves post-transplant lung edema and free radical injury. J Heart Lung Transplant 19 (2000) 173-178
42. Schütte H., Witzenrath M., Mayer K., Weissmann N., Schell A., Rosseau S., et al. The PDE inhibitor zaprinast enhances NO-mediated protection against vascular leakage in reperfused lungs. Am J Physiol Lung Cell Mol Physiol 19 (2000) 173-178
43. Sessa W.C. Regulation of endothelial derived nitric oxide in health and disease. Mem Inst Oswaldo Cruz 100 (2005) 15-18
44. Dudzinski D.M., and Michel T. Life history of eNOS: partners and pathways. Cardiovasc Res 75 (2007) 247-260
45. Alencar J.L., Lobysheva I., Geffard M., Sarr M., Schott C., Schini-Kerth V.B., et al. Role of S-nitrosation of cysteine residues in long-lasting inhibitor effect of nitric oxide on arterial tone. Mol Pharmacol 63 (2003) 1148-1158
46. Bryan N.S., Rassaf T., Maloney R.E., Rodriguez C.M., Saijo F., Rodriguez J.R., et al. Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo. Proc Natl Acad Sci USA 101 (2004) 4308-4313
47. Bacha E.A., Hervé P., Murakami S., Chapelier A., Mazmanian G.M., de Montpreville V., et al. Lasting beneficial effect of short-term inhaled nitric oxide on graft function after lung transplantation. J Thorac Cardiovasc Surg 112 (1996) 590-598
48. Bacha E.A., Sellak H., Murakami S., Mazmanian G.M., Détruit H., de Montpreville V., et al. Inhaled nitric oxide attenuates reperfusion injury in nonheartbeating-donor lung transplantation. Transplantation 63 (1997) 1380-1386
49. Sun Z., Sun B., Wang X., Wang W., and Zhu L. Anti-inflammatory effects of inhaled nitric oxide are optimized at lower oxygen concentration in experimental klebsiella pneumoniae pneumonia. Inflamm Res 55 (2006) 430-440
50. Clancy R.M., Leszczynska-Piziak J., and Abramson S.B. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest 90 (1992) 1116-1121
51. 2-terminal kinase signaling pathway confers susceptibility to hyperoxic lung injury in mice. Am J Physiol Lung Cell Mol Physiol 285 (2003) L250-L257
52. Otterbein L.E., Otterbein S.L., Ifedigbo E., Liu F., Morse D.E., Fearns C., et al. MKK3 mitogen-activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant-induced lung injury. Am J Pathol 163 (2003) 2555-2563
53. Yang G., Abate A., George A.G., Weng Y.H., and Dennery P.A. Maturational differences in lung NF-kappaB activation and their role in tolerance to hyperoxia. J Clin Invest 114 (2004) 669-678
54. Buckley S., Barsky L., Weinberg K., and Warburton D. In vivo inosine protects alveolar epithelial type 2 cells against hyperoxia-induced DNA damage through MAP kinase signaling. Am J Physiol Lung Cell Mol Physiol 288 (2005) L569-L575
55. Li L.F., Liao S.K., Ko Y.S., Lee C.H., and Quinn D.A. Hyperoxia increases ventilator-induced lung injury via mitogen-activated protein kinases: a prospective, controlled animal experiment. Crit Care 11 (2007) R25
56. Sakiyama S., de Perrot M., Han B., Waddell T.K., Keshavjee S., and Liu M. Ischemia-reperfusion decreases protein tyrosine phosporylation and p38 mitogen-activated protein kinase phophorylation in rat lung transplants. J Heart Lung Transplant 22 (2003) 338-346
57. 2-terminal kinase activity improves ischemia/reperfusion injury in rat lungs. J Immunol 172 (2004) 2569-2577
58. Fujita T., Asai T., Andrassy M., Stern D.M., Pinsky D.J., Zou Y.S., et al. PKCbeta regulates ischemia/reperfusion injury in the lung. J Clin Invest 113 (2004) 1615-1623
59. Farivar A.S., Woolley S.M., Fraga C.H., Byrne K., and Mulligan M.S. Proinflammatory response of alveolar type II pneumocytes to in vitro hypoxia and reoxygenation. Am J Transplant 4 (2004) 346-351
60. Matot I., Weiniger C.F., Zeira E., Galun E., Joshi B.V., and Jacobson K.A. A3 adenosine receptors and mitogen-activated protein kinases in lung injury following in vivo reperfusion. Crit Care 10 (2006) R65
61. Abe J., Baines C.P., and Berk B.C. Role of mitogen-activated protein kinases ischemia and reperfusion injury: the good and the bad. Circ Res 86 (2000) 607-609
62. Ahmad S., Ahmad A., and White C.W. Purinergic signaling and kinase activation for survival in pulmonary oxidative stress and disease. Free Radic Biol Med 41 (2006) 29-40
63. Hausenloy D.J., and Yellon D.M. Survival kinases in ischemic preconditioning and postconditioning. Cardiovasc Res 70 (2006) 240-253
64. Lu Y., Parkyn L., Otterbein L.E., Kureishi Y., Walsh K., Ray A., et al. Activated Akt protects the lung from oxidant-induced injury and delays death of mice. J Exp Med 193 (2001) 545-549
65. Truong S.V., Monick M.M., Yarovinsky T.O., Powers L.S., Nyunoya T., and Hunninghake G.W. Extracellular signal-regulated kinase activation delays hyperoxia-induced epithelial cell death in conditions of Akt downregulation. Am J Respir Cell Mol Biol 31 (2004) 611-618
66. Jope R.S., Yuskaitis C.J., and Beurel E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem Res 32 (2007) 577-595
67. Dugo L., Collin M., and Thiemermann C. Glycogen synthase kinase 3beta as a target for the therapy of shock and inflammation. Shock 27 (2007) 113-123
68. Cuzzocrea S., Mazzon E., Esposito E., Muià C., Abdelrahman M., Di Paola R., et al. Glycogen synthase kinase-3beta inhibition attenuates the development of ischaemia/reperfusion injury of the gut. Intensive Care Med 33 (2007) 880-893
69. Cuzzocrea S., Crisafulli C., Mazzon E., Esposito E., Muià C., Abdelrahman M., et al. Inhibition of glycogen synthase kinase-3beta attenuates the development of carrageenan-induced lung injury in mice. Br J Pharmacol 149 (2006) 687-702