Molecular biological effects of selective neuronal nitric oxide synthase inhibition in ovine lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 3, 2010, Pages

  Saunders, Fiona D ^a   Westphal, Martin ^a,b   Enkhbaatar, Perenlei ^a   Wang, Jianpu ^a   Pazdrak, Konrad ^a   Nakano, Yoshimitsu ^a   Hamahata, Atsumori ^a   Jonkam, Collette C ^a   Lange, Matthias ^a,b   Connelly, Rhykka L ^a   Kulp, Gabriela A ^a   Cox, Robert A ^a   Hawkins, Hal K ^a   Schmalstieg, Frank C ^a   Horvath, Eszter ^a   Szabo, Csaba ^a   Traber, Lillian D ^a   Whorton, Elbert ^c   Herndon, David N ^a   Traber, Daniel L ^a  

^a SHRINERS HOSPITALS FOR CHILDREN   (United States)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Acute lung injury; Pathogenesis

Indexed keywords

3 NITROTYROSINE; 7 NITROINDAZOLE; INTERLEUKIN 8; MALONALDEHYDE; MYELOPEROXIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRATE; NITRIC OXIDE SYNTHASE; NITRITE;

ACUTE LUNG INJURY; AIRWAY OBSTRUCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GAS EXCHANGE; HISTOPATHOLOGY; LUNG BLOOD VESSEL; LUNG BURN; LUNG HEMODYNAMICS; LUNG PARENCHYMA; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PULMONARY SHUNT;

AIRWAY OBSTRUCTION; ANIMALS; CELL NUCLEUS; ENZYME ACTIVATION; HEMODYNAMICS; INDAZOLES; INTERLEUKIN-8; LUNG INJURY; MALONDIALDEHYDE; NITRATES; NITRIC OXIDE SYNTHASE TYPE I; NITRITES; PEROXIDASE; POLY(ADP-RIBOSE) POLYMERASES; PRESSURE; REGIONAL BLOOD FLOW; RESPIRATORY FUNCTION TESTS; SHEEP; SURVIVAL ANALYSIS; TRACHEA; TRANSCRIPTION FACTOR RELA; TYROSINE;

EID: 77249163686     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00147.2009     Document Type: Article

References (55)

1. Adaikalakoteswari A, Rema M, Mohan V, Balasubramanyam M. Oxidative DNA damage and augmentation of poly(ADP-ribose) polymerase/ nuclear factor-kappa B signaling in patients with type 2 diabetes and microangiopathy. Int J Biochem Cell Biol 39: 1673-1684, 2007.
2. Bakondi E, Bai P, Szabo EE, Hunyadi J, Gergely P, Szabo C, Virag L. Detection of poly(ADP-ribose) polymerase activation in oxidatively stressed cells and tissues using biotinylated NAD substrate. J Histochem Cytochem 50: 91-98, 2002.
3. Barth E, Radermacher P, Szabo C. The world according to poly(ADPribose) polymerase (PARP)-update 2006. Intensive Care Med 32: 1470-1474, 2006.
4. Baxter CR, Shires T. Physiological response to crystalloid resuscitation of severe burns. Ann NY Acad Sci 150: 874-894, 1968.
5. Beller CJ, Radovits T, Kosse J, Gero D, Szabo C, Szabo G. Activation of the peroxynitrite-poly(adenosine diphosphate-ribose) polymerase pathway during neointima proliferation: a new target to prevent restenosis after endarterectomy. J Vasc Surg 43: 824-830, 2006.
6. Bland-Ward PA, Moore PK. 7-Nitro indazole derivatives are potent inhibitors of brain, endothelium and inducible isoforms of nitric oxide synthase. Life Sci 57: PL131-PL135, 1995.
7. Bredt DS, Hwang PM, Snyder SH. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347: 768-770, 1990.
8. Chatterjee A, Catravas JD. Endothelial nitric oxide (NO) and its pathophysiologic regulation. Vascul Pharmacol 49: 134-140, 2008.
9. Chen Y, Medhora M, Falck, Jr, Pritchard KA Jr, Jacobs ER. Mechanisms of activation of eNOS by 20-HETE and VEGF in bovine pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 291: L378-L385, 2006.
10. Cho HJ, Xie QW, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Nathan C. Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med 176: 599-604, 1992.
11. Cox RA, Burke AS, Oliveras G, Enkhbaatar P, Traber LD, Zwischenberger JB, Jeschke MG, Schmalstieg FC, Herndon DN, Traber DL, Hawkins HK. Acute bronchial obstruction in sheep: histopathology and gland cytokine expression. Exp Lung Res 31: 819-837, 2005.
12. Cox RA, Burke AS, Soejima K, Murakami K, Katahira J, Traber LD, Herndon DN, Schmalstieg FC, Traber DL, Hawkins HK. Airway obstruction in sheep with burn and smoke inhalation injuries. Am J Respir Cell Mol Biol 29: 295-302, 2003.
13. Demchenko IT, Atochin DN, Gutsaeva DR, Godfrey RR, Huang PL, Piantadosi CA, Allen BW. Contributions of nitric oxide synthase isoforms to pulmonary oxygen toxicity, local vs. mediated effects. Am J Physiol Lung Cell Mol Physiol 294: L984-L990, 2008.
14. Enkhbaatar P, Murakami K, Shimoda K, Mizutani A, Traber L, Phillips G, Parkinson J, Salsbury JR, Biondo N, Schmalstieg F, Burke A, Cox R, Hawkins H, Herndon D, Traber D. Inducible nitric oxide synthase dimerization inhibitor prevents cardiovascular and renal morbidity in sheep with combined burn and smoke inhalation injury. Am J Physiol Heart Circ Physiol 285: H2430-H2436, 2003.
15. Enkhbaatar P, Murakami K, Traber LD, Cox R, Parkinson JF, Westphal M, Esechie A, Morita N, Maybauer MO, Maybauer DM, Burke AS, Schmalstieg FC, Hawkins HK, Herndon DN, Traber DL. The inhibition of inducible nitric oxide synthase in ovine sepsis model. Shock 25: 522-527, 2006.
16. Enkhbaatar P, Traber DL. Pathophysiology of acute lung injury in combined burn and smoke inhalation injury. Clin Sci (Lond) 107: 137-143, 2004.
17. Fischer A, Hoffmann B. Nitric oxide synthase in neurons and nerve fibers of lower airways and in vagal sensory ganglia of man. Correlation with neuropeptides. Am J Respir Crit Care Med 154: 209-216, 1996.
18. Hamahata A, Enkhbaatar P, Kraft ER, Lange M, Leonard SW, Traber MG, Cox RA, Schmalstieg FC, Hawkins HK, Whorton EB, Horvath EM, Szabo C, Traber LD, Herndon DN, Traber DL. gamma-Tocopherol nebulization by a lipid aerosolization device improves pulmonary function in sheep with burn and smoke inhalation injury. Free Radic Biol Med 45: 425-433, 2008.
19. Hamahata A, Enkhbaatar P, Sakurai H, Nozaki M, Traber DL. Effect of ablated bronchial blood flow on survival rate and pulmonary function after burn and smoke inhalation in sheep. Burns 35: 802-810, 2009.
20. Hegedus C, Lakatos P, Olah G, Toth BI, Gergely S, Szabo E, Biro T, Szabo C, Virag L. Protein kinase C protects from DNA damage-induced necrotic cell death by inhibiting poly(ADP-ribose) polymerase-1. FEBS Lett 582: 1672-1678, 2008.
21. Hiroi Y, Guo Z, Li Y, Beggs AH, Liao JK. Dynamic regulation of endothelial NOS mediated by competitive interaction with alpha-actinin-4 and calmodulin. FASEB J 22: 1450-1457, 2008.
22. Hollingsworth JW, Chen BJ, Brass DM, Berman K, Gunn MD, Cook DN, Schwartz DA. The critical role of hematopoietic cells in lipopolysaccharide-induced airway inflammation. Am J Respir Crit Care Med 171: 806-813, 2005.
23. Kimura R, Traber LD, Herndon DN, Linares HA, Lubbesmeyer HJ, Traber DL. Increasing duration of smoke exposure induces more severe lung injury in sheep. J Appl Physiol 64: 1107-1113, 1988.
24. Lange M, Enkhbaatar P, Traber DL, Cox RA, Jacob S, Mathew BP, Hamahata A, Traber LD, Herndon DN, Hawkins HK. Role of calcitonin gene-related peptide (CGRP) in ovine burn and smoke inhalation injury. J Appl Physiol 107: 176-184, 2009.
25. Maybauer MO, Maybauer DM, Fraser JF, Traber LD, Westphal M, Enkhbaatar P, Cox RA, Huda R, Hawkins HK, Morita N, Murakami K, Mizutani A, Herndon DN, Traber DL. Recombinant human activated protein C improves pulmonary function in ovine acute lung injury resulting from smoke inhalation and sepsis. Crit Care Med 34: 2432-2438, 2006.
26. Maybauer MO, Maybauer DM, Traber LD, Westphal M, Enkhbaatar P, Morita N, Jodoin JM, Heggers JP, Herndon DN, Traber DL. Gentamicin improves hemodynamics in ovine septic shock after smoke inhalation injury. Shock 24: 226-231, 2005.
27. Maybauer MO, Rehberg S, Traber DL, Herndon DN, Maybauer DM. [Pathophysiology of acute lung injury in severe burn and smoke inhalation injury]. Anaesthesist 58: 805-812, 2009.
28. Meyer WJ, Patterson DR, Jaco M, Woodson L, Thomas C. Management of pain and other discomforts in burned patients. In: Total Burn Care, edited by Herndon D. Philadelphia, PA: Saunders Elsevier, 2007, p. 797-818.
29. Mlcak RP, Suman OE, Herndon DN. Respiratory management of inhalation injury. Burns 33: 2-13, 2007.
30. Murakami K, Enkhbaatar P, Shimoda K, Cox RA, Burke AS, Hawkins HK, Traber LD, Schmalstieg FC, Salzman AL, Mabley JG, Komjati K, Pacher P, Zsengeller Z, Szabo C, Traber DL. Inhibition of poly (ADP-ribose) polymerase attenuates acute lung injury in an ovine model of sepsis. Shock 21: 126-133, 2004.
31. Murakami K, Enkhbaatar P, Yu YM, Traber LD, Cox RA, Hawkins HK, Tompkins RG, Herndon D, Traber DL. L-Arginine attenuates acute lung injury after smoke inhalation and burn injury in sheep. Shock 28: 477-483, 2007.
32. Nys M, Deby-Dupont G, Habraken Y, Legrand-Poels S, Kohnen S, Ledoux D, Canivet JL, Damas P, Lamy M. Bronchoalveolar lavage fluids of ventilated patients with acute lung injury activate NF-kappaB in alveolar epithelial cell line: role of reactive oxygen/nitrogen species and cytokines. Nitric Oxide 9: 33-43, 2003.
33. Nys M, Deby-Dupont G, Habraken Y, Legrand-Poels S, Ledoux D, Canivet JL, Damas P, Lamy M. Bronchoalveolar lavage fluids of patients with lung injury activate the transcription factor nuclear factor-kappaB in an alveolar cell line. Clin Sci (Lond) 103: 577-585, 2002.
34. Pruitt BA, Wolf SE, Mason AD. Epidemiological, demographic, and outcome characteristics of burn injury. In: Total Burn Care (3rd ed.), edited by Herndon D. Philadelphia, PA: Saunders Elsevier, 2007, p. 14-32.
35. Rawlingson A, Greenacre SA, Brain SD. Generation of peroxynitrite in localised, moderate temperature burns. Burns 26: 223-227, 2000.
36. Sakurai H, Soejima K, Schmalstieg FC, Nozaki M, Traber DL. Inhibition of lung permeability changes after burn and smoke inhalation by an anti-interleukin-8 antibody in sheep. Surg Today 39: 399-406, 2009.
37. Schenarts PJ, Bone HG, Traber LD, Traber DL. Effect of severe smoke inhalation injury on systemic microvascular blood flow in sheep. Shock 6: 201-205, 1996.
38. Schmalstieg FC, Chow J, Savage C, Rudloff HE, Palkowetz KH, Zwischenberger JB. Interleukin-8, aquaporin-1, and inducible nitric oxide synthase in smoke and burn injured sheep treated with percutaneous carbon dioxide removal. ASAIO J 47: 365-371, 2001.
39. Schwela DH, Goldammer JG, Morawska LH, Simpson O. Health guidelines for vegetation fire events. Guideline Document. Singapore: Published on behalf of UNEP, WHO & WMO, 1999.
40. Shi XZ, Pazdrak K, Saada N, Dai B, Palade P, Sarna SK. Negative transcriptional regulation of human colonic smooth muscle Cav1.2 channels by p50 and p65 subunits of nuclear factor-kappaB. Gastroenterology 129: 1518-1532, 2005.
41. Shimoda K, Murakami K, Enkhbaatar P, Traber LD, Cox RA, Hawkins HK, Schmalstieg FC, Komjati K, Mabley JG, Szabo C, Salzman AL, Traber DL. Effect of poly(ADP ribose) synthetase inhibition on burn and smoke inhalation injury in sheep. Am J Physiol Lung Cell Mol Physiol 285: L240-L249, 2003.
42. Shirani KZ, Pruitt BA Jr, Mason AD Jr. The influence of inhalation injury and pneumonia on burn mortality. Ann Surg 205: 82-87, 1987.
43. Soejima K, Schmalstieg FC, Sakurai H, Traber LD, Traber DL. Pathophysiological analysis of combined burn and smoke inhalation injuries in sheep. Am J Physiol Lung Cell Mol Physiol 280: L1233-L1241, 2001.
44. Soejima K, Traber LD, Schmalstieg FC, Hawkins H, Jodoin JM, Szabo C, Szabo E, Virag L, Salzman A, Traber DL. Role of nitric oxide in vascular permeability after combined burns and smoke inhalation injury. Am J Respir Crit Care Med 163: 745-752, 2001.
45. Staub NC, Bland RD, Brigham KL, Demling R, Erdmann AJ 3rd, Woolverton WC. Preparation of chronic lung lymph fistulas in sheep. J Surg Res 19: 315-320, 1975.
46. Szabo C. Poly(ADP-ribose) polymerase activation by reactive nitrogen species-relevance for the pathogenesis of inflammation. Nitric Oxide 14: 169-179, 2006.
47. Szabo C, Zingarelli B, O'Connor M, Salzman AL. DNA strand breakage, activation of poly (ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite. Proc Natl Acad Sci USA 93: 1753-1758, 1996.
48. Traber DL, Hawkins HK, Enkhbaatar P, Cox RA, Schmalstieg FC, Zwischenberger JB, Traber LD. The role of the bronchial circulation in the acute lung injury resulting from burn and smoke inhalation. Pulm Pharmacol Ther 20: 163-166, 2007.
49. Traber MG, Shimoda K, Murakami K, Leonard SW, Enkhbaatar P, Traber LD, Traber DL. Burn and smoke inhalation injury in sheep depletes vitamin E: kinetic studies using deuterated tocopherols. Free Radic Biol Med 42: 1421-1429, 2007.
50. Weiss SM, Lakshminarayan S. Acute inhalation injury. Clin Chest Med 15: 103-116, 1994.
51. Westphal M, Cox RA, Traber LD, Morita N, Enkhbaatar P, Schmalstieg FC, Hawkins HK, Maybauer DM, Maybauer MO, Murakami K, Burke AS, Westphal-Varghese BB, Rudloff HE, Salsbury JR, Jodoin JM, Lee S, Traber DL. Combined burn and smoke inhalation injury impairs ovine hypoxic pulmonary vasoconstriction. Crit Care Med 34: 1428-1436, 2006.
52. Westphal M, Enkhbaatar P, Schmalstieg FC, Kulp GA, Traber LD, Morita N, Cox RA, Hawkins HK, Westphal-Varghese BB, Rudloff HE, Maybauer DM, Maybauer MO, Burke AS, Murakami K, Saunders F, Horvath EM, Szabo C, Traber DL. Neuronal nitric oxide synthase inhibition attenuates cardiopulmonary dysfunctions after combined burn and smoke inhalation injury in sheep. Crit Care Med 36: 1196-1204, 2008.
53. Yang XD, Corvalan JR, Wang P, Roy CM, Davis CG. Fully human anti-interleukin-8 monoclonal antibodies: potential therapeutics for the treatment of inflammatory disease states. J Leukoc Biol 66: 401-410, 1999.
54. Zerfaoui M, Suzuki Y, Naura AS, Hans CP, Nichols C, Boulares AH. Nuclear translocation of p65 NF-kappaB is sufficient for VCAM-1, but not ICAM-1, expression in TNF-stimulated smooth muscle cells: differential requirement for PARP-1 expression and interaction. Cell Signal 20: 186-194, 2008.
55. Zou MH, Shi C, Cohen RA. Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J Clin Invest 109: 817-826, 2002.