Renal hypoperfusion and impaired endothelium-dependent vasodilation in an animal model of VILI: The role of the peroxynitrite-PARP pathway

Critical Care

Volumn 14, Issue 2, 2010, Pages

  Vaschetto, Rosanna ^a,b   Kuiper, Jan W ^b   Musters, René J P ^b   Eringa, Etto C ^b   Della Corte, Francesco ^a   Murthy, Kanneganti ^c   Groeneveld, AB Johan ^b   Plötz, Frans B ^b  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c INOTEK CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; INORGANIC SALT; LIPOPOLYSACCHARIDE; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEROXYNITRITE; UNCLASSIFIED DRUG; WATER; WW 85; ENDOTHELIUM DERIVED RELAXING FACTOR; PEROXYNITROUS ACID;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL GAS; ARTICLE; ARTIFICIAL VENTILATION; ATTENUATION; BLOOD PRESSURE; BLOOD SAMPLING; CATALYST; CONTINUOUS INFUSION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; DECOMPOSITION; FROZEN SECTION; HYPOTENSION; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY ARTERY; KIDNEY BLOOD FLOW; KIDNEY DYSFUNCTION; KIDNEY FUNCTION; KIDNEY PARENCHYMA; KIDNEY PERFUSION; LEUKOCYTE; LOADING DRUG DOSE; LUNG EDEMA; LUNG HEMODYNAMICS; LUNG INJURY; LUNG VENTILATION; MALE; NONHUMAN; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TIDAL VOLUME; URINALYSIS; VASCULAR ENDOTHELIUM; VASODILATATION; VENTILATOR INDUCED LUNG INJURY; ACUTE KIDNEY FAILURE; ANIMAL; BLOOD GAS ANALYSIS; DRUG EFFECT; ENZYME ACTIVATION; HEMODYNAMICS; KIDNEY CIRCULATION; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD GAS ANALYSIS; ENDOTHELIUM-DEPENDENT RELAXING FACTORS; ENZYME ACTIVATION; HEMODYNAMICS; KIDNEY FAILURE, ACUTE; MALE; MODELS, ANIMAL; PEROXYNITROUS ACID; POLY(ADP-RIBOSE) POLYMERASES; POSITIVE-PRESSURE RESPIRATION; RATS; RATS, SPRAGUE-DAWLEY; RENAL CIRCULATION; TIDAL VOLUME; VASODILATION; VENTILATOR-INDUCED LUNG INJURY;

EID: 78149231704     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/cc8932     Document Type: Article

References (52)

1. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000, 342:1334-1349. 10.1056/NEJM200005043421806, 10793167.
2. Imai Y, Parodo J, Kajikawa O, de PM, Fischer S, Edwards V, Cutz E, Liu M, Keshavjee S, Martin TR, Marshall JC, Ranieri VM, Slutsky AS. Injurious mechanical ventilation and end-organ epithelial cell apoptosis and organ dysfunction in an experimental model of acute respiratory distress syndrome. JAMA 2003, 289:2104-2112. 10.1001/jama.289.16.2104, 12709468.
3. Ranieri VM, Suter PM, Tortorella C, De TR, Dayer JM, Brienza A, Bruno F, Slutsky AS. Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: a randomized controlled trial. JAMA 1999, 282:54-61. 10.1001/jama.282.1.54, 10404912.
4. Ranieri VM, Giunta F, Suter PM, Slutsky AS. Mechanical ventilation as a mediator of multisystem organ failure in acute respiratory distress syndrome. JAMA 2000, 284:43-44. 10.1001/jama.284.1.43, 10872010.
5. Vaschetto R, Kuiper JW, Chiang SR, Haitsma JJ, Juco JW, Uhlig S, Plotz FB, Corte FD, Zhang H, Slutsky AS. Inhibition of poly(adenosine diphosphate-ribose) polymerase attenuates ventilator-induced lung injury. Anesthesiology 2008, 108:261-268. 10.1097/01.anes.0000299434.86640.15, 18212571.
6. Uchino S, Kellum JA, Bellomo R, Doig GS, Morimatsu H, Morgera S, Schetz M, Tan I, Bouman C, Macedo E, Gibney N, Tolwani A, Ronco C. Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA 2005, 294:813-818. 10.1001/jama.294.7.813, 16106006.
7. Hoste EA, Clermont G, Kersten A, Venkataraman R, Angus DC, De Bacquer D, Kellum JA. RIFLE criteria for acute kidney injury are associated with hospital mortality in critically ill patients: a cohort analysis. Crit Care 2006, 10:R73. 10.1186/cc4915, 1550961, 16696865.
8. Crimi E, Zhang H, Han RN, Sorbo LD, Ranieri VM, Slutsky AS. Ischemia and reperfusion increases susceptibility to ventilator-induced lung injury in rats. Am J Respir Crit Care Med 2006, 174:178-186. 10.1164/rccm.200507-1178OC, 16645175.
9. Gurkan OU, O'Donnell C, Brower R, Ruckdeschel E, Becker PM. Differential effects of mechanical ventilatory strategy on lung injury and systemic organ inflammation in mice. Am J Physiol Lung Cell Mol Physiol 2003, 285:L710-L718.
10. Kuiper JW, Versteilen AM, Niessen HW, Vaschetto RR, Sipkema P, Heijnen CJ, Groeneveld AB, Plotz FB. Production of endothelin-1 and reduced blood flow in the rat kidney during lung-injurious mechanical ventilation. Anesth Analg 2008, 107:1276-1283. 10.1213/ane.0b013e31818067a2, 18806040.
11. Kuiper JW, Groeneveld AB, Slutsky AS, Plotz FB. Mechanical ventilation and acute renal failure. Crit Care Med 2005, 33:1408-1415. 10.1097/01.CCM.0000165808.30416.EF, 15942363.
12. Brodsky SV, Yamamoto T, Tada T, Kim B, Chen J, Kajiya F, Goligorsky MS. Endothelial dysfunction in ischemic acute renal failure: rescue by transplanted endothelial cells. Am J Physiol Renal Physiol 2002, 282:F1140-F1149.
13. Lieberthal W, Wolf EF, Rennke HG, Valeri CR, Levinsky NG. Renal ischemia and reperfusion impair endothelium-dependent vascular relaxation. Am J Physiol 1989, 256:F894-F900.
14. Molitoris BA, Sutton TA. Endothelial injury and dysfunction: role in the extension phase of acute renal failure. Kidney Int 2004, 66:496-499. 10.1111/j.1523-1755.2004.761_5.x, 15253696.
15. Hammerschmidt S, Sandvoss T, Gessner C, Schauer J, Wirtz H. High in comparison with low tidal volume ventilation aggravates oxidative stress-induced lung injury. Biochim Biophys Acta 2003, 1637:75-82.
16. Kim JH, Suk MH, Yoon DW, Kim HY, Jung KH, Kang EH, Lee SY, Lee SY, Suh IB, Shin C, Shim JJ, In KH, Yoo SH, Kang KH. Inflammatory and transcriptional roles of poly (ADP-ribose) polymerase in ventilator-induced lung injury. Crit Care 2008, 12:R108. 10.1186/cc6995, 2575597, 18718025.
17. Liaudet L, Pacher P, Mabley JG, Virag L, Soriano FG, Hasko G, Szabo C. Activation of poly(ADP-Ribose) polymerase-1 is a central mechanism of lipopolysaccharide-induced acute lung inflammation. Am J Respir Crit Care Med 2002, 165:372-377.
18. Stone DH, Al-Badawi H, Conrad MF, Stoner MC, Entabi F, Cambria RP, Watkins MT. PJ34, a poly-ADP-ribose polymerase inhibitor, modulates renal injury after thoracic aortic ischemia/reperfusion. Surgery 2005, 138:368-374. 10.1016/j.surg.2005.06.004, 16153449.
19. Ha HC, Snyder SH. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 1999, 96:13978-13982. 10.1073/pnas.96.24.13978, 24176, 10570184.
20. Virag L, Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 2002, 54:375-429. 10.1124/pr.54.3.375, 12223530.
21. Helyar SG, Patel B, Headington K, El-Assal M, Chatterjee PK, Pacher P, Mabley JG. PCB-induced endothelial cell dysfunction: role of poly (ADP-ribose) polymerase. Biochem Pharmacol 2009, 78(8):959-965. 10.1016/j.bcp.2009.06.019, 2756480, 19549508.
22. Mathews MT, Berk BC. PARP-1 inhibition prevents oxidative and nitrosative stress-induced endothelial cell death via transactivation of the VEGF receptor 2. Arterioscler Thromb Vasc Biol 2008, 28:711-717. 10.1161/ATVBAHA.107.156406, 18239155.
23. Tasatargil A, Dalaklioglu S, Sadan G. Inhibition of poly(ADP-ribose) polymerase prevents vascular hyporesponsiveness induced by lipopolysaccharide in isolated rat aorta. Pharmacol Res 2005, 51:581-586. 10.1016/j.phrs.2005.02.020, 15829440.
24. Cuzzocrea S, Misko TP, Costantino G, Mazzon E, Micali A, Caputi AP, Macarthur H, Salvemini D. Beneficial effects of peroxynitrite decomposition catalyst in a rat model of splanchnic artery occlusion and reperfusion. FASEB J 2000, 14:1061-1072.
25. Lancel S, Tissier S, Mordon S, Marechal X, Depontieu F, Scherpereel A, Chopin C, Neviere R. Peroxynitrite decomposition catalysts prevent myocardial dysfunction and inflammation in endotoxemic rats. J Am Coll Cardiol 2004, 43:2348-2358. 10.1016/j.jacc.2004.01.047, 15193704.
26. Pieper GM, Nilakantan V, Chen M, Zhou J, Khanna AK, Henderson JD, Johnson CP, Roza AM, Szabo C. Protective mechanisms of a metalloporphyrinic peroxynitrite decomposition catalyst, WW85, in rat cardiac transplants. J Pharmacol Exp Ther 2005, 314:53-60. 10.1124/jpet.105.083493, 15784653.
27. Peng X, Abdulnour RE, Sammani S, Ma SF, Han EJ, Hasan EJ, Tuder R, Garcia JG, Hassoun PM. Inducible nitric oxide synthase contributes to ventilator-induced lung injury. Am J Respir Crit Care Med 2005, 172:470-479. 10.1164/rccm.200411-1547OC, 2718528, 15937288.
28. Dos Santos CC, Slutsky AS. Invited review: mechanisms of ventilator-induced lung injury: a perspective. J Appl Physiol 2000, 89:1645-1655.
29. Dos Santos CC, Slutsky AS. The contribution of biophysical lung injury to the development of biotrauma. Annu Rev Physiol 2006, 68:585-618. 10.1146/annurev.physiol.68.072304.113443, 16460285.
30. Pontoppidan H, Geffin B, Lowenstein E. Acute respiratory failure in the adult. 3. N Engl J Med 1972, 287:799-806.
31. Goldfarb RD, Marton A, Szabo E, Virag L, Salzman AL, Glock D, Akhter I, McCarthy R, Parrillo JE, Szabo C. Protective effect of a novel, potent inhibitor of poly(adenosine 5'-diphosphate-ribose) synthetase in a porcine model of severe bacterial sepsis. Crit Care Med 2002, 30:974-980. 10.1097/00003246-200205000-00004, 12006790.
32. Nijveldt RJ, Prins HA, van Kemenade FJ, Teerlink T, van Lambalgen AA, Boelens PG, Rauwerda JA, van Leeuwen PA. Low arginine plasma levels do not aggravate renal blood flow after experimental renal ischaemia/reperfusion. Eur J Vasc Endovasc Surg 2001, 22:232-239. 10.1053/ejvs.2001.1444, 11506516.
33. Raab S, Thein E, Harris AG, Messmer K. A new sample-processing unit for the fluorescent microsphere method. Am J Physiol 1999, 276:H1801-H1806.
34. Versteilen AM, Korstjens IJ, Musters RJ, Groeneveld AB, Sipkema P. Rho kinase regulates renal blood flow by modulating eNOS activity in ischemia-reperfusion of the rat kidney. Am J Physiol Renal Physiol 2006, 291:F606-F611. 10.1152/ajprenal.00434.2005, 16525157.
35. Dhanireddy S, Altemeier WA, Matute-Bello G, O'Mahony DS, Glenny RW, Martin TR, Liles WC. Mechanical ventilation induces inflammation, lung injury, and extra-pulmonary organ dysfunction in experimental pneumonia. Lab Invest 2006, 86:790-799. 10.1038/labinvest.3700440, 16855596.
36. O'Mahony DS, Liles WC, Altemeier WA, Dhanireddy S, Frevert CW, Liggitt D, Martin TR, Matute-Bello G. Mechanical ventilation interacts with endotoxemia to induce extrapulmonary organ dysfunction. Crit Care 2006, 10:R136. 10.1186/cc5050, 1751060, 16995930.
37. Martinez-Caro L, Lorente JA, Marin-Corral J, Sanchez-Rodriguez C, Sanchez-Ferrer A, Nin N, Ferruelo A, de PM, Fernandez-Segoviano P, Barreiro E, Esteban A. Role of free radicals in vascular dysfunction induced by high tidal volume ventilation. Intensive Care Med 2009, 35:1110-1119. 10.1007/s00134-009-1469-5, 19360397.
38. Nin N, Valero JA, Lorente JA, de PM, Fernandez-Segoviano P, Sanchez-Ferrer A, Esteban A. Large tidal volume mechanical ventilation induces vascular dysfunction in rats. J Trauma 2005, 59:711-716.
39. Nin N, Penuelas O, de PM, Lorente JA, Fernandez-Segoviano P, Esteban A. Ventilation-induced lung injury in rats is associated with organ injury and systemic inflammation that is attenuated by dexamethasone. Crit Care Med 2006, 34:1093-1098. 10.1097/01.CCM.0000205663.92384.E7, 16484900.
40. Nin N, Lorente JA, de PM, El AM, Vallejo S, Penuelas O, Fernandez-Segoviano P, Ferruelo A, Sanchez-Ferrer A, Esteban A. Rats surviving injurious mechanical ventilation show reversible pulmonary, vascular and inflammatory changes. Intensive Care Med 2008, 34:948-956. 10.1007/s00134-007-0959-6, 18180906.
41. Piepot HA, Groeneveld AB, van Lambalgen AA, Sipkema P. Tumor necrosis factor-alpha impairs endothelium-dependent relaxation of rat renal arteries, independent of tyrosine kinase. Shock 2002, 17:394-398. 10.1097/00024382-200205000-00009, 12022760.
42. Piepot HA, Groeneveld AB, van Lambalgen AA, Sipkema P. Endotoxin impairs endothelium-dependent vasodilation more in the coronary and renal arteries than in other arteries of the rat. J Surg Res 2003, 110:413-418. 10.1016/S0022-4804(02)00043-4, 12788673.
43. Chen X, Liu X, Wan X, Wu Y, Chen Y, Cao C. Ischemic Preconditioning Attenuates Renal Ischemia-Reperfusion Injury by Inhibiting Activation of IKKbeta and Inflammatory Response. Am J Nephrol 2009, 30:287-294. 10.1159/000225928, 19546526.
44. Kinsey GR, Li L, Okusa MD. Inflammation in acute kidney injury. Nephron Exp Nephrol 2008, 109:e102-e107. 10.1159/000142934, 2614446, 18802372.
45. Chiumello D, Pristine G, Slutsky AS. Mechanical ventilation affects local and systemic cytokines in an animal model of acute respiratory distress syndrome. Am J Respir Crit Care Med 1999, 160:109-116.
46. Dahlem P, Bos AP, Haitsma JJ, Schultz MJ, Meijers JC, Lachmann B. Alveolar fibrinolytic capacity suppressed by injurious mechanical ventilation. Intensive Care Med 2005, 31:724-732. 10.1007/s00134-005-2588-2, 15754195.
47. Dahlem P, Bos AP, Haitsma JJ, Schultz MJ, Wolthuis EK, Meijers JC, Lachmann B. Mechanical ventilation affects alveolar fibrinolysis in LPS-induced lung injury. Eur Respir J 2006, 28:992-998. 10.1183/09031936.06.00133104, 16837499.
48. Haitsma JJ, Schultz MJ, Hofstra JJ, Kuiper JW, Juco J, Vaschetto R, Levi M, Zhang H, Slutsky AS. Ventilator-induced coagulopathy in experimental Streptococcus pneumoniae pneumonia. Eur Respir J 2008, 32:1599-1606. 10.1183/09031936.00045908, 18768578.
49. Gattinoni L, Carlesso E, Cadringher P, Valenza F, Vagginelli F, Chiumello D. Physical and biological triggers of ventilator-induced lung injury and its prevention. Eur Respir J Suppl 2003, 47:15s-25s. 10.1183/09031936.03.00021303, 14621113.
50. Hagberg H, Wilson MA, Matsushita H, Zhu C, Lange M, Gustavsson M, Poitras MF, Dawson TM, Dawson VL, Northington F, Johnston MV. PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury. J Neurochem 2004, 90:1068-1075. 10.1111/j.1471-4159.2004.02547.x, 15312162.
51. Mabley JG, Horvath EM, Murthy KG, Zsengeller Z, Vaslin A, Benko R, Kollai M, Szabo C. Gender differences in the endotoxin-induced inflammatory and vascular responses: potential role of poly(ADP-ribose) polymerase activation. J Pharmacol Exp Ther 2005, 315:812-820. 10.1124/jpet.105.090480, 16079296.
52. McCullough LD, Zeng Z, Blizzard KK, Debchoudhury I, Hurn PD. Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J Cereb Blood Flow Metab 2005, 25:502-512. 10.1038/sj.jcbfm.9600059, 15689952.