Pretreatment of sildenafil attenuates ischemia-reperfusion renal injury in rats

American Journal of Physiology - Renal Physiology

Volumn 297, Issue 2, 2009, Pages

  Choi, Dae Eun ^a   Jeong, Jin Young ^a   Lim, Beom Jin ^b   Chung, Sarah ^a   Chang, Yoon Kyung ^c   Lee, Sang Ju ^c   Na, Ki Ryang ^a   Kim, Seok Young ^c   Shin, Young Tai ^a   Lee, Kang Wook ^a  

^a Chungnam National University College of Medicine   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Daejeon St Mary's Hospital   (South Korea)

Author keywords

Apoptosis; ERK

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CASPASE 3; CREATININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BAX; PROTEIN BCL 2; SILDENAFIL; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; KIDNEY INJURY; KIDNEY ISCHEMIA; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; UREA NITROGEN BLOOD LEVEL;

EID: 68049109462     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90609.2008     Document Type: Article

References (47)

1. Bocchi EA, Guimaraes G, Mocelin A, Bacal F, Bellotti G, Ramires JF. Sildenafil effects on exercise, neurohormonal activation, and erectile dysfunction in congestive heart failure: a double-blind, placebo-controlled, randomized study followed by a prospective treatment for erectile dysfunction. Circulation 106: 1097-1103, 2002.
2. Boolell M, Allen MJ, Ballard SA, Gepi-Attee S, Muirhead GJ, Naylor AM, Osterloh IH, Gingell C. Sildenafil: an orally active type 5 cyclic GMP-specific phosphodiesterase inhibitor for the treatment of penile erectile dysfunction. Int J Impot Res 8: 47-52, 1996.
3. Chatterjee PK, Patel NS, Kvale EO, Cuzzocrea S, Brown PA, Stewart KN, Mota-Filipe H, Thiemermann C. Inhibition of inducible nitric oxide synthase reduces renal ischemia/reperfusion injury. Kidney Int 61: 862-871, 2002.
4. Chatterjee PK, Patel NS, Sivarajah A, Kvale EO, Dugo L, Cuzzocrea S, Brown PA, Stewart KN, Mota-Filipe H, Britti D, Yaqoob MM, Thiemermann C. GW274150, a potent and highly selective inhibitor of iNOS, reduces experimental renal ischemia/reperfusion injury. Kidney Int 63: 853-865, 2003.
5. Chiao H, Kohda Y, McLeroy P, Craig L, Housini I, Star RA. Alpha-melanocyte-stimulating hormone protects against renal injury after ischemia in mice and rats. J Clin Invest 99: 1165-1172, 1997.
6. Chintala MS, Chiu PJ, Vemulapalli S, Watkins RW, Sybertz EJ. Inhibition of endothelial derived relaxing factor (EDRF) aggravates ischemic acute renal failure in anesthetized rats. Naunyn Schmiedebergs Arch Pharmacol 348: 305-310, 1993.
7. Da Silva M, Petruzzo P, Virieux S, Tiollier J, Badet L, Martin X. A primate model of renal ischemia-reperfusion injury for preclinical evaluation of the antileukocyte function associated antigen 1 monoclonal antibody odulimonab. J Urol 166: 1915-1919, 2001.
8. Das A, Ockaili R, Salloum F, Kukreja RC. Protein kinase C plays an essential role in sildenafil-induced cardioprotection in rabbits. Am J Physiol Heart Circ Physiol 286: H1455-H1460, 2004.
9. Das A, Salloum FN, Xi L, Rao YJ, Kukreja RC. ERK phosphorylation mediates sildenafil-induced myocardial protection against ischemia-reperfusion injury in mice. Am J Physiol Heart Circ Physiol 296: H1236-H1243, 2009.
10. Das A, Xi L, Kukreja RC. Phosphodiesterase-5 inhibitor sildenafil preconditions adult cardiac myocytes against necrosis and apoptosis. Essential role of nitric oxide signaling. J Biol Chem 280: 12944-12955, 2005.
11. Das A, Xi L, Kukreja RC. Protein kinase G-dependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3beta. J Biol Chem 283: 29572-29585, 2008.
12. Donnahoo KK, Shames BD, Harken AH, Meldrum DR. Review article: the role of tumor necrosis factor in renal ischemia-reperfusion injury. J Urol 162: 196-203, 1999.
13. Elrod JW, Greer JJ, Lefer DJ. Sildenafil-mediated acute cardioprotection is independent of the NO/cGMP pathway. Am J Physiol Heart Circ Physiol 292: H342-H347, 2007.
14. Fisher PW, Salloum F, Das A, Hyder H, Kukreja RC. Phosphodiesterase-5 inhibition with sildenafil attenuates cardiomyocyte apoptosis and left ventricular dysfunction in a chronic model of doxorubicin cardiotoxicity. Circulation 111: 1601-1610, 2005.
15. Fuller TF, Serkova N, Niemann CU, Freise CE. Influence of donor pretreatment with N-acetylcysteine on ischemia/reperfusion injury in rat kidney grafts. J Urol 171: 1296-1300, 2004.
16. Furusu A, Miyazaki M, Abe K, Tsukasaki S, Shioshita K, Sasaki O, Miyazaki K, Ozono Y, Koji T, Harada T, Sakai H, Kohno S. Expression of endothelial and inducible nitric oxide synthase in human glomerulonephritis. Kidney Int 53: 1760-1768, 1998.
17. Goligorsky MS, Brodsky SV, Noiri E. Nitric oxide in acute renal failure: NOS versus NOS. Kidney Int 61: 855-861, 2002.
18. Goligorsky MS, Noiri E. Duality of nitric oxide in acute renal injury. Semin Nephrol 19: 263-271, 1999.
19. Guan Z, Miller SB, Greenwald JE. Zaprinast accelerates recovery from established acute renal failure in the rat. Kidney Int 47: 1569-1575, 1995.
20. Guazzi M, Tumminello G, Di Marco F, Fiorentini C, Guazzi MD. The effects of phosphodiesterase-5 inhibition with sildenafil on pulmonary hemodynamics and diffusion capacity, exercise ventilatory efficiency, and oxygen uptake kinetics in chronic heart failure. J Am Coll Cardiol 44: 2339-2348, 2004.
21. Hung CC, Ichimura T, Stevens JL, Bonventre JV. Protection of renal epithelial cells against oxidative injury by endoplasmic reticulum stress preconditioning is mediated by ERK1/2 activation. J Biol Chem 278: 29317-29326, 2003.
22. Kelly KJ, Williams WW Jr, Colvin RB, Meehan SM, Springer TA, Gutierrez-Ramos JC, and Bonventre JV. Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 97: 1056-1063, 1996.
23. Kiymaz N, Yilmaz N, Mumcu C, Anlar O, Ozen S, Kayaoglu CR. Protective effect of sildenafil (Viagra) in transient spinal cord ischemia. Pediatr Neurosurg 44: 22-28, 2008.
24. Kukreja RC, Salloum F, Das A, Ockaili R, Yin C, Bremer YA, Fisher PW, Wittkamp M, Hawkins J, Chou E, Kukreja AK, Wang X, Marwaha VR, Xi L. Pharmacological preconditioning with sildenafil: basic mechanisms and clinical implications. Vascul Pharmacol 42: 219-232, 2005.
25. Lieberthal W, Koh JS, Levine JS. Necrosis and apoptosis in acute renal failure. Semin Nephrol 18: 505-518, 1998.
26. Lopez-Marti J, Sola A, Pi F, Alfaro V, Marco A, Hotter G. Nucleotides modulate renal ischaemia-reperfusion injury by different effects on nitric oxide and superoxide. Clin Exp Pharmacol Physiol 30: 242-248, 2003.
27. Lopez-Neblina F, Paez AJ, Toledo AH, Toledo-Pereyra LH. Role of nitric oxide in ischemia/reperfusion of the rat kidney. Circ Shock 44: 91-95, 1994.
28. Michelakis E, Tymchak W, Lien D, Webster L, Hashimoto K, Archer S. Oral sildenafil is an effective and specific pulmonary vasodilator in patients with pulmonary arterial hypertension: comparison with inhaled nitric oxide. Circulation 105: 2398-2403, 2002.
29. Noiri E, Peresleni T, Miller F, Goligorsky MS. In vivo targeting of inducible NO synthase with oligodeoxynucleotides protects rat kidney against ischemia. J Clin Invest 97: 2377-2383, 1996.
30. Ockaili R, Salloum F, Hawkins J, Kukreja RC. Sildenafil (Viagra) induces powerful cardioprotective effect via opening of mitochondrial K(ATP) channels in rabbits. Am J Physiol Heart Circ Physiol 283: H1263-H1269, 2002.
31. Park KM, Byun JY, Kramers C, Kim JI, Huang PL, Bonventre JV. Inducible nitric-oxide synthase is an important contributor to prolonged protective effects of ischemic preconditioning in the mouse kidney. J Biol Chem 278: 27256-27266, 2003.
32. Rodriguez-Iturbe B, Ferrebuz A, Vanegas V, Quiroz Y, Espinoza F, Pons H, Vaziri ND. Early treatment with cGMP phosphodiesterase inhibitor ameliorates progression of renal damage. Kidney Int 68: 2131-2142, 2005.
33. Saikumar P, Dong Z, Patel Y, Hall K, Hopfer U, Weinberg JM, Venkatachalam MA. Role of hypoxia-induced Bax translocation and cytochrome c release in reoxygenation injury. Oncogene 17: 3401-3415, 1998.
34. Saikumar P, Dong Z, Weinberg JM, Venkatachalam MA. Mechanisms of cell death in hypoxia/reoxygenation injury. Oncogene 17: 3341-3349, 1998.
35. Salloum F, Yin C, Xi L, Kukreja RC. Sildenafil induces delayed preconditioning through inducible nitric oxide synthase-dependent pathway in mouse heart. Circ Res 92: 595-597, 2003.
36. Shoskes DA, Xie Y, Gonzalez-Cadavid NF. Nitric oxide synthase activity in renal ischemia-reperfusion injury in the rat: implications for renal transplantation. Transplantation 63: 495-500, 1997.
37. Thadhani R, Pascual M, Bonventre JV. Acute renal failure. N Engl J Med 334: 1448-1460, 1996.
38. Torras J, Herrero-Fresneda I, Lloberas N, Riera M, Ma Cruzado J, Ma Grinyo J. Promising effects of ischemic preconditioning in renal transplantation. Kidney Int 61: 2218-2227, 2002.
39. Troppmann C, Gillingham KJ, Benedetti E, Almond PS, Gruessner RW, Najarian JS, Matas AJ. Delayed graft function, acute rejection, and outcome after cadaver renal transplantation. The multivariate analysis. Transplantation 59: 962-968, 1995.
40. Vinas JL, Sola A, Genesca M, Alfaro V, Pi F, Hotter G. NO and NOS isoforms in the development of apoptosis in renal ischemia/reperfusion. Free Radic Biol Med 40: 992-1003, 2006.
41. Walker LM, Walker PD, Imam SZ, Ali SF, Mayeux PR. Evidence for peroxynitrite formation in renal ischemia-reperfusion injury: studies with the inducible nitric oxide synthase inhibitor L-N(6)-(1-iminoethyl)lysine. J Pharmacol Exp Ther 295: 417-422, 2000.
42. Waller HL, Harper SJ, Hosgood SA, Bagul A, Kay MD, Kaushik M, Yang B, Bicknell GR, Nicholson ML. Differential expression of cytoprotective and apoptotic genes in an ischaemia-reperfusion isolated organ perfusion model of the transplanted kidney. Transpl Int 20: 625-631, 2007.
43. Xu Z, Ji X, Boysen PG. Exogenous nitric oxide generates ROS and induces cardioprotection: involvement of PKG, mitochondrial KATP channels, and ERK. Am J Physiol Heart Circ Physiol 286: H1433-H1440, 2004.
44. Yamashita J, Ogata M, Itoh M, Yamasowa H, Shimeda Y, Takaoka M, Matsumura Y. Role of nitric oxide in the renal protective effects of ischemic preconditioning. J Cardiovasc Pharmacol 42: 419-427, 2003.
45. Yamasowa H, Shimizu S, Inoue T, Takaoka M, Matsumura Y. Endothelial nitric oxide contributes to the renal protective effects of ischemic preconditioning. J Pharmacol Exp Ther 312: 153-159, 2005.
46. Yu L, Gengaro PE, Niederberger M, Burke TJ, Schrier RW. Nitric oxide: a mediator in rat tubular hypoxia/reoxygenation injury. Proc Natl Acad Sci USA 91: 1691-1695, 1994.
47. Yuan Z, Hein TW, Rosa RH Jr, Kuo L. Sildenafil (Viagra) evokes retinal arteriolar dilation: dual pathways via NOS activation and phosphodiesterase inhibition. Invest Ophthalmol Vis Sci 49: 720-725, 2008.