PARP inhibition attenuates acute kidney allograft rejection by suppressing cell death pathways and activating PI-3K-Akt cascade

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Kalmar Nagy, Karoly ^a   Degrell, Peter ^a   Szabo, Aliz ^a   Sumegi, Katalin ^a   Wittmann, Istvan ^a   Gallyas Jr , Ferenc ^a,b   Sumegi, Balazs ^a,b  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYQUINAZOLINE; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE REPRESSION; GRAFT SURVIVAL; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY ALLOGRAFT REJECTION; KIDNEY INTERSTITIUM; KIDNEY TRANSPLANTATION; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; SIGNAL TRANSDUCTION;

ALLOGRAFTS; ANIMALS; CELL DEATH; CYTOPROTECTION; ENZYME INHIBITORS; GRAFT REJECTION; IMMUNOSUPPRESSIVE AGENTS; KIDNEY; KIDNEY TRANSPLANTATION; MALE; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; SIGNAL TRANSDUCTION;

EID: 84891714115     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081928     Document Type: Article

References (64)

1. Kellum JA (2008) Acute kidney injury. Crit Care Med 36: S141-145.
2. Ojo AO, Wolfe RA, Held PJ, Port FK, Schmouder RL (1997) Delayed graft function: risk factors and implications for renal allograft survival. Transplantation 63: 968-974.
3. de Menezes Neves PD, Machado JR, dos Reis MA, Faleiros AC, de Lima Pereira SA, et al. (2013) Distinct expression of interleukin 17, tumor necrosis factor α, transforming growth factor β, and forkhead box P3 in acute rejection after kidney transplantation. Ann Diagn Pathol 17: 75-79.
4. Sacks S, Karegli J, Farrar CA, Asgari E, Schwaeble W, et al. (2013) Targeting complement at the time of transplantation. Adv Exp Med Biol 735: 247-255.
5. Bedke J, Nelson PJ, Kiss E, Muenchmeier N, Rek A, et al. (2010) A novel CXCL8 protein-based antagonist in acute experimental renal allograft damage. Mol Immunol 47: 1047-1057.
6. Joo DJ, Huh KH, Cho Y, Jeong JH, Kim JY, et al. (2010) Change in serum lipid peroxide as an oxidative stress marker and its effects on kidney function after successful kidney transplantation. Transplant Proc 42: 729-732.
7. O'Connell S, Tuite N, Slattery C, Ryan MP, McMorrow T (2012) Cyclosporine A - induced oxidative stress in human renal mesangial cells: a role for ERK 1/2 MAPK signaling. Toxicol Sci126: 101-113.
8. Kidokoro K, Satoh M, Nagasu H, Sakuta T, Kuwabara A, et al. (2012) Tacrolimus Induces Glomerular Injury via Endothelial Dysfunction Caused by Reactive Oxygen Species and Inflammatory Change. Kidney Blood Press Res 35: 549-557.
9. Cassis P, Azzollini N, Solini S, Mister M, Aiello S, et al. (2011) Both darbepoetin alfa and carbamylated erythropoietin prevent kidney graft dysfunction due to ischemia/reperfusion in rats. Transplantation 92: 271-279.
10. Rogers NM, Stephenson MD, Kitching AR, Horowitz JD, Coates PT (2012) Amelioration of renal ischaemia-reperfusion injury by liposomal delivery of curcumin to renal tubular epithelial and antigen-presenting cells. Br J Pharmacol 166: 194-209.
11. Li X, Nemoto M, Xu Z, Yu SW, Shimoji M, et al. (2007) Influence of duration of focal cerebral ischemia and neuronal nitric oxide synthase on translocation of apoptosis-inducing factor to the nucleus. Neuroscience 144: 56-65.
12. Pacher P, Szabo C (2008) Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. Am J Pathol 173: 2-13.
13. Lee YR, Yu DS, Liang YC, Huang KF, Chou SJ, et al. (2013) Approaches of PARP-1 Inhibitors in Human Lung Cancer Cells and Cancer Stem-Like Cells by Some Selected Anthraquinone-Derived Small Molecules. PLoS One 8: e56284.
14. Lakatos P, Szabo E, Hegedus C, Hasko G, Gergely P, et al. (2013) 3-Aminobenzamide protects primary human keratinocytes from UV-induced cell death by a poly(ADP-ribosyl)ation independent mechanism. Biochim Biophys Acta1833: 743-751.
15. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, et al. (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263.
16. Veres B, Radnai B, Gallyas F Jr, Varbiro G, Berente Z, et al. (2004) Regulation of kinase cascades and transcription factors by a poly(ADP-ribose) polymerase-1 inhibitor, 4-hydroxyquinazoline, in lipopolysaccharide-induced inflammation in mice. J Pharmacol Exp Ther 310:247-255.
17. Wyrsch P, Blenn C, Bader J, Althaus FR(2012) Cell death and autophagy under oxidative stress: roles of poly(ADP-Ribose) polymerases and Ca(2+). Mol Cell Biol 32: 3541-3553.
18. Mester L, Szabo A, Atlasz T, Szabadfi K, Reglodi D, et al. (2009) Protection against chronic hypoperfusion-induced retinal neurodegeneration by PARP inhibition via activation of PI-3-kinase Akt pathway and suppression of JNK and p38 MAP kinases. Neurotox Res 16: 68-76.
19. Racz B, Hanto K, Tapodi A, Solti I, Kalman N, et al. (2010) Regulation of MKP-1 expression and MAPK activation by PARP-1 in oxidative stress: a new mechanism for the cytoplasmic effect of PARP-1 activation. Free Radic Biol Med 49: 1978-1988.
20. Veres B, Gallyas F Jr, Varbiro G, Berente Z, Osz E, et al. (2003) Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly-(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem Pharmacol 65: 1373-1382.
21. Bartha E, Solti I, Kereskai L, Lantos J, Plozer E, et al. (2009) PARP inhibition delays transition of hypertensive cardiopathy to heart failure in spontaneously hypertensive rats. Cardiovasc Res 83: 501-510.
22. Abd Elmageed ZY, Naura AS, Errami Y, Zerfaoui M(2012) The poly(ADP-ribose) polymerases (PARPs): new roles in intracellular transport. Cell Signal24: 1-8.
23. Germain M, Affar EB, D'Amours D, Dixit VM, Salvesen GS, et al. (1999) Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J Biol Chem 274: 28379-28384.
24. Szabo C, Zanchi A, Komjati K, Pacher P, Krolewski ASet al. (2002) Poly(ADPRibose) polymerase is activated in subjects at risk of developing type 2 diabetes and is associated with impaired vascular reactivity. Circulation 106:2680-2686.
25. Nasrabady SE, Kuzhandaivel A, Akrami A, Bianchetti E, Milanese M, et al. (2012) Unusual increase in lumbar network excitability of the rat spinal cord evoked by the PARP-1 inhibitor PJ-34 through inhibition of glutamate uptake. Neuropharmacology 63: 415-426.
26. Pacher P, Szabo C(2005) Role of poly(ADP-ribose) polymerase-1 activation in the pathogenesis of diabetic complications: endothelial dysfunction, as a common underlying theme. Antioxid Redox Signal 7: 1568-1580.
27. Kovacs K, Toth A, Deres P, Kalai T, Hideg K, et al. (2006) Critical role of PI3-kinase/Akt activation in the PARP inhibitor induced heart function recovery during ischemia-reperfusion. Biochem Pharmacol 71: 441-452.
28. Roesner JP, Mersmann J, Bergt S, Bohnenberg K, Barthuber C, et al. (2010) Therapeutic injection of PARP inhibitor INO-1001 preserves cardiac function in porcine myocardial ischemia and reperfusion without reducing infarct size. Shock 33: 507-512.
29. Xu B, Chiu J, Feng B, Chen S, Chakrabarti S (2008) PARP activation and the alteration of vasoactive factors and extracellular matrix protein in retina and kidney in diabetes. Diabetes Metab Res Rev 24: 404-412.
30. Rajesh M, Mukhopadhyay P, Godlewski G, Batkai S, Hasko G, et al. (2006) Poly(ADP-ribose)polymerase inhibition decreases angiogenesis. Biochem Biophys Res Commun 350: 1056-1062.
31. Halmosi R, Berente Z, Osz E, Toth K, Literati-Nagy P, et al. (2001) Effect of poly(ADP-ribose) polymerase inhibitors on the ischemia-reperfusion- induced oxidative cell damage and mitochondrial metabolism in Langendorff heart perfusion system. Mol Pharmacol 59: 1497-1505.
32. Veto S, Acs P, Bauer J, Lassmann H, Berente Z, et al. (2010) Inhibiting poly(ADP-ribose) polymerase: a potential therapy against oligodendrocyte death. Brain 133: 822-834.
33. Lee S (1967) An improved technique of renal transplantation in the rat. Surgery 61: 771-773.
34. Lindahl T, Satoh MS, Poirier GG, Klungland A. (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20: 405-411.
35. Nguyen KC, Willmore WG, Tayabali AF (2013) Cadmium telluride quantum dots cause oxidative stress leading to extrinsic and intrinsic apoptosis in hepatocellular carcinoma HepG2 cells. Toxicology306C: 114-123.
36. Hseu YC, Chou CW, Senthil Kumar KJ, Fu KT, et al. (2012) Ellagic acid protects human keratinocyte (HaCaT) cells against UVA-induced oxidative stress and apoptosis through the upregulation of the HO-1 and Nrf-2 antioxidant genes. Food Chem Toxicol 50: 1245-1255.
37. Fu H, Chen H, Wang C, Xu H, Liu F, et al. (2012) Flurbiprofen, a cyclooxygenase inhibitor, protects mice from hepatic ischemia/reperfusion injury by inhibiting GSK-3β signaling and mitochondrial permeability transition. Mol Med 18: 1128-1135.
38. Latchoumycandane C, Seah QM, Tan RC, Sattabongkot J, Beerheide W, et al. (2006) Leflunomide or A77 1726 protect from acetaminophen-induced cell injury through inhibition of JNK-mediated mitochondrial permeability transition in immortalized human hepatocytes. Toxicol Appl Pharmacol 217: 125-133.
39. Theruvath TP, Snoddy MC, Zhong Z, Lemasters JJ. (2008) Mitochondrial permeability transition in liver ischemia and reperfusion: role of c-Jun N-terminal kinase 2. Transplantation 85: 1500-1504.
40. Kȩdzierska K, Domański M, Sporniak-Tutak K, Dołȩgowska B, Ciechanowski K (2011) Oxidative stress and renal interstitial fibrosis in patients after renal transplantation: current state of knowledge. Transplant Proc 43: 3577-3583.
41. Erne BV, Jungraithmayr W, Buschmann J, Arni S, Weder W, et al. (2013) Effect of N-acetylcysteine on acute allograft rejection after rat lung transplantation. Ann Thorac Surg 95: 1021-1027.
42. D'Amico F, Vitale A, Piovan D, Bertacco A, Ramirez Morales R, et al. (2013) Use of N-acetylcysteine during liver procurement: a prospective randomized controlled study. Human Liver Transpl 19: 135-144.
43. Danilovic A, Lucon AM, Srougi M, Shimizu MH, Ianhez LE, et al. (2011) Protective effect of N-acetylcysteine on early outcomes of deceased renal transplantation. Transplant Proc 43: 1443-1449.
44. Ruiz Fuentes MC, Moreno Ayuso JM, Ruiz Fuentes N, Vargas Palomares JF, Asensio Peinado C, et al. (2008) Treatment with N-acetylcysteine in stable renal transplantation. Transplant Proc 40: 2897-2899.
45. Ying W, Alano CC, Garnier P, Swanson RA (2005) NAD+ as a metabolic link between DNA damage and cell death. J Neurosci Res 79: 216-223.
46. Tapodi A, Debreceni B, Hanto K, Bognar Z, Wittmann I, et al. (2005) Pivotal role of Akt activation in mitochondrial protection and cell survival by poly(ADP-ribose) polymerase-1 inhibition in oxidative stress. J Biol Chem 280: 35767- 35775.
47. Wang Y, Dawson VL, Dawson TM (2009) Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol 218: 193-202.
48. Komjáti K, Besson VC, Szabó C (2005) Poly (adp-ribose) polymerase inhibitors as potential therapeutic agents in stroke and neurotrauma. Curr Drug Targets CNS Neurol Disord 4: 179-194.
49. Szabó G, Bährle S, Sivanandam V, Stumpf N, Gerö D, et al. (2006) Immunomodulatory effects of poly(ADP-ribose) polymerase inhibition contribute to improved cardiac function and survival during acute cardiac rejection. J Heart Lung Transplant 25: 794-804.
50. Szabó G, Bährle S, Stumpf N, Szabó C, Hagl S (2006) Contractile dysfunction in experimental cardiac allograft rejection: role of the poly (ADP-ribose) polymerase pathway. Transpl Int 19: 506-513.
51. Farivar AS, McCourtie AS, MacKinnon-Patterson BC, Woolley SM, Barnes AD, et al. (2005) Poly (ADP) ribose polymerase inhibition improves rat cardiac allograft survival. Ann Thorac Surg 80: 950-956.
52. Garber K. (2013) PARP inhibitors bounce back. Nat Rev Drug Discov 12:725-727.
53. Ekblad T, Camaioni E, Schüler H, Macchiarulo A. (2013) PARP inhibitors: polypharmacology versus selective inhibition. FEBS J 280:3563-3575.
54. Zhang F, Wang Y, Wang L, Luo X, Huang K, et al. (2013) Poly(ADP-ribose) polymerase 1 is a key regulator of estrogen receptor α-dependent gene transcription. J Biol Chem 288:11348-11357.
55. Sarszegi Z, Bognar E, Gaszner B, Kónyi A, Gallyas F Jr, et al. (2012) BGP-15, a PARP-inhibitor, prevents imatinib-induced cardiotoxicity by activating Akt and suppressing JNK and p38 MAP kinases. Mol Cell Biochem 365: 129-137.
56. Rattanavich R, Plagov A, Kumar D, Rai P, Lederman R, et al. (2013) Deficit of p66ShcA restores redox-sensitive stress response program in cisplatin-induced acute kidney injury. Exp Mol Pathol 94: 445-452.
57. Kanai M, Hanashiro K, Kim SH, Hanai S, Boulares AH, et al. (2007) Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation. Nat Cell Biol 9: 1175-1183.
58. Rao P, Roccisana J, Takane KK, Bottino R, Zhao A, et al. (2005) Gene transfer of constitutively active Akt markedly improves human islet transplant outcomes in diabetic severe combined immunodeficient mice. Diabetes 54: 1664-1675.
59. Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, et al. (2007) Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9: 49-89.
60. Hsing CH, Lin MC, Choi PC, Huang WC, Kai JI, et al. (2011) Anesthetic propofol reduces endotoxic inflammation by inhibiting reactive oxygen species-regulated Akt/IKKβ/NF-κB signaling. PLoS One 6: e17598.
61. Schwabe RF, Uchinami H, Qian T, Bennett BL, Lemasters JJ, et al. (2004) Differential requirement for c-Jun NH2-terminal kinase in TNFalpha- and Fas-mediated apoptosis in hepatocytes. FASEB J 18: 720-722.
62. Xu Y, Huang S, Liu ZG, Han J. (2006) Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J Biol Chem 281: 8788-8795.
63. Ferencz A, Reglo di D, Kalmár-Nagy K, Horváth OP, Ro Th E, et al. (2009) Influence of pituitary adenylate cyclase-activating polypeptide on the activation of mitogen activated protein kinases following small bowel cold preservation. Transplant Proc 41: 60-62.
64. Varona-Santos JL, Pileggi A, Molano RD, Sanabria NY, Ijaz A, et al. (2008) c-Jun N-terminal kinase 1 is deleterious to the function and survival of murine pancreatic islets. Diabetologia 51: 2271-2280.