Olaparib protects cardiomyocytes against oxidative stress and improves graft contractility during the early phase after heart transplantation in rats

British Journal of Pharmacology

Volumn 175, Issue 2, 2018, Pages 246-261

  Korkmaz Icöz, Sevil ^a   Szczesny, Bartosz ^b   Marcatti, Michela ^b   Li, Shiliang ^a   Ruppert, Mihály ^a   Lasitschka, Felix ^c   Loganathan, Sivakkanan ^a   Szabó, Csaba ^b   Szabó, Gábor ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b University of Texas Medical Branch School of Medicine   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 12; CATALASE; GLUCOSE OXIDASE; HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; PROTEIN C JUN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PHTHALAZINE DERIVATIVE; PIPERAZINE DERIVATIVE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTECTIVE AGENT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC MUSCLE CELL; CELL DEATH; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION; HEART GRAFT; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CONTRACTILITY; HEART PROTECTION; HEART TRANSPLANTATION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; ANIMAL; CELL CULTURE; CELL SURVIVAL; DRUG EFFECT; METABOLISM; PROCEDURES;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; GENE EXPRESSION; HEART TRANSPLANTATION; MALE; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PHTHALAZINES; PIPERAZINES; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; PROTECTIVE AGENTS; RATS; VENTRICULAR FUNCTION, LEFT;

EID: 85044660428     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13983     Document Type: Article

References (83)

1. Ahmad A, Olah G, Herndon DN, Szabo C (2018). The clinically used PARP inhibitor olaparib improves organ function, suppresses inflammatory responses and accelerates wound healing in a murine model of third-degree burn injury. Br J Pharmacol 175: 232–245.
2. Alexander SPH, Fabbro D, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015). The Concise Guide to PHARMACOLOGY 2015/16: Enzymes. Br J Pharmacol 172: 6024–6109.
3. Bajaj G, Sharma RK (2006). TNF-alpha-mediated cardiomyocyte apoptosis involves caspase-12 and calpain. Biochem Biophys Res Commun 345: 1558–1564.
4. Berger NA (1985). Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res 101: 4–15.
5. Berger NA, Whitacre CM, Hashimoto H, Berger SJ, Chatterjee S (1995). NAD and poly(ADP-ribose) regulation of proteins involved in response to cellular stress and DNA damage. Biochimie 77: 364–367.
6. Berger NA, Besson VC, Boulares AH, Bürkle A, Chiarugi A, Clark RS et al. (2018). Opportunities for the repurposing of PARP inhibitors for the therapy of non-oncological diseases. Br J Pharmacol 175: 192–222.
7. Booz GW (2007). PARP inhibitors and heart failure – translational medicine caught in the act. Congest Heart Fail 13: 105–112.
8. Bowes J, Ruetten H, Martorana PA, Stockhausen H, Thiemermann C (1998). Reduction of myocardial reperfusion injury by an inhibitor of poly (ADP-ribose) synthetase in the pig. Eur J Pharmacol 359: 143–150.
9. Brunyanszki A, Szczesny B, Virág L, Szabó C (2016). Mitochondrial poly(ADP-ribose) polymerase: the Wizard of Oz at work. Free Radic Biol Med 100: 257–270.
10. Curtin NJ, Szabó C (2013). Therapeutic applications of PARP inhibitors: anticancer therapy and beyond. Mol Aspects Med 34: 1217–1256.
11. Curtis MJ, Bond RA, Spina D, Ahluwalia A, Alexander SP, Giembycz MA et al. (2015). Experimental design and analysis and their reporting: new guidance for publication in BJP. Br J Pharmacol 172: 3461–3471.
12. Deeks ED (2015). Olaparib: first global approval. Drugs 75: 231–240.
13. Docherty JC, Kuzio B, Silvester JA, Bowes J, Thiemermann C (1999). An inhibitor of poly (ADP-ribose) synthetase activity reduces contractile dysfunction and preserves high energy phosphate levels during reperfusion of the ischaemic rat heart. Br J Pharmacol 127: 1518–1524.
14. Drew Y (2015). The development of PARP inhibitors in ovarian cancer: from bench to bedside. Br J Cancer 113: S3–S9.
15. Eltze T, Boer R, Wagner T, Weinbrenner S, McDonald MC, Thiemermann C (2008). Imidazoquinolinone, imidazopyridine, and isoquinolindione derivatives as novel and potent inhibitors of the poly(ADP-ribose) polymerase (PARP): a comparison with standard PARP inhibitors. Mol Pharmacol 74: 1587–1598.
16. Ferdinandy P, Schulz R, Baxter GF (2007). Interaction of cardiovascular risk factors with myocardial ischemia/reperfusion injury, preconditioning, and postconditioning. Pharmacol Rev 59: 418–458.
17. Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R (2014). Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev 66: 1142–1174.
18. Fiorillo C, Pace S, Ponziani V, Nediani C, Perna AM, Liguori P et al. (2002). Poly(ADP-ribose) polymerase activation and cell injury in the course of rat heart heterotopic transplantation. Free Radic Res 36: 79–87.
19. Fiorillo C, Ponziani V, Giannini L, Cecchi C, Celli A, Nediani C et al. (2003). Beneficial effects of poly (ADP-ribose) polymerase inhibition against the reperfusion injury in heart transplantation. Free Radic Res 37: 331–339.
20. Gao L, Kwan JC, Macdonald PS, Yang L, Preiss T, Hicks M (2007). Improved poststorage cardiac function by poly (ADP-ribose) polymerase inhibition: role of phosphatidylinositol 3-kinase Akt pathway. Transplantation 84: 380–386.
21. García de la Cadena S, Massieu L (2016). Caspases and their role in inflammation and ischemic neuronal death. Focus on caspase-12. Apoptosis 21: 763–777.
22. Garcia Soriano F, Virág L, Jagtap P, Szabó E, Mabley JG, Liaudet L et al. (2001). Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nat Med 7: 108–113.
23. Gariani K, Ryu D, Menzies KJ, Yi HS, Stein S, Zhang H et al. (2017). Inhibiting poly ADP-ribosylation increases fatty acid oxidation and protects against fatty liver disease. J Hepatol 66: 132–141.
24. Gerö D, Szoleczky P, Chatzianastasiou A, Papapetropoulos A, Szabó C (2014). Modulation of poly(ADP-ribose) polymerase-1 (PARP-1)-mediated oxidative cell injury by ring finger protein 146 (RNF146) in cardiac myocytes. Mol Med 20: 313–328.
25. Ghonim MA, Pyakurel K, Ibba SV, Al-Khami AA, Wang J, Rodriguez P et al. (2015a). PARP inhibition by olaparib or gene knockout blocks asthma-like manifestation in mice by modulating CD4(+) T cell function. J Transl Med 13: 225.
26. Ghonim MA, Pyakurel K, Ibba SV, Wang J, Rodriguez P, Al-Khami AA et al. (2015b). PARP is activated in human asthma and its inhibition by olaparib blocks house dust mite-induced disease in mice. Clin Sci (Lond) 129: 951–962.
27. Gibson BA, Kraus WL (2012). New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13: 411–424.
28. Gilad E, Zingarelli B, Salzman AL, Szabó C (1997). Protection by inhibition of poly (ADP-ribose) synthetase against oxidant injury in cardiac myoblasts in vitro. J Mol Cell Cardiol 29: 2585–2597.
29. Goulooze SC, Cohen AF, Rissmann R (2016). Olaparib. Br J Clin Pharmacol 81: 171–173.
30. Grupp IL, Jackson TM, Hake P, Grupp G, Szabó C (1999). Protection against hypoxia-reoxygenation in the absence of poly (ADP-ribose) synthetase in isolated working hearts. J Mol Cell Cardiol 31: 297–303.
31. Gupte R, Liu Z, Kraus WL (2017). PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes. Genes Dev 31: 101–126.
32. Ha HC, Snyder SH (1999). Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci U S A 96: 13978–13982.
33. Hearse DJ, Bolli R (1992). Reperfusion induced injury: manifestations, mechanisms, and clinical relevance. Cardiovasc Res 26: 101–108.
34. Horváth EM, Benko R, Kiss L, Murányi M, Pék T, Fekete K et al. (2009). Rapid 'glycaemic swings' induce nitrosative stress, activate poly(ADP-ribose) polymerase and impair endothelial function in a rat model of diabetes mellitus. Diabetologia 52: 952–961.
35. Huang D, Wang Y, Yang C, Liao Y, Huang K (2009). Angiotensin II promotes poly(ADP-ribosyl)ation of c-Jun/c-Fos in cardiac fibroblasts. J Mol Cell Cardiol 46: 25–32.
36. Jagtap P, Szabó C (2005). Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 4: 421–440.
37. Jang KH, Do YJ, Son D, Son E, Choi JS, Kim E (2017). AIF-independent parthanatos in the pathogenesis of dry age-related macular degeneration. Cell Death Dis 8: e2526.
38. Kaplan J, O'Connor M, Hake PW, Zingarelli B (2005). Inhibitors of poly (ADP-ribose) polymerase ameliorate myocardial reperfusion injury by modulation of activator protein-1 and neutrophil infiltration. Shock 23: 233–238.
39. Kapoor K, Singla E, Sahu B, Naura AS (2015). PARP inhibitor, olaparib ameliorates acute lung and kidney injury upon intratracheal administration of LPS in mice. Mol Cell Biochem 400: 153–162.
40. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577–1579.
41. Kim J, Long KE, Tang K, Padanilam BJ (2012). Poly(ADP-ribose) polymerase 1 activation is required for cisplatin nephrotoxicity. Kidney Int 82: 193–203.
42. Liaudet L, Szabó E, Timashpolsky L, Virág L, Cziráki A, Szabó C (2001). Suppression of poly (ADP-ribose) polymerase activation by 3-aminobenzamide in a rat model of myocardial infarction: long-term morphological and functional consequences. Br J Pharmacol 133: 1424–1430.
43. Liaudet L, Pacher P, Virág L, Soriano FG, Hasko G, Szabó C (2002). Activation of poly(ADP-ribose) polymerase is a central mechanism of lipopolysaccharide-induced acute pulmonary inflammation. Am J Respir Crit Care Med 165: 372–377.
44. Liu Y, Son NH, Szabólcs MJ, Ma N, Sciacca RR, Albala A (2004). Effects of inhibition of poly(adenosine diphosphate-ribose) synthase on acute cardiac allograft rejection. Transplantation 78: 668–674.
45. Loganathan S, Korkmaz-Icoz S, Radovits T, Li S, Mikles B, Barnucz E et al. (2015). Effects of soluble guanylate cyclase activation on heart transplantation in a rat model. J Heart Lung Transplant 34: 1346–1353.
46. Mabley JG, Jagtap P, Perretti M, Getting SJ, Salzman AL, Virág L et al. (2001). Anti-inflammatory effects of a novel, potent inhibitor of poly (ADP-ribose) polymerase. Inflamm Res 50: 561–569.
47. McGrath JC, Lilley E (2015). Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. Br J Pharmacol 172: 3189–3193.
48. Mester L, Szabó A, Atlasz T, Szabadfi K, Reglodi D, Kiss P 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.
49. Módis K, Gero D, Erdélyi K, Szoleczky P, DeWitt D, Szabó C (2012). Cellular bioenergetics is regulated by PARP1 under resting conditions and during oxidative stress. Biochem Pharmacol 83: 633–643.
50. Morrow DA, Brickman CM, Murphy SA, Baran K, Krakover R, Dauerman H et al. (2009). A randomized, placebo-controlled trial to evaluate the tolerability, safety, pharmacokinetics, and pharmacodynamics of a potent inhibitor of poly(ADP-ribose) polymerase (INO-1001) in patients with ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention: results of the TIMI 37 trial. J Thromb Thrombolysis 27: 359–364.
51. Mukhopadhyay P, Horváth B, Rajesh M, Varga ZV, Gariani K, Ryu D et al. (2017). PARP inhibition protects against alcoholic and non-alcoholic steatohepatitis. J Hepatol 66: 589–600.
52. Oh KS, Lee S, Yi KY, Seo HW, Koo HN, Lee BH (2009). A novel and orally active poly(ADP-ribose) polymerase inhibitor, KR-33889 [2-[methoxycarbonyl(4-methoxyphenyl) methylsulfanyl]-1H-benzimidazole-4-carboxylic acid amide], attenuates injury in in vitro model of cell death and in vivo model of cardiac ischemia. J Pharmacol Exp Ther 328: 10–18.
53. Olah G, Szczesny B, Brunyánszki A, López-García IA, Gerö D, Radák Z et al. (2015). Differentiation-associated downregulation of poly(ADP-ribose) polymerase-1 expression in myoblasts serves to increase their resistance to oxidative stress. PLoS One 10: e0134227.
54. Pacher P, Szabó C (2008). Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. Am J Pathol 173: 2–13.
55. Pacher P, Nagayama T, Mukhopadhyay P, Batkai S, Kass DA (2008). Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 3: 1422–1434.
56. Pieper AA, Walles T, Wei G, Clements EE, Verma A, Snyder SH et al. (2000). Myocardial postischemic injury is reduced by polyADPripose polymerase-1 gene disruption. Mol Med 6: 271–282.
57. Radnai B, Antus C, Racz B, Engelmann P, Priber JK, Tucsek Z et al. (2012). Protective effect of the poly(ADP-ribose) polymerase inhibitor PJ34 on mitochondrial depolarization-mediated cell death in hepatocellular carcinoma cells involves attenuation of c-Jun N-terminal kinase-2 and protein kinase B/Akt activation. Mol Cancer 11: 34.
58. Radovits T, Zotkina J, Lin LN, Bömicke T, Arif R, Gerö D et al. (2007). Poly(ADP-Ribose) polymerase inhibition improves endothelial dysfunction induced by hypochlorite. Exp Biol Med (Maywood) 232: 1204–1212.
59. Roesner JP, Mersmann J, Bergt S, Bohnenberg K, Barthuber C, Szabó 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.
60. Song ZF, Ji XP, Li XX, Wang SJ, Wang SH, Zhang Y (2008). Inhibition of the activity of poly (ADP-ribose) polymerase reduces heart ischaemia/reperfusion injury via suppressing JNK-mediated AIF translocation. J Cell Mol Med 12: 1220–1228.
61. Song ZF, Chen DY, Du B, Ji XP (2013). Poly (ADP-ribose) polymerase inhibitor reduces heart ischaemia/reperfusion injury via inflammation and Akt signalling in rats. Chin Med J (Engl) 126: 1913–1917.
62. Sosna J, Voigt S, Mathieu S, Lange A, Thon L, Davarnia P et al. (2014). TNF-induced necroptosis and PARP-1-mediated necrosis represent distinct routes to programmed necrotic cell death. Cell Mol Life Sci 71: 331–348.
63. Southan C, Sharman JL, Benson HE, Faccenda E, Pawson AJ, Alexander SPH et al. (2016). The IUPHAR/BPS guide to PHARMACOLOGY in 2016: towards curated quantitative interactions between 1300 protein targets and 6000 ligands. Nucl Acids Res 44: D1054–D1068.
64. Szabó C (1998). Role of poly (ADP-ribose) synthetase in inflammation. Eur J Pharmacol 350: 1–19.
65. Szabó C, Lim LH, Cuzzocrea S, Getting SJ, Zingarelli B, Flower RJ et al. (1997). Inhibition of poly (ADP-ribose) synthetase attenuates neutrophil recruitment and exerts anti-inflammatory effects. J Exp Med 186: 1041–1049.
66. Szabó G, Bährle S, Stumpf N, Sonnenberg K, Szabó EE, Pacher P et al. (2002). Poly(ADP-Ribose) polymerase inhibition reduces reperfusion injury after heart transplantation. Circ Res 90: 100–106.
67. Szabó G, Liaudet L, Hagl S, Szabó C (2004). Poly(ADP-ribose) polymerase activation in the reperfused myocardium. Cardiovasc Res 61: 471–480.
68. Szabó G, Soós P, Heger U, Flechtenmacher C, Bährle S, Zsengellér Z et al. (2005). Poly(ADP-ribose) polymerase inhibition attenuates biventricular reperfusion injury after orthotopic heart transplantation. Eur J Cardiothorac Surg 27: 226–234.
69. Szabó G, Bährle S, Sivanandam V, Stumpf N, Gerö D, Berger I 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.
70. Szczesny B, Módis K, Yanagi K, Coletta C, Le Trionnaire S, Perry A et al. (2014). AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide 41: 120–130.
71. Teng F, Zhu L, Su J, Zhang X, Li N, Nie Z et al. (2016). Neuroprotective effects of poly(ADP-ribose)polymerase inhibitor olaparib in transient cerebral ischemia. Neurochem Res 41: 1516–1526.
72. Thiemermann C, Bowes J, Myint FP, Vane JR (1997). Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc Natl Acad Sci U S A 94: 679–683.
73. Virág L, Szabó C (2002). The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 54: 375–429.
74. Virág L, Scott GS, Cuzzocrea S, Marmer D, Salzman AL, Szabó C (1998). Peroxynitrite-induced thymocyte apoptosis: the role of caspases and poly (ADP-ribose) synthetase (PARS) activation. Immunology 94: 345–355.
75. Virág L, Robaszkiewicz A, Rodriguez-Vargas JM, Oliver FJ (2013). Poly(ADP-ribose) signaling in cell death. Mol Aspects Med 34: 1153–1167.
76. Xiao LY, Kan WM (2017). Poly ADP-ribose polymerase inhibition suppresses cisplatin toxicity in chronic myeloid leukemia cells. Anticancer Drugs 28: 316–321.
77. Xu JC, Fan J, Wang X, Eacker SM, Kam TI, Chen L et al. (2016). Cultured networks of excitatory projection neurons and inhibitory interneurons for studying human cortical neurotoxicity. Sci Transl Med 8: 333ra48.
78. Yang Z, Zingarelli B, Szabó C (2000). Effect of genetic disruption of poly (ADP-ribose) synthetase on delayed production of inflammatory mediators and delayed necrosis during myocardial ischemia-reperfusion injury. Shock 13: 60–66.
79. Zingarelli B, Cuzzocrea S, Zsengellér Z, Salzman AL, Szabó C (1997). Protection against myocardial ischemia and reperfusion injury by 3-aminobenzamide, an inhibitor of poly (ADP-ribose) synthetase. Cardiovasc Res 36: 205–215.
80. Zingarelli B, Salzman AL, Szabó C (1998). Genetic disruption of poly (ADP-ribose) synthetase inhibits the expression of P-selectin and intercellular adhesion molecule-1 in myocardial ischemia/reperfusion injury. Circ Res 83: 85–94.
81. Zingarelli B, Szabó C, Salzman AL (1999). Blockade of Poly(ADP-ribose) synthetase inhibits neutrophil recruitment, oxidant generation, and mucosal injury in murine colitis. Gastroenterology 116: 335–345.
82. Zingarelli B, Hake PW, O'Connor M, Denenberg A, Kong S, Aronow BJ (2003). Absence of poly(ADP-ribose)polymerase-1 alters nuclear factor-kappa B activation and gene expression of apoptosis regulators after reperfusion injury. Mol Med 9: 143–153.
83. Zingarelli B, Hake PW, O'Connor M, Denenberg A, Wong HR, Kong S et al. (2004). Differential regulation of activator protein-1 and heat shock factor-1 in myocardial ischemia and reperfusion injury: role of poly(ADP-ribose) polymerase-1. Am J Physiol Heart Circ Physiol 286: H1408–H1415.