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Role of Peroxynitrite-Induced Activation of Poly(ADP-Ribose) Polymerase (PARP) in Circulatory Shock and Related Pathological Conditions

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Abstract

Peroxynitrite is a powerful oxidant, formed from the reaction of nitric oxide and superoxide. It is known to interact and modify different biological molecules such as DNA, lipids and proteins leading to alterations in their structure and functions. These events elicit various cellular responses, including cell signaling, causing oxidative damage and committing cells to apoptosis or necrosis. This review discusses nitrosative stress-induced modification in the DNA molecule that results in the formation of 8-nitroguanine and 8-oxoguanine, and its role in disease conditions. Different approaches of cell death, such as necrosis and apoptosis, are modulated by cellular high-energy species, such as ATP and NAD+. High concentrations of peroxynitrite are known to cause necrosis, whereas low concentrations lead to apoptosis. Any damage to DNA activates cellular DNA repair machinery, like poly(ADP-ribose) polymerase (PARP). PARP-1, an isoform of PARP, is a DNA nick-sensing enzyme that becomes activated upon sensing DNA breakage and triggers the cleavage of NAD+ into nicotinamide and ADP-ribose and polymerizes the latter on nuclear acceptor proteins. Peroxynitrite-induced hyperactivation of PARP causes depletion of NAD+ and ATP culminating cell dysfunction, necrosis or apoptosis. This mechanistic pathway is implicated in the pathogenesis of a variety of diseases, including circulatory shock (which is characterized by cellular hypoxia triggered by systemic altered perfusion and tissue oxygen utilization leading end-organ dysfunction), sepsis and inflammation, injuries of the lung and the intestine. The cytotoxic effects of peroxynitrite centering on the participation of PARP-1 and ADP-ribose in previously stated diseases have also been discussed in this review.

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Abbreviations

dG:

Deoxyguanosine

PARP:

Poly(ADP-ribose) polymerase

8-NitroG:

8-Nitroguanine

8-OxoG:

8-Oxoguanine

NI:

5-Guanidino-4-nitroimidazole

Iz:

2,5-Diamino-4H-imidazol-4-one

Oz:

2,2,4-Triamino-5(2H)-oxazolone

AAP:

Acetaminophen

5-AIQ:

5-Aminoisoquinoline

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

3AB:

3-Aminobenzamide

IR:

Ischemia–reperfusion

DNBS:

Dinitrobenzene sulfonic acid

TNBS:

Trinitrobenzene sulfonic acid

iNOS:

Inducible nitric oxide synthase

TNFα:

Tumor necrosis factor alpha

MODS:

Multiple organ dysfunction syndrome

HMGB1:

High-mobility group protein 1

AIF:

Apoptosis-inducing factor

PARG:

PAR glycohydrolase

NAD+ :

Nicotinamide adenine dinucleotide (oxidized)

References

  1. Denicola, A., Souza, J. M., & Radi, R. (1998). Diffusion of peroxynitrite across erythrocyte membranes. Proceedings of the National Academy of Sciences of the United States of America, 95, 3566–3571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Radi, R., Beckman, J. S., Bush, K. M., & Freeman, B. A. (1991). Peroxynitrite oxidation of sulfhydryls: The cytotoxic potential of superoxide and nitric oxide. Journal of Biological Chemistry, 266, 4244–4250.

    CAS  PubMed  Google Scholar 

  3. Bartesaghi, S., Valez, V., Trujillo, M., Peluffo, G., Romero, N., Zhang, H., et al. (2006). Mechanistic studies of peroxynitrite-mediated tyrosine nitration in membranes using the hydrophobic probe N-t-BOC-l-tyrosine tert-butyl ester. Biochemistry, 45, 6813–6825.

    Article  CAS  PubMed  Google Scholar 

  4. Quijano, C., Alvarez, B., Gatti, R., Augusto, O., & Radi, R. (1997). Pathways of peroxynitrite oxidation of thiol groups. Biochemical Journal, 322, 167–173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bonini, M. G., & Augusto, O. (2001). Carbon dioxide stimulates the production of thiyl, sulfinyl, and disulfide radical anion from thiol oxidation by peroxynitrite. Journal of Biological Chemistry, 276, 9749–9754.

    Article  CAS  PubMed  Google Scholar 

  6. Salgo, M. G., Bermudez, E., Squadrito, G. L., & Pryor, W. A. (1995). Peroxynitrite causes DNA damage and oxidation of thiols in rat thymocytes. Archives of Biochemistry and Biophysics, 322, 500–505.

    Article  CAS  PubMed  Google Scholar 

  7. Szabó, C., & Ohshima, H. (1997). DNA damage induced by peroxynitrite: Subsequent biological effects. Nitric Oxide, 1, 373–385.

    Article  PubMed  Google Scholar 

  8. Burney, S., Niles, J. C., Dedon, P. C., & Tannenbaum, S. R. (1999). DNA damage in deoxynucleosides and oligonucleotides treated with peroxynitrite. Chemical Research in Toxicology, 12, 513–520.

    Article  CAS  PubMed  Google Scholar 

  9. Niles, J. C., Wishnok, J. S., & Tannenbaum, S. R. (2006). Peroxynitrite-induced oxidation and nitration products of guanine and 8-oxoguanine: Structures and mechanisms of product formation. Nitric Oxide, 14, 109–121.

    Article  CAS  PubMed  Google Scholar 

  10. Kennedy, L. J., Moore, K., Jr., Caulfield, J. L., Tannenbaum, S. R., & Dedon, P. C. (1997). Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chemical Research in Toxicology, 10, 386–392.

    Article  CAS  PubMed  Google Scholar 

  11. Radi, R. (2004). NO, oxidants, and protein tyrosine nitration. Proceedings of the National Academy of Sciences of the United States of America, 101, 4003–4008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Villa, L. M., Salas, E., Darley-Usmar, V. M., Radomski, M. W., & Moncada, S. (1994). Peroxynitrite induces both vasodilatation and impaired vascular relaxation in the isolated perfused rat heart. Proceedings of the National Academy of Sciences of the United States of America, 91, 12383–12387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rubbo, H., Radi, R., Trujillo, M., Telleri, R., Kalyanaraman, B., Barnes, S., et al. (1994). Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. Journal of Biological Chemistry, 269, 26066–26075.

    CAS  PubMed  Google Scholar 

  14. Violi, F., Marino, R., Milite, M. T., & Loffredo, L. (1999). NO and its role in lipid peroxidation. Diabetes Metabolism Research and Reviews, 15, 283–288.

    Article  CAS  PubMed  Google Scholar 

  15. Wright, M. M., Schopfer, F. J., Baker, P. R., Vidyasagar, V., Powell, P., Chumley, P., et al. (2006). Fatty acid transduction of nitric oxide signaling: Nitrolinoleic acid potently activates endothelial heme oxygenase 1 expression. Proceedings of the National Academy of Sciences of the United States of America, 103, 4299–4304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Milstien, S., & Katusic, Z. (1999). Oxidation of tetrahydrobiopterin by peroxynitrite: Implications for vascular endothelial function. Biochemical and Biophysical Research Communications, 263, 681–684.

    Article  CAS  PubMed  Google Scholar 

  17. Ischiropoulos, H., Zhu, L., & Beckman, J. S. (1992). Peroxynitrite formation from macrophage-derived nitric oxide. Archives of Biochemistry and Biophysics, 298, 446–451.

    Article  CAS  PubMed  Google Scholar 

  18. Lewis, R. S., Tamir, S., Tannenbaum, S. R., & Deen, W. M. (1995). Kinetic analysis of the fate of nitric oxide synthesized by macrophages in vitro. Journal of Biological Chemistry, 270, 29350–29355.

    Article  CAS  PubMed  Google Scholar 

  19. Faulkner, K. M., Liochev, S. I., & Fridowich, I. (1994). Stable Mn(III) prophyrins mimic cuperoxide dismutase in vitro and substitute for it in vivo. Journal of Biological Chemistry, 269, 23471–23476.

    CAS  PubMed  Google Scholar 

  20. Yermilov, V., Rubio, J., Becchi, M., Friesen, M. D., Pignatelli, B., & Ohshima, H. (1995). Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. Carcinogenesis, 16, 2045–2050.

    Article  CAS  PubMed  Google Scholar 

  21. Koppenol, W. H., Moreno, J. J., Pryor, W. A., Ischiropoulos, H., & Beckman, J. S. (1992). Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chemical Research in Toxicology, 5, 834–842.

    Article  CAS  PubMed  Google Scholar 

  22. Rubio, J., Yermilov, V., & Ohshima, H. (1996). DNA damage induced by peroxynitrite: Formation of 8-nitroguanine and base propenals. In Moncada, S., Stamler, J., Gross, S., & Higgs, E. A. (Eds.), The biology of nitric oxide (p. 34). London: Portland Press Proceedings, part 5.

  23. Yermilov, V., Yoshie, Y., Rubio, J., & Ohshima, H. (1996). Effects of carbon dioxide/bicarbonate on induction of DNA single-strand breaks and formation of 8-nitroguanine, 8-oxo-guanine and base-propenal mediated by peroxynitrite. FEBS Letters, 399, 67–70.

    Article  CAS  PubMed  Google Scholar 

  24. Yermilov, V., Rubio, J., & Ohshima, H. (1995). Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination. FEBS Letters, 376, 207–210.

    Article  CAS  PubMed  Google Scholar 

  25. Spencer, J. P., Wong, J., Jenner, A., Aruoma, O. I., Cross, C. E., & Halliwell, B. (1996). Base modification and strand breakage in isolated calf thymus DNA and in DNA from human skin epidermal keratinocytes exposed to peroxynitrite or 3-morpholinosydnonimine. Chemical Research in Toxicology, 9, 1152–1158.

    Article  CAS  PubMed  Google Scholar 

  26. Epe, B., Ballmaier, D., Roussyn, I., Briviba, K., & Sies, H. (1996). DNA damage by peroxynitrite characterized with DNA repair enzymes. Nucleic Acids Research, 24, 4105–4110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., & Freeman, B. A. (1990). Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proceedings of the National Academy of Sciences of the United States of America, 87, 1620–1624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Beckman, J. S., Estevez, A. G., Crow, J. P., & Barbeito, L. (2001). Superoxide dismutase and the death of motoneurons in ALS. Trends in Neurosciences, 24, S15–S20.

    Article  CAS  PubMed  Google Scholar 

  29. Beckman, J. S., Carson, M., Smith, C. D., & Koppenol, W. H. (1993). ALS, SOD and peroxynitrite. Nature, 364, 584.

    Article  CAS  PubMed  Google Scholar 

  30. Beckman, J. S., & Koppenol, W. H. (1996). Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. American Journal of Physiology Cell Physiology, 271, C1424–C1437.

    CAS  Google Scholar 

  31. Messmer, U. K., Reimer, D. M., Reed, J. C., & Brune, B. (1996). Nitric oxide induced poly(ADP-ribose) polymerase cleavage in RAS 264.7 macrophage apoptosis is blocked by Bcl-2. FEBS Letters, 384, 162–166.

    Article  CAS  PubMed  Google Scholar 

  32. Riquelme, P. T., Burzio, L. O., & Koide, S. S. (1979). ADP ribosylation of rat liver lysine-rich histone in vitro. Journal of Biological Chemistry, 254, 3018–3028.

    CAS  PubMed  Google Scholar 

  33. Suzuki, H., Quesada, P., Farina, B., & Leone, E. (1986). In vitro poly(ADP-ribosyl)ation of seminal ribonuclease. Journal of Biological Chemistry, 261, 6048–6055.

    CAS  PubMed  Google Scholar 

  34. Lautier, D., Lagueux, J., Thiboldeau, J., Menard, L., & Poirier, G. G. (1993). Molecular and biochemical features of poly(ADP-ribose)metabolism. Molecular and Cellular Biochemistry, 122, 171–193.

    Article  CAS  PubMed  Google Scholar 

  35. Min, W., & Wang, Z. Q. (2009). Poly(ADP-ribose) glycohydrolase (PARG) and its therapeutic potential. Frontiers in Bioscience (Landmark Edition), 14, 1619–1626.

    Article  CAS  Google Scholar 

  36. Otto, H., Reche, P. A., Bazan, F., Dittmar, K., Haag, F., & Koch-Nolte, F. (2005). In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics, 6, 139.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Hottiger, M. O., Hassa, P. O., Lüscher, B., Schüler, H., & Koch-Nolte, F. (2010). Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends in Biochemical Sciences, 35, 208–219.

    Article  CAS  PubMed  Google Scholar 

  38. Dantzer, F., Amé, J. C., Schreiber, V., Nakamura, J., Ménissier-de Murcia, J., & de Murcia, G. (2006). Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. Methods in Enzymology, 409, 493–510.

    Article  CAS  PubMed  Google Scholar 

  39. Hassa, P. O., & Hottiger, M. O. (2008). The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Frontiers Biosciences, 13, 3046–3082.

    Article  CAS  Google Scholar 

  40. Jagtap, P., & Szabó, C. (2005). Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nature Reviews Drug Discovery, 4, 421–440.

    Article  CAS  PubMed  Google Scholar 

  41. Beneke, S. (2008). Poly(ADP-ribose) polymerase activity in different pathologies—The link to inflammation and infarction. Experimental Gerontology, 43, 605–614.

    Article  CAS  PubMed  Google Scholar 

  42. Virág, L., & Szabó, C. (2002). The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacological Reviews, 54, 375–429.

    Article  PubMed  Google Scholar 

  43. Szabó, C., Ischiropoulos, H., & Radi, R. (2007). Peroxynitrite: Biochemistry, pathophysiology and development of therapeutics. Nature Reviews Drug Discovery, 6, 662–680.

    Article  PubMed  CAS  Google Scholar 

  44. Pacher, P., Beckman, J. S., & Liaudet, L. (2007). Nitric oxide and peroxynitrite in health and disease. Physiological Reviews, 87, 315–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Aguilar-Quesada, R., Muñoz-Gámez, J. A., Martín-Oliva, D., Peralta-Leal, A., Quiles-Pérez, R., Rodríguez-Vargas, J. M., et al. (2007). Modulation of transcription by PARP-1: Consequences in carcinogenesis and inflammation. Current Medicinal Chemistry, 14, 1179–1187.

    Article  CAS  PubMed  Google Scholar 

  46. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., et al. (1999). Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 397, 441–446.

    Article  CAS  PubMed  Google Scholar 

  47. MacMillan-Crow, L. A., & Thompson, J. A. (1999). Tyrosine modifications and inactivation of active site manganese superoxide dismutase mutant (Y34F) by peroxynitrite. Archives of Biochemistry and Biophysics, 366, 82–88.

    Article  CAS  PubMed  Google Scholar 

  48. Radi, R., Cassina, A., & Hodara, R. (2002). Nitric oxide and peroxynitrite interactions with mitochondria. Biological Chemistry, 383, 401–409.

    Article  CAS  PubMed  Google Scholar 

  49. Radi, R., Cassina, A., Hodara, R., Quijano, C., & Castro, L. (2002). Peroxynitrite reactions and formation in mitochondria. Free Radical Biology and Medicine, 33, 1451–1464.

    Article  CAS  PubMed  Google Scholar 

  50. Castro, L., Rodriguez, M., & Radi, R. (1994). Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. Journal of Biological Chemistry, 269, 29409–29415.

    CAS  PubMed  Google Scholar 

  51. Han, D., Canali, R., Garcia, J., Aguilera, R., Gallaher, T. K., & Cadenas, E. (2005). Sites and mechanisms of aconitase inactivation by peroxynitrite: Modulation by citrate and glutathione. Biochemistry, 44, 11986–11996.

    Article  CAS  PubMed  Google Scholar 

  52. Stachowiak, O., Dolder, M., Wallimann, T., & Richter, C. (1998). Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. Journal of Biological Chemistry, 273, 16694–16699.

    Article  CAS  PubMed  Google Scholar 

  53. Kumar, A., & Parrillo, J. E. (2001). Shock: Classification, pathophysiology, and approach to management. In J. D. Parillo & R. Dellinger (Eds.), Critical care medicine: Principles of diagnosis and management in the adult (2nd ed., pp. 371–420). St. Louis: Mosby.

    Google Scholar 

  54. Weil, M. H., & Shubin, H. (1971). Proposed reclassification of shock states with special reference to distributive defects. Advances in Experimental Medicine and Biology, 23, 13–23.

    Article  CAS  PubMed  Google Scholar 

  55. Levy, B., Collin, S., Sennoun, N., Ducrocq, N., Kimmoun, A., Asfar, P., et al. (2010). Vascular hyporesponsiveness to vasopressors in septic shock: From bench to bedside. Intensive Care Medicine, 36, 2019–2029.

    Article  CAS  PubMed  Google Scholar 

  56. Hollenberg, S. M. (2009). Inotrope and vasopressor therapy of septic shock. Critical Care Clinics, 25, 781–802.

    Article  CAS  PubMed  Google Scholar 

  57. Szabó, C., & Modis, K. (2010). Pathophysiological roles of peroxynitrite in circulatory shock. Shock, 34(Suppl 1), 4–14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Pacher, P., & Szabó, C. (2008). Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. American Journal of Pathology, 173, 2–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Esposito, E., & Cuzzocrea, S. (2009). Role of nitroso radicals as drug targets in circulatory shock. British Journal of Pharmacology, 157, 494–508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Jagtap, P., Soriano, F. G., Virág, L., Liaudet, L., Mabley, J., Szabó, E., et al. (2002). Novel phenanthridinone inhibitors of poly (adenosine 5′-diphosphate-ribose) synthetase: Potent cytoprotective and antishock agents. Critical Care Medicine, 30, 1071–1082.

    Article  CAS  PubMed  Google Scholar 

  61. Goldfarb, R. D., Marton, A., Szabó, E., Virág, L., Salzman, A. L., Glock, D., et al. (2002). Protective effect of a novel, potent inhibitor of poly(adenosine 5′-diphosphate-ribose) synthetase in a porcine model of severe bacterial sepsis. Critical Care Medicine, 30, 974–980.

    Article  CAS  PubMed  Google Scholar 

  62. Soriano, F. G., Liaudet, L., Szabó, E., Virág, L., Mabley, J. G., Pacher, P., et al. (2002). Resistance to acute septic peritonitis in poly(ADP-ribose) polymerase-1-deficient mice. Shock, 17, 286–292.

    Article  PubMed  Google Scholar 

  63. Liaudet, L., Soriano, F. G., Szabó, E., Virág, L., Mabley, J. G., Salzman, A. L., et al. (2000). Protection against hemorrhagic shock in mice genetically deficient in poly(ADP-ribose)polymerase. Proceedings of the National Academy of Sciences of the United States of America, 97, 10203–10208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Li, J., Li, W., Altura, B. T., & Altura, B. M. (2004). Peroxynitrite-induced relaxation in isolated canine cerebral arteries and mechanisms of action. Toxicology and Applied Pharmacology, 196, 176–182.

    Article  CAS  PubMed  Google Scholar 

  65. Ohashi, M., Faraci, F., & Heistad, D. (2005). Peroxynitrite hyperpolarizes smooth muscle and relaxes internal carotid artery in rabbit via ATP-sensitive K+ channels. American Journal of Physiology Heart and Circulatory Physiology, 289, H2244–H2250.

    Article  CAS  PubMed  Google Scholar 

  66. Cena, J. J., Lalu, M. M., Cho, W. J., Chow, A. K., Bagdan, M. L., Daniel, E. E., et al. (2010). Inhibition of matrix metalloproteinase activity in vivo protects against vascular hyporeactivity in endotoxemia. American Journal of Physiology Heart and Circulatory Physiology, 298, H45–H51.

    Article  CAS  PubMed  Google Scholar 

  67. Grover, A. K., Samson, S. E., Robinson, S., & Kwan, C. Y. (2003). Effects of peroxynitrite on sarcoplasmic reticulum Ca2+ pump in pig coronary artery smooth muscle. American Journal of Physiology. Cell Physiology, 284, C294–C301.

    Article  CAS  PubMed  Google Scholar 

  68. Martínez-Caro, L., Nin, N., Sánchez-Rodríguez, C., Ferruelo, A., El Assar, M., de Paula, M., et al. (2015). Inhibition of nitro-oxidative stress attenuates pulmonary and systemic injury induced by high-tidal volume mechanical ventilation. Shock, 44, 36–43.

    Article  PubMed  CAS  Google Scholar 

  69. Szabó, C., Cuzzocrea, S., Zingarelli, B., O’Connor, M., & Salzman, A. L. (1997). Endothelial dysfunction in a rat model of endotoxic shock. Importance of the activation of poly(ADP-ribose) synthetase by peroxynitrite. Journal of Clinical Investigation, 100, 723–735.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Merx, M. W., & Weber, C. (2007). Sepsis and the heart. Circulation, 116, 793–802.

    Article  CAS  PubMed  Google Scholar 

  71. Rudiger, A., & Singer, M. (2007). Mechanisms of sepsis-induced cardiac dysfunction. Critical Care Medicine, 35, 1599–1608.

    Article  PubMed  Google Scholar 

  72. Hunter, J. D., & Doddi, M. (2010). Sepsis and the heart. British Journal of Anaesthesia, 104, 3–11.

    Article  CAS  PubMed  Google Scholar 

  73. Levrand, S., Vannay-Bouchiche, C., Pesse, B., Pacher, P., Feihl, F., Waeber, B., et al. (2006). Peroxynitrite is a major trigger of cardiomyocyte apoptosis in vitro and in vivo. Free Radical Biology and Medicine, 41, 886–895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Pacher, P., Liaudet, L., Mabley, J. G., Cziráki, A., Haskó, G., & Szabó, C. (2006). Beneficial effects of a novel ultrapotent poly(ADP-ribose) polymerase inhibitor in murine models of heart failure. International Journal of Molecular Medicine, 17, 369–375.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Soriano, F. G., Nogueira, A. C., Caldini, E. G., Lins, M. H., Teixeira, A. C., Cappi, S. B., et al. (2006). Potential role of poly(adenosine 5′-diphosphate-ribose) polymerase activation in the pathogenesis of myocardial contractile dysfunction associated with human septic shock. Critical Care Medicine, 34, 1073–1079.

    Article  CAS  PubMed  Google Scholar 

  76. Lokuta, A. J., Maertz, N. A., Meethal, S. V., Potter, K. T., Kamp, T. J., Valdivia, H. H., et al. (2005). Increased nitration of sarcoplasmic reticulum Ca2+-ATPase in human heart failure. Circulation, 111, 988–995.

    Article  CAS  PubMed  Google Scholar 

  77. Snook, J. H., Li, J., Helmke, B. P., & Guilford, W. H. (2008). Peroxynitrite inhibits myofibrillar protein function in an in vitro assay of motility. Free Radical Biology and Medicine, 44, 14–23.

    Article  CAS  PubMed  Google Scholar 

  78. Borbély, A., Tóth, A., Edes, I., Virág, L., Papp, J. G., Varró, A., et al. (2005). Peroxynitrite-induced alpha-actinin nitration and contractile alterations in isolated human myocardial cells. Cardiovascular Research, 67, 225–233.

    Article  PubMed  CAS  Google Scholar 

  79. Mihm, M. J., Coyle, C. M., Schanbacher, B. L., Weinstein, D. M., & Bauer, J. A. (2001). Peroxynitrite induced nitration and inactivation of myofibrillar creatine kinase in experimental heart failure. Cardiovascular Research, 49, 798–807.

    Article  CAS  PubMed  Google Scholar 

  80. León, H., Baczkó, I., Sawicki, G., Light, P. E., & Schulz, R. (2008). Inhibition of matrix metalloproteinases prevents peroxynitrite-induced contractile dysfunction in the isolated cardiac myocyte. British Journal of Pharmacology, 153, 676–683.

    Article  PubMed  CAS  Google Scholar 

  81. Polewicz, D., Cadete, V. J., Doroszko, A., Hunter, B. E., Sawicka, J., Szczesna-Cordary, D., et al. (2011). Ischemia induced peroxynitrite dependent modifications of cardiomyocyte MLC1 increases its degradation by MMP-2 leading to contractile dysfunction. Journal of Cellular and Molecular Medicine, 15, 1136–1147.

    Article  CAS  PubMed  Google Scholar 

  82. Loukili, N., Rosenblatt-Velin, N., Rolli, J., Levrand, S., Feihl, F., Waeber, B., et al. (2010). Oxidants positively or negatively regulate nuclear factor kappaB in a context-dependent manner. Journal of Biological Chemistry, 285, 15746–15752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Pesse, B., Levrand, S., Feihl, F., Waeber, B., Gavillet, B., Pacher, P., et al. (2005). Peroxynitrite activates ERK via Raf-1 and MEK, independently from EGF receptor and p21Ras in H9C2 cardiomyocytes. Journal of Molecular and Cellular Cardiology, 38, 765–775.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Loukili, N., Rosenblatt-Velin, N., Li, J., Clerc, S., Pacher, P., Feihl, F., et al. (2011). Peroxynitrite induces HMGB1 release by cardiac cells in vitro and HMGB1 upregulation in the infarcted myocardium in vivo. Cardiovascular Research, 89, 586–594.

    Article  CAS  PubMed  Google Scholar 

  85. Gerö, D., & Szabó, C. (2008). Poly(ADP-ribose) polymerase: A new therapeutic target? Current Opinion in Anesthesiology, 21, 111–121.

    Article  PubMed  Google Scholar 

  86. Salvemini, D., Riley, D. P., Lennon, P. J., Wang, Z. Q., Currie, M. G., Macarthur, H., et al. (1999). Protective effects of a superoxide dismutase mimetic and peroxynitrite decomposition catalysts in endotoxin-induced intestinal damage. British Journal of Pharmacology, 127, 685–692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Vaschetto, R., Kuiper, J. W., Musters, R. J., Eringa, E. C., Della Corte, F., Murthy, K., et al. (2010). Renal hypoperfusion and impaired endothelium-dependent vasodilation in an animal model of VILI: The role of the peroxynitrite-PARP pathway. Critical Care, 14, R45.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Maybauer, D. M., Maybauer, M. O., Szabó, C., Cox, R. A., Westphal, M., Kiss, L., et al. (2011). The peroxynitrite catalyst WW-85 improves pulmonary function in ovine septic shock. Shock, 35, 148–155.

    Article  CAS  PubMed  Google Scholar 

  89. Hauschildt, S., Scheipers, P., Bessler, W., Schwarz, K., Ullmer, A., Flad, H. D., et al. (1997). Role of ADP-ribosylation in activated monocytes/macrophages. Advances in Experimental Medicine and Biology, 419, 249–252.

    Article  CAS  PubMed  Google Scholar 

  90. Szabó, C., Lim, L. H., Cuzzocrea, S., Getting, S. J., Zingarelli, B., Flower, R. J., et al. (1997). Inhibition of poly(ADP-ribose) synthetase attenuates neutrophil recruitment and exerts anti-inflammatory effects. Journal of Experimental Medicine, 186, 1041–1049.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Szabó, C., Zingarelli, B., & Salzman, A. L. (1996). Role of poly-ADP ribosyltransferase activation in the vascular contractile and energetic failure elicited by exogenous and endogenous nitric oxide and peroxynitrite. Circulation Research, 78, 1051–1063.

    Article  PubMed  Google Scholar 

  92. Iványi, Z., Hauser, B., Pittner, A., Asfar, P., Vassilev, D., Nalos, M., et al. (2003). Systemic and hepatosplanchnic hemodynamic and metabolic effects of the PARP inhibitor PJ34 during hyperdynamic porcine endotoxemia. Shock, 19, 415–421.

    Article  PubMed  CAS  Google Scholar 

  93. Stehr, A., Ploner, F., Tugtekin, I., Matejovic, M., Theisen, M., Zülke, C., et al. (2003). Effect of combining nicotinamide as a PARS-inhibitor with selective iNOS blockade during porcine endotoxemia. Intensive Care Medicine, 29, 995–1002.

    Article  CAS  PubMed  Google Scholar 

  94. Boulos, M., Astiz, M. E., Barua, R. S., & Osman, M. (2003). Impaired mitochondrial function induced by serum from septic shock patients is attenuated by inhibition of nitric oxide synthase and poly(ADP-ribose) synthase. Critical Care Medicine, 31, 353–358.

    Article  CAS  PubMed  Google Scholar 

  95. Szabó, C. (2007). Poly(ADP-ribose) polymerase activation and circulatory shock. In Novartis Foundation symposium (Vol. 280, pp. 92–103) (discussion 103–107, 160–164).

  96. Hauschildt, S., Scheipers, P., Bessler, W. G., & Mülsch, A. (1992). Induction of nitric oxide synthase in L929 cells by tumour-necrosis factor alpha is prevented by inhibitors of poly(ADP-ribose) polymerase. Biochemical Journal, 288, 255–260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Haddad, M., Rhinn, H., Bloquel, C., Coqueran, B., Szabó, C., Plotkine, M., et al. (2006). Anti-inflammatory effects of PJ34, a poly(ADP-ribose) polymerase inhibitor, in transient focal cerebral ischemia in mice. British Journal of Pharmacology, 149, 23–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Jijon, H. B., Churchill, T., Malfair, D., Wessler, A., Jewell, L. D., Parsons, H. G., et al. (2000). Inhibition of poly(ADP-ribose) polymerase attenuates inflammation in a model of chronic colitis. American Journal of Physiology Gastrointestinal and Liver Physiology, 279, G641–G651.

    CAS  PubMed  Google Scholar 

  99. Mazzon, E., Dugo, L., Li, J. H., Di Paola, R., Genovese, T., Caputi, A. P., et al. (2002). GPI 6150, a PARP inhibitor, reduces the colon injury caused by dinitrobenzene sulfonic acid in the rat. Biochemical Pharmacology, 64, 327–337.

    Article  CAS  PubMed  Google Scholar 

  100. Su, C. F., Liu, D. D., Kao, S. J., & Chen, H. I. (2007). Nicotinamide abrogates acute lung injury caused by ischaemia/reperfusion. European Respiratory Journal, 30, 199–204.

    Article  CAS  PubMed  Google Scholar 

  101. Zingarelli, B., Salzman, A. L., & 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. Circulation Research, 83, 85–94.

    Article  CAS  PubMed  Google Scholar 

  102. Szabó, C. (2006). Poly(ADP-ribose) polymerase activation by reactive nitrogen species—relevance for the pathogenesis of inflammation. Nitric Oxide, 14, 169–179.

    Article  PubMed  CAS  Google Scholar 

  103. Zingarelli, B., O’Connor, M., & Hake, P. W. (2003). Inhibitors of poly(ADP-ribose) polymerase modulate signal transduction pathways in colitis. European Journal of Pharmacology, 469, 183–194.

    Article  CAS  PubMed  Google Scholar 

  104. Di Paola, R., Mazzon, E., Xu, W., Genovese, T., Ferrraris, D., Muià, C., et al. (2005). Treatment with PARP-1 inhibitors, GPI 15427 or GPI 16539, ameliorates intestinal damage in rat models of colitis and shock. European Journal of Pharmacology, 527(1–3), 163–171.

    Article  PubMed  CAS  Google Scholar 

  105. Cuzzocrea, S., Zingarelli, B., Costantino, G., Szabó, A., Salzman, A. L., Caputi, A. P., et al. (1997). Beneficial effects of 3-aminobenzamide, an inhibitor of poly(ADP-ribose) synthetase in a rat model of splanchnic artery occlusion and reperfusion. British Journal of Pharmacology, 121, 1065–1074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Chen, C. F., Wang, D., Lin, H. I., Leu, F. J., Shen, C. Y., & Chou, C. C. (2007). Ischemia/reperfusion of the liver induces heart injury in rats. Transplantation Proceedings, 39, 855–857.

    Article  CAS  PubMed  Google Scholar 

  107. Szijártó, A., Batmunkh, E., Hahn, O., Mihály, Z., Kreiss, A., Kiss, A., et al. (2007). Effect of PJ-34 PARP-inhibitor on rat liver microcirculation and antioxidant status. Journal of Surgical Research, 142, 72–80.

    Article  PubMed  CAS  Google Scholar 

  108. Khandoga, A., Biberthaler, P., Enders, G., & Krombach, F. (2004). 5-Aminoisoquinolinone, a novel inhibitor of poly(adenosine disphosphate-ribose) polymerase, reduces microvascular liver injury but not mortality rate after hepatic ischemia-reperfusion. Critical Care Medicine, 32, 472–477.

    Article  CAS  PubMed  Google Scholar 

  109. Cover, C., Fickert, P., Knight, T. R., Fuchsbichler, A., Farhood, A., Trauner, M., et al. (2005). Pathophysiological role of poly(ADP-ribose) polymerase (PARP) activation during acetaminophen-induced liver cell necrosis in mice. Toxicological Sciences, 84, 201–208.

    Article  CAS  PubMed  Google Scholar 

  110. Yamamoto, K., Tsukidate, K., & Farber, J. L. (1993). Differing effects of the inhibition of poly(ADP-ribose) polymerase on the course of oxidative cell injury in hepatocytes and fibroblasts. Biochemical Pharmacology, 46, 483–491.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

One of the authors B. U. I. is thankful to UGC-MANF for financial support as Senior Research Fellow. Assistance from the Institution (AMU) as well as infrastructural support from DST-FIST to the department is also duly acknowledged.

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Islam, B.U., Habib, S., Ali, S.A. et al. Role of Peroxynitrite-Induced Activation of Poly(ADP-Ribose) Polymerase (PARP) in Circulatory Shock and Related Pathological Conditions. Cardiovasc Toxicol 17, 373–383 (2017). https://doi.org/10.1007/s12012-016-9394-7

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