Effect of nitric oxide on naphthoquinone toxicity in endothelial cells: Role of bioenergetic dysfunction and poly(ADP-ribose) polymerase activation

Biochemistry

Volumn 52, Issue 25, 2013, Pages 4364-4372

  Broniowska, Katarzyna A ^a   Diers, Anne R ^a   Corbett, John A ^b   Hogg, Neil ^a  

^a Redox Biology Program   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ,4-NAPHTHOQUINONES; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL FUNCTION; PATHOLOGICAL CONDITIONS; PHYSIOLOGICAL LEVELS; POLY(ADP-RIBOSE) POLYMERASE; PYRIDINE NUCLEOTIDES; REACTIVE OXYGEN SPECIES;

BIOCHEMISTRY; CELL DEATH; KETONES; MITOCHONDRIA; NITRIC OXIDE; OXIDANTS; OXYGEN;

ENDOTHELIAL CELLS;

1,4 NAPHTHOQUINONE; ADENINE NUCLEOTIDE; ADENOSINE TRIPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRIC OXIDE; OXIDIZING AGENT; PYRIDINE NUCLEOTIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ANIMAL CELL; ARTICLE; BIOENERGY; CELL ENERGY; CELL METABOLISM; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYME INHIBITION; EXPOSURE; INTRACELLULAR SIGNALING; MITOCHONDRIAL TOXICITY; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

ANIMALS; AORTA; CATTLE; CELL DEATH; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENERGY METABOLISM; MITOCHONDRIA; NAPHTHOQUINONES; NITRIC OXIDE; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES;

EID: 84879545058     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400342t     Document Type: Article

References (61)

1. Li, J. M. and Shah, A. M. (2004) Endothelial cell superoxide generation: Regulation and relevance for cardiovascular pathophysiology Am. J. Physiol. 287, R1014-R1030
2. Waldman, S. A. and Murad, F. (1988) Biochemical mechanisms underlying vascular smooth muscle relaxation: The guanylate cyclase-cyclic GMP system J. Cardiovasc. Pharmacol. 12 (Suppl. 5) S115-S118
3. Paravicini, T. M. and Touyz, R. M. (2008) NADPH oxidases, reactive oxygen species, and hypertension: Clinical implications and therapeutic possibilities Diabetes Care 31 (Suppl. 2) S170-S180
4. Vasquez-Vivar, J., Kalyanaraman, B., Martasek, P., Hogg, N., Masters, B. S., Karoui, H., Tordo, P., and Pritchard, K. A., Jr. (1998) Superoxide generation by endothelial nitric oxide synthase: The influence of cofactors Proc. Natl. Acad. Sci. U.S.A. 95, 9220-9225
5. Cadenas, E. (1995) Antioxidant and prooxidant functions of DT-diaphorase in quinone metabolism Biochem. Pharmacol. 49, 127-140
6. Watanabe, N. and Forman, H. J. (2003) Autoxidation of extracellular hydroquinones is a causative event for the cytotoxicity of menadione and DMNQ in A549-S cells Arch. Biochem. Biophys. 411, 145-157
7. Brunmark, A. and Cadenas, E. (1989) Redox and addition chemistry of quinoid compounds and its biological implications Free Radical Biol. Med. 7, 435-477
8. Chuang, Y. Y., Chen, Y., Gadisetti, Chandramouli, V. R., Cook, J. A., Coffin, D., Tsai, M. H., DeGraff, W., Yan, H., Zhao, S., Russo, A., Liu, E. T., and Mitchell, J. B. (2002) Gene expression after treatment with hydrogen peroxide, menadione, or t-butyl hydroperoxide in breast cancer cells Cancer Res. 62, 6246-6254
9. 2+ elevations and the mitochondrial permeability transition pore J. Cell Sci. 115, 485-497
10. Kim, K. A., Lee, J. Y., Park, K. S., Kim, M. J., and Chung, J. H. (1996) Mechanism of menadione-induced cytotoxicity in rat platelets Toxicol. Appl. Pharmacol. 138, 12-19
11. Loor, G., Kondapalli, J., Schriewer, J. M., Chandel, N. S., Vanden Hoek, T. L., and Schumacker, P. T. (2010) Menadione triggers cell death through ROS-dependent mechanisms involving PARP activation without requiring apoptosis Free Radical Biol. Med. 49, 1925-1936
12. Grishko, V., Solomon, M., Wilson, G. L., LeDoux, S. P., and Gillespie, M. N. (2001) Oxygen radical-induced mitochondrial DNA damage and repair in pulmonary vascular endothelial cell phenotypes Am. J. Physiol. 280, L1300-L1308
13. Luo, X., Pitkanen, S., Kassovska-Bratinova, S., Robinson, B. H., and Lehotay, D. C. (1997) Excessive formation of hydroxyl radicals and aldehydic lipid peroxidation products in cultured skin fibroblasts from patients with complex I deficiency J. Clin. Invest. 99, 2877-2882
14. Gant, T. W., Rao, D. N., Mason, R. P., and Cohen, G. M. (1988) Redox cycling and sulphydryl arylation; their relative importance in the mechanism of quinone cytotoxicity to isolated hepatocytes Chem.-Biol. Interact. 65, 157-173
15. Lee, M. Y. and Griendling, K. K. (2008) Redox signaling, vascular function, and hypertension Antioxid. Redox Signaling 10, 1045-1059
16. Szabo, C., Ischiropoulos, H., and Radi, R. (2007) Peroxynitrite: Biochemistry, pathophysiology and development of therapeutics Nat. Rev. Drug Discovery 6, 662-680
17. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624
18. 2-induced transferrin receptor-dependent apoptosis in endothelial cells: Role of ubiquitin-proteasome pathway Proc. Natl. Acad. Sci. U.S.A. 100, 10653-10658
19. Thomas, D. D., Ridnour, L. A., Espey, M. G., Donzelli, S., Ambs, S., Hussain, S. P., Harris, C. C., DeGraff, W., Roberts, D. D., Mitchell, J. B., and Wink, D. A. (2006) Superoxide fluxes limit nitric oxide-induced signaling J. Biol. Chem. 281, 25984-25993
20. Morgan, W. A. (1995) DNA single-strand breakage in mammalian cells induced by redox cycling quinones in the absence of oxidative stress J. Biochem. Toxicol. 10, 227-232
21. Hassa, P. O., Haenni, S. S., Elser, M., and Hottiger, M. O. (2006) Nuclear ADP-ribosylation reactions in mammalian cells: Where are we today and where are we going? Microbiol. Mol. Biol. Rev. 70, 789-829
22. Schreiber, V., Dantzer, F., Ame, J. C., and de Murcia, G. (2006) Poly(ADP-ribose): Novel functions for an old molecule Nat. Rev. Mol. Cell Biol. 7, 517-528
23. David, K. K., Andrabi, S. A., Dawson, T. M., and Dawson, V. L. (2009) Parthanatos, a messenger of death Front. Biosci. 14, 1116-1128
24. Zong, W. X., Ditsworth, D., Bauer, D. E., Wang, Z. Q., and Thompson, C. B. (2004) Alkylating DNA damage stimulates a regulated form of necrotic cell death Genes Dev. 18, 1272-1282
25. Garcia Soriano, F., Virag, L., Jagtap, P., Szabo, E., Mabley, J. G., Liaudet, L., Marton, A., Hoyt, D. G., Murthy, K. G., Salzman, A. L., Southan, G. J., and Szabo, C. (2001) Diabetic endothelial dysfunction: The role of poly(ADP-ribose) polymerase activation Nat. Med. 7, 108-113
26. Liaudet, L., Soriano, F. G., Szabo, E., Virag, L., Mabley, J. G., Salzman, A. L., and Szabo, C. (2000) Protection against hemorrhagic shock in mice genetically deficient in poly(ADP-ribose)polymerase Proc. Natl. Acad. Sci. U.S.A. 97, 10203-10208
27. Endres, M., Scott, G., Namura, S., Salzman, A. L., Huang, P. L., Moskowitz, M. A., and Szabo, C. (1998) Role of peroxynitrite and neuronal nitric oxide synthase in the activation of poly(ADP-ribose) synthetase in a murine model of cerebral ischemia-reperfusion Neurosci. Lett. 248, 41-44
28. Faro, R., Toyoda, Y., McCully, J. D., Jagtap, P., Szabo, E., Virag, L., Bianchi, C., Levitsky, S., Szabo, C., and Sellke, F. W. (2002) Myocardial protection by PJ34, a novel potent poly (ADP-ribose) synthetase inhibitor Annals of Thoracic Surgery 73, 575-581
29. Schriewer, J. M., Peek, C. B., Bass, J., and Schumacker, P. T. (2013) ROS-Mediated PARP Activity Undermines Mitochondrial Function After Permeability Transition Pore Opening During Myocardial Ischemia-Reperfusion J. Am. Heart Assoc. 2, e000159
30. Eliasson, M. J., Sampei, K., Mandir, A. S., Hurn, P. D., Traystman, R. J., Bao, J., Pieper, A., Wang, Z. Q., Dawson, T. M., Snyder, S. H., and Dawson, V. L. (1997) Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia Nat. Med. 3, 1089-1095
31. Broniowska, K. A. and Hogg, N. (2010) Differential mechanisms of inhibition of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosothiols and NO in cellular and cell-free conditions Am. J. Physiol. 299, H1212-H1219
32. Zielonka, J., Hardy, M., and Kalyanaraman, B. (2009) HPLC study of oxidation products of hydroethidine in chemical and biological systems: Ramifications in superoxide measurements Free Radical Biol. Med. 46, 329-338
33. Diers, A. R., Higdon, A. N., Ricart, K. C., Johnson, M. S., Agarwal, A., Kalyanaraman, B., Landar, A., and Darley-Usmar, V. M. (2010) Mitochondrial targeting of the electrophilic lipid 15-deoxy-Δ12,14-prostaglandin J2 increases apoptotic efficacy via redox cell signalling mechanisms Biochem. J. 426, 31-41
34. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays J. Immunol. Methods 65, 55-63
35. Ferrick, D. A., Neilson, A., and Beeson, C. (2008) Advances in measuring cellular bioenergetics using extracellular flux Drug Discovery Today 13, 268-274
36. Gerencser, A. A., Neilson, A., Choi, S. W., Edman, U., Yadava, N., Oh, R. J., Ferrick, D. A., Nicholls, D. G., and Brand, M. D. (2009) Quantitative microplate-based respirometry with correction for oxygen diffusion Anal. Chem. 81, 6868-6878
37. Nicholls, D. G., Darley-Usmar, V. M., Wu, M., Jensen, P. B., Rogers, G. W., and Ferrick, D. A. (2010) Bioenergetic profile experiment using C2C12 myoblast cells J. Visualized Exp. DOI:10.3791/2511
38. Dranka, B. P., Benavides, G. A., Diers, A. R., Giordano, S., Zelickson, B. R., Reily, C., Zou, L., Chatham, J. C., Hill, B. G., Zhang, J., Landar, A., and Darley-Usmar, V. M. (2011) Assessing bioenergetic function in response to oxidative stress by metabolic profiling Free Radical Biol. Med. 51, 1621-1635
39. Dranka, B. P., Hill, B. G., and Darley-Usmar, V. M. (2010) Mitochondrial reserve capacity in endothelial cells: The impact of nitric oxide and reactive oxygen species Free Radical Biol. Med. 48, 905-914
40. Merker, M. P., Bongard, R. D., Kettenhofen, N. J., Okamoto, Y., and Dawson, C. A. (2002) Intracellular redox status affects transplasma membrane electron transport in pulmonary arterial endothelial cells Am. J. Physiol. 282, L36-L43
41. Stocchi, V., Cucchiarini, L., Canestrari, F., Piacentini, M. P., and Fornaini, G. (1987) A very fast ion-pair reversed-phase HPLC method for the separation of the most significant nucleotides and their degradation products in human red blood cells Anal. Biochem. 167, 181-190
42. Perez, J., Hill, B. G., Benavides, G. A., Dranka, B. P., and Darley-Usmar, V. M. (2010) Role of cellular bioenergetics in smooth muscle cell proliferation induced by platelet-derived growth factor Biochem. J. 428, 255-267
43. Zielonka, J., Zielonka, M., Sikora, A., Adamus, J., Joseph, J., Hardy, M., Ouari, O., Dranka, B. P., and Kalyanaraman, B. (2012) Global profiling of reactive oxygen and nitrogen species in biological systems: High-throughput real-time analyses J. Biol. Chem. 287, 2984-2995
44. Keefer, L. K., Nims, R. W., Davies, K. M., and Wink, D. A. (1996) "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: Convenient nitric oxide dosage forms Methods Enzymol. 268, 281-293
45. Orsi, A., Beltran, B., Clementi, E., Hallen, K., Feelisch, M., and Moncada, S. (2000) Continuous exposure to high concentrations of nitric oxide leads to persistent inhibition of oxygen consumption by J774 cells as well as extraction of oxygen by the extracellular medium Biochem. J. 346 (Part 2) 407-412
46. Andreone, T., Meares, G. P., Hughes, K. J., Hansen, P. A., and Corbett, J. A. (2012) Cytokine-mediated β-cell damage in PARP-1-deficient islets Am. J. Physiol. 303, E172-E179
47. +: An old metabolite controlling new metabolic signaling pathways Endocr. Rev. 31, 194-223
48. Diers, A. R., Broniowska, K. A., Darley-Usmar, V. M., and Hogg, N. (2011) Differential regulation of metabolism by nitric oxide and S-nitrosothiols in endothelial cells Am. J. Physiol. 301, H803-H812
49. Mathews, M. T. and Berk, B. C. (2008) PARP-1 inhibition prevents oxidative and nitrosative stress-induced endothelial cell death via transactivation of the VEGF receptor 2 Arterioscler., Thromb., Vasc. Biol. 28, 711-717
50. Pryor, W. A. and Squadrito, G. L. (1995) The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide Am. J. Physiol. 268, L699-L722
51. Radi, R., Beckman, J. S., Bush, K. M., and Freeman, B. A. (1991) Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide J. Biol. Chem. 266, 4244-4250
52. Warren, M. C., Bump, E. A., Medeiros, D., and Braunhut, S. J. (2000) Oxidative stress-induced apoptosis of endothelial cells Free Radical Biol. Med. 29, 537-547
53. Gong, G., Liu, J., Liang, P., Guo, T., Hu, Q., Ochiai, K., Hou, M., Ye, Y., Wu, X., Mansoor, A., From, A. H., Ugurbil, K., Bache, R. J., and Zhang, J. (2003) Oxidative capacity in failing hearts Am. J. Physiol. 285, H541-H548
54. Hill, B. G., Dranka, B. P., Zou, L., Chatham, J. C., and Darley-Usmar, V. M. (2009) Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal Biochem. J. 424, 99-107
55. Diers, A., Broniowska, K., and Hogg, N. (2013) Nitrosative stress and redox-cycling agents synergize to cause mitochondrial dysfunction and cell death in endothelial cells Redox Biol. 1, 1-7
56. Watanabe, N., Dickinson, D. A., Liu, R. M., and Forman, H. J. (2004) Quinones and glutathione metabolism Methods Enzymol. 378, 319-340
57. Circu, M. L., Maloney, R. E., and Aw, T. Y. (2011) Disruption of pyridine nucleotide redox status during oxidative challenge at normal and low-glucose states: Implications for cellular adenosine triphosphate, mitochondrial respiratory activity, and reducing capacity in colon epithelial cells Antioxid. Redox Signaling 14, 2151-2162
58. Meares, G. P., Hughes, K. J., Naatz, A., Papa, F. R., Urano, F., Hansen, P. A., Benveniste, E. N., and Corbett, J. A. (2011) IRE1-dependent activation of AMPK in response to nitric oxide Mol. Cell. Biol. 31, 4286-4297
59. Zeng, J., Yang, G. Y., Ying, W., Kelly, M., Hirai, K., James, T. L., Swanson, R. A., and Litt, L. (2007) Pyruvate improves recovery after PARP-1-associated energy failure induced by oxidative stress in neonatal rat cerebrocortical slices J. Cereb. Blood Flow Metab. 27, 304-315
60. Mercer, J. R., Cheng, K. K., Figg, N., Gorenne, I., Mahmoudi, M., Griffin, J., Vidal-Puig, A., Logan, A., Murphy, M. P., and Bennett, M. (2010) DNA damage links mitochondrial dysfunction to atherosclerosis and the metabolic syndrome Circ. Res. 107, 1021-1031
61. +/NADPH in cellular functions and cell death: Regulation and biological consequences Antioxid. Redox Signaling 10, 179-206