Endogenous and exogenous nitric oxide enhance the DNA strand scission induced by tert-butylhydroperoxide in PC12 cells via peroxynitrite-dependent and independent mechanisms, respectively

European Journal of Neuroscience

Volumn 12, Issue 1, 2000, Pages 145-154

  Sestili, Piero ^c   Clementi, Emilio ^a,b   Guidarelli, Andrea ^c   Sciorati, Clara ^a   Cantoni, Orazio ^c  

^a CNR   (Italy)

^b UNIVERSITY OF CALABRIA   (Italy)

^c UNIVERSITY OF URBINO   (Italy)

Author keywords

Calcium ions; DNA damage; Mitochondria; Neuronal cells; Short chain hydroperoxides

Indexed keywords

BUTYL HYDROPEROXIDE; CALCIUM ION; DNA; IMIDAZOLINE DERIVATIVE; METHIONINE; MYXOTHIAZOL; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PEROXYNITRITE; ROTENONE; RUTHENIUM RED; SCAVENGER; TROLOX C;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSOL; DNA CLEAVAGE; DNA STRAND BREAKAGE; ELECTRON TRANSPORT; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0003179215     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2000.00891.x     Document Type: Article

References (37)

1. Alam, Z.L., Jenner, A., Daniel, S.E., Lees, A.J., Caims, N., Marsden, C.D., Jenner, P. & Halliwell, B. (1997) Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem., 139, 189-201.
2. Baker, M.A. & He, S. (1991) Elaboration of cellular DNA breaks by hydroperoxides. Free Rad. Biol. Med., 11, 563-572.
3. Beilharz, E.J., Williams, C.E., Dragunow, M., Sirimanne, E.S. & Gluckman, P.D. (1995) Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Mol. Brain Res., 29, 1-14.
4. Berridge, M.J. (1993) A tale of two messengers. Nature, 365, 388-389.
5. Budd, S.L. & Nicholls, D.G. (1996) A reevaluation of the role of mitochondria in neuronal calcium homeostasis. J. Neurochem., 66, 403-411,
6. Cadenas, E. & Boveris, A. (1980) Enhancement of hydrogen peroxide formation by protonophores and ionophores in antimycin-supplemented mitochondria. Biochem. J., 188, 31-37.
7. Cantoni, O., Murray, D. & Meyn, R.E. (1986) Effect of 3-aminobenzamide on DNA strand-break rejoining and cytotoxicity in CHO cells treated with hydrogen peroxide. Biochim. Biophys. Acta, 867, 135-143.
8. Carafoli, E. (1987) Intracellular calcium homeostasis. Annu. Rev. Biochem., 56, 395-433.
9. Clementi, E., Riccio, M., Sciorati, C., Nisticò, G. & Meldolesi, J. (1996) The type 2 ryanodine receptor of neurosecretory PC12 cells is activated by cyclic ADP ribose: role of the nitric oxide/cGMP pathway. J. Biol. Chem., 271, 17739-17745.
10. Clementi, E., Guidarelli, A. & Cantoni, O. (1998) The inositol 1,4,5-trisphosphate generating agonist ATP enhances DNA cleavage induced by tert-butylhydroperoxide. Exp. Cell Res., 239, 175-178.
11. Coleman, J.B., Gilfor, D. & Farber, J.L. (1989) Dissociation of the accumulation of single-strand breaks in DNA from killing of cultured hepatocytes by an oxidative stress. Mol. Pharmacol., 36, 193-200.
12. Didier, M., Bursztajn, S., Adamec, E., Passani, L., Nixon, R.A., Coyle, J.T., Wei, J.Y. & Berman, S.A. (1996) DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J. Neurosci., 16, 2238-2250.
13. Fiskum, G., Craig, S.W., Decker, G.L. & Lehninger, A.L. (1980) The cytoskeleton of digitonin-treated rat hepatocytes. Proc. Natl Acad. Sci. USA, 77, 3430-3434.
14. 2+ indicators with greatly improved fluorescent properties. J. Biol. Chem., 260, 3440-3450.
15. Guidarelli, A., Sestili, P., Cossarizza, A., Franceschi, C., Cattabeni, F. & Cantoni, O. (1995) Evidence for dissimilar mechanisms of enhancement of inorganic and organic hydroperoxide cytotoxicity by L-histidine. J. Pharmacol. Exp. Ther., 275, 1575-1582.
16. Guidarelli, A., Clementi, E., Sciorati, C., Cattabeni, F. & Cantoni, O. (1997a) Calcium-dependent mitochondrial formation of species mediating DNA single strand breakage in U937 cells exposed to sublethal concentrations of tert-butylhydroperoxide. J. Pharmacol. Exp. Ther., 283, 66-74.
17. Guidarelli, A., Brambilla, L., Clementi, E., Sciorati, C. & Cantoni, O. (1997b) Stimulation of oxygen consumption promotes mitochondrial calcium accumulation, a process associated with, and causally linked to, enhanced formation of tert-butylhydroperoxide-induced DNA single strand breaks. Exp. Cell Res., 237, 176-185.
18. Guidarelli, A., Clementi, E., Brambilla, L. & Cantoni, O. (1997c) Mechanism of the antimycin A-mediated enhancement of t-butylhydroperoxide-induced single-strand breakage in DNA. Biochem. J., 328, 801-806.
19. Guidarelli, A., Clementi, E., Sciorati, C. & Cantoni, O. (1998) The mechanism of the nitric oxide-mediated enhancement of tert-butylhydroperoxide-induced DNA single strand breakage. Br. J. Pharmacol., 125, 1074-1080.
20. Heneka, M.T., Loschmann, P.A., Gleichmann, M., Weller, M., Schulz, J.B., Wullner, U. & Klockgether, T. (1998) Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-α/lipopolysaccharide. J. Neurochem., 71, 88-94.
21. King, J.K., Egner, P.A. & Kensler, T.W. (1996) Generation of DNA base modification following treatment of cultured murine keratinocytes with benzoyl-peroxide. Carcinogenesis, 17, 317-320.
22. Knowles, R.G. & Moncada, S. (1994) Nitric oxide synthase in mammals. Biochem. J., 298, 249-258.
23. Kohn, K.W., Ewig, R.A.C., Erickson, L.C. & Zwelling, L.A. (1981) Measurement of strand breaks and crosslinks by alkaline elution. In Friedberg, E. & Hanawalt, P. (eds), DNA Repair: a Laboratory Manual of Research Procedures, Vol. I Part B. Marcel Dekker Inc, New York, pp. 397-401.
24. Latour, I., Demoulin, J.B. & Buc-Calderon, P. (1995) Oxidative DNA damage by t-butyl hydroperoxide causes DNA single strand breaks which are not linked to cell lysis. A mechanistic study in freshly isolated rat hepatocytes. FEBS Lett., 373, 299-302.
25. Mandir, A.S., Przedborski, S., Jackson-Lewis, V., Wang, Z.Q., Simbulan-Rosenthal, C.M., Smulson, M.E., Hoffman, B.E., Guastella, D.B., Dawson, V.L. & Dawson, T.M. (1999) Poly (ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) -induced parkinsonism. Proc. Natl Acad. Sci. USA, 96, 5774-5779.
26. Moncada, S., Palmer, R.M.J. & Higgs, E.A. (1991) Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol. Rev., 43, 109-142.
27. Müller, W.U., Bauch, T., Streffer, C., Niedereichholz, F. & Böcker, W. (1994) Comet assay studies of radiation-induced DNA damage and repair in various tumor cell lines. Int. J. Radiat. Biol., 65, 315-319.
28. Pieper, A.A., Verma, A., Zhang, J. & Snyder, S.H. (1999) Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol. Sci., 20, 171-181.
29. Pryor, W.A., Jin, X. & Squadrito, G.L. (1994) One-and two-electron oxidations of methionine by peroxynitrite. Proc. Natl Acad. Sci. USA, 91, 11173-11177.
30. Salgo, M.G. & Pryor, W.A. (1996) Trolox inhibits peroxynitrite-mediated oxidative stress and apoptosis in rat thymocytes. Arch. Binchem. Biophys., 333, 482-488.
31. Sandström, B.E. (1991) Induction and rejoining of DNA single-strand breaks in relation to cellular growth in human cells exposed to three hydroperoxides at 0°C and 37°C. Free Rad. Res. Comm., 15, 79-89.
32. 2+ transport by intact synaptosomes: intra-synaptosomal compartmentation and the role of the mitochondrial membrane potential. Biochem, J., 192, 873-880.
33. Sestili, P., Cattabeni, F. & Cantoni, O. (1995) Simultaneous determination of DNA double strand breaks and DNA fragment size in cultured mammalian cells exposed to hydrogen peroxide/histidine or etoposide with CHEF electrophoresis. Carcinogenesis, 16, 703-706.
34. Singh, N.P., McCoy, M.T., Tice, R.R. & Schneider, E.L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res., 175, 184-191.
35. Tominaga, T., Kure, S., Narisawa, K. & Yoshimoto, T. (1993) Endonuclease activation following focal ischemic injury in the rat brain. Brain Res., 608, 21-26.
36. Turrens, J.F., Alexandre, A. & Lehninger, A.L. (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys., 237, 408-414.
37. Wang, M.Y. & Liehr, J.G. (1995) Lipid hydroperoxide-induced endogenous DNA adducts in hamsters: possible mechanism of lipid hydroperoxide-mediated carcinogenesis. Arch. Biochem. Biophys., 316, 38-46.