Nitric oxide and superoxide anion differentially activate poly(ADP-ribose) polymerase-1 and Bax to induce nuclear translocation of apoptosis-inducing factor and mitochondrial release of cytochrome c after spinal cord injury

Journal of Neurotrauma

Volumn 26, Issue 7, 2009, Pages 965-977

  Wu, Kay L H ^a,b   Hsu, Chin ^b   Chan, Julie Y H ^a  

^a KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Mitochondrial respiratory enzyme complex; Nitric oxide; Spinal cord injury; Superoxide anion

Indexed keywords

APOPTOSIS INDUCING FACTOR; CYTOCHROME C; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NITRIC OXIDE; PROTEIN BAX; SUPEROXIDE; TEMPOL; ADENOSINE TRIPHOSPHATE; ADPRT PROTEIN, RAT; INDUCIBLE NITRIC OXIDE SYNTHASE; N-(OXO-5,6-DIHYDROPHENANTHRIDIN-2-YL)-N,N-DIMETHYLACETAMIDE HYDROCHLORIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHENANTHRENE DERIVATIVE; S-METHYLISOTHIOPSEUDOURONIUM; THIOUREA DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA FRAGMENTATION; ENZYME ACTIVITY; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OSMOTIC MINIPUMP; OSMOTIC PUMP; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT; UPREGULATION; ACTIVE TRANSPORT; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL NUCLEUS; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; MITOCHONDRION; SPINAL CORD; VERTEBRA; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELL NUCLEUS; CYTOCHROMES C; ENZYME-LINKED IMMUNOSORBENT ASSAY; ISOTHIURONIUM; MALE; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHENANTHRENES; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES; SUPEROXIDES; THORACIC VERTEBRAE;

EID: 69249132073     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0692     Document Type: Article

References (55)

1. Abdelkarim, G.E., Gertz, K., Harms, C., Katchanov, J., Dirnagl, U., Szabo, C., and Endres, M. (2001). Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke. Int. J. Mol. Med. 7, 255-260.
2. Aulak, K.S., Koeck, T., Crabb, J.W., and Stuehr, D.J. (2004). Dynamics of protein nitration in cells and mitochondria. Am. J. Physiol. Heart Circ. Physiol. 286, H30-H38.
3. Austin, J.W., and Fehlings, M.G. (2008) Molecular mechanisms of Fas-mediated cell death in oligodendrocytes. J. Neurotrauma 25, 411-426. (Pubitemid 351685488)
4. Bao, F., Chen, Y., Dekaban, G.A., and Weaver, L.C. (2004). Early anti-inflammatory treatment reduces lipid peroxidation and protein nitration after spinal cord injury in rats. J. Neurochem. 88,1335-1344. (Pubitemid 38366908)
5. Beattie, M.S., Hermann, G.E., Rogers, R.C., and Bresnahan, J.C. (2002). Cell death in models of spinal cord injury. Prog. Brain Res. 137, 37-47.
6. 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. USA 87, 1620-1624.
7. Besson, V.C., Zsengeller, Z., Plotkine, M., Szabo, C., and Marchand-Verrecchia, C. (2005). Beneficial effects of PJ34 and INO-1001, two novel water-soluble poly(ADP-ribose) polymerase inhibitors, on the consequences of traumatic brain injury in rat. Brain Res. 1041, 149-156. (Pubitemid 40501328)
8. Bonfoco, E., Ceccatelli, S., Manzo, L., and Nicotera, P. (1995). Colchicine induces apoptosis in cerebellar granule cells. Exp. Cell Res. 218, 189-200.
9. Brown, G.C. (1997). Nitric oxide inhibition of cytochrome oxidase and mitochondrial respiration: implications for inflammatory, neurodegenerative and ischaemic pathologies. Mol. Cell Biochem. 174, 189-192.
10. Brown, G.C. (1999). Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta 1411, 351-369.
11. Brown, G.C., and Borutaite, V. (2007). Nitric oxide and mitochondrial respiration in the heart. Cardiovasc. Res. 75, 283-290.
12. Carlson, G.D., and Gorden, C. (2002). Current developments in spinal cord injury research. Spine J. 2, 116-128.
13. Chan, J.Y.H., Chang, A.Y.W., Wang, L.L., Ou, C.C., and Chan, S.H.H. (2007). Protein kinase C-dependent mitochondrial translocation of proapoptotic protein Bax on activation of inducible nitric oxide synthase in rostral ventrolateral medulla mediates cardiovascular depression during experimental endotoxemia. Mol. Pharmacol. 71, 1129-1139.
14. Chan, S.H.H., Wu, K.L., Wang, L.L., and Chan, J.Y.H. (2005). Nitric oxide- and superoxide-dependent mitochondrial signaling in endotoxin-induced apoptosis in the rostral ventrolateral medulla of rats. Free Radic. Biol. Med. 39, 603-618.
15. Chuang, Y.C., Tsai, J.L., Chang, A.Y., Chan, J.Y.H., Liou, C.W., and Chan, S.H.H. (2002). Dysfunction of the mitochondrial respiratory chain in the rostral ventrolateral medulla during experimental endotoxemia in the rat. J. Biomed. Sci. 9, 542-548.
16. Clementi, E., Brown, G.C., Feelisch, M., and Moncada, S. (1998). Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. USA 95, 7631-7636.
17. Conti, A., Miscusi, M., Cardali, S., Germano, A., Suzuki, H., Cuzzocrea, S., and Tomasello, F. (2007). Nitric oxide in the injured spinal cord: syntheses cross-talk, oxidative stress and inflammation. Brain Res. Rev. 54, 205-218.
18. Crompton, M. (1999). The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341, 233-249. (Pubitemid 29373645)
19. Dawson, V.L., and Dawson, T.M. (2004). Deadly conversations: nuclear-mitochondrial cross-talk. J. Bioenerg. Biomembr. 36, 287-294.
20. Galkin, A., and Moncada, S. (2008). S-nitrosylation of mitochondrial complex I depends on its structural conformation. J. Biol. Chem. 282, 37448-37453.
21. Genovese, T., Mazzon, E., Di Paola, R., Muia, C., Threadgill, M.D., Caputi, A.P., Thiemermann, C., and Cuzzocrea, S. (2005). Inhibitors of poly(ADP-ribose) polymerase modulate signal transduction pathways and the development of bleomycin-induced lung injury. J. Pharmacol. Exp. Ther. 313, 529-538.
22. Hoch, F.L. (1998). Cardiolipins and mitochondrial protonselective leakage. J. Bioenerg. Biomembr. 30, 511-532.
23. Huie, R.E., and Padmaja, S. (1993). The reaction of NO with superoxide. Free Radic. Res. Commun. 18, 195-199.
24. Joseph, T.W., and Moll, U.M. (2003). Analysis of nuclear and cytoplasmic degradation of p53 in cells after stress. Methods Mol. Biol. 234, 211-217.
25. Kantrow, S.P., Taylor, D.E., Carraway, M.S., and Piantadosim, C.A. (1997). Oxidative metabolism in rat hepatocytes and mitochondria during sepsis. Arch. Biochem. Biophys. 345, 278-288.
26. Keane, R.W., Davis, A.R., and Dietrich, W.D. (2006). Inflammatory and apoptotic signaling after spinal cord injury. J. Neurotrauma 23, 335-344. (Pubitemid 43726314)
27. Kroemer, G., and Martin, S.J. (2005). Caspase-independent cell death. Nat. Med. 11, 725-730.
28. Kwak, E.K., Kim, J.W., Kang, K.S., Lee, Y.H., Hua, Q.H., Park, T.I., Park, J.Y., and Sohn, Y.K. (2005). The role of inducible nitric oxide synthase following spinal cord injury in rat. J. Korean Med. Sci. 20, 663-669.
29. Latini, A., Scussiato, K., Rosa, R.B., Leipnitz, G., Llesuy, S., Bello-Klein, A., Dutra-Filho, C.S., and Wajner, M. (2003). Induction of oxidative stress by L-2-hydroxyglutaric acid in rat brain. J. Neurosci. Res. 74, 103-110.
30. Maier, C., Scheuerle, A., Hauser, B., Schelzig, H., Szabó, C., Radermacher, P., and Kick, J. (2007). The selective poly(ADP)ribose-polymerase 1 inhibitor INO1001 reduces spinal cord injury during porcine aortic cross-clamping-induced ischemia/reperfusion injury. Intensive Care Med. 33, 845-850. (Pubitemid 46675322)
31. Meany, D.L., Poe, B.G., Navratil, M., Moraes, C.T., and Arriaga, E.A. (2006). Superoxide released into the mitochondrial matrix. Free Radic. Biol. Med. 41, 950-959.
32. Naithani, S., Saracco, S.A., Butler, C.A., and Fox, T.D. (2003). Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol. Biol. Cell 14, 324-333.
33. Nakahara, S., Yone, K., Setoguchi, T., Yamaura, I., Arishima, Y., Yoshino, S., and Komiya, S. (2002). Changes in nitric oxide and expression of nitric oxide synthase in spinal cord after acute traumatic injury in rats. J. Neurotrauma 19, 1467-1474. (Pubitemid 35403675)
34. Nomura, K., Imai, H., Koumura, T., and Nakagawa, Y. (2001). Involvement of mitochondrial phospholipid hydroperoxide glutathione peroxidase as an antiapoptotic factor. Biol. Signals Recept. 10, 81-92.
35. Opii, W.O., Nukala, V.N., Sultana, R., Pandya, J.D., Day, K.M., Merchant, M.L., Klein, J.B., Sullivan, P.G., and Butterfield, D.A. (2007). Proteomic identification of oxidized mitochondrial proteins following experimental traumatic brain injury. J. Neurotrauma 24, 772-789. (Pubitemid 46799270)
36. Paradies, G., Petrosillo, G., Pistolese, M., and Ruggiero, F.M. (2001). Reactive oxygen species generated by the mitochondrial respiratory chain affect the complex III activity via cardiolipin peroxidation in beef-heart submitochondrial particles. Mitochondrion 1, 151-159. (Pubitemid 33586026)
37. Sastre, J., Pallardo, F.V., and Vina, J. (2000). Mitochondrial oxidative stress plays a key role in aging and apoptosis. IUBMB Life 49, 427-435. (Pubitemid 30436178)
38. Satake, K., Matsuyama, Y., Kamiya, M., Kawakami, H., Iwata, H., Adachi, K., and Kiuchi, K. (2000). Nitric oxide via macrophage iNOS induces apoptosis following traumatic spinal cord injury. Mol. Brain Res. 28, 114-122.
39. 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.
40. Sheeran, F.L., and Pepe, S. (2006). Energy deficiency in the failing heart: linking increased reactive oxygen species and disruption of oxidative phosphorylation rate Biochem. Biophys. Acta 1757, 543-552.
41. Sheh, Y.L., Hsu, C., Chan, S.H.H., and Chan, J.Y.H. (2007). NADPH oxidase- and mitochondrion-derived superoxide at rostral ventrolateral medulla in endotoxin-induced cardiovascular depression. Free Radic. Biol. Med. 42, 1610-1623.
42. Stefanis, L. (2005). Caspase-dependent and -independent neuronal death: two distinct pathways to neuronal injury. Neuroscientist 11, 50-62. (Pubitemid 40223090)
43. Sugawara, T., Lewen, A., Gasche, Y., Yu, F., and Chan, P.H. (2002). Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. FASEB J. 16, 1997-1999.
44. Susin, S.A., Daugas, E., Ravagnan, L., Samejima, K., Zamzami, N., Loeffler, M., Costantini, P., Ferri, K.F., Irinopoulou, T., Prévost, M.C., Brothers, G., Mak, T.W., Penninger, J., Earnshaw, W.C., and Kroemer, G. (2000). Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192, 571-580.
45. Vaziri N.D., Lee Y.S., Lin C.Y., Lin V.W., and Sindhu R.K. (2004) NAD(P)H oxidase, superoxide dismutase, catalase, glutathione peroxidase and nitric oxide synthase expression in subacute spinal cord injury. Brain Res. 995, 76-83. (Pubitemid 37486017)
46. Wingrave, J.M., Schaecher, K.E., Scibnick, E.A., Wilford, G.G., Ray, S.K., Hazen-Martin, D.J., Hogan, E.L., and Banik, N.L. (2003). Early induction of secondary injury factors causing activation of calpain and mitochondria-mediated neuronal apoptosis following spinal cord injury in rats. J. Neurosci. Res. 73, 95-104.
47. Wu, K.L.H., Hsu, C., and Chan, J.Y.H. (2007). Impairment of the mitochondrial respiratory enzyme activity triggers sequential activation of apoptosis-inducing factor-dependent and caspase-dependent signaling pathways to induce apoptosis after spinal cord injury. J. Neurochem. 101, 1552-1566. (Pubitemid 46848847)
48. Xu, W., Chi, L., Xu, R., Ke, Y., Luo, C., Cai, J., Qiu, M., Gozal, D., and Liu, R. (2005). Increased production of reactive oxygen species contributes to motor neuron death in a compression mouse model of spinal cord injury. Spinal Cord 43, 204-213. (Pubitemid 40546718)
49. Xu, Z., Wang, B.R., Wang, X., Kuang, F., Duan, X.L., Jiao, X.Y., and Ju, G. (2006). ERK1/2 and p38 mitogen-activated protein kinase mediate iNOS-induced spinal neuron degeneration after acute traumatic spinal cord injury. Life Sci. 79, 1895-1905. (Pubitemid 44485117)
50. Yakovlev, A.G., and Faden, A.I. (2001). Caspase-dependent apoptotic pathways in CNS injury. Mol. Neurobiol. 24, 131-144.
51. Yeo, J.E., Kim, J.H., and Kang, S.K. (2008). Selenium attenuates ROS-mediated apoptotic cell death of injured spinal cord through prevention of mitochondria dysfunction; in vitro and in vivo study. Cell Physiol. Biochem. 21, 225-238.
52. Yu, F., Sugawara, T., Nishi, T., Liu, J., and Chan, P.H. (2006a). Overexpression of SOD1 in transgenic rats attenuates nuclear translocation of endonuclease G and apoptosis after spinal cord injury. J. Neurotrauma 23, 595-603. (Pubitemid 43728049)
53. Yu, S.W., Wang, H., Poitras, M.F., Coombs, C., Bowers, W.J., Federoff, H.J., Poirier, G.G., Dawson, T.M., and Dawson, V.L. (2002). Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297, 259-263. (Pubitemid 34761289)
54. Yu, S.W., Andrabi, S.A., Wang, H., Kim, N.S., Poirier, G.G., Dawson, T.M., and Dawson, V.L. (2006b). Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc. Natl. Acad. Sci. USA 103, 18314-18319.
55. Zhang, X., Chen, J., Graham, S.H., Draviam, R., Guo, F., Nathaniel, P.D., Szabó, C., Watkins, S.C., and Clark, R.S. (2002). Intranuclear localization of apoptosis-inducing factor (AIF) and large scale DNA fragmentation after traumatic brain injury in rats and in neuronal cultures exposed to peroxynitrite. J. Neurochem. 82, 181-191. (Pubitemid 34755263)