Attenuation in the evolution of experimental spinal cord trauma by treatment with melatonin

Journal of Pineal Research

Volumn 38, Issue 3, 2005, Pages 198-208

  Genovese, Tiziana ^a   Mazzon, Emanuela ^a   Muià, Carmelo ^a   Bramanti, Placido ^b   De Sarro, Angelina ^a   Cuzzocrea, Salvatore ^a,b  

^a Dept Clin Exp Med and Pharmacol ^*  (Italy)

^b UNIVERSITY OF MESSINA   (Italy)

Author keywords

Melatonin; Nuclear factor B; Peroxinitrite; Poly ADP ribose synthetase; Secondary injury; Spinal cord injury; Tunnel coloration

Indexed keywords

3 NITROTYROSINE; DNA NUCLEOTIDYLEXOTRANSFERASE; MALONALDEHYDE; MELATONIN; MYELOPEROXIDASE; PEROXYNITRITE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); SCAVENGER;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EDEMA; EVIDENCE BASED MEDICINE; HORMONE ACTION; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IMMUNOREACTIVITY; LAMINECTOMY; MYELITIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; RAT; SPINAL CORD INJURY;

ANIMALS; APOPTOSIS; DNA; ENZYME ACTIVATION; FREE RADICAL SCAVENGERS; I-KAPPA B PROTEINS; LIPID PEROXIDATION; MALE; MELATONIN; NEUTROPHILS; NF-KAPPA B; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; TYROSINE;

EID: 15444378210     PISSN: 07423098     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2004.00194.x     Document Type: Article

References (76)

1. KALTSCHMIDT B, BAUERLE PA. KALTSCHMIDT C. Potential involvement of the transcription factor NF-κB in neurological disorders. Mol Aspects Med 1993; 14:171-190.
2. BARTHOLDI D, SCHWAB ME. Methylprednisolone inhibits early inflammatory processes but not ischemic cell death after experimental spinal cord lesion in the rat. Brain Res 1995; 672:177-186.
3. BALENTINE JD. Hypotheses in spinal cord trauma research. In: Central Nervous System Trauma Status Report. Becker DP, Povlishock JT eds. NIH, Bethesda, MD, USA, 1985; pp. 455-461.
4. YOUNG W. Session 2: secondary CNS injury. J Neurotrauma 1988; 5:219-234.
5. CUZZOCREA S, RILEY DP, CAPUTI AP et al. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol Rev 2001; 53:135-159.
6. XU J, KIM GM, CHEN S et al. iNOS and nitrotyrosine expression after spinal cord injury. J Neurotrauma 2001; 18:523-532.
7. HAGLIND E, XIA G, RYLANDER R. Effects of antioxidants and PAF receptor antagonist in intestinal shock in the rat. Circ Shock 1994;42:83-91.
8. FANTONE JC, WARD PA. A review: role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. Am J Pathol 1982; 107:395-418.
9. LI Y, FERRANTE A, POULOS A et al. Neutrophil oxygen radical generation. Synergistic responses to tumor necrosis factor and mono/polyunsaturated fatty acids. J Clin Invest 1996; 97:1605-1609.
10. BOUGHTON-SMITH NK, EVANS SM, LASZLO F et al. The induction of nitric oxide synthase and intestinal vascular permeability by endotoxin in the rat. Br J Pharmacol 1993; 110:1189-1195.
11. SALVEMINI D, JENSEN MP, RILEY DP et al. Therapeutic manipulations of peroxynitrite. Drug News Persp 1998; 11:204-214.
12. Dix TA, HESS KM, MEDINA MA et al. Mechanism of site-selective DNA nicking by the hydrodioxyl (perhydroxyl) radical. Biochemistry 1996; 35:4578-4583.
13. BECKMAN JS, CROW LP. Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem Soc Trans 1993; 21:330-334.
14. CUZZOCREA S, CAPUTI AP, ZINGARELLI B. Peroxynitrite-mediated DNA strand breakage activates poly (ADP-ribose) synthetase and causes cellular energy depletion in carrageenan-induced pleurisy. Immunology 1998; 93:96-101.
15. SZABÒ C, VIRAG L, CUZZOCREA. S et al. Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly (ADP-ribose) synthetase. Proc Natl Acad Sci USA 1998; 95:3867-3872.
16. PETERS RT, LIAO SM, MANIATIS T. Ikkepsilon is part of a novel PMA-inducible IκappaB kinase complex. Mol Cell 2000; 5:513-522.
17. BOWIE A, O'NEILL LA. Oxidative stress and nuclear factor-κappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol 2000; 59:13-23.
18. MCKAY LI, CIDLOWSKI JA. Molecular control of immune/inflammatory responses: interactions between nuclear factor-kappa B and steroid receptor-signaling pathways. Endocr Rev 1999; 20:435-459.
19. GILAD E, CUZZOCREA S, ZINGARELLI B et al. Melatonin is a scavenger of peroxynitrite. Life Sci 1997; 60:PL169-PL174.
20. TAN DX, REITER RJ, MANCHESTER LC et al. Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2002; 2:181-197.
21. CAZEVIEILLE C, SAFA R, OSBORNE NN. Melatonin protects primary cultures of rat cortical neurons from NMDA excitotoxicity and hypoxia/reoxygenation. Brain Res 1997; 768:120-124.
22. GUERRERO JM, REITER RJ, ORTIZ GG et al. Melatonin prevents increases in neural nitric oxide and cyclic GMP production after transient brain ischemia and reperfusion in the Mongolian gerbil. J Pineal Res 1997; 23:24-31.
23. RIVLIN AS, TATOR CH. Effect of duration of acute spinal cord compression in a new acute cord injury model in the rat. Surg Neurol 1978; 10:38-43.
24. KIM GM, XU J, XU J et al. Tumor necrosis factor receptor deletion reduces nuclear factor-kappaB activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury. J Neurosci 2001; 21:6617-6625.
25. CUZZOCREA S, ZINGARELLI B, GILARD E et al. Protective effect of melatonin in carrageenan-induced models of local inflammation. J Pineal Res 1997; 23:106-116.
26. CUZZOCREA S, MISKO TP, COSTANTINO G et al. Beneficial effects of peroxynitrite decomposition catalyst in a rat model of splanchnic artery occlusion and reperfusion. Faseb J 2000; 14:1061-1072.
27. LIU D, LING X, WEN J et al. The role of reactive nitrogen species in secondary spinal cord injury: formation of nitric oxide, peroxynitrite, and nitrated protein. J Neurochem 2000; 75:2144-2154.
28. BAO F, LIU D. Peroxynitrite generated in the rat spinal cord induces neuron death and neurological deficits. Neuroscience 2002; 115:839-849.
29. SHEA TB. Technical report. An inexpensive densitometric analysis system using a Macintosh computer and a desktop scanner. Biotechniques 1994; 16:1126-1128.
30. MULLANE KM, KRAEMER R, SMITH B. Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischemic myocardium. J Pharmacol Meth 1985; 14:157-167.
31. HAMADA Y, IKATA T, KATOH S et al. Roles of nitric oxide in compression injury of rat spinal cord. Free Rad Biol Med 1996; 20:1-9.
32. OHKAWA H, OHISHI N, YAGI K. Assay for peroxidases in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95:351-358.
33. LIU JB, TANG TS, YANG HL et al. Antioxidation of melatonin against spinal cord injury in rats. Chin Med J (Engl) 2004; 117:571-575.
34. TARLOV IM, KLINGER H. Spinal cord compression studies. Arch Neurol Psychiat 1954; 71:271-290.
35. MAESTRONI GJ, CONTI A, PIERPAOLI W. Role of the pineal gland in immunity. Circadian synthesis and release of melatonin modulates the antibody response and antagonizes the immunosuppressive effect of corticosterone. J Neuroimmunol 1986; 13:19-30.
36. PIERI C, MARRA M, MORONI F et al. Melatonin: a peroxyl radical scavenger more effective than vitamin E. Life Sci 1994; 55:PL271-PL276.
37. REITER RJ. The role of the neurohormone melatonin as a buffer against macromolecular oxidative damage. Neurochem Int 1995; 27:453-460.
38. SEWERYNEK E, ABE M, REITER RJ et al. Melatonin administration prevents lipopolysaccharide-induced oxidative damage in phenobarbital-treated animals. J Cell Biochem 1995; 58:436-444.
39. MOHAN N, SADEGHI K, REITER RJ et al. The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-κappa B. Biochem Mol Biol Int 1995; 37:1063-1070.
40. ROBERTS ML, COWSERT LM. Interleukin-1 beta and reactive oxygen species mediate activation of c-Jun NH2-terminal kinases, in human epithelial cells, by two independent pathways. Biochem Biophys Res Commun 1998; 251:166-172.
41. GHOSH S, BALTIMORE D. Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature 1990; 344:678-682.
42. CHEN ZJ, PARENT L, MANIATIS T. Site-specific phosphorylation of I Kappa B alpha by a novel ubiquitination-dependent protein kinase activity. Cell 1996; 84:853-862.
43. GILAD E, WONG HR. ZINGARELLI B et al. Melatonin inhibits expression of the inducible isoform of nitric oxide synthase in murine macrophages: role of inhibition of NFκappaB activation. Faseb J 1998; 12:685-693.
44. STEPHENSON D, YIN T, SMALSTIG EB et al. Transcription factor nuclear factor-kappa B is activated in neurons after focal cerebral ischemia. J Cereb Blood Flow Metab 2000; 20:592-603.
45. ENDOH M, MAIESE K, WAGNER J. Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia. Brain Res 1994; 651:92-100.
46. REITER RJ, MELCHIORRI D, SEWERYNEK E et al. A review of the evidence supporting melatonin's role as an antioxidant. J Pineal Res 1995; 18:1-11.
47. MARSHALL KA, REITER RJ, POEGGELER B et al. Evaluation of the antioxidant activity of melatonin in vitro. Free Radical Biol Med 1996; 21:307-315.
48. BARLOW-WALDEN LR, REITER RJ, ABE M et al. Melatonin stimulates brain glutathione peroxidase activity. Neurochem Int 1995; 26:497-504.
49. ANTOLIN I, RODRIGUEZ C, SAINZ RM et al. Neurohormone melatonin prevents cell damage: effect on gene expression for antioxidant enzymes. Faseb J 1996; 10:882-890.
50. PABLOS MI, AGAPITO MT, GUTIERREZ R et al. Melatonin stimulates the activity of the detoxifying enzyme glutathione peroxidase in several tissues of chicks. J Pineal Res 1995; 19:111-115.
51. VISWANATHAN M, LAITINEN JT, SAAVEDRA JM. vascular melatonin receptors. Biol Signals 1993; 2:221-227.
52. CARLBERG C, WIESENBERG I. The orphan receptor family RZR/ROR, melatonin and 5-lipoxygenase: an unexpected relationship. J Pineal Res 1996; 18:171-178.
53. MISSBACH M, JAGHER B, SIGG I et al. Thiazolidine diones, specific ligands of the nuclear receptor retinoid Z receptor/retinoid acid receptor-related orphan receptor alpha with potent antiarthritic activity. J Biol Chem 1996; 271:13515-13522.
54. SZABO C, DAWSON VL. Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol Sci 1998; 19:287-298.
55. IKAI K, UEDA K. Immunohistochemical demonstration of poly (adenosine diphosphate-ribose) synthetase in bovine tissues. J Histochem Cytochem 1983; 31:261-264.
56. CHIARUGI A. Poly(ADP-ribose) polymerase: killer or conspirator? The 'suicide hypothesis' revisited. Trends Pharmacol Sci 2002; 23:22-129.
57. CHIARUGI A, MOSKOWITZ MA. Poly(ADP-ribose) polymerase-1 activity promotes NF-kappaB-driven transcription and microglial activation: implication for neurodegenerative disorders. J Neurochem 2003; 85:306-317.
58. SKAPER SD. Poly(ADP-Ribose) polymerase-1 in acute neuronal death and inflammation: a strategy for neuroprotection. Ann N Y Acad Sci 2003; 993:217-228.
59. DI MEGLIO S. TRAMONTANO F, CIMMINO G, JONES R, QUESADA P. Dual role for poly(ADP-ribose)polymerase-1 and -2 and poly(ADP-ribose)glycohydrolase as DNA-repair and pro-apoptotic factors in rat germinal cells exposed to nitric oxide donors. Biochim Biophys Acta 2004; 1692:35-44.
60. KIM YH, KOH JY. The role of NADPH oxidase and neuronal nitric oxide synthase in zinc-induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. Exp Neurol. 2002; 177:407-418.
61. LACZA Z, HORVATH EM, KOMJATI K et al. PARP inhibition improves the effectiveness of neural stem cell transplantation in experimental brain trauma. Int J Mol Med 2003; 12:153-159.
62. DUCROCQ S, BENJELLOUN N, PLOTKINE M et al. Poly(ADP-ribose) synthase inhibition reduces ischemic injury and inflammation in neonatal rat brain. J Neurochem 2000; 74:2504-2511.
63. LIN KT, XUE JY, NOMEN M et al. Peroxynitrite-induced apoptosis in HL-60 cells. J Biol Chem 1995; 94:16487-16490.
64. SZABO C, CUZZOCREA S, ZINGARELLI B et al. Endothelial dysfunction in endotoxic shock: importance of the activation of poly (ADP ribose) synthetase (PARS) by peroxynitrite. J Clin Invest 1997; 94:723-735.
65. VIRAG L, SCOTT GS, CUZZOCREA S et al. Peroxynitrite-induced thymocyte apoptosis: the role of caspases and poly (ADP-ribose) synthetase (PARS) activation. Immunology 1998; 94:345-355.
66. LEIST M, VOLBRACHT C, KUHNLE S et al. Caspase-mediated apoptosis in neuronal excitotoxicity triggered by nitric oxide. Mol Med 1997; 3:750-764.
67. SHUMAN SL, BRESNAHAN JC, BEATTIE MS. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res 1997; 1:798-808.
68. ABE Y, YAMAMOTO T, SUGIYAMA Y et al. Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J Neurotrauma 1999; 16:945-952,
69. CHEN KB, LIN AM, CHIU TH. Oxidative injury to the locus coeruleus of rat brain: neuroprotection by melatonin. J Pineal Res 2003; 35:109-117.
70. KUNDUZOVA OR, ESCOURROU G, SEGUELAS MH et al. Prevention of apoptotic and necrotic cell death, caspase-3 activation, and renal dysfunction by melatonin after ischemia/reperfusion. Faseb J 2003; 17:872-874.
71. FUJIMOTO T, NAKAMURA T, IKEDA T et al. Potent protective effects of melatonin on experimental spinal cord injury. Spine 2000; 25:769-775.
72. KAPTANOGLU E, TUNCEL M, PALAOGLU S et al. Comparison of the effects of melatonin and methylprednisolone in experimental spinal cord injury. J Neurosurg Spine 2000; 93:77-84.
73. ERTEN SF, KOCAK A, OZDEMIR I et al. Protective effect of melatonin on experimental spinal cord ischemia. Spinal Cord 2003; 41:533-538.
74. CUZZOCREA S, REITER RJ. Pharmacological actions of melatonin in acute and chronic inflammation. Curr Top Med Chem 2002; 2:153-165.
75. MANEV H, UZ T, KHARLAMOV A et al. Increased brain damage after stroke or excitotoxic seizures in melatonin-deficient rats. Faseb J 1996; 13:1546-1551.
76. CUZZOCREA S, TAN DX, COSTANTINO G et al. The protective role of endogenous melatonin in carrageenan-induced pleurisy in the rat. Faseb J 1999; 13:1930-1938.