Melatonin ameliorates neurologic damage and neurophysiologic deficits in experimental models of stroke

Annals of the New York Academy of Sciences

Volumn 993, Issue , 2003, Pages 35-47

  Reiter, Russel J ^a   Sainz, Rosa M ^a   Lopez Burillo, Silvia ^a   Mayo, Juan C ^a   Manchester, Lucien C ^a   Tan, Dun Xian ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Antioxidant; Brain; Ischemia reperfusion injury; Melatonin; Neuroprotection; Stroke

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; EXCISION REPAIR CROSS COMPLEMENTING FACTOR 6; GENE PRODUCT; LIPID; MELATONIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APOPTOSIS; BRAIN BLOOD FLOW; BRAIN INFARCTION; CAT; CELL SURVIVAL; CONFERENCE PAPER; CONTROLLED STUDY; EXCISION REPAIR; GENE EXPRESSION; GERBIL; GLIOSIS; ISCHEMIA; NERVOUS SYSTEM INJURY; NEUROPHYSIOLOGY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTO ONCOGENE; RAT; REPERFUSION INJURY; STROKE;

ANIMALIA; FELIS CATUS; GERBILLINAE;

EID: 0038389599     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2003.tb07509.x     Document Type: Conference Paper

References (89)

1. BERNAT, J.L. 1997. Systemic hypoperfusion brain injury. In Primer on Cerebrovascular Diseases. K.M.A. Welch, L.R. Caplan, D.J. Reis, et al., Eds.: 289-292. Academic Press, San Diego.
2. PESSIN, M.S. 1997. Anterior circulation - large artery occlusive disease and embolism. In Primer on Cerebrovascular Diseases. K.M.A. Welch, L.R. Caplan, D.J. Reis, et al., Eds.: 293-298. Academic Press, San Diego.
3. SAUER, D., J. NUGLISCH, C. ROSSBERG, et al. 1988. Phencyclidine reduces postischemic neuronal necrosis in rat hippocampus without changing blood flow. Neurosci. Lett. 91: 327-332.
4. STEINBERG, G.K., J. SALEH & D. KUNIS. 1988. Delayed treatment with dextromethorphan and dextrorphan reduces cerebral damage after transient focal ischemia. Neurosci. Lett. 84: 193-197.
5. RESPHANDE, J.K. & T. WIELOCK. 1985. Amelioration of ischemic brain damage following postischemic treatment with flunarizine. Neurol. Res. 7: 27-29.
6. NUGLISCH, J., C. KARKOUTLY, H.D. MENNEL, et al. 1990. Protective effect of nimodipine against ischemic neuronal damage in rat hippocampus without changing post-ischemic cerebral blood flow. J. Cereb. Blood Flow Metab. 10: 654-659.
7. BODE-GREVEL, K.M., J. KLISCH, E. HORVATH, et al. 1990. Effects of 5-hydroxytryptamine-receptor agonists on hippocampal damage after transient forebrain ischemia in the Mongolian gerbil. Stroke 21(Suppl. IV): 164-166.
8. PREHN, J.H.M., C. BACKHAUSS, C. KARTOUTLY, et al. 1991. Neuroprotective properties of 5-HT1A agonists in rodent models of focal and global cerebral ischemia. Eur. J. Pharmacol. 203: 231-222.
9. EVANS, M.C., J.H. SWAN & B.S. MELDRUM. 1987. An adenosine analogue 2-chloroadenosine, protects against long-term development of ischemic cell loss in the rat hippocampus. Neurosci. Lett. 83: 287-292.
10. SAUER, D., R. RISCHKE, T. BECK, et al. 1988. Vinpocetine prevents ischemic cell damage in rat hippocampus. Life Sci. 43: 1733-1739.
11. MARTZ, D., G. RAYOS, G.P. SCHIELKE & A.L. BETZ. 1989. Allopurinol and dimethythiourea reduce brain infarction following middle cerebral artery occlusion in the rat. Stroke 20: 488-494.
12. PREHN, J.H.M., C. KARKOUTLY, J. NUGLISCH, et al. 1992. Dihydrolipoate reduces neuronal injury after cerebral ischemia. J. Cereb. Blood Flow Metab. 12: 78-87.
13. WIELOCH, T., T. KOIDE & E. WESTERBERG. 1996. Inhibitory neurotransmitter and neuromodulators as protective agents against ischemic brain damage. In Pharmacology of Cerebral Ischemia. J. Krieglstein, Ed.: 191-197. Elsevier Science, Amsterdam.
14. GINSBERG, M.D. 1997. Animal models of global and focal cerebral ischemia. In Primer on Cerebrovascular Diseases. K.M.A. Welch, L.R. Caplan, D.J. Reis, et al., Eds.: 124-126. Academic Press, San Diego.
15. MENENDEZ-PELAEZ, A., B. POEGGELER, R.J. REITER, et al. 1993. Nuclear localization of melatonin in different mammalian tissues: immunocytochemical and radioimmunoassay evidence. J. Cell. Biochem. 53: 373-382.
16. TRICOIRE, H., A. LOCATELLI, P. CHEMINEAU & B. MALPAUX. 2002. Melatonin enters the cerebrospinal fluid through the pineal recess. Endocrinology 143: 84-90.
17. REITER, R.J. & D.X. TAN. 2002. Role of CSF in the transport of melatonin. J. Pineal Res. 33: 61.
18. REITER, R.J., D.X. TAN, C. OSUNA & E. GITTO. 2000. Actions of melatonin in the reduction of oxidative stress: a review. J. Biomed. Sci. 7: 444-458.
19. TAN, D.X., R.J. REITER, L.C. MANCHESTER, et al. 2002. Chemical and physiological properties and potential mechanisms: melatonin as a broad-spectrum antioxidant and free radical scavenger. Curr. Topics Med. Chem. 2: 181-198.
20. ALLEGRA, M., R.J. REITER, D.X. TAN, et al. 2003. The chemistry of melatonin's interaction with reactive species. J. Pineal Res. 34: 1-10.
21. REITER, R.J. 2000. Melatonin: lowering the high price of free radicals. News Physiol Sci. 15: 246-250.
22. TAN, D.X., L.C. MANCHESTER, R.J. REITER, et al. 1998. A novel melatonin metabolite, cyclic 3-hydroxymelatonin: A biomarker of melatonin interaction with hydroxyl radicals. Biochem. Biophys. Res. Commun. 253: 614-620.
23. POEGGELER, B., S. THEURMANN, A. ROSE, et al. 2002. Melatonin's unique radical scavenging properties - roles of its functional substituents as revealed by a comparison with its structural analogues. J. Pineal Res. 33: 20-30.
24. REITER, R.J. 1995. Oxidative processes and antioxidative defense mechanisms in the aging brain. FASEB J. 9: 526-533.
25. REITER, R.J. 1998. Oxidative damage in the central nervous system: protection by melatonin. Prog. Neurobiol. 56: 359-384.
26. CUZZOCREA, S. & R.J. REITER. 2001. Pharmacological action of melatonin in shock, inflammation and ischemia/reperfusion injury. Eur. J. Pharmacol. 426: 1-10.
27. JAHNKE, G., M. MARR, C. MUERS, et al. 1999. Maternal and developmental toxicity evaluation of melatonin administered orally to pregnant Sprague-Dawley rats. Toxicol. Res. 50: 271-274.
28. JAN, J.E., D. HAMILTON, N. SEWARD, et al. 2000. Clinical trails of controlled-release melatonin in children with sleep-wake cycle disorders. J. Pineal Res. 29: 34-39.
29. SEABRA, M.L.V., M. BIGNOTTO, L.R. PINTO, JR. & S. TUFIK. 2000. Randomized, double blind clinical trial, controlled with placebo, of the toxicology of chronic melatonin treatment. J. Pineal Res. 29: 193-200.
30. GITTO, E., M. KARBOWNIK, R.J. REITER, et al. 2001. Effects of melatonin treatment in septic newborns. Pediat. Res. 50: 756-760.
31. FULIA, F., E. GITTO, S. CUZZOCREA, et al. 2001. Increased levels of malondialdehyde and nitrite/nitrate in the blood of asphyxiated newborns: reduction by melatonin. J. Pineal Res. 31: 343-349.
32. FLAMM, E.S., H.B. DEMOPAULOS, M.L. SELIGMAN, et al. 1978. Free radicals in cerebral ischemia. Stroke 9: 445-447.
33. DEMOPOULUS, H.B., E.S. FLAMM, M.L. SELIGMAN, et al. 1979. Membrane perturbations in CNS injury: theoretical basis for free radical damage and a review of the experimental data. In Neural Trauma. A.J. Popp, R.S. Bourke, L.R. Nelson & H.K. Kimelberg, Eds.: 63-78. Raven, New York.
34. OLIVER, C.N., R.E. STARK-REED, E.R. STADTMAN, et al. 1990. Oxidative damage to brain proteins, loss of glutamine synthetase activity, and production of free radicals during ischemia/reperfusion-induced injury to gerbil brain. Proc. Natl. Acad. Sci. USA 87: 5144-5147.
35. FLOYD, R.A. & J.M. CARNEY. 1992. Free radical damage to proteins and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann. Neurol. 32: S22-S27.
36. DEL ZOPPO, G.J. 1997. Reperfusion damage: the role of PMN leucocytes. In Primer in Cerebrovascular Diseases. K.M.A. Welch, L.R. Caplan, D.J. Reis, et al., Eds.: 217-220. Academic Press, San Diego.
37. BECKMAN, J.S. 1991. The double-edged role of nitric oxide in brain function and superoxide-mediated injury. J. Dev. Physiol. 15: 53-59.
38. DALKARA, T. & M.A. MOSKOWITZ. 1994. Complex role of nitric oxide in cerebral ischemia. Brain Pathol. 4: 49-57.
39. DAWSON, T.M. & V.L. DAWSON. 1994. Nitric oxide: actions and pathological roles. Neuroscientist 1: 9-20.
40. KAYAMA, T., M. NAKAJIMA, K. OIKAWA & M. HIRAMATSU. 1996. Free radical imaging during ischemia in rat brain. In Free Radicals in Brain Physiology and Disorders. L. Packer, M. Hiramatsu & T. Yoshirkawa, Eds.: 279-285. Academic Press, San Diego.
41. HALL, N.C., J.M. CARNEY, M.S. CHENG & D.A. BUTTERFIELD. 1995. Prevention of ischemia/reperfusion-induced alterations in synaptosomal membrane-associated proteins and lipids by N-tert-butyl-α-phenylnitrone and difluoromethylornithine. Neuroscience 69: 591-600.
42. WOLF, P.A. 1997. Epidemiology and risk factors management. In Primer in Cerebrovascular Diseases. K.M.A. Welch, L.R. Caplan, D.J. Reis, et al., Eds.: 751-757. Academic Press, San Diego.
43. YASUI, Y., K. MAUATARI, Y. HIGUCHI, et al. 1996. Oxygen radicals in glutamate toxicity of C6 glioma cells via transporter system. In Free Radicals in Brain Physiology and Disorders, L. Packer, M. Hiramatsu & T. Yoshikawa, Eds.: 51-67. Academic Press, San Diego.
44. PABLOS, M.I., R.J. REITER, J.I. CHUANG, et al. 1997. Acutely administered melatonin reduces oxidative damage in lung and brain induced by hyperbaric oxygen. J. Appl. Physiol. 83: 354-358.
45. TAN, D.X., L.C. MANCHESTER, R.J. REITER, et al. 2000. Significance of melatonin in antioxidative defense system. Biol. Signals Recept. 9: 137-159.
46. REITER, R.J., D.X. TAN, L.C. MANCHESTER & W. QI. 2001. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem. Biophys. 34: 237-256.
47. REITER, R.J., D.X. TAN, L.C. MANCHESTER & J.R. CALVO. 2002. Antioxidative capacity of melatonin. In Handbook of Antioxidants, second edit. E. Cadenas & L. Packer, Eds.: 565-613. Dekker, New York.
48. SENER, G., A.O. SEHIRLI, H.Z. ALTUNBAS, et al. 2002. Melatonin protects against gentamicin-induced nephrotoxicity in rats. J. Pineal Res. 32: 231-236.
49. PAPPOLLA, M.A., Y.J. CHYAN, B. POEGGELER, et al. 2000. An assessment of the antioxidant and antiamyloidogenic properties of melatonin: implications for Alzheimer's disease. J. Neural Transm. 107: 203-231.
50. HSU, C.H., B.C. CHI & J.E. CASIDA. 2002. Melatonin reduces phosphine-induced lipid and DNA oxidation in vitro and in vivo in rat brain. J. Pineal Res. 32: 53-62.
51. +-induced neurodegeneration and glutathione impairment in the nigrostriatal dopaminergic pathway. J. Pineal Res. 32: 262-269.
52. TAN, D.X., L.D. CHEN, B. POEGGELER, et al. 1993. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocrine J. 1: 57-60.
53. HARDELAND, R., R.J. REITER, B. POEGGELER & D.X. TAN. 1993. The significance of the metabolism of the neurohormone melatonin: antioxidative protection and formation of bioactive substances. Neurosci. Biobehav. Dev. 17: 347-357.
54. MANEV, H., T. UZ, A. KHARLAMOV & J.Y. JOO. 1996. Increased brain damage after stroke or excitotoxic seizures in melatonin-deficient rats. FASEB J. 10: 1546-1551.
55. JOO, J.Y., T. UZ & H. MANEV. 1998. Opposite effects of pinealectomy and melatonin administration on brain damage following cerebral focal ischemia in rat. Rest. Neurol. Neurosci. 13: 185-191.
56. KILIC, E., Y.G. ÖZDEMIR, H. BOLAY, et al. 1999. Pinealectomy aggravates and melatonin administration attenuates brain damage in focal ischemia. J. Cerebr. Blood Flow Metab. 19: 511-516.
57. REITER, R.J. 1992. The aging pineal gland and its physiological consequences. BioEssays 14: 169-175.
58. MANEV, H. & T. UZ. 1998. The role of the light-dark cycle and melatonin in stroke outcome. J. Stroke Cerebrovasc. Dis. 7: 165-167.
59. CHO, S., T.H. JOH, H.H. BAIK, et al. 1997. Melatonin administration protects CA1 hippocampal neurons after transient forebrain ischemia in rats. Brain Res. 755: 335-338.
60. LI, X.J., L.M. ZHANG, J. GU, et al. 1997. Melatonin decreases production of the hydroxyl radical during cerebral ischemia-reperfusion. Acta Pharmacol. Sinica 18: 394-396.
61. SAINZ, R.M., J.C. MAYO, H. URIA, et al. 1995. The pineal neurohormone melatonin prevents in vivo and in vitro apoptosis in thymocytes. J. Pineal Res. 19: 178-188.
62. LEE, V., A.K. RANDHAWA & P.K. SINGAL. 1991. Adriamycin-induced myocardial dysfunction in vitro mediated by free radicals. Am. J. Physiol. 261: H985-H995.
63. MCLAUGHLIN, K.A., B.A. OSBOURNE & R.A. BOLDSBY. 1996. The role of oxygen in thymocytes apoptosis. Eur. J. Immunol. 26: 1170-1174.
64. SINHA, K., M.N. DEGAONKER, N.R. JAGANNATHAN & Y.K. GUPTA. 2002. Effect of melatonin on ischemia reperfusion injury induced by middle cerebral artery occlusion in rats. Eur. J. Pharmacol. 428: 185-192.
65. TATLISUMAK, T., R.A.D. CARANO, K. TAKANO, et al. 1998. A novel endothelium antagonist, A-1277ZZ, attenuates ischemic lesion size in rats with temporary middle cerebral artery occlusion: a diffusion and perfusion study. Stroke 29: 850-857.
66. PEI, Z., H.T. HO & R.T. CHEUNG. 2002. Pre-treatment with melatonin reduces volume of cerebral infarction in a permanent middle cerebral artery occlusion stroke model in the rat. Neurosci. Lett. 318: 1-4.
67. PEI, Z., S.F. PANG & R.T.F. CHEUNG. 2002. Pretreatment with melatonin reduces volume of cerebral infarction in a rat middle cerebral artery occlusion stroke model. J. Pineal Res. 32: 168-172.
68. PEI, Z., P.C.W. FUNG & R.T.F. CHEUNG. 2003. Melatonin reduces nitric oxide level during ischemia but not blood-brain-barrier breakdown during reperfusion in a rat middle cerebral artery occlusion stroke model. J. Pineal Res. 34: 110-118.
69. CSABA, S. 1996. The pathophysiological role of peroxynitrite in shock, inflammation and ischemia-reperfusion injury. Shock 6: 74-88.
70. SUN, F.Y., X. LIN, L.Z. MAO, et al. 2002. Neuroprotection by melatonin against ischemic neuronal injury associated with modulation of DNA damage and repair in the rat following a transient cerebral ischemia. J. Pineal Res. 33: 48-56.
71. WAKATSUKI, A., Y. OKATANI, C. IZUMIYA & N. IKENOUE. 1999. Melatonin protects against ischemia and reperfusion-induced oxidative lipid and DNA damage in fetal rat brain. J. Pineal Res. 26: 147-152.
72. WAKATSUKI, A., Y. OKATANI, K. SHINOHARA, et al. 2001. Melatonin protects against ischemia/reperfusion-induced oxidative damage to mitochondria in fetal rat brain. J. Pineal Res. 31: 167-172.
73. OKATANI, Y., K. OKAMOTO, K. HAYASHI, et al. 1998. Maternal-fetal transfer of melatonin in human pregnancy near term. J. Pineal Res. 25: 129-134.
74. GUERRERO, J.M., R.J. REITER, G.G. ORTIZ, et al. 1997. Melatonin prevents increases in nitric oxide and cyclic GMP production after transient brain ischemia and reperfusion in the Mongolian gerbil (Meriones unguiculatus). J. Pineal Res. 23: 24-31.
75. ORTIZ, G.G., J.M. GUERRERO, E. SEWERYNEK, et al. 1997. Melatonin is cytoprotective during neural ischemia-reperfusion injury in the Mongolian gerbil (Meriones unguiculatus). In Pineal Update. S.M. Webb, M. Puig-Domingo, M. Moller & P. Pevet, Eds.: 397-401. PJD Press, Westberg.
76. CUZZOCREA, S., G. COSTANTINO, E. GITTO, et al. 2000. Protective effects of melatonin in ischemic brain injury. J. Pineal Res. 29: 217-227.
77. LETECHIPIA-VALLEJO, G., I. GONZALEZ-BURGOS & M. CERVANTES. 2001. Neuroprotective effect of melatonin on brain damage induced by acute global ischemia in cats. Arch. Med. Res. 32: 186-192.
78. FUJIMOTO, T., T. NAKAMURA, T. IKEDA & K. TAKAGI. 2000. Potent protective effects of melatonin on experimental spinal cord injury. Spine 25: 769-775.
79. CHUANG, H.M., E.A. LING, C.F. CHEN, et al. 2002. Melatonin attenuates the neuronal NADPH-d/NOS expression in the nodose ganglion of acute hypoxic rats. J. Pineal Res. 32: 65-73.
80. KILIC, E., D.M. HERMANN, S. ISENMANN & M. BAHR. 2002. Effects of pinealectomy and melatonin on the retrograde degeneration of retinal ganglion cells in a novel model of intraorbital optic nerve transection. J. Pineal Res. 32: 106-112.
81. YILMAZ, T., S. CELEBI & A.S. KUKNER. 2002. The protective effects of melatonin, vitamin E and octreotide on retinal edema during ischemia-reperfusion in the guinea pig retina. Eur. J. Ophthalmol. 12: 443-449.
82. MONTILLA-LOPEZ, P., M.C. MUNOZ-AGUEDA, M.F. LOPEZ, et al. 2002. Comparison of melatonin versus vitamin C on oxidative stress and antioxidant enzyme activity in Alzheimer's disease induced by okadaic acid in neuroblastoma cells. Eur. J. Pharmacol. 451: 237-243.
83. ACUÑA-CASTROVIEJO, D., M. MARTIN, M. MACIAS, et al. 2001. Melatonin, mitochondria and cellular bioenergetics. J. Pineal Res. 30: 65-74.
84. ANTOLIN, I., C. RODRIQUEZ, R.M. SAINZ, et al. 1996. Neurohormone melatonin prevents cell damage: effect on gene expression for antioxidative enzymes. FASEB J. 10: 882-890.
85. ALBARRAN, M.T., S. LOPEZ-BURILLO, M.I. PABLOS, et al. 2001. Endogenous rhythms of melatonin, total antioxidant status and superoxide dismutase activity in several tissues of chick and their inhibition by light. J. Pineal Res. 30: 227-233.
86. EL-ABHAR, H.S., M. SHAALAN, M. BARAKAT & E.S. EL-DENSHARY. 2002. Effect of melatonin and nifedipine on some antioxidative enzymes and different energy fuels in the blood and brain of global ischemic rats. J. Pineal Res. 33: 87-94.
87. BORLONGAN, C.V., M. YAMAMOTO, N. TAKEI, et al. 2000. Glial cell survival is enhanced during melatonin-induced neuroprotection against cerebral ischemia. FASEB J. 14: 1307-1317.
88. CHUNG, S.Y. & S.H. HAN. 2003. Melatonin attenuated kainic acid-induced hippocampal neurodegeneration and oxidative stress through microglial inhibition. J. Pineal Res. 34: 95-104.
89. PAPPOLLA, M.A., M.J. SIMOVICH, T. BRYANT-THOMAS, et al. 2002. The neuroprotective activities of melatonin against Alzheimer β-protein are not mediated by membrane melatonin receptors. J. Pineal Res. 32: 135-142.