AM-36, a novel neuroprotective agent, profoundly reduces reactive oxygen species formation and dopamine release in the striatum of conscious rats after endothelin-1-induced middle cerebral artery occlusion

Neuropharmacology

Volumn 44, Issue 6, 2003, Pages 787-800

  Callaway, J K ^a   Lawrence, A J ^a   Jarrott, B ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Focal ischemia; Microdialysis; Neuroprotection; Reactive oxygen species; Salicylate hydroxylation

Indexed keywords

1 [2 (4 CHLOROPHENYL) 2 HYDROXY]ETHYL 4 [3,5 BIS(1,1 DIMETHYL) 4 HYDROXYPHENYL]METHYLPIPERAZINE; 2,3 DIHYDROXYBENZOIC ACID; AM 36; DOPAMINE; ENDOTHELIN 1; PIPERAZINE DERIVATIVE; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BEHAVIOR; BRAIN ISCHEMIA; CONTROLLED STUDY; CORPUS STRIATUM; DIALYSATE; DOPAMINE RELEASE; DRUG POTENCY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROXYLATION; IN VIVO STUDY; MALE; MICRODIALYSIS; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0037401507     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(03)00068-6     Document Type: Article

References (78)

1. Allen D.R., Wallis G.L., McCay P.B. Catechol adrenergic agents enhance hydroxyl radical generation in xanthine oxidase systems containing ferritin: implications for ischemia/reperfusion. Archives of Biochemistry and Biophysics. 315:1994;235-243.
2. Beckman J.S., Beckman T.W., Chen J., Marshall P.A. Apparent hydroxyl radical production by peroxinitrite: implications for endothelial injury from nitric oxide and superoxide. Proceedings of the National Academy of Sciences USA. 87:1990;1620-1624.
3. Beneviste H., Drejer J., Schousboe A., Diemer N.H. Elevation of the extracellular concentration of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. Journal of Neurochemistry. 43:1984;1369-1374.
4. Bhardwaj A., Brannan T., Weinberger J. Pentobarbital inhibits extracellular release of dopamine in the ischemic striatum. Journal of Neural Transmission. General Section. 82:1990;111-117.
5. Bogaert L., Sneller D., Moonen J., Sarre S., Smolders I., Ebinger G., et al. Neurochemical changes and laser Doppler flowmetry in the endothelin-1 rat model for focal cerebral ischemia. Brain Research. 887:2000;266-275.
6. Brown C.M., Calder C., Alps B.J., Spedding M. The effect of lifarizine (RS-87476), a novel sodium and calcium channel modulator, on ischaemic dopamine depletion in the corpus striatum of the gerbil. British Journal of Pharmacology. 109:1993;175-177.
7. Buisson A., Callebert J., Mathieu E., Plotkine M., Boulu R.G. Stiratal protection induced by lesioning of the substantia nigra of rats subjected to focal ischemia. Journal of Neurochemistry. 59:1992;1153-1157.
8. Callaway J.K. Investigation of AM-36: a novel neuroprotective agent. Clinical and Experimental Pharmacology and Physiology. 28:2001;913-918.
9. Callaway J.K., Jarrott B. AM-36 inhibits ischemia-induced free radical generation in the striatum of conscious rats. Proceedings of the Australian Neuroscience Society. 12:2001a;124.
10. Callaway J.K., Jarrott B. AM-36, a novel neuroprotective drug, inhibits both ischemia-induced increases in reactive oxygen species and dopamine release in the striatum of conscious rats. Society for Neuroscience. 27:2001b;762-768. (Abstract).
11. Callaway J.K., Knight M.J., Watkins D.J., Beart P.M., Jarrott B. Delayed treatment with AM-36, a novel neuroprotective agent, reduces neuronal damage after endothelin-1-induced middle cerebral artery occlusion in conscious rats. Stroke. 30:1999;2704-2712.
12. Callaway J.K., Knight M.J., Watkins D.J., Beart P.M., Jarrott B., Delaney P.M. A novel, rapid, computerised method for quantitation of neuronal damage in a rat model of stroke. Journal of Neuroscience Methods. 102:2000;53-60.
13. Callaway J.K., Beart P.M., Jarrott B., Giardina S.F. Incorporation of sodium channel blocking and free radical scavenging activities into a single drug, AM-36, results in profound inhibition of neuronal apoptosis. British Journal of Pharmacology. 132:2001;1691-1698.
14. Chabrier P.-E., Auguet M., Spinnerwyn B., Auvin S., Cornet S., Demerle-Pallardy C., Guilmard-Favre C., Marin J.G., Pignol B., Gillard-Roubert V., Roussillot-Charnet C., Schulz J., Voissat I., Bigg D., Moncada S. BN 80933, a dual inhibitor of neuronal nitric oxide synthase and lipid peroxidation: a promising neuroprotective stratery. Proceedings of the National Academy of Sciences USA. 96:1999;10824-10829.
15. Chan P.H. Reactive oxygen radicals in signalling and damage in the ischemic brain. Journal of Cerebral Blood Flow and Metabolism. 21:2001;2-14.
16. Chiueh C.C., Lrishna G., Tulsi P., Obata T., Lang K., Huang S.-J., et al. Intracranial microdialysis of salicylic acid to detect hydroxyl radical generation through dopamine autooxidation in the caudate nucleus: effect of MPP+. Free Radicals in Biology and Medicine. 13:1992;581-583.
17. Chiueh C.C., Miyake H., Peng M.-T. Role of dopamine autoxidation, hydroxyl radical generation, and calcium overload in underlying mechanisms involved in MPTP-induced Parkinsonism. Narabayashi H., Nagatsu T., Yanagisawa N., Mizuno Y. Advances in neurology. 1993;251-258 Raven Press, New York.
18. Clemens J.A., Phebus L.A. Dopamine depletion protects striatal neurons from ischemia-induced cell death. Life Sciences. 42:1988;707-713.
19. De Ryck M., Van Reempts J., Borgers M., Wauquier A., Janssen P.A.J. Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke. 20:1989;1383-1390.
20. Ding-Zhou L., Marchand-Verrecchia C., Croci N., Plotkine M., Margaill I. L-NAME reduces infarction, neurological deficit and blood brain barrier disruption following cerebral ischemia in mice. European Journal of Pharmacology. 457:2002;137-146.
21. Fisher M., Garcia J.H. Evolving stroke and the ischemic penumbra. Neurology. 47:1996;884-888.
22. Floyd R.A., Watson J.J., Wong P.K. Sensitive assay of hydroxyl free radical formation utilizing high pressure liquid chromatography with electrochemical detection of phenol and salicylate hydroxylation products. Journal of Biochemical and Biophysical Methods. 10:1984;221-235.
23. Garcia J.H. Experimental ischemic stroke: a review. Stroke. 15:1984;5-14.
24. Gido G., Cronberg T., Wieloch T. The effects of alpha-phenyl-tert-butyl nitrone (PBN) on free radical formation in transient focal ischemia measured by microdialysis and 3,4-dihydroxybenzoate formation. Acta Physiologica Scandinavica. 168:2000;277-285.
25. Globus M.Y.-T., Ginsberg M.D., Harik S.I., Busto R., Deitrich W.D. Role of dopamine in ischemia striatal injury: metabolic evidence. Neurology. 37:1987;1712-1719.
26. Globus M.Y.-T., Busto R., Lin B., Schnippering H., Ginsberg M.D. Detection of free radical activity during transient global ischemia and recirculation: effects of instrastriatal brain temperature modulation. Journal of Neurochemistry. 65:1995;1250-1256.
27. Hall E.D., Andrus P.K., Oostveen J.A., Althaus J.S., VonVoigtlander P.F. Neuroprotective effects of the dopamine D2/D3 agonist pramipexole against postischemic or methamphetamine-induced degeneration of nigrostriatal neurons. Brain Research. 742:1996;80-88.
28. Halliwell B., Kaur H., Ingelman-Sundberg M. Hydroxylation of salicylate as an assay for hydroxyl radicals: a cautionary note. Free Radicals in Biology and Medicine. 10:1991;439-441. (Letter to the Editor).
29. Hillered L., Hallstrom A., Segersvard S., Persson L., Ungerstedt U. Dynamics of extracellular metabolites in the striatum after middle cerebral artery occlusion in the rat monitored by intracerebral microdialysis. Journal of Cerebral Blood Flow and Metabolism. 9:1989;607.
30. Imai H., Masayasu H., Dewar D., Graham D.I., Macrae I.M. Ebselen protects both gray and white matter in a rodent model of focal cerebral ischemia. Stroke. 32:2001;2149-2154.
31. Jarrott, B., Beart, P.M., Jackson, W.R., Kenche, V.B., Robertson, A., Collis, M.P., 1997. Arylalkylpiperazine compounds as antioxidants. Patent Cooperation Treaty International Publication No. WO97/43259, Monash University.
32. Jarrott B., Callaway J.K., Jackson W.R., Beart P.M. Development of a novel arylalkylpiperazine compound (AM-36) as a hybrid neuroprotective drug. Drug Development Research. 46:1999;261-267.
33. Jianjun Z., Xinyi N. Changes of monoamines, purines and amino acids in rat striatum as measured by intracerebral microdialysis during ischemia/reperfusion. Chinese Medical Sciences Journal. 9:1994;225-229.
34. Kuroda S., Siesjo B.K. Reperfusion damage following focal ischemia:pathophysiology and therapeutic windows. Clinical Neuroscience. 4:1997;199-212.
35. Lamensdorf I., Hrycyna C., He L.-P., Nedhushtan A., Tjurmina O., Harvey-White J., Gisenhofer G., Rojas E., Kopin I.J. Acidic dopamine metabolites are actively extruded from PC12 cells by a novel sulfonylurea-sensitive transporter. Naunyn-Schmiedeberg's Archives of Pharmacology. 361:2000;654-664.
36. Lancelot E., Callebert J., Revaud M., Boulu R.G., Plotkine M. Detection of hydroxyl radicals in rat striatum during transient focal cerebral ischemia: possible implication in tissue damage. Neuroscience Letters. 197:1995;85-88.
37. Laschinski G., Kittner B., Brautigam M. Direct inhibition of tyrosine hydroxylase from PC-12 cells by catechol derivatives. Naunyn-Schmiedeberg's Archives of Pharmacology. 332:1986;346-350.
38. Lawrence A.J., Marsden C.A. Terminal autoreceptor control of 5-hydroxytryptamine release as measured by in vivo microdialysis in the conscious guinea pig. Journal of Neurochemistry. 58:1992;142-146.
39. Leach M.J., Swan J.H., Eisenthal D., Dopson M., Nobbs M. BW619C89, a glutamate release inhibitor, protects against focal cerebral ischemic damage. Stroke. 24:1993;1063-1067.
40. 2 production in the rat striatum following transient middle cerebral artery occlusion. Brain Research. 764:1997;299-302.
41. Li Y.-J., Zhang L.M., Gu J., Zhang A.Z., Sun F.Y. Melatonin decreases production of hydroxyl radical during cerebral ischemia-reperfusion. Zhongguo Yao Li Xue Bao. 18:1997;394-396.
42. Liu J., Mori A. Monoamine metabolism provides an antioxidant defense in the brain against oxidant- and fre radical-induced damage. Archives of Biochemistry and Biophysics. 302:1993;118-127.
43. + channel modulator and glutamate release inhibitor in cultured rat cerebellar neurons and in gerbil global brain ischemia. Stroke. 25:1994;2476-2482.
44. Macrae I.M. New models of focal cerebral ischemia. British Journal of Clinical Pharmacology. 34:1992;302-308.
45. Matsumiya N., Koehler R.C., Kirsch J.R., Traystman R.J. Conjugated superoxide dismutase reduces extent of caudate injury after transient focal ischemia in cats. Stroke. 22:1991;1193-1200.
46. Matsuo Y., Kihara T., Ikeda M., Nonomiya M., Onodera H., Kogure K. Role of neutrophils in radical production during ischemia and reperfusion of the rat brain: effect of neutrophil depletion on extracellular ascorbyl radical formation. Journal of Cerebral Blood Flow and Metabolism. 15:1995;941-947.
47. Mattson M.P., Culmsee C., Yu Z.F. Apoptotic and antiapoptotic mechanisms in stroke. Cell Tissue Research. 301:2000;173-187.
48. Morimoto T., Globus M.Y.-T., Busto R., Martinez E., Ginsberg M.D. Simultaneous measurement of salicylate hydroxylation and glutamate release in the penumbral cortex following transient middle cerebral artery occlusion. Journal of Cerebral Blood Flow and Metabolism. 16:1996;92-99.
49. Nappi A.J., Vass E., Prota G., Memoli S. The effects of hydroxyl radical attack on dopa, dopamine, 6-hydroxydopa, and 6-hydroxydopamine. Pigment Cell Research. 8:1995;283-293.
50. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1986;Academic Press, New York.
51. Phebus L.A., Clemens J.A. Effects of transient, global, cerebral ischemia on striatal extracellular dopamine, serotonin and their metabolites. Life Sciences. 44:1989;1335-1342.
52. Phebus L.A., Mincy R.E., Clemens J.A. Iscemia increases tissue and decreases extracellular levels of acid dopamine metabolites in the rat striatum: further evidence for active transport of metabolites. Life Sciences. 56:1995;1135-1141.
53. Piantadosi C.A., Zhang J. Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke. 27:1996;327-331.
54. Schallert T., Whishaw I.Q. Bilateral cutaneous stimulation of the somatosensory system in hemi-decorticate rats. Behavioural Neuroscience. 98:1984;518-540.
55. Sharkey J., Ritchie I.M., Kelly P.A.T. Perivascular microapplication of endothelin-1: a new model of focal cerebral ischaemia in the rat. Journal of Cerebral Blood Flow and Metabolism. 13:1993;865-871.
56. Shiekhatter R., Ghasemzadeh M.B., Adams R.N. Intracerebral infusion of DOPAC decreases striatal dopamine. Brain Research Bulletin. 29:1992;891-896.
57. Simonson S.G., Zhang J., Canada A.T., Su Y.-F., Beneviste H., Piantodosi C.A. Hydrogen peroxide production by monoamine oxidase during ischemia-reperfusion in the rat brain. Journal of Cerebral Blood Flow and Metabolism. 13:1993;125-134.
58. Solenski N.J., Kwan A.-L. Attenuation of free radical generation during reversible focal cerebral ischemia with the nitric oxide inhibitor, L-NAME (L-NG-nitro-L-arginine methyl ester). Brain Research. 862:2000;262-265.
59. Solenski N.J., Kwan A.-L., Yamamoto H., Bennett J.P., Kassell N.F., Lee K.S. Differential hydroxylation of salicylate in the core and penumbra regions during focal reversible cerebral ischemia. Stroke. 28:1997;2545-2551.
60. Ste-Marie L., Vachon P., Vachon L., Bemeur C., Guetin M.-C., Montgomery J. Hydroxyl radical production in the cortex and striatum in a rat model of focal cerebral ischemia. Canadian Journal of Neurological Science. 27:2000;152-159.
61. Stokes A.H., Hastings T., Vrana K.E. Cytotoxic and genotoxic potential of dopamine. Journal of Neuroscience Research. 55:1999;659-665.
62. Sun G.Y., Zhang J.-P., Lin T.A., Lin T.-N., He Y.Y., Hsu C.Y. Inositol triphosphate, polyphosphoinositide turnover, and high-energy metabolites in focal cerebral ischemia and reperfusion. Stroke. 26:1995;1893-1900.
63. Taylor C.P., Meldrum B.S. Sodium channels as targets for neuroprotective drugs. Trends in Pharmacological Sciences. 16:1995;309-316.
64. Taylor C.P., Burke S.P., Weber M.L. Hippocampal slices: glutamate overflow and cellular damage from ischemia are reduced by sodium channel blockade. Journal of Neuroscience Methods. 59:1995;121-128.
65. Toner C.C., Stamford J.A. Sodium channel blockade unmasks two temporally distinct mechanisms of striatal dopamine release during hypoxia/hypoglycaemia in vitro. Neuroscience. 81:1997;999-1007.
66. Tyson G.W., Teasdale G.M., Graham D.I., McCulloch J. Focal cerebral ischemia in the rat: topography of hemodynamic and histopathological changes. Annals of Neurology. 15:1984;559-567.
67. + channels: a rational and effective strategy against ischaemic brain damage. Pharmacological Reviews. 48:1996;21-67.
68. Wahl F., Allix M., Plotkine M., Boulu R.G. Neurological and behavioural outcomes of cerebral ischemia in rats. Stroke. 23:1992;267-272.
69. Warner D.S., McFarlane C., Todd M.M., Ludwig P., McAllister A.M. Sevoflurane and halothane reduce focal ischemic brain damage in the rat. Possible influence on thermoregulation. Anaesthesiology. 79:1993;985-992.
70. Weston R.M., Jarrott B., Callaway J.K. Neutrophil infiltration is reduced by AM-36 in a middle cerebral artery model of stroke in conscious rats. Proceedings of the Australian Neuroscience Society. 13:2002;149.
71. Yamaguchi T., Suzuki M., Yamamoto M. YM796, a novel muscarinic agonist, improves the impairment of learning behaviour in a rat model of chronic focal cerebral ischemia. Brain Research. 669:1995;107-114.
72. Yamamoto M., Tamura A., Kirino T., Shimizu M., Sano K. Behavioural changes after focal cerebral ischemia by left middle cerebral artery occlusion in rats. Brain Research. 452:1988;323-328.
73. Yamamoto T., Yuki S., Watanabe T., Mitsuka M., Saito K.-I., Kogure K. Delayed neuronal death prevented by inhibition of increased hydroxyl radical formation in a transient cerebral ischemia. Brain Research. 762:1997;240-242.
74. Yang C.S., Lin N.N., Tsai P.J., Liu L., Kuo J.S. In vivo evidence of hydroxyl radical formation induced by elevation of extracellular glutamate after cerebral ischemia in the cortex of anaesthetised rats. Free Radicals in Biology and Medicine. 20:1996;245-250.
75. Yu Z.F., Bruce-Keller A.J., Goodman Y., Mattson M.P. Uric acid protects neurons against excitiotoxic and metabolic insults in cell culture, and against focal ischemic brain injury in vivo. Journal of Neuroscience Research. 53:1998;613-625.
76. Zhang J., Beneviste H., Klitzman B., Piantadosi C.A. Nitric oxide synthase inhibition and extracellular glutamate concentration after cerebral ischemia/reperfusion. Stroke. 26:1995;298-304.
77. Zhao Q., Pahlmark K., Smith M.-L., Siesjo B.K. Delayed treatment with the spin trap a-phenyl-N-tert-butyl nitrone (PBN) reduces infarct size following transient middle cerebral artery occlusion in rats. Acta Physiologica Scandinavia. 152:1994;349-350.
78. Zini I., Tomasi A., Grimaldi R., Vannini V., Agnati L.F. Detection of free radicals during brain ischemia and reperfusion by spin trapping and microdialysis. Neuroscience Letters. 138:1992;279-282.