Different strains of rats show different sensitivity to block of long-term potentiation by nitric oxide synthase inhibitors

European Journal of Pharmacology

Volumn 457, Issue 2-3, 2002, Pages 99-106

  Hölscher, Christian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

(Rat); CA1 area; Hippocampus; Learning; Long term potentiation; Nitric oxide (NO)

Indexed keywords

1 (2 TRIFLUOROMETHYLPHENYL)IMIDAZOLE; 7 NITROINDAZOLE; NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG; 1-(2-TRIFLUOROMETHYLPHENYL)IMIDAZOLE; 7-NITROINDAZOLE; ENZYME INHIBITOR; IMIDAZOLE DERIVATIVE; INDAZOLE DERIVATIVE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; STRAIN DIFFERENCE; ANIMAL; BRAIN; DRUG ANTAGONISM; ELECTROSTIMULATION; ENZYMOLOGY; LONG EVANS RAT; PHYSIOLOGY; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT; WISTAR RAT;

ANIMALS; BRAIN; ELECTRIC STIMULATION; ENZYME INHIBITORS; IMIDAZOLES; INDAZOLES; LONG-TERM POTENTIATION; MALE; NITRIC OXIDE SYNTHASE; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; SPECIES SPECIFICITY;

EID: 0037147087     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-2999(02)02641-9     Document Type: Article

References (63)

1. Akira T., Henry D., Wasterlain C.G. Nitric oxide mediates the sustained opening of NMDA receptor-gated ionic channels which follows transient excitotoxic exposure in hippocampal slices. Brain Res. 652:1994;190-194.
2. Arnold J.C., Topple A.N., Mallet P.E., Hunt G.E., McGregor I.S. The distribution of cannabinoid-induced Fos expression in rat brain: differences between the Lewis and Wistar strain. Brain Res. 921:2001;240-255.
3. Babbedge R.C., Blandward P.A., Hart S.L., Moore P.K. Inhibition of rat acerebellar nitric-oxide synthase by 7-nitro-indazole and related substituted indazoles. Br. J. Pharmacol. 110:1993;225-228.
4. Bannerman D.M., Butcher S.P., Morris R.G.M. Intracerebroventricular injection of a nitric oxide synthase inhibitor does not affect long-term slope potentiation in vivo. Neuropharmacology. 33:1994;1387-1397.
5. Bannerman D.M., Chapman P.F., Kelly P.A.T., Butcher S.P., Morris R.G.M. Inhibition of nitric-oxide synthase does not impair spatial learning. J. Neurosci. 14:1994;7404-7414.
6. Bernabeu R., Destein M.L., Fin C., Izquierdo I., Medina J.H. Role of hippocampal NO in the acquisition and consolidation of inhibitory avoidance-learning. NeuroReport. 6:1995;1498-1500.
7. Bert B., Fink H., Sohr R., Rex A. Different effects of diazepam in Fischer rats and two stocks of Wistar rats in tests of anxiety. Pharmacol. Biochem. Behav. 70:2001;411-420.
8. Böhme G.A., Bon C., Stutzmann J.-M., Doble A., Blanchard J.-C. Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmacol. 199:1991;379-381.
9. Böhme G.A., Bon C., Lemaire M., Reibaud M., Piot O., Stutzmann J.-M., Doble A., Blanchard J.-C. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. Proc. Natl. Acad. Sci. U. S. A. 90:1993;9191-9194.
10. Bon C., Böhme G.A., Doble A., Stutzmann J.-M., Blanchard J.-C. A role for nitric oxide in long-term potentiation. Eur. J. Neurosci. 4:1992;420-424.
11. Boulton C.L., Garthwaite J. The Role of Nitric Oxide in Hippocampal Synaptic Plasticity. 1995;British Research Association, Oxford. Abstr. 17.2.
12. Bredt D.S., Snyder S.H. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. U. S. A. 87:1990;682-685.
13. Bredt D.S., Snyder S.H. Nitric oxide, a novel neuronal messenger. Neuron. 8:1992;3-11.
14. Chapman, P.F., Atkins, C.M., M.T., A., Haley, J.E., Steinmetz, J.E., 1992. Inhibition of nitric oxide synthesis impairs two different forms of learning. NeuroReport 3, 567-570.
15. Chapman P.F., Bannerman D.M., Kelly P.A.T., Morris R.G.M. Inhibition of Nitric Oxide Synthesis Raises the Threshold for the Induction of Long-Term Potentiation In Vivo. 1993;Brain Research Association, University of St. Andrews. Abstract 35.13.
16. Chetkovich D.M., Klann E., Sweatt J.D. Nitric Oxide Synthase Independent Long-Term Potentiation in Area CA1 of Hippocampus. NeuroReport. 4:1993;919-922.
17. Corbett J.A., Tilton R.G., Chang K., Hasan K.S., Ido Y., Wang J.L., Sweetland M.A., Lancaster J.R., Williamson J.R., McDaniel M.L. Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes. 41:1992;552-556.
18. Cummings J.A., Nicola S.M., Malenka R.C. Induction in the rat hippocampus of long-term potentiation (LTP) and long-term depression (LTD) in the presence of a nitric oxide synthase inhibitor. Neurosci. Lett. 176:1994;110-114.
19. Dinerman J.L., Dawson T.M., Schell M.J., Snowman A. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. U. S. A. 91:1994;2414-2418.
20. Doyle C.A., Slater P. Localization of neuronal and endothelial nitric oxide synthase isoforms in human hippocampus. Neuroscience. 76:1997;387-395.
21. Doyle C., Hölscher C., Rowan M.J., Anwyl R. The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J. Neurosci. 16:1996;418-426.
22. Farook J.M., Zhu Y.Z., Wang H., Moochhala S., Lee L., Wong P.T. Strain differences in freezing behavior of PVG hooded and Sprague-Dawley rats: differential cortical expression of cholecystokinin2 receptors. NeuroReport. 12:2001;2717-2720.
23. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:1991;60-67.
24. Gribkoff V.K., Lum-Ragan J.T. Evidence for nitric oxide synthase inhibitor sensitive and insensitive hippocampal synaptic potentiation. J. Neurophysiol. 68:1992;639-642.
25. Haley J.E., Madison D.V. Differential Effects of Nitric Oxide Synthase Inhibitors on LTP at Basal and Apical Synapses of Hippocampal CA1 Neurons. 1995;Soc. Neurosci, Miami, USA. Abstract 1809.
26. Haley J.E., Malen P.L., Chapman P.F. Nitric oxide synthase inhibitors block long-term potentiation induced by weak but not strong tetanic stimulation at physiological brain temperatures in rat hippocampal slices. Neurosci. Lett. 160:1993;85-88.
27. Handy R.L.C., Moore P.K. Mechanism of the inhibition of neuronal nitric oxide synthase by 1-(2-trifluoromethylphenyl) imidazole (TRIM). Life Sci. 60:1997;PL389-PL394.
28. Handy R.L.C., Wallace P., Gaffen Z.A., Whitehead K.J., Moore P.K. The antinociceptive effect of 1-(2-trifluoromethylphenyl) imidazole (TRIM), a potent inhibitor of neuronal nitric oxide synthase in vitro, in the mouse. Br. J. Pharmacol. 116:1995;2349-2350.
29. Hara H., Waeber C., Huang P.L., Fujii M., Fishman M.C., Moskowitz M.A. Brain distribution of nitric oxide synthase in neuronal or endothelial nitric oxide synthase mutant mice using [3H]L-NG-nitro-arginine autoradiography. Neuroscience. 75:1996;881-890.
30. Harbrecht B.G., Stadler J., Demetris A.J., Simmons R.L., Billiar T.R. Nitric oxide and prostaglandins interact to prevent hepatic damage during murine endotoxemia. Am. J. Physiol.: Gastrointest. Liver Physiol. 266:1994;G1004-G1010.
31. Hölscher C. 7-Nitro indazole, a neuron specific nitric oxide synthase inhibitor, produces amnesia in the chick. Learn. Memory. 1:1994;9-11.
32. Hölscher C. Inhibitors of cyclooxygenases but not lipoxygenases have amnestic effects in the chick. Eur. J. Neurosci. 7:1995;1360-1365.
33. Hölscher C. Release of prostaglandins during memory consolidation in the chick. Eur. J. Pharmacol. 294:1995;253-259.
34. Hölscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 20:1997;298-303.
35. Hölscher C. Additional information to Nitric oxide is required for expression of LTP that is induced by stimulation phase-locked with theta rhythm. Eur. J. Neurosci. 11:1999;2596-2597.
36. Hölscher C. Nitric oxide is required for expression of LTP that is induced by stimulation phase-locked with theta rhythm. Eur. J. Neurosci. 11:1999;335-343.
37. Hölscher C., Rose S.P.R. An inhibitor of nitric oxide synthesis prevents memory formation in the chick. Neurosci. Lett. 145:1992;165-167.
38. 2 and NO synthase cooperate in producing amnesia of a spatial task. NeuroReport. 6:1995;730-734.
39. Hölscher C., McGlinchey L., Anwyl R., Rowan M. 7-Nitro indazole, a selective neuronal nitric oxide synthase inhibitor, impairs spatial learning in the rat. Learn. Memory. 2:1996;267-278.
40. Hölscher C., Anwyl R., Rowan M. Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation which can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J. Neurosci. 17:1997;6470-6477.
41. Hölscher C., Gigg J., O'Mara S. Metabotropic glutamate receptor activation and blockade. Consequences for long-term potentiation, learning and neurotoxicity. Neurosci. Biobehav. Rev. 23:1999;399-410.
42. Hu J.R., El-Fakahany E.E. Intricate regulation of nitric oxide synthesis in neurons. Cell. Signal. 8:1996;185-189.
43. w-nitro-L-arginine methyl ester on in vivo long-term potentiation in the rat dentate gyrus. Eur. J. Pharmacol. 238:1993;395-398.
44. Jaffrey S.R., Snyder S.H. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science. 274:1996;774-777.
45. Johannesen J., Pociot F., Karlsen A.E., Mandrup P.T., Nerup J. Strain-dependent difference in inducible nitric oxide synthesis (iNOS) expression in rat pancreatic islets correlates with interferon regulating factor 1 (IRF-1) and heat shock protein 70 (HSP70) expression. Eur. Cytokine Netw. 12:2001;501-509.
46. Kantor D.B., Lanzrein M., Stary S.J., Sandoval G.M., Smith W.B., Sullivan B.M., Davidson N., Schuman E.M. A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science. 274:1996;1744-1748.
47. Kato H., Kogure K., Liu Y., Araki T., Itoyama Y. Induction of NADPH-diaphorase activity in the hippocampus in a rat model of cerebral ischemia and ischemic tolerance. Brain Res. 652:1994;71-75.
48. Lam H.H.D., Hanley D.F., Trapp B.D., Saito S., Raja S., Dawson T.M., Yamaguchi H. Induction of spinal cord neuronal nitric oxide synthase (NOS) after formalin injection in the rat hind paw. Neurosci. Lett. 210:1996;201-204.
49. Lum-Ragan J.T., Gribkoff V.K. The sensitivity of hippocampal long-term potentiation to nitric oxide synthase is dependent upon the pattern of conditioning stimulation. Neuroscience. 57:1993;900-987.
50. Manahan-Vaughan D. Group III metabotropic glutamate receptors modulate long-term depression in the hippocampal CA1 region of two rat strains in vivo. Neuropharmacology. 39:2000;1952-1958.
51. McMillan D.E., Li M. LAD rats learn a three-key drug discrimination more rapidly and achieve a higher level of performance than HAD rats. Behav. Pharmacol. 12:2001;545-548.
52. Minc-Golomb D., Schwartz J.P. Expression of constitutive nitric oxide synthase in a primary neuronal culture. NeuroReport. 5:1994;1466-1468.
53. Minc-Golomb D., Schwartz J.P. Expression of both constitutive and inducible nitric oxide synthases in neuronal and astrocyte cultures. Ann. N.Y. Acad. Sci. 738:1995;462-468.
54. Moore P.K., Babbedge R.C., Wallace P., Garren Z.A., Hart S.L. 7-Nitro indazole, an inhibitor of nitric oxide synthase, exhibits anti-nociceptive activity in the mouse without increasing blood pressure. Br. J. Pharmacol. 108:1993;296-297.
55. Murphy K.P.S.J., Williams J.H., Bettache N., Bliss T.V.P. Photolytic release of nitric oxide modulates NMDA receptor-mediated transmission but does not induce long-term potentiation at hippocampal synapses. Neuropharmacology. 33:1994;1375-1385.
56. Musleh W.Y., Shahi K., Baudry M. Further studies concerning the role of nitric oxide in LTP induction and maintenance. Synapse. 13:1993;370-375.
57. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. U. S. A. 88:1991;11285-11289.
58. Prendergast M.A., Buccafusco J.J., Terry A.J. Nitric oxide synthase inhibition impairs spatial navigation learning and induces conditioned taste aversion. Pharmacol. Biochem. Behav. 57:1997;347-352.
59. Saxon D.W., Beitz A.J. Cerebellar injury induces NOS in Purkinje cells and cerebellar afferent neurons. NeuroReport. 5:1994;809-812.
60. Schuman E.M., Madison D.V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science. 254:1991;1503-1506.
61. Son H., Hawkins R.D., Martin K., Kiebler M., Huang P.L., Fishman M.C., Kandel E.R. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell. 87:1996;1015-1023.
62. Southam E., Charles S.L., Garthwaite J. The nitric oxide-cyclic GMP pathway and synaptic plasticity in the rat superior cervical ganglion. Br. J. Pharmacol. 119:1996;527-532.
63. Williams J.H., Errington M.L., Li Y.-G., Lynch M.A., Bliss T.V.P. The search for retrograde messengers in long-term potentiation. The Neurosciences. 5:1993;149-158.