Involvement of the nitric oxide cascade in melatonin-induced inhibition of long-term potentiation at hippocampal CA1 synapses

Neuroscience Research

Volumn 69, Issue 1, 2011, Pages 1-7

  Takahashi, Yoshiyuki ^a   Okada, Takashi ^a  

^a SOPHIA UNIVERSITY   (Japan)

Author keywords

CA1; Hippocampus; Long term potentiation; Melatonin; Nitric oxide; Rat

Indexed keywords

MELATONIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SYNAPSE; TETANY;

ANIMALS; CA1 REGION, HIPPOCAMPAL; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; HYDRAZINES; LONG-TERM POTENTIATION; MALE; MELATONIN; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE DONORS; OMEGA-N-METHYLARGININE; PYRAMIDAL CELLS; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC TRANSMISSION; TETANUS TOXIN;

EID: 78649811486     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2010.09.004     Document Type: Article

References (50)

1. Arancio O., Kiebler M., Lee C.J., Lev-Ram V., Tsien R.Y., Kandel E.R., Hawkins R.D. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 1996, 87:1025-1035.
2. Bannerman D.M., Chapman P.F., Kelly P.A., Butcher S.P., Morris R.G. Inhibition of nitric oxide synthase does not prevent the induction of long-term potentiation in vivo. J. Neurosci. 1994, 14:7415-7425.
3. Böhme G.A., Bon C., Stutzmann J.M., Doble A., Blanchard J.C. Possible involvement of nitric oxide in long-term potentiation. Eur. J. Phamacol. 1991, 199:379-381.
4. Bon C.L., Garthwaite J. On the role of nitric oxide in hippocampal long-term potentiation. J. Neurosci. 2003, 23:1941-1948.
5. Cain S.W., Chou T., Ralph M.R. Circadian modulation of performance on an aversion-based place learning task in hamsters. Behav. Brain Res. 2004, 150:201-205.
6. Chaudhury D., Wang L.M., Colwell C.S. Circadian regulation of hippocampal long-term potentiation. J. Biol. Rhythms 2005, 20:225-236.
7. Collins D.R., Davies S.N. Melatonin blocks the induction of long-term potentiation in an N-methyl-d-aspartate independent manner. Brain Res. 1997, 767:162-165.
8. Costa E.J., Lopes R.H., Lamy-Freund M.T. Permeability of pure lipid bilayers to melatonin. J. Pineal Res. 1995, 19:123-126.
9. 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. 1996, 16:418-424.
10. Escames G., León J., López L.C., Acuña-Castroviejo D. Mechanisms of N-methyl-d-aspartate receptor inhibition by melatonin in the rat striatum. J. Neuroendocrinol. 2004, 16:929-935.
11. Esteban J.A., Shi S.H., Wilson C., Nuriya M., Huganir R.L., Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 2003, 6:136-143.
12. Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 1993, 260:1661-1664.
13. 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. 1993, 160:85-88.
14. Harris K.M., Teyler T.J. Age differences in a circadian influence on hippocampal LTP. Brain Res. 1983, 261:69-73.
15. Hopper R.A., Garthwaite J. Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J. Neurosci. 2006, 26:11513-11521.
16. Izumi Y., Clifford D.B., Zorumski C.F. Inhibition of long-term potentiation by NMDA-mediated nitric oxide release. Science 1992, 257:1273-1276.
17. Izumi Y., Tokuda K., Zorumski C.F. Long-term potentiation inhibition by low-level N-methyl-d-aspartate receptor activation involves calcineurin, nitric oxide, and p38 mitogen-activated protein kinase. Hippocampus 2008, 18:258-265.
18. Katafuchi T., Li A.J., Hirota S., Kitamura Y., Hori T. Impairment of spatial learning and hippocampal synaptic potentiation in c-kit mutant rats. Learn. Mem. 2000, 7:383-392.
19. Larson J., Jessen R.E., Uz T., Arslan A.D., Kurtuncu M., Imbesi M., Manev H. Impaired hippocampal long-term potentiation in melatonin MT2 receptor-deficient mice. Neurosci. Lett. 2006, 393:23-26.
20. León J., Escames G., Rodríguez M.I., López L.C., Tapias V., Entrena A., Camacho E., Carrión M.D., Gallo M.A., Espinosa A., Tan D.X., Reiter R.J., Acuña-Castroviejo D. Inhibition of neuronal nitric oxide synthase activity by N1-acetyl-5-methoxykynuramine, a brain metabolite of melatonin. J. Neurochem. 2006, 98:2023-2033.
21. León J., Macías M., Escames G., Camacho E., Khaldy H., Martín M., Espinosa A., Gallo M.A., Acuña-Castroviejo D. Structure-related inhibition of calmodulin-dependent neuronal nitric-oxide synthase activity by melatonin and synthetic kynurenines. Mol. Pharmacol. 2000, 58:967-975.
22. Mazzucchelli C., Pannacci M., Nonno R., Lucini V., Fraschini F., Stankov B.M. The melatonin receptor in the human brain: cloning experiments and distribution studies. Brain Res. Mol. Brain Res. 1996, 39:117-126.
23. Morris R.G., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature 1986, 319:774-776.
24. Musshoff U., Riewenherm D., Berger E., Fauteck J.D., Speckmann E.J. Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus 2002, 12:165-173.
25. Otmakhov N., Lisman J.E. Postsynaptic application of a cAMP analogue reverses long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2002, 87:3018-3032.
26. Ozcan M., Yilmaz B., Carpenter D.O. Effects of melatonin on synaptic transmission and long-term potentiation in two areas of mouse hippocampus. Brain Res. 2006, 1111:90-94.
27. Pandi-Perumal S.R., Trakht I., Srinivasan V., Spence D.W., Maestroni G.J., Zisapel N., Cardinali D.P. Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog. Neurobiol. 2008, 85:335-353.
28. Petit L., Lacroix I., de Coppet P., Strosberg A.D., Jockers R. Differential signaling of human Mel1a and Mel1b melatonin receptors through the cyclic guanosine 3′-5′-monophosphate pathway. Biochem. Pharmacol. 1999, 58:633-639.
29. Puzzo D., Vitolo O., Trinchese F., Jacob J.P., Palmeri A., Arancio O. Amyloid-β peptide inhibits activation of the nitric oxide/cGMP/cAMP-responsive element-binding protein pathway during hippocampal synaptic plasticity. J. Neurosci. 2005, 25:6887-6897.
30. Raghavan A.V., Horowitz J.M., Fuller C.A. Diurnal modulation of long-term potentiation in the hamster hippocampal slice. Brain Res. 1999, 833:311-314.
31. Ralph M.R., Ko C.H., Antoniadis E.A., Seco P., Irani F., Presta C., McDonald R.J. The significance of circadian phase for performance on a reward-based learning task in hamsters. Behav. Brain Res. 2002, 2002:179-184.
32. Rawashdeh O., de Borsetti N.H., Roman G., Cahill G.M. Melatonin suppresses nighttime memory formation in zebrafish. Science 2007, 318:1144-1146.
33. Reneerkens O.A., Rutten K., Steinbusch H.W., Blokland A., Prickaerts J. Selective phosphodiesterase inhibitors: a promising target for cognition enhancement. Psychopharmacology 2009, 202:419-443.
34. Savaskan E., Ayoub M.A., Ravid R., Angeloni D., Fraschini F., Meier F., Eckert A., Müller-Spahn F., Jockers R. Reduced hippocampal MT2 melatonin receptor expression in Alzheimer's disease. J. Pineal Res. 2005, 38:10-16.
35. Schuman E.M., Madison D.V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 1991, 254:1503-1506.
36. Serulle Y., Zhang S., Ninan I., Puzzo D., McCarthy M., Khatri L., Arancio O., Ziff E.B. A GluR1-cGKII interaction regulates AMPA receptor trafficking. Neuron 2007, 56:670-688.
37. Shida C.S., Castrucci A.M., Lamy-Freund M.T. High melatonin solubility in aqueous medium. J. Pineal Res. 1994, 16:198-201.
38. Skaper S.D., Ancona B., Facci L., Franceschini D., Giusti P. Melatonin prevents the delayed death of hippocampal neurons induced by enhanced excitatory neurotransmission and nitridergic pathway. FASEB J. 1998, 12:725-731.
39. 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 1996, 87:1015-1023.
40. Soto-Moyano R., Burgos H., Flores F., Valladares L., Sierralta W., Fernández V., Pérez H., Hernández P., Hernández A. Melatonin administration impairs visuo-spatial performance and inhibits neocortical long-term potentiation in rats. Pharmacol. Biochem. Behav. 2006, 85:408-414.
41. Tamura E.K., Silva C.L., Markus R.P. Melatonin inhibits endothelial nitric oxide production in vitro. J. Pineal Res. 2006, 41:267-274.
42. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature 1999, 401:63-69.
43. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87:1327-1338.
44. van Staveren W.C., Markerink-van Ittersum M., de Vente H.W., Vente J. The effects of phosphodiesterase inhibition on cyclic GMP and cyclic AMP accumulation in the hippocampus of the rat. Brain Res. 2001, 888:275-286.
45. von Gall C., Stehle J.H., Weaver D.R. Mammalian melatonin receptors: molecular biology and signal transduction. Cell Tissue Res. 2002, 309:151-162.
46. Wang L.M., Suthana N.A., Chaudhury D., Weaver D.R., Colwell C.S. Melatonin inhibits hippocampal long-term potentiation. Eur. J. Neurosci. 2005, 22:2231-2237.
47. Weisskopf M.G., Castillo P.E., Zalutsky R.A., Nicoll R.A. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 1994, 265:1878-1882.
48. Williams J.H., Li Y.G., Nayak A., Errington M.L., Murphy K.P., Bliss T.V. The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron 1993, 11:877-884.
49. Zhu L.Q., Wang S.H., Ling Z.Q., Wang D.L., Wang J.Z. Effect of inhibiting melatonin biosynthesis on spatial memory retention and tau phosphorylation in rat. J. Pineal Res. 2004, 37:71-77.
50. Zwiller J., Revel M.O., Basset P. Evidence for phosphorylation of rat brain guanylate cyclase by cyclic AMP-dependent protein kinase. Biochem. Biophys. Res. Commun. 1981, 101:1381-1387.