Effects of chronic nimodipine on working memory of old rats in relation to defects in synaptosomal calcium homeostasis

European Journal of Pharmacology

Volumn 350, Issue 2-3, 1998, Pages 141-150

  Batuecas, Alicia ^a   Pereira, Rodolfo ^c   Centeno, Carlos ^a   Pulido, Juan A ^b   Hernández, Miguel ^a   Bollati, Alicia ^c   Bogónez, Elena ^a   Satrústegui, Jorgina ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF ALCALÁ   (Spain)

^c UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

45Ca2+ accumulation; Ca2+ homeostasis; Calbindin D28K; Calreticulin; Cerebral cortex; Eight arm maze; Nimodipine; Old rat; Synaptosome; Working memory

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; NIMODIPINE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM HOMEOSTASIS; COGNITION; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; LONG TERM CARE; MALE; NERVE DEGENERATION; NONHUMAN; ORAL DRUG ADMINISTRATION; PRIORITY JOURNAL; RAT; SYNAPTOSOME; WORKING MEMORY;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN CHEMISTRY; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM RADIOISOTOPES; HOMEOSTASIS; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; NIMODIPINE; RATS; RATS, WISTAR; SYNAPTOSOMES;

EID: 0032486125     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-2999(98)00250-7     Document Type: Article

References (58)

1. Amenta F., Mancini M., Naves F.J., Vega J.A., Zaccheo D. Effect of treatment with the dihydropyridine-type calcium antagonist darodipine (PY 108-068) on the expression of calbindin D-28K immunoreactivity in the cerebellar cortex of aged rats. Mech. Ageing Dev. 77:1995;149-157.
2. Blanco P., Huidobro A., Villalba M., Gómez-Puertas P., Bogónez E., Pereira R., Martínez-Serrano A., Aparicio J.J., Satrústegui J. The activity of synaptosomal calcium channels is inversely correlated with working memory performance in memory impaired, aged rats. Neurosci. Lett. 165:1994;5-8.
3. Campbell L.W., Hao S.Y., Thibault O., Blalock E.M., Landfield P.W. Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J. Neurosci. 16:1996;6286-6295.
4. 2+ influx or efflux pathway. Biochim. Biophys. Acta. 1107:1992;175-178.
5. Chard P.S., Bleakman D., Christakos S., Fullner C.S., Miller R.J. Calcium buffering properties of calbindin-D28K and parvalbumin in rat sensory neurons. J. Physiol. 472:1993;341-357.
6. Chard P.S., Jordán J., Marcuccilli C.J., Miller R.J., Leiden J.M., Roos R.P., Ghadge G.D. Regulation of excitatory transmission at hippocampal synapses by calbindin D28K. Proc. Natl. Acad. Sci. U.S.A. 92:1995;5144-5148.
7. Chen C., Tonegawa S. Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain. Annu. Rev. Neurosci. 20:1997;157-184.
8. Chuang-Kuo W., Mesulam M.M., Geula C. Age-related loss of calbindin from human basal forebrain cholinergic neurons. NeuroReport. 8:1997;2209-2213.
9. De Jong G.I., Jansen A.S.P., Horvath E., Gispen W.H., Luiten P.G.M. Nimodipine effects on cerebral microvessels and sciatic nerve in aging rats. Neurobiol. Aging. 13:1991;73-81.
10. De Jong G.I., Nyakas C., Schuurman T., Luiten P.G.M. Aging-related alterations in behavioral activation an cerebrovascular integrity in rats are dose-dependently influenced by nimodipine. Neurosci. Res. Commun. 12:1993;1-8.
11. De Jong G.I., Naber P.A., Van der Zee E.A., Thompson L.T., Disterhoft J.F., Luiten P.G.M. Age-related loss of calcium binding proteins in rabbit hippocampus. Neurobiol. Aging. 17:1996;459-465.
12. Deyo R.A., Straube K.T., Disterhoft J.F. Nimodipine facilitates associative learning in aging rabbits. Science. 243:1989;809-811.
13. 2+ channels during opioid tolerance and supersensitivity in rats. J. Pharmacol. Exp. Ther. 274:1995;1538-1544.
14. Disterhoft J.F., Thompson L.T., Moyer J.R. Jr., Mogul D.J. Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus. Life Sci. 59:1996;413-420.
15. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48:1997;649-684.
16. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. USA. 93:1996;4765-4769.
17. 32P-prelabeled synaptosomes contain a phosphoprotein of apparent Mr 65,000 (pp65), a possible substrate for PKC J. Biol. Chem. 269:1994;7564-7570.
18. Goodman J.H., Wasterlain C.G., Mussarweh W.F., Dean E., Sollas A.L., Solviter R.S. Calbindin-D28K immunoreactivity and selective vulnerability to ischemia in the dentate gyrus of the developing rat brain. Brain Res. 606:1993;309-314.
19. Huang Y.C., Christakos S. Modulation of rat calbindin-D28K gene expression by 1,25 dihydroxyvitamin D3 and dietary alteration. Mol. Endocrinol. 2:1988;928-936.
20. Huidobro A., Blanco P., Villalba M., Gómez-Puertas P., Villa A., Pereira R., Bogónez E., Martínez-Serrano A., Aparicio J.J., Satrústegui J. Age-related changes in calcium homeostatic mechanisms in synaptosomes in relation with working memory deficiency. Neurobiol. Aging. 14:1993;479-486.
21. Iacopino A.M., Christakos S. Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc. Natl. Acad. Sci. USA. 87:1990;4078-4082.
22. Inada K., Yokoi Y., Kabuto H., Namba Y., Ogawa N. The effects of chronic administration of nimodipine on age-related changes in nitric oxide and its synthase in senescence-accelerated mouse brain. Biochem. Mol. Biol. Int. 41:1997;753-765.
23. Ingram D.K., Joseph J.A., Spangler E.L., Roberts D., Hengemihle J., Fanelli R.J. Chronic nimodipine treatment in aged rats: analysis of motor and cognitive effects and muscarinic-induced striatal dopamine release. Neurobiol. Aging. 15:1994;55-61.
24. Izquierdo Y., Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68:1997;285-316.
25. Kabuto H., Yokoi I., Mori A., Murakami M., Sawada S. Neurochemical changes related to ageing in the senescence-accelerated mouse brain and the effect of chronic administration of nimodipine. Mech. Ageing Dev. 80:1995;1-9.
26. Kazda S., Garthoff B., Krause H.P., Sclossmann K. Cerebrovascular effects of the calcium antagonistic dihydropyridine derivative, nimodipine, in animal experiments. Arzneim.-Forsch. 32:1982;331-338.
27. Kennedy T.E., Kuhl D., Barzilai A., Sweatt J.D., Kandel E.R. Long-term sensitization training in Aplysia leads to an increase in calreticulin, a major presynaptic calcium-binding protein. Neuron. 9:1992;1013-1024.
28. Krause K., Michalak M. Calreticulin. Cell. 88:1997;439-443.
29. Krywkowski P., Potier B., Billard J.M., Dutar P., Lamour Y. Synaptic mechanisms and calcium binding proteins in the aged rat. Life Sci. 59:1996;421-428.
30. Lanahan A., Lyford G., Stevenson G.S., Worley P.F., Barnes C.A. Selective alteration of long-term potentiation-induced transcriptional response in hippocampus of aged, memory-impaired rats. J. Neurosci. 17:1997;2876-2885.
31. Levere T.E., Walker A. Old age and cognition: enhancement of recent memory in aged rats by the calcium channel blocker nimodipine. Neurobiol. Aging. 13:1991;63-66.
32. Luine V., Bowling D., Hearns M. Spatial memory deficits in aged rats: contributions of monoaminergic systems. Brain Res. 537:1990;271-278.
33. Luiten P.G.M., Buwalda B., Träber J., Nyakas C. Induction of enhanced postnatal expression of immunoreactive calbindin-D28K in rat forebrain by the calcium antagonist nimodipine. Dev. Brain Res. 79:1994;10-11.
34. Martínez A., Vitórica A., Bogónez E., Satrústegui J. Differential effects of age on the pathways of calcium influx into nerve terminals. Brain Res. 435:1987;249-257.
35. Martínez-Serrano A., Björklund A. Immortalized neural progenitor cells for CNS gene transfer and repair. Trends Neurosci. 20:1997;530-538.
36. Martínez-Serrano A., Blanco P., Satrústegui J. Calcium binding to the cytosol and calcium extrusion mechanisms in intact synaptosomes and their alterations with aging. J. Biol. Chem. 267:1997;4672-4679.
37. Maruyama K., Ebisawa K., Nonomura Y. Purification of Vitamin D-dependent 28000-Mr calcium-binding protein from bovine cerebellum and kidney by calcium-dependent elution from deae-cellulose DE-52 column chromatography. Anal. Biochem. 151:1985;1-6.
38. Mattson M.P., Rychlick B., Chu C., Christakos S. Evidence for calcium reducing and excitoprotective roles for calcium binding protein calbindin-D28K in cultured hippocampal neurones. Neuron. 6:1991;41-51.
39. 2+ regulation. Mech. Ageing Dev. 25:1984;215-225.
40. Nakamura-Palacios E.M., Caldas C.K., Fiorini A., Chagas K.D., Chagas K.N., Vasquez E.C. Deficits in spatial learning and working memory in spontaneously hypertensive rats. Behav. Brain Res. 74:1996;217-227.
41. Olton D.S., Samuelson R.J. Remembrance of places passed: spatial memory in rats. J. Exp. Psychol.: Anim. Behav. Processes. 2:1976;97-116.
42. Orrenius S., Burkitt M.M.J., Kass G.E.N., Dypbukt J.M., Nicotera P. Calcium ions and oxidative cell injury. Ann. Neurol. 32:1992;535-542.
43. Peterson C., Nicholls D.G., Gibson G.E. Subsynaptosomal calcium distribution during ageing and 3,4-diaminopyridine treatment. Neurobiol. Aging. 6:1985;297-304.
44. Reddy D.R., Pollock A.S., Clark S.A., Sooy K., Vasavada R.C., Stewart A.F., Honeyman T., Christakos S. Transfection and overexpression of the calcium binding protein calbindin-D28K results in a stimulatory effect on insulin synthesis in a rat β cell line (RIN 1046-38). Proc. Natl. Acad. Sci. USA. 94:1997;1961-1966.
45. Riekkinen M., Schmidt B., Kuitunen J., Riekkinen P. Jr. Effects of combined chronic nimodipine and acute metrifonate treatment on spatial and avoidance behavior. Eur. J. Pharmacol. 322:1997;1-9.
46. Satrústegui J., Villalba M., Pereira R., Bogónez E., Martínez-Serrano A. Cytosolic and mitochondrial calcium in synaptosomes during aging. Life Sci. 59:1996;429-434.
47. Schurmans S., Schiffmann S.N., Gurden H., Lemaire M., Lipp H.P., Schwam V., Pochet R., Imperato A., Bohme G.A., Parmentier M. Impaired long-term potentiation induction in dentate gyrus of calretinin-deficient mice. Proc. Natl. Acad. Sci. USA. 94:1997;10415-10420.
48. Schwob J.E., Fuller T., Price J.L., Olney J.W. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 5:1980;991-1014.
49. Scribiane A., Schuurman T., Traber J. Pharmacological basis for the use of nimodipine in central nervous system disorders. FASEB J. 3:1989;1799-1806.
50. Stewart J., Mitchell J., Kalant N. The effect of life-long food restriction on spatial memory in young and aged Fischer 344 rats measured in the eight-arm radial and the Morris water mazes. Neurobiol. Aging. 10:1989;669-675.
51. Thibault O., Landfield P.W. Increase in single L-type calcium channels in hippocampal neurons during aging. Science. 272:1996;1017-1020.
52. Verkhratsky A., Toescu E.C. Calcium and neuronal ageing. Trends Neurosci. 21:1998;2-7.
53. 2+ binding proteins during rat brain ageing: loss of calbindin and calretinin in the hippocampus, with no change in the cerebellum. Eur. J. Neurosci. 6:1994;1491-1499.
54. Villalba M., Pereira R., Martínez-Serrano A., Satrústegui J. Altered cell calcium regulation in synaptosomes and brain cells of the 30-month-old rat: prominent effects in hippocampus. Neurobiol. Aging. 16:1995;809-816.
55. Vitórica J., Satrústegui J. Involvement of mitochondria in the age-dependent decrease in calcium uptake in rat brain synaptosomes. Brain Res. 378:1986;36-48.
56. Waser M., Mesaeli N., Spencer C., Michalak M. Regulation of calreticulin gene expression by calcium. J. Cell Biol. 138:1997;547-557.
57. Wasserman R.H., Corradino R.A., Taylor A.N. Vitamin D-dependent calcium-binding protein. J. Biol. Chem. 243:1968;3978-3986.
58. Yamada S., Uchida S., Ohkura T., Yamaguchi M., Suzuki M., Yamamoto M. Alterations in calcium antagonist receptors and calcium content in senescent brain and attenuation by nimodipine and nicardipine. J. Pharmacol. Exp. Ther. 277:1996;721-727.