Anti-amnesic properties of (±)-PPCC, a novel sigma receptor ligand, on cognitive dysfunction induced by selective cholinergic lesion in rats

Journal of Neurochemistry

Volumn 109, Issue 3, 2009, Pages 744-754

  Antonini, Vuokko ^a   Prezzavento, Orazio ^b   Coradazzi, Marino ^a   Marrazzo, Agostino ^b   Ronsisvalle, Simone ^b   Arena, Emanuela ^b   Leanza, Giampiero ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

Acetylcholine; Alzheimer's disease; Immunotoxin; Rat; Sigma 1 receptors; Spatial learning

Indexed keywords

2 [4 HYDROXY 4 PHENYLPIPERIDIN 1 YLMETHYL] 1 (4 METHYLPHENYL)CYCLOPROPANECARBOXYLATE; SIGMA 1 OPIATE RECEPTOR; SIGMA RECEPTOR LIGAND; UNCLASSIFIED DRUG;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE SEVERITY; DRUG ACTIVITY; DRUG RECEPTOR BINDING; FEMALE; LEARNING DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; WORKING MEMORY;

ACETYLCHOLINE; ANIMALS; ANTIBODIES, MONOCLONAL; ATROPINE; BEHAVIOR, ANIMAL; COGNITION DISORDERS; CYCLOPROPANES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHYLENEDIAMINES; FEMALE; MAZE LEARNING; MEMORY, SHORT-TERM; MOTOR ACTIVITY; MUSCARINIC ANTAGONISTS; NOOTROPIC AGENTS; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, SIGMA; RIBOSOME INACTIVATING PROTEINS, TYPE 1;

ANIMALIA; RATTUS;

EID: 64149122516     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06000.x     Document Type: Article

References (66)

1. Alonso G., Phan V., Guillemain I., Saunier M., Legrand A., Anoal M. Maurice T. (2000) Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system. Neuroscience 97, 155 170.
2. Antonini V., Marrazzo A., Boffo S., Aniskovich N., Ronsisvalle S., Prezzavento O., Ronsisvalle G. Leanza G. (2007) MR22, a novel sigma-1 receptor agonist: effects on lesion-induced memory dysfunction and amyloid deposition in rats. Front. CNS Oncol. Med. Chem. 41, 56.
3. Arendash G. W., King D. L., Gordon M. N., Morgan D., Hatcher J. M., Hope C. E. Diamond D. M. (2001) Progressive, age-related behavioral impairments in transgenic mice carrying both mutant amyloid precursor protein and presenilin-1 transgenes. Brain Res. 891, 42 53.
4. Aztiria E., Cataudella T., Spampinato S. Leanza G. (2008) Septal grafts restore cognitive abilities and amyloid precursor protein metabolism. Neurobiol. Aging [Epub ahead of print] doi:.
5. Bartus R. T., Dean R. L. 3rd., Beer B. Lippa A. S. (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408 414.
6. Baskin D. S., Browning J. L., Pirozzolo F. J., Korporaal S., Baskin J. A. Appel S. H. (1999) Brain choline acetyltransferase and mental function in Alzheimer disease. Arch. Neurol. 56, 1121 1123.
7. Becker R., Giacobini E., Elble R., McIlhany M. Sherman K. (1988) Potential pharmacotherapy of Alzheimer disease. a comparison of various forms of physostigmine administration. Acta Neurol. Scand. 116, 19 32.
8. Berger-Sweeney J., Heckers S., Mesulam M. M., Wiley R. G., Lappi D. A. Sharma M. (1994) Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J. Neurosci. 14, 4507 4519.
9. Bouchard P. Quirion R. (1997) [3H]1,3-di(2-tolyl)guanidine and [3H](+)pentazocine binding sites in the rat brain: autoradiographic visualization of the putative sigma1 and sigma2 receptor subtypes. Neuroscience 76, 467 477.
10. Collerton D. (1986) Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience 19, 1 28.
11. Coyle J. T., Price D. L. DeLong M. R. (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219, 1184 1190.
12. Cummings J. L., Donohue J. A. Brooks R. L. (2000) The relationship between donepezil and behavioral disturbances in patients with Alzheimer's disease. Am. J. Geriatr. Psychiatry 8, 134 140.
13. Diamond D. M., Park C. R., Heman K. L. Rose G. M. (1999) Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9, 542 552.
14. Doody R. S., Dunn J. K., Clark C. M., Farlow M., Foster N. L., Liao T., Gonzales N., Lai E. Massman P. (2001) Chronic donepezil treatment is associated with slowed cognitive decline in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 12, 295 300.
15. Earley B., Burke M., Leonard B. E., Gouret C. J. Junien J. L. (1991) Evidence for an anti-amnesic effect of JO 1784 in the rat: a potent and selective ligand for the sigma receptor. Brain Res. 546, 282 286.
16. Guitart X., Codony X. Monroy X. (2004) Sigma receptors: biology and therapeutic potential. Psychopharmacology 174, 301 319.
17. Hayashi T. Su T.-P. (2005) The sigma receptor: evolution of the concept in neuropsychopharmacology. Curr. Neuropharmacol. 3, 267 280.
18. 2+ signalling and cell survival. Cell 131, 596 610.
19. Hayashi T., Maurice T. Su T. P. (2000) Ca(2+) signaling via sigma(1)-receptors: novel regulatory mechanism affecting intracellular Ca(2+) concentration. J. Pharmacol. Exp. Ther. 293, 788 798.
20. Heckers S., Ohtake T., Wiley R. G., Lappi D. A., Geula C. Mesulam M. M. (1994) Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J. Neurosci. 14, 1271 1289.
21. Hellewell S. B. Bowen W. D. (1990) A sigma-like binding site in rat pheochromocytoma (PC12) cells: decreased affinity for (+)-benzomorphans and lower molecular weight suggest a different sigma receptor form from that of guinea pig brain. Brain Res. 527, 244 253.
22. Ishima T., Nishimura T., Iyo M. Hashimoto K. (2008) Potentiation of nerve growth factor-induced neurite outgrowth in PC12 cells by donepezil: role of sigma-1 receptors and IP(3) receptors. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1656 1659.
23. Junien J. L., Roman F. J., Brunelle G. Pascaud X. (1991) JO1784, a novel sigma ligand, potentiates [3H]acetylcholine release from rat hippocampal slices. Eur. J. Pharmacol. 200, 343 345.
24. Leanza G. (1998) Chronic elevation of amyloid precursor protein expression in the neocortex and hippocampus of rats with selective cholinergic lesions. Neurosci. Lett. 257, 53 56.
25. Leanza G., Nilsson O. G., Wiley R. G. Bjorklund A. (1995) Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci. 7, 329 343.
26. Leanza G., Muir J., Nilsson O. G., Wiley R. G., Dunnett S. B. Bjorklund A. (1996) Selective immunolesioning of the basal forebrain cholinergic system disrupts short-term memory in rats. Eur. J. Neurosci. 8, 1535 1544.
27. Leanza G., Martinez-Serrano A. Bjorklund A. (1998) Amelioration of spatial navigation and short-term memory deficits by grafts of foetal basal forebrain tissue placed into the hippocampus and cortex of rats with selective cholinergic lesions. Eur. J. Neurosci. 10, 2353 2370.
28. Lin L., LeBlanc C. J., Deacon T. W. Isacson O. (1998) Chronic cognitive deficits and amyloid precursor protein elevation after selective immunotoxin lesions of the basal forebrain cholinergic system. Neuroreport 9, 547 552.
29. Lin L., Georgievska B., Mattsson A. Isacson O. (1999) Cognitive changes and modified processing of amyloid precursor protein in the cortical and hippocampal system after cholinergic synapsed loss and muscarinic receptor activation. Proc. Natl Acad. Sci. USA 96, 12108 12113.
30. Martin W. R., Eades C. G., Thompson J. A., Huppler R. E. Gilbert P. E. (1976) The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmacol. Exp. Ther. 197, 517 532.
31. Matsuno K., Matsunaga K., Senda T. Mita S. (1993) Increase in extracellular acetylcholine level by sigma ligands in rat frontal cortex. J. Pharmacol. Exp. Ther. 265, 851 859.
32. Matsuno K., Senda T., Matsunaga K. Mita S. (1994) Ameliorating effects of sigma receptor ligands on the impairment of passive avoidance tasks in mice: involvement in the central acetylcholinergic system. Eur. J. Pharmacol. 261, 221 224.
33. Matsuno K., Senda T., Kobayashi T. Mita S. (1995) Involvement of sigma1 receptor in (+)-N-allylnormetazocine-stimulated hippocampal cholinergic functions in rats. Brain Res. 690, 200 206.
34. Maurice T. (2007) Cognitive effects of sigma receptor ligands, in Sigma Receptors. Chemistry, Cell Biology and Clinical Implications (Matsumoto R. R., Bowen W. D. Su T.-P., eds pp. 237 271. Springer, New York.
35. Maurice T., Lockhart B. P. Privat A. (1996) Amnesia induced in mice by centrally administered β-amyloid involves cholinergic dysfunction. Brain Res. 706, 181 193.
36. Maurice T., Su T. P. Privat A. (1998) Sigma1 (sigma 1) receptor agonists and neurosteroids attenuate β25-35-amyloid peptide-induced amnesia in mice through a common mechanism. Neuroscience 83, 413 428.
37. Mesulam M. (2004) The cholinergic lesion of Alzheimer's disease: pivotal factor or side show? Learn Mem. 11, 43 49.
38. Meunier J., Ieni J. Maurice T. (2006a) Antiamnesic and neuroprotective effects of donepezil against learning impairments induced in mice by exposure to carbon monoxide gas. J. Pharmacol. Exp. Ther. 317, 1307 1319.
39. Meunier J., Ieni J. Maurice T. (2006b) The anti-amnesic and neuroprotective effects of donepezil against amyloid beta25-35 peptide-induced toxicity in mice involve an interaction with the sigma1 receptor. Br. J. Pharmacol. 149, 998 1012.
40. Minger S. L., Esiri M. M., McDonald B., Keene J., Carter J., Hope T. Francis P. T. (2000) Cholinergic deficits contribute to behavioral disturbance in patients with dementia. Neurology 55, 1460 1467.
41. Morin-Surun M. P., Collin T., Denavit-Saubie M., Baulieu E. E. Monnet F. P. (1999) Intracellular sigma1 receptor modulates phospholipase C and protein kinase C activities in the brainstem. Proc. Natl Acad. Sci. USA 96, 8196 8199.
42. Morris R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47 60.
43. Netto C. A., Hodges H., Sinden J. D., Le Peillet E., Kershaw T., Sowinski P., Meldrum B. S. Gray J. A. (1993) Effects of fetal hippocampal field grafts on ischaemic-induced deficits in spatial navigation in the water maze. Neuroscience 54, 69 92.
44. Pappas B. A., Bayley P. J., Bui B. K., Hansen L. A. Thal L. J. (2000) Choline acetyltransferase activity and cognitive domain scores of Alzheimer's patients. Neurobiol. Aging 21, 11 17.
45. Parent M. B. Baxter M. G. (2004) Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn Mem. 11, 9 20.
46. Paxinos G. Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, San Diego.
47. Prezzavento O., Campisi A., Ronsisvalle S. et al. (2007) Novel sigma receptor ligands: synthesis and biological profile. J. Med. Chem. 50, 951 961.
48. Prezzavento O., Parenti C., Marrazzo A., Ronsisvalle S., Vittorio F., Arico G., Scoto G. M. Ronsisvalle G. (2008) A new sigma ligand, (+/-)-PPCC, antagonizes kappa opioid receptor-mediated antinociceptive effect. Life Sci. 82, 549 553.
49. Quirion R., Bowen W. D., Itzhak Y., Junien J. L., Musacchio J. M., Rothman R. B., Su T. P., Tam S. W. Taylor D. P. (1992) A proposal for the classification of sigma binding sites. Trends Pharmacol. Sci. 13, 85 86.
50. Reisberg B., Doody R., Stoffler A., Schmitt F., Ferris S. Mobius H. J. (2003) Memantine in moderate-to-severe Alzheimer's disease. N. Engl. J. Med. 348, 1333 1341.
51. Rogers S. L., Farlow M. R., Doody R. S., Mohs R. Friedhoff L. T. (1998) A 24-week, double-blind, placebo-controlled trial of donepezil in patients with Alzheimer's disease. Donepezil Study Group. Neurology 50, 136 145.
52. Scarpini E., Scheltens P. Feldman H. (2003) Treatment of Alzheimer's disease: current status and new perspectives. Lancet Neurol. 2, 539 547.
53. Senda T., Matsuno K., Kobayashi T., Nakazawa M., Nikata K. Mita S. (1998) Ameliorative effect of SA4503, a novel cognitive enhancer on the basal forebrain lesion-induced impairment of the spatial learning performance in rats. Pharmacol. Biochem. Behav. 59, 129 134.
54. Steckler T., Keith A. B., Wiley R. G. Sahgal A. (1995) Cholinergic lesions by 192 IgG-saporin and short-term recognition memory: role of the septohippocampal projection. Neuroscience 66, 101 114.
55. Summers W. K., Majovski L. V., Marsh G. M., Tachiki K. Kling A. (1986) Oral tetrahydroaminoacridine in long-term treatment of senile dementia, Alzheimer type. N. Engl. J. Med. 315, 1241 1245.
56. Tariot P. N., Solomon P. R., Morris J. C., Kershaw P., Lilienfeld S. Ding C. (2000) A 5-month, randomized, placebo-controlled trial of galantamine in AD. The galantamine USA-10 Study Group. Neurology 54, 2269 2276.
57. Torres E. M., Perry T. A., Blockland A., Wilkinson L. S., Wiley R. G., Lappi D. A. Dunnet S. B. (1994) Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63, 95 122.
58. Tottori K., Nakai M., Uwahodo Y., Miwa T., Yamada S., Oshiro Y., Kikuchi T. Altar C. A. (2002) Attenuation of scopolamine-induced and age-associated memory impairments by the sigma and 5-hydroxytryptamine(1A) receptor agonist OPC-14523 (1-[3-[4-(3-chlorophenyl)-1-piperazinyl]propyl]-5-methoxy-3,4-dihydro- 2[1H]-quinolinone monomethanesulfonate). J. Pharmacol. Exp. Ther. 301, 249 257.
59. Waite J. J., Chen A. D., Wardlow M. L., Wiley R. G., Lappi D. A. Thal L. J. (1995) 192 immunoglobulin G-saporin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells. Neuroscience 65, 463 476.
60. Walker J. M., Bowen W. D., Walker F. O., Matsumoto R. R., De Costa B. Rice K. C. (1990) Sigma receptors: biology and function. Pharmacol. Rev. 42, 355 402.
61. Walker J. M., Martin W. J., Hohmann A. G., Hemstreet M. K., Roth J. S., Leitner M. S., Weised S. D., Patrick S. L., Patrick R. L. Matsumoto R. R. (1994) Role of sigma receptors in brain mechanisms of movement. in Sigma Receptors (Itzhak Y., ed.), pp. 205 224. Academic Press, San Diego.
62. Whitehouse P. J., Price D. L., Clark A. W., Coyle J. T. DeLong M. R. (1981) Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann. Neurol. 10, 122 126.
63. Wiley R. G. Kline R. H. I. V. (2000) Neuronal lesioning with axonally transported toxins. J. Neurosci. Methods 103, 73 82.
64. Wiley R. G., Oeltmann T. N. Lappi D. A. (1991) Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res. 562, 149 153.
65. Winblad B. Poritis N. (1999) Memantine in severe dementia: results of the 9M-Best Study (Benefit and efficacy in severely demented patients during treatment with memantine). Int. J. Geriatr. Psychiatry 14, 135 146.
66. Wrenn C. C. Wiley R. G. (1998) The behavioral functions of the cholinergic basal forebrain: lessons from 192 IgG-saporin. Int. J. Dev. Neurosci. 16, 595 602.