Galantamine counteracts development of learning impairment in guinea pigs exposed to the organophosphorus poison soman: Clinical significance

NeuroToxicology

Volumn 32, Issue 6, 2011, Pages 785-798

  Mamczarz, Jacek ^a   Kulkarni, Girish S ^a   Pereira, Edna F R ^a   Albuquerque, Edson X ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Cholinesterease; Galantamine; Guinea pig; Morris water maze; Organophosphorus; Soman

Indexed keywords

ACETYLCHOLINESTERASE; GALANTAMINE; ORGANOPHOSPHORUS COMPOUND; SOMAN;

ACUTE TOXICITY; AMNESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PROTECTION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; EXPERIMENTAL GUINEA PIG; FEMALE; LD 50; LEARNING DISORDER; LONG TERM EXPOSURE; MAZE TEST; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE; TREATMENT DURATION;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CHOLINESTERASE INHIBITORS; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; EXTINCTION, PSYCHOLOGICAL; FEMALE; GALANTAMINE; GUINEA PIGS; LETHAL DOSE 50; MAZE LEARNING; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; NOOTROPIC AGENTS; REACTION TIME; SOMAN; TIME FACTORS;

ANIMALIA; CAVIA;

EID: 80055078018     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.07.001     Document Type: Article

References (59)

1. Acheson S.K., Moore N.L., Kuhn C.M., Wilson W.A., Swartzwelder H.S. The synthetic cannabinoid WIN 55212-2 differentially modulates thigmotaxis but not spatial learning in adolescent and adult animals. Neurosci Lett 2011, 487:411-414.
2. Albuquerque E.X., Deshpande S.S., Kawabuchi M., AracavaY, Idriss M., Rickett D.L., et al. Multiple actions of anticholinesterase agents on chemosensitive synapses: molecular basis for prophylaxis and treatment of organophosphate poisoning. Fundam Appl Toxicol 1985, 5:S182-S203.
3. Albuquerque E.X., Pereira E.F.R., Aracava Y., Fawcett W.P., Oliveira M., Randall W.R., et al. Effective countermeasure against poisoning by organophosphorus insecticides and nerve agents. Proc Natl Acad Sci USA 2006, 103:13220-13225.
4. Albuquerque E.X., Pereira E.F.R., Alkondon M., Rogers S.W. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 2009, 89:73-120.
5. Alexandrova E.A., Aracava Y., Pereira E.F.R., Albuquerque E.X. Pretreatment of guinea pigs with galantamine prevents immediate and delayed effects of soman on inhibitory synaptic transmission in the hippocampus. J Pharmacol Exp Ther 2010, 334:1051-1058.
6. Alkondon M., Aracava Y., Pereira E.F.R., Albuquerque E.X. A single in vivo application of cholinesterase inhibitors has neuron type-specific effects on nicotinic receptor activity in guinea pig hippocampus. J Pharmacol Exp Ther 2009, 328:69-82.
7. Aracava Y., Pereira E.F.R., Akkerman M., Adler M., Albuquerque E.X. Effectiveness of donepezil, rivastigmine, and ±huperzine A in counteracting the acute toxicity of organophosphorus nerve agents: comparison with galantamine. J Pharmacol Exp Ther 2009, 331:1014-1024.
8. Byrnes M.L., Richardson D.P., Brien J.F., Reynolds J.N., Dringenberg H.C. Spatial acquisition in the Morris water maze and hippocampal long-term potentiation in the adult guinea pig following brain growth spurt-prenatal ethanol exposure. Neurotoxicol Teratol 2004, 26:543-551.
9. Cain D.P., Boon F., Corcoran M.E. Thalamic and hippocampal mechanisms in spatial navigation: a dissociation between brain mechanisms for learning how versus learning where to navigate. Behav Brain Res 2006, 170:241-256.
10. Corey-Bloom J. Galantamine: a review of its use in Alzheimer's disease and vascular dementia. Int J Clin Pract 2003, 57:219-223.
11. Coupland R., Leins KR Science and prohibited weapons. Science 2005, 308:1841.
12. de Groot D.M., Bierman E.P., Bruijnzeel P.L., Carpentier P., Kulig B.M., Lallement G., et al. Beneficial effects of TCP on soman intoxication in guinea pigs: seizures, brain damage and learning behaviour. J Appl Toxicol 2001, 21:S57-S65.
13. Devan B.D., McDonald R.J., White NM Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: relation to thigmotaxis. Behav Brain Res 1999, 100:5-14.
14. Dringenberg H.C., Richardson D.P., Brien J.F., Reynolds J.N. Spatial learning in the guinea pig: cued versus non-cued learning, sex differences, and comparison with rats. Behav Brain Res 2001, 124:97-101.
15. Filliat P., Baubichon D., Burckhart M.F., Pernot-Marino I., Foquin A., Masqueliez C., et al. Memory impairment after soman intoxication in rat: correlation with central neuropathology. Improvement with anticholinergic and antiglutamatergic therapeutics. Neurotoxicology 1999, 20:535-549.
16. Filliat P., Coubard S., Pierard C., Liscia P., Beracochea D., Four E., et al. Long-term behavioral consequences of soman poisoning in mice. Neurotoxicology 2007, 28:508-519.
17. Filliat P., Foquin A., Lallement G. Effects of chronic administration of huperzine A on memory in guinea pigs. Drug Chem Toxicol 2002, 25:9-24.
18. Gröhn O.H., Lukkarinen J.A., Oja J.M., van Zijl P.C., Ulatowski J.A., Traystman R.J., et al. Noninvasive detection of cerebral hypoperfusion and reversible ischemia from reductions in the magnetic resonance imaging relaxation time, T2. J Cereb Blood Flow Metab 1998, 18:911-920.
19. Gullapalli R.P., Aracava Y., Zhuo J., Helal Neto E., Wang J., Makris G., et al. Magnetic resonance imaging reveals that galantamine prevents structural brain damage induced by an acute exposure of guinea pigs to soman. Neurotoxicology 2010, 31:67-76.
20. Hood E. The Tokyo attacks in retrospect: sarin leads to memory loss. Environ Health Perspect 2001, 109:A542.
21. Institute of Laboratory Animal Resources Guide for the care and use of laboratory animals 1996, Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council, Washington (DC). 7th ed.
22. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Da Silva W.C., Medina J.H., et al. The connection between the hippocampal and the striatal memory systems of the brain: a review of recent findings. Neurotox Res 2006, 10:113-121.
23. Johnson E.A., Daugherty K.S., Gallagher S.J., Moran A.V., DeFord S.M. Glutamate receptor pathology is present in the hippocampus following repeated sub-lethal soman exposure in the absence of spatial memory deficits. Neurotoxicology 2008, 29:73-80.
24. Kallai J., Makany T., Karadi K., Jacobs W.J. Spatial orientation strategies in Morris-type virtual water task for humans. Behav Brain Res 2005, 159:187-196.
25. Kassa J., Krejcová G., Vachek J. The impairment of spatial memory following low-level sarin inhalation exposure and antidotal treatment in rats. Acta Medica (Hradec Kralove) 2002, 45:149-153.
26. Lau W.M., Freeman S.E., Szilagyi M. Binding of some organophosphorus compounds at adenosine receptors in guinea pig brain membranes. Neurosci Lett 1988, 94:125-130.
27. Lewejohann L., Pickel T., Sachser N., Kaiser S. Wild genius - domestic fool? Spatial learning abilities of wild and domestic guinea pigs. Front Zool 2010, 7:9.
28. Lintern M.C., Wetherell J.R., Smith M.E. Differential recovery of acetylcholinesterase in guinea pig muscle and brain regions after soman treatment. Hum Exp Toxicol 1998, 17:157-162.
29. Mamczarz J., Pereira E.F.R., Aracava Y., Adler M., Albuquerque E.X. An acute exposure to a sub-lethal dose of soman triggers anxiety-related behavior in guinea pigs: interactions with acute restraint. Neurotoxicology 2010, 31:77-84.
30. Markowska A.L., Long J.M., Johnson C.T., Olton D.S. Variable-interval probe test as a tool for repeated measurements of spatial memory in the water maze. Behav Neurosci 1993, 107:627-632.
31. Maxwell D.M., Brecht K.M., O'Neill B.L. The effect of carboxylesterase inhibition on interspecies differences in soman toxicity. Toxicol Lett 1987, 39:35-42.
32. McDonald R.J., White N.M. Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 1994, 61:260-270.
33. McDonough J.H., Shih T.M. Neuropharmacological mechanisms of nerve agent-induced seizure and neuropathology. Neurosci Biobehav Rev 1997, 21:559-579.
34. 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.
35. Newmark J. Nerve agents. Neurologist 2007, 13:20-32.
36. Nishiwaki Y., Maekawa K., Ogawa Y., Asukai N., Minami M., Omae K. Effects of sarin on the nervous system in rescue team staff members and police officers 3 years after the Tokyo subway sarin attack. Environ Health Perspect 2001, 109:1169-1173.
37. Noda Y., Mouri A., Ando Y., Yukari Wakia1, Yamada S.-N., Yoshimi A., et al. Galantamine ameliorates the impairment of recognition memory in mice repeatedly treated with methamphetamine: involvement of allosteric potentiation of nicotinic acetylcholine receptors and dopaminergic-ERK1/2 systems. Intern J Neuropsychopharmacol 2010, 13:1343-1354.
38. Ohtani T., Iwanami A., Kasai K., Yamasue H., Kato T., Sasaki T., et al. Post-traumatic stress disorder symptoms in victims of Tokyo subway attack: a 5-year follow-up study. Psychiatry Clin Neurosci 2004, 58:624-629.
39. Okumura T., Takasu N., Ishimatsu S., Miyanoki S., Mitsuhashi A., Kumada K. Report on 640 victims of the Tokyo subway sarin attack. Ann Emerg Med 1996, 28:129-135.
40. Osterreicher J., Pejchal J., Kassa J. Alteration of mitogen-activated protein kinase pathway after soman poisoning. Drug Chem Toxicol 2007, 30:283-291.
41. Packard M.G., Cahill L., McGaugh J.L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci USA 1994, 91:8477-8481.
42. Packard M.G., McGaugh J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav Neurosci 1992, 106:439-446.
43. Pereira E.F.R., Aracava Y., Alkondon M., Akkerman M., Merchenthaler I., Albuquerque E.X. Molecular and cellular actions of galantamine: clinical implications for treatment of organophosphorus poisoning. J Mol Neurosci 2010, 40:196-203.
44. Raveh L., Weissman B.A., Cohen G., Alkalay D., Rabinovitz I., Sonego H., et al. Caramiphen and scopolamine prevent soman-induced brain damage and cognitive dysfunction. Neurotoxicology 2002, 23:7-17.
45. Romano J.A., King J.M. Psychological casualties resulting from chemical and biological weapons. Mil Med 2001, 166:21-22.
46. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000, 874:123-130.
47. Shih T.M., Kan R.K., McDonough J.H. In vivo cholinesterase inhibitory specificity of organophosphorus nerve agents. Chem Biol Interact 2005, 157-158:293-303.
48. Silveira C.L., Eldefrawi A.T., Eldefrawi M.E. Putative M2 muscarinic receptors of rat heart have high affinity for organophosphorus anticholinesterases. Toxicol Appl Pharmacol 1990, 103:474-481.
49. Simon P., Dupuis R., Costentin J. Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 1994, 61:59-64.
50. Sweeney J.E., Höhmann C.F., Moran T.H., Coyle J.T. A long-acting cholinesterase inhibitor reverses spatial memory deficits in mice. Pharmacol Biochem Behav 1988, 31:141-147.
51. Sweeney J.E., Bachman E.S., Coyle J.T. Effects of different doses of galanthamine, a long-acting acetylcholinesterase inhibitor, on memory in mice. Psychopharmacology (Berl) 1990, 102:191-200.
52. Taube J.S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 1995, 15:70-86.
53. Treit D., Fundytus M. Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 1988, 31:959-962.
54. Van Dam D., Abramowski D., Staufenbiel M., De Deyn P.P. Symptomatic effect of donepezil, rivastigmine, galantamine and memantine on cognitive deficits in the APP23 model. Psychopharmacology (Berl) 2005, 180:177-190.
55. Van Dam D., De Deyn P.P. Cognitive evaluation of disease-modifying efficacy of galantamine and memantine in the APP23 model. Eur. Neuropsychopharmacol 2006, 16:59-69.
56. Wicke K.M., Rex A., Jongen-Relo A., Groth I., Gross G. The guinea pig forced swim test as a new behavioral despair model to characterize potential antidepressants. Psychopharmacology (Berl) 2007, 195:95-102.
57. Wilber C.G. Some factors which are correlated with swimming capacity in guinea pigs. J Appl Physiol 1959, 14:199-203.
58. Woodruff-Pak D.S., Santos I.S. Nicotinic modulation in an animal model of a form of associative learning impaired in Alzheimer's disease. Behav Brain Res 2000, 113:11-19.
59. Woodruff-Pak D.S., Vogel R.W., Wenk G.L. Galantamine: effect on nicotinic receptor binding, acetylcholinesterase inhibition, and learning. Proc Natl Acad Sci USA 2001, 98:2089-2094.