Effects of subchronic exposure to benzo[a]pyrene (B[a]P) on learning and memory, and neurotransmitters in male Sprague-Dawley rat

NeuroToxicology

Volumn 32, Issue 2, 2011, Pages 188-198

  Xia, Yinyin ^a   Cheng, Shuqun ^a   He, Junlin ^a   Liu, Xueqing ^a   Tang, Yan ^a   Yuan, Haiyan ^a   He, Lijun ^a   Lu, Tao ^a   Tu, Baijie ^a   Wang, Yingxiong ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Benzo a pyrene (B a P); Hippocampus; Neurotransmitter; Rat; Water maze

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; ACETYLCHOLINE; ACETYLCHOLINESTERASE; ADRENALIN; BENZO[A]PYRENE; CHOLINE ACETYLTRANSFERASE; DOPAMINE; MALONALDEHYDE; MONOAMINE; NEUROTRANSMITTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NORADRENALIN; SEROTONIN; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BEHAVIOR DISORDER; CONTROLLED STUDY; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; LATENT PERIOD; LEARNING; LONG TERM EXPOSURE; MALE; MAZE TEST; MEMORY; NEUROTOXICITY; NONHUMAN; POLLUTANT; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; SWIMMING;

ANIMALS; BENZO(A)PYRENE; HIPPOCAMPUS; LEARNING; MALE; MEMORY; NEUROTRANSMITTER AGENTS; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

MAMMALIA; RATTUS;

EID: 79551648770     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2010.12.015     Document Type: Article

References (87)

1. AI-Zahrani S.S., Ho M.Y., Martinz D.N., Cabrera M., Bradshaw C.M., Szabadi E. Effect of destruction of the 5-hydroxytryptaminergic pathways on the acquisition of temporal discrimination and memory for duration in a delayed condition discrimination task. Psychopharmacology 1996, 123:103-110.
2. Altman H.J., Normile H.J. Enhancement of the memory of a previously learned aversive habit following pre-test administration of a variety of serotonergic anatgonists in mice. Psychopharmacology 1986, 90:24-27.
3. Andersson H.E., Lindqvist R., Westerholm K., Gragg J., Almen, Olson L. Neurotoxic effects of fractionated diesel exhausts following microinjections in rat hippocampus and striatum. Environ Res 1998, 76:41-51.
4. ATSDR Toxicological profile for polycyclic aromatic hydrocarbons (PAHs) update 1995, Agency for Toxic Substances and Disease Registry, Atlanta, GA, p. 458.
5. Baldi E., Bucherelli C. The inverted " u-shaped" dose-effect relationships in learning and memory: modulation of arousal and consolidation. Nonlinearity Biol Toxicol Med 2005, 3:9-21.
6. Bouayed J., Desor F., Rammal H., Kiemer A.K., Tybl E., Schroeder H., et al. Effects of lactational exposure to benzo[α]pyrene (B[α]P) on postnatal neurodevelopment, neuronal receptor gene expression and behaviour in mice. Toxicology 2009, 259:97-106.
7. Boussel J., Grova N., Feidt C., Desor D., Rychen G., Schroeder H. Short- and long-term effects of a neonatal exposure to benzo[a]pyrene (BaP) or 3,3′,4,4′,5-pentachlorobiphenyl (PCB126) on behaviour of rat pups. Toxcicol Lett 2006, 164(Suppl. 1):80-81.
8. Brody J.F. Behavioral effects of serotonin depletion and of p-chlorophenylalanine (a serotonin depletor) in rats. Psychopharmacology 1970, 17:14-33.
9. Bucci D.J., Chiba A.A., Gallagher M. Spatial learning in male and female Long-Evans rats. Behav Neurosci 1995, 109:180-183.
10. Canal C.E., Chang Q., Gold P.E. Amnesia produced by altered release of neurotransmitters after intra-amygdala injections of a protein synthesis inhibitor. Proc Natl Acad Sci USA 2007, 104:12500-12505.
11. Cardozo P.F., Song S., Parthasarathy A., Hazzi C., Naidu K., Ramos R.J. Oxidative DNA damage in the aging mouse brain. Mov Disord 1999, 14:972-980.
12. Castellano C., Cabib S., Puglisi-Allegra S. Psychopharmacology of memory modulation: evidence for multiple interaction among neurotransmitters and hormones. Behav Brain Res 1996, 77:1-21.
13. Chang Q., Gold P.E. Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J Neurosci 2003, 23:3001-3005.
14. Cini M., Fariello R.G., Bianchetti A., Moretti A. Studies in lipid peroxidation in the rat brain. Neurochem Res 1994, 19:283-288.
15. Das M., Mukhtar H., Seth P. Distribution of benzo[a]pyrene in discrete regions of the rat brain. Bull Environ Contam Toxicol 1985, 35:500-504.
16. Dayal H., Gupta S., Trieff N., Maierson D., Reich D. Symptom clusters in a community with chronic exposure to chemicals in two superfund sites. Arch Environ Health 1995, 50:108-111.
17. Edwards T.M., Rickard N.S. New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes. Neurosci Biobehav Rev 2007, 31:413-425.
18. Eichenbaum H. How does the brain organize memories?. Science 1997, 277:330-332.
19. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961, 7:88-95.
20. Estall L.B., Grant S.J., Cicala G.A. Inhibition of nitric oxide (NO) production selectively impairs learning and memory in the rat. Pharmacol Biochem Behav 1993, 46:959-962.
21. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annu Rev Psychol 1997, 48:649-684.
22. Fadda F., Cocco S., Stancampiano R. Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport 2000, 11:2265-2269.
23. Gold P.E. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol Learn Mem 2003, 80:194-210.
24. Gold P.E., van Buskirk R. Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behav Biol 1975, 13:145-153.
25. Gold P.E., van Buskirk R. Effects of posttrial hormone injections on memory processes. Horm Behav 1976, 7:509-517.
26. Gold P.E., van Buskirk R. Posttraining brain norepinephrine concentrations: Correlation with retention performance of avoidance training and with peripheral epinephrine modulation of memory processing. Behav Biol 1978, 23:509-520.
27. Gold P.E., van Buskirk R., Haycock J.W. Effects of posttraining epinephrine injections on retention of avoidance training in mice. Behav Biol 1977, 20:197-204.
28. Grova N., Valley A., Turner J.D., Morel A., Muller C.P., Schroeder H. Modulation of behavior and NMDA-R1 gene mRNA expression in adult female mice after sub-acute administration of benzo[a]pyrene. Neurotoxicology 2007, 28:630-636.
29. Grova N., Schroeder H., Farinelle S., Prodhomme E., Valley A., Muller C.P. Sub-acute administration of benzo[a]pyrene (B[a]P) reduces anxiety-related behaviour in adult mice and modulates regional expression of N-methyl-d-aspartate (NMDA) receptors genes in relevant brain regions. Chemosphere 2008, S295-S302.
30. Hestrin S. The reaction of acetylcholine and other carboxylic acid derivatives with hydro-xylamine, and its analytical application. J Biol Chem 1949, 189:249-261.
31. Huber S.J., Shulman H.G., Paulson G.W., Shuttleworth E.C. Dose-dependent memory impairment in Parkinson's disease. Neurology 1989, 39:438-440.
32. IARC Polynuclear aromatic compounds. Part I. Chemical, environmental and experimental data 1983, International Agency for Research on Cancer. IARC Monograph 32, Lyon.
33. Introini-Collison I., Saghafi D., Novack G.D., McGaugh J.L. Memory-enhancing effects of post-training dipivefrin and epinephrine: involvement of peripheral and central adrenergic receptors. Brain Res 1992, 572:81-86.
34. IPCS Selected non-heterocyclic polycyclic aromatic hydrocarbons. International Program on Chemical Safety 1998, World Health Organization, Geneva, p. 175-91.
35. Jayasekara S., Sharma R.P., Drown D.B. Effects of benzo[a]pyrene on steady-state levels of biogenic amines and metabolizing enzymes in mouse brain regions. Ecotoxicol Environ Saf 1992, 24:1-12.
36. Jett D., Navoa R.V., Lyons M. Additive inhibitory action of chlorpyrifos and PAHs on acetylcholinesterase activity in vitro. Toxicol Lett 1999, 105:223-229.
37. Kilburn K.H., Warshaw R.H. Neurotoxic effects from residential exposure to chemicals from an oil reprocessing facility and superfund site. Neurotoxicol Teratol 1995, 17:89-102.
38. Knuckles M.E., Inyang F., Ramesh A. Acute and subchronic oral toxicities of benzo[a]pyrene in F-344 rats. Toxicol Sci 2001, 61:382-388.
39. Konstandi M., Harkitis P., Thermos K., Ogren S.O., Johnson E.O., Tzimas P., et al. Modification of inherent and drug-induced dopaminergic activity after exposure to benzo(alpha)pyrene. Neurotoxicology 2007, 28:860-867.
40. Leadon S.A., Stampfer M.R., Bartley J. Production of oxidative DNA damage during the metabolic activation of benzo[a]pyrene in human mammary epithelial cells correlates with cell killing. Proc Natl Acad Sci USA 1988, 85:4365-4368.
41. Lebel C. Oxygen radicals: common mediators of neurotoxicity. Neurotoxicol Teratol 1991, 13:341-346.
42. Levey A.I., Wainer B.H., Mufson E.J., Mesulam M.M. Co-localization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 1983, 9:9-22.
43. Liang K.C., McGaugh J.L., Yao H.Y. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res 1990, 508:225-233.
44. Liu S.H., Wang J.H., Chuu J.J., Lin-Shiau S.Y. Alterations of motor nerve functions in animals exposed to motorcycle exhaust. J Toxicol Environ Health A 2002, 65:803-812.
45. Louin G., Besson V.C., Royo N.C., Bonnefont-Rousselot D., Marchand-Verrecchia C., Plotkine M., et al. Cortical calcium increase following traumatic brain injury represents a pitfall in the evaluation of Ca2+-independent NOS activity. J Neurosci Methods 2004, 138:73-79.
46. Lowry O.H., Rosenbrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
47. Majchrzak R., Sroczynski J., Chelmecka E. Evaluation of the nervous system in workers in the furnace and coal divisions of the coke-producing plants. Med Pr 1990, 41:108-113.
48. Markovits P., Maunoury R., Tripier M.F., Coulomb B., Levy S., Papadopoulo D., et al. Normal and benzo[a]pyrene-transformed fetal mouse brain cells: I. Tumorigenicity and immunochemical detection of glial fibrillary acidic protein. Arch Neuropathol 1979, 47:197-203.
49. McEntee W.J., Crook T.H. Serotonin, memory, and the aging brain. Psychopharmacology 1991, 103:143-149.
50. Mohapel P., Leanza G., Kokaia M., Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging 2005, 26:939-946.
51. Moir D., Viau A., Chu I., Withey J., McMullen E. Pharmacokinetics of benzo[a]pyrene in the rat. J Toxicol Environ Health 1998, 53:507-530.
52. Molinengo L., Ghi P. Behavioral and neurochemical effects induced by subchronic l-deprenyl administration. Pharmacol Biochem Behav 1997, 58:649-655.
53. Morice E., Billard J.M., Denis C., Mathieu F., Betancur C., Epelbaum J., et al. Parallel loss of hippocampal LTD and cognitive flexibility in a genetic model of hyperdopaminergia. Neuropsychopharmacology 2007, 32:2108-2116.
54. Morris R.G.M. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11:47-60.
55. Morris R.G.M., Garrud P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
56. Moser E.I., Kropf E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 2008, 31:69.
57. Mössner R., Schmitt A., Syagailo Y., Gerlach M., Riederer P., Lesch K.P. The serotonin transporter in Alzheimer's and Parkinson's disease. J Neural Transm (Suppl.) 2000, 60:345-350.
58. Muir J.L., Page K.J., Sirinathsinghji D.J.S., Robbins T.W., Everitt B.J. Excitotoxic lesions of basal forebrain cholinergic neurons: effects on learning, memory and attention. Behav Brain Res 1993, 57:123-131.
59. Murphy B.L., Arnsten A.F.T., Goldman-Rakic P.S., Roth R.H. Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proc Natl Acad Sci USA 1996, 93:1325-1329.
60. Myslivecek J., Hassmannova J., Barcal J., Safanda J., Zalud V. Inhibitory learning and memory in newborn rats influenced by nitric oxide. Neuroscience 1996, 71:299-312.
61. Myslivecek J., Safanda J., Hassmannova J. The role of nitric oxide in the very early learning and memory. Studia Psychol 1994, 36:327-329.
62. Nie J.S., Zhao J., Zhang H.M., Niu Q. Effects of benro[a]pyrene on learning and memory and the content of monoamine neurotransmitters in rats. Wei Sheng Yan Jiu 2008, 37:517-520.
63. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-358.
64. O'Keefe J. Do hippocampal pyramidal cells signal non-spatial as well as spatial information?. Hippocampus 1999, 9:352-364.
65. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Oxford University Press.
66. Oyanagui Y. Reevaluation of assay methods and establishment of kit for super-oxide dismutase activity. Anal Biochem 1984, 142:290-296.
67. Prado-Alcala R.A., Ruiloba M.I., Rubio L., Solana-Figueroa R., Medina C., Salado-Castillo R., et al. Regional infusions of serotonin into the striatum and memory consolidation. Synapse 2003, 47:169-175.
68. Qi Z., Gold P.E. Intrahippocampal infusions of anisomycin produce amnesia: contribution of increased release of norepinephrine, dopamine, and acetylcholine. Learn Mem 2009, 16:308-314.
69. Rolls E.T. Memory systems in the brain. Annu Rev Psychol 2000, 51:599-630.
70. Saunders C.R., Shockley D.C., Knuckles M.E. Behavioral effects induced by acute exposure to benzo[a]pyrene in F-344 rats. Neurotoxicol Res 2001, 3:557-579.
71. Saunders C.R., Ramesh A., Shockley D.C. Modulation of neurotoxic behavior in F-344 rats by temporal disposition of benzo[a]pyrene. Toxicol Lett 2002, 129:33-45.
72. Saunders C.R., Shockley D.C., Knuckles M.E. Fluoranthene-induced neurobehavioral toxicity in F-344 rats. Int J Toxicol 2003, 22:263-276.
73. Saunders C.R., Das S.K., Ramesh A., Shockley D., Mukherjee S. Benzo[a]pyrene-induced acute neurotoxicity in the F-344 rat: role of oxidative stress. J Appl Toxicol 2006, 26:427-438.
74. Snyder S.H. Nitric oxide: first in a new class of neurotransmitters. Science 1992, 257(5069):494-496.
75. Stephanou P., Konstandi M., Pappas P., Marselos M. Alterations in central monoaminergic neurotransmission induced by polycyclic aromatic hydrocarbons in rats. Eur J Drug Metab Pharmacokinet 1998, 23:475-481.
76. Stewart C.A., Morris R.G.M. The watermaze. Behavioural neuroscience. A practical approach 1993, vol. 1:107-122. IRL Press, Oxford.
77. Stuehr D.J., Know N.S., Gross S.S. Synthesis of nitrogen oxides from l-arginine by macrophage cytosol: requirement for inducible and constitutive components. Biochem Biophys Res Commun 1989, 161:420-426.
78. Szczeklik A., Szczeklik J., Galuszka Z., Musial J., Kolarzyk E., Targosz D. Humoral immunosuppression in men exposed to polycyclic aromatic hydrocarbons and related carcinogens in polluted environments. Environ Health Perspect 1994, 102:302-304.
79. Tu B.J., Chen S., Xiao C.F. Study on neurotoxicity of benzo[a]pyrene in mice by microscope, electron-microscope and behavioral methods. Ind Health Occup Dis 2002, 28:94-98.
80. Valzelli L., Pawlowski L. Effect of p-chlorophenylalanine on avoidance learning of two differentially housed mouse strains. Neuropsychobiology 1979, 5:121-128.
81. Vincent S.R. Nitric oxide: a radical neurotransmitter in the central nervous system. Prog Neurobiol 1994, 42:129-160.
82. Wetzel W., Getsova V.M., Jork R., Matthies H. Effect of serotonin on Y-maze retention and hippocampal protein synthesis in rats. Phrmacol Biochem Behav 1980, 12:319-322.
83. Whishaw I.Q., Tomie J.A. Cholinergic receptor blockade produces impairments in a sensorimotor subsystem for place navigation in the rat: evidence from sensory, motor and acquisition tests in a swimming pool. Behav Neurosci 1987, 101:603-616.
84. Wolfgram F. Spectrophotometric assay for cholineacetyltransferase. Anal Biochem 1972, 46:114.
85. Wormley D.D., Chirwa S., Nayyar T., Wu J., Johnson S., Brown L.A., et al. Inhaled benzo[a]pyrene impairs long-term potentiation in the F1 generation rat dentate gyrus. Cell Mol Biol 2004, 50:715-721.
86. Wormley D.D., Ramesh A., Hood D.B. Environmental contaminant-mixture effects on CNS development, plasticity, and behavior. Toxicol Appl Pharmacol 2004, 197:49-65.
87. Wu J., Nayyar T., Tu S., Johnson S., Greenwood M., Hood D.B. Benzo[a]pyrene and dioxin induced downregulation of hippocampal NMDAR1 expression and deficits in fixed-ratio performance in F1generation rats. Toxicol 2003, 72(Suppl. 1):125.