Protective role of noradrenaline in benzo[a]pyrene-induced learning impairment in developing rat

Journal of Neuroscience Research

Volumn 91, Issue 11, 2013, Pages 1450-1462

  Patri, Manorama ^a,b   Singh, Abhishek ^a   Mallick, Birendra Nath ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b RAVENSHAW UNIVERSITY   (India)

Author keywords

Brain development; Calcium; Carcinogen; Intracisternal injection; Neuron glia interaction; Neurotoxicity; NMDA receptor subunits

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NORADRENALIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BENZO[A]PYRENE INDUCED LEARNING IMPAIRMENT; CELL LINE; CONTROLLED STUDY; DENSITY; GLIA; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; LEARNING; LEARNING DISORDER; MALE; MAZE TEST; MEMORY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT;

BRAIN DEVELOPMENT; CALCIUM; CARCINOGEN; INTRACISTERNAL INJECTION; NEURON-GLIA INTERACTION; NEUROTOXICITY; NMDA RECEPTOR SUBUNITS;

ANIMALS; BENZO(A)PYRENE; BRAIN; CARCINOGENS; IMMUNOHISTOCHEMISTRY; LEARNING; MALE; MEMORY; NEURONS; NOREPINEPHRINE; RATS; RATS, WISTAR;

EID: 84884717255     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23265     Document Type: Article

References (61)

1. ATSDR. 1995. Toxicological profile for polycyclic aromatic hydrocarbons (PAHs). Atlanta: U.S. Department of Health and Human Services.
2. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
3. Bouayed J, Desor F, Rammal H, Kiemer AK, Tybl E, Schroeder H, Rychen G, Soulimani R. 2009. Effects of lactational exposure to benzo[alpha]pyrene (B[alpha]P) on postnatal neurodevelopment, neuronal receptor gene expression and behaviour in mice. Toxicology 259:97-106.
4. Breese GR, Traylor TD. 1972. Developmental characteristics of brain catecholamines and tyrosine hydroxylase in the rat: effects of 6-hydroxydopamine. Br J Pharmacol 44:210-222.
5. Brown LA, Khousbouei H, Goodwin JS, Irvin-Wilson CV, Ramesh A, Sheng L, McCallister MM, Jiang GC, Aschner M, Hood DB. 2007. Downregulation of early ionotrophic glutamate receptor subunit developmental expression as a mechanism for observed plasticity deficits following gestational exposure to benzo(a)pyrene. Neurotoxicology 28:965-978.
6. Burgess N. 2002. The hippocampus, space, and viewpoints in episodic memory. Q J Exp Psychol A 55:1057-1080.
7. Chen C, Tang Y, Jiang X, Qi Y, Cheng S, Qiu C, Peng B, Tu B. 2012. Early postnatal benzo(a)pyrene exposure in Sprague-Dawley rats causes persistent neurobehavioral impairments that emerge postnatally and continue into adolescence and adulthood. Toxicol Sci 125:248-261.
8. Choi DW. 1988. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11:465-469.
9. Colgin LL, Moser EI, Moser MB. 2008. Understanding memory through hippocampal remapping. Trends Neurosci 31:469-477.
10. Cull-Candy S, Brickley S, Farrant M. 2001. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
11. Das G, Gopalakrishnan A, Faisal M, Mallick BN. 2008. Stimulatory role of calcium in rapid eye movement sleep deprivation-induced noradrenaline-mediated increase in Na-K-ATPase activity in rat brain. Neuroscience 155:76-89.
12. Das M, Seth PK, Mukhtar H. 1985. Distribution of benzo(a)pyrene in discrete regions of rat brain. Bull Environ Contam Toxicol 35:500-504.
13. Dudai Y. 2004. The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51-86.
14. Dutta K, Ghosh D, Nazmi A, Kumawat KL, Basu A. 2010. A common carcinogen benzo[a]pyrene causes neuronal death in mouse via microglial activation. PLoS One 5:e9984.
15. Dygalo NN, Iushkova AA, Kalinina TS, Surnina N, Mel'nikova LB, Shishkina GT. 2000. The ontogenetic correlations of noradrenaline level and adrenergic receptor density in the rat brain. Ontogenez 31:53-56.
16. Eichenbaum H. 1997. How does the brain organize memories? Science 277:330-332.
17. Fellin T, Pascual O, Haydon PG. 2006. Astrocytes coordinate synaptic networks: balanced excitation and inhibition. Physiology 21:208-215.
18. Gold PE, McGaugh JL. 1977. Hormones and memory. Adv Biochem Psychopharmacol 17:127-143.
19. Gold PE, Van Buskirk RB. 1975. Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behav Biol 13:145-153.
20. Good M, Honey RC. 1997. Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111:487-493.
21. Grova N, Valley A, Turner JD, Morel A, Muller CP, Schroeder H. 2007. Modulation of behavior and NMDA-R1 gene mRNA expression in adult female mice after sub-acute administration of benzo(a)pyrene. Neurotoxicology 28:630-636.
22. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
23. Hack M, Breslau N, Weissman B, Aram D, Klein N, Borawski E. 1991. Effect of very low birth weight and subnormal head size on cognitive abilities at school age. N Engl J Med 325:231-237.
24. Ishido M, Masuo Y, Sayato-Suzuki J, Oka S, Niki E, Morita M. 2004. Dicyclohexylphthalate causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity. J Neurochem 91:69-76.
25. Ivanov A, Pellegrino C, Rama S, Dumalska I, Salyha Y, Ben-Ari Y, Medina I. 2006. Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons. J Physiol 572:789-798.
26. Kennedy MB. 1989. Regulation of neuronal function by calcium. Trends Neurosci 12:417-420.
27. Konstandi M, Lang MA, Kostakis D, Johnson EO, Marselos M. 2008. Predominant role of peripheral catecholamines in the stress-induced modulation of CYP1A2 inducibility by benzo(alpha)pyrene. Basic Clin Pharmacol Toxicol 102:35-44.
28. Le Ferrec E, Lagadic-Gossmann D, Rauch C, Bardiau C, Maheo K, Massiere F, Le Vee M, Guillouzo A, Morel F. 2002. Transcriptional induction of CYP1A1 by oltipraz in human Caco-2 cells is aryl hydrocarbon receptor- and calcium-dependent. J Biol Chem 277:24780-24787.
29. Liang KC, McGaugh JL, Yao HY. 1990. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res 508:225-233.
30. Liu Y, Zhang J. 2000. Recent development in NMDA receptors. Chin Med J (Engl) 113:948-956.
31. Majumdar S, Mallick BN. 2003. Increased levels of tyrosine hydroxylase and glutamic acid decarboxylase in locus coeruleus neurons after rapid eye movement sleep deprivation in rats. Neurosci Lett 338:193-196.
32. Majumdar S, Faisal M, Madan V, Mallick BN. 2003. Increased turnover of Na-K ATPase molecules in rat brain after rapid eye movement sleep deprivation. J Neurosci Res 73:870-875.
33. Mallick BN, Singh A. 2011. REM sleep loss increases brain excitability: role of noradrenaline and its mechanism of action. Sleep Med Rev 15:165-178.
34. Mallick BN, Singh A, Khanday MA. 2012. Activation of inactivation process initiates rapid eye movement sleep. Prog Neurobiol 97:259-276.
35. Mao W, Qin F, Iwai C, Vulapalli R, Keng PC, Liang CS. 2004. Extracellular norepinephrine reduces neuronal uptake of norepinephrine by oxidative stress in PC12 cells. Am J Physiol Heart Circ Physiol 287:H29-H39.
36. McCallister MM, Maguire M, Ramesh A, Aimin Q, Liu S, Khoshbouei H, Aschner M, Ebner FF, Hood DB. 2008. Prenatal exposure to benzo(a)pyrene impairs later-life cortical neuronal function. Neurotoxicology 29:846-854.
37. Mitchell CE. 1982. Distribution and retention of benzo(A)pyrene in rats after inhalation. Toxicol Lett 11:35-42.
38. Morris R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
39. O'Keefe J, Nadel L. 1978. The hippocarnpus as a cognitive map. Oxford: Clarendon Press.
40. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
41. Perera FP, Rauh V, Tsai WY, Kinney P, Camann D, Barr D, Bernert T, Garfinkel R, Tu YH, Diaz D, Dietrich J, Whyatt RM. 2003. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect 111:201-205.
42. Perera FP, Rauh V, Whyatt RM, Tang D, Tsai WY, Bernert JT, Tu YH, Andrews H, Barr DB, Camann DE, Diaz D, Dietrich J, Reyes A, Kinney PL. 2005. A summary of recent findings on birth outcomes and developmental effects of prenatal ETS, PAH, and pesticide exposures. Neurotoxicology 26:573-587.
43. Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, Diaz D, Hoepner L, Barr D, Tu YH, Camann D, Kinney P. 2006. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect 114:1287-1292.
44. Persson E, Larsson P, Tjalve H. 2002. Cellular activation and neuronal transport of intranasally instilled benzo(a)pyrene in the olfactory system of rats. Toxicol Lett 133:211-219.
45. 2+ transport and ryanodine receptor function. Mol Pharmacol 59:506-513.
46. Porkka-Heiskanen T, Smith SE, Taira T, Urban JH, Levine JE, Turek FW, Stenberg D. 1995. Noradrenergic activity in rat brain during rapid eye movement sleep deprivation and rebound sleep. Am J Physiol 268:R1456-R1463.
47. Rauh VA, Whyatt RM, Garfinkel R, Andrews H, Hoepner L, Reyes A, Diaz D, Camann D, Perera FP. 2004. Developmental effects of exposure to environmental tobacco smoke and material hardship among inner-city children. Neurotoxicol Teratol 26:373-385.
48. Rice D, Barone S Jr. 2000. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511-533.
49. Riedel G, Platt B, Micheau J. 2003. Glutamate receptor function in learning and memory. Behav Brain Res 140:1-47.
50. Sara SJ. 2009. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10:211-223.
51. Saunders CR, Shockley DC, Knuckles ME. 2001. Behavioral effects induced by acute exposure to benzo(a)pyrene in F-344 rats. Neurotox Res 3:557-579.
52. Saunders CR, Das SK, Ramesh A, Shockley DC, Mukherjee S. 2006. Benzo(a)pyrene-induced acute neurotoxicity in the F-344 rat: role of oxidative stress. J Appl Toxicol 26:427-438.
53. Shaywitz BA, Teicher MH, Cohen DJ, Anderson GM, Young JG, Levitt P. 1984. Dopaminergic but not noradrenergic mediation of hyperactivity and performance deficits in the developing rat pup. Psychopharmacology 82:73-77.
54. Tanaka M, Yoshida M, Emoto H, Ishii H. 2000. Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies. Eur J Pharmacol 405:397-406.
55. Troadec JD, Marien M, Darios F, Hartmann A, Ruberg M, Colpaert F, Michel PP. 2001. Noradrenaline provides long-term protection to dopaminergic neurons by reducing oxidative stress. J Neurochem 79:200-210.
56. Trump BF, Berezesky IK. 1995. Calcium-mediated cell injury and cell death. FASEB J 9:219-228.
57. Tully K, Bolshakov VY. 2010. Emotional enhancement of memory: how norepinephrine enables synaptic plasticity. Mol Brain 3:15.
58. Wenzel A, Fritschy JM, Mohler H, Benke D. 1997. NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68:469-478.
59. Wormley DD, Chirwa S, Nayyar T, Wu J, Johnson S, Brown LA, Harris E, Hood DB. 2004a. Inhaled benzo(a)pyrene impairs long-term potentiation in the F1 generation rat dentate gyrus. Cell Mol Biol 50:715-721.
60. Wormley DD, Ramesh A, Hood DB. 2004b. Environmental contaminant-mixture effects on CNS development, plasticity, and behavior. Toxicol Appl Pharmacol 197:49-65.
61. Xia Y, Cheng S, He J, Liu X, Tang Y, Yuan H, He L, Lu T, Tu B, Wang Y. 2011. Effects of subchronic exposure to benzo[a]pyrene (B[a]P) on learning and memory, and neurotransmitters in male Sprague-Dawley rat. Neurotoxicology 32:188-198.