Early postnatal nicotine exposure causes hippocampus-dependent memory impairments in adolescent mice: Association with altered nicotinic cholinergic modulation of LTP, but not impaired LTP

Neurobiology of Learning and Memory - Tập 118 - Trang 178-188 - 2015
Sakura Nakauchi1, Melissa Malvaez1, Hailing Su1, Elise Kleeman1, Richard Dang1, Marcelo A. Wood1, Katumi Sumikawa1
1Department of Neurobiology and Behavior, University of California Irvine, Irvine, CA 92697-4550, USA

Tài liệu tham khảo

Adams, 2002, Development of the alpha7 nicotinic cholinergic receptor in rat hippocampal formation, Brain Research Developmental Brain Research, 139, 175, 10.1016/S0165-3806(02)00547-3 Ankarberg, 2001, Neurobehavioural defects in adult mice neonatally exposed to nicotine: Changes in nicotine-induced behaviour and maze learning performance, Behavioural Brain Research, 123, 185, 10.1016/S0166-4328(01)00207-8 Assini, 2009, Object location memory in mice: Pharmacological validation and further evidence of hippocampal CA1 participation, Behavioural Brain Research, 204, 206, 10.1016/j.bbr.2009.06.005 Bannerman, 2004, Regional dissociations within the hippocampus–memory and anxiety, Neuroscience and Biobehavioral Reviews, 28, 273, 10.1016/j.neubiorev.2004.03.004 Barrett, 2011, Hippocampal focal knockout of CBP affects specific histone modifications, long-term potentiation, and long-term memory, Neuropsychopharmacology, 36, 1545, 10.1038/npp.2011.61 Batstra, 2003, Effect of antenatal exposure to maternal smoking on behavioural problems and academic achievement in childhood: Prospective evidence from a Dutch birth cohort, Early Human Development, 75, 21, 10.1016/j.earlhumdev.2003.09.001 Britton, 2007, Perinatal nicotine exposure eliminates peak in nicotinic acetylcholine receptor response in adolescent rats, The Journal of Pharmacology and Experimental Therapeutics, 320, 871, 10.1124/jpet.106.112730 Bruin, 2010, Long-term consequences of fetal and neonatal nicotine exposure: A critical review, Toxicological Sciences, 116, 364, 10.1093/toxsci/kfq103 Cutler, 1996, Prenatal cocaine and/or nicotine exposure in rats: Preliminary findings on long-term cognitive outcome and genital development at birth, Neurotoxicology and Teratology, 18, 635, 10.1016/S0892-0362(96)00125-0 Damborsky, 2012, Chronic neonatal nicotine exposure increases excitation in the young adult rat hippocampus in a sex-dependent manner, Brain Research, 1430, 8, 10.1016/j.brainres.2011.10.039 Danglot, 2006, The development of hippocampal interneurons in rodents, Hippocampus, 16, 1032, 10.1002/hipo.20225 de Graaf-Peters, 2006, Ontogeny of the human central nervous system: What is happening when?, Early Human Development, 82, 257, 10.1016/j.earlhumdev.2005.10.013 Dwyer, 2009, The dynamic effects of nicotine on the developing brain, Pharmacology & Therapeutics, 122, 125, 10.1016/j.pharmthera.2009.02.003 Eppolito, 2006, Long-term behavioral and developmental consequences of pre- and perinatal nicotine, Pharmacology, Biochemistry, and Behavior, 85, 835, 10.1016/j.pbb.2006.11.020 Eriksson, 2000, Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nicotinic receptors and in behaviour of adult mice, Brain Research, 853, 41, 10.1016/S0006-8993(99)02231-3 Fried, 2003, Differential effects on cognitive functioning in 13- to 16-year-olds prenatally exposed to cigarettes and marihuana, Neurotoxicology and Teratology, 25, 427, 10.1016/S0892-0362(03)00029-1 Gu, 2012, Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity, The Journal of Neuroscience, 32, 12337, 10.1523/JNEUROSCI.2129-12.2012 Gu, 2011, Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity, Neuron, 71, 155, 10.1016/j.neuron.2011.04.026 Haettig, 2013, Cell-type specific inactivation of hippocampal CA1 disrupts location-dependent object recognition in the mouse, Learning & Memory, 20, 139, 10.1101/lm.027847.112 Halff, 2014, A novel mechanism for nicotinic potentiation of glutamatergic synapses, The Journal of Neuroscience, 34, 2051, 10.1523/JNEUROSCI.2795-13.2014 Huang, 2007, Chronic neonatal nicotine increases anxiety but does not impair cognition in adult rats, Behavioral Neuroscience, 121, 1342, 10.1037/0735-7044.121.6.1342 Huang, 2006, Chronic neonatal nicotine upregulates heteromeric nicotinic acetylcholine receptor binding without change in subunit mRNA expression, Brain Research, 1113, 94, 10.1016/j.brainres.2006.06.084 Ishibashi, 2014, Nicotinic and muscarinic agonists and acetylcholinesterase inhibitors stimulate a common pathway to enhance GluN2B-NMDAR responses, Proceedings of the National Academy of Sciences of the United States of America, 111, 12538, 10.1073/pnas.1408805111 Ishii, 2005, Comparison of alpha2 nicotinic acetylcholine receptor subunit mRNA expression in the central nervous system of rats and mice, The Journal of Comparative Neurology, 493, 241, 10.1002/cne.20762 Ji, 2001, Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity, Neuron, 31, 131, 10.1016/S0896-6273(01)00332-4 Kenney, 2008, Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine, Molecular Neurobiology, 38, 101, 10.1007/s12035-008-8037-9 Kjelstrup, 2002, Reduced fear expression after lesions of the ventral hippocampus, Proceedings of the National Academy of Sciences of the United States of America, 99, 10825, 10.1073/pnas.152112399 Levin, 1993, Chronic nicotinic stimulation and blockade effects on working memory, Behavioural Pharmacology, 4, 179, 10.1097/00008877-199304000-00010 Liu, 2006, Sequential interplay of nicotinic and GABAergic signaling guides neuronal development, Science, 314, 1610, 10.1126/science.1134246 Liu, 2007, Role of endogenous nicotinic signaling in guiding neuronal development, Biochemical Pharmacology, 74, 1112, 10.1016/j.bcp.2007.05.022 Maggi, 2003, Nicotine activates immature “silent” connections in the developing hippocampus, Proceedings of the National Academy of Sciences of the United States of America, 100, 2059, 10.1073/pnas.0437947100 Maggi, 2004, Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus, The Journal of Physiology, 559, 863, 10.1113/jphysiol.2004.067041 Mahar, 2012, Developmental hippocampal neuroplasticity in a model of nicotine replacement therapy during pregnancy and breastfeeding, PLos One, 7, e37219, 10.1371/journal.pone.0037219 McNew, 1966, Role of the limbic system in active and passive avoidance conditioning in the rat, Journal of Comparative and Physiological Psychology, 61, 173, 10.1037/h0023127 McQuown, 2011, HDAC3 is a critical negative regulator of long-term memory formation, The Journal of Neuroscience, 31, 764, 10.1523/JNEUROSCI.5052-10.2011 Miao, 1998, Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain, Journal of Neurochemistry, 70, 752, 10.1046/j.1471-4159.1998.70020752.x Moscarello, 2013, Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions, The Journal of Neuroscience, 33, 3815, 10.1523/JNEUROSCI.2596-12.2013 Moses, 2005, Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships, Brain Research Bulletin, 67, 62, 10.1016/j.brainresbull.2005.05.026 Naeff, 1992, Pre- and postnatal development of high-affinity [3H]nicotine binding sites in rat brain regions: An autoradiographic study, Brain Research Developmental Brain Research, 68, 163, 10.1016/0165-3806(92)90058-5 Nakauchi, 2007, Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2∗ nicotinic ACh receptors, The European Journal of Neuroscience, 25, 2666, 10.1111/j.1460-9568.2007.05513.x Nakauchi, 2012, Endogenously released ACh and exogenous nicotine differentially facilitate long-term potentiation induction in the hippocampal CA1 region of mice, The European Journal of Neuroscience, 35, 1381, 10.1111/j.1460-9568.2012.08056.x Narayanan, 2002, Nicotinic receptor expression following nicotine exposure via maternal milk, Neuroreport, 13, 961, 10.1097/00001756-200205240-00012 Norman, 2004, Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions, Behavioural Brain Research, 148, 79, 10.1016/S0166-4328(03)00176-1 Pauly, 2008, Maternal tobacco smoking, nicotine replacement and neurobehavioural development, Acta Paediatrica, 97, 1331, 10.1111/j.1651-2227.2008.00852.x Portugal, 2012, Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning, Neurobiology of Learning and Memory, 97, 482, 10.1016/j.nlm.2012.04.003 Posadas, 2013, Nicotinic receptors in neurodegeneration, Current Neuropharmacology, 11, 298, 10.2174/1570159X11311030005 Roozendaal, 2010, Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification, The Journal of Neuroscience, 30, 5037, 10.1523/JNEUROSCI.5717-09.2010 Seress, 2007, Comparative anatomy of the hippocampal dentate gyrus in adult and developing rodents, non-human primates and humans, Progress in Brain Research, 163, 23, 10.1016/S0079-6123(07)63002-7 Seress, 2001, Cell formation in the human hippocampal formation from mid-gestation to the late postnatal period, Neuroscience, 105, 831, 10.1016/S0306-4522(01)00156-7 Shacka, 1998, Exposure to prenatal nicotine transiently increases neuronal nicotinic receptor subunit alpha7, alpha4 and beta2 messenger RNAs in the postnatal rat brain, Neuroscience, 84, 1151, 10.1016/S0306-4522(97)00564-2 Son, 2006, Postnatal expression of alpha2 nicotinic acetylcholine receptor subunit mRNA in developing cortex and hippocampus, Journal of Chemical Neuroanatomy, 32, 179, 10.1016/j.jchemneu.2006.09.001 Sorenson, 1991, The effects of prenatal nicotine on radial-arm maze performance in rats, Pharmacology, Biochemistry, and Behavior, 40, 991, 10.1016/0091-3057(91)90117-K Stefanko, 2009, Modulation of long-term memory for object recognition via HDAC inhibition, Proceedings of the National Academy of Sciences of the United States of America, 106, 9447, 10.1073/pnas.0903964106 Tominaga, 2000, Quantification of optical signals with electrophysiological signals in neural activities of Di-4-ANEPPS stained rat hippocampal slices, Journal of Neuroscience Methods, 102, 11, 10.1016/S0165-0270(00)00270-3 Tong, 2013, Trends in smoking before, during, and after pregnancy–pregnancy risk assessment monitoring system, United States, 40 sites, 2000–2010, Morbidity and Mortality Weekly Report Surveillance Summaries, 62, 1 Tribollet, 2004, Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: An autoradiographic study in the rat brain, Neuroscience, 124, 405, 10.1016/j.neuroscience.2003.09.028 Vaglenova, 2004, An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure, Behavioural Brain Research, 150, 159, 10.1016/j.bbr.2003.07.005 Vogel-Ciernia, 2013, The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory, Nature Neuroscience, 16, 552, 10.1038/nn.3359 Wada, 1989, Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization histochemical study in the rat, The Journal of Comparative Neurology, 284, 314, 10.1002/cne.902840212 Winzer-Serhan, 2005, Expression of alpha5 nicotinic acetylcholine receptor subunit mRNA during hippocampal and cortical development, The Journal of Comparative Neurology, 481, 19, 10.1002/cne.20357 Yamazaki, 2005, Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction, The European Journal of Neuroscience, 22, 845, 10.1111/j.1460-9568.2005.04259.x Yamazaki, 2006, Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus, The European Journal of Neuroscience, 23, 1819, 10.1111/j.1460-9568.2006.04714.x Yanai, 1992, Alterations in hippocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine, Brain Research Bulletin, 29, 363, 10.1016/0361-9230(92)90069-A Zoli, 1995, Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems, The Journal of Neuroscience, 15, 1912, 10.1523/JNEUROSCI.15-03-01912.1995