Chronic nicotine improves cognitive and social impairment in mice overexpressing wild type α-synuclein

Abbott, 2007, Bowel movement frequency in late-life and incidental Lewy bodies, Mov. Disord., 22, 1581, 10.1002/mds.21560 Anderson, 2013, Social problem solving, social cognition, and mild cognitive impairment in Parkinson's disease, Behav. Neurosci., 127, 184, 10.1037/a0030250 Barker, 2009, Critical role of the cholinergic system for object-in-place associative recognition memory, Learn. Mem., 16, 8, 10.1101/lm.1121309 Bassetti, 2011, Nonmotor disturbances in Parkinson's disease, Neurodegener. Dis., 8, 95, 10.1159/000316613 Bitner, 2010, In vivo pharmacological characterization of a novel selective α7 neuronal nicotinic acetylcholine receptor agonist ABT-107: preclinical considerations in Alzheimer's disease, J. Pharmacol. Exp. Ther., 334, 875, 10.1124/jpet.110.167213 Bloch, 2006, α-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects, Neuropathol. Appl. Neurobiol., 32, 284, 10.1111/j.1365-2990.2006.00727.x Boess, 2013, Pharmacological and behavioral profile of N-[(3R)-1-azabicyclo[2.2.2]oct-3-yl]-6-chinolincarboxamide (EVP-5141), a novel α7 nicotinic acetylcholine receptor agonist/serotonin 5-HT3 receptor antagonist, Psychopharmacology, 227, 1, 10.1007/s00213-012-2933-4 Bohnen, 2009, Cholinergic denervation occurs early in Parkinson disease, Neurology, 73, 256, 10.1212/WNL.0b013e3181b0bd3d Bohnen, 2015, Frequency of cholinergic and caudate nucleus dopaminergic deficits across the predemented cognitive spectrum of Parkinson disease and evidence of interaction effects, JAMA Neurol., 72, 194, 10.1001/jamaneurol.2014.2757 Botton, 2010, Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice, Behav. Brain Res., 214, 254, 10.1016/j.bbr.2010.05.034 Braak, 2003, Staging of brain pathology related to sporadic Parkinson's disease, Neurobiol. Aging, 24, 197, 10.1016/S0197-4580(02)00065-9 Braak, 2006, Gastric α-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology, Neurosci. Lett., 396, 67, 10.1016/j.neulet.2005.11.012 Chaudhuri, 2011, Parkinson's disease: the non-motor issues, Parkinsonism Relat. Disord., 17, 717, 10.1016/j.parkreldis.2011.02.018 Checkoway, 2002, Parkinson's disease risks associated with cigarette smoking, alcohol consumption, and caffeine intake, Am. J. Epidemiol., 155, 732, 10.1093/aje/155.8.732 Chesselet, 2011, Modelling of Parkinson's disease in mice, Lancet Neurol., 10, 1108, 10.1016/S1474-4422(11)70227-7 Chesselet, 2012, A progressive mouse model of Parkinson's disease: the Thy1-aSyn ("Line 61") mice, Neurotherapeutics, 9, 297, 10.1007/s13311-012-0104-2 Clemens, 1995, The short-term effect of nicotine chewing gum in patients with Parkinson's disease, Psychopharmacology, 117, 253, 10.1007/BF02245195 Costa, 2001, Nicotine prevents striatal dopamine loss produced by 6-hydroxydopamine lesion in the substantia nigra, Brain Res., 888, 336, 10.1016/S0006-8993(00)03087-0 de Bruin, 2006, Beneficial effects of galantamine on performance in the object recognition task in Swiss mice: deficits induced by scopolamine and by prolonging the retention interval, Pharmacol. Biochem. Behav., 85, 253, 10.1016/j.pbb.2006.08.007 Edwards, 2010, Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease, Ann. Hum. Genet., 74, 97, 10.1111/j.1469-1809.2009.00560.x Emre, 2004, Rivastigmine for dementia associated with Parkinson's disease, N. Engl. J. Med., 351, 2509, 10.1056/NEJMoa041470 Everitt, 1997, Central cholinergic systems and cognition, Annu. Rev. Psychol., 48, 649, 10.1146/annurev.psych.48.1.649 Fernagut, 2007, Behavioral and histopathological consequences of paraquat intoxication in mice: effects of α-synuclein over-expression, Synapse, 61, 991, 10.1002/syn.20456 Feuerbach, 2009, The selective nicotinic acetylcholine receptor α7 agonist JN403 is active in animal models of cognition, sensory gating, epilepsy and pain, Neuropharmacology, 56, 254, 10.1016/j.neuropharm.2008.08.025 Fleming, 2004, Early and progressive sensorimotor anomalies in mice overexpressing wild-type human α-synuclein, J. Neurosci., 24, 9434, 10.1523/JNEUROSCI.3080-04.2004 Fleming, 2008, Olfactory deficits in mice overexpressing human wildtype α-synuclein, Eur. J. Neurosci., 28, 247, 10.1111/j.1460-9568.2008.06346.x Fleming, 2011, A pilot trial of the microtubule-interacting peptide (NAP) in mice overexpressing α-synuclein shows improvement in motor function and reduction of α-synuclein inclusions, Mol. Cell. Neurosci., 46, 597, 10.1016/j.mcn.2010.12.011 Fujita, 2006, Widespread decrease of nicotinic acetylcholine receptors in Parkinson's disease, Ann. Neurol., 59, 174, 10.1002/ana.20688 Gee, 2017, First in human trial of a type I positive allosteric modulator of α7-nicotinic acetylcholine receptors: pharmacokinetics, safety, and evidence for neurocognitive effect of AVL-3288, J. Psychopharmacol., 31, 434, 10.1177/0269881117691590 Gorell, 1999, Smoking and Parkinson's disease: a dose-response relationship, Neurology, 52, 115, 10.1212/WNL.52.1.115 Grace, 2009, A double-blind comparison of galantamine hydrobromide ER and placebo in Parkinson disease, J. Neurol. Neurosurg. Psychiatry, 80, 18, 10.1136/jnnp.2008.144048 Hambsch, 2014, Chronic nicotine improves short-term memory selectively in a G72 mouse model of schizophrenia, Br. J. Pharmacol., 171, 1758, 10.1111/bph.12578 Hanagasi, 2017, Dementia in Parkinson's disease, J. Neurol. Sci., 374, 26, 10.1016/j.jns.2017.01.012 Harris, 2004, Effects of nicotine on cognitive deficits in schizophrenia, Neuropsychopharmacology, 29, 1378, 10.1038/sj.npp.1300450 Hatami, 2015, Transgenic rodent models to study α-synuclein pathogenesis, with a focus on cognitive deficits, Curr. Top. Behav. Neurosci., 22, 303, 10.1007/7854_2014_355 Henderson, 2015, Inside-out neuropharmacology of nicotinic drugs, Neuropharmacology, 96, 178, 10.1016/j.neuropharm.2015.01.022 Henderson, 2014, Nicotine exploits a COPI-mediated process for chaperone-mediated up-regulation of its receptors, J. Gen. Physiol., 143, 51, 10.1085/jgp.201311102 Hershey, 2014, Smoking and Parkinson disease: where there is smoke there may not be fire, Neurology, 83, 1392, 10.1212/WNL.0000000000000896 Hong, 2009, Smoking and Parkinson's disease: does nicotine affect α-synuclein fibrillation?, Biochim. Biophys. Acta, 1794, 282, 10.1016/j.bbapap.2008.09.026 Khwaja, 2007, Nicotine partially protects against paraquat-induced nigrostriatal damage in mice; link to α6β2* nAChRs, J. Neurochem., 100, 180, 10.1111/j.1471-4159.2006.04177.x Kruger, 1998, Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease, Nat. Genet., 18, 106, 10.1038/ng0298-106 Lam, 2011, Elevated tonic extracellular dopamine concentration and altered dopamine modulation of synaptic activity precede dopamine loss in the striatum of mice overexpressing human α-synuclein, J. Neurosci. Res., 89, 1091, 10.1002/jnr.22611 Lee, 2011, Enhanced phosphatase activity attenuates alpha-synucleinopathy in a mouse model, J. Neurosci., 31, 6963, 10.1523/JNEUROSCI.6513-10.2011 Lelong-Boulouard, 2006, Interactions of buprenorphine and dipotassium clorazepate on anxiety and memory functions in the mouse, Drug Alcohol Depend., 85, 103, 10.1016/j.drugalcdep.2006.03.017 Lester, 2009, Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery, AAPS J., 11, 167, 10.1208/s12248-009-9090-7 Magen, 2011, Mouse models of cognitive deficits due to α-synuclein pathology, J Parkinsons Dis., 1, 217, 10.3233/JPD-2011-11043 Magen, 2012, Cognitive deficits in a mouse model of pre-manifest Parkinson's disease, Eur. J. Neurosci., 35, 870, 10.1111/j.1460-9568.2012.08012.x Magen, 2014, Intranasal NAP (davunetide) decreases tau hyperphosphorylation and moderately improves behavioral deficits in mice overexpressing α-synuclein, Pharmacol. Res. Perspect., 2, 10.1002/prp2.65 Magen, 2015, Social cognition impairments in mice overexpressing α-synuclein under the thy1 promoter, a model of pre-manifest parkinson's disease, J Parkinsons Dis., 5, 669, 10.3233/JPD-140503 Mamikonyan, 2015, Rivastigmine for mild cognitive impairment in Parkinson disease: a placebo-controlled study, Mov. Disord., 30, 912, 10.1002/mds.26236 McDowell, 2014, Sleep dysfunction and EEG alterations in mice overexpressing α-synuclein, J Parkinsons Dis., 4, 531, 10.3233/JPD-140374 Meyer, 2009, Reduced α4β2*-nicotinic acetylcholine receptor binding and its relationship to mild cognitive and depressive symptoms in Parkinson disease, Arch. Gen. Psychiatry, 66, 866, 10.1001/archgenpsychiatry.2009.106 Moy, 2004, Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice, Genes Brain Behav., 3, 287, 10.1111/j.1601-1848.2004.00076.x Nashmi, 2007, Chronic nicotine cell specifically upregulates functional α4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path, J. Neurosci., 27, 8202, 10.1523/JNEUROSCI.2199-07.2007 Oishi, 2007, Quantification of nicotinic acetylcholine receptors in Parkinson's disease with (123)I-5IA SPECT, J. Neurol. Sci., 256, 52, 10.1016/j.jns.2007.02.014 Ono, 2007, Anti-fibrillogenic and fibril-destabilizing activity of nicotine in vitro: implications for the prevention and therapeutics of Lewy body diseases, Exp. Neurol., 205, 414, 10.1016/j.expneurol.2007.03.002 Perry, 1992, Autoradiographic distribution of [3H]nicotine binding in human cortex: relative abundance in subicular complex, J. Chem. Neuroanat., 5, 399, 10.1016/0891-0618(92)90056-V Pfeiffer, 2014, Cognitive impairment in early-stage non-demented Parkinson's disease patients, Acta Neurol. Scand., 129, 307, 10.1111/ane.12189 Picciotto, 2008, Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer's and Parkinson's disease, Front. Biosci., 13, 492, 10.2741/2695 Pimlott, 2004, Nicotinic acetylcholine receptor distribution in Alzheimer's disease, dementia with Lewy bodies, Parkinson's disease, and vascular dementia: in vitro binding study using 5-[(125)i]-a-85380, Neuropsychopharmacology, 29, 108, 10.1038/sj.npp.1300302 Polymeropoulos, 1997, Mutation in the α-synuclein gene identified in families with Parkinson's disease, Science, 276, 2045, 10.1126/science.276.5321.2045 Poorthuis, 2009, Nicotinic actions on neuronal networks for cognition: general principles and long-term consequences, Biochem. Pharmacol., 78, 668, 10.1016/j.bcp.2009.04.031 Postuma, 2012, Identifying prodromal Parkinson's disease: pre-motor disorders in Parkinson's disease, Mov. Disord., 27, 617, 10.1002/mds.24996 Preskorn, 2014, Normalizing effects of EVP-6124, an α-7 nicotinic partial agonist, on event-related potentials and cognition: a proof of concept, randomized trial in patients with schizophrenia, J. Psychiatr. Pract., 20, 12, 10.1097/01.pra.0000442935.15833.c5 Quik, 2000, Nicotinic receptors and Parkinson's disease, Eur. J. Pharmacol., 393, 223, 10.1016/S0014-2999(99)00888-2 Quik, 2012, Nicotine as a potential neuroprotective agent for Parkinson's disease, Mov. Disord., 27, 947, 10.1002/mds.25028 Quik, 2013, Nicotine reduces established levodopa-induced dyskinesias in a monkey model of Parkinson's disease, Mov. Disord., 28, 1398, 10.1002/mds.25594 Quik, 2015, Nicotine and nicotinic receptor drugs: potential for Parkinson's disease and drug-induced movement disorders, Int. Rev. Neurobiol., 124, 247, 10.1016/bs.irn.2015.07.005 Richter, 2014, A GCase chaperone improves motor function in a mouse model of synucleinopathy, Neurotherapeutics, 11, 840, 10.1007/s13311-014-0294-x Richter, 2014, Chronic administration of cholesterol oximes in mice increases transcription of cytoprotective genes and improves transcriptome alterations induced by α-synuclein overexpression in nigrostriatal dopaminergic neurons, Neurobiol. Dis., 69, 263, 10.1016/j.nbd.2014.05.012 Rinne, 1991, A postmortem study of brain nicotinic receptors in Parkinson's and Alzheimer's disease, Brain Res., 547, 167, 10.1016/0006-8993(91)90588-M Ritz, 2014, Parkinson disease and smoking revisited: ease of quitting is an early sign of the disease, Neurology, 83, 1396, 10.1212/WNL.0000000000000879 Rockenstein, 2002, Differential neuropathological alterations in transgenic mice expressing α-synuclein from the platelet-derived growth factor and Thy-1 promoters, J. Neurosci. Res., 68, 568, 10.1002/jnr.10231 Ross, 2006, Association of olfactory dysfunction with incidental Lewy bodies, Mov. Disord., 21, 2062, 10.1002/mds.21076 Ryan, 2001, Dose-related neuroprotective effects of chronic nicotine in 6-hydroxydopamine treated rats, and loss of neuroprotection in α4 nicotinic receptor subunit knockout mice, Br. J. Pharmacol., 132, 1650, 10.1038/sj.bjp.0703989 Salas, 2013, Abnormal social behavior in nicotinic acetylcholine receptor β4 subunit-null mice, Nicotine Tob. Res., 15, 983, 10.1093/ntr/nts215 Sarter, 2009, nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms, Biochem. Pharmacol., 78, 658, 10.1016/j.bcp.2009.04.019 Singleton, 2003, α-Synuclein locus triplication causes Parkinson's disease, Science, 302, 841, 10.1126/science.1090278 Soleimani, 2014, Disrupted social connectedness in people with Parkinson's disease, Br J Community Nurs., 19, 136, 10.12968/bjcn.2014.19.3.136 Sossi, 2010, Dopamine turnover increases in asymptomatic LRRK2 mutations carriers, Mov. Disord., 25, 2717, 10.1002/mds.23356 Spillantini, 2000, The α-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy, Ann. N. Y. Acad. Sci., 920, 16, 10.1111/j.1749-6632.2000.tb06900.x Spillantini, 1997, α-synuclein in Lewy bodies, Nature, 388, 839, 10.1038/42166 Srinivasan, 2014, Pharmacological chaperoning of nAChRs: a therapeutic target for Parkinson's disease, Pharmacol. Res., 83C, 20, 10.1016/j.phrs.2014.02.005 Srinivasan, 2016, Smoking-relevant nicotine concentration attenuates the unfolded protein response in dopaminergic neurons, J. Neurosci., 36, 65, 10.1523/JNEUROSCI.2126-15.2016 Subramaniam, 2014, Region specific mitochondrial impairment in mice with widespread overexpression of α-synuclein, Neurobiol. Dis., 70, 204, 10.1016/j.nbd.2014.06.017 Sugita, 2001, Meta-analysis for epidemiologic studies on the relationship between smoking and Parkinson's disease, J Epidemiol., 11, 87, 10.2188/jea.11.87 Tanner, 2002, Smoking and Parkinson's disease in twins, Neurology, 58, 581, 10.1212/WNL.58.4.581 Timmermann, 2012, Augmentation of cognitive function by NS9283, a stoichiometry-dependent positive allosteric modulator of α2- and α4-containing nicotinic acetylcholine receptors, Br. J. Pharmacol., 167, 164, 10.1111/j.1476-5381.2012.01989.x Toulorge, 2011, Neuroprotection of midbrain dopamine neurons by nicotine is gated by cytoplasmic Ca2+, FASEB J., 25, 2563, 10.1096/fj.11-182824 Vieregge, 2001, Transdermal nicotine in PD: a randomized, double-blind, placebo-controlled study, Neurology, 57, 1032, 10.1212/WNL.57.6.1032 Villafane, 2007, Chronic high dose transdermal nicotine in Parkinson's disease: an open trial, Eur. J. Neurol., 14, 1313, 10.1111/j.1468-1331.2007.01949.x Wall, 2002, Infralimbic κ opioid and muscarinic M1 receptor interactions in the concurrent modulation of anxiety and memory, Psychopharmacology, 160, 233, 10.1007/s00213-001-0979-9 Wallace, 2011, Targeting the nicotinic α7 acetylcholine receptor to enhance cognition in disease, Biochem. Pharmacol., 82, 891, 10.1016/j.bcp.2011.06.034 Wang, 2012, Mice overexpressing wild-type human α-synuclein display alterations in colonic myenteric ganglia and defecation, Neurogastroenterol. Motil., 24, e425, 10.1111/j.1365-2982.2012.01974.x Wang, 2015, Efficacy and safety of cholinesterase inhibitors and memantine in cognitive impairment in Parkinson's disease, Parkinson's disease dementia, and dementia with Lewy bodies: systematic review with meta-analysis and trial sequential analysis, J. Neurol. Neurosurg. Psychiatry, 86, 135, 10.1136/jnnp-2014-307659 Watson, 2009, Alterations in corticostriatal synaptic plasticity in mice overexpressing human α-synuclein, Neuroscience, 159, 501, 10.1016/j.neuroscience.2009.01.021 Watson, 2012, Regionally-specific microglial activation in young mice over-expressing human wildtype α-synuclein, Exp. Neurol., 237, 318, 10.1016/j.expneurol.2012.06.025 Wolters, 2009, Non-motor extranigral signs and symptoms in Parkinson's disease, Parkinsonism Relat. Disord., 15, S6, 10.1016/S1353-8020(09)70770-9 Wrasidlo, 2016, A de novo compound targeting α-synuclein improves deficits in models of Parkinson's disease, Brain, 139, 3217, 10.1093/brain/aww238 Wu, 2010, α-synuclein overexpression in mice alters synaptic communication in the corticostriatal pathway, J. Neurosci. Res., 88, 1764 Yang, 2016, Parkinson's disease and cognitive impairment, Parkinsons Dis., 2016 Zarow, 2003, Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases, Arch. Neurol., 60, 337, 10.1001/archneur.60.3.337