{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T00:33:06Z","timestamp":1791419586310,"version":"4.3.3"},"reference-count":59,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2012,5,11]],"date-time":"2012-05-11T00:00:00Z","timestamp":1336694400000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0036752","type":"journal-article","created":{"date-parts":[[2012,5,11]],"date-time":"2012-05-11T20:58:02Z","timestamp":1336769882000},"page":"e36752","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":113,"title":["Cigarette Smoking Accelerated Brain Aging and Induced Pre-Alzheimer-Like Neuropathology in Rats"],"prefix":"10.1371","volume":"7","author":[{"given":"Yuen-Shan","family":"Ho","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xifei","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sze-Chun","family":"Yeung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kin","family":"Chiu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chi-Fai","family":"Lau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea Wing-Ting","family":"Tsang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Judith Choi-Wo","family":"Mak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raymond Chuen-Chung","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2012,5,11]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1093\/aje\/kwm116","article-title":"Smoking as a risk factor for dementia and cognitive decline: a meta-analysis of prospective studies.","volume":"166","author":"KJ Anstey","year":"2007","journal-title":"Am J Epidemiol"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1212\/01.WNL.0000115110.35610.80","article-title":"Effect of smoking on global cognitive function in nondemented elderly.","volume":"62","author":"A Ott","year":"2004","journal-title":"Neurology"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"465","DOI":"10.3233\/JAD-2010-1240","article-title":"Cigarette smoking is a risk factor for Alzheimer's Disease: an analysis controlling for tobacco industry affiliation.","volume":"19","author":"JK Cataldo","year":"2010","journal-title":"J Alzheimers Dis"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1840","DOI":"10.1016\/S0140-6736(97)07541-7","article-title":"Smoking and risk of dementia and Alzheimer's disease in a population-based cohort study: the Rotterdam Study.","volume":"351","author":"A Ott","year":"1998","journal-title":"Lancet"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"b462","DOI":"10.1136\/bmj.b462","article-title":"Exposure to secondhand smoke and cognitive impairment in non-smokers: national cross sectional study with cotinine measurement.","volume":"338","author":"DJ Llewellyn","year":"2009","journal-title":"BMJ"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1093\/aje\/kwp376","article-title":"Secondhand smoke, vascular disease, and dementia incidence: findings from the cardiovascular health cognition study.","volume":"171","author":"DE Barnes","year":"2010","journal-title":"Am J Epidemiol"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1212\/01.WNL.0000156912.54593.65","article-title":"Smoking affects the phenotype of Alzheimer disease.","volume":"64","author":"MN Sabbagh","year":"2005","journal-title":"Neurology"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1007\/s004010050732","article-title":"Does smoking protect from Alzheimer's disease? Alzheimer-type changes in 301 unselected brains from patients with known smoking history.","volume":"94","author":"J Ulrich","year":"1997","journal-title":"Acta Neuropathol"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/S0197-4580(02)00156-2","article-title":"Mid-life smoking and late-life dementia: the Honolulu-Asia Aging Study.","volume":"24","author":"SL Tyas","year":"2003","journal-title":"Neurobiol Aging"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1007\/BF01273157","article-title":"Synaptic pathology in Alzheimer's disease: relation to severity of dementia, but not to senile plaques, neurofibrillary tangles, or the ApoE4 allele.","volume":"103","author":"K Blennow","year":"1996","journal-title":"J Neural Transm"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1001\/archneur.55.3.326","article-title":"Clinicopathologic studies in cognitively healthy aging and Alzheimer's disease: relation of histologic markers to dementia severity, age, sex, and apolipoprotein E genotype.","volume":"55","author":"L Berg","year":"1998","journal-title":"Arch Neurol"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/j.1749-6632.1993.tb23028.x","article-title":"Synaptic pathology of Alzheimer's disease.","volume":"695","author":"H Lassmann","year":"1993","journal-title":"Ann NY Acad Sci"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.exger.2007.06.011","article-title":"Smoking, aging and the centenarians.","volume":"43","author":"V Nicita-Mauro","year":"2008","journal-title":"Exp Gerontol"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1016\/S0140-6736(05)66630-5","article-title":"Obesity, cigarette smoking, and telomere length in women.","volume":"366","author":"AM Valdes","year":"2005","journal-title":"Lancet"},{"key":"ref15","first-page":"BR218","article-title":"Organ-related cigarette smoke-induced oxidative stress is strain-dependent.","volume":"16","author":"CR Rueff-Barroso","year":"2010","journal-title":"Med Sci Monit"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.exger.2006.09.016","article-title":"Cigarette smoke\u2013an aging accelerator?","volume":"42","author":"D Bernhard","year":"2007","journal-title":"Exp Gerontol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.neulet.2010.03.030","article-title":"Effects of moderate exercise on cigarette smoke exposure-induced hippocampal oxidative stress values and neurological behaviors in mice.","volume":"475","author":"T Tuon","year":"2010","journal-title":"Neurosci Lett"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1378","DOI":"10.1016\/j.lfs.2005.07.030","article-title":"Effect of bacoside A on brain antioxidant status in cigarette smoke exposed rats.","volume":"78","author":"K Anbarasi","year":"2006","journal-title":"Life Sci"},{"key":"ref19","first-page":"128","article-title":"Cortical synaptic changes and gliosis in normal aging, Alzheimer's disease and frontal lobe degeneration.","volume":"7","author":"X Liu","year":"1996","journal-title":"Dementia"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.1016\/j.neurobiolaging.2005.09.012","article-title":"Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment.","volume":"27","author":"SW Scheff","year":"2006","journal-title":"Neurobiol Aging"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/0306-4522(94)00422-2","article-title":"Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease.","volume":"64","author":"O Heinonen","year":"1995","journal-title":"Neuroscience"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"2415","DOI":"10.1016\/0024-3205(96)00245-7","article-title":"An experimental model for studying passive cigarette smoking effects on gastric ulceration.","volume":"58","author":"JY Chow","year":"1996","journal-title":"Life Sci"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"1746","DOI":"10.1016\/j.rmed.2009.04.027","article-title":"Chinese green tea ameliorates lung injury in cigarette smoke-exposed rats.","volume":"103","author":"KH Chan","year":"2009","journal-title":"Respir Med"},{"key":"ref24","first-page":"2546","article-title":"Increase of a type of oxidative DNA damage, 8-hydroxyguanine, and its repair activity in human leukocytes by cigarette smoking.","volume":"56","author":"S Asami","year":"1996","journal-title":"Cancer Res"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1191\/0748233705th211oa","article-title":"Active smoking causes oxidative stress and decreases blood melatonin levels.","volume":"21","author":"F Ozguner","year":"2005","journal-title":"Toxicol Ind Health"},{"key":"ref26","article-title":"The influence of cigarette smoking on circulating concentrations of antioxidant micronutrients.","volume":"121\u2013137","author":"A Alberg","year":"2002","journal-title":"Toxicology 180,"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/S0899-9007(02)01002-X","article-title":"Influence of smoking on markers of oxidative stress and serum mineral concentrations in teenage girls in Korea.","volume":"19","author":"SH Kim","year":"2003","journal-title":"Nutrition"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1002\/ana.21508","article-title":"Free radical damage to cerebral cortex in Alzheimer's disease, microvascular brain injury, and smoking.","volume":"65","author":"JA Sonnen","year":"2009","journal-title":"Ann Neurol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"1210","DOI":"10.1093\/ntr\/ntr154","article-title":"Vitamin E Decreased the Activity of Acetylcholinesterase and Level of Lipid Peroxidation in Brain of Rats Exposed to Aged and Diluted Sidestream Smoke.","volume":"13","author":"GR Thome","year":"2011","journal-title":"Nicotine Tob Res"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/S0021-9258(18)48474-8","article-title":"8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G\u2013T and A\u2013C substitutions.","volume":"267","author":"KC Cheng","year":"1992","journal-title":"J Biol Chem"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"1959","DOI":"10.1523\/JNEUROSCI.19-06-01959.1999","article-title":"RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease.","volume":"19","author":"A Nunomura","year":"1999","journal-title":"J Neurosci"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1093\/jnen\/60.8.759","article-title":"Oxidative damage is the earliest event in Alzheimer disease.","volume":"60","author":"A Nunomura","year":"2001","journal-title":"J Neuropathol Exp Neurol"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1007\/s00415-009-5333-x","article-title":"Levels of reduced and oxidized coenzyme Q-10 and 8-hydroxy-2\u2032-deoxyguanosine in the CSF of patients with Alzheimer's disease demonstrate that mitochondrial oxidative damage and\/or oxidative DNA damage contributes to the neurodegenerative process.","volume":"257","author":"C Isobe","year":"2010","journal-title":"J Neurol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/s12031-009-9316-2","article-title":"Effects of environmental tobacco smoke on adult rat brain biochemistry.","volume":"41","author":"BF Fuller","year":"2010","journal-title":"J Mol Neurosci"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/S0006-3223(03)00610-3","article-title":"Differences between smokers and nonsmokers in regional gray matter volumes and densities.","volume":"55","author":"AL Brody","year":"2004","journal-title":"Biol Psychiatry"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"1744","DOI":"10.1111\/j.1460-9568.2006.05050.x","article-title":"Smoking and structural brain deficits: a volumetric MR investigation.","volume":"24","author":"J Gallinat","year":"2006","journal-title":"Eur J Neurosci"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/s00429-011-0308-y","article-title":"Morphological changes in nerve cells during normal aging.","volume":"216","author":"E Pannese","year":"2011","journal-title":"Brain Struct Funct"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1002\/j.1460-2075.1995.tb06995.x","article-title":"Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine.","volume":"14","author":"L Edelmann","year":"1995","journal-title":"EMBO J"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1126\/science.8430330","article-title":"Synaptic vesicle phosphoproteins and regulation of synaptic function.","volume":"259","author":"P Greengard","year":"1993","journal-title":"Science"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"7161","DOI":"10.1523\/JNEUROSCI.16-22-07161.1996","article-title":"Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex.","volume":"16","author":"K Hayashi","year":"1996","journal-title":"J Neurosci"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"3918","DOI":"10.1523\/JNEUROSCI.19-10-03918.1999","article-title":"Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons.","volume":"19","author":"K Hayashi","year":"1999","journal-title":"J Neurosci"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1002\/jnr.490430111","article-title":"Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease.","volume":"43","author":"Y Harigaya","year":"1996","journal-title":"J Neurosci Res"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1097\/00005072-200606000-00007","article-title":"Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment.","volume":"65","author":"SE Counts","year":"2006","journal-title":"J Neuropathol Exp Neurol"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.nbd.2011.03.012","article-title":"Hippocampal dysregulation of synaptic plasticity-associated proteins with age-related cognitive decline.","volume":"43","author":"HD VanGuilder","year":"2011","journal-title":"Neurobiol Dis"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"R18","DOI":"10.1016\/j.cub.2006.11.036","article-title":"Microtubule modification: acetylation speeds anterograde traffic flow.","volume":"17","author":"JC Bulinski","year":"2007","journal-title":"Curr Biol"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"964","DOI":"10.1097\/00005072-199609000-00003","article-title":"Reduction of acetylated alpha-tubulin immunoreactivity in neurofibrillary tangle-bearing neurons in Alzheimer's disease.","volume":"55","author":"B Hempen","year":"1996","journal-title":"J Neuropathol Exp Neurol"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1056\/NEJMra0909142","article-title":"Alzheimer's disease.","volume":"362","author":"HW Querfurth","year":"2010","journal-title":"N Engl J Med"},{"key":"ref48","article-title":"Microtubule-associated protein tau in development, degeneration and protection of neurons.","volume":"148\u2013175","author":"JZ Wang","year":"2008","journal-title":"Prog Neurobiol 85,"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1046\/j.1471-4159.2000.0751200.x","article-title":"MPTP activates c-Jun NH(2)-terminal kinase (JNK) and its upstream regulatory kinase MKK4 in nigrostriatal neurons in vivo.","volume":"75","author":"MS Saporito","year":"2000","journal-title":"J Neurochem"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.neulet.2009.12.013","article-title":"SA4503, a sigma-1 receptor agonist, prevents cultured cortical neurons from oxidative stress-induced cell death via suppression of MAPK pathway activation and glutamate receptor expression.","volume":"469","author":"T Tuerxun","year":"2010","journal-title":"Neurosci Lett"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.neulet.2009.11.010","article-title":"Chronic oxidative stress causes increased tau phosphorylation in M17 neuroblastoma cells.","volume":"468","author":"B Su","year":"2010","journal-title":"Neurosci Lett"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/s11010-006-9333-1","article-title":"Nicotine induces oxidative stress and activates nuclear transcription factor kappa B in rat mesencephalic cells.","volume":"297","author":"J Barr","year":"2007","journal-title":"Mol Cell Biochem"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"3046","DOI":"10.1073\/pnas.0408500102","article-title":"Chronic nicotine administration exacerbates tau pathology in a transgenic model of Alzheimer's disease.","volume":"102","author":"S Oddo","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1016\/j.neuint.2009.06.012","article-title":"Oxidative stress promotes JNK-dependent amyloidogenic processing of normally expressed human APP by differential modification of alpha-, beta- and gamma-secretase expression.","volume":"55","author":"R Quiroz-Baez","year":"2009","journal-title":"Neurochem Int"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"17721","DOI":"10.1074\/jbc.M800013200","article-title":"Hydrogen peroxide promotes Abeta production through JNK-dependent activation of gamma-secretase.","volume":"283","author":"C Shen","year":"2008","journal-title":"J Biol Chem"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1038\/nn.2583","article-title":"Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks.","volume":"13","author":"JJ Palop","year":"2010","journal-title":"Nat Neurosci"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.mcn.2009.01.006","article-title":"Low molecular weight Abeta induces collapse of endoplasmic reticulum.","volume":"41","author":"CS Lai","year":"2009","journal-title":"Mol Cell Neurosci"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1111\/j.1471-4159.2010.06643.x","article-title":"Abeta promotes Alzheimer's disease-like cytoskeleton abnormalities with consequences to APP processing in neurons.","volume":"113","author":"AG Henriques","year":"2010","journal-title":"J Neurochem"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1016\/S1474-4422(11)70072-2","article-title":"The projected effect of risk factor reduction on Alzheimer's disease prevalence.","volume":"10","author":"DE Barnes","year":"2011","journal-title":"Lancet Neurol"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0036752","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,1,15]],"date-time":"2022-01-15T13:02:30Z","timestamp":1642251750000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0036752"}},"subtitle":[],"editor":[{"given":"Stephen D.","family":"Ginsberg","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2012,5,11]]},"references-count":59,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2012,5,11]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0036752","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,5,11]]}}}