Neuropathology of cigarette smoking

Acta Neuropathologica

Volumn 127, Issue 1, 2014, Pages 53-69

  Chang, Raymond Chuen Chung ^a,b   Ho, Yuen Shan ^c   Wong, Shun ^d   Gentleman, Stephen M ^e   Ng, Ho Keung ^f  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

^d Princess Margret Hospital   (Hong Kong)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

Alzheimer's disease; Atherosclerosis; Cigarette smoking; Neurodegeneration; Parkinson's disease; Prenatal exposure to maternal cigarette smoking

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; ARTERY DISEASE; ARTICLE; ATHEROSCLEROSIS; BLOOD BRAIN BARRIER; BRAIN ATROPHY; BRAIN NERVE CELL; BRAIN REGION; BRAIN SIZE; CELL LOSS; CEREBROVASCULAR DISEASE; CHILD DEVELOPMENT; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; EXPERIMENTAL ANIMAL; HUMAN; MATERNAL SMOKING; NERVOUS SYSTEM INFLAMMATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; OXIDATIVE STRESS; PARKINSON DISEASE; PRENATAL EXPOSURE; PRIORITY JOURNAL; SENILE PLAQUE; SMOKING; WHITE MATTER INJURY;

ALZHEIMER DISEASE; ANIMALS; BRAIN; CEREBROVASCULAR DISORDERS; FEMALE; HUMANS; NEURODEGENERATIVE DISEASES; PARKINSON DISEASE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SMOKING;

EID: 84892670560     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1210-x     Document Type: Article

References (138)

1. Abbruscato TJ, Lopez SP, Mark KS, Hawkins BT, Davis TP (2002) Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J Pharm Sci 91:2525-2538
2. Abdel-Rahman A, Dechkovskaia A, Mehta-Simmons H, Guan X, Khan W, bou-Donia M (2003) Increased expression of glial fibrillary acidic protein in cerebellum and hippocampus: differential effects on neonatal brain regional acetylcholinesterase following maternal exposure to combined chlorpyrifos and nicotine. J Toxicol Environ Health A 66:2047-2066
3. Abdel-Rahman A, Dechkovskaia AM, Mehta-Simmons H et al (2004) Maternal exposure to nicotine and chlorpyrifos, alone and in combination, leads to persistently elevated expression of glial fibrillary acidic protein in the cerebellum of the offspring in late puberty. Arch Toxicol 78:467-476
4. Ahlsen G, Rosengren L, Belfrage M et al (1993) Glial fibrillary acidic protein in the cerebrospinal fluid of children with autism and other neuropsychiatric disorders. Biol Psychiatry 33:734-743
5. Alberg A (2002) The influence of cigarette smoking on circulating concentrations of antioxidant micronutrients. Toxicology 180:121-137
6. Ali M, Yu Z, Jabbour PM et al (2012) Cigarette smoke directly produces a pro-inflammatory/matrix remodeling phenotype in cerebral vascular smooth muscle cells via KLF4: a potential mechanism for cerebral aneurysm pathogenesis. Stroke 43:A112
7. Almeida OP, Garrido GJ, Lautenschlager NT, Hulse GK, Jamrozik K, Flicker L (2008) Smoking is associated with reduced cortical regional gray matter density in brain regions associated with incipient Alzheimer disease. Am J Geriatr Psychiatry 16:92-98
8. Anblagan D, Jones NW, Costigan C et al (2013) Maternal smoking during pregnancy and fetal organ growth: a magnetic resonance imaging study. PLoS ONE 8:e67223
9. Aoki T, Kataoka H, Ishibashi R, Nozaki K, Morishita R, Hashimoto N (2009) Reduced collagen biosynthesis is the hallmark of cerebral aneurysm: contribution of interleukin-1beta and nuclear factor-kappaB. Arterioscler Thromb Vasc Biol 29:1080-1086
10. Aoki T, Kataoka H, Shimamura M et al (2007) NF-kappaB is a key mediator of cerebral aneurysm formation. Circulation 116:2830-2840
11. Back SA, Kroenke CD, Sherman LS et al (2011) White matter lesions defined by diffusion tensor imaging in older adults. Ann Neurol 70:465-476
12. Bailey EL, Smith C, Sudlow CL, Wardlaw JM (2012) Pathology of lacunar ischemic stroke in humans - a systematic review. Brain Pathol 22:583-591
13. Bakhru A, Erlinger TP (2005) Smoking cessation and cardiovascular disease risk factors: results from the Third National Health and Nutrition Examination Survey. PLoS Med 2:e160
14. Baloyannis SJ (2011) Mitochondria are related to synaptic pathology in Alzheimer's disease. Int J Alzheimers Dis 2011:305395
15. Barbieri SS, Zacchi E, Amadio P et al (2011) Cytokines present in smokers' serum interact with smoke components to enhance endothelial dysfunction. Cardiovasc Res 90:475-483
16. Barnes DE, Yaffe K (2011) The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol 10:819-828
17. Batty GD, Der G, Deary IJ (2006) Effect of maternal smoking during pregnancy on offspring's cognitive ability: empirical evidence for complete confounding in the US national longitudinal survey of youth. Pediatrics 118:943-950
18. Bennett DS, Mohamed FB, Carmody DP et al (2009) Response inhibition among early adolescents prenatally exposed to tobacco: an fMRI study. Neurotoxicol Teratol 31:283-290
19. Bernhard D, Moser C, Backovic A, Wick G (2007) Cigarette smoke - an aging accelerator? Exp Gerontol 42:160-165
20. Boets B, Ghesquiere P, van Wieringen A, Wouters J (2007) Speech perception in preschoolers at family risk for dyslexia: relations with low-level auditory processing and phonological ability. Brain Lang 101:19-30
21. Borsello T, Forloni G (2007) JNK signalling: a possible target to prevent neurodegeneration. Curr Pharm Des 13:1875-1886
22. Bradford ST, Stamatovic SM, Dondeti RS, Keep RF, Andjelkovic AV (2011) Nicotine aggravates the brain postischemic inflammatory response. Am J Physiol Heart Circ Physiol 300:H1518-H1529
23. Brody AL, Mandelkern MA, Jarvik ME et al (2004) Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry 55:77-84
24. Broe GA, Henderson AS, Creasey H et al (1990) A case-control study of Alzheimer's disease in Australia. Neurology 40:1698-1707
25. Butler NR, Goldstein H (1973) Smoking in pregnancy and subsequent child development. Br Med J 4:573-575
26. Church DF, Pryor WA (1985) Free-radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 64:111-126
27. Cooper JK, Mungas D (1993) Risk factor and behavioral differences between vascular and Alzheimer's dementias: the pathway to end-stage disease. J Geriatr Psychiatry Neurol 6:29-33
28. Court JA, Johnson M, Religa D et al (2005) Attenuation of Abeta deposition in the entorhinal cortex of normal elderly individuals associated with tobacco smoking. Neuropathol Appl Neurobiol 31:522-535
29. Cowperthwaite B, Hains SM, Kisilevsky BS (2007) Fetal behavior in smoking compared to non-smoking pregnant women. Infant Behav Dev 30:422-430
30. Csiszar A, Podlutsky A, Wolin MS, Losonczy G, Pacher P, Ungvari Z (2009) Oxidative stress and accelerated vascular aging: implications for cigarette smoking. Front Biosci 14:3128-3144
31. Csordas A, Bernhard D (2013) The biology behind the atherothrombotic effects of cigarette smoke. Nat Rev Cardiol 10:219-230
32. Csordas A, Wick G, Laufer G, Bernhard D (2008) An evaluation of the clinical evidence on the role of inflammation and oxidative stress in smoking-mediated cardiovascular disease. Biomark Insights 3:127-139
33. Deng J, Shen C, Wang YJ et al (2010) Nicotine exacerbates tau phosphorylation and cognitive impairment induced by amyloid-beta 25-35 in rats. Eur J Pharmacol 637:83-88
34. Derauf C, Lester BM, Neyzi N et al (2012) Subcortical and cortical structural central nervous system changes and attention processing deficits in preschool-aged children with prenatal methamphetamine and tobacco exposure. Dev Neurosci 34:327-341
35. Ekblad M, Gissler M, Lehtonen L, Korkeila J (2010) Prenatal smoking exposure and the risk of psychiatric morbidity into young adulthood. Arch Gen Psychiatry 67:841-849
36. Ekblad M, Korkeila J, Parkkola R, Lapinleimu H, Haataja L, Lehtonen L (2010) Maternal smoking during pregnancy and regional brain volumes in preterm infants. J Pediatr 156:185-190
37. Eliez S, Reiss AL (2000) MRI neuroimaging of childhood psychiatric disorders: a selective review. J Child Psychol Psychiatry 41:679-694
38. Eppolito AK, Bachus SE, McDonald CG, Meador-Woodruff JH, Smith RF (2010) Late emerging effects of prenatal and early postnatal nicotine exposure on the cholinergic system and anxiety-like behavior. Neurotoxicol Teratol 32:336-345
39. Eppolito AK, Smith RF (2006) Long-term behavioral and developmental consequences of pre- and perinatal nicotine. Pharmacol Biochem Behav 85:835-841
40. Ezzati M, Lopez AD (2003) Estimates of global mortality attributable to smoking in 2000. Lancet 362:847-852
41. Feigin VL, Rinkel GJ, Lawes CM, Algra A, Bennett DA, van Gijn J, Anderson CS (2005) Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies. Stroke 36:2773-2780
42. Filipek PA, Semrud-Clikeman M, Steingard RJ, Renshaw PF, Kennedy DN, Biederman J (1997) Volumetric MRI analysis comparing subjects having attention-deficit hyperactivity disorder with normal controls. Neurology 48:589-601
43. Fogelman K (1980) Smoking in pregnancy and subsequent development of the child. Child Care Health Dev 6:233-249
44. French LR, Schuman LM, Mortimer JA, Hutton JT, Boatman RA, Christians B (1985) A case-control study of dementia of the Alzheimer type. Am J Epidemiol 121:414-421
45. Fried PA, O'Connell CM, Watkinson B (1992) 60- and 72-month follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol: cognitive and language assessment. J Dev Behav Pediatr 13:383-391
46. Fried PA, Watkinson B (1990) 36- and 48-month neurobehavioral follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol. J Dev Behav Pediatr 11:49-58
47. Gallinat J, Meisenzahl E, Jacobsen LK et al (2006) Smoking and structural brain deficits: a volumetric MR investigation. Eur J Neurosci 24:1744-1750
48. Gilman SE, Gardener H, Buka SL (2008) Maternal smoking during pregnancy and children's cognitive and physical development: a causal risk factor? Am J Epidemiol 168:522-531
49. Giwa MO, Williams J, Elderfield K et al (2012) Neuropathologic evidence of endothelial changes in cerebral small vessel disease. Neurology 78:167-174
50. Gouw AA, Seewann A, van der Flier WM et al (2011) Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry 82:126-135
51. Graves AB, van Duijn CM, Chandra V et al (1991) Alcohol and tobacco consumption as risk factors for Alzheimer's disease: a collaborative re-analysis of case-control studies. EURODEM Risk Factors Research Group. Int J Epidemiol 20 (Suppl 2):S48-S57
52. Hawkins BT, Abbruscato TJ, Egleton RD et al (2004) Nicotine increases in vivo blood-brain barrier permeability and alters cerebral microvascular tight junction protein distribution. Brain Res 1027:48-58
53. Hebert LE, Scherr PA, Beckett LA et al (1992) Relation of smoking and alcohol consumption to incident Alzheimer's disease. Am J Epidemiol 135:347-355
54. Hedberg MM, Svedberg MM, Mustafiz T et al (2008) Transgenic mice overexpressing human acetylcholinesterase and the Swedish amyloid precursor protein mutation: effect of nicotine treatment. Neuroscience 152:223-233
55. Hellstrom-Lindahl E, Moore H, Nordberg A (2000) Increased levels of tau protein in SH-SY5Y cells after treatment with cholinesterase inhibitors and nicotinic agonists. J Neurochem 74:777-784
56. Hellstrom-Lindahl E, Mousavi M, Ravid R, Nordberg A (2004) Reduced levels of Abeta 40 and Abeta 42 in brains of smoking controls and Alzheimer's patients. Neurobiol Dis 15:351-360
57. Heyman A, Wilkinson WE, Stafford JA, Helms MJ, Sigmon AH, Weinberg T (1984) Alzheimer's disease: a study of epidemiological aspects. Ann Neurol 15:335-341
58. Ho YS, Yang X, Yeung SC et al (2012) Cigarette smoking accelerated brain aging and induced pre-Alzheimer-like neuropathology in rats. PLoS One 7:e36752
59. Hong DP, Fink AL, Uversky VN (2009) Smoking and Parkinson's disease: does nicotine affect alpha-synuclein fibrillation? Biochim Biophys Acta 1794:282-290
60. Hossain M, Sathe T, Fazio V et al (2009) Tobacco smoke: a critical etiological factor for vascular impairment at the blood-brain barrier. Brain Res 1287:192-205
61. Huang LH, He JY, Yuan BX, Cao YX (2010) Lipid soluble smoke particles upregulate endothelin receptors in rat basilar artery. Toxicol Lett 197:243-255
62. Huang SH, Wang L, Chi F et al (2013) Circulating brain microvascular endothelial cells (cBMECs) as potential biomarkers of the blood-brain barrier disorders caused by microbial and non-microbial factors. PLoS One 8:e62164
63. Hung CH, Ho YS, Chang RCC (2010) Modulation of mitochondrial calcium as a pharmacological target for Alzheimer's disease. Ageing Res Rev 9:447-456
64. Jackson CA, Hutchison A, Dennis MSATAL (2010) Differing risk factor profiles of ischemic stroke subtypes: evidence for a distinct lacunar arteriopathy? Stroke 41:624-629
65. Jacobsen LK, Picciotto MR, Heath CJ et al (2007) Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. J Neurosci 27:13491-13498
66. Jayaraman T, Paget A, Shin YS et al (2008) TNF-alpha-mediated inflammation in cerebral aneurysms: a potential link to growth and rupture. Vasc Health Risk Manag 4:805-817
67. Kable JA, Coles CD, Lynch ME, Carroll J (2009) The impact of maternal smoking on fast auditory brainstem responses. Neurotoxicol Teratol 31:216-224
68. Kallen K (2000) Maternal smoking during pregnancy and infant head circumference at birth. Early Hum Dev 58:197-204
69. Khan U, Porteous L, Hassan A, Markus H (2007) Risk factor profile of cerebral small vessel disease and its subtypes. J Neurol Neurosurg Psychiatry 78:702-706
70. Khanna A, Guo M, Mehra M, Royal W (2013) Inflammation and oxidative stress induced by cigarette smoke in Lewis rat brains. J Neuroimmunol 254:69-75
71. Kim SH, Kim JS, Shin HS, Keen CL (2003) Influence of smoking on markers of oxidative stress and serum mineral concentrations in teenage girls in Korea. Nutrition 19:240-243
72. Kitada K, Ohkita M, Matsumura Y (2012) Pathological importance of the endothelin-1/ET(B) receptor system on vascular diseases. Cardiol Res Pract 2012:731970
73. Lambe M, Hultman C, Torrang A, Maccabe J, Cnattingius S (2006) Maternal smoking during pregnancy and school performance at age 15. Epidemiology 17:524-530
74. Lau WK, Mak JC, Chan KH, Law AC (2012) Cigarette smoke-induced cerebral cortical interleukin-6 elevation is not mediated through oxidative stress. Neurotox Res 22:170-176
75. Lin F, Wu G, Zhu L, Lei H (2013) Heavy smokers show abnormal microstructural integrity in the anterior corpus callosum: a diffusion tensor imaging study with tract-based spatial statistics. Drug Alcohol Depend 129:82-87
76. Lindley AA, Becker S, Gray RH, Herman AA (2000) Effect of continuing or stopping smoking during pregnancy on infant birth weight, crown-heel length, head circumference, ponderal index, and brain:body weight ratio. Am J Epidemiol 152:219-225
77. Liu J, Lester BM, Neyzi N et al (2013) Regional brain morphometry and impulsivity in adolescents following prenatal exposure to cocaine and tobacco. JAMA Pediatr 167:348-354
78. Liu Q, Zhang J, Zhu H, Qin C, Chen Q, Zhao B (2007) Dissecting the signaling pathway of nicotine-mediated neuroprotection in a mouse Alzheimer disease model. FASEB J 21:61-73
79. McCartney JS, Fried PA, Watkinson B (1994) Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxicol Teratol 16:269-276
80. Middleton FA, Strick PL (2001) Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 21:700-712
81. Miller AH, Maletic V, Raison CL (2009) Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65:732-741
82. Miyake Y, Tanaka K, Fukushima W et al (2012) SNCA polymorphisms, smoking, and sporadic Parkinson's disease in Japanese. Parkinsonism Relat Disord 18:557-561
83. Miyao M, Furuta M, Matsushita Y, Ogiso M, Ishihara S, Teo PC (1995) A matched-pair longitudinal study on the relationship between maternal smoking and head circumference of newborns. Tohoku J Exp Med 175:135-137
84. Moreno-Gonzalez I, Estrada LD, Sanchez-Mejias E, Soto C (2013) Smoking exacerbates amyloid pathology in a mouse model of Alzheimer's disease. Nat Commun 4:1495
85. Mousavi M, Hellstrom-Lindahl E (2009) Nicotinic receptor agonists and antagonists increase sAPPalpha secretion and decrease Abeta levels in vitro. Neurochem Int 54:237-244
86. Mouton-Liger F, Paquet C, Dumurgier J et al (2012) Oxidative stress increases BACE1 protein levels through activation of the PKR-eIF2alpha pathway. Biochim Biophys Acta 1822:885-896
87. Newby AC (2007) Metalloproteinases and vulnerable atherosclerotic plaques. Trends Cardiovasc Med 17:253-258
88. Nie HZ, Li ZQ, Yan QX et al (2011) Nicotine decreases beta-amyloid through regulating BACE1 transcription in SH-EP1-alpha4beta2 nAChR-APP695 cells. Neurochem Res 36:904-912
89. O'Callaghan FV, Al MA, O'Callaghan M, Alati R, Williams GM, Najman JM (2010) Is smoking in pregnancy an independent predictor of academic difficulties at 14 years of age? A birth cohort study. Early Hum Dev 86:71-76
90. O'Donnell MJ, Xavier D, Liu L et al (2010) Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet 376:112-123
91. Oddo S, Caccamo A, Green KN (2005) Chronic nicotine administration exacerbates tau pathology in a transgenic model of Alzheimer's disease. Proc Natl Acad Sci USA 102:3046-3051
92. Ogata J, Yamanishi H, Ishibashi-Ueda H (2011) Review: role of cerebral vessels in ischaemic injury of the brain. Neuropathol Appl Neurobiol 37:40-55
93. Ono K, Hasegawa K, Yamada M, Naiki H (2002) Nicotine breaks down preformed Alzheimer's beta-amyloid fibrils in vitro. Biol Psychiatry 52:880-886
94. Orejana L, Barros-Minones L, Aguirre N, Puerta E (2013) Implication of JNK pathway on tau pathology and cognitive decline in a senescence-accelerated mouse model. Exp Gerontol 48:565-571
95. Pan P, Shi H, Zhong J, Xiao P, Shen Y, Wu L, Song Y, He G (2012) Chronic smoking and brain gray matter changes: evidence from meta-analysis of voxel-based morphometry studies. Neurol Sci 34:813-817
96. Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689-701
97. Paulson JR, Roder KE, McAfee G, Allen DD, Van der Schyf CJ, Abbruscato TJ (2006) Tobacco smoke chemicals attenuate brain-to-blood potassium transport mediated by the Na, K, 2Cl-cotransporter during hypoxia-reoxygenation. J Pharmacol Exp Ther 316:248-254
98. Paulson JR, Yang T, Selvaraj PK et al (2010) Nicotine exacerbates brain edema during in vitro and in vivo focal ischemic conditions. J Pharmacol Exp Ther 332:371-379
99. Paus T, Nawazkhan I, Leonard G et al (2008) Corpus callosum in adolescent offspring exposed prenatally to maternal cigarette smoking. Neuroimage 40:435-441
100. Peck JD, Neas B, Robledo C, Saffer E, Beebe L, Wild RA (2010) Intrauterine tobacco exposure may alter auditory brainstem responses in newborns. Acta Obstet Gynecol Scand 89(4):592-596
101. Peterson BS, Vohr B, Staib LH et al (2000) Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 284:1939-1947
102. Peterson J, Taylor HG, Minich N, Klein N, Hack M (2006) Subnormal head circumference in very low birth weight children: neonatal correlates and school-age consequences. Early Hum Dev 82:325-334
103. Qi XL, Zhang XL, Ou-Yang K, Shan KR, Guan ZZ (2013) The influence of inhibiting or stimulating the expression of the alpha3 subunit of the nicotinic receptor in SH-SY5Y cells on levels of amyloid-beta peptide and beta-secretase. Neurochem Int 62:79-83
104. Quik M (2004) Smoking, nicotine and Parkinson's disease. Trends Neurosci 27:561-568
105. Quik M, Perez XA, Bordia T (2012) Nicotine as a potential neuroprotective agent for Parkinson's disease. Mov Disord 27:947-957
106. Quiroz-Baez R, Rojas E, Arias C (2009) Oxidative stress promotes JNK-dependent amyloidogenic processing of normally expressed human APP by differential modification of alpha-, beta- and gamma-secretase expression. Neurochem Int 55:662-670
107. Rao JS, Kim HW, Harry GJ, Rapoport SI, Reese EA (2013) Increased neuroinflammatory and arachidonic acid cascade markers, and reduced synaptic proteins, in the postmortem frontal cortex from schizophrenia patients. Schizophr Res 147:24-31
108. Rivkin MJ, Davis PE, Lemaster JL et al (2008) Volumetric MRI study of brain in children with intrauterine exposure to cocaine, alcohol, tobacco, and marijuana. Pediatrics 121:741-750
109. Roy TS, Sabherwal U (1994) Effects of prenatal nicotine exposure on the morphogenesis of somatosensory cortex. Neurotoxicol Teratol 16:411-421
110. Roy TS, Sabherwal U (1998) Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol Teratol 20:465-473
111. Roy TS, Seidler FJ, Slotkin TA (2002) Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther 300:124-133
112. Roza SJ, Verburg BO, Jaddoe VW et al (2007) Effects of maternal smoking in pregnancy on prenatal brain development. The Generation R Study. Eur J Neurosci 25:611-617
113. Salomon AR, Marcinowski KJ, Friedland RP, Zagorski MG (1996) Nicotine inhibits amyloid formation by the beta-peptide. Biochemistry 35:13568-13578
114. Sandhu H, Xu CB, Edvinsson L (2010) Upregulation of contractile endothelin type B receptors by lipid-soluble cigarette smoking particles in rat cerebral arteries via activation of MAPK. Toxicol Appl Pharmacol 249:25-32
115. Schreiber S, Bueche CZ, Garz C, Braun H (2013) Blood brain barrier breakdown as the starting point of cerebral small vessel disease? - New insights from a rat model. Exp Transl Stroke Med 5:4
116. Schwartz RS, Halliday GM, Cordato DJ, Kril JJ (2012) Small-vessel disease in patients with Parkinson's disease: a clinicopathological study. Mov Disord 27:1506-1512
117. Shen C, Chen Y, Liu H et al (2008) Hydrogen peroxide promotes Abeta production through JNK-dependent activation of gamma-secretase. J Biol Chem 283:17721-17730
118. Sonnen JA, Larson EB, Gray SL et al (2009) Free radical damage to cerebral cortex in Alzheimer's disease, microvascular brain injury, and smoking. Ann Neurol 65:226-229
119. Sowell ER, Thompson PM, Welcome SE, Henkenius AL, Toga AW, Peterson BS (2003) Cortical abnormalities in children and adolescents with attention-deficit hyperactivity disorder. Lancet 362:1699-1707
120. Stene-Larsen K, Borge AI, Vollrath ME (2009) Maternal smoking in pregnancy and externalizing behavior in 18-month-old children: results from a population-based prospective study. J Am Acad Child Adolesc Psychiatry 48:283-289
121. Stevenson SF, Doubal FN, Shuler K, Wardlaw JM (2010) A systematic review of dynamic cerebral and peripheral endothelial function in lacunar stroke versus controls. Stroke 41:e434-e442
122. Topakian R, Barrick TR, Howe FA, Markus HS (2010) Blood-brain barrier permeability is increased in normal-appearing white matter in patients with lacunar stroke and leucoaraiosis. J Neurol Neurosurg Psychiatry 81:192-197
123. Toro R, Leonard G, Lerner JV et al (2008) Prenatal exposure to maternal cigarette smoking and the adolescent cerebral cortex. Neuropsychopharmacology 33:1019-1027
124. Tsuang D, Larson EB, Li G, Shofer JB, Montine KS, Thompson ML, Sonnen JA, Crane PK, Leverenz JB, Montine TJ (2010) Association between lifetime cigarette smoking and lewy body accumulation. Brain Pathol 20:412-418
125. Tyas SL, White LR, Petrovitch H et al (2003) Mid-life smoking and late-life dementia: the Honolulu-Asia Aging Study. Neurobiol Aging 24:589-596
126. UK Department of Health (2012) Half of all smokers underestimate the health and financial impacts of smoking. 1-1-2012. Ref Type: Report
127. Ulrich J, Johannson-Locher G, Seiler WO, Stahelin HB (1997) Does smoking protect from Alzheimer's disease? Alzheimer-type changes in 301 unselected brains from patients with known smoking history. Acta Neuropathol 94:450-454
128. van Dijk EJ, Prins ND, Vrooman HA, Hofman A, Koudstaal PJ, Breteler MM (2008) Progression of cerebral small vessel disease in relation to risk factors and cognitive consequences: Rotterdam Scan study. Stroke 39:2712-2719
129. Vikman P, Xu CB, Edvinsson L (2009) Lipid-soluble cigarette smoking particles induce expression of inflammatory and extracellular-matrix-related genes in rat cerebral arteries. Vasc Health Risk Manag 5:333-341
130. Wang HY, Li W, Benedetti NJ, Lee DH (2003) Alpha 7 nicotinic acetylcholine receptors mediate beta-amyloid peptide-induced tau protein phosphorylation. J Biol Chem 278:31547-31553
131. Wardlaw JM (2010) Blood-brain barrier and cerebral small vessel disease. J Neurol Sci 299:66-71
132. Wardlaw JM, Doubal F, Armitage P, Chappell F, Carpenter T, Munoz MS, Farrall A, Sudlow C, Dennis M, Dhillon B (2009) Lacunar stroke is associated with diffuse blood-brain barrier dysfunction. Ann Neurol 65:194-202
133. Wardlaw JM, Smith C, Dichgans M (2013) Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol 12:483-497
134. Wirdefeldt K, Adami HO, Cole P, Trichopoulos D, Mandel J (2011) Epidemiology and etiology of Parkinson's disease: a review of the evidence. Eur J Epidemiol 26(Suppl 1):S1-S58
135. World Health Organization (2011) Global status report on noncommunicable diseases 2010 - Description of the gobal burden of NCDs, their risk factors and determinants. World Health Organization, editor. 1-31. 4-20-2011
136. Xu CB, Zheng JP, Zhang W, Zhang Y, Edvinsson L (2008) Lipid-soluble smoke particles upregulate vascular smooth muscle ETB receptors via activation of mitogen-activating protein kinases and NF-kappaB pathways. Toxicol Sci 106:546-555
137. Zhang JY, Cao YX, Xu CB, Edvinsson L (2006) Lipid-soluble smoke particles damage endothelial cells and reduce endothelium-dependent dilatation in rat and man. BMC Cardiovasc Disord 6:3
138. Zhang X, Salmeron BJ, Ross TJ, Geng X, Yang Y, Stein EA (2011) Factors underlying prefrontal and insula structural alterations in smokers. Neuroimage 54:42-48