Startseite Revisiting nicotine’s role in the ageing brain and cognitive impairment
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Revisiting nicotine’s role in the ageing brain and cognitive impairment

  • Alireza Majdi , Farzin Kamari , Manouchehr Seyedi Vafaee und Saeed Sadigh-Eteghad EMAIL logo
Veröffentlicht/Copyright: 6. Juni 2017
Veröffentlichen auch Sie bei De Gruyter Brill

Abstract

Brain ageing is a complex process which in its pathologic form is associated with learning and memory dysfunction or cognitive impairment. During ageing, changes in cholinergic innervations and reduced acetylcholinergic tonus may trigger a series of molecular pathways participating in oxidative stress, excitotoxicity, amyloid-β toxicity, apoptosis, neuroinflammation, and perturb neurotrophic factors in the brain. Nicotine is an exogenous agonist of nicotinic acetylcholine receptors (nAChRs) and acts as a pharmacological chaperone in the regulation of nAChR expression, potentially intervening in age-related changes in diverse molecular pathways leading to pathology. Although nicotine has therapeutic potential, paradoxical effects have been reported, possibly due to its inverted U-shape dose-response effects or pharmacokinetic factors. Additionally, nicotine administration should result in optimum therapeutic effects without imparting abuse potential or toxicity. Overall, this review aims to compile the previous and most recent data on nicotine and its effects on cognition-related mechanisms and age-related cognitive impairment.

Acknowledgements

The authors are grateful to Dr. Mehdi Farhoudi, director of Neurosciences Research Center (NSRC), for his assistance through this work. The authors also acknowledge manuscript editing by Inglewood Biomedical Editing. This work was in part supported by the Lundbeckfonden for visiting professor, grant R24-2015-159.

  1. Conflict of interest statement: The author declares that he has no conflict of interest.

References

Adams, J., Mukherjee, S., Klaidman, L., Chang, M., and Yasharel, R. (1996). Apoptosis and oxidative stress in the aging brain. Ann. NY Acad. Sci. 786, 135–151.10.1111/j.1749-6632.1996.tb39058.xSuche in Google Scholar

Andreasen, J.T., Henningsen, K., Bate, S., Christiansen, S., and Wiborg, O. (2011). Nicotine reverses anhedonic-like response and cognitive impairment in the rat chronic mild stress model of depression: comparison with sertraline. J. Psychopharmacol. 25, 1134–1141.10.1177/0269881110391831Suche in Google Scholar PubMed

Arroyo, S., Bennett, C., and Hestrin, S. (2014). Nicotinic modulation of cortical circuits. Front. Neural Circuits 8, 30.10.3389/fncir.2014.00030Suche in Google Scholar PubMed

Balakumar, P. and Kaur, J. (2009). Is nicotine a key player or spectator in the induction and progression of cardiovascular disorders? Pharmacol. Res. 60, 361–368.Suche in Google Scholar

Banks, W.A., Farr, S.A., Butt, W., Kumar, V.B., Franko, M.W., and Morley, J.E. (2001). Delivery across the blood-brain barrier of antisense directed against amyloid β: reversal of learning and memory deficits in mice overexpressing amyloid precursor protein. J. Pharmacol. Exp. Ther. 297, 1113–1121.Suche in Google Scholar PubMed

Bañuelos, C., LaSarge, C.L., McQuail, J.A., Hartman, J.J., Gilbert, R.J., Ormerod, B.K., and Bizon, J.L. (2013). Age-related changes in rostral basal forebrain cholinergic and GABAergic projection neurons: relationship with spatial impairment. Neurobiol. Aging 34, 845–862.10.1016/j.neurobiolaging.2012.06.013Suche in Google Scholar PubMed

Barr, R.S., Culhane, M.A., Jubelt, L.E., Mufti, R.S., Dyer, M.A., Weiss, A.P., Deckersbach, T., Kelly, J.F., Freudenreich, O., and Goff, D.C. (2008). The effects of transdermal nicotine on cognition in nonsmokers with schizophrenia and nonpsychiatric controls. Neuropsychopharmacology 33, 480–490.10.1038/sj.npp.1301423Suche in Google Scholar PubMed

Beach, T.G., Kuo, Y.-M., Schwab, C., Walker, D.G., and Roher, A.E. (2001). Reduction of cortical amyloid β levels in guinea pig brain after systemic administration of physostigmine. Neurosci. Lett. 310, 21–24.10.1016/S0304-3940(01)02076-6Suche in Google Scholar PubMed

Bencherif, M., Lippiello, P.M., Lucas, R., and Marrero, M.B. (2011). Alpha7 nicotinic receptors as novel therapeutic targets for inflammation-based diseases. Cell Mol. Life Sci. 68, 931–949.10.1007/s00018-010-0525-1Suche in Google Scholar PubMed PubMed Central

Benowitz, N.L. (2010). Nicotine addiction. N. Engl. J. Med. 362, 2295–2303.10.1056/NEJMra0809890Suche in Google Scholar PubMed PubMed Central

Benowitz, N.L., Jacob P., III, Ahijevych, K., Jarvis, M.J., Hall, S., LeHouezec, J., Hansson, A., Lichtenstein, E., Henningfield, J., and Tsoh, J. (2002). Biochemical verification of tobacco use and cessation. Nicotine Tob. Res. 4, 149–159.10.1080/14622200210123581Suche in Google Scholar PubMed

Berrendero, F., Robledo, P., Trigo, J.M., Martín-García, E., and Maldonado, R. (2010). Neurobiological mechanisms involved in nicotine dependence and reward: participation of the endogenous opioid system. Neurosci. Biobehav. Rev. 35, 220–231.10.1016/j.neubiorev.2010.02.006Suche in Google Scholar PubMed PubMed Central

Bhagwat, S.V., Vijayasarathy, C., Raza, H., Mullick, J., and Avadhani, N.G. (1998). Preferential effects of nicotine and 4-(N-methyl-N-nitrosamino)-1-(3-pyridyl)-1-butanone on mitochondrial glutathione S-transferase A4-4 induction and increased oxidative stress in the rat brain. Biochem. Pharmacol. 56, 831–839.10.1016/S0006-2952(98)00228-7Suche in Google Scholar PubMed

Blasko, I., Stampfer-Kountchev, M., Robatscher, P., Veerhuis, R., Eikelenboom, P., and Grubeck-Loebenstein, B. (2004). How chronic inflammation can affect the brain and support the development of Alzheimer’s disease in old age: the role of microglia and astrocytes. Aging Cell 3, 169–176.10.1111/j.1474-9728.2004.00101.xSuche in Google Scholar PubMed

Buisson, B. and Bertrand, D. (2002). Nicotine addiction: the possible role of functional upregulation. Trends Pharmacol. Sci. 23, 130–136.10.1016/S0165-6147(00)01979-9Suche in Google Scholar PubMed

Chen, G., Gong, M., Yan, M., and Zhang, X. (2013). Sevoflurane induces endoplasmic reticulum stress mediated apoptosis in hippocampal neurons of aging rats. PLoS One 8, e57870.10.1371/journal.pone.0057870Suche in Google Scholar PubMed

Corsini, S., Tortora, M., and Nistri, A. (2016). Nicotinic receptor activation contrasts pathophysiological bursting and neurodegeneration evoked by glutamate uptake block on rat hypoglossal motoneurons. J. Physiol. 594, 6777–6798.10.1113/JP272591Suche in Google Scholar PubMed

Court, J., Keverne, J., Svedberg, M., Lee, M., Marutle, A., Thomas, A., Perry, E., Bednar, I., and Nordberg, A. (2004). Nicotine reduces Aβ in the brain and cerebral vessels of APPsw mice. Eur. J. Neurosci. 19, 2703–2710.10.1111/j.0953-816X.2004.03377.xSuche in Google Scholar

Craik, F.I. and Rose, N.S. (2012). Memory encoding and aging: a neurocognitive perspective. Neurosci. Biobehav. Rev. 36, 1729–1739.10.1016/j.neubiorev.2011.11.007Suche in Google Scholar PubMed

Cui, W., Hu, S., Chan, H.H., Luo, J., Li, W., Mak, S., Choi, T.C., Rong, J., Carlier, P.R., and Han, Y. (2013). Bis (12)-hupyridone, a novel acetylcholinesterase inhibitor, protects against glutamate-induced neuronal excitotoxicity via activating α7 nicotinic acetylcholine receptor/phosphoinositide 3-kinase/Akt cascade. Chem. Biol. Interact. 203, 365–370.10.1016/j.cbi.2012.10.003Suche in Google Scholar PubMed

Czubak, A., Nowakowska, E., Kus, K., Burda, K., Metelska, J., Baer-Dubowska, W., and Cichocki, M. (2009). Influences of chronic venlafaxine, olanzapine and nicotine on the hippocampal and cortical concentrations of brain-derived neurotrophic factor (BDNF). Pharmacol. Rep. 61, 1017–1023.10.1016/S1734-1140(09)70163-XSuche in Google Scholar PubMed

Czubak, A., Nowakowska, E., Kus, K., Matschay, A., and Kokot, Z. (2007). P. 1. c. 021 The effect of nicotine and mecamylamine on spatial memory in rats. Eur. Neuropsychopharmacol. 17, S253–S254.10.1016/S0924-977X(07)70345-0Suche in Google Scholar

Dajas-Bailador, F.A., Lima, P.A., and Wonnacott, S. (2000). The α7 nicotinic acetylcholine receptor subtype mediates nicotine protection against NMDA excitotoxicity in primary hippocampal cultures through a Ca2+ dependent mechanism. Neuropharmacology 39, 2799–2807.10.1016/S0028-3908(00)00127-1Suche in Google Scholar

Dani, J.A. and Heinemann, S. (1996). Molecular and cellular aspects of nicotine abuse. Neuron 16, 905–908.10.1016/S0896-6273(00)80112-9Suche in Google Scholar PubMed

Darsow, T., Booker, T., Piña-Crespo, J.C., and Heinemann, S.F. (2005). Exocytic trafficking is required for nicotine-induced up-regulation of α4β2 nicotinic acetylcholine receptors. J. Biol. Chem. 280, 18311–18320.10.1074/jbc.M501157200Suche in Google Scholar PubMed

Daugherty, A.M. and Raz, N. (2015). Appraising the role of iron in brain aging and cognition: promises and limitations of MRI methods. Neuropsychol. Rev. 25, 272–287.10.1007/s11065-015-9292-ySuche in Google Scholar PubMed

de Azevedo Cardoso, T., Mondin, T.C., Wiener, C.D., Marques, M.B., de Avila Fucolo, B., Pinheiro, R.T., de Souza, L.D.M., da Silva, R.A., Jansen, K., and Oses, J.P. (2014). Neurotrophic factors, clinical features and gender differences in depression. Neurochem. Res. 39, 1571–1578.10.1007/s11064-014-1349-4Suche in Google Scholar PubMed

De Rosa, R., Garcia, A.A., Braschi, C., Capsoni, S., Maffei, L., Berardi, N., and Cattaneo, A. (2005). Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc. Natl. Acad. Sci. USA 102, 3811–3816.10.1073/pnas.0500195102Suche in Google Scholar

Decker, M.W., Majchrzak, M.J., and Anderson, D.J. (1992). Effects of nicotine on spatial memory deficits in rats with septal lesions. Brain Res. 572, 281–285.10.1016/0006-8993(92)90485-RSuche in Google Scholar PubMed

Dietz, P. (2016). Physiology of Nicotine, Tobacco Cessation and Substance Abuse Treatment in Women’s Healthcare (Switzerland: Springer), pp. 25–32.Suche in Google Scholar

Dineley, K.T., Westerman, M., Bui, D., Bell, K., Ashe, K.H., and Sweatt, J.D. (2001). β-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal α7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer’s disease. J. Neurosci. 21, 4125–4133.10.1523/JNEUROSCI.21-12-04125.2001Suche in Google Scholar PubMed

Dumas, J.A. and Newhouse, P.A. (2011). The cholinergic hypothesis of cognitive aging revisited again: cholinergic functional compensation. Pharmacol. Biochem. Behav. 99, 254–261.10.1016/j.pbb.2011.02.022Suche in Google Scholar PubMed PubMed Central

Eilers, H., Schaeffer, E., Bickler, P.E., and Forsayeth, J.R. (1997). Functional deactivation of the major neuronal nicotinic receptor caused by nicotine and a protein kinase C-dependent mechanism. Mol. Pharmacol. 52, 1105–1112.10.1124/mol.52.6.1105Suche in Google Scholar

Erraji-Benchekroun, L., Underwood, M.D., Arango, V., Galfalvy, H., Pavlidis, P., Smyrniotopoulos, P., Mann, J.J., and Sibille, E. (2005). Molecular aging in human prefrontal cortex is selective and continuous throughout adult life. Biol. Psychiatry 57, 549–558.10.1016/j.biopsych.2004.10.034Suche in Google Scholar PubMed

Esposito, Z., Belli, L., Toniolo, S., Sancesario, G., Bianconi, C., and Martorana, A. (2013). Amyloid β, glutamate, excitotoxicity in Alzheimer’s disease: are we on the right track? CNS Neurosci. Ther. 19, 549–555.10.1111/cns.12095Suche in Google Scholar

Faghih, R., Gfesser, G.A., and Gopalakrishnan, M. (2007). Advances in the discovery of novel positive allosteric modulators of the α7 nicotinic acetylcholine receptor. Recent Pat. CNS Drug Discov. 2, 99–106.10.2174/157488907780832751Suche in Google Scholar PubMed

Fasoli, F., Moretti, M., Zoli, M., Pistillo, F., Crespi, A., Clementi, F., Mc Clure-Begley, T., Marks, M., and Gotti, C. (2016). In vivo chronic nicotine exposure differentially and reversibly affects upregulation and stoichiometry of α4β2 nicotinic receptors in cortex and thalamus. Neuropharmacology 108, 324–331.10.1016/j.neuropharm.2016.04.048Suche in Google Scholar PubMed

Ferger, B., Spratt, C., Earl, C.D., Teismann, P., Oertel, W.H., and Kuschinsky, K. (1998). Effects of nicotine on hydroxyl free radical formation in vitro and on MPTP-induced neurotoxicity in vivo. Naunyn-Schmiedeberg’s Arch. Pharmacol. 358, 351–359.10.1007/PL00005264Suche in Google Scholar

Ferrea, S. and Winterer, G. (2009). Neuroprotective and neurotoxic effects of nicotine. Pharmacopsychiatry 42, 255–265.10.1055/s-0029-1224138Suche in Google Scholar PubMed

Ferreira, L.K. and Busatto, G.F. (2013). Resting-state functional connectivity in normal brain aging. Neurosci. Biobehav. Rev. 37, 384–400.10.1016/j.neubiorev.2013.01.017Suche in Google Scholar PubMed

Fischer, W., Bjorklund, A., Chen, K., and Gage, F. (1991). NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 11, 1889–1906.10.1523/JNEUROSCI.11-07-01889.1991Suche in Google Scholar PubMed

Freedman, R., Wetmore, C., Stromberg, I., Leonard, S., and Olson, L. (1993). Alpha-bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression. J. Neurosci. 13, 1965–1975.10.1523/JNEUROSCI.13-05-01965.1993Suche in Google Scholar PubMed

Fukumoto, H., Asami-Odaka, A., Suzuki, N., Shimada, H., Ihara, Y., and Iwatsubo, T. (1996). Amyloid β protein deposition in normal aging has the same characteristics as that in Alzheimer’s disease. Predominance of Aβ 42 (43) and association of Aβ 40 with cored plaques. Am. J. Pathol. 148, 259–265.Suche in Google Scholar

Garrido, R., King-Pospisil, K., Son, K.W., Hennig, B., and Toborek, M. (2003). Nicotine upregulates nerve growth factor expression and prevents apoptosis of cultured spinal cord neurons. Neurosci Res. 47, 349–355.10.1016/S0168-0102(03)00222-0Suche in Google Scholar PubMed

Garrido, R., Mattson, M.P., Hennig, B., and Toborek, M. (2001). Nicotine protects against arachidonic-acid-induced caspase activation, cytochrome c release and apoptosis of cultured spinal cord neurons. J. Neurochem. 76, 1395–1403.10.1046/j.1471-4159.2001.00135.xSuche in Google Scholar PubMed

Gause, G. (1941). Analysis of various biological processes by the study of the differential action of optical isomers. Biodynamica 3, 217–246.Suche in Google Scholar

Glorioso, C. and Sibille, E. (2011). Between destiny and disease: genetics and molecular pathways of human central nervous system aging. Prog. Neurobiol. 93, 165–181.10.1016/j.pneurobio.2010.11.006Suche in Google Scholar PubMed

Godbout, J.P. and Johnson, R.W. (2009). Age and neuroinflammation: a lifetime of psychoneuroimmune consequences. Immunol. Allergy Clin. North Am. 29, 321–337.10.1016/j.iac.2009.02.007Suche in Google Scholar PubMed

Goerig, P.-D.D.M., Ullrich, V., Schettler, G., Foltis, C., and Habenicht, A. (1992). A new role for nicotine: selective inhibition of thromboxane formation by direct interaction with thromboxane synthase in human promyelocytic leukaemia cells differentiating into macrophages. Clin. Investig. 70, 239–243.10.1007/BF00184657Suche in Google Scholar PubMed

Gould, T.J., Wilkinson, D.S., Yildirim, E., Poole, R.L., Leach, P.T., and Simmons, S.J. (2014). Nicotine shifts the temporal activation of hippocampal protein kinase A and extracellular signal-regulated kinase 1/2 to enhance long-term, but not short-term, hippocampus-dependent memory. Neurobiol. Learn. Mem. 109, 151–159.10.1016/j.nlm.2014.01.009Suche in Google Scholar PubMed

Govind, A.P., Vezina, P., and Green, W.N. (2009). Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction. Biochem. Pharmacol. 78, 756–765.10.1016/j.bcp.2009.06.011Suche in Google Scholar PubMed

Govind, A.P., Walsh, H., and Green, W.N. (2012). Nicotine-induced upregulation of native neuronal nicotinic receptors is caused by multiple mechanisms. J. Neurosci. 32, 2227–2238.10.1523/JNEUROSCI.5438-11.2012Suche in Google Scholar PubMed

Guan, Z.-Z., Yu, W.-F., and Nordberg, A. (2003). Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells. Neurochem. Int. 43, 243–249.10.1016/S0197-0186(03)00009-3Suche in Google Scholar PubMed

Haass, M. and Kübler, W. (1997). Nicotine and sympathetic neurotransmission. Cardiovasc. Drugs Ther. 10, 657–665.10.1007/BF00053022Suche in Google Scholar PubMed

Haddadi, M., Jahromi, S.R., Sagar, B.C., Patil, R.K., Shivanandappa, T., and Ramesh, S. (2014). Brain aging, memory impairment and oxidative stress: a study in Drosophila melanogaster. Behav. Brain Res. 259, 60–69.10.1016/j.bbr.2013.10.036Suche in Google Scholar PubMed

Han, Y. and Lau, Y.-l. (2014). Nicotine, an anti-inflammation molecule. Inflamm. Cell Signal. 1, e155.Suche in Google Scholar

Hao, J., Simard, A.R., Turner, G.H., Wu, J., Whiteaker, P., Lukas, R.J., and Shi, F.-D. (2011). Attenuation of CNS inflammatory responses by nicotine involves α7 and non-α7 nicotinic receptors. Exp. Neurol. 227, 110–119.10.1016/j.expneurol.2010.09.020Suche in Google Scholar PubMed

Harada, C. and Harada, T. (2014). Neurotrophic factors, Neuroprotection and Neuroregeneration for Retinal Diseases (Japan: Springer), pp. 99–112.Suche in Google Scholar

Hejmadi, M., Dajas-Bailador, F., Barns, S., Jones, B., and Wonnacott, S. (2003). Neuroprotection by nicotine against hypoxia-induced apoptosis in cortical cultures involves activation of multiple nicotinic acetylcholine receptor subtypes. Mol. Cell. Neurosci. 24, 779–786.10.1016/S1044-7431(03)00244-6Suche in Google Scholar PubMed

Henningfield, J.E. (1995). Nicotine medications for smoking cessation. N. Engl. J. Med. 333, 1196–1203.10.1056/NEJM199511023331807Suche in Google Scholar PubMed

Hernandez, C.M. and Terry, A.V. (2005). Repeated nicotine exposure in rats: effects on memory function, cholinergic markers and nerve growth factor. Neuroscience 130, 997–1012.10.1016/j.neuroscience.2004.10.006Suche in Google Scholar PubMed

Heusch, W.L. and Maneckjee, R. (1998). Signalling pathways involved in nicotine regulation of apoptosis of human lung cancer cells. Carcinogens 19, 551–556.10.1093/carcin/19.4.551Suche in Google Scholar

Holmes, C., Boche, D., Wilkinson, D., Yadegarfar, G., Hopkins, V., Bayer, A., Jones, R.W., Bullock, R., Love, S., and Neal, J.W. (2008). Long-term effects of Aβ 42 immunisation in Alzheimer’s disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372, 216–223.10.1016/S0140-6736(08)61075-2Suche in Google Scholar PubMed

Hughes, J.R. (1998). Dependence on and abuse of nicotine replacement medications: an update. Nicotine Safety Toxicity (New York: Oxford University Press), pp. 147–157.Suche in Google Scholar

Inestrosa, N.C., Godoy, J.A., Vargas, J.Y., Arrazola, M.S., Rios, J.A., Carvajal, F.J., Serrano, F.G., and Farias, G.G. (2013). Nicotine prevents synaptic impairment induced by amyloid-β oligomers through α7-nicotinic acetylcholine receptor activation. Neuromol. Med. 15, 549–569.10.1007/s12017-013-8242-1Suche in Google Scholar PubMed

Inestrosa, N.C., Montecinos-Oliva, C., and Fuenzalida, M. (2012). Wnt signaling: role in Alzheimer disease and schizophrenia. J. Neuroimmun. Pharmacol. 7, 788–807.10.1007/s11481-012-9417-5Suche in Google Scholar PubMed

Jensen, K., Nizamutdinov, D., Guerrier, M., Afroze, S., Dostal, D., and Glaser, S. (2012). General mechanisms of nicotine-induced fibrogenesis. FASEB J. 26, 4778–4787.10.1096/fj.12-206458Suche in Google Scholar PubMed PubMed Central

Kiss, T. (2010). Apoptosis and its functional significance in molluscs. Apoptosis 15, 313–321.10.1007/s10495-009-0446-3Suche in Google Scholar PubMed

Kumar, V.B., Farr, S.A., Flood, J.F., Kamlesh, V., Franko, M., Banks, W.A., and Morley, J.E. (2000). Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides 21, 1769–1775.10.1016/S0196-9781(00)00339-9Suche in Google Scholar PubMed

Le Houezec, J. (2003). Role of nicotine pharmacokinetics in nicotine addiction and nicotine replacement therapy: a review. Int. J. Tuberc. Lung Dis. 7, 811–819.Suche in Google Scholar PubMed

Lemay, S., Chouinard, S., Blanchet, P., Masson, H., Soland, V., Beuter, A., and Bédard, M.-A. (2004). Lack of efficacy of a nicotine transdermal treatment on motor and cognitive deficits in Parkinson’s disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 28, 31–39.10.1016/S0278-5846(03)00172-6Suche in Google Scholar PubMed

Levin, E.D., McClernon, F.J., and Rezvani, A.H. (2006). Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology 184, 523–539.10.1007/s00213-005-0164-7Suche in Google Scholar PubMed

Levin, E.D. and Torry, D. (1996). Acute and chronic nicotine effects on working memory in aged rats. Psychopharmacology 123, 88–97.10.1007/BF02246285Suche in Google Scholar PubMed

LI, Y.-T., JIN, G.-R., and XU, H.-R. (2005). The effect of GDNF on the proliferating cells of SVZ and SGZ as well as the recovery of learning and memory in adult rats after focal cerebral ischemia. J Apoplexy Nerv. Dis. 2, 004.Suche in Google Scholar

Liechti, M.E. and Markou, A. (2008). Role of the glutamatergic system in nicotine dependence. CNS Drugs 22, 705–724.10.2165/00023210-200822090-00001Suche in Google Scholar PubMed

Liepelt, I., Gaenslen, A., Godau, J., Di Santo, A., Schweitzer, K.J., Gasser, T., and Berg, D. (2010). Rivastigmine for the treatment of dementia in patients with progressive supranuclear palsy: clinical observations as a basis for power calculations and safety analysis. Alzheimers Dement. 6, 70–74.10.1016/j.jalz.2009.04.1231Suche in Google Scholar PubMed

Linert, W., Bridge, M., Huber, M., Bjugstad, K., Grossman, S., and Arendash, G. (1999). In vitro and in vivo studies investigating possible antioxidant actions of nicotine: relevance to Parkinson’s and Alzheimer’s diseases. Biochim. Biophys. Acta 1454, 143–152.10.1016/S0925-4439(99)00029-0Suche in Google Scholar PubMed

Liu, Q., and Zhao, B. (2004). Nicotine attenuates β-amyloid peptide-induced neurotoxicity, free radical and calcium accumulation in hippocampal neuronal cultures. Br. J. Pharmacol. 141, 746–754.10.1038/sj.bjp.0705653Suche in Google Scholar PubMed PubMed Central

Liu, Y., Hu, J., Wu, J., Zhu, C., Hui, Y., Han, Y., Huang, Z., Ellsworth, K., and Fan, W. (2012). α7 nicotinic acetylcholine receptor-mediated neuroprotection against dopaminergic neuron loss in an MPTP mouse model via inhibition of astrocyte activation. J. Neuroinflamm. 9, 98.10.1186/1742-2094-9-98Suche in Google Scholar PubMed PubMed Central

Logemann, H., Böcker, K., Deschamps, P., Kemner, C., and Kenemans, J. (2014). The effect of enhancing cholinergic neurotransmission by nicotine on EEG indices of inhibition in the human brain. Pharmacol. Biochem. Behav. 122, 89–96.10.1016/j.pbb.2014.03.019Suche in Google Scholar PubMed

Lu, B., Nagappan, G., and Lu, Y. (2014). BDNF and Synaptic Plasticity, Cognitive Function, and Dysfunction, Neurotrophic Factors (Berlin Heidelberg: Springer), pp. 223–250.10.1007/978-3-642-45106-5_9Suche in Google Scholar PubMed

Mai, H., May, W.S., Gao, F., Jin, Z., and Deng, X. (2003). A functional role for nicotine in Bcl2 phosphorylation and suppression of apoptosis. J. Biol. Chem. 278, 1886–1891.10.1074/jbc.M209044200Suche in Google Scholar PubMed

Majdi, A., Mahmoudi, J., Sadigh-Eteghad, S., Farhoudi, M., and Shotorbani, S.S. (2016a). The interplay of microRNAs and post-ischemic glutamate excitotoxicity: an emergent research field in stroke medicine. Neurol. Sci. 37, 1765–1771.10.1007/s10072-016-2643-5Suche in Google Scholar PubMed

Majdi, A., Mahmoudi, J., Sadigh-Eteghad, S., Golzari, S.E., Sabermarouf, B., and Reyhani-Rad, S. (2016b). Permissive role of cytosolic pH acidification in neurodegeneration: a closer look at its causes and consequences. J. Neurosci. Res. 94, 879–887.10.1002/jnr.23757Suche in Google Scholar PubMed

Mansvelder, H.D., Mertz, M., and Role, L.W. (2009). Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits. Semin. Cell Dev. Biol. 20, 432–440.10.1016/j.semcdb.2009.01.007Suche in Google Scholar PubMed PubMed Central

Markou, A. and Paterson, N.E. (2001). The nicotinic antagonist methyllycaconitine has differential effects on nicotine self-administration and nicotine withdrawal in the rat. Nicotine Tob. Res. 3, 361–373.10.1080/14622200110073380Suche in Google Scholar PubMed

Marks, M.J., Pauly, J.R., Gross, S.D., Deneris, E.S., Hermans-Borgmeyer, I., Heinemann, S.F., and Collins, A.C. (1992). Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 12, 2765–2784.10.1523/JNEUROSCI.12-07-02765.1992Suche in Google Scholar PubMed

Marrero, M.B. and Bencherif, M. (2009). Convergence of alpha 7 nicotinic acetylcholine receptor-activated pathways for anti-apoptosis and anti-inflammation: central role for JAK2 activation of STAT3 and NF-κB. Brain Res. 1256, 1–7.10.1016/j.brainres.2008.11.053Suche in Google Scholar PubMed

Martínez-Rodríguez, R., Toledano, A., Alvarez, M., Turégano, L., Colman, O., Rosés, P., Gómez de Segura, I., and De Miguel, E. (2003). Chronic nicotine administration increases NGF-like immunoreactivity in frontoparietal cerebral cortex. J. Neurosci. Res. 73, 708–716.10.1002/jnr.10688Suche in Google Scholar PubMed

Maskos, U., Molles, B., Pons, S., Besson, M., Guiard, B., Guilloux, J.-P., Evrard, A., Cazala, P., Cormier, A., and Mameli-Engvall, M. (2005). Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436, 103–107.10.1038/nature03694Suche in Google Scholar PubMed

Matta, S.G., Balfour, D.J., Benowitz, N.L., Boyd, R.T., Buccafusco, J.J., Caggiula, A.R., Craig, C.R., Collins, A.C., Damaj, M.I., and Donny, E.C. (2007). Guidelines on nicotine dose selection for in vivo research. Psychopharmacology 190, 269–319.10.1007/s00213-006-0441-0Suche in Google Scholar PubMed

McEwen, B.S. (2000). Allostasis, allostatic load, and the aging nervous system: role of excitatory amino acids and excitotoxicity. Neurochem. Res. 25, 1219–1231.10.1023/A:1007687911139Suche in Google Scholar PubMed

Mora, F. (2013). Successful brain aging: plasticity, environmental enrichment, and lifestyle. Dialogues Clin. Neurosci. 15, 45–52.10.31887/DCNS.2013.15.1/fmoraSuche in Google Scholar PubMed

Mora, F., Segovia, G., and del Arco, A. (2007). Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res. Rev. 55, 78–88.10.1016/j.brainresrev.2007.03.011Suche in Google Scholar PubMed

Moragrega, I., Carrasco, M., Vicens, P., and Redolat, R. (2003). Spatial learning in male mice with different levels of aggressiveness: effects of housing conditions and nicotine administration. Behav. Brain Res. 147, 1–8.10.1016/S0166-4328(03)00112-8Suche in Google Scholar PubMed

Morley, J.E., Kumar, V.B., Bernardo, A.E., Farr, S.A., Uezu, K., Tumosa, N., and Flood, J.F. (2000). β-Amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 21, 1761–1767.10.1016/S0196-9781(00)00342-9Suche in Google Scholar PubMed

Mufson, E.J., Counts, S.E., Perez, S.E., and Ginsberg, S.D. (2008). Cholinergic system during the progression of Alzheimer’s disease: therapeutic implications. Expert Rev Neurother. 8, 1703–1718.10.1586/14737175.8.11.1703Suche in Google Scholar PubMed PubMed Central

Nakauchi, S. and Sumikawa, K. (2012). Endogenously released ACh and exogenous nicotine differentially facilitate long-term potentiation induction in the hippocampal CA1 region of mice. Eur. J. Neurosci. 35, 1381–1395.10.1111/j.1460-9568.2012.08056.xSuche in Google Scholar PubMed PubMed Central

Newhouse, P., Kellar, K., Aisen, P., White, H., Wesnes, K., Coderre, E., Pfaff, A., Wilkins, H., Howard, D., and Levin, E. (2012). Nicotine treatment of mild cognitive impairment: a 6-month double-blind pilot clinical trial. Neurology 78, 91–101.10.1212/WNL.0b013e31823efcbbSuche in Google Scholar PubMed PubMed Central

Newhouse, P.A., Sunderland, T., Tariot, P.N., Blumhardt, C., Weingartner, H., Mellow, A., and Murphy, D. (1988). Intravenous nicotine in Alzheimer’s disease: a pilot study. Psychopharmacology 95, 171–175.10.1007/BF00174504Suche in Google Scholar PubMed

Nizri, E., Irony-Tur-Sinai, M., Lory, O., Orr-Urtreger, A., Lavi, E., and Brenner, T. (2009). Activation of the cholinergic anti-inflammatory system by nicotine attenuates neuroinflammation via suppression of Th1 and Th17 responses. J. Immunol. 183, 6681–6688.10.4049/jimmunol.0902212Suche in Google Scholar PubMed

Nordberg, A., Hellström-Lindahl, E., Lee, M., Johnson, M., Mousavi, M., Hall, R., Perry, E., Bednar, I., and Court, J. (2002). Chronic nicotine treatment reduces β-amyloidosis in the brain of a mouse model of Alzheimer’s disease (APPsw). J. Neurochem. 81, 655–658.10.1046/j.1471-4159.2002.00874.xSuche in Google Scholar PubMed

Ono, K., Hasegawa, K., Yamada, M., and Naiki, H. (2002). Nicotine breaks down preformed Alzheimer’s β-amyloid fibrils in vitro. Biol. Psychiatry 52, 880–886.10.1016/S0006-3223(02)01417-8Suche in Google Scholar PubMed

Ortega, L.A., Tracy, B.A., Gould, T.J., and Parikh, V. (2013). Effects of chronic low-and high-dose nicotine on cognitive flexibility in C57BL/6J mice. Behav. Brain Res. 238, 134–145.10.1016/j.bbr.2012.10.032Suche in Google Scholar PubMed

Oz, M., Petroianu, G., and Lorke, D.E. (2016). α7-Nicotinic acetylcholine receptors: new therapeutic avenues in Alzheimer’s disease. Nicotinic Acetylcholine Receptor Technologies, Ming D. Li, ed. (New York: Springer), pp. 149–169.10.1007/978-1-4939-3768-4_9Suche in Google Scholar

Pachauri, V. and Flora, S. (2013). Effect of nicotine pretreatment on arsenic-induced oxidative stress in male Wistar rats. Hum. Exp. Toxicol. 32, 972–982.10.1177/0960327112474833Suche in Google Scholar PubMed

Padurariu, M., Ciobica, A., Hritcu, L., Stoica, B., Bild, W., and Stefanescu, C. (2010). Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer’s disease. Neurosci Lett. 469, 6–10.10.1016/j.neulet.2009.11.033Suche in Google Scholar PubMed

Papke, R.L., Kem, W.R., Soti, F., Lopez-Hernandez, G.Y., and Horenstein, N.A. (2009). Activation and desensitization of nicotinic α7-type acetylcholine receptors by benzylidene anabaseines and nicotine. J. Pharmacol. Exp. Ther. 329, 791–807.10.1124/jpet.108.150151Suche in Google Scholar PubMed

Pavlov, V. and Tracey, K. (2006). Controlling inflammation: the cholinergic anti-inflammatory pathway. Biochem. Soc. T. 34, 1037–1040.10.1042/BST0341037Suche in Google Scholar

Peng, X., Gerzanich, V., Anand, R., Whiting, P.J., and Lindstrom, J. (1994). Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol. Pharmacol. 46, 523–530.Suche in Google Scholar PubMed

Picciotto, M.R. (2003). Nicotine as a modulator of behavior: beyond the inverted U. Trends Pharmacol. Sci. 24, 493–499.10.1016/S0165-6147(03)00230-XSuche in Google Scholar PubMed

Pons, S., Fattore, L., Cossu, G., Tolu, S., Porcu, E., McIntosh, J.M., Changeux, J., Maskos, U., and Fratta, W. (2008). Crucial role of α4 and α6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J. Neurosci. 28, 12318–12327.10.1523/JNEUROSCI.3918-08.2008Suche in Google Scholar PubMed PubMed Central

Potter, A.S. and Newhouse, P.A. (2008). Acute nicotine improves cognitive deficits in young adults with attention-deficit/hyperactivity disorder. Pharmacol. Biochem. Behav. 88, 407–417.10.1016/j.pbb.2007.09.014Suche in Google Scholar PubMed

Pourmemar, E., Majdi, A., Haramshahi, M., Talebi, M., Karimi, P., and Sadigh-Eteghad, S. (2017). Intranasal cerebrolysin attenuates learning and memory impairments in D-galactose-induced senescence in mice. Exp. Gerontol. 87, 16–22.10.1016/j.exger.2016.11.011Suche in Google Scholar PubMed

Powledge, T.M. (2004). Nicotine as therapy. PLoS Biol. 2, e404.10.1371/journal.pbio.0020404Suche in Google Scholar PubMed PubMed Central

Quik, M., O’Leary, K., and Tanner, C.M. (2008). Nicotine and Parkinson’s disease: implications for therapy. Mov. Disord. 23, 1641–1652.10.1002/mds.21900Suche in Google Scholar PubMed PubMed Central

Razani-Boroujerdi, S., Boyd, R.T., Dávila-García, M.I., Nandi, J.S., Mishra, N.C., Singh, S.P., Pena-Philippides, J.C., Langley, R., and Sopori, M.L. (2007). T cells express α7-nicotinic acetylcholine receptor subunits that require a functional TCR and leukocyte-specific protein tyrosine kinase for nicotine-induced Ca2+ response. J. Immunol. 179, 2889–2898.10.4049/jimmunol.179.5.2889Suche in Google Scholar PubMed

Rezvani, K., Teng, Y., Shim, D., and De Biasi, M. (2007). Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J. Neurosci. 27, 10508–10519.10.1523/JNEUROSCI.3353-07.2007Suche in Google Scholar PubMed PubMed Central

Rodrigue, K., Kennedy, K., Devous, M., Rieck, J., Hebrank, A., Diaz-Arrastia, R., Mathews, D., and Park, D. (2012). β-Amyloid burden in healthy aging Regional distribution and cognitive consequences. Neurology 78, 387–395.10.1212/WNL.0b013e318245d295Suche in Google Scholar PubMed PubMed Central

Russell, M.A. (1991). The future of nicotine replacement. Br. J. Addict. 86, 653–658.10.1111/j.1360-0443.1991.tb01825.xSuche in Google Scholar PubMed

Russo, I., Barlati, S., and Bosetti, F. (2011). Effects of neuroinflammation on the regenerative capacity of brain stem cells. J. Neurochem. 116, 947–956.10.1111/j.1471-4159.2010.07168.xSuche in Google Scholar PubMed PubMed Central

Sadigh-Eteghad, S., Talebi, M., Farhoudi, M., Golzari, S.E., Sabermarouf, B., and Mahmoudi, J. (2014). Beta-amyloid exhibits antagonistic effects on alpha 7 nicotinic acetylcholine receptors in orchestrated manner. J Med Hypotheses Ideas 8, 49–52.10.1016/j.jmhi.2014.01.001Suche in Google Scholar

Sadigh-Eteghad, S., Majdi, A., Talebi, M., Mahmoudi, J., and Babri, S. (2015a). Regulation of nicotinic acetylcholine receptors in Alzheimer’s disease: a possible role of chaperones. Eur. J. Pharmacol. 755, 34–41.10.1016/j.ejphar.2015.02.047Suche in Google Scholar PubMed

Sadigh-Eteghad, S., Talebi, M., Mahmoudi, J., Babri, S., and Shanehbandi, D. (2015b). Selective activation of α 7 nicotinic acetylcholine receptor by PHA-543613 improves Aβ 25–35-mediated cognitive deficits in mice. Neuroscience 298, 81–93.10.1016/j.neuroscience.2015.04.017Suche in Google Scholar PubMed

Sadigh-Eteghad, S., Askari-Nejad, M.S., Mahmoudi, J., and Majdi, A. (2016a). Cargo trafficking in Alzheimer’s disease: the possible role of retromer. Neurol Sci. 37, 17–22.10.1007/s10072-015-2399-3Suche in Google Scholar PubMed

Sadigh-Eteghad, S., Majdi, A., Mahmoudi, J., Golzari, S.E., and Talebi, M. (2016b). Astrocytic and microglial nicotinic acetylcholine receptors: an overlooked issue in Alzheimer’s disease. J. Neural. Transm. 123, 1359–1367.10.1007/s00702-016-1580-zSuche in Google Scholar PubMed

Sahakian, B., Jones, G., Levy, R., Gray, J., and Warburton, D. (1989). The effects of nicotine on attention, information processing, and short-term memory in patients with dementia of the Alzheimer type. Br. J. Psychiatry 154, 797–800.10.1192/bjp.154.6.797Suche in Google Scholar PubMed

Sallette, J., Pons, S., Devillers-Thiery, A., Soudant, M., de Carvalho, L.P., Changeux, J.-P., and Corringer, P.J. (2005). Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46, 595–607.10.1016/j.neuron.2005.03.029Suche in Google Scholar PubMed

Samaha, A.-N. and Robinson, T.E. (2005). Why does the rapid delivery of drugs to the brain promote addiction? Trends Pharmacol. Sci. 26, 82–87.Suche in Google Scholar

Scherma, M., Fadda, P., Foll, B.L., Forget, B., Fratta, W., Goldberg, S.R., and Tanda, G. (2008). The endocannabinoid system: a new molecular target for the treatment of tobacco addiction. CNS Neurol. Disord. Drug Targets 7, 468–481.10.2174/187152708786927859Suche in Google Scholar PubMed PubMed Central

Schliebs, R. and Arendt, T. (2011). The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 221, 555–563.10.1016/j.bbr.2010.11.058Suche in Google Scholar PubMed

Shen, H., Kihara, T., Hongo, H., Wu, X., Kem, W., Shimohama, S., Akaike, A., Niidome, T., and Sugimoto, H. (2010). Neuroprotection by donepezil against glutamate excitotoxicity involves stimulation of α7 nicotinic receptors and internalization of NMDA receptors. Br. J. Pharmacol. 161, 127–139.10.1111/j.1476-5381.2010.00894.xSuche in Google Scholar PubMed PubMed Central

Shi, F.-D., Piao, W.-H., Kuo, Y.-P., Campagnolo, D.I., Vollmer, T.L., and Lukas, R.J. (2009). Nicotinic attenuation of central nervous system inflammation and autoimmunity. J. Immunol. 182, 1730–1739.10.4049/jimmunol.182.3.1730Suche in Google Scholar PubMed

Shimohama, S. (2009). Nicotinic receptor-mediated neuroprotection in neurodegenerative disease models. Biol. Pharm. Bull. 32, 332–336.10.1248/bpb.32.332Suche in Google Scholar PubMed

Shimohama, S., Greenwald, D., Shafron, D., Akaika, A., Maeda, T., Kaneko, S., Kimura, J., Simpkins, C., Day, A., and Meyer, E. (1998). Nicotinic α7 receptors protect against glutamate neurotoxicity and neuronal ischemic damage. Brain Res. 779, 359–363.10.1016/S0006-8993(97)00194-7Suche in Google Scholar PubMed

Shytle, R.D., Mori, T., Townsend, K., Vendrame, M., Sun, N., Zeng, J., Ehrhart, J., Silver, A.A., Sanberg, P.R., and Tan, J. (2004). Cholinergic modulation of microglial activation by α7 nicotinic receptors. J. Neurochem. 89, 337–343.10.1046/j.1471-4159.2004.02347.xSuche in Google Scholar PubMed

Sibille, E. (2013). Molecular aging of the brain, neuroplasticity, and vulnerability to depression and other brain-related disorders. Dialogues Clin. Neurosci. 15, 53–65.10.31887/DCNS.2013.15.1/esibilleSuche in Google Scholar PubMed

Skaper, S.D. (2012). The neurotrophin family of neurotrophic factors: an overview. Methods Mol. Biol. 846, 1–12.10.1007/978-1-61779-536-7_1Suche in Google Scholar PubMed

Smith, R.C., Warner-Cohen, J., Matute, M., Butler, E., Kelly, E., Vaidhyanathaswamy, S., and Khan, A. (2006). Effects of nicotine nasal spray on cognitive function in schizophrenia. Neuropsychopharmacology 31, 637–643.10.1038/sj.npp.1300881Suche in Google Scholar PubMed

Socci, D.J., Sanberg, P.R., and Arendash, G.W. (1995). Nicotine enhances Morris water maze performance of young and aged rats. Neurobiol. Aging 16, 857–860.10.1016/0197-4580(95)00091-RSuche in Google Scholar

Song, G., Nesil, T., Cao, J., Yang, Z., Chang, S.L., and Li, M.D. (2016). Nicotine mediates expression of genes related to antioxidant capacity and oxidative stress response in HIV-1 transgenic rat brain. J. Neurovirol. 22, 114–124.10.1007/s13365-015-0375-6Suche in Google Scholar PubMed

Soto-Otero, R., Méndez-Álvarez, E.A., Hermida-Ameijeiras, A., López-Real, A.M.A., and Labandeira-Garcı́a, J.L. (2002). Effects of (−)-nicotine and (−)-cotinine on 6-hydroxydopamine-induced oxidative stress and neurotoxicity: relevance for Parkinson’s disease. Biochem. Pharmacol. 64, 125–135.10.1016/S0006-2952(02)01070-5Suche in Google Scholar PubMed

Srivareerat, M., Tran, T.T., Salim, S., Aleisa, A.M., and Alkadhi, K.A. (2011). Chronic nicotine restores normal Aβ levels and prevents short-term memory and E-LTP impairment in Aβ rat model of Alzheimer’s disease. Neurobiol. Aging 32, 834–844.10.1016/j.neurobiolaging.2009.04.015Suche in Google Scholar PubMed

Suzuki, T., Hide, I., Matsubara, A., Hama, C., Harada, K., Miyano, K., Andrä, M., Matsubayashi, H., Sakai, N., and Kohsaka, S. (2006). Microglial α7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. J. Neurosci. Res. 83, 1461–1470.10.1002/jnr.20850Suche in Google Scholar PubMed

Sweatt, J.D. (2004). Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 14, 311–317.10.1016/j.conb.2004.04.001Suche in Google Scholar PubMed

Tizabi, Y., Manaye, K.F., and Taylor, R.E. (2005). Nicotine blocks ethanol-induced apoptosis in primary cultures of rat cerebral cortical and cerebellar granule cells. Neurosci Res. 7, 319–322.10.1007/BF03033888Suche in Google Scholar PubMed

Toescu, E.C., Verkhratsky, A., and Landfield, P.W. (2004). Ca2+ regulation and gene expression in normal brain aging. Trends Neurosci. 27, 614–620.10.1016/j.tins.2004.07.010Suche in Google Scholar PubMed

Trachtenberg, J.T., Chen, B.E., Knott, G.W., Feng, G., Sanes, J.R., Welker, E., and Svoboda, K. (2002). Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788–794.10.1038/nature01273Suche in Google Scholar PubMed

Tyler, W.J., Alonso, M., Bramham, C.R., and Pozzo-Miller, L.D. (2002). From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn. Mem. 9, 224–237.10.1101/lm.51202Suche in Google Scholar PubMed PubMed Central

Utsuki, T., Shoaib, M., Holloway, H.W., Ingram, D.K., Wallace, W.C., Haroutunian, V., Sambamurti, K., Lahiri, D.K., and Greig, N.H. (2002). Nicotine lowers the secretion of the Alzheimer’s amyloid β-protein precursor that contains amyloid β-peptide in rat. J. Alzheimers Dis. 4, 405–415.10.3233/JAD-2002-4507Suche in Google Scholar PubMed

Vafaee, M.S., Gjedde, A., Imamirad, N., Vang, K., Chakravarty, M.M., Lerch, J.P., and Cumming, P. (2015). Smoking normalizes cerebral blood flow and oxygen consumption after 12-hour abstention. J. Cereb. Blood Flow Metab. 35, 699–705.10.1038/jcbfm.2014.246Suche in Google Scholar PubMed PubMed Central

Vaya, J. (2013). Exogenous markers for the characterization of human diseases associated with oxidative stress. Biochimie 95, 578–584.10.1016/j.biochi.2012.03.005Suche in Google Scholar PubMed

Ward, R.J., Zucca, F.A., Duyn, J.H., Crichton, R.R., and Zecca, L. (2014). The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 13, 1045–1060.10.1016/S1474-4422(14)70117-6Suche in Google Scholar PubMed

Wei, P., Liu, Q., Li, D., Zheng, Q., Zhou, J., and Li, J. (2015). Acute nicotine treatment attenuates lipopolysaccharide-induced cognitive dysfunction by increasing BDNF expression and inhibiting neuroinflammation in the rat hippocampus. Neurosci Lett. 604, 161–166.10.1016/j.neulet.2015.08.008Suche in Google Scholar PubMed

Whalley, L.J., Deary, I.J., Appleton, C.L., and Starr, J.M. (2004). Cognitive reserve and the neurobiology of cognitive aging. Ageing Res. Rev. 3, 369–382.10.1016/j.arr.2004.05.001Suche in Google Scholar PubMed

White, H.K. and Levin, E.D. (1999). Four-week nicotine skin patch treatment effects on cognitive performance in Alzheimer’s disease. Psychopharmacology 143, 158–165.10.1007/s002130050931Suche in Google Scholar PubMed

White, H.K. and Levin, E.D. (2004). Chronic transdermal nicotine patch treatment effects on cognitive performance in age-associated memory impairment. Psychopharmacology 171, 465–471.10.1007/s00213-003-1614-8Suche in Google Scholar PubMed

Wilson, A.L., Langley, L.K., Monley, J., Bauer, T., Rottunda, S., McFalls, E., Kovera, C., and McCarten, J.R. (1995). Nicotine patches in Alzheimer’s disease: pilot study on learning, memory, and safety. Pharmacol. Biochem. Behav. 51, 509–514.10.1016/0091-3057(95)00043-VSuche in Google Scholar PubMed

Wongtrakool, C., Grooms, K., Bijli, K.M., Crothers, K., Fitzpatrick, A.M., and Hart, C.M. (2014). Nicotine stimulates nerve growth factor in lung fibroblasts through an NFκB-dependent mechanism. PLos One 9, e109602.10.1371/journal.pone.0109602Suche in Google Scholar PubMed

Wonnacott, S. (1990). The paradox of nicotinic acetylcholine receptor upregulation by nicotine. Trends Pharmacol. Sci. 11, 216–219.10.1016/0165-6147(90)90242-ZSuche in Google Scholar PubMed

Wozniak, D.F., Hartman, R.E., Boyle, M.P., Vogt, S.K., Brooks, A.R., Tenkova, T., Young, C., Olney, J.W., and Muglia, L.J. (2004). Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol. Dis. 17, 403–414.10.1016/j.nbd.2004.08.006Suche in Google Scholar PubMed

Xiaolin, Z., Fei, G., and Etang, T. (2002). Effects of nicotine on GDNF and dopamine content in striatum of Parkinson’s disease rats. J. Clin. Neurol. 3, 004.Suche in Google Scholar

Yamada, K., Mizuno, M., and Nabeshima, T. (2002). Role for brain-derived neurotrophic factor in learning and memory. Life Sci. 70, 735–744.10.1016/S0024-3205(01)01461-8Suche in Google Scholar PubMed

Yamazaki, Y., Hamaue, N., and Sumikawa, K. (2002). Nicotine compensates for the loss of cholinergic function to enhance long-term potentiation induction. Brain Res. 946, 148–152.10.1016/S0006-8993(02)02935-9Suche in Google Scholar PubMed

Yildiz, D., Ercal, N., and Armstrong, D.W. (1998). Nicotine enantiomers and oxidative stress. Toxicology 130, 155–165.10.1016/S0300-483X(98)00105-XSuche in Google Scholar PubMed

Yoshikawa, H., Kurokawa, M., Ozaki, N., Nara, K., Atou, K., Takada, E., Kamochi, H., and Suzuki, N. (2006). Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-κB phosphorylation and nuclear factor-κB transcriptional activity through nicotinic acetylcholine receptor α7. Clin. Exp. Immunol. 146, 116–123.10.1111/j.1365-2249.2006.03169.xSuche in Google Scholar PubMed PubMed Central

Ypsilanti, A.R., da Cruz, M.T.G., Burgess, A., and Aubert, I. (2008). The length of hippocampal cholinergic fibers is reduced in the aging brain. Neurobiol. Aging 29, 1666–1679.10.1016/j.neurobiolaging.2007.04.001Suche in Google Scholar PubMed

Yu, W., Mechawar, N., Krantic, S., and Quirion, R. (2011). α7 Nicotinic receptor activation reduces β-amyloid-induced apoptosis by inhibiting caspase-independent death through phosphatidylinositol 3-kinase signaling. J. Neurochem. 119, 848–858.10.1111/j.1471-4159.2011.07466.xSuche in Google Scholar PubMed

Zahs, K.R. and Ashe, K.H. (2013). β-Amyloid oligomers in aging and Alzheimer’s disease. Front. Aging Neurosci. 5, 28.10.3389/fnagi.2013.00028Suche in Google Scholar PubMed PubMed Central

Zouridakis, M., Zisimopoulou, P., Poulas, K., and Tzartos, S.J. (2009). Recent advances in understanding the structure of nicotinic acetylcholine receptors. IUBMB Life 61, 407–423.10.1002/iub.170Suche in Google Scholar PubMed

Received: 2017-2-4
Accepted: 2017-4-12
Published Online: 2017-6-6
Published in Print: 2017-10-26

©2017 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 16.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2017-0008/html
Button zum nach oben scrollen