Startseite BDNF and nicotine dependence: associations and potential mechanisms
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

BDNF and nicotine dependence: associations and potential mechanisms

  • Zeyi Huang , Daichao Wu , Xilin Qu , Meixiang Li EMAIL logo , Ju Zou und Sijie Tan EMAIL logo
Veröffentlicht/Copyright: 4. September 2020
Veröffentlichen auch Sie bei De Gruyter Brill

Abstract

Smoking is the leading preventable cause of death worldwide and tobacco addiction has become a serious public health problem. Nicotine is the main addictive component of tobacco, and the majority of people that smoke regularly develop nicotine dependence. Nicotine addiction is deemed to be a chronic mental disorder. Although it is well known that nicotine binds to the nicotinic acetylcholine receptors (nAChRs) and activates the mesolimbic dopaminergic system (MDS) to generate the pleasant and rewarding effects, the molecular mechanisms of nicotine addiction are not fully understood. Brain-derived neurotrophic factor (BDNF) is the most prevalent growth factor in the brain, which regulates neuron survival, differentiation, and synaptic plasticity, mainly through binding to the high affinity receptor tyrosine kinase receptor B (TrkB). BDNF gene polymorphisms are associated with nicotine dependence and blood BDNF levels are altered in smokers. In this review, we discussed the effects of nicotine on BDNF expression in the brain and summarized the underlying signaling pathways, which further indicated BDNF as a key regulator in nicotine dependence. Further studies that aim to understand the neurobiological mechanism of BDNF in nicotine addcition would provide a valuable reference for quitting smoking and developing the treatment of other addictive substances.


Corresponding authors: Meixiang Li, Department of Histology and Embryology, Institute of Clinical Anatomy & Reproductive Medicine, Hunan Province Cooperative Innovation Center for Molecular Target New Drug Study, Hengyang Medical College, University of South China, 28 W. Changsheng Road, Hengyang421001, Hunan, China, E-mail: ; and Sijie Tan, Department of Histology and Embryology, Institute of Clinical Anatomy & Reproductive Medicine, Hunan Province Cooperative Innovation Center for Molecular Target New Drug Study, Hengyang Medical College, University of South China, 28 W. Changsheng Road, Hengyang 421001, Hunan, China, E-mail:
Zeyi Huang and Daichao Wu contributed equally to this work.

Funding source: National Science Foundation of China

Award Identifier / Grant number: 81301144

Funding source: Hunan Provincial Natural Science Foundation

Award Identifier / Grant number: 2019JJ40250

Funding source: Natural Science Foundation of Hunan Province

Funding source: National Natural Science Foundation of China

Funding source: University of South China

  1. Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was supported by grants from the Hunan Provincial Natural Science Foundation (2019JJ40250), National Science Foundation of China (NSFC 81301144), Research Learning and Innovative Experiment Project for University Students of University of South China (2018XJX377) and Outstanding Youth Project of Hunan Education Department (18B262 and 19B475).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Altar, C. A., Cai, N., Bliven, T., Juhasz, M., Conner, J. M., Acheson, A. L., Lindsay, R. M., and Wiegand, S. J. (1997). Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389: 856–860, https://doi.org/10.1038/39885.Suche in Google Scholar PubMed

Andresen, J. H., Loberg, E. M., Wright, M., Goverud, I. L., Stray-Pedersen, B., and Saugstad, O. D. (2009). Nicotine affects the expression of brain-derived neurotrophic factor mRNA and protein in the hippocampus of hypoxic newborn piglets. J. Perinat. Med. 37: 553–560, https://doi.org/10.1515/jpm.2009.081.Suche in Google Scholar PubMed

Autry, A. E. and Monteggia, L. M. (2012). Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol. Rev. 64: 238–258, https://doi.org/10.1124/pr.111.005108.Suche in Google Scholar PubMed PubMed Central

Balfour, D. J. (2009). The neuronal pathways mediating the behavioral and addictive properties of nicotine. Handb. Exp. Pharmacol. 192: 209–233, https://doi.org/10.1007/978-3-540-69248-5_8.Suche in Google Scholar PubMed

Barde, Y. A., Edgar, D., and Thoenen, H. (1982). Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1: 549–553, https://doi.org/10.1002/j.1460-2075.1982.tb01207.x.Suche in Google Scholar PubMed PubMed Central

Bath, K. G. and Lee, F. S. (2006). Variant BDNF (Val66Met) impact on brain structure and function. Cognit. Affect Behav. Neurosci. 6: 79–85, https://doi.org/10.3758/cabn.6.1.79.Suche in Google Scholar PubMed

Benowitz, N. L., Porchet, H., Sheiner, L., and Jacob, P. R. (1988). Nicotine absorption and cardiovascular effects with smokeless tobacco use: comparison with cigarettes and nicotine gum. Clin. Pharmacol. Therapeut. 44: 23–28, https://doi.org/10.1038/clpt.1988.107.Suche in Google Scholar PubMed

Besusso, D., Geibel, M., Kramer, D., Schneider, T., Pendolino, V., Picconi, B., Calabresi, P., Bannerman, D. M., and Minichiello, L. (2013). BDNF-TrkB signaling in striatopallidal neurons controls inhibition of locomotor behavior. Nat. Commun. 4: 2031, https://doi.org/10.1038/ncomms3031.Suche in Google Scholar PubMed PubMed Central

Beuten, J., Ma, J. Z., Payne, T. J., Dupont, R. T., Quezada, P., Huang, W., Crews, K. M., and Li, M. D. (2005). Significant association of BDNF haplotypes in European-American male smokers but not in European-American female or African-American smokers. Am J Med Genet B Neuropsychiatr Genet 139B: 73–80, https://doi.org/10.1002/ajmg.b.30231.Suche in Google Scholar PubMed

Bhang, S. Y., Choi, S. W., and Ahn, J. H. (2010). Changes in plasma brain-derived neurotrophic factor levels in smokers after smoking cessation. Neurosci. Lett. 468: 7–11, https://doi.org/10.1016/j.neulet.2009.10.046.Suche in Google Scholar PubMed

Bhang, S., Ahn, J. H., and Choi, S. W. (2011). Brain-derived neurotrophic factor and serotonin transporter gene-linked promoter region genes alter serum levels of brain-derived neurotrophic factor in humans. J. Affect. Disord. 128: 299–304, https://doi.org/10.1016/j.jad.2010.07.008.Suche in Google Scholar PubMed

Breetvelt, E. J., Numans, M. E., Aukes, M. F., Hoeben, W., Strengman, E., Luykx, J. J., Bakker, S. C., Kahn, R. S., Ophoff, R. A., and Boks, M. P. (2012). The association of the alpha-5 subunit of the nicotinic acetylcholine receptor gene and the brain-derived neurotrophic factor gene with different aspects of smoking behavior. Psychiatr. Genet. 22: 96–98, https://doi.org/10.1097/ypg.0b013e32834c0c75.Suche in Google Scholar

Breslau, N., Johnson, E. O., Hiripi, E., and Kessler, R. (2001). Nicotine dependence in the United States: prevalence, trends, and smoking persistence. Arch. Gen. Psychiatr. 58: 810–816, https://doi.org/10.1001/archpsyc.58.9.810.Suche in Google Scholar PubMed

Brody, A. L., Mandelkern, M. A., Olmstead, R. E., Scheibal, D., Hahn, E., Shiraga, S., Zamora-Paja, E., Farahi, J., Saxena, S., London, E. D., et al. (2006). Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. Arch. Gen. Psychiatr. 63: 808–816, https://doi.org/10.1001/archpsyc.63.7.808.Suche in Google Scholar PubMed PubMed Central

Brunzell, D. H., Mineur, Y. S., Neve, R. L., and Picciotto, M. R. (2009). Nucleus accumbens CREB activity is necessary for nicotine conditioned place preference. Neuropsychopharmacology 34: 1993–2001, https://doi.org/10.1038/npp.2009.11.Suche in Google Scholar PubMed PubMed Central

Brunzell, D. H. and Mcintosh, J. M. (2012). Alpha7 nicotinic acetylcholine receptors modulate motivation to self-administer nicotine: implications for smoking and schizophrenia. Neuropsychopharmacology 37: 1134–1143, https://doi.org/10.1038/npp.2011.299.Suche in Google Scholar PubMed PubMed Central

Buck, J. M., O’Neill, H. C., and Stitzel, J. A. (2019). Developmental nicotine exposure elicits multigenerational disequilibria in proBDNF proteolysis and glucocorticoid signaling in the frontal cortices, striata, and hippocampi of adolescent mice. Biochem. Pharmacol. 168: 438–451, https://doi.org/10.1016/j.bcp.2019.08.003.Suche in Google Scholar PubMed PubMed Central

Buisson, B. and Bertrand, D. (2001). Chronic exposure to nicotine upregulates the human (alpha)4 (beta)2 nicotinic acetylcholine receptor function. J. Neurosci. 21: 1819–1829, https://doi.org/10.1523/jneurosci.21-06-01819.2001.Suche in Google Scholar

Bus, B. A., Molendijk, M. L., Penninx, B. J., Buitelaar, J. K., Kenis, G., Prickaerts, J., Elzinga, B. M., and Voshaar, R. C. (2011). Determinants of serum brain-derived neurotrophic factor. Psychoneuroendocrinology 36: 228–239, https://doi.org/10.1016/j.psyneuen.2010.07.013.Suche in Google Scholar PubMed

Bus, B. A., Tendolkar, I., Franke, B., de Graaf, J., den Heijer, M., Buitelaar, J. K., and Oude, V. R. (2012). Serum brain-derived neurotrophic factor: determinants and relationship with depressive symptoms in a community population of middle-aged, and elderly people. World J. Biol. Psychiatr. 13: 39–47, https://doi.org/10.3109/15622975.2010.545187.Suche in Google Scholar PubMed PubMed Central

Castino, M. R., Baker-Andresen, D., Ratnu, V. S., Shevchenko, G., Morris, K. V., Bredy, T. W., Youngson, N. A., and Clemens, K. J. (2018). Persistent histone modifications at the BDNF and Cdk-5 promoters following extinction of nicotine-seeking in rats. Gene Brain Behav. 17: 98–106, https://doi.org/10.1111/gbb.12421.Suche in Google Scholar PubMed PubMed Central

Centers for Disease Control and Prevention (US). (2010). How Tobacco smoke causes disease: The biology and behavioral basis for Smoking-attributable disease: A report of the surgeon general: Centers for disease control and prevention (US).National center for chronic disease prevention and health promotion (US), office on smoking and health (US).Suche in Google Scholar

Chan, K. L., Tong, K. Y., and Yip, S. P. (2008). Relationship of serum brain-derived neurotrophic factor (BDNF) and health-related lifestyle in healthy human subjects. Neurosci. Lett. 447: 124–128, https://doi.org/10.1016/j.neulet.2008.10.013.Suche in Google Scholar PubMed

Chao, M. V. (2003). Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4: 299–309, https://doi.org/10.1038/nrn1078.Suche in Google Scholar PubMed

Chase, K. A. and Sharma, R. P. (2013). Nicotine induces chromatin remodelling through decreases in the methyltransferases GLP, G9a, Setdb1 and levels of H3K9me2. Int. J. Neuropsychopharmacol. 16: 1129–1138, https://doi.org/10.1017/s1461145712001101.Suche in Google Scholar PubMed

Chellian, R., Pandy, V., and Mohamed, Z. (2018). Alpha-asarone attenuates depression-like behavior in nicotine-withdrawn mice: evidence for the modulation of hippocampal pCREB levels during nicotine-withdrawal. Eur. J. Pharmacol. 818: 10–16, https://doi.org/10.1016/j.ejphar.2017.10.025.Suche in Google Scholar PubMed

Chen, D. C., Wang, J., Wang, B., Yang, S. C., Zhang, C. X., Zheng, Y. L., Li, Y. L., Wang, N., Yang, K. B., Xiu, M. H., et al. (2009). Decreased levels of serum brain-derived neurotrophic factor in drug-naive first-episode schizophrenia: relationship to clinical phenotypes. Psychopharmacology (Berlin) 207: 375–380. https://doi.org/10.1007/s00213-009-1665-6.Suche in Google Scholar PubMed

Chen, Y. H., Lin, B. J., Hsieh, T. H., Kuo, T. T., Miller, J., Chou, Y. C., Huang, E. Y., and Hoffer, B. J. (2019). Differences in nicotine encoding dopamine release between the striatum and shell portion of the nucleus accumbens. Cell Transplant. 28: 248–261, https://doi.org/10.1177/0963689718775382.Suche in Google Scholar PubMed PubMed Central

Consortium, T. A. G. (2010). Genome-wide meta-analyses identify multiple loci associated with smoking behavior. Nat. Genet. 42: 441–447, https://doi.org/10.1038/ng.571.Suche in Google Scholar PubMed PubMed Central

Dani, J. A. and Harris, R. A. (2005). Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat. Neurosci. 8: 1465–1470, https://doi.org/10.1038/nn1580.Suche in Google Scholar PubMed

Davis, M. I. (2008). Ethanol-BDNF interactions: still more questions than answers. Pharmacol. Ther. 118: 36–57, https://doi.org/10.1016/j.pharmthera.2008.01.003.Suche in Google Scholar PubMed PubMed Central

De Biasi, M. and Dani, J. A. (2011). Reward, addiction, withdrawal to nicotine. Annu. Rev. Neurosci. 34: 105–130, https://doi.org/10.1146/annurev-neuro-061010-113734.Suche in Google Scholar

Di Chiara, G. (2000). Role of dopamine in the behavioural actions of nicotine related to addiction. Eur. J. Pharmacol. 393: 295–314, https://doi.org/10.1016/s0014-2999(00)00122-9.Suche in Google Scholar

Faure, P., Tolu, S., Valverde, S., and Naude, J. (2014). Role of nicotinic acetylcholine receptors in regulating dopamine neuron activity. Neuroscience 282: 86–100, https://doi.org/10.1016/j.neuroscience.2014.05.040.Suche in Google Scholar

Fernandes, B. S., Gama, C. S., Cereser, K. M., Yatham, L. N., Fries, G. R., Colpo, G., de Lucena, D., Kunz, M., Gomes, F. A., and Kapczinski, F. (2011). Brain-derived neurotrophic factor as a state-marker of mood episodes in bipolar disorders: a systematic review and meta-regression analysis. J. Psychiatr. Res. 45: 995–1004, https://doi.org/10.1016/j.jpsychires.2011.03.002.Suche in Google Scholar

Fisher, J. L., Pidoplichko, V. I., and Dani, J. A. (1998). Nicotine modifies the activity of ventral tegmental area dopaminergic neurons and hippocampal GABAergic neurons. J. Physiol. Paris 92: 209–213, https://doi.org/10.1016/s0928-4257(98)80012-0.Suche in Google Scholar

Fisher, M. L., Lemalefant, R. M., Zhou, L., Huang, G., and Turner, J. R. (2017). Distinct roles of CREB within the ventral and dorsal hippocampus in mediating nicotine withdrawal phenotypes. Neuropsychopharmacology 42: 1599–1609, https://doi.org/10.1038/npp.2016.257.Suche in Google Scholar PubMed PubMed Central

Ghasemzadeh, Z., Sardari, M., Javadi, P., and Rezayof, A. (2020). Expression analysis of hippocampal and amygdala CREB-BDNF signaling pathway in nicotine-induced reward under stress in rats. Brain Res. 1741: 146885, https://doi.org/10.1016/j.brainres.2020.146885.Suche in Google Scholar PubMed

Guillin, O., Diaz, J., Carroll, P., Griffon, N., Schwartz, J. C., and Sokoloff, P. (2001). BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature 411: 86–89, https://doi.org/10.1038/35075076.Suche in Google Scholar PubMed

Horger, B. A., Iyasere, C. A., Berhow, M. T., Messer, C. J., Nestler, E. J., and Taylor, J. R. (1999). Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor. J. Neurosci. 19: 4110–4122, https://doi.org/10.1523/jneurosci.19-10-04110.1999.Suche in Google Scholar

Huang, E. J. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24: 677–736, https://doi.org/10.1146/annurev.neuro.24.1.677.Suche in Google Scholar PubMed PubMed Central

Hughes, J. R., Stead, L. F., and Lancaster, T. (2007). Antidepressants for smoking cessation. Cochrane Database Syst. Rev. 1: CD000031.10.1002/14651858.CD000031.pub3Suche in Google Scholar

Hyman, C., Hofer, M., Barde, Y. A., Juhasz, M., Yancopoulos, G. D., Squinto, S. P., and Lindsay, R. M. (1991). BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350: 230–232, https://doi.org/10.1038/350230a0.Suche in Google Scholar

Inoue, Y., Yao, L., Hopf, F. W., Fan, P., Jiang, Z., Bonci, A., and Diamond, I. (2007). Nicotine and ethanol activate protein kinase a synergistically via G(i) betagamma subunits in nucleus accumbens/ventral tegmental cocultures: the role of dopamine D(1)/D(2) and adenosine A(2A) receptors. J. Pharmacol. Exp. Therapeut. 322: 23–29, https://doi.org/10.1124/jpet.107.120675.Suche in Google Scholar

Jamal, M., Van der Does, W., Elzinga, B. M., Molendijk, M. L., and Penninx, B. W. (2015). Association between smoking, nicotine dependence, and BDNF Val66Met polymorphism with BDNF concentrations in serum. Nicotine Tob. Res. 17: 323–329, https://doi.org/10.1093/ntr/ntu151.Suche in Google Scholar

Janhunen, S., and Ahtee, L. (2007). Differential nicotinic regulation of the nigrostriatal and mesolimbic dopaminergic pathways: implications for drug development. Neurosci. Biobehav. Rev. 31: 287–314, https://doi.org/10.1016/j.neubiorev.2006.09.008.Suche in Google Scholar

Jindal, R. D., Pillai, A. K., Mahadik, S. P., Eklund, K., Montrose, D. M., and Keshavan, M. S. (2010). Decreased BDNF in patients with antipsychotic naive first episode schizophrenia. Schizophr. Res. 119: 47–51, https://doi.org/10.1016/j.schres.2009.12.035.Suche in Google Scholar

Johansson, J., Formaggio, E., Fumagalli, G., and Chiamulera, C. (2009). Choline up-regulates BDNF and down-regulates TrkB neurotrophin receptor in rat cortical cell culture. Neuroreport 20: 828–832, https://doi.org/10.1097/wnr.0b013e32832b7324.Suche in Google Scholar

Jones, I. W. and Wonnacott, S. (2004). Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J. Neurosci. 24: 11244–11252, https://doi.org/10.1523/jneurosci.3009-04.2004.Suche in Google Scholar

Jung, Y., Hsieh, L. S., Lee, A. M., Zhou, Z., Coman, D., Heath, C. J., Hyder, F., Mineur, Y. S., Yuan, Q., Goldman, D., et al. (2016). An epigenetic mechanism mediates developmental nicotine effects on neuronal structure and behavior. Nat. Neurosci. 19: 905–914, https://doi.org/10.1038/nn.4315.Suche in Google Scholar

Kamata, A., Takeuchi, Y., and Fukunaga, K. (2006). Identification of the isoforms of Ca2+/calmodulin-dependent protein kinase II and expression of brain-derived neurotrophic factor mRNAs in the substantia nigra. J. Neurochem. 96: 195–203, https://doi.org/10.1111/j.1471-4159.2005.03531.x.Suche in Google Scholar

Karege, F., Schwald, M., and Cisse, M. (2002). Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci. Lett. 328: 261–264, https://doi.org/10.1016/s0304-3940(02)00529-3.Suche in Google Scholar

Kenny, P. J., File, S. E., and Rattray, M. (2000). Acute nicotine decreases, and chronic nicotine increases the expression of brain-derived neurotrophic factor mRNA in rat hippocampus. Brain Res Mol Brain Res 85: 234–238, https://doi.org/10.1016/s0169-328x(00)00246-1.Suche in Google Scholar

Kenny, P. J. and Markou, A. (2001). Neurobiology of the nicotine withdrawal syndrome. Pharmacol. Biochem. Behav. 70: 531–549, https://doi.org/10.1016/s0091-3057(01)00651-7.Suche in Google Scholar

Kessler, D. A., Natanblut, S. L., Wilkenfeld, J. P., Lorraine, C. C., Mayl, S. L., Bernstein, I. B., and Thompson, L. (1997). Nicotine addiction: a pediatric disease. J. Pediatr. 130: 518–524, https://doi.org/10.1016/s0022-3476(97)70232-4.Suche in Google Scholar

Kim, T. S., Kim, D. J., Lee, H., and Kim, Y. K. (2007). Increased plasma brain-derived neurotrophic factor levels in chronic smokers following unaided smoking cessation. Neurosci. Lett. 423: 53–57, https://doi.org/10.1016/j.neulet.2007.05.064.Suche in Google Scholar PubMed

Kishioka, S., Kiguchi, N., Kobayashi, Y., and Saika, F. (2014). Nicotine effects and the endogenous opioid system. J. Pharmacol. Sci. 125: 117–124, https://doi.org/10.1254/jphs.14r03cp.Suche in Google Scholar PubMed

Kivinummi, T., Kaste, K., Rantamaki, T., Castren, E., and Ahtee, L. (2011). Alterations in BDNF and phospho-CREB levels following chronic oral nicotine treatment and its withdrawal in dopaminergic brain areas of mice. Neurosci. Lett. 491: 108–112, https://doi.org/10.1016/j.neulet.2011.01.015.Suche in Google Scholar PubMed

Klein, A. B., Williamson, R., Santini, M. A., Clemmensen, C., Ettrup, A., Rios, M., Knudsen, G. M., and Aznar, S. (2011). Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int. J. Neuropsychopharmacol. 14: 347–353, https://doi.org/10.1017/s1461145710000738.Suche in Google Scholar PubMed

Koob, G. F. and Le Moal, M. (2008). Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363: 3113–3123, https://doi.org/10.1098/rstb.2008.0094.Suche in Google Scholar PubMed PubMed Central

Korhonen, T., Loukola, A., Hallfors, J., Salomaa, V., and Kaprio, J. (2018). Is brain derived neurotrophic factor (Bdnf) associated with smoking initiation? Replication using a large Finnish population sample. Nicotine Tob. Res. 22: 293–296, https://doi.org/10.1093/ntr/nty218.Suche in Google Scholar PubMed

Kumar, V., Zhang, M. X., Swank, M. W., Kunz, J., and Wu, G. Y. (2005). Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci. 25: 11288–11299, https://doi.org/10.1523/jneurosci.2284-05.2005.Suche in Google Scholar PubMed PubMed Central

Lang, U. E., Sander, T., Lohoff, F. W., Hellweg, R., Bajbouj, M., Winterer, G., and Gallinat, J. (2007). Association of the met66 allele of brain-derived neurotrophic factor (BDNF) with smoking. Psychopharmacology (Berlin) 190: 433–439, https://doi.org/10.1007/s00213-006-0647-1.Suche in Google Scholar PubMed

Lanz, T. A., Bove, S. E., Pilsmaker, C. D., Mariga, A., Drummond, E. M., Cadelina, G. W., Adamowicz, W. O., Swetter, B. J., Carmel, S., Dumin, J. A., et al. (2012). Robust changes in expression of brain-derived neurotrophic factor (BDNF) mRNA and protein across the brain do not translate to detectable changes in BDNF levels in CSF or plasma. Biomarkers 17: 524–531, https://doi.org/10.3109/1354750x.2012.694476.Suche in Google Scholar

Le Foll, B., Diaz, J., and Sokoloff, P. (2003). Increased dopamine D3 receptor expression accompanying behavioral sensitization to nicotine in rats. Synapse 47: 176–183, https://doi.org/10.1002/syn.10170.Suche in Google Scholar PubMed

Le Foll, B. and Goldberg, S. R. (2009). Effects of nicotine in experimental animals and humans: an update on addictive properties. Handb. Exp. Pharmacol. 192: 335–367, https://doi.org/10.1007/978-3-540-69248-5_12.Suche in Google Scholar PubMed PubMed Central

Leao, R. M., Cruz, F. C., Carneiro-De-Oliveira, P. E., Rossetto, D. B., Valentini, S. R., Zanelli, C. F., and Planeta, C. S. (2013). Enhanced nicotine-seeking behavior following pre-exposure to repeated cocaine is accompanied by changes in BDNF in the nucleus accumbens of rats. Pharmacol. Biochem. Behav. 104: 169–176, https://doi.org/10.1016/j.pbb.2013.01.007.Suche in Google Scholar PubMed

Lee, B. G., Agustin, A., Hempstead, B. L., Lee, F. S., and Blendy, J. A. (2015). Effects of the BDNF Val66Met polymorphism on Anxiety-Like behavior following nicotine withdrawal in mice. Nicotine Tob. Res. 17: 1428–1435, https://doi.org/10.1093/ntr/ntv047.Suche in Google Scholar PubMed PubMed Central

Lee, J., Duan, W., and Mattson, M. P. (2002). Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J. Neurochem. 82: 1367–1375, https://doi.org/10.1046/j.1471-4159.2002.01085.x.Suche in Google Scholar PubMed

Li, M. D., Ma, J. Z., Cheng, R., Dupont, R. T., Williams, N. J., Crews, K. M., Payne, T. J., and Elston, R. C. (2003). A genome-wide scan to identify loci for smoking rate in the Framingham Heart Study population. BMC Genet. 4 (Suppl 1): S103, https://doi.org/10.1186/1471-2156-4-s1-s35.Suche in Google Scholar PubMed PubMed Central

Lopez-Hernandez, G.Y., Sanchez-Padilla, J., Ortiz-Acevedo, A., Lizardi-Ortiz, J., Salas-Vincenty, J., Rojas, L. V., and Lasalde-Dominicci, J. A. (2004). Nicotine-induced up-regulation, and desensitization of alpha4beta2 neuronal nicotinic receptors depend on subunit ratio. J. Biol. Chem. 279: 38007–38015, https://doi.org/10.1074/jbc.m403537200.Suche in Google Scholar PubMed

Luo, Y., Kuang, S., Li, H., Ran, D., and Yang, J. (2017). CAMP/PKA-CREB-BDNF signaling pathway in hippocampus mediates cyclooxygenase 2-induced learning/memory deficits of rats subjected to chronic unpredictable mild stress. Oncotarget 8: 35558–35572, https://doi.org/10.18632/oncotarget.16009.Suche in Google Scholar PubMed PubMed Central

Maggio, R., Riva, M., Vaglini, F., Fornai, F., Molteni, R., Armogida, M., Racagni, G., and Corsini, G. U. (1998). Nicotine prevents experimental parkinsonism in rodents and induces striatal increase of neurotrophic factors. J. Neurochem. 71: 2439–2446, https://doi.org/10.1046/j.1471-4159.1998.71062439.x.Suche in Google Scholar

Maggio, R., Riva, M., Vaglini, F., Fornai, F., Racagni, G., and Corsini, G. U. (1997). Striatal increase of neurotrophic factors as a mechanism of nicotine protection in experimental parkinsonism. J. Neural. Transm. 104: 1113–1123, https://doi.org/10.1007/bf01273324.Suche in Google Scholar

Maisonpierre, P. C., Le Beau, M. M., Espinosa, R. R., Ip, N. Y., Belluscio, L., de la Monte, S. M., Squinto, S., Furth, M. E., and Yancopoulos, G. D. (1991). Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations. Genomics 10: 558–568, https://doi.org/10.1016/0888-7543(91)90436-i.Suche in Google Scholar

Mansvelder, H. D., Keath, J. R., and Mcgehee, D. S. (2002). Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33: 905–919, https://doi.org/10.1016/s0896-6273(02)00625-6.Suche in Google Scholar

Mansvelder, H. D. and Mcgehee, D. S. (2000). Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27: 349–357, https://doi.org/10.1016/s0896-6273(00)00042-8.Suche in Google Scholar

Marco, E. M., Granstrem, O., Moreno, E., Llorente, R., Adriani, W., Laviola, G., and Viveros, M. P. (2007). Subchronic nicotine exposure in adolescence induces long-term effects on hippocampal and striatal cannabinoid-CB1, and mu-opioid receptors in rats. Eur. J. Pharmacol. 557: 37–43, https://doi.org/10.1016/j.ejphar.2006.11.013.Suche in Google Scholar PubMed

Markou, A. (2008). Review. Neurobiology of nicotine dependence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363: 3159–3168, https://doi.org/10.1098/rstb.2008.0095.Suche in Google Scholar PubMed PubMed Central

Marshall, D. L., Redfern, P. H., and Wonnacott, S. (1997). Presynaptic nicotinic modulation of dopamine release in the three ascending pathways studied by in vivo microdialysis: comparison of naive and chronic nicotine-treated rats. J. Neurochem. 68: 1511–1519, https://doi.org/10.1046/j.1471-4159.1997.68041511.x.Suche in Google Scholar PubMed

Mathieu-Kia, A. M., Kellogg, S. H., Butelman, E. R., and Kreek, M. J. (2002). Nicotine addiction: insights from recent animal studies. Psychopharmacology (Berlin) 162: 102–118, https://doi.org/10.1007/s00213-002-1096-0.Suche in Google Scholar PubMed

Montag, C., Basten, U., Stelzel, C., Fiebach, C. J., and Reuter, M. (2008). The BDNF Val66Met polymorphism and smoking. Neurosci. Lett. 442: 30–33, https://doi.org/10.1016/j.neulet.2008.06.064.Suche in Google Scholar PubMed

Montag, C., Markett, S., Basten, U., Stelzel, C., Fiebach, C., Canli, T., and Reuter, M. (2010a). Epistasis of the DRD2/ANKK1 Taq Ia and the BDNF Val66Met polymorphism impacts novelty seeking and harm avoidance. Neuropsychopharmacology 35: 1860–1867, https://doi.org/10.1038/npp.2010.55.Suche in Google Scholar

Montag, C., Weber, B., Jentgens, E., Elger, C., and Reuter, M. (2010b). An epistasis effect of functional variants on the BDNF and DRD2 genes modulates gray matter volume of the anterior cingulate cortex in healthy humans. Neuropsychologia 48: 1016–1021, https://doi.org/10.1016/j.neuropsychologia.2009.11.027.Suche in Google Scholar

Naoe, Y., Shinkai, T., Hori, H., Fukunaka, Y., Utsunomiya, K., Sakata, S., Matsumoto, C., Shimizu, K., Hwang, R., Ohmori, O., et al. (2007). No association between the brain-derived neurotrophic factor (BDNF) Val66Met polymorphism and schizophrenia in Asian populations: evidence from a case-control study and meta-analysis. Neurosci. Lett. 415: 108–112, https://doi.org/10.1016/j.neulet.2007.01.006.Suche in Google Scholar

Numakawa, T., Suzuki, S., Kumamaru, E., Adachi, N., Richards, M., and Kunugi, H. (2010). BDNF function and intracellular signaling in neurons. Histol. Histopathol. 25: 237–258.Suche in Google Scholar

Pan, W., Banks, W. A., Fasold, M. B., Bluth, J., and Kastin, A. J. (1998). Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 37: 1553–1561, https://doi.org/10.1016/s0028-3908(98)00141-5.Suche in Google Scholar

Panja, D., Kenney, J. W., D’Andrea, L., Zalfa, F., Vedeler, A., Wibrand, K., Fukunaga, R., Bagni, C., Proud, C. G., and Bramham, C. R. (2014). Two-stage translational control of dentate gyrus LTP consolidation is mediated by sustained BDNF-TrkB signaling to MNK. Cell Rep. 9: 1430–1445, https://doi.org/10.1016/j.celrep.2014.10.016.Suche in Google Scholar PubMed

Panja, D. and Bramham, C. R. (2014). BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacology 76 Pt:664–676, https://doi.org/10.1016/j.neuropharm.2013.06.024.Suche in Google Scholar PubMed

Pei, Y., Jiao, Z., Dong, W., Pei, L., He, X., Wang, H., and Xu, D. (2019). Excitotoxicity and compensatory upregulation of GAD67 in fetal rat hippocampus caused by prenatal nicotine exposure are associated with inhibition of the BDNF pathway. Food Chem. Toxicol. 123: 314–325, https://doi.org/10.1016/j.fct.2018.10.062.Suche in Google Scholar PubMed

Picciotto, M. R., Zoli, M., Rimondini, R., Lena, C., Marubio, L. M., Pich, E. M., Fuxe, K., and Changeux, J. P. (1998). Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391: 173–177, https://doi.org/10.1038/34413.Suche in Google Scholar PubMed

Pirildar, S., Gonul, A. S., Taneli, F., and Akdeniz, F. (2004). Low serum levels of brain-derived neurotrophic factor in patients with schizophrenia do not elevate after antipsychotic treatment. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 28: 709–713.10.1016/j.pnpbp.2004.05.008Suche in Google Scholar PubMed

Pitts, E. G., Taylor, J. R., and Gourley, S. L. (2016). Prefrontal cortical BDNF: a regulatory key in cocaine- and food-reinforced behaviors. Neurobiol. Dis. 91: 326–335, https://doi.org/10.1016/j.nbd.2016.02.021.Suche in Google Scholar PubMed PubMed Central

Qian, J., Mummalaneni, S. K., Alkahtani, R. M., Mahavadi, S., Murthy, K. S., Grider, J. R., and Lyall, V. (2016). Nicotine-Induced effects on nicotinic acetylcholine receptors (nAChRs), Ca2+, and brain-derived neurotrophic factor (BDNF) in STC-1 cells. PloS One 11: e166565, https://doi.org/10.1371/journal.pone.0166565.Suche in Google Scholar

Rasmussen, P., Brassard, P., Adser, H., Pedersen, M. V., Leick, L., Hart, E., Secher, N. H., Pedersen, B. K., and Pilegaard, H. (2009). Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol. 94: 1062–1069, https://doi.org/10.1113/expphysiol.2009.048512.Suche in Google Scholar

Rosa, A., Cuesta, M. J., Fatjo-Vilas, M., Peralta, V., Zarzuela, A., and Fananas, L. (2006). The Val66Met polymorphism of the brain-derived neurotrophic factor gene is associated with risk for psychosis: evidence from a family-based association study. Am J Med Genet B Neuropsychiatr Genet 141B: 135–138, https://doi.org/10.1002/ajmg.b.30266.Suche in Google Scholar

Sasi, M., Vignoli, B., Canossa, M., and Blum, R. (2017). Neurobiology of local and intercellular BDNF signaling. Pflügers Archiv 469: 593–610, https://doi.org/10.1007/s00424-017-1964-4.Suche in Google Scholar

Satta, R., Maloku, E., Zhubi, A., Pibiri, F., Hajos, M., Costa, E., and Guidotti, A. (2008). Nicotine decreases DNA methyltransferase 1 expression and glutamic acid decarboxylase 67 promoter methylation in GABAergic interneurons. Proc. Natl. Acad. Sci. U. S. A. 105: 16356–16361, https://doi.org/10.1073/pnas.0808699105.Suche in Google Scholar

Schreckenberger, M., Amberg, R., Scheurich, A., Lochmann, M., Tichy, W., Klega, A., Siessmeier, T., Grunder, G., Buchholz, H. G., Landvogt, C., et al. (2004). Acute alcohol effects on neuronal and attentional processing: striatal reward system and inhibitory sensory interactions under acute ethanol challenge. Neuropsychopharmacology 29: 1527–1537, https://doi.org/10.1038/sj.npp.1300453.Suche in Google Scholar

Seroogy, K. B., Lundgren, K. H., Tran, T. M., Guthrie, K. M., Isackson, P. J., and Gall, C. M. (1994). Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs. J. Comp. Neurol. 342: 321–334, https://doi.org/10.1002/cne.903420302.Suche in Google Scholar

Serres, F. and Carney, S. L. (2006). Nicotine regulates SH-SY5Y neuroblastoma cell proliferation through the release of brain-derived neurotrophic factor. Brain Res. 1101: 36–42, https://doi.org/10.1016/j.brainres.2006.05.023.Suche in Google Scholar

Soderpalm, B., Ericson, M., Olausson, P., Blomqvist, O., and Engel, J. A. (2000). Nicotinic mechanisms involved in the dopamine activating and reinforcing properties of ethanol. Behav. Brain Res. 113: 85–96, https://doi.org/10.1016/s0166-4328(00)00203-5.Suche in Google Scholar

Son, J. H. and Winzer-Serhan, U. H.(2009). Chronic neonatal nicotine exposure increases mRNA expression of neurotrophic factors in the postnatal rat hippocampus. Brain Res. 1278: 1–14, https://doi.org/10.1016/j.brainres.2009.04.046.Suche in Google Scholar PubMed

Suriyaprom, K., Tungtrongchitr, R., Thawnashom, K., and Pimainog, Y. (2013). BDNF Val66Met polymorphism and serum concentrations of BDNF with smoking in Thai males. Genet. Mol. Res. 12: 4925–4933, https://doi.org/10.4238/2013.october.24.3.Suche in Google Scholar

Takeuchi, Y., Fukunaga, K., and Miyamoto, E. (2002). Activation of nuclear Ca2+/calmodulin-dependent protein kinase II and brain-derived neurotrophic factor gene expression by stimulation of dopamine D2 receptor in transfected NG108-15 cells. J. Neurochem. 82: 316–328, https://doi.org/10.1046/j.1471-4159.2002.00967.x.Suche in Google Scholar

Tan, S., Xue, S., Behnood-Rod, A., Chellian, R., Wilson, R., Knight, P., Panunzio, S., Lyons, H., Febo, M., and Bruijnzeel, A. W. (2019). Sex differences in the reward deficit and somatic signs associated with precipitated nicotine withdrawal in rats. Neuropharmacology 160: 107756, https://doi.org/10.1016/j.neuropharm.2019.107756.Suche in Google Scholar

Tan, Y. L., Zhou, D. F., Cao, L. Y., Zou, Y. Z., and Zhang, X. Y. (2005). Decreased BDNF in serum of patients with chronic schizophrenia on long-term treatment with antipsychotics. Neurosci. Lett. 382: 27–32, https://doi.org/10.1016/j.neulet.2005.02.054.Suche in Google Scholar

Tang, S., Machaalani, R., and Waters, K. A. (2008). Brain-derived neurotrophic factor (BDNF) and TrkB in the piglet brainstem after post-natal nicotine and intermittent hypercapnic hypoxia. Brain Res. 1232: 195–205, https://doi.org/10.1016/j.brainres.2008.07.039.Suche in Google Scholar

Tapper, A. R., Mckinney, S. L., Nashmi, R., Schwarz, J., Deshpande, P., Labarca, C., Whiteaker, P., Marks, M. J., Collins, A. C., and Lester, H. A. (2004). Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization. Science 306: 1029–1032, https://doi.org/10.1126/science.1099420.Suche in Google Scholar

Telles-Longui, M., Mourelle, D., Schowe, N. M., Cipolli, G. C., Malerba, H. N., Buck, H. S., and Viel, T. A. (2019). Alpha7 nicotinic ACh receptors are necessary for memory recovery and neuroprotection promoted by attention training in amyloid-beta-infused mice. Br. J. Pharmacol. 176: 3193–3205, https://doi.org/10.1111/bph.14744.Suche in Google Scholar

Thoenen, H. (1995). Neurotrophins and neuronal plasticity. Science 270: 593–598, https://doi.org/10.1126/science.270.5236.593.Suche in Google Scholar

Torregrossa, M. M., Corlett, P. R., and Taylor, J. R. (2011). Aberrant learning and memory in addiction. Neurobiol. Learn. Mem. 96: 609–623, https://doi.org/10.1016/j.nlm.2011.02.014.Suche in Google Scholar

Toyooka, K., Asama, K., Watanabe, Y., Muratake, T., Takahashi, M., Someya, T., and Nawa, H. (2002). Decreased levels of brain-derived neurotrophic factor in serum of chronic schizophrenic patients. Psychiatr. Res. 110: 249–257, https://doi.org/10.1016/s0165-1781(02)00127-0.Suche in Google Scholar

Turner, J. R., Gold, A., Schnoll, R., and Blendy, J. A. (2013). Translational research in nicotine dependence. Cold Spring Harb Perspect Med 3: a12153, https://doi.org/10.1101/cshperspect.a012153.Suche in Google Scholar PubMed PubMed Central

Turner, J. R., Ray, R., Lee, B., Everett, L., Xiang, J., Jepson, C., Kaestner, K. H., Lerman, C., and Blendy, J. A. (2014). Evidence from mouse and man for a role of neuregulin 3 in nicotine dependence. Mol. Psychiatr. 19: 801–810, https://doi.org/10.1038/mp.2013.104.Suche in Google Scholar PubMed PubMed Central

Uhl, G. R., Liu, Q. R., Walther, D., Hess, J., and Naiman, D. (2001). Polysubstance abuse-vulnerability genes: genome scans for association, using 1,004 subjects and 1,494 single-nucleotide polymorphisms. Am. J. Hum. Genet. 69: 1290–1300, https://doi.org/10.1086/324467.Suche in Google Scholar PubMed PubMed Central

Varnas, K., Lawyer, G., Jonsson, E. G., Kulle, B., Nesvag, R., Hall, H., Terenius, L., and Agartz, I. (2008). Brain-derived neurotrophic factor polymorphisms and frontal cortex morphology in schizophrenia. Psychiatr. Genet. 18: 177–183, https://doi.org/10.1097/ypg.0b013e3283050a94.Suche in Google Scholar PubMed

Walters, C. L., Cleck, J. N., Kuo, Y. C., and Blendy, J. A. (2005). Mu-opioid receptor and CREB activation are required for nicotine reward. Neuron 46: 933–943, https://doi.org/10.1016/j.neuron.2005.05.005.Suche in Google Scholar PubMed

Wang, X. Y. (2015). The exposure to nicotine affects expression of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in neonate rats. Neurol. Sci. 36: 289–295.10.1007/s10072-014-1934-ySuche in Google Scholar PubMed

Wang, Z. R., Zhou, D. F., Cao, L. Y., Tan, Y. L., Zhang, X. Y., Li, J., Lu, L., Wu, G. Y., Kosten, T. A., and Kosten, T. R. (2007). Brain-derived neurotrophic factor polymorphisms and smoking in schizophrenia. Schizophr. Res. 97: 299–301, https://doi.org/10.1016/j.schres.2007.08.012.Suche in Google Scholar PubMed

Wei, P., Liu, Q., Li, D., Zhang, 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. 161–166. https://doi.org/10.1016/j.neulet.2015.08.008.Suche in Google Scholar PubMed

WHO (2019). WHO global report on trends in prevalence of tobacco use 2000-2025. Geneva.Suche in Google Scholar

Wilar, G., Shinoda, Y., Sasaoka, T., and Fukunaga, K. (2019). Crucial role of dopamine D2 receptor signaling in nicotine-induced conditioned place preference. Mol. Neurobiol. 56: 7911–928, https://doi.org/10.1007/s12035-019-1635-x.Suche in Google Scholar PubMed

Winther, K. and Fornitz, G. G. (1999). The effect of cigarette smoking and nicotine chewing gum on platelet function and fibrinolytic activity. J. Cardiovasc. Risk 6: 303–306, https://doi.org/10.1177/204748739900600505.Suche in Google Scholar PubMed

Wong, Y. H., Lee, C. M., Xie, W., Cui, B., and Poo, M. M. (2015). Activity-dependent BDNF release via endocytic pathways is regulated by synaptotagmin-6, and complexin. Proc. Natl. Acad. Sci. U. S. A. 112: E4475–E4484, https://doi.org/10.1073/pnas.1511830112.Suche in Google Scholar PubMed PubMed Central

Wook, K. J., Labonte, B., Engmann, O., Calipari, E. S., Juarez, B., Lorsch, Z., Walsh, J. J., Friedman, A. K., Yorgason, J. T., Han, M. H., et al. (2016). Essential role of mesolimbic brain-derived neurotrophic factor in chronic social stress-induced depressive behaviors. Biol. Psychiatr. 80: 469–478, https://doi.org/10.1016/j.biopsych.2015.12.009.Suche in Google Scholar PubMed PubMed Central

Xia, H., Du, X., Yin, G., Zhang, Y., Li, X., Cai, J., Huang, X., Ning, Y., Soares, J. C., Wu, F., et al. (2019). Efects of smoking on cognition and BDNF levels in a male Chinese population-relationship with BDNF Val66Met polymorphism. Sci. Rep. 1: 417, https://doi.org/10.1038/s41598-018-36419-8.Suche in Google Scholar PubMed PubMed Central

Xu, M. Q., St, C. D., Ott, J., Feng, G. Y., and He, L. (2007). Brain-derived neurotrophic factor gene C-270T and Val66Met functional polymorphisms and risk of schizophrenia: a moderate-scale population-based study and meta-analysis. Schizophr. Res. 91: 6–13, https://doi.org/10.1016/j.schres.2006.12.008.Suche in Google Scholar PubMed

Yeom, M., Shim, I., Lee, H. J., and Hahm, D. H. (2005). Proteomic analysis of nicotine-associated protein expression in the striatum of repeated nicotine-treated rats. Biochem. Biophys. Res. Commun. 326: 321–328, https://doi.org/10.1016/j.bbrc.2004.11.034.Suche in Google Scholar PubMed

Yi, Z., Zhang, C., Wu, Z., Hong, W., Li, Z., Fang, Y., and Yu, S. (2011). Lack of effect of brain derived neurotrophic factor (BDNF) Val66Met polymorphism on early onset schizophrenia in Chinese Han population. Brain Res. 1417: 146–150, https://doi.org/10.1016/j.brainres.2011.08.037.Suche in Google Scholar PubMed

Zhang, X. Y., Chen, D. C., Tan, Y. L., Luo, X., Zuo, L., Lv, M. H., Shah, N. N., Zunta-Soares, G. B., and Soares, J. C. (2015). Smoking and BDNF Val66Met polymorphism in male schizophrenia: a case-control study. J. Psychiatr. Res. 60: 49–55, https://doi.org/10.1016/j.jpsychires.2014.09.023.Suche in Google Scholar PubMed

Zhang, X. Y., Chen, D. C., Xiu, M. H., Luo, X., Zuo, L., Haile, C. N., Kosten, T. A., and Kosten, T. R. (2012). BDNF Val66Met variant and smoking in a Chinese population. PloS One 7: e53295, https://doi.org/10.1371/journal.pone.0053295.Suche in Google Scholar PubMed PubMed Central

Zhang, X. Y., Xiu, M. H., Chen, D. C., Yang, F. D., Wu, G. Y., Lu, L., Kosten, T. A., and Kosten, T. R. (2010). Nicotine dependence and serum BDNF levels in male patients with schizophrenia. Psychopharmacology (Berlin) 212: 301–307, https://doi.org/10.1007/s00213-010-1956-y.Suche in Google Scholar PubMed

Zhou, D. H., Yan, Q. Z., Yan, X. M., Li, C. B., Fang, H., Zheng, Y. L., Zhang, C. X., Yao, H. J., Chen, D. C., Xiu, M. H., et al. (2010). The study of BDNF Val66Met polymorphism in Chinese schizophrenic patients. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 34: 930–933, https://doi.org/10.1016/j.pnpbp.2010.04.019.Suche in Google Scholar PubMed

Received: 2020-05-26
Accepted: 2020-07-18
Published Online: 2020-09-04
Published in Print: 2021-01-27

© 2020 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 18.11.2025 von https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2020-0044/pdf
Button zum nach oben scrollen