Effects of smoking on cognition and BDNF levels in a male Chinese population: relationship with BDNF Val66Met polymorphism

Recent studies demonstrate that brain-derived neurotrophic factor (BDNF) might be associated with nicotine addiction, and circulating BDNF is a biomarker of memory and general cognitive function. Moreover, studies suggest that a functional polymorphism of the BDNF Val66Met may mediate hippocampal-dependent cognitive functions. We aimed to explore the relationships between smoking, cognitive performance and BDNF in a normal Chinese Han population. We recruited 628 male healthy subjects, inducing 322 smokers and 306 nonsmokers, and genotyped them the BDNF Val66Met polymorphism. Of these, we assessed 114 smokers and 98 nonsmokers on the repeatable battery for the assessment of neuropsychological status (RBANS), and 103 smokers and 89 nonsmokers on serum BDNF levels. Smokers scored lower than the nonsmokers on RBANS total score (p = 0.002), immediate memory (p = 0.003) and delayed memory (p = 0.021). BDNF levels among the smokers who were Val allele carriers were correlated with the degree of cognitive impairments, especially attention, as well as with the carbon monoxide concentrations. Our findings suggest that smoking is associated with cognitive impairment in a male Chinese Han population. The association between higher BDNF levels and cognitive impairment, mainly attention in smokers appears to be dependent on the BDNF Val66Met polymorphism.

[1]  Elliot A. Stein,et al.  Dual role of nicotine in addiction and cognition: A review of neuroimaging studies in humans , 2014, Neuropharmacology.

[2]  M. Kassiou,et al.  Determination and reduction of translocator protein (TSPO) ligand rs6971 discrimination† †The authors declare no competing interests. , 2016, MedChemComm.

[3]  R. Ophoff,et al.  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. , 2012, Psychiatric genetics.

[4]  S. Bhang,et al.  Changes in plasma brain-derived neurotrophic factor levels in smokers after smoking cessation , 2010, Neuroscience Letters.

[5]  C. Montag,et al.  Epistasis of the DRD2/ANKK1 Taq Ia and the BDNF Val66Met Polymorphism Impacts Novelty Seeking and Harm Avoidance , 2010, Neuropsychopharmacology.

[6]  F. Joseph McClernon,et al.  Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization , 2006, Psychopharmacology.

[7]  Low BDNF is associated with cognitive impairment in chronic patients with schizophrenia , 2012, Psychopharmacology.

[8]  C. A. Johnson,et al.  Tobacco smoking, quitting, and relapsing among adult males in Mainland China: the China Seven Cities Study. , 2013, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[9]  Ian J Deary,et al.  Smoking, childhood IQ, and cognitive function in old age. , 2012, Journal of psychosomatic research.

[10]  C. Montag,et al.  The BDNF Val66Met polymorphism and smoking , 2008, Neuroscience Letters.

[11]  I. Agartz,et al.  Brain-derived neurotrophic factor polymorphisms and frontal cortex morphology in schizophrenia , 2008, Psychiatric genetics.

[12]  D. Drobes,et al.  Nicotine self‐medication of cognitive‐attentional processing , 2009, Addiction biology.

[13]  A. Ciobica,et al.  Nicotine-induced memory impairment by increasing brain oxidative stress , 2009, Central European Journal of Biology.

[14]  J. Baraban,et al.  Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation , 2009, Proceedings of the National Academy of Sciences.

[15]  I. Deary,et al.  Smoking and cognitive change from age 11 to 66 years: a confirmatory investigation. , 2007, Addictive behaviors.

[16]  P. Hardy,et al.  Tobacco use is associated with increased plasma BDNF levels in depressed patients , 2016, Psychiatry Research.

[17]  Chapel Hill Genome-wide meta-analyses identify multiple loci associated with smoking behavior. , 2010 .

[18]  S. Calza,et al.  Low brain‐derived neurotrophic factor (BDNF) levels in serum of Huntington's disease patients , 2007, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[19]  Paresh D Patel,et al.  Variant Brain-Derived Neurotrophic Factor (BDNF) (Met66) Alters the Intracellular Trafficking and Activity-Dependent Secretion of Wild-Type BDNF in Neurosecretory Cells and Cortical Neurons , 2004, The Journal of Neuroscience.

[20]  Falk W. Lohoff,et al.  Association of the met66 allele of brain-derived neurotrophic factor (BDNF) with smoking , 2007, Psychopharmacology.

[21]  Kaarin J Anstey,et al.  Smoking as a risk factor for dementia and cognitive decline: a meta-analysis of prospective studies. , 2007, American journal of epidemiology.

[22]  S. File,et al.  Acute nicotine decreases, and chronic nicotine increases the expression of brain-derived neurotrophic factor mRNA in rat hippocampus. , 2000, Brain research. Molecular brain research.

[23]  Vital signs: current cigarette smoking among adults aged ≥18 years--United States, 2005-2010. , 2011, MMWR. Morbidity and mortality weekly report.

[24]  B. Penninx,et al.  Effect of variation in BDNF Val(66)Met polymorphism, smoking, and nicotine dependence on symptom severity of depressive and anxiety disorders. , 2015, Drug and alcohol dependence.

[25]  Y. Fang,et al.  Lack of effect of brain derived neurotrophic factor (BDNF) Val66Met polymorphism on early onset schizophrenia in Chinese Han population , 2011, Brain Research.

[26]  Zhijun Zhang,et al.  Cognitive and serum BDNF correlates of BDNF Val66Met gene polymorphism in patients with schizophrenia and normal controls , 2012, Human Genetics.

[27]  C. Randolph,et al.  The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): preliminary clinical validity. , 1998, Journal of clinical and experimental neuropsychology.

[28]  B. Lu,et al.  Modulation of hippocampal synaptic transmission and plasticity by neurotrophins. , 2000, Progress in brain research.

[29]  T. Kosten,et al.  The study of BDNF Val66Met polymorphism in Chinese schizophrenic patients , 2010, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[30]  P. Newhouse,et al.  Effects of nicotinic stimulation on cognitive performance. , 2004, Current opinion in pharmacology.

[31]  Xiang Yang Zhang,et al.  Decreased serum BDNF levels in chronic institutionalized schizophrenia on long-term treatment with typical and atypical antipsychotics , 2009, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[32]  E. Esposito,et al.  The neurobiological bases for the pharmacotherapy of nicotine addiction. , 2007, Current pharmaceutical design.

[33]  M. Egan,et al.  Brain-Derived Neurotrophic Factor val66met Polymorphism Affects Human Memory-Related Hippocampal Activity and Predicts Memory Performance , 2003, The Journal of Neuroscience.

[34]  A Hofman,et al.  Effect of smoking on global cognitive function in nondemented elderly , 2004, Neurology.

[35]  R. Coletta,et al.  Impact of smoking on inflammation: overview of molecular mechanisms , 2011, Inflammation Research.

[36]  Mu-ming Poo,et al.  Neurotrophins as synaptic modulators , 2001, Nature Reviews Neuroscience.

[37]  T. Kosten,et al.  BDNF Levels and Genotype are Associated with Antipsychotic-Induced Weight Gain in Patients with Chronic Schizophrenia , 2008, Neuropsychopharmacology.

[38]  W. Verschuren,et al.  Smoking and cognitive decline among middle-aged men and women: the Doetinchem Cohort Study. , 2008, American journal of public health.

[39]  C. Siao,et al.  Genetic Variant BDNF (Val66Met) Polymorphism Alters Anxiety-Related Behavior , 2006, Science.

[40]  Z. Bao Repeatable Battery for the Assessment of Neuropsychological Status as a Screening Test in Chinese:Reliability and Validity , 2008 .

[41]  Muriel Walshe,et al.  Association between BDNF val66 met genotype and episodic memory , 2005, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[42]  W. Au,et al.  Cigarette smoking in China: public health, science, and policy , 2012, Reviews on environmental health.

[43]  Zhijun Zhang,et al.  Association study of the decreased serum BDNF concentrations in amnestic mild cognitive impairment and the Val66Met polymorphism in Chinese Han. , 2008, The Journal of clinical psychiatry.

[44]  S. Heishman,et al.  Meta-analysis of the acute effects of nicotine and smoking on human performance , 2010, Psychopharmacology.

[45]  G. Zunta-Soares,et al.  Effects of cigarette smoking and alcohol use on neurocognition and BDNF levels in a Chinese population , 2015, Psychopharmacology.

[46]  Ming D. Li,et al.  Significant association of BDNF haplotypes in European‐American male smokers but not in European‐American female or African‐American smokers , 2005, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[47]  Tuomo Hänninen,et al.  BDNF is a novel marker of cognitive function in ageing women: The DR’s EXTRA Study , 2008, Neurobiology of Learning and Memory.

[48]  Ming D. Li,et al.  Genome-wide meta-analyses identify multiple loci associated with smoking behavior , 2010, Nature Genetics.

[49]  K. Fagerström,et al.  Measuring degree of physical dependence to tobacco smoking with reference to individualization of treatment. , 1978, Addictive behaviors.

[50]  J. Leon,et al.  A meta-analysis of worldwide studies demonstrates an association between schizophrenia and tobacco smoking behaviors , 2005, Schizophrenia Research.

[51]  Y. Barde,et al.  Regional distribution of brain‐derived neurotrophic factor mRNA in the adult mouse brain. , 1990, The EMBO journal.

[52]  S. Tsai,et al.  Effects of BDNF polymorphisms on brain function and behavior in health and disease , 2011, Brain Research Bulletin.

[53]  K. Bath,et al.  BDNF control of adult SVZ neurogenesis. , 2012, Developmental psychobiology.

[54]  Ming D. Li,et al.  A genome-wide scan to identify loci for smoking rate in the Framingham Heart Study population , 2003, BMC Genetics.

[55]  M. Marmot,et al.  Smoking history and cognitive function in middle age from the Whitehall II study. , 2008, Archives of internal medicine.

[56]  G Kishi,et al.  Reliability and Validity , 1999 .

[57]  M. Egan,et al.  The BDNF val66met Polymorphism Affects Activity-Dependent Secretion of BDNF and Human Memory and Hippocampal Function , 2003, Cell.

[58]  A. Benitez,et al.  Serum Brain-Derived Neurotrophic Factor Is Associated With Cognitive Function in Healthy Older Adults , 2008, Journal of geriatric psychiatry and neurology.

[59]  Gary E. Swan,et al.  The Effects of Tobacco Smoke and Nicotine on Cognition and the Brain , 2007, Neuropsychology Review.

[60]  B. Penninx,et al.  Association between smoking, nicotine dependence, and BDNF Val66Met polymorphism with BDNF concentrations in serum. , 2015, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[61]  A. Nordberg,et al.  Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells , 2003, Neurochemistry International.