How cigarette smoking may increase the risk of anxiety symptoms and anxiety disorders: A critical review of biological pathways

Brain and Behavior

Volumn 3, Issue 3, 2013, Pages 302-326

  Moylan, Steven ^a   Jacka, Felice N ^a,b   Pasco, Julie A ^a,b   Berk, Michael ^a,b,c,d  

^a DEAKIN UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

Anxiety; Anxiety disorder; Cigarette; Epigenetic; Inflammation; Mitochondria; Neurodevelopment; Neurotransmitters; Neurotrophins; Nicotine; Nitrosative stress; Oxidative stress

Indexed keywords

AMFEBUTAMONE; BRAIN DERIVED NEUROTROPHIC FACTOR; CIGARETTE SMOKE; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MECAMYLAMINE; NERVE GROWTH FACTOR; NEUROTROPHIN; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; SOLUBLE INTERLEUKIN 2 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANXIETY DISORDER; ARTICLE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DEPRESSION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EARLY LIFE STRESS; EPIGENETICS; HUMAN; IMMUNOREACTIVITY; INFLAMMATION; LIPID PEROXIDATION; MITOCHONDRIAL ENERGY TRANSFER; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK ASSESSMENT; SMOKING; SMOKING CESSATION;

EID: 84890199570     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.137     Document Type: Article

References (291)

1. Abdel-Rahman, A., A. M. Dechkovskaia, J. M. Sutton, W. C. Chen, X. Guan, W. A. Khan, et al. 2005. Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and elevated expression of glial fibrillary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty. Toxicology 209:245-261.
2. Abreu-Villaca, Y., F. J. Seidler, and T. A. Slotkin. 2003a. Impact of adolescent nicotine exposure on adenylyl cyclase-mediated cell signaling: enzyme induction, neurotransmitter-specific effects, regional selectivities, and the role of withdrawal. Brain Res. 988:164-172.
3. Abreu-Villaca, Y., F. J. Seidler, C. A. Tate, and T. A. Slotkin. 2003b. Nicotine is a neurotoxin in the adolescent brain: critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations. Brain Res. 979:114-128.
4. Abreu-Villaca, Y., F. J. Seidler, D. Qiao, C. A. Tate, M. M. Cousins, I. Thillai, et al. 2003c. Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: critical periods, patterns of exposure, dose thresholds. Neuropsychopharmacology 28:1935-1949.
5. Aksu, I., B. Baykara, S. Ozbal, F. Cetin, A. R. Sisman, A. Dayi, et al. 2012. Maternal treadmill exercise during pregnancy decreases anxiety and increases prefrontal cortex VEGF and BDNF levels of rat pups in early and late periods of life. Neurosci. Lett. 516:221-225.
6. Alleva, E., and N. Francia. 2009. Psychiatric vulnerability: suggestions from animal models and role of neurotrophins. Neurosci. Biobehav. Rev. 33:525-536.
7. Aloe, L., E. Alleva, A. Bohm, and R. Levi-Montalcini. 1986. Aggressive behavior induces release of nerve growth factor from mouse salivary gland into the bloodstream. Proc. Natl. Acad. Sci. USA 83:6184-6187.
8. Aloe, L., L. Bracci-Laudiero, E. Alleva, A. Lambiase, A. Micera, and P. Tirassa. 1994. Emotional stress induced by parachute jumping enhances blood nerve growth factor levels and the distribution of nerve growth factor receptors in lymphocytes. Proc. Natl. Acad. Sci. USA 91:10440-10444.
9. Aloe, L., E. Alleva, and M. Fiore. 2002. Stress and nerve growth factor: findings in animal models and humans. Pharmacol. Biochem. Behav. 73:159-166.
10. Ambrose, J. A., and R. S. Barua. 2004. The pathophysiology of cigarette smoking and cardiovascular disease: an update. J. Am. Coll. Cardiol. 43:1731-1737.
11. Ameringer, K. J., and A. M. Leventhal. 2010. Applying the tripartite model of anxiety and depression to cigarette smoking: an integrative review. Nicotine Tob. Res. 12:1183-1194.
12. Anbarasi, K., G. Vani, K. Balakrishna, and C. S. Devi. 2005a. Effect of bacoside A on membrane-bound ATPases in the brain of rats exposed to cigarette smoke. J. Biochem. Mol. Toxicol. 19:59-65.
13. Anbarasi, K., G. Vani, and C. S. Devi. 2005b. Protective effect of bacoside A on cigarette smoking-induced brain mitochondrial dysfunction in rats. J. Environ. Pathol. Toxicol. Oncol. 24:225-234.
14. Anbarasi, K., G. Vani, K. Balakrishna, and C. S. Devi. 2006a. Effect of bacoside A on brain antioxidant status in cigarette smoke exposed rats. Life Sci. 78:1378-1384.
15. Anbarasi, K., G. Kathirvel, G. Vani, G. Jayaraman, and C. S. Shyamala Devi. 2006b. Cigarette smoking induces heat shock protein 70 kDa expression and apoptosis in rat brain: modulation by bacoside A. Neuroscience 138:1127-1135.
16. Anglin, R. E., S. L. Garside, M. A. Tarnopolsky, M. F. Mazurek, and P. I. Rosebush. 2012. The psychiatric manifestations of mitochondrial disorders: a case and review of the literature. J. Clin. Psychiatry 73:506-512.
17. Argyropoulos, S. V., S. D. Hood, M. Adrover, C. J. Bell, A. S. Rich, J. R. Nash, et al. 2004. Tryptophan depletion reverses the therapeutic effect of selective serotonin reuptake inhibitors in social anxiety disorder. Biol. Psychiatry 56:503-509.
18. Arias, H. R. 2009. Is the inhibition of nicotinic acetylcholine receptors by bupropion involved in its clinical actions? Int. J. Biochem. Cell Biol. 41:2098-2108.
19. Armani, C., L. Jr Landini, and A. Leone. 2009. Molecular and biochemical changes of the cardiovascular system due to smoking exposure. Curr. Pharm. Des. 15:1038-1053.
20. Asami, T., F. Hayano, M. Nakamura, H. Yamasue, K. Uehara, T. Otsuka, et al. 2008. Anterior cingulate cortex volume reduction in patients with panic disorder. Psychiatry Clin. Neurosci. 62:322-330.
21. Asami, T., H. Yamasue, F. Hayano, M. Nakamura, K. Uehara, T. Otsuka, et al. 2009. Sexually dimorphic gray matter volume reduction in patients with panic disorder. Psychiatry Res. 173:128-134.
22. Atluri, P., M. W. Fleck, Q. Shen, S. J. Mah, D. Stadfelt, W. Barnes, et al. 2001. Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev. Biol. 240:143-156.
23. Atmaca, M., M. Kuloglu, E. Tezcan, and B. Ustundag. 2008. Antioxidant enzyme and malondialdehyde levels in patients with social phobia. Psychiatry Res. 159:95-100.
24. Ayling, E., M. Aghajani, J. P. Fouche, and N. van der Wee. 2012. Diffusion tensor imaging in anxiety disorders. Curr. Psychiatry Rep. 14:197-202.
25. Bandiera, F. C., A. K. Richardson, D. J. Lee, J. P. He, and K. R. Merikangas. 2011. Secondhand smoke exposure and mental health among children and adolescents. Arch. Pediatr. Adolesc. Med. 165:332-338.
26. Barrot, M., D. L. Wallace, C. A. Bolanos, D. L. Graham, L. I. Perrotti, R. L. Neve, et al. 2005. Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 102:8357-8362.
27. Baskaran, S., S. Lakshmi, and P. R. Prasad. 1999. Effect of cigarette smoke on lipid peroxidation and antioxidant enzymes in albino rat. Indian J. Exp. Biol. 37:1196-1200.
28. Baur, V., J. Hanggi, M. Rufer, A. Delsignore, L. Jancke, U. Herwig, et al. 2011. White matter alterations in social anxiety disorder. J. Psychiatr. Res. 45:1366-1372.
29. Bejerot, S., and M. Humble. 1999. Low prevalence of smoking among patients with obsessive-compulsive disorder. Compr. Psychiatry 40:268-272.
30. Bell, C. J., S. D. Hood, and D. J. Nutt. 2005. Acute tryptophan depletion. Part II: clinical effects and implications. Aust. NZ J. Psychiatry 39:565-574.
31. Belluardo, N., G. Mudo, M. Blum, N. Itoh, L. Agnati, and K. Fuxe. 2004. Nicotine-induced FGF-2 mRNA in rat brain is preserved during aging. Neurobiol. Aging 25:1333-1342.
32. Berk, M., H. Plein, and D. Ferreira. 2001. Platelet glutamate receptor supersensitivity in major depressive disorder. Clin. Neuropharmacol. 24:129-132.
33. Berk, M., F. Kapczinski, A. C. Andreazza, O. M. Dean, F. Giorlando, M. Maes, et al. 2011. Pathways underlying neuroprogression in bipolar disorder: focus on inflammation, oxidative stress and neurotrophic factors. Neurosci. Biobehav. Rev. 35:804-817.
34. Berk, M., O. M. Dean, S. M. Cotton, C. S. Gama, F. Kapczinski, B. Fernandes, et al. 2012. Maintenance N-acetyl cysteine treatment for bipolar disorder: a double-blind randomised placebo controlled trial. BMC Med. 10:91.
35. Berry, A., V. Bellisario, S. Capoccia, P. Tirassa, A. Calza, E. Alleva, et al. 2012. Social deprivation stress is a triggering factor for the emergence of anxiety- and depression-like behaviours and leads to reduced brain BDNF levels in C57BL/6J mice. Psychoneuroendocrinology 37:762-772.
36. Bertrand, D. 2010. Neurocircuitry of the nicotinic cholinergic system. Dialogues Clin. Neurosci. 12:463-470.
37. Bhagwat, S. V., C. Vijayasarathy, H. Raza, J. Mullick, and N. G. Avadhani. 1998. Preferential effects of nicotine and 4-(N-methyl-N-nitrosamine)-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.
38. Bhalla, D. K., F. Hirata, A. K. Rishi, and C. G. Gairola. 2009. Cigarette smoke, inflammation, and lung injury: a mechanistic perspective. J. Toxicol. Environ. Health B Crit. Rev. 12:45-64.
39. Bhang, S. Y., S. W. Choi, and J. H. Ahn. 2010. Changes in plasma brain-derived neurotrophic factor levels in smokers after smoking cessation. Neurosci. Lett. 468:7-11.
40. Bhang, S. Y., K. Kim, S. W. Choi, and J. H. Ahn. 2012. Do levels of brain-derived neurotrophic factor (BDNF) in plasma correlate with psychopathology in healthy subjects? Neurosci. Lett. 512:72-77.
41. Bob, P., J. Raboch, M. Maes, M. Susta, J. Pavlat, D. Jasova, et al. 2010. Depression, traumatic stress and interleukin-6. J. Affect. Disord. 120:231-234.
42. Bolam, B., R. West, and D. Gunnell. 2011. Does smoking cessation cause depression and anxiety? Findings from the ATTEMPT cohort. Nicotine Tob. Res. 13:209-214.
43. Brambilla, F., G. Perna, L. Bellodi, C. Arancio, A. Bertani, G. Perini, et al. 1997. Plasma interleukin-1 beta and tumor necrosis factor concentrations in obsessive-compulsive disorders. Biol. Psychiatry 42:976-981.
44. Brambilla, F., L. Bellodi, and G. Perna. 1999. Plasma levels of tumor necrosis factor-alpha in patients with panic disorder: effect of alprazolam therapy. Psychiatry Res. 89:21-27.
45. Branchi, I., N. Francia, and E. Alleva. 2004. Epigenetic control of neurobehavioural plasticity: the role of neurotrophins. Behav. Pharmacol. 15:353-362.
46. Breslau, N., and D. F. Klein. 1999. Smoking and panic attacks: an epidemiologic investigation. Arch. Gen. Psychiatry 56:1141-1147.
47. Breslau, N., M. Kilbey, and P. Andreski. 1991. Nicotine dependence, major depression, and anxiety in young adults. Arch. Gen. Psychiatry 48:1069-1074.
48. Brion, M. J., C. Victora, A. Matijasevich, B. Horta, L. Anselmi, C. Steer, et al. 2010. Maternal smoking and child psychological problems: disentangling causal and noncausal effects. Pediatrics 126:e57-e65.
49. Brody, A. L., M. A. Mandelkern, M. E. Jarvik, G. S. Lee, E. C. Smith, J. C. Huang, et al. 2004. Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol. Psychiatry 55:77-84.
50. Brody, A. L., M. A. Mandelkern, R. E. Olmstead, Z. Allen-Martinez, D. Scheibal, A. L. Abrams, et al. 2009. Ventral striatal dopamine release in response to smoking a regular vs a denicotinized cigarette. Neuropsychopharmacology 34:282-289.
51. Brown, R. W., and B. Kolb. 2001. Nicotine sensitization increases dendritic length and spine density in the nucleus accumbens and cingulate cortex. Brain Res. 899:94-100.
52. Brown, R. A., P. M. Lewinsohn, J. R. Seeley, and E. F. Wagner. 1996. Cigarette smoking, major depression, and other psychiatric disorders among adolescents. J. Am. Acad. Child Adolesc. Psychiatry 35:1602-1610.
53. Casarotto, P. C., V. C. de Bortoli, and H. Jr Zangrossi. 2012. Intrahippocampal injection of brain-derived neurotrophic factor increases anxiety-related, but not panic-related defensive responses: involvement of serotonin. Behav. Pharmacol. 23:80-88.
54. Casolini, P., A. Catalani, A. R. Zuena, and L. Angelucci. 2002. Inhibition of COX-2 reduces the age-dependent increase of hippocampal inflammatory markers, corticosterone secretion, and behavioral impairments in the rat. J. Neurosci. Res. 68:337-343.
55. Chakraborty, S., O. P. Singh, A. Dasgupta, N. Mandal, and H. Nath Das. 2009. Correlation between lipid peroxidation-induced TBARS level and disease severity in obsessive-compulsive disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 33:363-366.
56. Chan, S. H., C. W. Wu, A. Y. Chang, K. S. Hsu, and J. Y. Chan. 2010. Transcriptional upregulation of brain-derived neurotrophic factor in rostral ventrolateral medulla by angiotensin II: significance in superoxide homeostasis and neural regulation of arterial pressure. Circ. Res. 107:1127-1139.
57. Chandrashekara, S., K. Jayashree, H. B. Veeranna, H. S. Vadiraj, M. N. Ramesh, A. Shobha, et al. 2007. Effects of anxiety on TNF-alpha levels during psychological stress. J. Psychosom. Res. 63:65-69.
58. Cheeta, S., P. J. Kenny, and S. E. File. 2000. The role of 5-HT1A receptors in mediating the anxiogenic effects of nicotine following lateral septal administration. Eur. J. Neurosci. 12:3797-3802.
59. Chenevier-Gobeaux, C., C. Simonneau, P. Therond, D. Bonnefont-Rousselot, S. Poiraudeau, O. G. Ekindjian, et al. 2007. Implication of cytosolic phospholipase A2 (cPLA2) in the regulation of human synoviocyte NADPH oxidase (Nox2) activity. Life Sci. 81:1050-1058.
60. Chou, K. L., C. S. Mackenzie, K. Liang, and J. Sareen. 2011. Three-year incidence and predictors of first-onset of DSM-IV mood, anxiety, and substance use disorders in older adults: results from Wave 2 of the National Epidemiologic Survey on Alcohol and Related Conditions. J. Clin. Psychiatry 72:144-155.
61. Cirulli, F., A. Berry, L. T. Bonsignore, F. Capone, I. D'Andrea, L. Aloe, et al. 2010. Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci. Biobehav. Rev. 34:808-820.
62. Covey, L. S., A. H. Glassman, and F. Stetner. 1998. Cigarette smoking and major depression. J. Addict. Dis. 17:35-46.
63. Cuijpers, P., F. Smit, M. ten Have, and R. de Graaf. 2007. Smoking is associated with first-ever incidence of mental disorders: a prospective population-based study. Addiction 102:1303-1309.
64. Damsa, C., M. Kosel, and J. Moussally. 2009. Current status of brain imaging in anxiety disorders. Curr. Opin. Psychiatry 22:96-110.
65. Dani, J. A., and D. Bertrand. 2007. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47:699-729.
66. Dantzer, R., J. C. O'Connor, G. G. Freund, R. W. Johnson, and K. W. Kelley. 2008. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9:46-56.
67. Das, S., N. Gautam, S. K. Dey, T. Maiti, and S. Roy. 2009. Oxidative stress in the brain of nicotine-induced toxicity: protective role of Andrographis paniculata Nees and vitamin E. Appl. Physiol. Nutr. Metab. 34:124-135.
68. De Bellis, M. D., B. J. Casey, R. E. Dahl, B. Birmaher, D. E. Williamson, K. M. Thomas, et al. 2000. A pilot study of amygdala volumes in pediatric generalized anxiety disorder. Biol. Psychiatry 48:51-57.
69. DeBry, S. C., and S. T. Tiffany. 2008. Tobacco-induced neurotoxicity of adolescent cognitive development (TINACD): a proposed model for the development of impulsivity in nicotine dependence. Nicotine Tob. Res. 10:11-25.
70. Deckersbach, T., D. D. Dougherty, and S. L. Rauch. 2006. Functional imaging of mood and anxiety disorders. J. Neuroimaging 16:1-10.
71. Delibas, N., R. Ozcankaya, I. Altuntas, and R. Sutcu. 2003. Effect of cigarette smoke on lipid peroxidation, antioxidant enzymes and NMDA receptor subunits 2A and 2B concentration in rat hippocampus. Cell Biochem. Funct. 21:69-73.
72. Denys, D., S. Fluitman, A. Kavelaars, C. Heijnen, and H. Westenberg. 2004. Decreased TNF-alpha and NK activity in obsessive-compulsive disorder. Psychoneuroendocrinology 29:945-952.
73. Descarries, L., V. Gisiger, and M. Steriade. 1997. Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol. 53:603-625.
74. Djuric, V. J., E. Dunn, D. H. Overstreet, A. Dragomir, and M. Steiner. 1999. Antidepressant effect of ingested nicotine in female rats of Flinders resistant and sensitive lines. Physiol. Behav. 67:533-537.
75. Dome, P., J. Lazary, M. P. Kalapos, and Z. Rihmer. 2010. Smoking, nicotine and neuropsychiatric disorders. Neurosci. Biobehav. Rev. 34:295-342.
76. Doura, M. B., T. V. Luu, N. H. Lee, and D. C. Perry. 2010. Persistent gene expression changes in ventral tegmental area of adolescent but not adult rats in response to chronic nicotine. Neuroscience 170:503-513.
77. van Duinen, M. A., K. R. Schruers, G. R. Kenis, A. Wauters, J. Delanghe, E. J. Griez, et al. 2008. Effects of experimental panic on neuroimmunological functioning. J. Psychosom. Res. 64:305-310.
78. Durazzo, T. C., D. J. Meyerhoff, and S. J. Nixon. 2010. Chronic cigarette smoking: implications for neurocognition and brain neurobiology. Int. J. Environ. Res. Public Health 7:3760-3791.
79. Dwyer, J. B., R. S. Broide, and F. M. Leslie. 2008. Nicotine and brain development. Birth Defects Res. C Embryo Today 84:30-44.
80. Einat, H., P. Yuan, and H. K. Manji. 2005. Increased anxiety-like behaviors and mitochondrial dysfunction in mice with targeted mutation of the Bcl-2 gene: further support for the involvement of mitochondrial function in anxiety disorders. Behav. Brain Res. 165:172-180.
81. Eppolito, A. K., S. E. Bachus, C. G. McDonald, J. H. Meador-Woodruff, and R. F. Smith. 2010. Late emerging effects of prenatal and early postnatal nicotine exposure on the cholinergic system and anxiety-like behavior. Neurotoxicol. Teratol. 32:336-345.
82. Ersan, S., S. Bakir, E. Erdal Ersan, and O. Dogan. 2006. Examination of free radical metabolism and antioxidant defence system elements in patients with obsessive-compulsive disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 30:1039-1042.
83. Filiou, M. D., Y. Zhang, L. Teplytska, S. Reckow, P. Gormanns, G. Maccarrone, et al. 2011. Proteomics and metabolomics analysis of a trait anxiety mouse model reveals divergent mitochondrial pathways. Biol. Psychiatry 70:1074-1082.
84. Fluitman, S., D. Denys, N. Vulink, S. Schutters, C. Heijnen, and H. Westenberg. 2010. Lipopolysaccharide-induced cytokine production in obsessive-compulsive disorder and generalized social anxiety disorder. Psychiatry Res. 178:313-316.
85. Formaggio, E., F. Fazzini, A. C. Dalfini, M. Di Chio, C. Cantu, I. Decimo, et al. 2010. Nicotine increases the expression of neurotrophin receptor tyrosine kinase receptor A in basal forebrain cholinergic neurons. Neuroscience 166:580-589.
86. Fowler, J. S., N. D. Volkow, G. J. Wang, N. Pappas, J. Logan, C. Shea, et al. 1996a. Brain monoamine oxidase A inhibition in cigarette smokers. Proc. Natl. Acad. Sci. USA 93:14065-14069.
87. Fowler, J. S., N. D. Volkow, G. J. Wang, N. Pappas, J. Logan, R. MacGregor, et al. 1996b. Inhibition of monoamine oxidase B in the brains of smokers. Nature 379:733-736.
88. French, S. J., T. Humby, C. H. Horner, M. V. Sofroniew, and M. Rattray. 1999. Hippocampal neurotrophin and trk receptor mRNA levels are altered by local administration of nicotine, carbachol and pilocarpine. Brain Res. Mol. Brain Res. 67:124-136.
89. Fuller, B. F., M. S. Gold, K. K. Wang, and A. K. Ottens. 2010. Effects of environmental tobacco smoke on adult rat brain biochemistry. J. Mol. Neurosci. 41:165-171.
90. Gallinat, J., E. Meisenzahl, L. K. Jacobsen, P. Kalus, J. Bierbrauer, T. Kienast, et al. 2006. Smoking and structural brain deficits: a volumetric MR investigation. Eur. J. Neurosci. 24:1744-1750.
91. Gellert, C., B. Schottker, and H. Brenner. 2012. Smoking and all-cause mortality in older people: systematic review and meta-analysis smoking and all-cause mortality in older people. Arch. Intern. Med. 172:837-844.
92. Gentry, C. L., and R. J. Lukas. 2002. Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr. Drug Targets CNS Neurol. Disord. 1:359-385.
93. George, T. P., K. A. Sacco, J. C. Vessicchio, A. H. Weinberger, and R. D. Shytle. 2008. Nicotinic antagonist augmentation of selective serotonin reuptake inhibitor-refractory major depressive disorder: a preliminary study. J. Clin. Psychopharmacol. 28:340-344.
94. Gergalova, G. L., and M. V. Skok. 2011. Nicotine effects on mitochondria membrane potential: participation of nicotinic acetylcholine receptors. Ukr. Biokhim. Zh. 83:13-21.
95. Giannopoulou, C., J. J. Kamma, and A. Mombelli. 2003. Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J. Clin. Periodontol. 30:145-153.
96. Gill, J. M., L. Saligan, S. Woods, and G. Page. 2009. PTSD is associated with an excess of inflammatory immune activities. Perspect. Psychiatr. Care 45:262-277.
97. Gold, A. B., A. B. Keller, and D. C. Perry. 2009. Prenatal exposure of rats to nicotine causes persistent alterations of nicotinic cholinergic receptors. Brain Res. 1250:88-100.
98. Gomez-Pinilla, F., and S. Vaynman. 2005. A "deficient environment" in prenatal life may compromise systems important for cognitive function by affecting BDNF in the hippocampus. Exp. Neurol. 192:235-243.
99. Gons, R. A., A. G. van Norden, K. F. de Laat, L. J. van Oudheusden, I. W. van Uden, M. P. Zwiers, et al. 2011. Cigarette smoking is associated with reduced microstructural integrity of cerebral white matter. Brain 134(Pt 7):2116-2124.
100. Goodwin, R. D., P. M. Lewinsohn, and J. R. Seeley. 2005. Cigarette smoking and panic attacks among young adults in the community: the role of parental smoking and anxiety disorders. Biol. Psychiatry 58:686-693.
101. Grady, S. R., C. R. Wageman, N. E. Patzlaff, and M. J. Marks. 2012. Low concentrations of nicotine differentially desensitize nicotinic acetylcholine receptors that include α5 or α6 subunits and that mediate synaptosomal neurotransmitter release. Neuropharmacology 62:1935-1943.
102. Grybko, M. J., E. T. Hahm, W. Perrine, J. A. Parnes, W. S. Chick, G. Sharma, et al. 2011. A transgenic mouse model reveals fast nicotinic transmission in hippocampal pyramidal neurons. Eur. J. Neurosci. 33:1786-1798.
103. Guan, Z. Z., W. F. Yu, and A. Nordberg. 2003. Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells. Neurochem. Int. 43:243-249.
104. Gupta, R. K., R. Kumar, and M. Bassett. 2006. Interferon-induced depressive illness in hep C patients responds to SSRI antidepressant treatments. Neuropsychiatr. Dis. Treat. 2:355-358.
105. Hambsch, B. 2011. Altered glyoxalase 1 expression in psychiatric disorders: cause or consequence? Semin. Cell Dev. Biol. 22:302-308.
106. Han, D. H., P. F. Renshaw, S. R. Dager, A. Chung, J. Hwang, M. A. Daniels, et al. 2008. Altered cingulate white matter connectivity in panic disorder patients. J. Psychiatr. Res. 42:399-407.
107. Harvey, B. H., F. Oosthuizen, L. Brand, G. Wegener, and D. J. Stein. 2004. Stress-restress evokes sustained iNOS activity and altered GABA levels and NMDA receptors in rat hippocampus. Psychopharmacology 175:494-502.
108. Hayano, F., M. Nakamura, T. Asami, K. Uehara, T. Yoshida, T. Roppongi, et al. 2009. Smaller amygdala is associated with anxiety in patients with panic disorder. Psychiatry Clin. Neurosci. 63:266-276.
109. Herken, H., O. Akyol, H. R. Yilmaz, H. Tutkun, H. A. Savas, M. E. Ozen, et al. 2006. Nitric oxide, adenosine deaminase, xanthine oxidase and superoxide dismutase in patients with panic disorder: alterations by antidepressant treatment. Hum. Psychopharmacol. 21:53-59.
110. Hernandez, C. M., and A. V. Jr Terry. 2005. Repeated nicotine exposure in rats: effects on memory function, cholinergic markers and nerve growth factor. Neuroscience 130:997-1012.
111. Hettema, J. M., C. A. Prescott, J. M. Myers, M. C. Neale, and K. S. Kendler. 2005. The structure of genetic and environmental risk factors for anxiety disorders in men and women. Arch. Gen. Psychiatry 62:182-189.
112. Hettema, J. M., B. Kettenmann, V. Ahluwalia, C. McCarthy, W. R. Kates, J. E. Schmitt, et al. 2012. Pilot multimodal twin imaging study of generalized anxiety disorder. Depress. Anxiety 29:202-209.
113. Hilbert, J., and V. Mohsenin. 1996. Adaptation of lung antioxidants to cigarette smoking in humans. Chest 110:916-920.
114. Hoge, E. A., K. Brandstetter, S. Moshier, M. H. Pollack, K. K. Wong, and N. M. Simon. 2009. Broad spectrum of cytokine abnormalities in panic disorder and posttraumatic stress disorder. Depress. Anxiety 26:447-455.
115. Holzschneider, K., and C. Mulert. 2011. Neuroimaging in anxiety disorders. Dialogues Clin. Neurosci. 13:453-461.
116. Hovatta, I., R. S. Tennant, R. Helton, R. A. Marr, O. Singer, J. M. Redwine, et al. 2005. Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438:662-666.
117. Hovatta, I., J. Juhila, and J. Donner. 2010. Oxidative stress in anxiety and comorbid disorders. Neurosci. Res. 68:261-275.
118. Hsu, H. R., T. Y. Chen, M. H. Chan, and H. H. Chen. 2007. Acute effects of nicotine on restraint stress-induced anxiety-like behavior, c-Fos expression, and corticosterone release in mice. Eur. J. Pharmacol. 566:124-131.
119. Hudkins, M., J. O'Neill, M. C. Tobias, G. Bartzokis, and E. D. London. 2012. Cigarette smoking and white matter microstructure. Psychopharmacology 221:285-295.
120. Hulea, S. A., R. Olinescu, S. Nita, D. Crocnan, and F. A. Kummerow. 1995. Cigarette smoking causes biochemical changes in blood that are suggestive of oxidative stress: a case-control study. J. Environ. Pathol. Toxicol. Oncol. 14:173-180.
121. Hurt, R. D., D. P. Sachs, E. D. Glover, K. P. Offord, J. A. Johnston, L. C. Dale, et al. 1997. A comparison of sustained-release bupropion and placebo for smoking cessation. N. Engl. J. Med. 337:1195-1202.
122. Iniguez, S. D., B. L. Warren, E. M. Parise, L. F. Alcantara, B. Schuh, M. L. Maffeo, et al. 2009. Nicotine exposure during adolescence induces a depression-like state in adulthood. Neuropsychopharmacology 34:1609-1624.
123. Irie, M., M. Miyata, and H. Kasai. 2005. Depression and possible cancer risk due to oxidative DNA damage. J. Psychiatr. Res. 39:553-560.
124. Isensee, B., H. U. Wittchen, M. B. Stein, M. Hofler, and R. Lieb. 2003. Smoking increases the risk of panic: findings from a prospective community study. Arch. Gen. Psychiatry 60:692-700.
125. Jacobsen, L. K., M. R. Picciotto, C. J. Heath, S. J. Frost, K. A. Tsou, R. A. Dwan, et al. 2007. Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. J. Neurosci. 27:13491-13498.
126. Jamal, M., A. J. Does, B. W. Penninx, and P. Cuijpers. 2011. Age at smoking onset and the onset of depression and anxiety disorders. Nicotine Tob. Res. 13:809-819.
127. Janowsky, D. S., M. K. el-Yousef, and J. M. Davis. 1974. Acetylcholine and depression. Psychosom. Med. 36:248-257.
128. Johnson, J. G., P. Cohen, D. S. Pine, D. F. Klein, S. Kasen, and J. S. Brook. 2000. Association between cigarette smoking and anxiety disorders during adolescence and early adulthood. JAMA 284:2348-2351.
129. Jorenby, D. E., S. J. Leischow, M. A. Nides, S. I. Rennard, J. A. Johnston, A. R. Hughes, et al. 1999. A controlled trial of sustained-release bupropion, a nicotine patch, or both for smoking cessation. N. Engl. J. Med. 340:685-691.
130. Kalman, D., S. B. Morissette, and T. P. George. 2005. Co-morbidity of smoking in patients with psychiatric and substance use disorders. Am. J. Addict. 14:106-123.
131. Kenny, P. J., S. E. File, and M. Rattray. 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.
132. Kessler, R. C., W. T. Chiu, O. Demler, K. R. Merikangas, and E. E. Walters. 2005. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 62:617-627.
133. Kim, M. J., and P. J. Whalen. 2009. The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. J. Neurosci. 29:11614-11618.
134. Kim, M. J., I. K. Lyoo, S. J. Kim, M. Sim, N. Kim, N. Choi, et al. 2005. Disrupted white matter tract integrity of anterior cingulate in trauma survivors. Neuroreport 16:1049-1053.
135. Kim, T. S., D. J. Kim, H. Lee, and Y. K. Kim. 2007. Increased plasma brain-derived neurotrophic factor levels in chronic smokers following unaided smoking cessation. Neurosci. Lett. 423:53-57.
136. Klein, D. F. 1993. False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch. Gen. Psychiatry 50:306-317.
137. de Knegt, R. J., G. Bezemer, A. R. Van Gool, J. P. Drenth, B. E. Hansen, H. A. Droogleever Fortuyn, et al. 2011. Randomised clinical trial: escitalopram for the prevention of psychiatric adverse events during treatment with peginterferon-alfa-2a and ribavirin for chronic hepatitis C. Aliment. Pharmacol. Ther. 34:1306-1317.
138. Konuk, N., I. O. Tekin, U. Ozturk, L. Atik, N. Atasoy, S. Bektas, et al. 2007. Plasma levels of tumor necrosis factor-alpha and interleukin-6 in obsessive compulsive disorder. Mediators Inflamm. 2007:65704.
139. Kuloglu, M., M. Atmaca, E. Tezcan, B. Ustundag, and S. Bulut. 2002. Antioxidant enzyme and malondialdehyde levels in patients with panic disorder. Neuropsychobiology 46:186-189.
140. Kulz, A. K., S. Meinzer, M. Kopasz, and U. Voderholzer. 2007. Effects of tryptophan depletion on cognitive functioning, obsessive-compulsive symptoms and mood in obsessive-compulsive disorder: preliminary results. Neuropsychobiology 56:127-131.
141. Lambers, D. S., and K. E. Clark. 1996. The maternal and fetal physiologic effects of nicotine. Semin. Perinatol. 20:115-126.
142. Lasser, K., J. W. Boyd, S. Woolhandler, D. U. Himmelstein, D. McCormick, and D. H. Bor. 2000. Smoking and mental illness: a population-based prevalence study. JAMA 284:2606-2610.
143. Launay, J. M., M. Del Pino, G. Chironi, J. Callebert, K. Peoc'h, J. L. Megnien, et al. 2009. Smoking induces long-lasting effects through a monoamine-oxidase epigenetic regulation. PLoS One 4:e7959.
144. Lawrence, D., J. Considine, F. Mitrou, and S. R. Zubrick. 2010. Anxiety disorders and cigarette smoking: results from the Australian Survey of Mental Health and Wellbeing. Aust. NZ J. Psychiatry 44:520-527.
145. Lee, E., and H. Son. 2009. Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep. 42:239-244.
146. Lee, I. N., M. H. Lin, C. Y. Chung, M. H. Lee, H. H. Weng, and J. T. Yang. 2012. Chronic cigarette smoke exposure enhances brain-derived neurotrophic factor expression in rats with traumatic brain injury. Metab. Brain Dis. 27:197-204.
147. Levin, E. D., and T. A. Slotkin. 1998. Developmental neurotoxicity of nicotine. Academic Press, San Diego.
148. Li, Y., M. A. King, and E. M. Meyer. 2000. alpha7 nicotinic receptor-mediated protection against ethanol-induced oxidative stress and cytotoxicity in PC12 cells. Brain Res. 861:165-167.
149. Li, M. D., J. K. Kane, J. Wang, and J. Z. Ma. 2004. Time-dependent changes in transcriptional profiles within five rat brain regions in response to nicotine treatment. Brain Res. Mol. Brain Res. 132:168-180.
150. Lichtensteiger, W., U. Ribary, M. Schlumpf, B. Odermatt, and H. R. Widmer. 1988. Prenatal adverse effects of nicotine on the developing brain. Prog. Brain Res. 73:137-157.
151. Linn, M. W. 1986. Modifiers and Perceived Stress Scale. J. Consult. Clin. Psychol. 54:507-513.
152. Lucca, G., C. M. Comim, S. S. Valvassori, G. Z. Reus, F. Vuolo, F. Petronilho, et al. 2009. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem. Int. 54:358-362.
153. Lucey, J. V., G. Butcher, A. W. Clare, and T. G. Dinan. 1993. Elevated growth hormone responses to pyridostigmine in obsessive-compulsive disorder: evidence of cholinergic supersensitivity. Am. J. Psychiatry 150:961-962.
154. Luchese, C., S. Pinton, and C. W. Nogueira. 2009. Brain and lungs of rats are differently affected by cigarette smoke exposure: antioxidant effect of an organoselenium compound. Pharmacol. Res. 59:194-201.
155. Ma, Z., R. E. Strecker, J. T. McKenna, M. M. Thakkar, R. W. McCarley, and R. Tao. 2005. Effects on serotonin of (-)nicotine and dimethylphenylpiperazinium in the dorsal raphe and nucleus accumbens of freely behaving rats. Neuroscience 135:949-958.
156. Maes, M., H. Y. Meltzer, and E. Bosmans. 1994. Psychoimmune investigation in obsessive-compulsive disorder: assays of plasma transferrin, IL-2 and IL-6 receptor, and IL-1 beta and IL-6 concentrations. Neuropsychobiology 30:57-60.
157. Maes, M., C. Song, A. Lin, R. De Jongh, A. Van Gastel, G. Kenis, et al. 1998. The effects of psychological stress on humans: increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety. Cytokine 10:313-318.
158. Maes, M., A. H. Lin, L. Delmeire, A. Van Gastel, G. Kenis, R. De Jongh, et al. 1999. Elevated serum interleukin-6 (IL-6) and IL-6 receptor concentrations in posttraumatic stress disorder following accidental man-made traumatic events. Biol. Psychiatry 45:833-839.
159. Maes, M., S. Bonaccorso, V. Marino, A. Puzella, M. Pasquini, M. Biondi, et al. 2001. Treatment with interferon-alpha (IFN alpha) of hepatitis C patients induces lower serum dipeptidyl peptidase IV activity, which is related to IFN alpha-induced depressive and anxiety symptoms and immune activation. Mol. Psychiatry 6:475-480.
160. Maes, M., M. Kubera, E. Obuchowiczwa, L. Goehler, and J. Brzeszcz. 2011a. Depression's multiple comorbidities explained by (neuro)inflammatory and oxidative & nitrosative stress pathways. Neuro. Endocrinol. Lett. 32:7-24.
161. Maes, M., P. Galecki, Y. S. Chang, and M. Berk. 2011b. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog. Neuropsychopharmacol. Biol. Psychiatry 35:676-692.
162. Maes, M., I. Mihaylova, M. Kubera, and K. Ringel. 2012. Activation of cell-mediated immunity in depression: association with inflammation, melancholia, clinical staging and the fatigue and somatic symptom cluster of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 36:169-175.
163. Maggio, R., M. Riva, F. Vaglini, F. Fornai, G. Racagni, and G. U. Corsini. 1997. Striatal increase of neurotrophic factors as a mechanism of nicotine protection in experimental parkinsonism. J. Neural Transm. 104:1113-1123.
164. Malone, K. M., C. Waternaux, G. L. Haas, T. B. Cooper, S. Li, and J. J. Mann. 2003. Cigarette smoking, suicidal behavior, and serotonin function in major psychiatric disorders. Am. J. Psychiatry 160:773-779.
165. Manji, H., T. Kato, N. A. Di Prospero, S. Ness, M. F. Beal, M. Krams, et al. 2012. Impaired mitochondrial function in psychiatric disorders. Nat. Rev. Neurosci. 13:293-307.
166. Mantamadiotis, T., T. Lemberger, S. C. Bleckmann, H. Kern, O. Kretz, A. Martin Villalba, et al. 2002. Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31:47-54.
167. Marazziti, D., F. Ambrogi, R. Vanacore, V. Mignani, M. Savino, L. Palego, et al. 1992. Immune cell imbalance in major depressive and panic disorders. Neuropsychobiology 26:23-26.
168. Masood, A., Y. Huang, H. Hajjhussein, L. Xiao, H. Li, W. Wang, et al. 2009. Anxiolytic effects of phosphodiesterase-2 inhibitors associated with increased cGMP signaling. J. Pharmacol. Exp. Ther. 331:690-699.
169. McClernon, F. J., F. B. Hiott, E. C. Westman, J. E. Rose, and E. D. Levin. 2006. Transdermal nicotine attenuates depression symptoms in nonsmokers: a double-blind, placebo-controlled trial. Psychopharmacology 189:125-133.
170. McDermott, M. S., T. M. Marteau, G. J. Hollands, M. Hankins, and P. Aveyard. 2013. Change in anxiety following successful and unsuccessful attempts at smoking cessation: cohort study. Br. J. Psychiatry 202:62-67.
171. McFarland, B. J., F. J. Seidler, and T. A. Slotkin. 1991. Inhibition of DNA synthesis in neonatal rat brain regions caused by acute nicotine administration. Brain Res. Dev. Brain Res. 58:223-229.
172. McGranahan, T. M., N. E. Patzlaff, S. R. Grady, S. F. Heinemann, and T. K. Booker. 2011. α4β2 nicotinic acetylcholine receptors on dopaminergic neurons mediate nicotine reward and anxiety relief. J. Neurosci. 31:10891-10902.
173. Milham, M. P., A. C. Nugent, W. C. Drevets, D. P. Dickstein, E. Leibenluft, M. Ernst, et al. 2005. Selective reduction in amygdala volume in pediatric anxiety disorders: a voxel-based morphometry investigation. Biol. Psychiatry 57:961-966.
174. Miller, A. H., V. Maletic, and C. L. Raison. 2009. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 65:732-741.
175. Mineur, Y. S., and M. R. Picciotto. 2010. Nicotine receptors and depression: revisiting and revising the cholinergic hypothesis. Trends Pharmacol. Sci. 31:580-586.
176. Miro, O., J. R. Alonso, D. Jarreta, J. Casademont, A. Urbano-Marquez, and F. Cardellach. 1999. Smoking disturbs mitochondrial respiratory chain function and enhances lipid peroxidation on human circulating lymphocytes. Carcinogenesis 20:1331-1336.
177. Miyaoka, H., Y. Suzuki, M. Taniyama, Y. Miyaoka, K. Shishikura, K. Kamijima, et al. 1997. Mental disorders in diabetic patients with mitochondrial transfer RNA(Leu) (UUR) mutation at position 3243. Biol. Psychiatry 42:524-526.
178. Monteleone, P., F. Catapano, M. Fabrazzo, A. Tortorella, and M. Maj. 1998. Decreased blood levels of tumor necrosis factor-alpha in patients with obsessive-compulsive disorder. Neuropsychobiology 37:182-185.
179. Morissette, S. B., M. T. Tull, S. B. Gulliver, B. W. Kamholz, and R. T. Zimering. 2007. Anxiety, anxiety disorders, tobacco use, and nicotine: a critical review of interrelationships. Psychol. Bull. 133:245-272.
180. Moylan, S., F. N. Jacka, J. A. Pasco, and M. Berk. 2012a. Cigarette smoking, nicotine dependence and anxiety disorders: a systematic review of population-based, epidemiological studies. BMC Med. 10:123.
181. Moylan, S., M. Maes, N. R. Wray, and M. Berk. 2012b. The neuroprogressive nature of major depressive disorder: pathways to disease evolution and resistance, and therapeutic implications. Mol. Psychiatry doi: 10.1038/mp.2012.33. [Epub ahead of print].
182. Moylan, S., H. A. Eyre, M. Maes, B. T. Baune, F. Jacka, and M. Berk. 2013. Exercising the worry away: how inflammation, oxidative and nitrogen stress mediates the beneficial effect of physical activity on anxiety disorder symptoms and behaviours. Neurosci. Biobehav. Rev. doi: 10.1016/j.neubiorev.2013.02.003. [Epub ahead of print].
183. Mueller, V., R. F. Mucha, and P. Pauli. 1998. Dependence on smoking and the acoustic startle response in healthy smokers. Pharmacol. Biochem. Behav. 59:1031-1038.
184. Mukhopadhyay, P., K. H. Horn, R. M. Greene, and M. Michele Pisano. 2010. Prenatal exposure to environmental tobacco smoke alters gene expression in the developing murine hippocampus. Reprod. Toxicol. 29:164-175.
185. Muller, N., M. J. Schwarz, S. Dehning, A. Douhe, A. Cerovecki, B. Goldstein-Muller, et al. 2006. The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine. Mol. Psychiatry 11:680-684.
186. Nakauchi, S., and K. Sumikawa. 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.
187. Navarro, H. A., F. J. Seidler, W. L. Whitmore, and T. A. Slotkin. 1988. Prenatal exposure to nicotine via maternal infusions: effects on development of catecholamine systems. J. Pharmacol. Exp. Ther. 244:940-944.
188. Neigh, G. N., K. Karelina, E. R. Glasper, S. L. Bowers, N. Zhang, P. G. Popovich, et al. 2009. Anxiety after cardiac arrest/cardiopulmonary resuscitation: exacerbated by stress and prevented by minocycline. Stroke 40:3601-3607.
189. Newman, M. B., G. W. Arendash, R. D. Shytle, P. C. Bickford, T. Tighe, and P. R. Sanberg. 2002a. Nicotine's oxidative and antioxidant properties in CNS. Life Sci. 71:2807-2820.
190. Newman, M. B., J. J. Manresa, P. R. Sanberg, and R. D. Shytle. 2002b. Anxiolytic effects of mecamylamine in two animal models of anxiety. Exp. Clin. Psychopharmacol. 10:18-25.
191. Nicoll-Griffith, D. A., J. M. Silva, N. Chauret, S. Day, Y. Leblanc, P. Roy, et al. 2001. Application of rat hepatocyte culture to predict in vivo metabolic auto-induction: studies with DFP, a cyclooxygenase-2 inhibitor. Drug Metab. Dispos. 29:159-165.
192. Niedermaier, O. N., M. L. Smith, L. A. Beightol, Z. Zukowska-Grojec, D. S. Goldstein, and D. L. Eckberg. 1993. Influence of cigarette smoking on human autonomic function. Circulation 88:562-571.
193. Nikota, J. K., and M. R. Stampfli. 2012. Cigarette smoke-induced inflammation and respiratory host defense: Insights from animal models. Pulm. Pharmacol. Ther. 25:257-262.
194. Nooyens, A. C., B. M. van Gelder, and W. M. Verschuren. 2008. Smoking and cognitive decline among middle-aged men and women: the Doetinchem Cohort Study. Am. J. Public Health 98:2244-2250.
195. Nunes, S. O., H. O. Vargas, J. Brum, E. Prado, M. M. Vargas, M. R. de Castro, et al. 2012. A comparison of inflammatory markers in depressed and nondepressed smokers. Nicotine Tob. Res. 14:540-546.
196. O'Donovan, A., B. M. Hughes, G. M. Slavich, L. Lynch, M. T. Cronin, C. O'Farrelly, et al. 2010. Clinical anxiety, cortisol and interleukin-6: evidence for specificity in emotion-biology relationships. Brain Behav. Immun. 24:1074-1077.
197. de Oliveira, M. R., R. B. Silvestrin, E. S. T. Mello, and J. C. Moreira. 2007. Oxidative stress in the hippocampus, anxiety-like behavior and decreased locomotory and exploratory activity of adult rats: effects of sub acute vitamin A supplementation at therapeutic doses. Neurotoxicology 28:1191-1199.
198. Oliveira-da-Silva, A., F. B. Vieira, F. Cristina-Rodrigues, C. C. Filgueiras, A. C. Manhaes, and Y. Abreu-Villaca. 2009. Increased apoptosis and reduced neuronal and glial densities in the hippocampus due to nicotine and ethanol exposure in adolescent mice. Int. J. Dev. Neurosci. 27:539-548.
199. Olivenza, R., M. A. Moro, I. Lizasoain, P. Lorenzo, A. P. Fernandez, J. Rodrigo, et al. 2000. Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. J. Neurochem. 74:785-791.
200. Ozdemir, E., S. Cetinkaya, S. Ersan, S. Kucukosman, and E. E. Ersan. 2009. Serum selenium and plasma malondialdehyde levels and antioxidant enzyme activities in patients with obsessive-compulsive disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 33:62-65.
201. Papakostas, G. I., M. H. Trivedi, J. E. Alpert, C. A. Seifert, A. Krishen, E. P. Goodale, et al. 2008. Efficacy of bupropion and the selective serotonin reuptake inhibitors in the treatment of anxiety symptoms in major depressive disorder: a meta-analysis of individual patient data from 10 double-blind, randomized clinical trials. J. Psychiatr. Res. 42:134-140.
202. Park, J. E., S. W. Kim, Q. Park, D. U. Jeong, and B. H. Yu. 2005. Lymphocyte subsets and mood states in panic disorder patients. J. Korean Med. Sci. 20:215-219.
203. Park, D. I., H. G. Kim, W. R. Jung, M. K. Shin, and K. L. Kim. 2011. Mecamylamine attenuates dexamethasone-induced anxiety-like behavior in association with brain derived neurotrophic factor upregulation in rat brains. Neuropharmacology 61:276-282.
204. Patton, G. C., J. B. Carlin, C. Coffey, R. Wolfe, M. Hibbert, and G. Bowes. 1998. Depression, anxiety, and smoking initiation: a prospective study over 3 years. Am. J. Public Health 88:1518-1522.
205. Paul, R. H., S. M. Grieve, R. Niaura, S. P. David, D. H. Laidlaw, R. Cohen, et al. 2008. Chronic cigarette smoking and the microstructural integrity of white matter in healthy adults: a diffusion tensor imaging study. Nicotine Tob. Res. 10:137-147.
206. Pedersen, W., and T. von Soest. 2009. Smoking, nicotine dependence and mental health among young adults: a 13-year population-based longitudinal study. Addiction 104:129-137.
207. Perez, J. A., S. M. Clinton, C. A. Turner, S. J. Watson, and H. Akil. 2009. A new role for FGF2 as an endogenous inhibitor of anxiety. J. Neurosci. 29:6379-6387.
208. Peters, R., R. Poulter, J. Warner, N. Beckett, L. Burch, and C. Bulpitt. 2008. Smoking, dementia and cognitive decline in the elderly, a systematic review. BMC Geriatr. 8:36.
209. Phan, K. L., A. Orlichenko, E. Boyd, M. Angstadt, E. F. Coccaro, I. Liberzon, et al. 2009. Preliminary evidence of white matter abnormality in the uncinate fasciculus in generalized social anxiety disorder. Biol. Psychiatry 66:691-694.
210. Picciotto, M. R., D. H. Brunzell, and B. J. Caldarone. 2002. Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport 13:1097-1106.
211. Picciotto, M. R., N. A. Addy, Y. S. Mineur, and D. H. Brunzell. 2008. It is not "either/or": activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood. Prog. Neurobiol. 84:329-342.
212. Piper, M. E., J. W. Cook, T. R. Schlam, D. E. Jorenby, and T. B. Baker. 2011. Anxiety diagnoses in smokers seeking cessation treatment: relations with tobacco dependence, withdrawal, outcome and response to treatment. Addiction 106:418-427.
213. Piquero, A. R., C. L. Gibson, S. G. Tibbetts, M. G. Turner, and S. H. Katz. 2002. Maternal cigarette smoking during pregnancy and life-course-persistent offending. Int. J. Offender Ther. Comp. Criminol. 46:231-248.
214. Plein, H., and M. Berk. 1999. The platelet intracellular calcium response to serotonin and thrombin in patients with panic disorder. Eur. Neuropsychopharmacol. 9:107-110.
215. Plein, H., and M. Berk. 2001. The platelet as a peripheral marker in psychiatric illness. Hum. Psychopharmacol. 16:229-236.
216. Polesskaya, O. O., K. J. Fryxell, A. D. Merchant, L. L. Locklear, K. F. Ker, C. G. McDonald, et al. 2007. Nicotine causes age-dependent changes in gene expression in the adolescent female rat brain. Neurotoxicol. Teratol. 29:126-140.
217. Preter, M., and D. F. Klein. 2008. Panic, suffocation false alarms, separation anxiety and endogenous opioids. Prog. Neuropsychopharmacol. Biol. Psychiatry 32:603-612.
218. Qiao, D., F. J. Seidler, J. D. Violin, and T. A. Slotkin. 2003. Nicotine is a developmental neurotoxicant and neuroprotectant: stage-selective inhibition of DNA synthesis coincident with shielding from effects of chlorpyrifos. Brain Res. Dev. Brain Res. 147:183-190.
219. Qiao, D., F. J. Seidler, and T. A. Slotkin. 2005. Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicol. Appl. Pharmacol. 206:17-26.
220. Rakofsky, J. J., K. J. Ressler, and B. W. Dunlop. 2012. BDNF function as a potential mediator of bipolar disorder and post-traumatic stress disorder comorbidity. Mol. Psychiatry 17:22-35.
221. Rapaport, M. H. 1998. Circulating lymphocyte phenotypic surface markers in anxiety disorder patients and normal volunteers. Biol. Psychiatry 43:458-463.
222. Reckziegel, P., N. Boufleur, R. C. Barcelos, D. M. Benvegnu, C. S. Pase, L. G. Muller, et al. 2011. Oxidative stress and anxiety-like symptoms related to withdrawal of passive cigarette smoke in mice: beneficial effects of pecan nut shells extract, a by-product of the nut industry. Ecotoxicol. Environ. Saf. 74:1770-1778.
223. Reichborn-Kjennerud, T., E. Roysamb, K. Tambs, S. Torgersen, E. Kringlen, P. Magnus, et al. 2004. Genetic and environmental influences on the association between smoking and panic attacks in females: a population-based twin study. Psychol. Med. 34:1271-1277.
224. Rendu, F., K. Peoc'h, I. Berlin, D. Thomas, and J. M. Launay. 2011. Smoking related diseases: the central role of monoamine oxidase. Int. J. Environ. Res. Public Health 8:136-147.
225. Reuben, M., and P. B. Clarke. 2000. Nicotine-evoked [3H]5-hydroxytryptamine release from rat striatal synaptosomes. Neuropharmacology 39:290-299.
226. Richards, M., M. J. Jarvis, N. Thompson, and M. E. Wadsworth. 2003. Cigarette smoking and cognitive decline in midlife: evidence from a prospective birth cohort study. Am. J. Public Health 93:994-998.
227. Roni, M. A., and S. Rahman. 2011. Neuronal nicotinic receptor antagonist reduces anxiety-like behavior in mice. Neurosci. Lett. 504:237-241.
228. Ross, S. A., J. Y. Wong, J. J. Clifford, A. Kinsella, J. S. Massalas, M. K. Horne, et al. 2000. Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J. Neurosci. 20:6431-6441.
229. Roth, T. L., and J. D. Sweatt. 2011. Epigenetic marking of the BDNF gene by early-life adverse experiences. Horm. Behav. 59:315-320.
230. Roth, T. L., F. D. Lubin, A. J. Funk, and J. D. Sweatt. 2009. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol. Psychiatry 65:760-769.
231. Roy, T. S., and U. Sabherwal. 1994. Effects of prenatal nicotine exposure on the morphogenesis of somatosensory cortex. Neurotoxicol. Teratol. 16:411-421.
232. Roy, T. S., J. E. Andrews, F. J. Seidler, and T. A. Slotkin. 1998. Nicotine evokes cell death in embryonic rat brain during neurulation. J. Pharmacol. Exp. Ther. 287:1136-1144.
233. Roy, T. S., F. J. Seidler, and T. A. Slotkin. 2002. Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J. Pharmacol. Exp. Ther. 300:124-133.
234. Rueff-Barroso, C. R., E. T. Trajano, J. N. Alves, R. O. Paiva, M. Lanzetti, K. M. Pires, et al. 2010. Organ-related cigarette smoke-induced oxidative stress is strain-dependent. Med. Sci. Monit. 16:BR218-BR226.
235. Sabia, S., A. Elbaz, A. Dugravot, J. Head, M. Shipley, G. Hagger-Johnson, et al. 2012. Impact of smoking on cognitive decline in early old age: the whitehall II cohort study. Arch. Gen. Psychiatry 69:627-635.
236. Salim, S., M. Asghar, M. Taneja, I. Hovatta, G. Chugh, C. Vollert, et al. 2011. Potential contribution of oxidative stress and inflammation to anxiety and hypertension. Brain Res. 1404:63-71.
237. Schaap, M. M., and A. E. Kunst. 2009. Monitoring of socio-economic inequalities in smoking: learning from the experiences of recent scientific studies. Public Health 123:103-109.
238. Schienle, A., F. Ebner, and A. Schafer. 2011. Localized gray matter volume abnormalities in generalized anxiety disorder. Eur. Arch. Psychiatry Clin. Neurosci. 261:303-307.
239. Schneider, A. S., P. Atluri, Q. Shen, W. Barnes, S. J. Mah, D. Stadfelt, et al. 2002. Functional nicotinic acetylcholine receptor expression on stem and progenitor cells of the early embryonic nervous system. Ann. NY Acad. Sci. 971:135-138.
240. Schuff, N., Y. Zhang, W. Zhan, M. Lenoci, C. Ching, L. Boreta, et al. 2011. Patterns of altered cortical perfusion and diminished subcortical integrity in posttraumatic stress disorder: an MRI study. Neuroimage 54(Suppl. 1):S62-S68.
241. Seidler, F. J., E. D. Levin, S. E. Lappi, and T. A. Slotkin. 1992. Fetal nicotine exposure ablates the ability of postnatal nicotine challenge to release norepinephrine from rat brain regions. Brain Res. Dev. Brain Res. 69:288-291.
242. Semba, J., C. Mataki, S. Yamada, M. Nankai, and M. Toru. 1998. Antidepressantlike effects of chronic nicotine on learned helplessness paradigm in rats. Biol. Psychiatry 43:389-391.
243. Shumway, S. D., M. Maki, and S. Miyamoto. 1999. The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. J. Biol. Chem. 274:30874-30881.
244. Shytle, R. D., A. A. Silver, R. J. Lukas, M. B. Newman, D. V. Sheehan, and P. R. Sanberg. 2002. Nicotinic acetylcholine receptors as targets for antidepressants. Mol. Psychiatry 7:525-535.
245. Sivonova, M., I. Zitnanova, L. Hlincikova, I. Skodacek, J. Trebaticka, and Z. Durackova. 2004. Oxidative stress in university students during examinations. Stress 7:183-188.
246. Skurlova, M., A. Stofkova, and J. Jurcovicova. 2011. Anxiety-like behavior in the elevated-plus maze tests and enhanced IL-1β, IL-6, NADPH oxidase-1, and iNOS mRNAs in the hippocampus during early stage of adjuvant arthritis in rats. Neurosci. Lett. 487:250-254.
247. Slikker, W., Jr., Z. A. Xu, E. D. Levin, and T. A. Slotkin. 2005. Mode of action: disruption of brain cell replication, second messenger, and neurotransmitter systems during development leading to cognitive dysfunction-developmental neurotoxicity of nicotine. Crit. Rev. Toxicol. 35:703-711.
248. Slotkin, T. A. 2004. Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 198:132-151.
249. Slotkin, T. A., S. E. Lappi, M. I. Tayyeb, and F. J. Seidler. 1991. Chronic prenatal nicotine exposure sensitizes rat brain to acute postnatal nicotine challenge as assessed with ornithine decarboxylase. Life Sci. 49:665-670.
250. Smith, L. N., C. G. McDonald, H. C. Bergstrom, J. M. Brielmaier, A. K. Eppolito, T. L. Wheeler, et al. 2006. Long-term changes in fear conditioning and anxiety-like behavior following nicotine exposure in adult versus adolescent rats. Pharmacol. Biochem. Behav. 85:91-97.
251. Sobczak, A., D. Golka, and I. Szoltysek-Boldys. 2004. The effects of tobacco smoke on plasma alpha- and gamma-tocopherol levels in passive and active cigarette smokers. Toxicol. Lett. 151:429-437.
252. Son, J. H., and U. H. Winzer-Serhan. 2009. Chronic neonatal nicotine exposure increases mRNA expression of neurotrophic factors in the postnatal rat hippocampus. Brain Res. 1278:1-14.
253. Sonntag, H., H. U. Wittchen, M. Hofler, R. C. Kessler, and M. B. Stein. 2000. Are social fears and DSM-IV social anxiety disorder associated with smoking and nicotine dependence in adolescents and young adults? Eur. Psychiatry 15:67-74.
254. Speck, A. E., D. Fraga, P. Soares, D. L. Scheffer, L. A. Silva, A. S. Jr Aguiar, et al. 2011. Cigarette smoke inhibits brain mitochondrial adaptations of exercised mice. Neurochem. Res. 36:1056-1061.
255. Spigset, O. 1999. Adverse reactions of selective serotonin reuptake inhibitors: reports from a spontaneous reporting system. Drug Saf. 20:277-287.
256. Stangherlin, E. C., C. Luchese, A. P. Ardais, and C. W. Nogueira. 2009. Passive smoke exposure induces oxidative damage in brains of rat pups: protective role of diphenyl diselenide. Inhal. Toxicol. 21:868-874.
257. Stedman, R. L. 1968. The chemical composition of tobacco and tobacco smoke. Chem. Rev. 68:153-207.
258. Stefanova, N. A., A. Fursova, and N. G. Kolosova. 2010. Behavioral effects induced by mitochondria-targeted antioxidant SkQ1 in Wistar and senescence-accelerated OXYS rats. J. Alzheimers Dis. 21:479-491.
259. Swan, G. E., and C. N. Lessov-Schlaggar. 2007. The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychol. Rev. 17:259-273.
260. Swendsen, J., K. P. Conway, L. Degenhardt, M. Glantz, R. Jin, K. R. Merikangas, et al. 2010. Mental disorders as risk factors for substance use, abuse and dependence: results from the 10-year follow-up of the National Comorbidity Survey. Addiction 105:1117-1128.
261. Tekinay, A. B., Y. Nong, J. M. Miwa, I. Lieberam, I. Ibanez-Tallon, P. Greengard, et al. 2009. A role for LYNX2 in anxiety-related behavior. Proc. Natl. Acad. Sci. USA 106:4477-4482.
262. Tezcan, E., M. Atmaca, M. Kuloglu, and B. Ustundag. 2003. Free radicals in patients with post-traumatic stress disorder. Eur. Arch. Psychiatry Clin. Neurosci. 253:89-91.
263. Thome, G. R., R. M. Spanevello, A. Mazzanti, A. M. Fiorenza, M. M. Duarte, S. C. da Luz, et al. 2011. Vitamin E decreased the activity of acetylcholinesterase and level of lipid peroxidation in brain of rats exposed to aged and diluted sidestream smoke. Nicotine Tob. Res. 13:1210-1219.
264. Tizabi, Y., D. H. Overstreet, A. H. Rezvani, V. A. Louis, E. Jr Clark, D. S. Janowsky, et al. 1999. Antidepressant effects of nicotine in an animal model of depression. Psychopharmacology 142:193-199.
265. Tizabi, Y., M. Al-Namaeh, K. F. Manaye, and R. E. Taylor. 2003. Protective effects of nicotine on ethanol-induced toxicity in cultured cerebellar granule cells. Neurotox. Res. 5:315-321.
266. Tjora, T., J. Hetland, L. E. Aaro, and S. Overland. 2011. Distal and proximal family predictors of adolescents' smoking initiation and development: a longitudinal latent curve model analysis. BMC Public Health 11:911.
267. Tobias, M., R. Templeton, and S. Collings. 2008. How much do mental disorders contribute to New Zealand's tobacco epidemic? Tob. Control 17:347-350.
268. van Tol, M. J., N. J. van der Wee, O. A. van den Heuvel, M. M. Nielen, L. R. Demenescu, A. Aleman, et al. 2010. Regional brain volume in depression and anxiety disorders. Arch. Gen. Psychiatry 67:1002-1011.
269. Trauth, J. A., F. J. Seidler, E. C. McCook, and T. A. Slotkin. 1999. Persistent c-fos induction by nicotine in developing rat brain regions: interaction with hypoxia. Pediatr. Res. 45:38-45.
270. Trauth, J. A., F. J. Seidler, and T. A. Slotkin. 2000. An animal model of adolescent nicotine exposure: effects on gene expression and macromolecular constituents in rat brain regions. Brain Res. 867:29-39.
271. Tuon, T., S. S. Valvassori, J. Lopes-Borges, G. R. Fries, L. A. Silva, F. Kapczinski, et al. 2010. Effects of moderate exercise on cigarette smoke exposure-induced hippocampal oxidative stress values and neurological behaviors in mice. Neurosci. Lett. 475:16-19.
272. Turner, C. A., S. M. Clinton, R. C. Thompson, S. J. Jr Watson, and H. Akil. 2011. Fibroblast growth factor-2 (FGF2) augmentation early in life alters hippocampal development and rescues the anxiety phenotype in vulnerable animals. Proc. Natl. Acad. Sci. USA 108:8021-8025.
273. Uddin, M., K. C. Koenen, A. E. Aiello, D. E. Wildman, R. de los Santos, and S. Galea. 2011. Epigenetic and inflammatory marker profiles associated with depression in a community-based epidemiologic sample. Psychol. Med. 41:997-1007.
274. Uysal, N., A. R. Sisman, A. Dayi, I. Aksu, F. Cetin, C. Gencoglu, et al. 2011. Maternal exercise decreases maternal deprivation induced anxiety of pups and correlates to increased prefrontal cortex BDNF and VEGF. Neurosci. Lett. 505:273-278.
275. Valko, M., D. Leibfritz, J. Moncol, M. T. Cronin, M. Mazur, and J. Telser. 2007. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39:44-84.
276. Villablanca, A. C., K. E. Pinkerton, and J. C. Rutledge. 2010. Maternal and neonatal exposure to environmental tobacco smoke targets pro-inflammatory genes in neonatal arteries. J. Cardiovasc. Transl. Res. 3:696-703.
277. Vizi, E. S., A. Fekete, R. Karoly, and A. Mike. 2010. Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. Br. J. Pharmacol. 160:785-809.
278. Wadee, A., R. Kuschke, S. Kometz, and M. Berk. 2001. Personality factors, stress and immunity. Stress Health 17:25-40.
279. Wager-Smith, K., and A. Markou. 2011. Depression: a repair response to stress-induced neuronal microdamage that can grade into a chronic neuroinflammatory condition? Neurosci. Biobehav. Rev. 35:742-764.
280. Westlye, L. T., A. Bjornebekk, H. Grydeland, A. M. Fjell, and K. B. Walhovd. 2011. Linking an anxiety-related personality trait to brain white matter microstructure: diffusion tensor imaging and harm avoidance. Arch. Gen. Psychiatry 68:369-377.
281. Yeom, M., I. Shim, H. J. Lee, and D. H. Hahm. 2005. Proteomic analysis of nicotine-associated protein expression in the striatum of repeated nicotine-treated rats. Biochem. Biophys. Res. Commun. 326:321-328.
282. Yildiz, D., N. Ercal, and D. W. Armstrong. 1998. Nicotine enantiomers and oxidative stress. Toxicology 130:155-165.
283. Yildiz, D., Y. S. Liu, N. Ercal, and D. W. Armstrong. 1999. Comparison of pure nicotine- and smokeless tobacco extract-induced toxicities and oxidative stress. Arch. Environ. Contam. Toxicol. 37:434-439.
284. Yu, H., and Z. Y. Chen. 2011. The role of BDNF in depression on the basis of its location in the neural circuitry. Acta Pharmacol. Sin. 32:3-11.
285. Zhang, X., E. A. Stein, and L. E. Hong. 2010a. Smoking and schizophrenia independently and additively reduce white matter integrity between striatum and frontal cortex. Biol. Psychiatry 68:674-677.
286. Zhang, J., X. Y. Huang, M. L. Ye, C. X. Luo, H. Y. Wu, Y. Hu, et al. 2010b. Neuronal nitric oxide synthase alteration accounts for the role of 5-HT1A receptor in modulating anxiety-related behaviors. J. Neurosci. 30:2433-2441.
287. Zhang, X., B. J. Salmeron, T. J. Ross, X. Geng, Y. Yang, and E. A. Stein. 2011a. Factors underlying prefrontal and insula structural alterations in smokers. Neuroimage 54:42-48.
288. Zhang, L., Y. Zhang, L. Li, Z. Li, W. Li, N. Ma, et al. 2011b. Different white matter abnormalities between the first-episode, treatment-naive patients with posttraumatic stress disorder and generalized anxiety disorder without comorbid conditions. J. Affect. Disord. 133:294-299.
289. Zvolensky, M., and A. Bernstein. 2005. Cigarette smoking and panic psychopathology. Curr. Dir. Psychol. Sci. 14:301-305.
290. Zvolensky, M. J., N. B. Schmidt, and B. T. McCreary. 2003. The impact of smoking on panic disorder: an initial investigation of a pathoplastic relationship. J. Anxiety Disord. 17:447-460.
291. Zvolensky, M. J., M. T. Feldner, E. W. Leen-Feldner, and A. C. McLeish. 2005. Smoking and panic attacks, panic disorder, and agoraphobia: a review of the empirical literature. Clin. Psychol. Rev. 25:761-789.