Nicotinic acetylcholine receptors as targets for antidepressants

Shytle, R D; Silver, A A; Lukas, R J; Newman, M B; Sheehan, D V; Sanberg, P R

doi:10.1038/sj.mp.4001035

Cited by 279Nicotinic Acetylcholine Receptors StudyTreatment of Major DepressionNeuroscience and Neuropharmacology Research

Nicotinic acetylcholine receptors as targets for antidepressants

Shytle, R D, Silver, A A, Lukas, R J, Newman, M B, Sheehan, D V, Sanberg, P R·2002·Molecular Psychiatry

DOI 10.1038/sj.mp.4001035

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Abstract

While the monoamine deficiency hypothesis of depression is still most commonly used to explain the actions of antidepressant drugs, a growing body of evidence has accumulated that is not adequately explained by the hypothesis. This article draws attention to contributions from another apparently common pharmacological property of antidepressant medications--the inhibition of nicotinic acetylcholine receptors (nAChR). Evidence is presented suggesting the hypercholinergic neurotransmission, which is associated with depressed mood states, may be mediated through excessive neuronal nicotinic receptor activation and that the therapeutic actions of many antidepressants may be, in part, mediated through inhibition of these receptors. In support of this hypothesis, preliminary evidence is presented suggesting that the potent, centrally acting nAChR antagonist, mecamylamine, which is devoid of monoamine reuptake inhibition, may reduce symptoms of depression and mood instability in patients with comorbid depression and bipolar disorder. If this hypothesis is supported by further preclinical and clinical research, nicotinic acetylcholine receptor antagonists may represent a novel class of therapeutic agents for treating mood disorders.

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Several classes of nicotinic agonists have antidepressant actions in human studies and animal models, but several nicotinic antagonists have potent antidepressant effects.
“several classes of nicotinic agonists have antidepressant actions in both human studies and animal models (Ferguson et al., 2000; Gatto et al., 2004) but several nicotinic antagonists have shown to have potent antidepressant effects (Ferguson et al., 2000; Shytle et al., 2002).”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Shytle et al., 2002
Many commonly used antidepressants can block nAChRs in in vitro and in vivo assays.
“a significant body of evidence is accumulating suggesting that many of the commonly used antidepressants can also block nAChRs in a number of in vitro and in vivo assays (see (Shytle et al., 2002) for a detailed review).”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Shytle et al., 2002
The agonist nicotine and the antagonist mecamylamine both exert antidepressant-like effects.
“Behavioral studies also show that the agonist nicotine and the antagonist mecamylamine both improve memory-related task performance in rodents and monkeys (Buccafusco and Jackson, 1991;Terry et al., 1999) and exert antidepressant-like effects (Semba et al., 1998;Tizabi et al., 1998;Shytle et al., 2002;Gatto et al., 2004).”
From Nicotinic receptor-mediated reduction in l-DOPA-induced dyskinesias may occur via desensitization (2010) · cites this paper as Shytle et al., 2002
Commonly used antidepressants can act as α4β2* nAChR antagonists in cell-based assays.
“commonly used antidepressants can also act as α4β2* nAChR antagonists in cell-based assays (Shytle et al., 2002; Slemmer et al., 2000)”
From Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states (2015) · cites this paper as Shytle et al., 2002
Further decreased ACh signaling, in addition to the small effect that SSRIs have on AChR activity via their weak nicotinic acetylcholine receptor antagonist properties, can significantly enhance the antidepressant effects of SSRIs.
“This is consistent with the notion that further decreased ACh signaling, in addition to the small effect that SSRIs have on AChR activity via their weak nicotinic acetylcholine receptor antagonist properties (Shytle et al, 2002), can significantly enhance the antidepressant effects of SSRIs.”
From Varenicline has antidepressant-like activity in the forced swim test and augments sertraline's effect (2009) · cites this paper as Shytle et al, 2002

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Minireview: Nicotinic Acetylcholine Receptors on Hippocampal Neurons: Distribution on the Neuronal Surface and Modulation of Receptor Activity
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A cholinergic antagonist, mecamylamine, blocks the phase-shifting effects of light on the circadian rhythm of locomotor activity in the golden hamster
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Inhibition of neuronal nicotinic acetylcholine receptors by imipramine and desipramine
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Nicotinic acetylcholine receptor antagonist effect of fluoxetine in rat hippocampal slices
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Activation and inhibition of rat neuronal nicotinic receptors by ABT‐418
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A cholinergic antagonist, mecamylamine, blocks light-induced Fos immunoreactivity in specific regions of the hamster suprachiasmatic nucleus
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The presence of corticotropin-releasing factor-like immunoreactive synaptic vesicles in axon terminals with nicotinic acetylcholine receptor-like immunoreactivity in the median eminence of the rat
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Comorbid bipolar disorder in Tourette’s syndrome responds to the nicotinic receptor antagonist mecamylamine (Inversine)
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Sexual diergism in rat hypothalamic-pituitary-adrenal axis responses to cholinergic stimulation and antagonism
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Inhibition of 22Na influx by tricyclic and tetracyclic antidepressants and binding of [3H]imipramine in bovine adrenal medullary cells.
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Functional Modulation of Human "Ganglionic-like" Neuronal Nicotinic Acetylcholine Receptors (nAChRs) by L-Type Calcium-Channel Antagonists
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Tricyclic antidepressants block cholinergic nicotinic receptors and ATP secretion in bovine chromaffin cells
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Histological and Behavioral Protection by (−)-Nicotine against Quinolinic Acid-Induced Neurodegeneration in the Hippocampus
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Interaction of impramine with the ionic channel of the acetylcholine receptor of motor endplate and electric organ
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Tobacco withdrawal signs and symptoms among women with and without a history of depression.
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Toward a better understanding of depression: New mechanistic considerations of antidepressant action provide a basis for development of delay-free drugs
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Pharmacological Challenge Strategies
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Hyperfrontality of Cerebral Blood Flow in Depressed Adolescents
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Major depressive disorder
Belmaker, R. H., & Agam, G. (2008) · New England Journal of Medicine · doi:10.1056/nejmra073096 · Cited by 2,166 · see citing works
A biosocial developmental model of borderline personality: Elaborating and extending linehan’s theory.
Crowell, S. E., Beauchaine, T. P., & Linehan, M. M. (2009) · Psychological Bulletin · doi:10.1037/a0015616 · Cited by 1,292 · see citing works
Pharmacology of nicotine: addiction, smoking-induced disease, and therapeutics
Benowitz, N. L. (2009) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.48.113006.094742 · Cited by 979 · see citing works
Brain nicotinic acetylcholine receptors: native subtypes and their relevance
Gotti, C., Zoli, M., & Clementi, F. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.07.004 · Cited by 882 · see citing works
It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood
PICCIOTTO, M., ADDY, N., MINEUR, Y., & BRUNZELL, D. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.12.005 · Cited by 451 · see citing works
Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents
Shirayama, Y., & Chaki, S. (2006) · Current Neuropharmacology · doi:10.2174/157015906778520773 · Cited by 225 · see citing works
The vigilance regulation model of affective disorders and ADHD
Hegerl, U., & Hensch, T. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.10.008 · Cited by 212 · see citing works
How cigarette smoking may increase the risk of anxiety symptoms and anxiety disorders: a critical review of biological pathways
Moylan, S., Jacka, F. N., Pasco, J. A., & Berk, M. (2013) · Brain and Behavior · doi:10.1002/brb3.137 · Cited by 186 · see citing works
Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states
Picciotto, M. R., Lewis, A. S., van Schalkwyk, G. I., & Mineur, Y. S. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.028 · Cited by 157 · see citing works
Subtypes of nicotinic acetylcholine receptors in nicotine reward, dependence, and withdrawal: evidence from genetically modified mice
Fowler, C. D., Arends, M. A., & Kenny, P. J. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32830c360e · Cited by 131 · see citing works
The nicotinic antagonist mecamylamine has antidepressant-like effects in wild-type but not β2- or α7-nicotinic acetylcholine receptor subunit knockout mice
Rabenstein, R. L., Caldarone, B. J., & Picciotto, M. R. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0568-z · Cited by 129 · see citing works
Nicotinic Antagonist Augmentation of Selective Serotonin Reuptake Inhibitor-Refractory Major Depressive Disorder: A Preliminary Study
George, T. P., Sacco, K. A., Vessicchio, J. C., Weinberger, A. H., & Shytle, R. D. (2008) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e318172b49e · Cited by 128 · see citing works
Self-citation
High-affinity nicotinic acetylcholine receptors are required for antidepressant effects of amitriptyline on behavior and hippocampal cell proliferation
Caldarone, B. J., Harrist, A., Cleary, M. A., Beech, R. D., King, S. L., & Picciotto, M. R. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.08.010 · Cited by 122 · see citing works
Persistent β <sub>2</sub> *-Nicotinic Acetylcholinergic Receptor Dysfunction in Major Depressive Disorder
Saricicek, A., Esterlis, I., Maloney, K. H., Mineur, Y. S., Ruf, B. M., Muralidharan, A., Chen, J. I., Cosgrove, K. P., Kerestes, R., Ghose, S., et al. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2012.11101546 · Cited by 118 · see citing works
Antidepressant-like effects of nicotinic acetylcholine receptor antagonists, but not agonists, in the mouse forced swim and mouse tail suspension tests
Andreasen, J., Olsen, G., Wiborg, O., & Redrobe, J. (2009) · Journal of Psychopharmacology · doi:10.1177/0269881108091587 · Cited by 101 · see citing works
Two Decades of Smoking Cessation Treatment Research on Smokers with Depression: 1990-2010
Weinberger, A. H., Mazure, C. M., Morlett, A., & McKee, S. A. (2013) · Nicotine & Tobacco Research · doi:10.1093/ntr/nts213 · Cited by 96 · see citing works
Mecamylamine - a nicotinic acetylcholine receptor antagonist with potential for the treatment of neuropsychiatric disorders
Bacher, I., Wu, B., Shytle, D. R., & George, T. P. (2009) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656560903329102 · Cited by 96 · see citing works
Striatal structure and function in mood disorders: a comprehensive review
Marchand, W. R., & Yurgelun‐Todd, D. (2010) · Bipolar Disorders · doi:10.1111/j.1399-5618.2010.00874.x · Cited by 91 · see citing works
Varenicline Augmentation in Depressed Smokers: An 8-Week, Open-Label Study
Philip, N. S., Carpenter, L. L., Tyrka, A. R., Whiteley, L. B., & Price, L. H. (2009) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.08m04441 · Cited by 86 · see citing works
Varenicline has antidepressant-like activity in the forced swim test and augments sertraline's effect
Rollema, H., Guanowsky, V., Mineur, Y. S., Shrikhande, A., Coe, J. W., Seymour, P. A., & Picciotto, M. R. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.01.002 · Cited by 87 · see citing works
Nicotinic receptor-mediated reduction in l-DOPA-induced dyskinesias may occur via desensitization
Bordia, T., Campos, C., McIntosh, J. M., & Quik, M. (2010) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.162396 · Cited by 82 · see citing works
Changes in the Cholinergic System between Bipolar Depression and Euthymia as Measured with [123I]5IA Single Photon Emission Computed Tomography
Hannestad, J. O., Cosgrove, K. P., DellaGioia, N. F., Perkins, E., Bois, F., Bhagwagar, Z., Seibyl, J. P., McClure-Begley, T. D., Picciotto, M. R., & Esterlis, I. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.04.004 · Cited by 63 · see citing works
Biological basis for the co-morbidity between smoking and mood disorders
Mineur, Y. S., & Picciotto, M. R. (2009) · Journal of Dual Diagnosis · doi:10.1080/15504260902869964 · Cited by 51 · see citing works
Dissociation between duration of action in the forced swim test in mice and nicotinic acetylcholine receptor occupancy with sazetidine, varenicline, and 5-I-A85380
Caldarone, B. J., Wang, D., Paterson, N. E., Manzano, M., Fedolak, A., Cavino, K., Kwan, M., Hanania, T., Chellappan, S. K., Kozikowski, A. P., et al. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2271-y · Cited by 47 · see citing works
Nicotinic cholinergic antagonists: A novel approach for the treatment of autism
Lippiello, P. M. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2005.11.015 · Cited by 43 · see citing works
Efficacy and tolerability of flexibly-dosed adjunct TC-5214 (dexmecamylamine) in patients with major depressive disorder and inadequate response to prior antidepressant
Vieta, E., Thase, M. E., Naber, D., D’Souza, B., Rancans, E., Lepola, U., Olausson, B., Szamosi, J., Wilson, E., Hosford, D., et al. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.12.008 · Cited by 43 · see citing works
Ventral tegmental area cholinergic mechanisms mediate behavioral responses in the forced swim test
Addy, N. A., Nunes, E. J., & Wickham, R. J. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.002 · Cited by 42 · see citing works
Chemistry and Pharmacology of Nicotinic Ligands Based on 6‐[5‐(Azetidin‐2‐ylmethoxy)pyridin‐3‐yl]hex‐5‐yn‐1‐ol (AMOP‐H‐OH) for Possible Use in Depression
Kozikowski, A. P., Eaton, J. B., Bajjuri, K. M., Chellappan, S. K., Chen, Y., Karadi, S., He, R., Caldarone, B., Manzano, M., Yuen, P., et al. (2009) · ChemMedChem · doi:10.1002/cmdc.200900079 · Cited by 36 · see citing works
Self-citation
The β4 nicotinic receptor subunit modulates the chronic antidepressant effect mediated by bupropion
Radhakrishnan, R., Santamaría, A., Escobar, L., & Arias, H. R. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.08.009 · Cited by 12 · see citing works

Nicotinic Receptor Systems and Neurobehavioral Function in Zebrafish
Levin, E. D. (2010) · Neuromethods · doi:10.1007/978-1-60761-922-2_4 · Cited by 1 · see citing works
Differential Effect of Nicotinic Agonists on the [3H]Norepinephrine Release from Rat Hippocampal Slices
Kiss, J., Windisch, K., Oliveira, K. D., Hennings, E. C. P., Mike, Á., & Szász, B. K. (2001) · Neurochemical Research · doi:10.1023/a:1012384517784 · Cited by 13 · see citing works
Nicotine-improved aspects of psychomotor performance and cognitive ability: Fact or fiction
Hindmarch, I. (1995) · Pharmacological Research · doi:10.1016/1043-6618(95)86341-9
Nicotinic-catecholaminergic interactions in rat brain: evidence for cholinergic nicotinic and muscarinic interactions with hypothalamic epinephrine.
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Authors: Shytle, R. D., Silver, A. A., Lukas, R. J., Newman, M. B., Sheehan, D. V., & Sanberg, P. R.
Affiliations: University of South Florida (US)
Barrow Neurological Institute (US)
Corresponding author: Shytle, R D
ORCID: Shytle, R D
Sheehan, D V
Sanberg, P R
Venue: Molecular Psychiatry
Publisher: Springer Science and Business Media LLC
Published: 2002-07-01
Volume: 7
Issue: 6
Pages: 525-535
ISSN: 1359-4184 (ISSN-L)
1476-5578
DOI: 10.1038/sj.mp.4001035
OpenAlex: W2077857371
Cited by: 279
References: 143
Citations by year: 2026: 3 · 2025: 5 · 2024: 5 · 2023: 5 · 2022: 11 · 2021: 7 · 2020: 7 · 2019: 6 · 2018: 9 · 2017: 9 · 2016: 9 · 2015: 13 · 2014: 12 · 2013: 18 · 2012: 13
FWCI: 0.55
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Molecular Psychiatry (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: nicotinic acetylcholine receptors, antidepressants, depression, mecamylamine, bipolar disorder, nicotinic antagonists, mood instability, mood disorders
MeSH terms: Antidepressive Agents, Brain, Depression, Depressive Disorder, Humans, Models, Neurological, Nicotine, Receptors, Nicotinic, Drug Design, Nicotinic Antagonists

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Nicotinic acetylcholine receptors as targets for antidepressants

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