GABAA-benzodiazepine receptor availability in smokers and nonsmokers: Relationship to subsyndromal anxiety and depression

Synapse

Volumn 63, Issue 12, 2009, Pages 1089-1099

  Esterlis, Irina ^a,c   Cosgrove, Kelly P ^a   Batis, Jeffery C ^a   Bois, Frederic ^a   Kloczynski, Tracy A ^a   Stiklus, Stephanie M ^a   Perry, Edward ^a   Tamagnan, Gilles D ^a,b   Seibyl, John P ^a,b   Makuch, Robert ^a   Krishnan Sarin, Suchitra ^a   O'Malley, Stephanie ^a   Staley, Julie K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE FOR NEURODEGENERATIVE DISORDERS   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

Anxiety; Brain; Depression; GABAA benzodiazepine receptor; SPECT; Tobacco smoke

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BENZODIAZEPINE RECEPTOR; COTININE; DRUG DERIVATIVE; FLUMAZENIL; IOMAZENIL;

ADULT; ANXIETY; ARTICLE; BLOOD LEVEL; CEREBELLUM; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; FEMALE; FRONTAL CORTEX; HUMAN; MALE; NOCICEPTION; OCCIPITAL CORTEX; PAIN; PAIN THRESHOLD; PARIETAL LOBE; PRIORITY JOURNAL; RATING SCALE; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SMOKING; TEMPORAL CORTEX; TOBACCO; URINE LEVEL; BRAIN; BRAIN MAPPING; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN ASSESSMENT; PSYCHOLOGICAL RATING SCALE; QUESTIONNAIRE; SCINTISCANNING;

ADULT; ANXIETY; BRAIN; BRAIN MAPPING; DEPRESSION; FEMALE; FLUMAZENIL; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; PAIN; PAIN MEASUREMENT; PSYCHIATRIC STATUS RATING SCALES; QUESTIONNAIRES; RECEPTORS, GABA-A; SMOKING; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 70349871322     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20688     Document Type: Article

References (68)

1. Abi-Dargham A, Laruelle M, Seibyl J, Rattner Z, Baldwin R, Zoghbi S, Zea-Ponce Y, Bremner J, Hyde T, Charney D, Hoffer P, Innis R. 1994. SPECT measurement of benzodiazepine receptors in human brain with [123I]Iomazenil: Kinetic and equilibrium paradigms. J Nucl Med 35:228-238. (Pubitemid 24048309)
2. Abi-Dargham A, Gandelman M, Zoghbi S, Laruelle M, Baldwin R, Randall P, Zea-Ponce Y, Charney D, Hoffer P, Innis R. 1995. Reproducibility of SPECT measurement of benzodiazepine receptors in human brain with iodine-123- iomazenil. J Nucl Med 36:167-175.
3. Anda R, Williamson D, Escobedo L, Mast E, Giovino G, Remington P. 1990. Depression and the dynamics of smoking: A national perspective. JAMA 264:1541-1545. (Pubitemid 20303383)
4. Borrelli B, Marcus B, Clark M, Bock B, King T, Roberts M. 1999. History of dperession and subsyndromal depression in women smokers. Addict Behav 24:781-794.
5. Brambilla P, Perez J, Barale F, Schettini G, Soares J. 2003. GABAergic dysfunction in mood disorders. Mol Psychiatry 8:721-737.
6. Brioni J, O'Neill A, Kim D, Buckley M, Decker M, Arneric SP. 1994. Anxiolytic-like effects of the novelcholinergic channel activator ABT-418. J Pharmacol Exp Ther 271:353-361. (Pubitemid 24333149)
7. Brown R, Kahler C, Zvolensky M, Lejuez C, Ramsey S. 2001. Anxiety sensitivity. Relationship to negative affect smoking and smoking cessation in smokers with past major depressive disorder. Addict Behav 26:887-899.
8. A-benzodiazepine binding sites in insular cortex of individuals with panic disorder. Arch Gen Psychiatry 64:793-800.
9. Catley D, Harris K, Okuyemi K, Mayo M, Pankey E, Ahluwalia J. 2005. The influence of depressive symptoms on smoking cessation among African Americans in a randomized trial of bupropion. Nicotine Tobacco Res 7:859-870. (Pubitemid 43101704)
10. Cheeta S, Irvine E, Kenny P, File S. 2001. The dorsal raphe nucleus is a crucial structure mediating nicotine's anxiolytic effects and the development of tolerance and withdrawal responses. Psychopharmacology 155:78-85. (Pubitemid 32295772)
11. Cooney J, Stevens T, Cooney N. 1998. Comorbidity of nicotine dependence with psychiatric and substance-use disorders. In: Kranzler H, Rounsaville B, editors. Dual diagnosis and treatment. New York: Marcel Dekker.
12. Costall B, Kelly M, Naylor R, Onaivi E. 1989. The actions of nicotine and cocaine in a mouse model of anxiety. Pharmacol Biochem Behav 33:197-203. (Pubitemid 19202627)
13. Covey L, Glassman A, Stetner F. 1990. Depression and depressive symptoms in smoking cessation. Compr Psychiatry 31:350-354. (Pubitemid 20333849)
14. Domino EF, Minoshima S, Guthrie SK, Ohl L, Ni L, Koeppe RA, Cross DJ, Zubieta J-K. 2000. Effects of nicotine on regional cerebral glucose metabolism in awake resting tobacco smokers. Neuroscience 101:277-282. (Pubitemid 30829423)
15. Epperson C, Czarkowski K, Gueorguieva R, Jatlow P, Sanacora G, Rothman D, Krystal J, Mason G. 2005. Sex, GABA, and nicotine: The impact of smoking on cortical GABA levels across the menstrual cycle as measured with proton magnetic resonance. Biological Psychiatry 57:44-48. (Pubitemid 39647590)
16. Erhardt S, Schwieler L, Engberg G. 2002. Excitatory and inhibitory responses of dopamine neurons in the ventral tegmental area to nicotine. Synapse 43:227-237. (Pubitemid 34118259)
17. Fedele E, Varnier G, Ansaldo MA, Raiteri M. 1998. Nicotine administration stimulates the in vivo N-methyl-D-aspartate receptor/nitric oxide/cyclic GMP pathway in rat hippocampus through glutamate release. Br J Pharmacol 125:1042-1048. (Pubitemid 28495366)
18. Ghatan PH, Ingvar M, Eriksson L, Stone-Elander S, Serrander M, Ekberg K, Wahren J. 1998. Cerebral effects of nicotine during cognition in smokers and non-smokers. Psychopharmacology 136: 179-189. (Pubitemid 28137958)
19. Gilbert D. 1996. Depression, smoking, and nicotine: Toward a bio-informational situation by trait model. Drug Dev Res 38:267-277. (Pubitemid 27034044)
20. Gilbert D, McClernon F, Rabinovich N, Plath L, Masson C. 2002. Mood disturbance fails to resolve across 31 days of cigarette abstinence in women. J Consult Clin Psychol 70:142-152. (Pubitemid 34150981)
21. Glassman A. 1993. Cigarette smoking: Implications for psychiatric illness. Am J Psychiatry 150:546-553. (Pubitemid 23109920)
22. Hatsukami D, Dahlgren L, Zimmerman R, Hughes J. 1988. Symptoms of tobacco withdrawal from total cigarette: Cessation vs partial cigarette reduction. Psychopharmacology 94:242-247. (Pubitemid 18040703)
23. Heatherton T, Kozlowski L, Frecker R, Fagerstrom K. 1991. The Fagerstrom test for nicotine dependence: A revision of the Fagerstrom tolerance questionnaire. Br J Addict 86:1119-1127.
24. Hughes J. 1991. Distinguishing withdrawal relief and direct effects of smoking. Psychopharmacology 104:409-410.
25. Innis R, Cunningham V, Delforge J, Fujita M, Gjedde A, Gunn R, Holden J, Houle S, Huang SC, Ichise M, Iida H, Ito H, Kimura Y, Koeppe R, Knudsen G, Knuuti J, Lammertsma A, Laruelle M, Logan J, Maguire R, Mintun M, Morris E, Parsey R, Price J, Slifstein M, Sossi V, Suhara T, Votaw J, Wong D, Carson R. 2007. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab 27:1533-1539. (Pubitemid 47301451)
26. Jarvik M, Caskey N, Rose J, Herskovic J, Sadeghpour M. 1989. Anxiolytic effects of smoking associated with four stressors. Addict Behav 14:379-386. (Pubitemid 19208698)
27. Kaschka W, Feistel H, Ebert D, Joraschky P, Marienhagen J. 1992. Cerebral GABAA/benzodiazepine receptor distribution in anxiety disorders. Clin Neuropharm 15(Suppl):27B.
28. Kaschka W, Feistel H, Ebert D. 1995. Reduced benzodiazepine receptor binding in panic disorders measured by iomazenil SPECT. J Psychiatry Res 29:427-434.
29. Katsura M, Ohkuma S, Chen D, Tsujimura A, Kuriyama K. 1994. Nicotine increases diazepam binding inhibitor (DBI) mRNA in primary cultured neurons. Neurosci Lett 168:1-4. (Pubitemid 24097308)
30. Kessler R. 2003. Epidemiology of women and depression. J Affect Disord 74:5-13.
31. Kessler R. 2004. The epidemiology of dual diagnosis. Biol Psychiatry 456:730-737.
32. 123I]iomazenil SPECT. Biol Psychiatry 54:792-799.
33. Lazarus R. 1991. Emotion and adaptation. London: Oxford University Press.
34. Levy R, Proudfit H. 1977. The analgesic action of baclofen [β-(4- chlorophenyl)-γ-amynobutiryc acid]. J Pharmacol Exp Therapy 202:437-445. (Pubitemid 8168207)
35. Lydiard R. 2003. The role of GABA in anxiety disorders. J Clin Psychol 64:21-27.
36. Magata Y, Kitano H, Shiozaki T, Iida Y, Nishizawa S, Saji H, Konishi J. 2000. Effect of chronic (-) nicotine treatment on rat cerebral benzodiazepine receptors. Nucl Med Biol 27:57-60. (Pubitemid 30099615)
37. Malizia A, Coupland N, Nutt D. 1995. Benzodiazepine receptor function in anxiety disorders. In: Biggio G, Sanna E, Serra M, Costa E, editors. GABAA receptors and anxiety: From neurobiology to treatment. New York: Raven. p 115-133.
38. Mansvelder HD, Keath JR, McGehee DS. 2002. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33:905-919.
39. Merikangas K, Mehta R, Molnar B, Walters E, Swendsen J, Aguilar- Gaziola S, Bijl R, Borges G, Caraveo-Anduaga J, De Wit D, Kolody B, Vega W, Wittchen H, Kessler R. 1998. Comorbidity of substance use disorders with mood and anxiety disorders: Results of the international consortium in psychiatric epidemiology. Addict Behav 23:893-907. (Pubitemid 28443200)
40. Meshul CK, Kamel D, Moore C, Kay TS, Krentz L. 2002. Nicotine alters striatal glutamate function and decreases the apomorphineinduced contralateral rotations in 6-OHDA-lesioned rats. Exp Neurol 175:257-274. (Pubitemid 34507927)
41. Nemeroff C. 2003. The role of GABA in the pathophysiology and treatment of anxiety disorders. Psychopharmacol Bull 37:133-146.
42. Nutt D, Glue P, Lawson C, Wilson S. 1990. Flumazenil provocation of panic attacks. Arch Gen Psychiatry 47:917-925.
43. Perkins K. 1995. Individual variability in response to nicotine. Behav Genet 25:119-132.
44. Petty F. 1995. GABA and mood disorders: A brief review and hypothesis. J Affect Disord 34:275-281.
45. Picciotto M, Addy N, Mineur Y, Brunzell D. 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.
46. Pickering C, Bergenheim V, Scioth H, Ericson M. 2008. Sensitization to nicotine significantly descreases expression of GABA transporter GAT-1 in the medial prefrontal cortex. Prog Neuro- Psychopharmacol Biol Psychiatry 32:1521-1526.
47. Poindexter E, Carpenter R. 1962. The isolation of harmane and norharmane from tobacco and cigarette smoke. Phytochemistry 1:215-222.
48. Pomerleau O, Pomerleau C, Mehringer A, Snedecor S, Ninwoski R, Sen A. 2004. Nicotine dependence, depression, and gender: Characterizing phenotypes based on withdrawal discomfort, response to smoking, and ability to abstain. Nicotine Tobacco Res 7:91-102. (Pubitemid 40613166)
49. Pomerleau O, Turk D, Fertig J. 1984. The effects of cigarette smoking on pain and anxiety. Addict Behav 9:256-271. (Pubitemid 14062005)
50. Porcu P, Sogliano C, Cinus M, Purdy R, Biggio G, Concas A. 2003. Nicotine induced changes in cerebrocortical neuroactive steroids and plasma corticosterone concentrations in the rat. Pharmacol Biochem Behav 74:683-690. (Pubitemid 36126547)
51. Radloff L. 1977. The CES-D scale: A self-report depression scale for research in the general population. Appl Psychol Meas 1:385-401.
52. Rajeevan N, Zubal I, Rambsy S, Zoghbi S, Seibyl J, Innis R. 1998. Significance of nonuniform attenuation correction in quantitative brain SPECT imaging. J Nucl Med 39:1719-1726. (Pubitemid 28473520)
53. Reid MS, Fox L, Ho LB, Berger SP. 2000. Nicotine stimulation of extracellular glutamate levels in the nucleus accumbens: Neuropharmacological characterization. Synapse 35:129-136. (Pubitemid 30036189)
54. Rommelspacher H, Nanz C, Borbe H, Fehske K, Müller W, Wollert U. 1981. Benzodiazepine antagonism by harmane and other β-carbolines in vitro and in vivo. Eur J Pharmacol 70:409-416. (Pubitemid 11149332)
55. Sanacora G, Gueorguieva R, Epperson C, Wu Y-T, Appel M, Rothman D, Krystal J. 2004. Subtype-specific alterations of GABA and glutamate in major depression. Arch Gen Psychiatry 6C:705-713.
56. Schlegel S, Steinert H, Bockisch A, Hahn K, Schloesser R, Benkert O. 1994. Decreased benzodiazepine receptor binding in panic disorder measured by iomazenil-SPECT: A preliminary report. Eur Arch Psychiatry Clin Neurosci 244:49-51. (Pubitemid 24189935)
57. Spielberger C, Corsuch R, editors. 1983. Manual for state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press.
58. Staley J, Dyck Cv, Weinzimmer D, Brenner E, Baldwin R, Tamagnan G, Riccardi P, Mitsis E, Seibyl J. 2005. Iodine-123-5-IA- 85380 SPECT measurement of nicotinic acetylcholine receptors in human brain by the constant infusion paradigm: Feasibility and reproducibility. J Nucl Med 46:1466-1472. (Pubitemid 46173258)
59. Staley J, Krishnan-Sarin S, Cosgrove K, Krantzler E, Frohlich E, Perry E, Dubin J, Estok K, Brenner E, Baldwin R, Tamagnan G, Seibyl J, Jatlow P, Picciotto M, London E, O'Malley S, Dyck Cv. 2006. Human tobacco smokers in early abstinence have higher levels of β2-nicotinic acetylcholine receptors than nonsmokers. J Neurosci 26:8707-8714.
60. Tiffany S, Drobes D. 1991. The development and initial validation of a questionnaire on smoking urges. Br J Addict 86:1467-1476.
61. Tiihonen J, Kuikka J, Rasanen P, Lepola U, Koponen H, Liuska A, Lehmusvaara A, Vainio P, Kononen M, Bergstrom K, Yu M, Kinnunen I, Akerman K, Karhu J. 1997. Cerebral benzodiazepine receptor binding and distribution in generalized anxiety disorder: A fractal analysis. Mol Psychiatry 2:463-471. (Pubitemid 27482948)
62. Uman L, Stewart S, Watt M, Johnston A. 2006. Differences in high and low anxiety sensitivity women's responses to a laboratory-based cold pressor task. Cog Beh Therapy 35:189-197. (Pubitemid 46002443)
63. Vaiva G, Thomas P, Ducrocq F, Fontaine M, Boss V, Devos P, Rascle C, Cottencin O, Brunet A, Laffargue P, Goudemand M. 2004. Low posttrauma GABA plasma levels as a predictive factor in the development of acute posttraumatic stress disorder. Biol Psychiatry 55:250-254. (Pubitemid 38117160)
64. Vaught J, Pelley K, Costa L, Settler P, Enna S. 1985. A comparison of the antinociceptive responses to the GABA receptor antagonists THIP and baclofen. Neuropharmacology 24:211-216. (Pubitemid 15051588)
65. Walsh NE, Shoenfeld L, Ramamurthy S, Hoffman J. 1989. Normative model for cold pressor test. Am J Phys Med Rehabil 68:6-11. (Pubitemid 19080269)
66. Zarrindast M, Solati J, Oryan S, Parivar K. 2008. Effect of intra-amygdala injection of nicotine and GABA receptor agents on anxiety-like behaviour in rats. Pharmacology 82:276-284.
67. Zoen S, Enna S. 1985. GABA uptake inhibitors produce greater antinociceptive response in the mouse tail immersion assay than other types of GABAergic drugs. Life Sci 37:1901-1912. (Pubitemid 16213544)
68. 123I]iomazenil in human and nonhuman primates. Nucl Med Biol-Int J Rad Appl B 19: 881-888.