Dopamine transporter genotype modulation of neural responses to smoking cues: Confirmation in a new cohort

Addiction Biology

Volumn 16, Issue 2, 2011, Pages 308-322

  Franklin, Teresa R ^a   Wang, Ze ^a   Li, Yin ^a   Suh, Jesse J ^a   Goldman, Marina ^a   Lohoff, Falk W ^a   Cruz, Jeffrey ^a   Hazan, Rebecca ^a   Jens, Will ^a   Detre, John A ^a   Berrettini, Wade ^a   O'Brien, Charles P ^a   Childress, Anna Rose ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Addiction; dopamine transporter; genetic variability; neuroimaging; relapse vulnerability; smoking cues

Indexed keywords

DOPAMINE TRANSPORTER; PROTEIN SLC6A3; UNCLASSIFIED DRUG;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN PERFUSION; CONTROLLED STUDY; CORPUS STRIATUM; DIAGNOSIS, MEASUREMENT AND ANALYSIS; FAGERSTROM TEST FOR NICOTINE DEPENDENCE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; INSULA; MALE; MIDDLE TEMPORAL GYRUS; NERVE CELL; NERVE POTENTIAL; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; RATING SCALE; SHIFFMAN JARVIK WITHDRAWAL SCALE; SMOKING; SUPERIOR FRONTAL GYRUS; WITHDRAWAL SYNDROME;

ADOLESCENT; ADULT; ALLELES; AMYGDALA; BASAL GANGLIA; BRAIN MAPPING; CEREBRAL CORTEX; COHORT STUDIES; CUES; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; FEMALE; FRONTAL LOBE; GENOTYPE; HETEROZYGOTE DETECTION; HOMOZYGOTE; HUMANS; MALE; MIDDLE AGED; MOTIVATION; PARIETAL LOBE; POLYMORPHISM, GENETIC; PREFRONTAL CORTEX; SMOKING; SMOKING CESSATION; TOBACCO USE DISORDER; YOUNG ADULT;

EID: 79952506841     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2010.00277.x     Document Type: Article

References (82)

1. Anon, (2000) Bupropion to aid smoking cessation. Drug Ther Bull 38: 73-75.
2. Aguirre GK, Detre JA, Wang J, (2005) Perfusion fMRI for functional neuroimaging. Int Rev Neurobiol 66: 213-236. (Pubitemid 43588593)
3. American Lung Association (2008) Helping Smokers Quit: State Cessation Coverage 2008, 1-24. Available from.
4. Baker TB, Morse E, Sherman JE, (1986) The motivation to use drugs: a psychobiological analysis of urges. Nebr Symp Motiv 34: 257-323.
5. Benowitz NL, (2009) Pharmacology of nicotine: addiction, smoking-induced disease, and therapeutics. Annu Rev Pharmacol Toxicol 49: 57-71.
6. Biberman R, Neumann R, Katzir I, Gerber Y, (2003) A randomized controlled trial of oral selegiline plus nicotine skin patch compared with placebo plus nicotine skin patch for smoking cessation. Addiction 98: 1403-1407. (Pubitemid 37297247)
7. Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, Bota RG, Ho ML, Saxena S, Baxter LR Jr, Madsen D, Jarvik ME, (2002) Brain metabolic changes during cigarette craving. Arch Gen Psychiatry 59: 1162-1172. (Pubitemid 35424027)
8. Brody AL, Mandelkern MA, Olmstead RE, Scheibal D, Hahn E, Shiraga S, Zamora-Paja E, Farahi J, Saxena S, London ED, McCracken JT, (2006) Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. Arch Gen Psychiatry 63: 808-816.
9. Caggiula AR, Donny EC, White AR, Chaudhri N, Booth S, Gharib MA, Hoffman A, Perkins KA, Sved AF, (2001) Cue dependency of nicotine self-administration and smoking. Pharmacol Biochem Behav 70: 515-530. (Pubitemid 34131646)
10. Cardinal RN, Parkinson JA, Hall J, Everitt BJ, (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26: 321-352. (Pubitemid 34555410)
11. Childress AR, Ehrman RN, Wang Z, Li Y, Sciortino N, Hakun J, Jens W, Suh J, Listerud J, Marquez K, Franklin T, Langleben D, Detre J, O'Brien CP, (2008) Prelude to passion: limbic activation by 'unseen' drug and sexual cues. Plos ONE 3: e1506.
12. Coe JW, Brooks PR, Vetelino MG, Wirtz MC, Arnold EP, Huang J, Sands SB, Davis TI, Lebel LA, Fox CB, Shrikhande A, Heym JH, Schaeffer E, Rollema H, Lu Y, Mansbach RS, Chambers LK, Rovetti CC, Schulz DW, Tingley FD 3rd, O'Neill BT, (2005) Varenicline: an alpha4beta2 nicotinic receptor partial agonist for smoking cessation. J Med Chem 48: 3474-3477. (Pubitemid 40664098)
13. Craig AD, (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59-70.
14. Dagher A, Tannenbaum B, Hayashi T, Pruessner JC, McBride D, (2009) An acute psychosocial stress enhances the neural response to smoking cues. Brain Res 1293: 40-48.
15. David SP, Munafo MR, Johansen-Berg H, Smith SM, Rogers RD, Matthews PM, Walton RT, (2005) Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study. Biol Psychiatry 58: 488-494. (Pubitemid 41393611)
16. Detre JA, Wang J, (2002) Technical aspects and utility of fMRI using BOLD and ASL. Clin Neurophysiol 113: 621-634. (Pubitemid 34439266)
17. Di Chiara G, (2000) Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 393: 295-314. (Pubitemid 30193428)
18. Di Chiara G, Tanda G, Bassareo V, Pontieri F, Acquas E, Fenu S, Cadoni C, Carboni E, (1999) Drug addiction as a disorder of associative learning. Role of nucleus accumbens shell/extended amygdala dopamine. Ann NY Acad Sci 877: 461-485. (Pubitemid 29351873)
19. Dijkstra A, Tromp D, (2002) Is the FTND a measure of physical as well as psychological tobacco dependence? J Subst Abuse Treat 23: 367-374. (Pubitemid 35477816)
20. Droungas A, Ehrman RN, Childress AR, O'Brien CP, (1995) Effect of smoking cues and cigarette availability on craving and smoking behavior. Addict Behav 20: 657-673.
21. Drummond DC, (2000) What does cue-reactivity have to offer clinical research? Addiction 95 (Suppl. 2): S129-S144.
22. Due DL, Huettel SA, Hall WG, Rubin DC, (2002) Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. Am J Psychiatry 159: 954-960. (Pubitemid 34586940)
23. Duvernoy HM, (1999) The Human Brain: Surface, Three-Dimensional Sectional Anatomy with Magnetic Resonance Imaging and Blood Supply, 2nd edn. New York: Springer-Verlag Wien.
24. Fagerstrom KO, Schneider NG, (1989) Measuring nicotine dependence: a review of the Fagerstrom Tolerance Questionnaire. J Behav Med 12: 159-182. (Pubitemid 19191503)
25. Floyd TF, Ratcliffe SJ, Wang J, Resch B, Detre JA, (2003) Precision of the CASL-perfusion MRI technique for the measurement of cerebral blood flow in whole brain and vascular territories. J Magn Reson Imaging 18: 649-655. (Pubitemid 37467265)
26. Franklin TR, Druhan JP, (2000) Involvement of the nucleus accumbens and medial prefrontal cortex in the expression of conditioned hyperactivity to a cocaine-associated environment in rats. Neuropsychopharmacology 23: 633-644.
27. Franklin TR, Ehrman R, Lynch KG, Harper D, Sciortino N, O'Brien CP, Childress AR, (2008) Menstrual cycle phase at quit date predicts smoking status in an NRT treatment trial: a retrospective analysis. J Womens Health (Larchmt) 17: 287-292. (Pubitemid 351631249)
28. Franklin TR, Lohoff FW, Wang Z, Sciortino N, Harper D, Li Y, Jens W, Cruz J, Kampman K, Ehrman R, Berrettini W, Detre JA, O'Brien CP, Childress AR, (2009) DAT genotype modulates brain and behavioral responses elicited by cigarette cues. Neuropsychopharmacology 34: 717-728.
29. Franklin TR, Napier K, Ehrman R, Gariti P, O'Brien CP, Childress AR, (2004) Retrospective study: influence of menstrual cycle on cue-induced cigarette craving. Nicotine Tob Res 6: 171-175. (Pubitemid 38372486)
30. Franklin TR, Wang Z, Wang J, Sciortino N, Harper D, Li Y, Ehrman R, Kampman K, O'Brien CP, Detre JA, Childress AR, (2007) Limbic activation to cigarette smoking cues independent of nicotine withdrawal: a perfusion fMRI study. Neuropsychopharmacology 32: 2301-2309. (Pubitemid 47587682)
31. Fuke S, Suo S, Takahashi N, Koike H, Sasagawa N, Ishiura S, (2001) The VNTR polymorphism of the human dopamine transporter (DAT1) gene affects gene expression. Pharmacogenomics J 1: 152-156. (Pubitemid 33757602)
32. Heimer L, (2003) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 160: 1726-1739. (Pubitemid 41103306)
33. Heinz A, Goldman D, Jones DW, Palmour R, Hommer D, Gorey JG, Lee KS, Linnoila M, Weinberger DR, (2000) Genotype influences in vivo dopamine transporter availability in human striatum. Neuropsychopharmacology 22: 133-139. (Pubitemid 30016015)
34. Heinz A, Smolka MN, (2006) The effects of catechol O-methyltransferase genotype on brain activation elicited by affective stimuli and cognitive tasks. Rev Neurosci 17: 359-367. (Pubitemid 44077517)
35. Ho MK, Tyndale RF, (2007) Overview of the pharmacogenomics of cigarette smoking. Pharmacogenomics J 7: 81-98. (Pubitemid 46577845)
36. Hughes JR, (2007) Effects of abstinence from tobacco: valid symptoms and time course. Nicotine Tob Res 9: 315-327. (Pubitemid 46404264)
37. Hughes JR, Shiffman S, Callas P, Zhang J, (2003) A meta-analysis of the efficacy of over-the-counter nicotine replacement. Tob Control 12: 21-27. (Pubitemid 39456686)
38. Hutchison KE, LaChance H, Niaura R, Bryan A, Smolen A, (2002) The DRD4 VNTR polymorphism influences reactivity to smoking cues. J Abnorm Psychol 111: 134-143. (Pubitemid 34154877)
39. Jorenby DE, Hays JT, Rigotti NA, Azoulay S, Watsky EJ, Williams KE, Billing CB, Gong J, Reeves KR, (2006) Efficacy of varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, vs placebo or sustained-release bupropion for smoking cessation: a randomized controlled trial. JAMA 296: 56-63.
40. Kozlowski LT, Porter CQ, Orleans CT, Pope MA, Heatherton T, (1994) Predicting smoking cessation with self-reported measures of nicotine dependence: FTQ, FTND, and HSI. Drug Alcohol Depend 34: 211-216.
41. Kringelbach ML, (2005) The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 6: 691-702. (Pubitemid 43160318)
42. Lahiri DK, Nurnberger JI Jr, (1991) A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Res 19: 5444.
43. Lancaster T, Stead LF, (2000) Mecamylamine (a nicotine antagonist) for smoking cessation. Cochrane Database Syst Rev: CD001009.
44. Langleben DD, Ruparel K, Elman I, Busch-Winokur S, Pratiwadi R, Loughead J, O'Brien CP, Childress AR, (2008) Acute effect of methadone maintenance dose on brain FMRI response to heroin-related cues. Am J Psychiatry 165: 390-394. (Pubitemid 351704496)
45. Le Foll B, Goldberg SR, (2005) Control of the reinforcing effects of nicotine by associated environmental stimuli in animals and humans. Trends Pharmacol Sci 26: 287-293. (Pubitemid 40733521)
46. Liu X, Powell DK, Wang H, Gold BT, Corbly CR, Joseph JE, (2007) Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J Neurosci 27: 4587-4597. (Pubitemid 46663580)
47. McBride D, Barrett SP, Kelly JT, Aw A, Dagher A, (2006) Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study. Neuropsychopharmacology 31: 2728-2738. (Pubitemid 44764169)
48. McClernon FJ, Hiott FB, Huettel SA, Rose JE, (2005) Abstinence-induced changes in self-report craving correlate with event-related FMRI responses to smoking cues. Neuropsychopharmacology 30: 1940-1947. (Pubitemid 41486419)
49. McClernon FJ, Hiott FB, Liu J, Salley AN, Behm FM, Rose JE, (2007a) Selectively reduced responses to smoking cues in amygdala following extinction-based smoking cessation: results of a preliminary functional magnetic resonance imaging study. Addict Biol 12: 503-512. (Pubitemid 47196350)
50. McClernon FJ, Hutchison KE, Rose JE, Kozink RV, (2007b) DRD4 VNTR polymorphism is associated with transient fMRI-BOLD responses to smoking cues. Psychopharmacology (Berl) 194: 433-441. (Pubitemid 47492991)
51. McClernon FJ, Kozink RV, Rose JE, (2008) Individual differences in nicotine dependence, withdrawal symptoms, and sex predict transient fMRI-BOLD responses to smoking cues. Neuropsychopharmacology 33: 2148-2157. (Pubitemid 351992088)
52. Mai JK, Voss T, Paxinos G, (2008) Atlas of the Human Brain, 3rd edn. New York: Elsevier Academic Press.
53. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN, (2007) Wandering minds: the default network and stimulus-independent thought. Science 315: 393-395. (Pubitemid 46175523)
54. Mill J, Asherson P, Browes C, D'Souza U, Craig I, (2002) Expression of the dopamine transporter gene is regulated by the 3â UTR VNTR: evidence from brain and lymphocytes using quantitative RT-PCR. Am J Med Genet 114: 975-979. (Pubitemid 35379243)
55. Naqvi NH, Rudrauf D, Damasio H, Bechara A, (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315: 531-534. (Pubitemid 46175760)
56. Okuyemi KS, Powell JN, Savage CR, Hall SB, Nollen N, Holsen LM, McClernon FJ, Ahluwalia JS, (2006) Enhanced cue-elicited brain activation in African American compared with Caucasian smokers: an fMRI study. Addict Biol 11: 97-106. (Pubitemid 46696741)
57. Payne TJ, Smith PO, Adams SG, Diefenbach L, (2006) Pretreatment cue reactivity predicts end-of-treatment smoking. Addict Behav 31: 702-710.
58. Perkins KA, (2001) Smoking cessation in women. Special considerations. CNS Drugs 15: 391-411. (Pubitemid 32487995)
59. Perkins KA, Donny E, Caggiula AR, (1999) Sex differences in nicotine effects and self-administration: review of human and animal evidence. Nicotine Tob Res 1: 301-315.
60. Perkins KA, Marcus MD, Levine MD, D'Amico D, Miller A, Broge M, Ashcom J, Shiffman S, (2001) Cognitive-behavioral therapy to reduce weight concerns improves smoking cessation outcome in weight-concerned women. J Consult Clin Psychol 69: 604-613. (Pubitemid 32803849)
61. Pomerleau CS, Carton SM, Lutzke ML, Flessland KA, Pomerleau OF, (1994) Reliability of the fagerstrom tolerance questionnaire and the fagerstrom test for nicotine dependence. Addict Behav 19: 33-39. (Pubitemid 24072190)
62. Prevention CfDCa (2008) Smoking-attributable mortality, years of potential life lost, and productivity losses-United States, 2000-2004. MMWR 57: 1226-1228.
63. Rollema H, Coe JW, Chambers LK, Hurst RS, Stahl SM, Williams KE, (2007) Rationale, pharmacology and clinical efficacy of partial agonists of alpha4beta2 nACh receptors for smoking cessation. Trends Pharmacol Sci 28: 316-325. (Pubitemid 47016686)
64. Rose JE, (2006) Nicotine and nonnicotine factors in cigarette addiction. Psychopharmacology (Berl) 184: 274-285. (Pubitemid 43255844)
65. Rose JE, Behm FM, Salley AN, Bates JE, Coleman RE, Hawk TC, Turkington TG, (2007) Regional brain activity correlates of nicotine dependence. Neuropsychopharmacology 32: 2441-2452. (Pubitemid 350126832)
66. Schultz W, Tremblay L, Hollerman JR, (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10: 272-284.
67. Sharma D, Money S, (2009) Carryover effects to addiction-associated stimuli in a group of marijuana and cocaine users. J Psychopharmacol 24: 1309-1316.
68. Sheehan B, Lecrubier Y, Sheehan K, (1998) The Mini International Neuropsychiatric Interview (MINI): the development and validation of structured diagnostic interview for DSM-IV and ICD-10. J Clin Psychiatry 59: 22-33. (Pubitemid 29001829)
69. Shiffman S, Jarvik ME, (1976) Smoking withdrawal symptoms in two weeks of abstinence. Psychopharmacology 50: 35-39.
70. Sinha R, Li CS, (2007) Imaging stress- and cue-induced drug and alcohol craving: association with relapse and clinical implications. Drug Alcohol Rev 26: 25-31.
71. Smolka MN, Buhler M, Klein S, Zimmermann U, Mann K, Heinz A, Braus DF, (2006) Severity of nicotine dependence modulates cue-induced brain activity in regions involved in motor preparation and imagery. Psychopharmacology (Berl) 184: 577-588. (Pubitemid 43255874)
72. van Dyck CH, Malison RT, Jacobsen LK, Seibyl JP, Staley JK, Laruelle M, Baldwin RM, Innis RB, Gelernter J, (2005) Increased dopamine transporter availability associated with the 9-repeat allele of the SLC6A3 gene. J Nucl Med 46: 745-751.
73. Vandenbergh DJ, Bennett CJ, Grant MD, Strasser AA, O'Connor R, Stauffer RL, Vogler GP, Kozlowski LT, (2002) Smoking status and the human dopamine transporter variable number of tandem repeats (VNTR) polymorphism: failure to replicate and finding that never-smokers may be different. Nicotine Tob Res 4: 333-340. (Pubitemid 34994147)
74. Vandenbergh DJ, Persico AM, Hawkins AL, Griffin CA, Li X, Jabs EW, Uhl GR, (1992) Human dopamine transporter gene (DAT1) maps to chromosome 5p15.3 and displays a VNTR. Genomics 14: 1104-1106. (Pubitemid 23053054)
75. Wang Z, Aguirre GK, Rao H, Wang J, Fernandez-Seara MA, Childress AR, Detre JA, (2008) Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn Reson Imaging 26: 261-269.
76. Wang GJ, Volkow ND, Fowler JS, Cervany P, Hitzemann RJ, Pappas NR, Wong CT, Felder C, (1999) Regional brain metabolic activation during craving elicited by recall of previous drug experiences. Life Sci 64: 775-784. (Pubitemid 29098972)
77. Waters AJ, Sayette MA, Franken IH, Schwartz JE, (2005) Generalizability of carry-over effects in the emotional Stroop task. Behav Res Ther 43: 715-732. (Pubitemid 40693697)
78. Waters AJ, Shiffman S, Sayette MA, Paty JA, Gwaltney CJ, Balabanis MH, (2004) Cue-provoked craving and nicotine replacement therapy in smoking cessation. J Consult Clin Psychol 72: 1136-1143. (Pubitemid 39658546)
79. Weinberger AH, Reutenauer EL, Allen TM, Termine A, Vessicchio JC, Sacco KA, Easton CJ, McKee SA, George TP, (2007) Reliability of the fagerstrom test for nicotine dependence, minnesota nicotine withdrawal scale, and tiffany questionnaire for smoking urges in smokers with and without schizophrenia. Drug Alcohol Depend 86: 278-282. (Pubitemid 44821602)
80. Weschler D, (1999) Wechsler Abbreviated Scale of Intelligence Manual. San Antonio, TX: Harcourt Brace & Company.
81. Wilson SJ, Sayette MA, Fiez JA, Brough E, (2007) Carry-over effects of smoking cue exposure on working memory performance. Nicotine Tob Res 9: 613-619. (Pubitemid 46672440)
82. Wu P, Wilson K, Dimoulas P, Mills EJ, (2006) Effectiveness of smoking cessation therapies: a systematic review and meta-analysis. BMC Public Health 6: 300.