Epistasis between 5-HTTLPR and ADRA2B polymorphisms influences attentional bias for emotional information in healthy volunteers

International Journal of Neuropsychopharmacology

Volumn 15, Issue 8, 2012, Pages 1027-1036

  Naudts, Kris H ^a   Azevedo, Ruben T ^a   David, Anthony S ^a   Van Heeringen, Kees ^b   Gibbs, Ayana A ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GHENT UNIVERSITY   (Belgium)

^c BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

Author keywords

5 HTTLPR; ADRA2B; emotional processing

Indexed keywords

ALPHA 2B ADRENERGIC RECEPTOR; SEROTONIN TRANSPORTER;

ADULT; ALLELE; ARTICLE; ATTENTIONAL BLINK; AVERSION; COGNITION; EMOTION; EPISTASIS; GENE DELETION; GENE INSERTION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; INDEL MUTATION; MALE; MUTATIONAL ANALYSIS; NORADRENERGIC SYSTEM; NORMAL HUMAN; PRIORITY JOURNAL; SEROTONINERGIC SYSTEM;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ATTENTION; BIAS (EPIDEMIOLOGY); EMOTIONS; EPISTASIS, GENETIC; FEMALE; GENE FREQUENCY; GENOTYPE; HUMANS; MALE; MUTATION; NEUROPSYCHOLOGICAL TESTS; POLYMORPHISM, GENETIC; RECEPTORS, ADRENERGIC, ALPHA-2; SEQUENCE DELETION; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; YOUNG ADULT;

EID: 84864537351     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145711001295     Document Type: Article

References (83)

1. Anderson AK (2005). Affective influences on the attentional dynamics supporting awareness. Journal of Experimental Psychology: General 134, 258-281.
2. Anderson AK, Phelps EA (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305-309.
3. Arce E, Simmons A, Lovero K, Stein M, et al. (2008). Escitalopram effects on insula and amygdala BOLD activation during emotional processing. Psychopharmacology 196, 661-672.
4. Arnone D, Horder J, Cowen P, Harmer C (2009). Early effects of mirtazapine on emotional processing. Psychopharmacology 203, 685-691.
5. Beevers CG, Ellis AJ, Wells TT, McGeary JE (2010). Serotonin transporter gene promoter region polymorphism and selective processing of emotional images. Biological Psychology 83, 260-265.
6. Beevers CG, Gibb BE, McGeary JE, Miller IW (2007). Serotonin transporter genetic variation and biased attention for emotional word stimuli among psychiatric inpatients. Journal of Abnormal Psychology 116, 208-212.
7. Beevers CG, Marti CN, Lee HJ, Stote DL, et al. (2011). Associations between serotonin transporter gene promoter region (5-HTTLPR) polymorphism and gaze bias for emotional information. Journal of Abnormal Psychology 120, 187-197.
8. Bertolino A, Arciero G, Rubino V, Latorre V, et al. (2005). Variation of human amygdala response during threatening stimuli as a function of 5kHTTLPR genotype and personality style. Biological Psychiatry 57, 1517-1525.
9. Bradley MM, Lawson ML (1999). Affective Norms for English Words (ANEW). Gainsville, FL: NIMH Center for the Study of Emotion and Attention.
10. Browning M, Reid C, Cowen PJ, Goodwin GM, et al. (2007). A single dose of citalopram increases fear recognition in healthy subjects. Journal of Psychopharmacology 21, 684-690.
11. Brühl AB, Kaffenberger T, Herwig U (2009). Serotonergic and noradrenergic modulation of emotion processing by single dose antidepressants. Neuropsychopharmacology 35, 521-533.
12. Burghardt NS, Sullivan GM,McEwen BS, Gorman JM, et al. (2004). The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biological Psychiatry 55, 1171-1178.
13. Canli T, Omura K, Haas B, Fallgatter A, et al. (2005). Beyond affect: a role for genetic variation of the serotonin transporter in neural activation during a cognitive attention task. Proceedings of the National Academy of Sciences USA 102, 12224-12229.
14. Caspi A, Hariri AR, Holmes A, Uher R, et al. (2010). Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry 167, 509-527.
15. Caspi A, Sugden K, Moffitt TE, Taylor A, et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389.
16. Clement HW, Gemsa D, Wesemann W (1992). The effect of adrenergic drugs on serotonin metabolism in the nucleus raphe dorsalis of the rat, studied by in vivo voltammetry. European Journal of Pharmacology 217, 43-48.
17. Cordell HJ (2009). Detecting gene-gene interactions that underlie human diseases. Nature Reviews Genetics 10, 392-404.
18. de Boer T (1995). The effects of mirtazapine on central noradrenergic and serotonergic neurotransmission. International Clinical Psychopharmacology 10 (Suppl. 4), 19-23.
19. De Boer T, Nefkens F, Van Helvoirt A (1994). The a2-adrenoceptor antagonist org 3770 enhances serotonin transmission in vivo. European Journal of Pharmacology 253, R5-R6.
20. De Martino B, Strange B, Dolan R (2008). Noradrenergic neuromodulation of human attention for emotional and neutral stimuli. Psychopharmacology 197, 127-136.
21. de Quervain DJF, Kolassa IT, Ertl V, Onyut PL, et al. (2007). A deletion variant of the a2b-adrenoceptor is related to emotional memory in Europeans and Africans. Nature Neuroscience 10, 1137-1139.
22. Firk C, Markus C (2009). Differential effects of 5-HTTLPR genotypes on mood, memory, and attention bias following acute tryptophan depletion and stress exposure. Psychopharmacology 203, 805-818.
23. Fox E, Ridgewell A, Ashwin C (2009). Looking on the bright side: biased attention and the human serotonin transporter gene. Proceedings of the Royal Society of London, Series B: Biological Sciences 276, 1747-1751.
24. Gibbs A, Naudts K, Spencer E, David A (2007). The role of dopamine in attentional and memory biases for emotional information. American Journal of Psychiatry 164, 1603-1609.
25. Gibbs AA, Naudts KH, Azevedo RT, David AS (2010). Deletion variant of a2b-adrenergic receptor gene moderates the effect of COMT val158met polymorphism on episodic memory performance. European Neuropsychopharmacology 20, 272-275.
26. Hamann S, Canli T (2004). Individual differences in emotion processing. Current Opinion in Neurobiology 14, 233-238.
27. Hariri AR, Drabant EM, Munoz KE, Kolachana BS, et al. (2005). A susceptibility gene for affective disorders and the response of the human amygdala. Archives of General Psychiatry 62, 146-152.
28. Hariri AR, Mattay VS, Tessitore A, Kolachana B, et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science 297, 400-403.
29. Harmer C, Heinzen J, O'Sullivan U, Ayres R, et al. (2008). Dissociable effects of acute antidepressant drug administration on subjective and emotional processing measures in healthy volunteers. Psychopharmacology 199, 495-502.
30. Harmer CJ, Bhagwagar Z, Perrett DI, Völlm BA, et al. (2003). Acute SSRI administration affects the processing of social cues in healthy volunteers. Neuropsychopharmacology 28, 152.
31. Harmer CJ, Goodwin GM, Cowen PJ (2009). Why do antidepressants take so long to work? A cognitive neuropsychological model of antidepressant drug action. British Journal of Psychiatry 195, 102-108.
32. Harmer CJ, Shelley NC, Cowen PJ, Goodwin GM (2004). Increased positive vs. negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition. American Journal of Psychiatry 161, 1256-1263.
33. Hayward G, Goodwin GM, Cowen PJ, Harmer CJ (2005). Low-dose tryptophan depletion in recovered depressed patients induces changes in cognitive processing without depressive symptoms. Biological Psychiatry 57, 517-524.
34. Heils A, Teufel A, Petri S, Stöber G, et al. (1996). Allelic variation of human serotonin transporter gene expression. Journal of Neurochemistry 66, 2621-2624.
35. Heinz A, Braus DF, Smolka MN, Wrase J, et al. (2004). Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nature Neuroscience 8, 20-21.
36. Hu X, Oroszi G, Chun J, Smith TL, et al. (2005). An expanded evaluation of the relationship of four alleles to the level of response to alcohol and the alcoholism risk. Alcoholism: Clinical and Experimental Research 29, 8-16.
37. Hu XZ, Lipsky RH, Zhu G, Akhtar LA, et al. (2006). Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. American Journal of Human Genetics 78, 815-826.
38. Hu XZ, Rush AJ, Charney D, Wilson AF, et al. (2007). Association between a functional serotonin transporter promoter polymorphism and citalopram treatment in adult outpatients with major depression. Archives of General Psychiatry 64, 783-792.
39. Keil A, Ihssen N (2004). Identification facilitation for emotionally arousing verbs during the attentional blink. Emotion 4, 23-35.
40. Kucera H, FrancisW(1967). Computational Analysis of Present-Day American English. Providence: Brown University Press.
41. Kwang T, Wells TT, McGeary JE, Swann WB, et al. (2010). Association of the serotonin transporter promoter region polymorphism with biased attention for negative word stimuli. Depression and Anxiety 27, 746-751.
42. Leppanen JM (2006). Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Current Opinion in Psychiatry 19, 34-39.
43. Lesch K-P, Bengel D, Heils A, Sabol S, et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531.
44. Lesch KP, Gutknecht L (2005). Pharmacogenetics of the serotonin transporter. Progress in Neuro-Psychopharmacology and Biological Psychiatry 29, 1062-1073.
45. Markus CR, De Raedt R (2011). Differential effects of 5-HTTLPR genotypes on inhibition of negative emotional information following acute stress exposure and tryptophan challenge. Neuropsychopharmacology 36, 819-826.
46. Markus CR, Firk C (2009). Differential effects of tri-allelic 5-HTTLPR polymorphisms in healthy subjects on mood and stress performance after tryptophan challenge. Neuropsychopharmacology 34, 2667-2674.
47. McGaugh JL (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 27, 1-28.
48. McMahon FJ, Buervenich S, Charney D, Lipsky R, et al. (2006). Variation in the gene encoding the serotonin 2A receptor is associated with outcome of antidepressant treatment. American Journal of Human Genetics 78, 804-814.
49. Mongeau R, Blier P, Montigny C (1993). In vivo electrophysiological evidence for tonic activation by endogenous noradrenaline of a2-adrenoceptors on 5-hydroxytryptamine terminals in the rat hippocampus. Naunyn-Schmiedeberg's Archives of Pharmacology 347, 266-272.
50. Moore JH (2008). Analysis of gene-gene interactions. Current Protocols in Human Genetics 59, 1.14.1-1.14.10.
51. Munafò MR, Brown SM, Hariri AR (2008). Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biological Psychiatry 63, 852-857.
52. Munafò MR, Johnstone EC, Mackintosh B (2005). Association of serotonin transporter genotype with selective processing of smoking-related stimuli in current smokers and ex-smokers. Nicotine and Tobacco Research 7, 773-778.
53. Murphy F, Smith B, Cowen P, Robbins T, et al. (2002). The effects of tryptophan depletion on cognitive and affective processing in healthy volunteers. Psychopharmacology 163, 42-53.
54. Murphy SE, Norbury R, O'Sullivan U, Cowen PJ, et al. (2009a). Effect of a single dose of citalopram on amygdala response to emotional faces. British Journal of Psychiatry 194, 535-540.
55. Murphy SE, Yiend J, Lester KJ, Cowen PJ, et al. (2009b). Short-term serotonergic but not noradrenergic antidepressant administration reduces attentional vigilance to threat in healthy volunteers. International Journal of Neuropsychopharmacology 12, 169-179.
56. Murthy NV, Selvaraj S, Cowen PJ, Bhagwagar Z, et al. (2010). Serotonin transporter polymorphisms (SLC6A4 insertion/deletion and rs25531) do not affect the availability of 5-HTT to 11C DASB binding in the living human brain. NeuroImage 52, 50-54.
57. NCI-NHGRI Working Group on Replication in Association Studies (2007). Replicating genotype-phenotype associations. Nature 447, 655-660.
58. Nelson H (1982). The National Adult Reading Test (NART). Windsor: NEFR-Nelson.
59. Norbury R, Mackay CE, Cowen PJ, Goodwin GM, et al. (2007). Short-term antidepressant treatment and facial processing: functional magnetic resonance imaging study. British Journal of Psychiatry 190, 531-532.
60. Nutt DJ (2002). The neuropharmacology of serotonin and noradrenaline in depression. International Clinical Psychopharmacology 17, S1-S12.
61. Osinsky R, Reuter M, Kupper Y, Schmitz A, et al. (2008). Variation in the serotonin transporter gene modulates selective attention to threat. Emotion 8, 584-588.
62. Paddock S, Laje G, Charney D, Rush AJ, et al. (2007). Association of GRIK4 with outcome of antidepressant treatment in the STAR*D cohort. American Journal of Psychiatry 164, 1181-1188.
63. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski B, et al. (2005). 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience 8, 828-834.
64. Praschak-Rieder N, Kennedy J, Wilson AA, Hussey D, et al. (2007). Novel 5-HTTLPR allele associates with higher serotonin transporter binding in putamen: a 11CDASB positron emission tomography study. Biological Psychiatry 62, 327-331.
65. Rasch B, Spalek K, Buholzer S, Luechinger R, et al. (2009). A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proceedings of the National Academy of Sciences USA 106, 19191-19196.
66. Rawlings N, Norbury R, Cowen P, Harmer C (2010). A single dose of mirtazapine modulates neural responses to emotional faces in healthy people. Psychopharmacology 212, 625-634.
67. Raymond JE, Shapiro KL, Arnell KM (1992). Temporary suppression of visual processing in an RSVP task: an attentional blink? Journal of Experimental Psychology: Human Perception and Performance 18, 849-860.
68. Reimold M, Smolka MN, Schumann G, Zimmer A, et al. (2007). Midbrain serotonin transporter binding potential measured with 11CDASB is affected by serotonin transporter genotype. Journal of Neural Transmission 114, 635-639.
69. Roiser JP, Mü ller U, Clark L, Sahakian BJ (2007). The effects of acute tryptophan depletion and serotonin transporter polymorphism on emotional processing in memory and attention. International Journal of Neuropsychopharmacology 10, 449-461.
70. Routledge C, Middlemiss D (1996). The 5HT hypothesis of depression revisited. Molecular Psychiatry 1, 437.
71. Rubinsztein J, Rogers R, Riedel WJ,Mehta MA, et al. (2001). Acute dietary tryptophan depletion impairs maintenance of 'affective set' and delayed visual recognition in healthy volunteers. Psychopharmacology 154, 319-326.
72. Schosser A, Kasper S (2009). The role of pharmacogenetics in the treatment of depression and anxiety disorders. International Clinical Psychopharmacology 24, 277-288.
73. Serretti A, Kato M, De Ronchi D, Kinoshita T (2007). Metaanalysis of serotonin transporter gene promoter polymorphism (5-HTTLPR) association with selective serotonin reuptake inhibitor efficacy in depressed patients. Molecular Psychiatry 12, 247-257.
74. Small KM, Brown KM, Forbes SL, Liggett SB (2001). Polymorphic deletion of three intracellular acidic residues of the alpha 2B-adrenergic receptor decreases g proteincoupled receptor kinase-mediated phosphorylation and desensitization. Journal of Biological Chemistry 276, 4917-4922.
75. Souery D, Amsterdam J, de Montigny C, Lecrubier Y, et al. (1999). Treatment resistant depression: methodological overview and operational criteria. European Neuropsychopharmacology 9, 83-91.
76. Todd RM, Anderson AK (2009). The neurogenetics of remembering emotions past. Proceedings of the National Academy of Sciences USA 106, 18881-18882.
77. Todd RM, Palombo DJ, Levine B, Anderson AK (2011). Genetic differences in emotionally enhanced memory. Neuropsychologia 49, 734-744.
78. Uher R, Huezo-Diaz P, Perroud N, Smith R, et al. (2009). Genetic predictors of response to antidepressants in the GENDEP project. Pharmacogenomics Journal 9, 225-233.
79. Van Dyck CH, Malison RT, Staley JK, Jacobsen LK, et al. (2004). Central serotonin transporter availability measured with 123Ib-CIT SPECT in relation to serotonin transporter genotype. American Journal of Psychiatry 161, 525-531.
80. Vuilleumier P (2005). How brains beware: neural mechanisms of emotional attention. Trends in Cognitive Sciences 9, 585-594.
81. Wakeno MM, Kato MM, Okugawa GM, Fukuda TP, et al. (2008). The alpha 2A-adrenergic receptor gene polymorphism modifies antidepressant responses to milnacipran. Journal of Clinical Psychopharmacology 28, 518-524.
82. Wendland JR, Martin BJ, Kruse MR, Lesch KP, et al. (2006). Simultaneous genotyping of four functional loci of human SLC6A4, with a reappraisal of 5-HTTLPR and rs25531. Molecular Psychiatry 11, 224-226.
83. Willeit M, Praschak-Rieder N, Neumeister A, Pirker W, et al. (2000). 123I-beta-CIT SPECT imaging shows reduced brain serotonin transporter availability in drug-free depressed patients with seasonal affective disorder. Biological Psychiatry 47, 482-489.