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Association and Linkage of Anxiety-Related Traits with a Functional Polymorphism of the Serotonin Transporter Gene Regulatory Re

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Molecular Psychiatry (2000) 5, 216–219 2000 Macmillan Publishers Ltd All rights reserved 1359-4184/00 $15.00 www.nature.com/mp ORIGINAL RESEARCH ARTICLE Association and linkage of anxiety-related traits with a functional polymorphism of the serotonin transporter gene regulatory region in Israeli sibling pairs Y Osher1, D Hamer2 and J Benjamin3 1Beer Sheva Mental Health Center, Faculty of Health Sciences, Ben Gurion University of the Negev, POB 4600, Beer Sheva, Israel; 2Laboratory of Biochemistry, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA; 3Soroka Medical Center, Department of Psychiatry, Ben Gurion University of the Negev, POB 151, Beer Sheva, Israel Keywords: neuroticism; harm avoidance; anxiety; genetics; to any TPQ traits, which led to the proposal that the serotonin transport effects of this gene might vary across ethnic groups or 11 A functional polymorphism in the regulatory region of cultures. In possible support of this idea, a United the serotonin transporter gene (5-HTTLPR) has been States study12 found a significant interaction between reported to be both associated and linked to anxiety- 5-HTTLPR genotype and race for NEO-PI-R neuroti- related personality measures, although other studies cism, which suggests that the relationship between the have not replicated these findings. The current study allele and anxiety-related traits may be obscured by the examines both association and linkage of the gene to effects of differing phenotypes and differing gene fre- two major anxiety-related personality measures, the quencies in different populations (population harm avoidance scale on the Tridimensional Personality stratification). Several other studies13–15 found no Questionnaire and the neuroticism scale of the NEO-PI- R, in a sample of 148 Israeli subjects comprising 74 association of the 5-HTTLPR with various personality same-sex sibling pairs. We replicated the reported measures. Unfortunately, none of the negative studies association between the short allele and higher scores included family material, which is essential to dis- on the TPQ harm avoidance scale (P = 0.03), including tinguish genuine genetic transmission, or its lack, from the subscale of shyness (P = 0.02), and also found artifacts of population stratification. We therefore association in the same direction between the short examined both association and linkage of the gene to allele and the NEO-PI-R neuroticism subscales of anxi- two major anxiety-related personality measures, the ety (P = 0.03) and depression (P = 0.04). Sib-pair linkage TPQ harm avoidance scale and the NEO neuroticism analysis, using the regression method, further sup- scale, in a sample of 148 healthy Israeli volunteers ported a role of the 5-HTTLPR in anxiety-related person- comprising 74 same-sex sibling pairs. ality traits. Molecular Psychiatry (2000) 5, 216–219. Allele frequencies were 48.9% for the long allele and 51.1% for the short allele. Genotype frequencies were Examination of the possible relationship between a in Hardy–Weinberg equilibrium (24.3% for long/long, functional polymorphism in the promoter region of the 49.3% for long/short, and 26.4% for short/short). serotonin transporter gene (5-HTTLPR) and clinical The association results are summarized in Table 1, anxiety disorders has yielded suggestive but inconclus- which shows the average TPQ and NEO-PI-R person- ive results.1–3 Studies of anxiety-related temperament ality test scores after stratifying the population by and personality dimensions, rather than overt psycho- genotype. Based on prior biochemical and behavioural pathology, have also yielded inconsistent findings. evidence,4,16 the statistical analysis focused on the Lesch et al4 originally reported an association in comparison between individuals with either one or United States subjects between the short form of the two short alleles (the ‘short’ group) as compared to polymorphism and higher scores on the Neuroticism individuals homozygous for the long allele (the ‘long’ scale of Costa and McRae’s NEO-PI-R5 and with higher group). The significance of association was determined estimated scores for Cloninger’s Tridimensional Per- by ANOVA with age, sex and ethnicity entered as sonality Questionnaire6 (TPQ) scale of harm avoidance. covariates. These findings were supported by a study7 of older The short genotype was significantly associated with United States subjects using the actual TPQ instrument higher overall harm avoidance scores (F = 4.61; and by two Japanese studies, one using the TPQ8 and P = 0.03) including its subscale of shyness (F = 5.93; the other using a self-report anxiety and depression P = 0.02). By contrast, between-group differences were questionnaire.9 Another study, in Finnish subjects, not significant for the other three TPQ scales of novelty found linkage but not association of the 5-HTTLPR seeking, reward dependence, and persistence. The with facets of harm avoidance.10 However, a study of short genotype also tended to be associated with higher Israeli subjects found no association of the 5-HTTLPR total neuroticism scores (F = 3.40; P = 0.06), and this 5-HTTLPR and anxiety traits Y Osher et al 217 Table 1 Personality scale scores (means ± standard deviation) by serotonin transporter regulatory region (5-HTTP) genotype Genotype short/short short/long any short long/long TPQ n = 39 n = 73 n = 112 n = 36 Novelty seeking 16.18 ± 4.53 14.88 ± 4.71 15.33 ± 4.67 16.44 ± 4.30 Harm avoidance 14.62 ± 6.93 14.37 ± 6.37 14.46 ± 6.54 11.81 ± 6.80** HA 1—Worry 4.00 ± 2.37 3.71 ± 2.33 3.81 ± 2.34 3.22 ± 2.72 HA 2—Fear of uncertainty 4.92 ± 2.16 4.62 ± 1.82 4.72 ± 1.94 4.08 ± 1.84 HA 3—Shyness 3.03 ± 1.97 2.92 ± 1.88 2.96 ± 1.90 2.11 ± 1.70** HA 4—Fatigability 2.67 ± 2.66 3.12 ± 2.33 2.96 ± 2.45 2.39 ± 2.42 Reward dependence 13.82 ± 3.88 13.52 ± 3.64 13.63 ± 3.71 14.36 ± 3.57 Persistence 4.92 ± 2.25 4.75 ± 2.01 4.81 ± 2.09 5.36 ± 2.10 NEO-PI-R n = 39 n = 70 n = 109 n = 35 Neuroticism 91.5 ± 25.6 92.8 ± 23.8 92.3 ± 24.3 85.1 ± 24.6* N 1—Anxiety 17.3 ± 6.1 17.6 ± 6.1 17.5 ± 6.1 15.1 ± 6.6** N 2—Angry hostility 14.5 ± 5.4 14.4 ± 5.1 14.4 ± 5.2 13.6 ± 5.4 N 3—Depression 14.2 ± 5.9 16.0 ± 5.5 15.4 ± 5.7 13.3 ± 6.2** N 4—Self-consciousness 16.8 ± 5.6 16.0 ± 4.5 16.2 ± 5.0 15.0 ± 4.9 N 5—Impulsiveness 17.7 ± 4.1 17.0 ± 4.4 17.3 ± 4.3 16.8 ± 5.3 N 6—Vulnerability 11.2 ± 5.6 11.6 ± 4.9 11.5 ± 5.1 10.9 ± 5.2 Extroversion 114.7 ± 24.6 111.0 ± 22.9 112.3 ± 23.5 120.3 ± 24.2 Openness 115.8 ± 18.1 114.2 ± 17.5 114.7 ± 17.6 111.7 ± 19.1 Agreeableness 114.9 ± 16.1 112.8 ± 17.2 113.5 ± 16.8 111.6 ± 19.8 Conscientiousness 125.8 ± 21.7 122.9 ± 20.8 123.9 ± 21.1 128.6 ± 17.1 Any short vs long/long (df = 1): **P Ͻ 0.05 after correcting for sex, age, and ethnic group as covariates. *P Ͻ 0.07 after correcting for sex, age, and ethnic group as covariates. was significant for the two neuroticism subscales of Table 2 Linkage results anxiety (F = 4.86; P = 0.03) and depression (F = 4.15; = P 0.04). There was no significant association with any B3 P other NEO-PI-R scale. In agreement with previous results, the short allele had more of a dominant than TPQ recessive effect (based on analyses of s/s vs s/l vs l/l, Novelty seeking −0.041 ns not shown; see Table 1). Harm avoidance 0.289 0.07 Since population-based association studies are sub- HA1 0.004 ns ject to false positive findings due to population strati- HA2 0.281 0.06 fication, within-family analyses are also important. HA3 0.327 0.04 HA4 0.246 0.09 Analysis of discordant sib-pairs revealed that sibs with Reward dependence −0.010 ns the short allele tended to have slightly higher harm Persistence −0.285 ns avoidance scores than did sibs homozygous for the long allele, but the difference was not significant NEO (HA = 14.55 ± 4.67 for short vs HA = 13.27 ± 5.95 for Neuroticism 0.292 0.0652 long, n = 22 pairs; paired t = 0.838, df = 21, P = 0.41). N1 0.114 ns Neuroticism scores in the discordant sib-pairs also did N2 0.122 ns not differ significantly (N = 93.10 ± 18.67 for short vs N3 0.127 ns − N = 92.86 ± 22.35 for long, n = 21 pairs; paired t = 0.41, N4 0.294 ns df = 20, P = 0.97). N5 0.531 0.0007 N6 0.211 ns Linkage is an alternative method to assess the Extroversion 0.020 ns relationship between a gene and a trait within families. Openness −0.221 ns Sib-pair linkage analysis by the regression method of Agreeableness 0.028 ns 17 Cardon et al gave the results shown in Table 2. There Conscientiousness −0.041 ns was suggestive evidence for linkage with total HA = = scores (P 0.07), with the HA shyness subscale B3 regression coefficient for linkage. = = (P 0.04), and with two other HA subscales (fear: P one-sided significance level of B3.
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