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Relationship Between Leukocyte Telomere Length and Personality Traits in Healthy Subjects

Published online by Cambridge University Press:  15 April 2020

R. Sadahiro
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
A. Suzuki
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
M. Enokido
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
Y. Matsumoto
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
N. Shibuya
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
M. Kamata
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
K. Goto
Affiliation:
Department of Anatomy and Cell Biology, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
K. Otani
Affiliation:
Department of Psychiatry, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata990-9585, Japan
Corresponding
E-mail address:

Abstract

Background:

It has been shown that certain personality traits are related to mortality and disease morbidity, but the biological mechanism linking them remains unclear. Telomeres are tandem repeat DNA sequences located at the ends of chromosomes, and shorter telomere length is a predictor of mortality and late-life disease morbidity. Thus, it is possible that personality traits influence telomere length. In the present study, we examined the relationship of leukocyte telomere length with personality traits in healthy subjects.

Subjects and methods:

The subjects were 209 unrelated healthy Japanese who were recruited from medical students at 4th–5th grade. Assessment of personality traits was performed by the Revised NEO Personality Inventory (NEO-PI-R) and the Temperament and Character Inventory (TCI). Leukocyte relative telomere length was determined by a quantitative real-time PCR method for a ratio of telomere/single copy gene.

Results:

In the stepwise multiple regression analysis, shorter telomere length was related to lower scores of neuroticism (P < 0.01) and conscientiousness (P < 0.05) of the NEO-PI-R, and lower scores of harm avoidance (P < 0.05) and reward dependence (P < 0.05) of the TCI.

Conclusions:

The present study suggests that leukocyte telomere length is associated with some personality traits, and this association may be implicated in the relationship between personality traits and mortality.

Type
Original article
Copyright
Copyright © Elsevier Masson SAS 2014

1. Introduction

There is increasing evidence suggesting that certain personality traits are associated with mortality [Reference Friedman, Kern and Reynolds14,Reference Weiss and Costa35] and disease morbidity such as coronary heart disease [Reference Smith and MacKenzie33]. Specifically, individuals low in conscientiousness, as measured by the NEO Personality Inventory [Reference Costa and McCrae11], were reported to display early mortality [Reference Friedman, Kern and Reynolds14,Reference Weiss and Costa35,Reference Wilson, Mendes de Leon, Bienias, Evans and Bennett37] and this finding was confirmed by meta-analyses [Reference Bogg and Roberts3,Reference Jokela, Batty, Nyberg, Virtanen, Nabi and Singh-Manoux19,Reference Roberts, Kuncel, Shiner, Caspi and Goldberg30]. Meanwhile, there have been several studies suggesting the associations of early mortality with high neuroticism and low agreeableness [Reference Wilson, Mendes de Leon, Bienias, Evans and Bennett37], but two meta-analyses produced inconsistent results [Reference Jokela, Batty, Nyberg, Virtanen, Nabi and Singh-Manoux19,Reference Roberts, Kuncel, Shiner, Caspi and Goldberg30]. Although involvement of health-harming behaviors such as smoking, alcohol use and overeating has been suggested [Reference Bogg and Roberts3], the biological mechanism linking personality traits and mortality remains unclear.

Telomeres are tandem repeat DNA sequences (TTAGGG)n located at the ends of chromosomes and play a crucial role in preventing chromosome fusion and in maintaining genome stability [Reference Blackburn2]. Prospective studies have shown that shorter telomere length is a predictor of coronary heart disease [Reference Brouilette, Moore, McMahon, Thompson, Ford and Shepherd4], cancer [Reference Ma, Zhou, Wei, Liu, Pooley and Dunning22,Reference Willeit, Willeit, Mayr, Weger, Oberhollenzer and Brandstatter36], progression of diabetic nephropathy in patients with type 1 diabetes [Reference Fyhrquist, Tiitu, Saijonmaa, Forsblom, Groop and FinnDiane Study Group16], dementia in post-stroke patients [Reference Martin-Ruiz, Dickinson, Keys, Rowan, Kenny and Von Zglinicki23], and mortality [Reference Cawthon, Smith, O’Brien, Sivatchenko and Kerber6,Reference Fitzpatrick, Kronmal, Kimura, Gardner, Psaty and Jenny13]. It has been reported that telomere length is influenced by a wide range of factors such as age, gender, race, smoking, physical activity, socioeconomic status, obesity, multivitamin intake, alcohol consumption and hormone replacement therapy [Reference Mather, Jorm, Parslow and Christensen24].

Recent studies focusing on the relationships between telomere length and psychological factors suggested that shorter telomere length was associated with current life stress [Reference Epel, Blackburn, Lin, Dhabhar, Adler and Morrow12,Reference Parks, Miller, McCanlies, Cawthon, Andrew and DeRoo28] and maltreatment [Reference Tyrka, Price, Kao, Porton, Marsella and Carpenter34] and adversity [Reference Kananen, Surakka, Pirkola, Suvisaari, Lönnqvist and Peltonen20,Reference O’Donovan, Epel, Lin, Wolkowitz, Cohen and Maguen26] during childhood. In relation to personality, shorter leukocyte telomere length was associated with high pessimism, as assessed by the Revised Life Orientation Test [Reference Scheier, Carver and Bridges31] in one study [Reference O’Donovan, Lin, Dhabhar, Wolkowitz, Tillie and Blackburn27], and with high hostility, as evaluated by using the Cook Medley Hostility Scale [Reference Cook and Medley10] in other study [Reference Brydon, Lin, Butcher, Hamer, Erusalimsky and Blackburn5]. However, these studies focused on specific personality traits only and thus, the association of telomere length with broad dimensions of personality remains to be elucidated. Therefore, in the present study, we examined the relationship of telomere length with broad dimensions of personality assessed by the most widely used scales, i.e., the revised NEO Personality Inventory (NEO-PI-R) [Reference Costa and McCrae11] and the Temperament and Character Inventory (TCI) [Reference Cloninger, Przybeck, Svrakic and Wetzel9]. The hypothesis of the present study is that shorter telomere length is associated with low conscientiousness and possibly with high neuroticism and low agreeableness. Because of the involvement of various factors such as age and race in telomere length as mentioned above, the subjects were limited to Japanese medical students with a relatively narrow age range (20–30 years old).

2. Subjects and methods

2.1. Participants

Originally, 249 physically healthy Japanese were recruited from medical students at 4th–5th grade of Yamagata University School of Medicine. Psychiatric screening was conducted by interviews by well-trained psychiatrists and a questionnaire on psychiatric treatment and diagnosis. Out of the 249 cases, 11 had psychiatric disorders and three had missing data. Data of 26 subjects were excluded due to failure of DNA extraction or PCR amplification. The remaining 209 subjects were used for analyses. One hundred twenty-eight were males and 81 were females. The mean ± SD (range) of age was 23.3 ± 1.7 (20–30) years. The subject's characteristics are shown in Table 1. The study protocol was approved by the ethics committee of the Yamagata University School of Medicine. After complete description of the study to the subjects, written informed consent was obtained from all subjects. Data collection was performed from January 2009 to October 2011.

Table 1 Characteristics of subjects, relative telomere length, NEO-PI-R scores, and TCI scores.

NEO-PI-R: Revised NEO Personality Inventory; TCI: Temperament and Character Inventory.

* P < 0.05

** P < 0.01 compared to males in the Student t-test.

2.2. Assessment for personality traits

Both the NEO-PI-R [Reference Costa and McCrae11] and the TCI [Reference Cloninger, Przybeck, Svrakic and Wetzel9] are self-report scales with 240 items that evaluate broad dimensions of personality. The NEO-PI-R consists of five domains, i.e., neuroticism, extraversion, openness to experience, agreeableness, and conscientiousness [Reference Costa and McCrae11]. The TCI has seven dimensions, i.e., novelty seeking, harm avoidance, reward dependence, persistence, self-directedness, cooperativeness, and self-transcendence [Reference Cloninger, Przybeck, Svrakic and Wetzel9]. In the present study, assessment of personality traits was performed using the Japanese version of the NEO-PI-R [Reference Shimonaka, Nakazato, Gondo and Takayama32] and the TCI [Reference Kijima, Saito, Suzuki, Yoshino, Ono and Kato21], which have been verified to have high reliability and validity.

2.3. Leukocyte telomere length

Genomic DNA was extracted from peripheral leucocytes using a QIAamp DNA Blood Kit (Qiagen, Tokyo, Japan), and was stored at −80 °C. Leukocyte relative telomere length, assessed by a ratio of telomere/single copy gene with the mean data from the triplicate runs, was determined by a quantitative real-time PCR method of Cawthon [Reference Cawthon7] with the following modifications. The 36B4 gene was used as a single copy reference gene. PCR reactions were performed separately for the telomere and 36B4 in 96-well plates in which well positions were matched between the telomere and 36B4. Genomic DNA dilution series (2.5, 5.0, 10.0, 20.0, 40.0, and 80.0 ng) were included in every plate to create a standard curve, which was used to perform absolute quantification of each DNA sample. Twenty ng of DNA was used for each individual reaction. The primers were as follows; Tel-1b (5′-CGG TTT GTT TGG GTT TGG GTT TGG GTT TGG GTT TGG GTT-3′) and Tel-2b (5′-GGC TTG CCT TAC CCT TAC CCT TAC CCT TAC CCT TAC CCT-3′) for the telomere and 36B4-F (5′-AGC ACA TAA TAG CAA TTC ACA-3′) and 36B4-R (5′-TGG CTT TAG TCA CAT TAA ATA G-3′) for the 36B4. The amplification was carried out in a 25 μL volume containing genomic DNA, each primer set (0.1 μM of Tel-1b and 0.8 μM of Tel-2b for the telomere and 0.3 μM of 36B4-F and 36B4-R for the 36B4), and 12.5 μL of SYBR Premix DimerEraser (Takara Bio Inc, Otsu, Japan). The PCR amplification and the fluorescence detection were performed using the Thermal Cycler Dice@ TP800 Real Time System (Takara Bio Inc, Otsu, Japan). Cycle conditions were as follows; 30 s at 95 °C followed by 25 cycles at 95 °C for five seconds and 52 °C for 60 s for the telomere reaction, and 30 s at 95 °C followed by 35 cycles at 95 °C for five seconds, 55 °C for 30 s, and 72 °C for 60 s for the 36B4 reaction. All plates included a genomic DNA control sample for the calibration of plate and well effects. Specificity of primer binding was monitored by melting curve analysis. The mean correlation coefficients of the standard curves in the telomere and 36B4 assay were 0.997 and 0.999, respectively, and the corresponding mean PCR efficacies were 98.6% and 90.5%, respectively. The mean coefficient of variation was 4.4% for the telomere reaction, 4.3% for the 36B4 reaction, and 13.5% for the telomere/single copy gene. Relative telomere length was expressed as a standardized z-score.

2.4. Statistical analyses

Gender differences and inter-correlations in relative telomere length, NEO-PI-R scores, TCI scores, and age were tested by the Student's t-test and the Pearson's linear regression test, respectively. Relationships of relative telomere length with the NEO-PI-R scores or the TCI scores were analyzed by the stepwise multiple regression analyses with telomere length as a dependent variable and with the NEO-PI-R scores or the TCI scores, age, and gender as independent variables. A dummy variable was used for gender (female = 0, male = 1). In the multiple regression analyses, age, gender, and 5 domain scores of the NEO-PI-R or 7 dimension scores of the TCI were entered all in once. All statistical analyses were performed by SPSS 14.0 J for Windows (SPSS Japan Inc, Tokyo, Japan), and a P value of less than 0.05 (two-tailed) was regarded as significant.

3. Results

The relative telomere length, NEO-PI-R scores, and TCI scores in total subjects, males, and females are shown in Table 1. Females had higher scores of neuroticism, openness to experience, and agreeableness of the NEO-PI-R, and reward dependence and Cooperativeness of the TCI compared to males (Table 1).

Univariate correlations among relative telomere length, NEO-PI-R scores, TCI scores, and age are shown in Table 2. Significant positive correlations of telomere length were found with the scores of neuroticism of the NEO-PI-R and reward dependence of the TCI, while there were inter-correlations among the 5 domain scores of the NEO-PI-R and among the 7 dimension scores of the TCI (Table 2). Age was not correlated with telomere length (Table 2), probably due to the narrow age range of the present sample.

Table 2 Univariate correlations among relative telomere length, NEO PI-R scores, TCI scores, and age.

NEO-PI-R: Revised NEO Personality Inventory; TCI: Temperament and Character Inventory.

Figures on the table show the Pearson's correlation coefficient.

* P < 0.05

** P < 0.01 in the Pearson's linear regression test.

In the multiple regression analysis with telomere length as a dependent variable and with the 5 domain scores of the NEO-PI-R, age, and gender as independent variables, shorter telomere length was related to lower scores of neuroticism and conscientiousness of the NEO-PI-R (Table 3, Fig. 1). In the multiple regression analysis with telomere length as a dependent variable and with the 7 dimension scores of the TCI, age, and gender as independent variables, shorter telomere length was associated with lower scores of harm avoidance and reward dependence (Table 4, Fig. 2).

Fig. 1 Relationships of telomere length with neuroticism (left) and conscientiousness (right) of the NEO-PI-R. Shorter telomere length was related (multiple correlation coefficient = 0.209, P < 0.01) to lower scores of neuroticism (partial correlation coefficient, b = 0.010, se = 0.003, t = 2.893, P < 0.01) and conscientiousness (b = 0.008, se = 0.004, t = 2.024, P < 0.05) of the NEO-PI-R. NEO-PI-R: the revised NEO Personality Inventory.

Fig. 2 PACE early intervention trial: SI demonstrated greater efficacy in preventing transition to first-episode psychosis after 6 months, compared with the NBI group. (Adapted from McGorry et al.

Table 3 Stepwise multiple regression analysis of relative telomere length with NEO-PI-R scores, age, and gender.

95% CI: 95% confidence interval, NEO-PI-R: Revised NEO Personality Inventory.

* P < 0.05

** P < 0.01 in the stepwise multiple regression analysis.

Table 4 Stepwise multiple regression analysis of relative telomere length with TCI scores, age, and gender.

95% CI: 95% confidence interval, TCI: Temperament and Character Inventory.

* P < 0.05

** P < 0.01 in the stepwise multiple regression analysis.

4. Discussion

This study was the first attempt to examine the relationship between telomere length and broad dimensions of personality. The subjects with shorter leukocyte telomere length displayed lower scores of conscientiousness of the NEO-PI-R and reward dependence of the TCI. Individuals scoring low in conscientiousness are described to be easygoing, disorganized, and purposeless [Reference Costa and McCrae11], while those scoring low in Reward dependence are practical, withdrawn, and independent [Reference Cloninger, Przybeck, Svrakic and Wetzel9]. It has been reported that subjects scoring low in conscientiousness [Reference Bogg and Roberts3] and reward dependence [Reference Abbate-Daga, Gramaglia, Malfi, Pierò and Fassino1,Reference Heath, Madden, Slutske and Martin17,Reference Puttonen, Elovainio, Kivimäki, Koskinen, Pulkki-Råback and Viikari29] are apt to engage in health-harming behaviors such as smoking, excessive alcohol consumption, and unhealthy eating. Meanwhile, these health-harming behaviors have been associated with shorter telomere length in cross sectional studies [Reference Mather, Jorm, Parslow and Christensen24]. Therefore, it is possible that the relationships of shorter telomere length with low conscientiousness and reward dependence are mediated by these health-harming behaviors.

In the present study, shorter telomere length was associated with lower scores of neuroticism of the NEO-PI-R and harm avoidance of the TCI, which are strongly related to each other [Reference Cloninger, Przybeck, Svrakic and Wetzel9]. It is described that individuals scoring low in neuroticism and harm avoidance are relaxed, secure, and outgoing [Reference Cloninger, Przybeck, Svrakic and Wetzel9,Reference Costa and McCrae11]. There have been two studies examining the association between neuroticism-related personality traits and telomere length; shorter telomere length was associated with higher pessimism in 36 mostly white post-menopausal women with a mean age of 60.7 years old [Reference O’Donovan, Lin, Dhabhar, Wolkowitz, Tillie and Blackburn27], and higher hostility in a 434 white European community sample with a mean age of 63.3 years old [Reference Brydon, Lin, Butcher, Hamer, Erusalimsky and Blackburn5]. Based on these reports, we had expected that shorter telomere length would be associated with higher neuroticism/harm avoidance. However, contrary to our expectation, the present study showed the association between shorter telomere length and lower neuroticism/harm avoidance in 209 healthy Japanese with a mean age of 23.3 years old. The similar inconsistency was also found in the studies examining the relationship between neuroticism and mortality suggesting that early mortality was related to high [Reference Roberts, Kuncel, Shiner, Caspi and Goldberg30] or low neuroticism [Reference Jokela, Batty, Nyberg, Virtanen, Nabi and Singh-Manoux19]. In relation to this, Friedman et al. [Reference Fitzpatrick, Kronmal, Kimura, Gardner, Psaty and Jenny13,Reference Friedman15] suggested the concept of “healthy neuroticism”, i.e., relatively high neuroticism leads one to be very vigilant about germs, symptoms needing attention, medical developments, and cooperation with treatment and thus preventing disease before long-term damage accumulates, while subjects with extremely high neuroticism may be apt to use substance, avoid interpersonal assistance, and develop clinical depression, leading to early mortality. The same may be true of the relationship between telomere length and neuroticism/harm avoidance, i.e., individuals with relatively high neuroticism/harm avoidance may take care of their health problems, resulting in longer telomere length, while extremely high neuroticism/harm avoidance may be related to depression and health-harming behaviors such as smoking, excessive alcohol consumption, and unhealthy eating, resulting in shorter telomere length. In fact, the present study did not assess these health-harming behaviors, and did not include the subjects with depression, which was shown to be associated with high neuroticism [Reference Christensen and Kessing8]. These findings suggest the possibility that subjects with extremely high neuroticism might be excluded from the present study. There is also the possibility that the relationships of telomere length with neuroticism/harm avoidance are different among ethnic groups, since it was reported that there were ethnic differences in telomere length [Reference Hunt, Chen, Gardner, Kimura, Srinivasan and Eckfeldt18]. Meanwhile, it is well established that there are negative correlations between age and neuroticism/harm avoidance [Reference Cloninger, Przybeck, Svrakic and Wetzel9,Reference Costa and McCrae11], and high neuroticism/harm avoidance was suggested to reflect a degree of immaturity or slower rates of biological aging [Reference McCrae25,Reference Weiss and Costa35]. Thus, it is possible that, although telomere length in the subjects with higher scores of neuroticism/harm avoidance may be longer due to slower biological aging in younger age, it may be getting shorter due to various life stress in later life [Reference Epel, Blackburn, Lin, Dhabhar, Adler and Morrow12,Reference Parks, Miller, McCanlies, Cawthon, Andrew and DeRoo28].

Previous studies showed that low scores in conscientiousness and neuroticism were related to early mortality [Reference Friedman, Kern and Reynolds14,Reference Weiss and Costa35]. Meanwhile, prospective studies demonstrated that shorter leukocyte telomere length was associated with early mortality [Reference Cawthon, Smith, O’Brien, Sivatchenko and Kerber6,Reference Fitzpatrick, Kronmal, Kimura, Gardner, Psaty and Jenny13]. Therefore, the present results showing the association of shorter leukocyte telomere length with lower conscientiousness and neuroticism may explain the biological mechanism underlying the relationship between the personality traits and mortality.

Up to here, we have discussed from the perspective that some personality traits may affect telomere length. However, it has been reported that telomere deletion and genetic defects in telomere-associated protein cause neuropsychological abnormalities including mental retardation, microcephaly, cerebellar developmental defects, ant ataxia in humans and mice [Reference Zhang, Dilley and Mattson38]. Therefore, the possibility that telomere length characterizes human mental functions and behaviors including personality traits cannot be excluded.

There are several limitations in the present study. Firstly, the subjects of this study were all Japanese medical students. Although this homogeneity of subjects is often an advantage in genetic association studies, it may make extrapolation of the present results to general populations or other ethnic groups difficult. Secondly, the present study was a cross-sectional design, i.e., personality traits and leukocyte telomere length were assessed simultaneously. Thus, the causal relationship between personality traits and telomere length remains unclear. Thirdly, the present study did not assess health-harming behaviors, i.e., smoking, excessive alcohol consumption and unhealthy eating. Therefore, it remains unclear that the relationship between telomere length and personality traits is due to biological impacts of personality on telomere length or due to effects of health-harming behaviors mediated by personality on telomere length. In further studies on the relationship between telomere length and personality traits, the assessment of health-harming behaviors is needed. Lastly, the subjects in the present study were relatively young, suggesting the possibility that at this age the effects of personality and/or health-harming behaviors mediated by personality on telomere length are lessened, and that the effects may be exaggerated or nullified in later life. To confirm this point, the relationship between telomere length and personality traits should be examined in prospective studies.

5. Conclusion

Shorter telomere length was related to lower scores of neuroticism and conscientiousness of the NEO-PI-R, and lower scores of harm avoidance and reward dependence of the TCI. The present study suggests that leukocyte telomere length is associated with some personality traits and this association may be implicated in the relationship between personality traits and mortality.

Disclosure of interest

The authors declare that they have no conflicts of interest concerning this article.

Acknowledgements

This study was supported by a funding from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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