Cited by 1,655Neurotransmitter Receptor Influence on BehaviorGenetic Associations and EpidemiologyStress Responses and Cortisol

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Interaction Between the Serotonin Transporter Gene (5-HTTLPR), Stressful Life Events, and Risk of Depression: A Meta-analysis

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Risch, Neil, Herrell, Richard, Lehner, Thomas, Liang, Kung-Yee, Eaves, Lindon, Hoh, Josephine, Griem, Andrea, Kovacs, Maria, Ott, Jurg, Merikangas, Kathleen Ries·2009·JAMA

DOI 10.1001/jama.2009.878PMC PMC2938776

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Abstract

CONTEXT: Substantial resources are being devoted to identify candidate genes for complex mental and behavioral disorders through inclusion of environmental exposures following the report of an interaction between the serotonin transporter linked polymorphic region (5-HTTLPR) and stressful life events on an increased risk of major depression. OBJECTIVE: To conduct a meta-analysis of the interaction between the serotonin transporter gene and stressful life events on depression using both published data and individual-level original data. DATA SOURCES: Search of PubMed, EMBASE, and PsycINFO databases through March 2009 yielded 26 studies of which 14 met criteria for the meta-analysis. STUDY SELECTION: Criteria for studies for the meta-analyses included published data on the association between 5-HTTLPR genotype (SS, SL, or LL), number of stressful life events (0, 1, 2, > or = 3) or equivalent, and a categorical measure of depression defined by the Diagnostic and Statistical Manual of Mental Disorders (Fourth Edition) or the International Statistical Classification of Diseases, 10th Revision (ICD-10) or use of a cut point to define depression from standardized rating scales. To maximize our ability to use a common framework for variable definition, we also requested original data from all studies published prior to 2008 that met inclusion criteria. Of the 14 studies included in the meta-analysis, 10 were also included in a second sex-specific meta-analysis of original individual-level data. DATA EXTRACTION: Logistic regression was used to estimate the effects of the number of short alleles at 5-HTTLPR, the number of stressful life events, and their interaction on depression. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated separately for each study and then weighted averages of the individual estimates were obtained using random-effects meta-analysis. Both sex-combined and sex-specific meta-analyses were conducted. Of a total of 14,250 participants, 1769 were classified as having depression; 12,481 as not having depression. RESULTS: In the meta-analysis of published data, the number of stressful life events was significantly associated with depression (OR, 1.41; 95% CI,1.25-1.57). No association was found between 5-HTTLPR genotype and depression in any of the individual studies nor in the weighted average (OR, 1.05; 95% CI, 0.98-1.13) and no interaction effect between genotype and stressful life events on depression was observed (OR, 1.01; 95% CI, 0.94-1.10). Comparable results were found in the sex-specific meta-analysis of individual-level data. CONCLUSION: This meta-analysis yielded no evidence that the serotonin transporter genotype alone or in interaction with stressful life events is associated with an elevated risk of depression in men alone, women alone, or in both sexes combined.

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BackgroundInfluential
Replicating genotype–phenotype associations
NCI-NHGRI Working Group on Replication in Association Studies, Chanock, S. J., Manolio, T., Boehnke, M., Boerwinkle, E., Hunter, D. J., Thomas, G., Hirschhorn, J. N., Abecasis, G., Altshuler, D., et al. (2007) · Nature · doi:10.1038/447655a · Cited by 1,352
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Method
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“Surtees et al,25 2006 4175 (1950) 60 (41-80) 33 49 18 Crosssectional No List of Threatening Eventsb Major depression (DSM-IV) Failed to replicate”
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A translational neuroscience framework for the development of socioemotional functioning in health and psychopathology
Wiggins, J. L., & Monk, C. S. (2013) · Development and Psychopathology · doi:10.1017/s095457941300062x · Cited by 21
“Two meta-analyses failed to find an association between 5-HTTLPR and depression (Munafo, Durrant, Lewis, & Flint, 2009; Risch et al., 2009).”
Background
5-HT1A receptor blockade targeting the basolateral amygdala improved stress-induced impairment of memory consolidation and retrieval in rats
Sardari, M., Rezayof, A., & Zarrindast, M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.031 · Cited by 20
“Serotonergic neurotransmission plays an important role in modulating the behavioral responses to stress and stressrelated disorders (Chung et al., 1999; Risch et al., 2009).”
Background
The Developmental Psychobiology of Stress and Emotion in Childhood
Hostinar, C. E., & Gunnar, M. R. (2012) · Wiley eBooks · doi:10.1002/9781118133880.hop206005 · Cited by 20
Serotonin transporter genotype differentially modulates neural responses to emotional words following tryptophan depletion in patients recovered from depression and healthy volunteers
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“Jonathan Roiser, Institute of Cognitive Neuroscience, 17 Queen Square, London, WC1N 3AR, UK Email: j.roiser@ucl.ac.uk results for the latter association (Risch et al., 2009).”
BackgroundResult
The expression of serotonin transporter protein in the skin of patients with chronic spontaneous urticaria and its relation with depression and anxiety
Zabolinejad, N., Molkara, S., Bakhshodeh, B., Ghaffari-Nazari, H., & Khoshkhui, M. (2019) · Archives of Dermatological Research · doi:10.1007/s00403-019-01969-y · Cited by 19
“Alterations in the serotonergic system, especially serotonin transporters, have been associated with a variety of psychological conditions [2, 19, 30, 32].”
Background
Serotonin Transporter Genotype Moderates the Link Between Children’s Reports of Overprotective Parenting and Their Behavioral Inhibition
Burkhouse, K. L., Gibb, B. E., Coles, M. E., Knopik, V. S., & McGeary, J. E. (2011) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-011-9526-2 · Cited by 20
SERT and NET polymorphisms, temperament and antidepressant response
Andre, K., Kampman, O., Illi, A., Viikki, M., Setälä-Soikkeli, E., Mononen, N., Lehtimäki, T. J., Haraldsson, S., Koivisto, P. A., & Leinonen, E. V. J. (2015) · Nordic Journal of Psychiatry · doi:10.3109/08039488.2015.1012554 · Cited by 20
The Use of Cognitive Bias Modification and Imagery in the Understanding and Treatment of Depression
Browning, M. D., Blackwell, S. E., & Holmes, E. A. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_212 · Cited by 20
Data overuse in aging research: Emerging issues and potential solutions.
Mroczek, D. K., Weston, S. J., Graham, E. K., & Willroth, E. C. (2021) · Psychology and Aging · doi:10.1037/pag0000605 · Cited by 20
Influence of 5-HTTLPR polymorphism on postpartum depressive and posttraumatic symptoms
Landoni, M., Missaglia, S., Tavian, D., Ionio, C., & Blasio, P. D. (2021) · Psychiatric Genetics · doi:10.1097/ypg.0000000000000299 · Cited by 19
“Compatible with previous research, we found no association between the polymorphism and the depressive symptoms (Doornbos et al., 2009; Risch et al., 2009; Costas et al., 2010; Khabour et al., 2013).”
Result
Differential serotonin transport is linked to the rh5-HTTLPR in peripheral blood cells
Singh, Y. S., Altieri, S. C., Gilman, T. L., Michael, H. M., Tomlinson, I. D., Rosenthal, S. J., Swain, G. M., Murphey‐Corb, M., Ferrell, R. E., & Andrews, A. M. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.2 · Cited by 19
Influence of the Interaction between the Serotonin 1A Receptor C-1019G Polymorphism and Negative Life Stressors on the Development of Depression
Kim, H. K., Kim, S. J., Lee, Y. J., Lee, H., Kang, S., Choi, J.-E., Yun, K. W., & Lim, W. (2011) · Neuropsychobiology · doi:10.1159/000322144 · Cited by 19
Family of Origin, Race/Ethnicity, and Socioeconomic Attainment: Genotype and Intraindividual Processes
Wickrama, K. A. S., & O’Neal, C. W. (2013) · Journal of Marriage and the Family · doi:10.1111/j.1741-3737.2012.01027.x · Cited by 21
Interaction of the 5-HTTLPR and childhood trauma influences memory bias in healthy individuals
Vrijsen, J. N., Tendolkar, I., Vásquez, A. A., Franke, B., Schene, A. H., Fernández, G., & van Oostrom, I. (2015) · Journal of Affective Disorders · doi:10.1016/j.jad.2015.06.008 · Cited by 20
Anthropology’s Science Wars
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Depression Among People Who Inject Drugs and Their Intimate Partners in Kazakhstan
Shaw, S. A., El‐Bassel, N., Gilbert, L., Terlikbayeva, A., Hunt, T., Primbetova, S., Rozental, Y., & Chang, M. (2015) · Community Mental Health Journal · doi:10.1007/s10597-015-9883-3 · Cited by 20
“2006) point to the importance of examining risks associated with depression among both women and men separately (Risch et al. 2009).”
Background
Implication of serotonin-transporter (5-HTT) gene polymorphism in subjective memory complaints and mild cognitive impairment (MCI)
Marini, S., Bagnoli, S., Bessi, V., Tedde, A., Bracco, L., Sorbi, S., & Nacmias, B. (2010) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2010.06.006 · Cited by 19
The serotonin transporter gene polymorphism (5HTTLPR) moderates the effect of adolescent environmental conditions on self-esteem in young adulthood: A structural equation modeling approach
Jonassaint, C. R., Ashley‐Koch, A. E., Whitfield, K. E., Hoyle, R. H., Richman, L. S., Siegler, I. C., Royal, C. D. M., & Williams, R. B. (2012) · Biological Psychology · doi:10.1016/j.biopsycho.2012.05.004 · Cited by 20
Serotonin and urocortin 1 in the dorsal raphe and Edinger–Westphal nuclei after early life stress in serotonin transporter knockout rats
van der Doelen, R. H. A., Robroch, B., Arnoldussen, I. A. C., Schulpen, M., Homberg, J. R., & Kozicz, T. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.072 · Cited by 20
The ‘affect tagging and consolidation’ (ATaC) model of depression vulnerability
Harrington, M. O., Pennington, K., & Durrant, S. J. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.02.003 · Cited by 19
“…other studies and meta-analyses which suggest a relationship between the 5-HTTLPR S allele and MDD risk (Bogdan, Agrawal, Gaffrey, Tillman, & Luby, 2014; Kim et al., 2007; Kiyohara & Yoshimasu, 2010), although other meta-analyses have failed to replicate this finding (e.g. Risch et al., 2009).”
Associations between serotonin transporter and behavioral traits and diagnoses related to anxiety
Talati, A., Odgerel, Z., WICKRAMARATNE, P. J., Norcini-Pala, A., Skipper, J., Gingrich, J. A., & Weissman, M. M. (2017) · Psychiatry Research · doi:10.1016/j.psychres.2017.03.033 · Cited by 21
“…them such as neuroticism, equally as many others report either no associations, or associations only in the presence of specific early life stressors (Brandt et al., 2015; Caspi et al., 2003; Clarke et al., 2010; Mazzanti et al., 1998; Munafo et al., 2008; Odgerel et al., 2013; Risch et al., 2009).”
Background
Glucocorticoid Negative Feedback in Regulation of the Hypothalamic-Pituitary-Adrenal Axis in Rhesus Monkeys With Various Types of Adaptive Behavior: Individual and Age-Related Differences
Goncharova, N. D., Chigarova, О. А., Rudenko, N., & Oganyan, T. E. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00024 · Cited by 17
Suicide and Attempted Suicide
Mann, J. J., & Currier, D. (2016) · Springer eBooks · doi:10.1007/978-1-4939-2528-5_33 · Cited by 19
Gene-Environment Interactions and Depression
Koenen, K. C. (2009) · JAMA · doi:10.1001/jama.2009.1575 · Cited by 20
Genetic variants within the serotonin transporter associated with familial risk for major depression
Talati, A., Guffanti, G., Odgerel, Z., Ionita‐Laza, I., Malm, H. T., Sourander, A., Brown, A. S., WICKRAMARATNE, P. J., Gingrich, J. A., & Weissman, M. M. (2015) · Psychiatry Research · doi:10.1016/j.psychres.2015.04.015 · Cited by 19
“Given this, coupled with the heterogeneity of depression itself, it is unsurprising that even meta-analyses have yielded inconsistent patterns (Munafo et al., 2008; Risch et al., 2009).”
Pharmacogenetics and Imaging–Pharmacogenetics of Antidepressant Response: Towards Translational Strategies
Lett, T. A. P., Walter, H., & Brandl, E. J. (2016) · CNS Drugs · doi:10.1007/s40263-016-0385-9 · Cited by 19
microRNAs and Gene–Environment Interactions in Autism: Effects of Prenatal Maternal Stress and the SERT Gene on Maternal microRNA Expression
Beversdorf, D. Q., Shah, A., Jhin, A., Noel‐MacDonnell, J., Hecht, P. M., Ferguson, B. J., Bruce, D., Tilley, M. R., & Talebizadeh, Z. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.668577 · Cited by 19
Exploring the role of ketone bodies in the diagnosis and treatment of psychiatric disorders
Omori, N. E., Malys, M. K., Woo, G. H., & Mansor, L. S. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1142682 · Cited by 19
Depression
Fancher, T. L., & Kravitz, R. L. (2010) · Annals of Internal Medicine · doi:10.7326/0003-4819-152-9-201005040-01005 · Cited by 20
THE SEROTONIN TRANSPORTER GENE AND DEPRESSION
Munafo, M. R. (2012) · Depression and Anxiety · doi:10.1002/da.22009 · Cited by 18
Genetic Indeterminism, the 5-HTTLPR, and the Paths Forward in Neuropsychiatric Genetics
Blakely, R., & Veenstra-VanderWeele, J. M. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.34 · Cited by 16
Droplets of black bile? Development of vulnerability and resilience to depression in young age
Harro, J., & Kiive, E. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.02.009 · Cited by 18
Influence of 5-HTTLPR polymorphism on resting state perfusion in patients with major depression
Brockmann, H., Zobel, A. W., Schuhmacher, A., Daamen, M., Joe, A., Biermann, K., Schwab, S. G., Biersack, H., Maier, W., & Boecker, H. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.08.016 · Cited by 18
Effects of repeated adolescent stress and serotonin transporter gene partial knockout in mice on behaviors and brain structures relevant to major depression
Spinelli, S., Müller, T., Friedel, M., Sigrist, H., Lesch, K., Henkelman, R. M., Rudin, M., Seifritz, E., & Pryce, C. R. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00215 · Cited by 17
“Although the findings have been questioned (Munafo et al., 2009; Risch et al., 2009), a recent meta-analysis confirms an increased risk of developing depression following childhood maltreatment in s allele carriers relative to s allele carriers not exposed to childhood maltreatment and to long (l)…”
Result
Validating psychosocial pathways of risk between neuroticism and late life depression using a polygenic score approach.
Li, J. J., Hilton, E. C., Lu, Q., Hong, J., Greenberg, J. S., & Seltzer, M. M. (2019) · Journal of Abnormal Psychology · doi:10.1037/abn0000419 · Cited by 19
“Second, although candidate gene-environment interactions have been well studied in depression (Lesch, 2004; Risch et al., 2009), few studies have focused on gene-environment correlations.”
Toward an animal model of borderline personality disorder
Corniquel, M., Koenigsberg, H. W., & Likhtik, E. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05289-x · Cited by 20
“…stress (i.e., questionnaires vs. clinical interviews), the types of stressors included in the sample, and genotype characterization between studies (Risch et al. 2009; Karg et al. 2011; Culverhouse et al. 2017; Bleys et al. 2018; Middeldorp et al. 2007; Munafò et al. 2009; Schinka et al. 2004; Sen…”
Alternating optimization for G × E modelling with weighted genetic and environmental scores: Examples from the MAVAN study.
Jolicoeur‐Martineau, A., Wazana, A. D., Székely, E., Steiner, M. S., Fleming, A. S., Kennedy, J. L., Meaney, M. J., & Greenwood, C. M. T. (2018) · Psychological Methods · doi:10.1037/met0000175 · Cited by 19
Decision Models and Technology Can Help Psychiatry Develop Biomarkers
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“An example is whether brain structure in a group of depressed patients diﬀers from a group of non-depressed controls (20) or whether genetic variants of the serotonin transporter gene diﬀer in depressed and non-depressed patients who have experienced life stressors (21, 22).”
Background
The Pervasive and Persistent Neurobiological and Clinical Aftermath of Child Abuse and Neglect
Nemeroff, C. B., & Seligman, F. (2013) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.13com08633 · Cited by 18
Gene × Environment Interaction Models in Psychiatric Genetics
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IMPLICATIONS OF THE USE OF GENETIC TESTS IN PSYCHIATRY, WITH A FOCUS ON MAJOR DEPRESSIVE DISORDER: A REVIEW
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“[30] Three meta-analyses of this literature have been recently reported, with both negative[31, 32] and positive findings.”
Background
Sex-Hormone Genes and Gender Difference in Ultimatum Game: Experimental Evidence from China and Israel
Chew, S. H., Ebstein, R. P., & Zhong, S. (2011) · Journal of Economic Behavior & Organization · doi:10.1016/j.jebo.2013.03.008 · Cited by 18
The Role of Gene-Environment Interaction in Mental Health and Susceptibility to the Development of Psychiatric Disorders
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Psychodynamic Treatment for Borderline Personality Disorder and Mood Disorders: A Mentalizing Perspective
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Genome‐wide association analysis accounting for environmental factors through propensity‐score matching: Application to stressful live events in major depressive disorder
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Evaluation of heritable determinants of blood and brain serotonin homeostasis using recombinant inbred mice
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“Although a subject of significant debate (Risch et al. 2009), biochemical and genetic evidence continues to drive consideration that risk for depression in some individuals may be linked to a limited capacity for normal brain 5-HT signaling.”
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Early Life Adversity and Risk for Depression
Pagliaccio, D., & Barch, D. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802456-0.00002-9 · Cited by 16
Financial difficulties but not other types of recent negative life events show strong interactions with 5-HTTLPR genotype in the development of depressive symptoms
Gonda, X., Eszlári, N., Kovács, D., Anderson, I. M., Deakin, J. F. W., Juhász, G., & Bagdy, G. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.57 · Cited by 17
Sculpting infant soothability: the role of prenatal SSRI antidepressant exposure and neonatal SLC6A4 methylation status
Gartstein, M. A., Hookenson, K., Brain, U. M., Devlin, A. M., GRUNAU, R. E., & Oberlander, T. F. (2016) · Developmental Psychobiology · doi:10.1002/dev.21414 · Cited by 18
Prediction of Possible Biomarkers and Novel Pathways Conferring Risk to Post-Traumatic Stress Disorder
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Authors: Risch, N., Herrell, R., Lehner, T., Liang, K.-Y., Eaves, L., Hoh, J., Griem, A., Kovacs, M., Ott, J., & Merikangas, K. R.
Affiliations: University of California, San Francisco (US)
National Institutes of Health (US)
ORCID: Risch, Neil
Lehner, Thomas
Merikangas, Kathleen Ries
Venue: JAMA
Publisher: American Medical Association (AMA)
Published: 2009-06-17
Volume: 301
Issue: 23
Pages: 2462
ISSN: 0002-9955 (ISSN-L)
0098-7484
DOI: 10.1001/jama.2009.878
PMC: PMC2938776
OpenAlex: W2042170262
Cited by: 1,655
References: 69
Citations by year: 2026: 14 · 2025: 18 · 2024: 12 · 2023: 33 · 2022: 21 · 2021: 49 · 2020: 68 · 2019: 64 · 2018: 70 · 2017: 89 · 2016: 114 · 2015: 138 · 2014: 130 · 2013: 147 · 2012: 176
FWCI: 94.79
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: JAMA (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (UL1TR000005)
National Institute of Mental Health (Z01MH002804)
National Center for Advancing Translational Sciences
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: 5-HTTLPR, serotonin transporter gene, life events, major depressive disorder, gene-environment interaction, short allele, depression risk, sex differences, genetic susceptibility, microdata
MeSH terms: Depressive Disorder, Major, Major Depressive Disorder, Female, Genotype, Humans, Life Change Events, Male, Risk Factors, Stress, Psychological, Serotonin Plasma Membrane Transport Proteins

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Interaction Between the Serotonin Transporter Gene (5-HTTLPR), Stressful Life Events, and Risk of Depression: A Meta-analysis

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