Computational identification of gene–social environment interaction at the human IL6 locus
Open accessAbstract
To identify genetic factors that interact with social environments to impact human health, we used a bioinformatic strategy that couples expression array–based detection of environmentally responsive transcription factors with in silico discovery of regulatory polymorphisms to predict genetic loci that modulate transcriptional responses to stressful environments. Tests of one predicted interaction locus in the human IL6 promoter (SNP rs1800795) verified that it modulates transcriptional response to β-adrenergic activation of the GATA1 transcription factor in vitro. In vivo validation studies confirmed links between adverse social conditions and increased transcription of GATA1 target genes in primary neural, immune, and cancer cells. Epidemiologic analyses verified the health significance of those molecular interactions by documenting increased 10-year mortality risk associated with late-life depressive symptoms that occurred solely for homozygous carriers of the GATA1-sensitive G allele of rs1800795. Gating of depression-related mortality risk by IL6 genotype pertained only to inflammation-related causes of death and was associated with increased chronic inflammation as indexed by plasma C-reactive protein. Computational modeling of molecular interactions, in vitro biochemical analyses, in vivo animal modeling, and human molecular epidemiologic analyses thus converge in identifying β-adrenergic activation of GATA1 as a molecular pathway by which social adversity can alter human health risk selectively depending on individual genetic status at the IL6 locus.
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Adrenergic signaling suppresses transcription of antiviral type I IFN genes and up-regulates transcription of proinflammatory immune response genes IL1, TNF, and IL6, leading to increases in systemic inflammatory activity.
“This adrenergic signaling cascade suppresses transcription of antiviral type I IFN genes”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
High levels of social-environmental stress were associated with increased mortality risk for rs1800795 G homozygotes; C allele carriers exhibited no increases in mortality risk under high levels of stress.
“high levels of social-environmental stress were associated with increased mortality risk for rs1800795 G homozygotes; C allele carriers, in contrast, exhibited no increases in mortality risk under high levels of stress”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
A regulatory SNP in the human IL6 promoter moderates inflammatory responses to social stress.
“a regulatory SNP in the human IL6 promoter, that moderate inflammatory responses to social stress”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
The effect of this SNP on mortality was completely attenuated when the survival analyses adjusted for levels of CRP.
“the effect of this SNP on mortality was completely attenuated when the survival analyses adjusted for levels of CRP”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
This effect amounted to a 2.8-year shorter average life span for persons who were homozygous for the G allele.
“this effect amounted to a 2.8-year shorter average life span for persons who were homozygous for the G allele”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
The effect of this genotype on mortality risk was entirely specific to inflammation-related causes of death (e.g., cardiovascular and neurodegenerative diseases).
“the effect of this genotype on mortality risk was entirely specific to inflammation-related causes of death (e.g., cardiovascular and neurodegenerative diseases)”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
SNS activation enhances transcription of proinflammatory immune response genes, increasing systemic inflammatory activity that aids in combating bacteria and other extracellular pathogens.
“SNS activation enhances transcription of proinflammatory immune response genes (S. W. Cole et al., 2010; Grebe et al., 2010), which increases systemic inflammatory activity that aids in combating bacteria and other extracellular pathogens”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as S. W. Cole et al., 2010
SNS activation of the CTRA is mediated in large part by beta-adrenergic receptors, which stimulate transcription factors such as NF-kB, GATA, and CREB to up-regulate proinflammatory genes while inhibiting interferon response factor family transcription factors that control Type I interferon genes.
“SNS activation of the CTRA is mediated in large part by β-adrenergic receptors, which stimulate transcription factors such as nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB), GATA, and cAMP response element-binding protein (CREB) to selectively up-regulate transcription of proinflammatory genes (e.g., IL6 [19]) while simultaneously inhibiting the activity of transcription”
From Human Social Genomics (2014) · cites this paper as [19]
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Neuroendocrine influences on cancer progression
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Self-citationSustained Adrenergic Signaling Promotes Intratumoral Innervation through BDNF Induction
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Negative affective responses to a speech task predict changes in interleukin (IL)-6
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Self-citationElevating the perspective on human stress genomics
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The embodied mind: A review on functional genomic and neurological correlates of mind-body therapies
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Self-citationCytokine Genetic Variations and Fatigue Among Patients With Breast Cancer
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Self-citationNegative Emotions Predict Elevated Interleukin-6 in the United States but not in Japan
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How Genes and the Social Environment Moderate Each Other
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When grief makes you sick: Bereavement induced systemic inflammation is a question of genotype
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Higher Vagal Activity as Related to Survival in Patients With Advanced Breast Cancer
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Self-citationSocial environmental effects on gene regulation
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Self-citationEarly adversity, neural development, and inflammation
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Behavioral and Transcriptomic Fingerprints of an Enriched Environment in Horses (Equus caballus)
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Self-citationInflammatory response to mental stress and mental stress induced myocardial ischemia
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Self-citationDepressive symptoms and immune transcriptional profiles in late adolescents
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Divergent gene expression responses to Complicated Grief and Non-complicated Grief
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Self-citation
- Authors
- Cole, S. W., Arevalo, J. M. G., Takahashi, R., Sloan, E. K., Lutgendorf, S. K., Sood, A. K., Sheridan, J. F., & Seeman, T. E.
- Affiliations
- Department of Medicine and
- University of California, Los Angeles (US)
- University of Iowa (US)
- The University of Texas MD Anderson Cancer Center (US)
- The Ohio State University (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-02-22
- Volume
- 107
- Issue
- 12
- Pages
- 5681-5686
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2851818
- OpenAlex
- W2133353372
- Cited by
- 256
- References
- 66
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 15 · 2023: 8 · 2022: 13 · 2021: 6 · 2020: 15 · 2019: 11 · 2018: 14 · 2017: 13 · 2016: 14 · 2015: 19 · 2014: 36 · 2013: 20 · 2012: 23
- FWCI
- 12.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG028748, AG107265, P60AG010415, AG010415, P30AG028748)
- National Institute of Mental Health (MH046801, R01MH046801)
- National Cancer Institute (CA 109298, R01CA110793, CA 110793, R01CA109298, R01CA116778, R01CA104825, CA-116778)
- National Institute of Allergy and Infectious Diseases (R01AI052737, AI052737)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- gene-environment interaction, rs1800795, beta-adrenergic signaling, social adversity, depression, mortality risk, chronic inflammation, C-reactive protein, regulatory polymorphisms
- MeSH terms
- Base Sequence, DNA, Humans, Models, Genetic, Promoter Regions, Genetic, Social Environment, Stress, Psychological, Sympathetic Nervous System, Transcription Factors, Transcriptional Activation, Interleukin-6, Molecular Epidemiology, Computational Biology, Oligonucleotide Array Sequence Analysis, Polymorphism, Single Nucleotide, RNA, Small Interfering, GATA1 Transcription Factor
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