Transcriptional modulation of the developing immune system by early life social adversity
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To identify molecular mechanisms by which early life social conditions might influence adult risk of disease in rhesus macaques ( Macaca mulatta ), we analyze changes in basal leukocyte gene expression profiles in 4-mo-old animals reared under adverse social conditions. Compared with the basal condition of maternal rearing (MR), leukocytes from peer-reared (PR) animals and PR animals provided with an inanimate surrogate mother (surrogate/peer reared, SPR) show enhanced expression of genes involved in inflammation, cytokine signaling, and T-lymphocyte activation, and suppression of genes involved in several innate antimicrobial defenses including type I interferon (IFN) antiviral responses. Promoter-based bioinformatic analyses implicate increased activity of CREB and NF-κB transcription factors and decreased activity of IFN response factors (IRFs) in structuring the observed differences in gene expression. Transcript origin analyses identify monocytes and CD4 + T lymphocytes as primary cellular mediators of transcriptional up-regulation and B lymphocytes as major sources of down-regulated genes. These findings show that adverse social conditions can become embedded within the basal transcriptome of primate immune cells within the first 4 mo of life, and they implicate sympathetic nervous system-linked transcription control pathways as candidate mediators of those effects and potential targets for health-protective intervention.
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The increased proinflammatory/reduced antiviral skewing of the basal gene expression profile, called the basal transcriptome, appears to represent a conserved transcriptional response to adversity (CTRA) that is adaptive in countering injuries associated with actual physical threat.
“As depicted in Figure 1 and described more fully by Slavich and Cole (2013), this increased proinflammatory/ reduced antiviral skewing of our basal gene expression profile, called the basal transcriptome, appears to represent a conserved transcriptional response to adversity (CTRA) that is adaptive in countering injuries associated with actual physical threat”
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., 2012
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Experimental — accuracy not yet measuredActivation of the CTRA by modern-day social, symbolic, anticipated, and imagined threats leads to increased risk for several inflammation-related conditions, including depression.
“The CTRA can also be activated by modernday social, symbolic, anticipated, and imagined threats, however, leading to increased risk for several inflammation-related conditions, including depression”
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., 2012
The Discussion (page not available in our copy) reports that experimentally imposed early-life social adversity activated CTRA dynamics in infant rhesus macaques. It does not establish activation by symbolic, anticipated, or imagined threats, or show that CTRA activation increases the risk of depression; it treats later disease effects as a possibility requiring further study. (LLM, conf=0.87)
Experimental — accuracy not yet measuredDisrupted caregiving may result in impaired negative feedback within immune cells via increased intracellular inflammatory gene expression and decreased glucocorticoid receptor sensitivity, promoting inflammatory cytokine production despite elevated glucocorticoids.
“Disrupted caregiving may also result in impaired negative feedback within immune cells via increased intracellular inflammatory gene expression and decreased glucocorticoid receptor sensitivity which promotes production of inflammatory cytokines despite the presence of elevated glucocorticoids (Cole et al., 2012).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as Cole et al., 2012
Disrupted caregiving may impair coordination between glucocorticoids and immune cells, such as glucocorticoid insensitivity contributing to elevated circulating inflammation despite the presence of glucocorticoids.
“Disrupted caregiving may impair coordination between glucocorticoids and immune cells, such as glucocorticoid insensitivity in immune cells that may contribute to elevated circulating inflammation despite the presence of glucocorticoids (Cole, 2008; Cole et al., 2012).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as Cole et al., 2012
Experimental animal models show that CTRA gene expression profiles can be induced in leukocytes by repeated social threat, unstable social hierarchies, and low social status.
“Subsequent studies using experimental animal models has shown that CTRA gene expression profiles can be induced in leukocytes by repeated social threat [9], unstable social hierarchies [8], [29], and low social status [7].”
From Human Social Genomics (2014) · cites this paper as [8]
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Self-citationKohrt, B. A., Worthman, C. M., Adhikari, R. P., Luitel, N. P., Arevalo, J. M. G., Ma, J., McCreath, H., Seeman, T. E., Crimmins, E. M., & Cole, S. W. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1601301113 · Cited by 110 · see citing works
Self-citationAntoni, M. H., Bouchard, L. C., Jacobs, J. M., Lechner, S. C., Jutagir, D. R., Gudenkauf, L. M., Carver, C. S., Lutgendorf, S., Cole, S. W., Lippman, M., et al. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.012 · Cited by 89 · see citing works
Self-citationWingo, A. P., & Gibson, G. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.09.016 · Cited by 59 · see citing works
Gupta, A., Mayer, E. A., Acosta, J. R., Hamadani, K., Torgerson, C., van Horn, J. D., Chang, L., Naliboff, B., Tillisch, K., & Labus, J. S. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.02.003 · Cited by 56 · see citing works
Nervous system regulation of the cancer genome
Cole, S. W. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.11.008 · Cited by 41 · see citing works
Self-citationSimons, R. L., Lei, M.-K., Beach, S. R. H., Barr, A. B., Cutrona, C. E., Gibbons, F. X., & Philibert, R. A. (2017) · Social Science & Medicine · doi:10.1016/j.socscimed.2017.03.005 · Cited by 38 · see citing works
- Authors
- Cole, S. W., Conti, G., Arevalo, J. M. G., Ruggiero, A. M., Heckman, J. J., & Suomi, S. J.
- Affiliations
- Department of Medicine, Division of Hematology-Oncology, and Department of Psychiatry and Biobehavioral Sciences, University of California School of Medicine, Los Angeles, CA 90095;
- University of Chicago (US)
- University of California, Los Angeles (US)
- National Institutes of Health (US)
- University College Dublin (IE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-11-26
- Volume
- 109
- Issue
- 50
- Pages
- 20578-20583
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3528538
- OpenAlex
- W2078858790
- Cited by
- 207
- References
- 72
- Citations by year
- 2026: 5 · 2025: 19 · 2024: 11 · 2023: 13 · 2022: 10 · 2021: 16 · 2020: 17 · 2019: 19 · 2018: 5 · 2017: 16 · 2016: 21 · 2015: 21 · 2014: 15 · 2013: 15 · 2012: 3
- FWCI
- 7.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (R01AG034679, P30AG012857, P30AG107265, P60AG010415)
- National Cancer Institute (R01CA116778)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R37HD065072, R01HD054702)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Keywords
- immune system development, leukocyte gene expression, rhesus monkeys, inflammation, cytokine signaling, T cell activation, type I interferon, innate immunity, CREB, NF-κB, monocytes, CD4+ T cells, B cells, sympathetic nervous system, maternal care, peer rearing, surrogate mothers, transcriptional regulation
- MeSH terms
- Animals, Animals, Newborn, Female, Macaca mulatta, Male, Maternal Behavior, Social Behavior, Social Environment, Computational Biology, Databases, Genetic, Transcriptome
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