Social status alters chromatin accessibility and the gene regulatory response to glucocorticoid stimulation in rhesus macaques

Snyder‐Mackler, Noah; Sanz, Joaquín; Kohn, Jaden R.; Voyles, Tawni; Piqué-Regi, Roger; Wilson, Mark; Barreiro, Luis B.; Tung, Jenny

doi:10.1073/pnas.1811758115

Cited by 77 publications

(60 citation statements)

References 120 publications

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“…The impact of social and environmental effects on gene regulation is an area of active research, but the mechanisms underlying changes in gene expression in response to environmental stimuli remain unclear. In rhesus macaques, social status has been shown to modify chromatin accessibility and immune gene expression (Snyder-Mackler et al, 2018), and, in humans, environmental conditions in early life (nutritional, microbial, and psychosocial) have been shown to affect DNA methylation in adulthood, in turn modifying inflammatory responses (McDade et al, 2017). Together, these studies highlight the importance of stress-driven conditions relating to social environment in the regulatory landscape of immune genes and, more generally, in physiological responses to environmental stimuli and human health (Cole, 2014).…”

Section: Discussionmentioning

confidence: 99%

Human Immunology through the Lens of Evolutionary Genetics

Quintana-Murci

2019

Cell

121

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Pathogen-imposed selection pressures have been paramount during human evolution. Detecting such selection signatures in ancient and modern human genomes can thus help us to identify genes of temporal and spatial immunological relevance. Admixture with ancient hominins and between human populations has been a source of genetic diversity open to selection by infections. Furthermore, cultural transitions, such as the advent of agriculture, have exposed humans to new microbial threats, with impacts on host defense mechanisms. The integration of population genetics and systems immunology holds great promise for the increased understanding of the factors driving immune response variation between individuals and populations.

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Section: Discussionmentioning

confidence: 99%

Human Immunology through the Lens of Evolutionary Genetics

Quintana-Murci

2019

Cell

121

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“…This difference is meaningful because this indicates that social status within primate groups is dependent on group membership, which may change and consequently change social status (i.e., Snyder‐Mackler et al., ; Tung et al., ), whereas SES in humans is theoretically independent of group membership and potentially stable. However, given that the group memberships remained stable throughout the study period and that the broad definition of SES in humans refers to the relative access to power with which they can obtain resources (McLoyd, ), we and others (e.g., Jarrell et al., ; Massart et al., ; Snyder‐Mackler et al., ; Vandeleest et al., ) argue that the social construct of status in nonhuman primates is still a good translational model for humans.…”

Section: Introductionmentioning

confidence: 92%

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

Wooddell¹,

Simpson

Murphy

et al. 2018

Developmental Science

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In humans, socioeconomic status (SES) has profound outcomes on socio-emotional development and health. However, while much is known about the consequences of SES, little research has examined the predictors of SES due to the longitudinal nature of such studies. We sought to explore whether interindividual differences in neonatal sociality, temperament, and early social experiences predicted juvenile social status in rhesus monkeys (Macaca mulatta), as a proxy for SES in humans. We performed neonatal imitation tests in infants' first week of life and emotional reactivity assessments at 2 and 4 weeks of age. We examined whether these traits, as well as the rearing environment in the first 8 months of life (with the mother or with same-aged peers only) and maternal social status predicted juvenile (2-3 years old) social status following the formation of peer social groups at 8 months. We found that infants who exhibited higher rates of neonatal imitation and newborn emotional reactivity achieved higher social status as juveniles, as did infants who were reared with their mothers, compared to infants reared with peers. Maternal social status was only associated with juvenile status for infant dyads reared in the same maternal group, indicating that relative social relationships were transferred through social experience. These results suggest that neonatal imitation and emotional reactivity may reflect ingrained predispositions toward sociality that predict later outcomes, and that nonnormative social experiences can alter socio-developmental trajectories. Our results indicate that neonatal characteristics and early social experiences predict later social outcomes in adolescence, including gradients of social stratification.

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“…Indeed, various forms of social adversity are associated with elevated expression of proinflammatory genes and decreased expression of genes related to innate immune responses in humans [69] and rhesus macaques [70]. Low macaque dominance rank, for instance, has been causally linked to altered glucocorticoid and immune regulation and a polarisation of some immune pathways towards a proinflammatory response [71][72][73][74]. Immune signatures of social status in macaques and ageing in humans have also been shown to overlap substantially in their transcriptional profiles [75], suggesting that chronic social adversity may accelerate physiological aging.…”

Section: Ageing Across the Bodymentioning

confidence: 99%

Rhesus macaques as a tractable physiological model of human ageing

Chiou

Montague

Goldman

et al. 2020

Preprint

Self Cite

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Research in the basic biology of ageing is increasingly identifying mechanisms and modifiers of ageing in short-lived organisms such as worms and mice. The ultimate goal of such work is to improve human health, particularly in the growing segment of the population surviving into old age. Thus far, few interventions have robustly transcended species boundaries in the laboratory, suggesting that changes in approach are needed to avoid costly failures in translational human research. In this review, we discuss both well-established and alternative model organisms for ageing research and outline how research in nonhuman primates is sorely needed, first, to translate findings from shorter-lived organisms to humans, and second, to understand key aspects of ageing that are unique to primate biology. We focus on rhesus macaques as a particularly promising model organism for ageing research due to their social and physiological similarity to humans as well as the existence of key resources that have been developed for this species. As a case study, we compare gene regulatory signatures of ageing in the peripheral immune system between humans and rhesus macaques from a free-ranging study population in Cayo Santiago. We show that both mRNA expression and DNA methylation signatures of immune ageing are broadly shared between macaques and humans, indicating strong conservation of the trajectory of ageing in the immune system. We conclude with a review of key issues in the biology of ageing for which macaques and other nonhuman primates may uniquely contribute valuable insights, including the effects of social gradients on health and ageing. We anticipate that continuing research in rhesus macaques and other nonhuman primates will play a critical role in conjunction with model organism and human biodemographic research in ultimately improving translational outcomes and extending health and longevity in our ageing population.

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Social status alters chromatin accessibility and the gene regulatory response to glucocorticoid stimulation in rhesus macaques

Cited by 77 publications

References 120 publications

Human Immunology through the Lens of Evolutionary Genetics

Human Immunology through the Lens of Evolutionary Genetics

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

Rhesus macaques as a tractable physiological model of human ageing

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