Social history and exposure to pathogen signals modulate social status effects on gene regulation in rhesus macaques

Sanz, Joaquín; Maurizio, Paul L.; Snyder‐Mackler, Noah; Simons, Noah D.; Voyles, Tawni; Kohn, Jaden R.; Michopoulos, Vasiliki; Wilson, Mark; Tung, Jenny; Barreiro, Luis B.

doi:10.1073/pnas.1820846116

Cited by 34 publications

(36 citation statements)

References 49 publications

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“…Interestingly, almost all sites (35 of 38) tended to be associated with adversity occurring at ≤3 y of age compared with more recent events (37). These studies suggest that the timing of an early experience plays a role in biological embedding, although we note that the biological embedding of experience can occur across the lifespan (38).…”

Section: Dna Modificationsmentioning

confidence: 63%

Biological embedding of experience: A primer on epigenetics

Aristizabal

Anreiter

Halldorsdottir

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

178

102

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Biological embedding occurs when life experience alters biological processes to affect later life health and well-being. Although extensive correlative data exist supporting the notion that epigenetic mechanisms such as DNA methylation underlie biological embedding, causal data are lacking. We describe specific epigenetic mechanisms and their potential roles in the biological embedding of experience. We also consider the nuanced relationships between the genome, the epigenome, and gene expression. Our ability to connect biological embedding to the epigenetic landscape in its complexity is challenging and complicated by the influence of multiple factors. These include cell type, age, the timing of experience, sex, and DNA sequence. Recent advances in molecular profiling and epigenome editing, combined with the use of comparative animal and human longitudinal studies, should enable this field to transition from correlative to causal analyses.

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Section: Dna Modificationsmentioning

confidence: 63%

Biological embedding of experience: A primer on epigenetics

Aristizabal

Anreiter

Halldorsdottir

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

178

102

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“…Sanz et al (75) show that the response of the rhesus macaque immune system is affected by current social conditions and a biological memory of past conditions. A history of social subordination in female rhesus monkeys changes the blood geneexpression responses to experimentally induced bacterial and viral challenges.…”

Section: Content Of the Special Issuementioning

confidence: 99%

Genes and environments, development and time

Boyce

Sokolowski

Robinson

2020

Proc. Natl. Acad. Sci. U.S.A.

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A now substantial body of science implicates a dynamic interplay between genetic and environmental variation in the development of individual differences in behavior and health. Such outcomes are affected by molecular, often epigenetic, processes involving gene–environment (G–E) interplay that can influence gene expression. Early environments with exposures to poverty, chronic adversities, and acutely stressful events have been linked to maladaptive development and compromised health and behavior. Genetic differences can impart either enhanced or blunted susceptibility to the effects of such pathogenic environments. However, largely missing from present discourse regarding G–E interplay is the role of time, a “third factor” guiding the emergence of complex developmental endpoints across different scales of time. Trajectories of development increasingly appear best accounted for by a complex, dynamic interchange among the highly linked elements of genes, contexts, and time at multiple scales, including neurobiological (minutes to milliseconds), genomic (hours to minutes), developmental (years and months), and evolutionary (centuries and millennia) time. This special issue of PNAS thus explores time and timing among G–E transactions: The importance of timing and timescales in plasticity and critical periods of brain development; epigenetics and the molecular underpinnings of biologically embedded experience; the encoding of experience across time and biological levels of organization; and gene-regulatory networks in behavior and development and their linkages to neuronal networks. Taken together, the collection of papers offers perspectives on how G–E interplay operates contingently within and against a backdrop of time and timescales.

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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 history and exposure to pathogen signals modulate social status effects on gene regulation in rhesus macaques

Cited by 34 publications

References 49 publications

Biological embedding of experience: A primer on epigenetics

Biological embedding of experience: A primer on epigenetics

Genes and environments, development and time

Rhesus macaques as a tractable physiological model of human ageing

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