Harlow, H. F., Dodsworth, R. O. & Harlow, M. K. Total social isolation in monkeys. Proc. Natl Acad. Sci. USA 54, 90–97 (1965).
Google Scholar
Levine, S. Infantile experience and resistance to physiological stress. Science 126, 405 (1957).
Google Scholar
Liu, D. et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659–1662 (1997).
Google Scholar
Francis, D., Diorio, J., Liu, D. & Meaney, M. J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155–1158 (1999).
Google Scholar
Caldji, C. et al. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl Acad. Sci. USA 95, 5335–5340 (1998).
Google Scholar
Vargas, J., Junco, M., Gomez, C. & Lajud, N. Early life stress increases metabolic risk, HPA axis reactivity, and depressive-like behavior when combined with postweaning social isolation in rats. PLoS ONE 11, 1–21 (2016).
Google Scholar
Sánchez, M. M. et al. Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biol. Psychiatry 57, 373–381 (2005).
Google Scholar
Fries, A. B. W., Shirtcliff, E. A. & Pollak, S. D. Neuroendocrine dysregulation following early social deprivation in children. Dev. Psychobiol. 50, 588–599 (2008).
Google Scholar
Li, E. & Bird, A. In Epigenetics (eds Allis, C. D., Jenuwein, T., Reinberg, D. & Caparros, M.-L.), 343–356 (Cold Spring Harbor Laboratory Press, 2007).
Weaver, I. C. G. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847–854 (2004).
Google Scholar
Anier, K. et al. Maternal separation is associated with DNA methylation and behavioural changes in adult rats. Eur. Neuropsychopharmacol. 24, 459–468 (2014).
Google Scholar
Provencal, N. et al. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. J. Neurosci. 32, 15626–15642 (2012).
Google Scholar
Unternaehrer, E. et al. Childhood maternal care is associated with DNA methylation of the genes for brain-derived neurotrophic factor (BDNF) and oxytocin receptor (OXTR) in peripheral blood cells in adult men and women. Stress 18, 451–461 (2015).
Google Scholar
Sánchez, M. M., Ladd, C. O. & Plotsky, P. M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 13, 419–449 (2001).
Google Scholar
Van Bodegom, M., Homberg, J. R. & Henckens, M. J. A. G. Modulation of the hypothalamic-pituitary-adrenal axis by early life stress exposure. Front. Cell. Neurosci. 11, 1–33 (2017).
Moore, S. R. et al. Epigenetic correlates of neonatal contact in humans. Dev. Psychopathol. 29, 1517–1538 (2017).
Google Scholar
Sanchez, M. M. The impact of early adverse care on HPA axis development: nonhuman primate models. Horm. Behav. 50, 623–631 (2006).
Google Scholar
Houtepen, L. C. et al. Genome-wide DNA methylation levels and altered cortisol stress reactivity following childhood trauma in humans. Nat. Commun. 7, 10967 (2016).
Coley, E. J. L. et al. Cross-generational transmission of early life stress effects on HPA regulators and bdnf are mediated by sex, lineage, and upbringing. Front. Behav. Neurosci. 13, 1–17 (2019).
Google Scholar
Kember, R. L. et al. Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse. Brain Behav. 2, 455–467 (2012).
Google Scholar
Dunn, E. C. et al. Sensitive periods for the effect of childhood adversity on DNA methylation: results from a prospective, longitudinal study. Biol. Psychiatry 85, 838–849 (2019).
Google Scholar
Hennessy, M. B., Hornschuh, G., Kaiser, S. & Sachser, N. Cortisol responses and social buffering: a study throughout the life span. Horm. Behav. 49, 383–390 (2006).
Google Scholar
Kent, W. J. et al. The Human Genome Browser at UCSC. Genome Res. 12, 996–1006 (2002).
Google Scholar
Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).
Google Scholar
Kornienko, O., Clemans, K. H., Out, D. & Granger, D. A. Hormones, behavior, and social network analysis: exploring associations between cortisol, testosterone, and network structure. Horm. Behav. 66, 534–544 (2014).
Google Scholar
Kornienko, O., Clemans, K. H., Out, D. & Granger, D. A. Friendship network position and salivary cortisol levels. Soc. Neurosci. 8, 385–396 (2013).
Google Scholar
Ponzi, D., Muehlenbein, M. P., Geary, D. C. & Flinn, M. V. Cortisol, salivary alpha-amylase and children’s perceptions of their social networks. Soc. Neurosci. 11, 164–174 (2016).
Google Scholar
Wittig, R. M. et al. Focused grooming networks and stress alleviation in wild female baboons. Horm. Behav. 54, 170–177 (2008).
Google Scholar
Wey, T. W. & Blumstein, D. T. Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success. Behav. Ecol. Sociobiol. 66, 1075–1085 (2012).
Google Scholar
Priebe, K. et al. Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/CJ mice: a cross-fostering study. Dev. Psychobiol. 47, 398–407 (2005).
Google Scholar
McLaughlin, K. A. et al. Causal effects of the early caregiving environment on development of stress response systems in children. Proc. Natl Acad. Sci. USA 112, 5637–5642 (2015).
Google Scholar
Sheriff, M. J., Dantzer, B., Delehanty, B., Palme, R. & Boonstra, R. Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166, 869–887 (2011).
Google Scholar
Goymann, W. On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. Methods Ecol. Evol. 3, 757–765 (2012).
Google Scholar
Laubach, Z. M. et al. Early life social and ecological determinants of global DNA methylation in wild spotted hyenas. Mol. Ecol. 28, 3799–3812 (2019).
Google Scholar
Greenberg, J. R. Developmental Flexibility in Spotted Hyneas (Crocuta crocuta): The Role of Maternal and Anthropogenic Effects (Michigan State University, 2017).
Turner, J. W., Bills, P. S. & Holekamp, K. E. Ontogenetic change in determinants of social network position in the spotted hyena. Behav. Ecol. Sociobiol. 72, 1–5 (2018).
Smolarek, I. et al. Global DNA methylation changes in blood of patients with essential hypertension. Med. Sci. Monit. 16, 149–155 (2010).
Zinellu, A. et al. Blood global DNA methylation is decreased in non-severe chronic obstructive pulmonary disease (COPD) patients. Pulm. Pharmacol. Ther. 46, 11–15 (2017).
Google Scholar
Dong, Y. et al. Associations between global DNA methylation and telomere length in healthy adolescents. Sci. Rep. 7, 1–6 (2017).
Google Scholar
Wong, J. Y. Y. et al. The association between global DNA methylation and telomere length in a longitudinal study of boilermakers. Genet. Epidemiol. 38, 254–264 (2014).
Google Scholar
Woo, H. D. & Kim, J. Global DNA hypomethylation in peripheral blood leukocytes as a biomarker for cancer risk: A meta-analysis. PLoS ONE 7, e34615 (2012).
Google Scholar
Sharma, P. et al. Detection of altered global DNA methylation in coronary artery disease patients. DNA Cell Biol. 27, 357–365 (2008).
Google Scholar
Ono, H. et al. Association of dietary and genetic factors related to one-carbon metabolism with global methylation level of leukocyte DNA. Cancer Sci. 103, 2159–2164 (2012).
Google Scholar
Basu, N. et al. Effects of methylmercury on epigenetic markers in three model species: mink, chicken and yellow perch Niladri. Comp. Biochem. Physiol. C 157, 322–327 (2013).
Google Scholar
Laubach, Z. M. et al. Socioeconomic status and DNA methylation from birth through mid-childhood: a prospective study in Project Viva. Epigenomics https://doi.org/10.2217/epi-2019-0040 (2019).
Meissner, A. et al. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res. 33, 5868–5877 (2005).
Google Scholar
Brown, G. R. et al. Gene: a gene-centered information resource at NCBI. Nucleic Acids Res. 43, D36–D42 (2015).
Google Scholar
National Library of Medicine (US), National Center for Biotechnology Information. Gene. https://www.ncbi.nlm.nih.gov/gene/ (2004).
Binns, D. et al. QuickGO: a web-based tool for Gene Ontology searching. Bioinformatics 25, 3045–3046 (2009).
Google Scholar
Huntley, R. P. et al. The GOA database: Gene Ontology annotation updates for 2015. Nucleic Acids Res. 43, D1057–D1063 (2015).
Google Scholar
Chang, I. & Parrilla, M. Expression patterns of homeobox genes in the mouse vomeronasal organ at postnatal stages. Gene Expr. Patterns 21, 69–80 (2016).
Google Scholar
Santos, J. S., Fonseca, N. A., Vieira, C. P., Vieira, J. & Casares, F. Phylogeny of the teashirt-related zinc finger (tshz) gene family and analysis of the developmental expression of tshz2 and tshz3b in the zebrafish. Dev. Dyn. 239, 1010–1018 (2010).
Google Scholar
Zhou, T. et al. Peripheral blood gene expression as a novel genomic biomarker in complicated sarcoidosis. PLoS ONE 7, 1–13 (2012).
Google Scholar
Scheinfeldt, L. B. et al. Using the Coriell Personalized Medicine Collaborative Data to conduct a genome-wide association study of sleep duration. Am. J. Med. Genet. B 168, 697–705 (2015).
Google Scholar
Riku, M. et al. Down-regulation of the zinc-finger homeobox protein TSHZ2 releases GLI1 from the nuclear repressor complex to restore its transcriptional activity during mammary tumorigenesis. Oncotarget 7, 5690–5701 (2016).
Google Scholar
Tapia-Carrillo, D., Tovar, H., Velazquez-Caldelas, T. E. & Hernandez-Lemus, E. Master regulators of signaling pathways: an application to the analysis of gene regulation in breast cancer. Front. Genet. 10, 1–11 (2019).
Google Scholar
Yamamoto, M., Cid, E., Bru, S. & Yamamoto, F. Rare and frequent promoter methylation, respectively, of TSHZ2 and 3 genes that are both downregulated in expression in breast and prostate cancers. PLoS ONE 6, 1–10 (2011).
Google Scholar
Zhou, S. et al. Proteomic landscape of TGF-β1-induced fibrogenesis in renal fibroblasts. Sci. Rep. 10, 1–17 (2020).
Google Scholar
Seto, S., Tsujimura, K. & Koide, Y. Rab GTPases regulating phagosome maturation are differentially recruited to mycobacterial phagosomes. Traffic 12, 407–420 (2011).
Google Scholar
Kretzer, N. M. et al. RAB43 facilitates cross-presentation of cell-associated antigens by CD8α+ dendritic cells. J. Exp. Med. 213, 2871–2883 (2016).
Google Scholar
Huang, Z., Liang, H. & Chen, L. Rab43 promotes gastric cancer cell proliferation and metastasis via regulating the pi3k/akt signaling pathway. OncoTargets Ther. 13, 2193–2202 (2020).
Google Scholar
Han, M. Z. et al. High expression of RAB43 predicts poor prognosis and is associated with epithelial-mesenchymal transition in gliomas. Oncol. Rep. 37, 903–912 (2017).
Google Scholar
Blackburn, M. R., Datta, S. K., Wakamiya, M., Vartabedian, B. S. & Kellems, R. E. Metabolic and immunologic consequences of limited adenosine deaminase expression in mice. J. Biol. Chem. 271, 15203–15210 (1996).
Google Scholar
Bradford, K. L., Moretti, F. A., Carbonaro-Sarracino, D. A., Gaspar, H. B. & Kohn, D. B. Adenosine deaminase (ADA)-deficient severe combined immune deficiency (SCID): molecular pathogenesis and clinical manifestations. J. Clin. Immunol. 37, 626–637 (2017).
Google Scholar
Parish, S. T. et al. Adenosine deaminase modulation of telomerase activity and replicative senescence in human CD8 T lymphocytes. J. Immunol. 184, 2847–2854 (2010).
Google Scholar
Sánchez-Melgar, A., Albasanz, J. L., Pallàs, M. & Martín, M. Adenosine metabolism in the cerebral cortex from several mice models during aging. Int. J. Mol. Sci. 21, 1–20 (2020).
Google Scholar
Geiger, J. D. & Nagy, J. I. Ontogenesis of adenosine deaminase activity in rat brain. J. Neurochem. 48, 147–153 (1987).
Google Scholar
Vasudha, K. C., Nirmal Kumar, A. & Venkatesh, T. Studies on the age dependent changes in serum adenosine deaminase activity and its changes in hepatitis. Indian J. Clin. Biochem. 21, 116–120 (2006).
Google Scholar
Sims, B., Powers, R. E., Sabina, R. L. & Theibert, A. B. Elevated adenosine monophosphate deaminase activity in Alzheimer’s disease brain. Neurobiol. Aging 19, 385–391 (1998).
Google Scholar
Singh, L. S. & Sharma, R. Developmental expression and corticosterone inhibition of adenosine deaminase activity in different tissues of mice. Mech. Ageing Dev. 80, 85–92 (1995).
Google Scholar
McGowan, P. O. et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12, 342–348 (2009).
Google Scholar
Pan, P., Fleming, A. S., Lawson, D., Jenkins, J. M. & McGowan, P. O. Within- and between-litter maternal care alter behavior and gene regulation in female offspring. Behav. Neurosci. 128, 736–748 (2014).
Google Scholar
Romero, L. M., Dickens, M. J. & Cyr, N. E. The Reactive Scope Model – a new model integrating homeostasis, allostasis, and stress. Horm. Behav. 55, 375–389 (2009).
Google Scholar
Kamin, H. S. & Kertes, D. A. Cortisol and DHEA in development and psychopathology. Horm. Behav. 89, 69–85 (2017).
Google Scholar
Engler, H., Bailey, M. T., Engler, A. & Sheridan, J. F. Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen. J. Neuroimmunol. 148, 106–115 (2004).
Google Scholar
Kruuk, H. The Spotted Hyena: A Study of Predation and Social Behavior (University of Chicago Press, 1972).
Holekamp, K., Smale, L. & Szykman, M. Rank and reproduction in the female spotted hyaena. J. Reprod. Fertil. 108, 229–237 (1996).
Google Scholar
Holekamp, K. E. & Smale, L. Behavioral development in the spotted hyena. Bioscience 48, 997–1005 (1998).
Google Scholar
Holekamp, K. E. et al. Patterns of association among female spotted hyenas (Crocuta crocuta). J. Mammal. 78, 55–64 (1997).
Google Scholar
Turner, J. W., Robitaille, A. L., Bills, P. S. & Holekamp, K. E. Early-life relationships matter: social position during early life predicts fitness among female spotted hyenas. J. Anim. Ecol. 90, 183–196 (2021).
Google Scholar
Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, 227–267 (1974).
Google Scholar
Karimi, M., Johansson, S. & Ekström, T. J. Using LUMA. A luminometric-based assay for global DNA methylation. Epigenetics 1, 45–48 (2006).
Google Scholar
Coluccio, A. et al. Individual retrotransposon integrants are differentially controlled by KZFP/KAP1-dependent histone methylation, DNA methylation and TET-mediated hydroxymethylation in naïve embryonic stem cells. Epigenet. Chromatin 11, 1–18 (2018).
Google Scholar
Eden, A., Gaudet, F., Waghmare, A. & Jaenisch, R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 300, 455 (2003).
Google Scholar
Lev Maor, G., Yearim, A. & Ast, G. The alternative role of DNA methylation in splicing regulation. Trends Genet. 31, 274–280 (2015).
Google Scholar
Doherty, T. S., Forster, A. & Roth, T. L. Global and gene-specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment. Behav. Brain Res. 298, 55–61 (2016).
Google Scholar
Noguera, J. C. & Velando, A. Bird embryos perceive vibratory cues of predation risk from clutch mates. Nat. Ecol. Evol. 3, 1225–1232 (2019).
Google Scholar
Crudo, A. et al. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology 153, 3269–3283 (2012).
Google Scholar
Garrett-Bakelman, F. E. et al. Enhanced reduced representation bisulfite sequencing for assessment of DNA nethylation at base pair resolution. J. Vis. Exp. https://doi.org/10.3791/52246, 1–15 (2015).
Yang, C. et al. A draft genome assembly of spotted hyena, Crocuta crocuta. Sci. Data 7, 1–10 (2020).
Google Scholar
Mccormick, J. A. et al. 5’-Heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Mol. Endocrinol. 14, 506–517 (2000).
Google Scholar
Szyf, M., Weaver, I. C. G., Champagne, F. A., Diorio, J. & Meaney, M. J. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front. Neuroendocrinol. 26, 139–162 (2005).
Google Scholar
Van Meter, P. E. et al. Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm. Behav. 55, 329–337 (2009).
Google Scholar
Dloniak, S. M. et al. Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta). Gen. Comp. Endocrinol. 135, 51–61 (2004).
Google Scholar
Laubach, Z. M., Murray, E. J., Hoke, K. L., Safran, R. J. & Perng, W. A biologist’s guide to model selection and causal inference. Proc. R. Soc. Ser. B https://doi.org/10.1098/rspb.2020.2815 (2021).
Engh, A. L., Esch, K., Smale, L. & Holekamp, K. E. Mechanisms of maternal rank ‘inheritance’ in the spotted hyaena, Crocuta crocuta. Anim. Behav. 60, 323–332 (2000).
Google Scholar
Baron, R. M. & Kenny, D. A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J. Pers. Soc. Psychol. 51, 1173–1182 (1986).
Google Scholar
Chadeau-Hyam, M. et al. Meeting-in-the-middle using metabolic profiling-a strategy for the identification of intermediate biomarkers in cohort studies. Biomarkers 16, 83–88 (2011).
Google Scholar
Lea, A. J., Altmann, J., Alberts, S. C. & Tung, J. Resource base influences genome-wide DNA methylation levels in wild baboons (Papio cynocephalus). Mol. Ecol. 25, 1681–1696 (2016).
Google Scholar
Lea, A. J., Tung, J. & Zhou, X. A flexible, efficient binomial mixed model for identifying differential DNA methylation in bisulfite sequencing data. PLoS Genet. 11, 1–31 (2015).
Google Scholar
van Iterson, M. et al. Controlling bias and inflation in epigenome- and transcriptome-wide association studies using the empirical null distribution. Genome Biol. 18, 1–13 (2017).
Google Scholar
Hochberg, Y. & Benjamini, Y. More powerful procedures for multiple statistical significance testing. Stat. Med. 9, 811–818 (1990).
Google Scholar
Laubach, Z. M. et al. Early-life social experience affects offspring DNA methylation and later life stress phenotype. https://doi.org/10.5281/zenodo.4967924 (2021).
Source: Ecology - nature.com