The Effects of Social Experience on the Stress System and Immune Function in Nonhuman Primates

  • Jordan Kohn
  • Leonidas Panagiotakopoulos
  • Gretchen N. NeighEmail author
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


There is growing recognition that social factors, such as low socioeconomic status, can predispose individuals to certain illnesses throughout their lifespan and that the physiological mechanisms involve complex interactions between the hypothalamic-pituitary-adrenal axis, the sympathetic nervous system, and the immune system. Here, we reviewed studies in nonhuman primate models of social adversity, specifically social subordination and social instability which suggest that similar stress-related biomarkers of allostasis in human social adversity, such as glucocorticoid resistance and systemic inflammation, are also found in nonhuman primates. Although many statistically significant effects of social stress have been identified in nonhuman primates, the importance of sex, individual, and species-level differences is less clear.


Social stress Nonhuman primates Primates HPA axis Immune system Stress system Stress effect Rhesus macaques Rhesus monkeys 


  1. Abbott DH et al (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43(1):67–82PubMedCrossRefGoogle Scholar
  2. Adam TC, Epel ES (2007) Stress, eating and the reward system. Physiol Behav 91(4):449–458PubMedCrossRefGoogle Scholar
  3. Alberts SC, Sapolsky RM, Altmann J (1992) Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav 26(2):167–178PubMedCrossRefGoogle Scholar
  4. Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51(6):1269–1277CrossRefGoogle Scholar
  5. Archie EA (2013) Wound healing in the wild: stress, sociality, and energetic costs affect wound healing in natural populations. Parasite ImmunolGoogle Scholar
  6. Archie EA, Altmann J, Alberts SC (2012) Social status predicts wound healing in wild baboons. Proc Natl Acad Sci USA 109(23):9017–9022PubMedPubMedCentralCrossRefGoogle Scholar
  7. Azhar S, Nomoto A, Reaven E (2002) Hormonal regulation of adrenal microvillar channel formation. J Lipid Res 43(6):861–871PubMedGoogle Scholar
  8. Bamberger CM et al (1995) Glucocorticoid receptor beta, a potential endogenous inhibitor of glucocorticoid action in humans. J Clin Invest 95(6):2435–2441PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bartanusz V et al (2004) Local gamma-aminobutyric acid and glutamate circuit control of hypophyseotrophic corticotropin-releasing factor neuron activity in the paraventricular nucleus of the hypothalamus. Eur J Neurosci 19(3):777–782PubMedCrossRefGoogle Scholar
  10. Bauer SA et al (2010) Retrospective case-control study of hyperglycemia in group-housed, mature female cynomolgus macaques (Macaca fascicularis). J Med Primatol 39(6):408–416PubMedCrossRefGoogle Scholar
  11. Bellinger DL, Lorton D (2014) Autonomic regulation of cellular immune function. Auton Neurosci 182:15–41PubMedCrossRefGoogle Scholar
  12. Benschop RJ, Rodriguez-Feuerhahn M, Schedlowski M (1996) Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav Immun 10(2):77–91PubMedCrossRefGoogle Scholar
  13. Bergman TJ et al (2005) Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Anim Behav 70(3):703–713CrossRefGoogle Scholar
  14. Bernstein IS, Gordon TP, Rose RM (1974) Aggression and social controls in rhesus monkey (Macaca mulatta) groups revealed in group formation studies. Folia Primatol (Basel) 21(2):81–107CrossRefGoogle Scholar
  15. Beutler B et al (1986) Control of cachectin (tumor necrosis factor) synthesis: mechanisms of endotoxin resistance. Science 232(4753):977–980PubMedCrossRefGoogle Scholar
  16. Blackwell GJ et al (1980) Macrocortin: a polypeptide causing the anti-phospholipase effect of glucocorticoids. Nature 287(5778):147–149PubMedCrossRefGoogle Scholar
  17. Blomquist GE, Turnquist JE (2011) Selection on adult female body size in Rhesus macaques. J Hum Evol 60(6):677–683PubMedCrossRefGoogle Scholar
  18. Boynton-Jarrett R et al (2008) Cumulative violence exposure and self-rated health: longitudinal study of adolescents in the United States. Pediatrics 122(5):961–970PubMedCrossRefGoogle Scholar
  19. Brady SS, Matthews KA (2002) The influence of socioeconomic status and ethnicity on adolescents’ exposure to stressful life events. J Pediatr Psychol 27(7):575–583PubMedCrossRefGoogle Scholar
  20. Braun CM et al (1997) Corticosteroid modulation of human, antigen-specific Th1 and Th2 responses. J Allergy Clin Immunol 100(3):400–407PubMedCrossRefGoogle Scholar
  21. Brown MS, Kovanen PT, Goldstein JL (1979) Receptor-mediated uptake of lipoprotein-cholesterol and its utilization for steroid synthesis in the adrenal cortex. Recent Prog Horm Res 35:215–257PubMedGoogle Scholar
  22. Buckingham JC, Hodges JR (1979) Hypothalamic receptors influencing the secretion of corticotrophin releasing hormone in the rat. J Physiol 290(2):421–431PubMedPubMedCentralCrossRefGoogle Scholar
  23. Calogero AE et al (1988) Multiple feedback regulatory loops upon rat hypothalamic corticotropin-releasing hormone secretion. Potential clinical implications. J Clin Invest 82(3):767–774PubMedPubMedCentralCrossRefGoogle Scholar
  24. Calogero AE et al (1990) Mechanisms of serotonin receptor agonist-induced activation of the hypothalamic-pituitary-adrenal axis in the rat. Endocrinology 126(4):1888–1894PubMedCrossRefGoogle Scholar
  25. Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci USA 106(33):13850–13853PubMedPubMedCentralCrossRefGoogle Scholar
  26. Cannon WB (1915) Bodily changes in pain, hunger, fear and rage: an account of recent researches into the function of emotional excitement, vol xiii. D. Appleton, New York, London, 311pGoogle Scholar
  27. Capitanio JP, Cole SW (2015) Social instability and immunity in rhesus monkeys: the role of the sympathetic nervous system. Philos Trans R Soc Lond B Biol Sci 370(1669)Google Scholar
  28. Capitanio JP, Lerche NW (1998) Social separation, housing relocation, and survival in simian AIDS: a retrospective analysis. Psychosom Med 60(3):235–244PubMedCrossRefGoogle Scholar
  29. Capitanio JP et al (1998) Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proc Natl Acad Sci USA 95(8):4714–4719PubMedPubMedCentralCrossRefGoogle Scholar
  30. Cavigelli SA, Caruso MJ (2015) Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Philos Trans R Soc Lond B Biol Sci 370(1669)Google Scholar
  31. Cavigelli SA, Chaudhry HS (2012) Social status, glucocorticoids, immune function, and health: can animal studies help us understand human socioeconomic-status-related health disparities? Horm Behav 62(3):295–313PubMedCrossRefGoogle Scholar
  32. Chambers DA, Cohen RL, Perlman RL (1993) Neuroimmune modulation: signal transduction and catecholamines. Neurochem Int 22(2):95–110PubMedCrossRefGoogle Scholar
  33. Chang SW et al (2013) Neuroethology of primate social behavior. Proc Natl Acad Sci USA 110(Suppl 2):10387–10394PubMedPubMedCentralCrossRefGoogle Scholar
  34. Charmandari E, Tsigos C, Chrousos G (2005) Endocrinology of the stress response. Annu Rev Physiol 67:259–284PubMedCrossRefGoogle Scholar
  35. Charmandari E et al (2012) Stress response and child health. Sci Signal 5(248):mr1Google Scholar
  36. Charron J, Drouin J (1986) Glucocorticoid inhibition of transcription from episomal proopiomelanocortin gene promoter. Proc Natl Acad Sci USA 83(23):8903–8907PubMedPubMedCentralCrossRefGoogle Scholar
  37. Chen E, Miller GE (2013) Socioeconomic status and health: mediating and moderating factors. Annu Rev Clin Psychol 9:723–749PubMedCrossRefGoogle Scholar
  38. Chen CC et al (2000) TNF-alpha-induced cyclooxygenase-2 expression in human lung epithelial cells: involvement of the phospholipase C-gamma 2, protein kinase C-alpha, tyrosine kinase, NF-kappa B-inducing kinase, and I-kappa B kinase 1/2 pathway. J Immunol 165(5):2719–2728PubMedCrossRefGoogle Scholar
  39. Chen E, Cohen S, Miller GE (2010) How low socioeconomic status affects 2-year hormonal trajectories in children. Psychol Sci 21(1):31–37PubMedCrossRefGoogle Scholar
  40. Chrousos GP (2000) The role of stress and the hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndrome: neuro-endocrine and target tissue-related causes. Int J Obes Relat Metab Disord 24(Suppl 2):S50–S55PubMedCrossRefGoogle Scholar
  41. Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267(9):1244–1252PubMedCrossRefGoogle Scholar
  42. Chrousos GP, Loriaux DL, Gold PW (1988) Mechanisms of physical and emotional stress. Based on the proceedings of an NIH symposium. November 6–8, 1986, Bethesda, Maryland. Adv Exp Med Biol 245:1–530Google Scholar
  43. Chung BC, Guo IC, Chou SJ (1997) Transcriptional regulation of the CYP11A1 and ferredoxin genes. Steroids 62(1):37–42PubMedCrossRefGoogle Scholar
  44. Cohen JJ (1992) Glucocorticoid-induced apoptosis in the thymus. Semin Immunol 4(6):363–369PubMedGoogle Scholar
  45. Cohen S et al (1997) Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 59(3):213–221PubMedCrossRefGoogle Scholar
  46. Cohen S et al (2012) Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc Natl Acad Sci USA 109(16):5995–5999PubMedPubMedCentralCrossRefGoogle Scholar
  47. Cole SW (2008) Social regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity. Brain Behav Immun 22(7):1049–1055PubMedPubMedCentralCrossRefGoogle Scholar
  48. Cole SW, Mendoza SP, Capitanio JP (2009) Social stress desensitizes lymphocytes to regulation by endogenous glucocorticoids: insights from in vivo cell trafficking dynamics in rhesus macaques. Psychosom Med 71(6):591–597PubMedPubMedCentralCrossRefGoogle Scholar
  49. Connelly MA, Williams DL (2003) SR-BI and cholesterol uptake into steroidogenic cells. Trends Endocrinol Metab 14(10):467–472PubMedCrossRefGoogle Scholar
  50. Crockett CM, Sackett GP, Bowden DM (1993) Urinary cortisol responses of longtailed macaques to five cage size, tethering, sedation, and room change. Am J Primatol 30:55–74CrossRefGoogle Scholar
  51. Crockett CM, Shimoji M, Bowden DM (2000) Behavior, appetite, and urinary cortisol responses by adult female pigtailed macaques to cage size, cage level, room change, and ketamine sedation. Am J Primatol 52(2):63–80PubMedCrossRefGoogle Scholar
  52. Crouch JL et al (2000) Income, race/ethnicity, and exposure to violence in youth: results from the national survey of adolescents. J Community Psychol 28(6):625–641CrossRefGoogle Scholar
  53. Cunnick JE et al (1991) Alterations in specific antibody production due to rank and social instability. Brain Behav Immun 5(4):357–369PubMedCrossRefGoogle Scholar
  54. de Waal FB (1986) The integration of dominance and social bonding in primates. Q Rev Biol 61(4):459–479PubMedCrossRefGoogle Scholar
  55. Debold CR et al (1989) Effects of ovine corticotropin-releasing hormone on adrenocorticotropin secretion in the absence of glucocorticoid feedback inhibition in man. J Clin Endocrinol Metab 68(2):431–437PubMedCrossRefGoogle Scholar
  56. DeCherney GS et al (1985) Diurnal variation in the response of plasma adrenocorticotropin and cortisol to intravenous ovine corticotropin-releasing hormone. J Clin Endocrinol Metab 61(2):273–279PubMedCrossRefGoogle Scholar
  57. Dhabhar FS (2009) A hassle a day may keep the pathogens away: the fight-or-flight stress response and the augmentation of immune function. Integr Comp Biol 49(3):215–236PubMedCrossRefGoogle Scholar
  58. Dhabhar FS et al (1995) Effects of stress on immune cell distribution. Dynamics and hormonal mechanisms. J Immunol 154(10):5511–5527PubMedGoogle Scholar
  59. Di S et al (2003) Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 23(12):4850–4857PubMedGoogle Scholar
  60. Dubuc C, Coyne SP, Maestripieri D (2013) Effect of mating activity and dominance rank on male masturbation among free-ranging male Rhesus macaques. Ethology 119(11)Google Scholar
  61. Dufour S et al (2009) Regulation of net hepatic glycogenolysis and gluconeogenesis by epinephrine in humans. Am J Physiol Endocrinol Metab 297(1):E231–E235PubMedPubMedCentralCrossRefGoogle Scholar
  62. Elenkov IJ, Chrousos GP (2002) Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann N Y Acad Sci 966:290–303PubMedCrossRefGoogle Scholar
  63. Evans GW, English K (2002) The environment of poverty: multiple stressor exposure, psychophysiological stress, and socioemotional adjustment. Child Dev 73(4):1238–1248PubMedCrossRefGoogle Scholar
  64. Faust JR, Goldstein JL, Brown MS (1977) Receptor-mediated uptake of low density lipoprotein and utilization of its cholesterol for steroid synthesis in cultured mouse adrenal cells. J Biol Chem 252(14):4861–4871PubMedGoogle Scholar
  65. Foerster S, Monfort SL (2010) Fecal glucocorticoids as indicators of metabolic stress in female Sykes’ monkeys (Cercopithecus mitis albogularis). Horm Behav 58(4):685–697PubMedCrossRefGoogle Scholar
  66. Fujiwara T, Kawachi I (2008) Social capital and health. A study of adult twins in the U.S. Am J Prev Med 35(2):139–144PubMedCrossRefGoogle Scholar
  67. Fuller RW (1992) The involvement of serotonin in regulation of pituitary-adrenocortical function. Front Neuroendocrinol 13(3):250–270PubMedGoogle Scholar
  68. Fuller RW (1996) Serotonin receptors involved in regulation of pituitary-adrenocortical function in rats. Behav Brain Res 73(1–2):215–219PubMedGoogle Scholar
  69. Galic MA, Riazi K, Pittman QJ (2012) Cytokines and brain excitability. Front Neuroendocrinol 33(1):116–125PubMedPubMedCentralCrossRefGoogle Scholar
  70. Gambacciani M et al (1987) Intrinsic pulsatility of ACTH release from the human pituitary in vitro. Clin Endocrinol (Oxf) 26(5):557–563CrossRefGoogle Scholar
  71. Gesquiere LR et al (2011) Life at the top: rank and stress in wild male baboons. Science 333(6040):357–360PubMedPubMedCentralCrossRefGoogle Scholar
  72. Glozier N et al (2013) Psychosocial risk factors for coronary heart disease. Med J Aust 199(3):179–180PubMedCrossRefGoogle Scholar
  73. Goo GP, Sassenrath EN (1980) Persistent adrenocortical activation in female rhesus monkeys after new breeding groups formation. J Med Primatol 9(6):325–334PubMedGoogle Scholar
  74. Gordon TP et al (1992) Social separation and reunion affects immune system in juvenile rhesus monkeys. Physiol Behav 51(3):467–472PubMedCrossRefGoogle Scholar
  75. Gust DA et al (1992) Removal from natal social group to peer housing affects cortisol levels and absolute numbers of T cell subsets in juvenile rhesus monkeys. Brain Behav Immun 6(2):189–199PubMedCrossRefGoogle Scholar
  76. Gust DA et al (1994) Effect of a preferred companion in modulating stress in adult female rhesus monkeys. Physiol Behav 55(4):681–684PubMedCrossRefGoogle Scholar
  77. Habig B, Archie EA (2015) Social status, immune response and parasitism in males: a meta-analysis. Philos Trans R Soc Lond B Biol Sci 370(1669)Google Scholar
  78. Hausfater G, Watson DF (1976) Social and reproductive correlates of parasite ova emissions by babonns. Nature 262(5570):688–689PubMedCrossRefGoogle Scholar
  79. Heilig M et al (1993) Sympathetic regulation of T-helper cell function. Brain Behav Immun 7(2):154–163PubMedCrossRefGoogle Scholar
  80. Hennessy MB et al (1995) Endocrine sensitivity to novelty in squirrel monkeys and titi monkeys: species differences in characteristic modes of responding to the environment. Physiol Behav 57(2):331–338PubMedCrossRefGoogle Scholar
  81. Heraclides AM et al (2012) Work stress, obesity and the risk of type 2 diabetes: gender-specific bidirectional effect in the Whitehall II study. Obesity (Silver Spring) 20(2):428–433CrossRefGoogle Scholar
  82. Hirata F (1983) Lipomodulin: a possible mediator of the action of glucocorticoids. Adv Prostaglandin Thromboxane Leukot Res 11:73–78PubMedCrossRefGoogle Scholar
  83. Hodge S et al (1999) Methyl-prednisolone up-regulates monocyte interleukin-10 production in stimulated whole blood. Scand J Immunol 49(5):548–553PubMedCrossRefGoogle Scholar
  84. Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7(7):e1000316PubMedPubMedCentralCrossRefGoogle Scholar
  85. Howell BR, Sanchez MM (2011) Understanding behavioral effects of early life stress using the reactive scope and allostatic load models. Dev Psychopathol 23(4):1001–1016PubMedPubMedCentralCrossRefGoogle Scholar
  86. Hristova M, Aloe L (2006) Metabolic syndrome–neurotrophic hypothesis. Med Hypotheses 66(3):545–549PubMedCrossRefGoogle Scholar
  87. Hu MC et al (2001) Functions of the upstream and proximal steroidogenic factor 1 (SF-1)-binding sites in the CYP11A1 promoter in basal transcription and hormonal response. Mol Endocrinol 15(5):812–818PubMedCrossRefGoogle Scholar
  88. Johnson EO et al (1996) The biobehavioral consequences of psychogenic stress in a small, social primate (Callithrix jacchus jacchus). Biol Psychiatry 40(5):317–337PubMedCrossRefGoogle Scholar
  89. Jonsdottir IH (2000) Exercise immunology: neuroendocrine regulation of NK-cells. Int J Sports Med 21(Suppl 1):S20–S23PubMedCrossRefGoogle Scholar
  90. Kamp Dush CM, Schmeer KK, Taylor KK (2013) Chaos as a social determinant of child health: Reciprocal associations? Soc Sci Med 95:69–76PubMedPubMedCentralCrossRefGoogle Scholar
  91. Kaplan JR, Manuck SB (1999) Status, stress, and atherosclerosis: the role of environment and individual behavior. Ann N Y Acad Sci 896:145–161PubMedCrossRefGoogle Scholar
  92. Kaplan JR et al (1982) Social status, environment, and atherosclerosis in cynomolgus monkeys. Arteriosclerosis 2(5):359–368PubMedCrossRefGoogle Scholar
  93. Kaplan JR, Chen H, Manuck SB (2009) The relationship between social status and atherosclerosis in male and female monkeys as revealed by meta-analysis. Am J Primatol 71(9):732–741PubMedPubMedCentralCrossRefGoogle Scholar
  94. Kavelaars A, van Der Voort CR, Heijnen CJ (1999) Adrenergic receptor subtypes in human peripheral blood lymphocytes. Hypertension 34(5):e5PubMedCrossRefGoogle Scholar
  95. Keller-Wood M (1988) Control of canine ACTH by corticosteroids: interaction between dose and time. Am J Physiol 254(1 Pt 2):R23–R26PubMedGoogle Scholar
  96. Keller-Wood ME, Dallman MF (1984) Corticosteroid inhibition of ACTH secretion. Endocr Rev 5(1):1–24PubMedCrossRefGoogle Scholar
  97. Kemeny ME, Schedlowski M (2007) Understanding the interaction between psychosocial stress and immune-related diseases: a stepwise progression. Brain Behav Immun 21(8):1009–1018PubMedCrossRefGoogle Scholar
  98. Kiecolt-Glaser JK et al (2003) Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci USA 100(15):9090–9095PubMedPubMedCentralCrossRefGoogle Scholar
  99. Kiss A, Aguilera G (1992) Participation of alpha 1-adrenergic receptors in the secretion of hypothalamic corticotropin-releasing hormone during stress. Neuroendocrinology 56(2):153–160PubMedCrossRefGoogle Scholar
  100. Koenig A et al (2004) Agonistic behavior and dominance relationships in female Phayre’s leaf monkeys—preliminary results. Am J Primatol 64(3):351–357PubMedCrossRefGoogle Scholar
  101. Kohm AP, Sanders VM (2001) Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4 + T and B lymphocyte function in vitro and in vivo. Pharmacol Rev 53(4):487–525PubMedGoogle Scholar
  102. Krishnan KR et al (1990) Nocturnal and early morning secretion of ACTH and cortisol in humans. Biol Psychiatry 28(1):47–57PubMedCrossRefGoogle Scholar
  103. Krysiak R, Obuchowicz E, Herman ZS (1999) Interactions between the neuropeptide Y system and the hypothalamic-pituitary-adrenal axis. Eur J Endocrinol 140(2):130–136PubMedCrossRefGoogle Scholar
  104. La Baer J, Yamamoto KR (1994) Analysis of the DNA-binding affinity, sequence specificity and context dependence of the glucocorticoid receptor zinc finger region. J Mol Biol 239(5):664–688PubMedCrossRefGoogle Scholar
  105. Lampert R et al (2005) Depressed autonomic nervous system function in African Americans and individuals of lower social class: a potential mechanism of race- and class-related disparities in health outcomes. Am Heart J 150(1):153–160PubMedCrossRefGoogle Scholar
  106. Leavitt MG et al (1997) Inhibition of fetal adrenal adrenocorticotropin receptor messenger ribonucleic acid expression by betamethasone administration to the baboon fetus in late gestation. Endocrinology 138(7):2705–2712PubMedGoogle Scholar
  107. Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46(6):1000–1015PubMedCrossRefGoogle Scholar
  108. Lepine S, Sulpice JC, Giraud F (2005) Signaling pathways involved in glucocorticoid-induced apoptosis of thymocytes. Crit Rev Immunol 25(4):263–288PubMedCrossRefGoogle Scholar
  109. Lew W, Oppenheim JJ, Matsushima K (1988) Analysis of the suppression of IL-1 alpha and IL-1 beta production in human peripheral blood mononuclear adherent cells by a glucocorticoid hormone. J Immunol 140(6):1895–1902PubMedGoogle Scholar
  110. Line SW et al (1996) Effects of social reorganization on cellular immunity in male cynomolgus monkeys. Am J Primatol 39(4):235–249CrossRefGoogle Scholar
  111. Liu Z, Simpson ER (1997) Steroidogenic factor 1 (SF-1) and SP1 are required for regulation of bovine CYP11A gene expression in bovine luteal cells and adrenal Y1 cells. Mol Endocrinol 11(2):127–137PubMedCrossRefGoogle Scholar
  112. Loucks EB et al (2009) Life-course socioeconomic position and incidence of coronary heart disease: the Framingham offspring study. Am J Epidemiol 169(7):829–836PubMedPubMedCentralCrossRefGoogle Scholar
  113. Ma XM, Lightman SL (1998) The arginine vasopressin and corticotrophin-releasing hormone gene transcription responses to varied frequencies of repeated stress in rats. J Physiol 510(Pt 2):605–614PubMedPubMedCentralCrossRefGoogle Scholar
  114. Madden KS et al (1994) Sympathetic nervous system modulation of the immune system. III. Alterations in T and B cell proliferation and differentiation in vitro following chemical sympathectomy. J Neuroimmunol 49(1–2):77–87PubMedCrossRefGoogle Scholar
  115. Madden KS, Sanders VM, Felten DL (1995) Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu Rev Pharmacol Toxicol 35:417–448PubMedCrossRefGoogle Scholar
  116. Maestroni GJ, Conti A (1994) Noradrenergic modulation of lymphohematopoiesis. Int J Immunopharmacol 16(2):117–122PubMedCrossRefGoogle Scholar
  117. Marmot MG, Shipley MJ, Rose G (1984) Inequalities in death–specific explanations of a general pattern? Lancet 1(8384):1003–1006PubMedCrossRefGoogle Scholar
  118. Marsh JW, Vehe KL, White HM (1992) Immunosuppressants. Gastroenterol Clin North Am 21(3):679–693PubMedGoogle Scholar
  119. McEwen BS (2012) Brain on stress: how the social environment gets under the skin. Proc Natl Acad Sci USA 109(Suppl 2):17180–17185PubMedPubMedCentralCrossRefGoogle Scholar
  120. McEwen BS, Stellar E (1993) Stress and the individual. Mechanisms leading to disease. Arch Intern Med 153(18):2093–2101PubMedCrossRefGoogle Scholar
  121. McFarland R, Majolo B (2013) Coping with the cold: predictors of survival in wild Barbary macaques, Macaca sylvanus. Biol Lett 9(4):20130428PubMedPubMedCentralCrossRefGoogle Scholar
  122. Meltzer H (1989) Serotonergic dysfunction in depression. Br J Psychiatry 8:25–31Google Scholar
  123. Mendoza SP et al (1978) The physiological response to group formation in adult male squirrel monkeys. Psychoneuroendocrinology 3(3–4):221–229PubMedCrossRefGoogle Scholar
  124. Meyer JS, Hamel AF (2014) Models of stress in nonhuman primates and their relevance for human psychopathology and endocrine dysfunction. ILAR J 55(2):347–360PubMedPubMedCentralCrossRefGoogle Scholar
  125. Miller GE, Chen E, Zhou ES (2007) If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol Bull 133(1):25–45PubMedCrossRefGoogle Scholar
  126. Miller GE et al (2009) Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci USA 106(34):14716–14721PubMedPubMedCentralCrossRefGoogle Scholar
  127. Mizuno H et al (1997) Glucocorticoid induced the expression of mRNA and the secretion of lipocortin 1 in rat astrocytoma cells. Brain Res 746(1–2):256–264PubMedCrossRefGoogle Scholar
  128. Mosmann TR, Sad S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17(3):138–146PubMedCrossRefGoogle Scholar
  129. Muehlenbein MP, Bribiescas RG (2005) Testosterone-mediated immune functions and male life histories. Am J Hum Biol 17(5):527–558PubMedCrossRefGoogle Scholar
  130. Muehlenbein MP, Watts DP (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med 4:21PubMedPubMedCentralCrossRefGoogle Scholar
  131. Myers DA et al (1992) Effect of implantation of dexamethasone adjacent to the paraventricular nucleus on messenger ribonucleic acid for corticotropin-releasing hormone and proopiomelanocortin during late gestation in fetal sheep. Endocrinology 130(4):2167–2172PubMedGoogle Scholar
  132. Netter FH, Hansen JT, Lambert DR (2005) Netter’s clinical anatomy, vol ix, 1st edn. Icon Learning Systems, Carlstadt, N.J, 668 pGoogle Scholar
  133. Norcross JL, Newman JD (1999) Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus). Am J Primatol 47(3):209–222PubMedCrossRefGoogle Scholar
  134. Norgren RB Jr (2013) Improving genome assemblies and annotations for nonhuman primates. ILAR J 54(2):144–153PubMedPubMedCentralCrossRefGoogle Scholar
  135. O’Connor KA et al (2011) The effects of a long-term psychosocial stress on reproductive indicators in the baboon. Am J Phys Anthropol 145(4):629–638PubMedPubMedCentralCrossRefGoogle Scholar
  136. Olshansky B et al (2008) Parasympathetic nervous system and heart failure: pathophysiology and potential implications for therapy. Circulation 118(8):863–871PubMedCrossRefGoogle Scholar
  137. Osnes J, Oye I (1975) Relationship between cyclic AMP metabolism and inotropic response of perfused rat hearts to phenylephrine and other adrenergic amines. Adv Cyclic Nucleotide Res 5:415–433PubMedGoogle Scholar
  138. Overton JM, Fisher LA (1989) Modulation of central nervous system actions of corticotropin-releasing factor by dynorphin-related peptides. Brain Res 488(1–2):233–240PubMedCrossRefGoogle Scholar
  139. Paiardini M et al (2009) T-cell phenotypic and functional changes associated with social subordination and gene polymorphisms in the serotonin reuptake transporter in female rhesus monkeys. Brain Behav Immun 23(2):286–293PubMedPubMedCentralCrossRefGoogle Scholar
  140. Panagiotakopoulos L, Neigh GN (2014) Development of the HPA axis: Where and when do sex differences manifest? Front NeuroendocrinolGoogle Scholar
  141. Papanicolaou DA et al (1998) The pathophysiologic roles of interleukin-6 in human disease. Ann Intern Med 128(2):127–137PubMedCrossRefGoogle Scholar
  142. Paul K et al (2008) The relationship between racial identity, income, stress and C-reactive protein among parous women: implications for preterm birth disparity research. J Natl Med Assoc 100(5):540–546PubMedCrossRefGoogle Scholar
  143. Phillips KA et al (2014) Why primate models matter. Am J Primatol 76(9):801–827PubMedPubMedCentralCrossRefGoogle Scholar
  144. Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277(5327):828–831PubMedCrossRefGoogle Scholar
  145. Qin DD et al (2013) Social rank and cortisol among female rhesus macaques (Macaca mulatta). Dongwuxue Yanjiu 34(E2):E42–E49PubMedGoogle Scholar
  146. Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model—a new model integrating homeostasis, allostasis, and stress. Horm Behav 55(3):375–389PubMedCrossRefGoogle Scholar
  147. Ruffolo RR Jr (1985) Distribution and function of peripheral alpha-adrenoceptors in the cardiovascular system. Pharmacol Biochem Behav 22(5):827–833PubMedCrossRefGoogle Scholar
  148. Rushworth MF, Mars RB, Sallet J (2013) Are there specialized circuits for social cognition and are they unique to humans? Curr Opin Neurobiol 23(3):436–442PubMedCrossRefGoogle Scholar
  149. Russell GM et al (2010) Rapid glucocorticoid receptor-mediated inhibition of hypothalamic-pituitary-adrenal ultradian activity in healthy males. J Neurosci 30(17):6106–6115PubMedCrossRefGoogle Scholar
  150. Rybak SM, Ramachandran J (1982) Mechanism of induction of delta 5-3 beta-hydroxysteroid dehydrogenase-isomerase activity in rat adrenocortical cells by corticotropin. Endocrinology 111(2):427–433PubMedCrossRefGoogle Scholar
  151. Sabbah W et al (2008) Effects of allostatic load on the social gradient in ischaemic heart disease and periodontal disease: evidence from the third national health and nutrition examination survey. J Epidemiol Community Health 62(5):415–420PubMedCrossRefGoogle Scholar
  152. Sage AT et al (2012) Metabolic syndrome and acute hyperglycemia are associated with endoplasmic reticulum stress in human mononuclear cells. Obesity (Silver Spring) 20(4):748–755CrossRefGoogle Scholar
  153. Sanders VM (2012) The beta2-adrenergic receptor on T and B lymphocytes: do we understand it yet? Brain Behav Immun 26(2):195–200PubMedPubMedCentralCrossRefGoogle Scholar
  154. Sanders VM, Kohm AP (2002) Sympathetic nervous system interaction with the immune system. Int Rev Neurobiol 52:17–41PubMedCrossRefGoogle Scholar
  155. Santini G et al (2001) The human pharmacology of monocyte cyclooxygenase 2 inhibition by cortisol and synthetic glucocorticoids. Clin Pharmacol Ther 70(5):475–483PubMedCrossRefGoogle Scholar
  156. Sapolsky RM (1983) Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol 5(4):365–379CrossRefGoogle Scholar
  157. Sapolsky RM (1991) Testicular function, social rank and personality among wild baboons. Psychoneuroendocrinology 16(4):281–293PubMedCrossRefGoogle Scholar
  158. Sapolsky RM (1992) Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology 17(6):701–709PubMedCrossRefGoogle Scholar
  159. Sapolsky RM (1993) Endocrinology alfresco: psychoendocrine studies of wild baboons. Recent Prog Horm Res 48:437–468PubMedGoogle Scholar
  160. Sapolsky RM (2004) Social status and health in humans and other animals. Annu Rev Anthropol 33:393–418 (ArticleType: research-article/Full publication date: 2004/Copyright © 2004 Annual Reviews)Google Scholar
  161. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(5722):648–652PubMedCrossRefGoogle Scholar
  162. Sawchenko PE, Arias C (1995) Evidence for short-loop feedback effects of ACTH on CRF and vasopressin expression in parvocellular neurosecretory neurons. J Neuroendocrinol 7(9):721–731PubMedCrossRefGoogle Scholar
  163. Seeman T et al (2010) Socio-economic differentials in peripheral biology: cumulative allostatic load. Ann N Y Acad Sci 1186:223–239PubMedCrossRefGoogle Scholar
  164. Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:34CrossRefGoogle Scholar
  165. Selye H (1950) The physiology and pathology of exposure to stress: a treatise based on the concepts of the general-adaptation-syndrome and the diseases of adaptation, vol xx, 1st edn. Acta, Montreal, 822, 203 R pGoogle Scholar
  166. Selye H (1955) Stress and disease. Science 122(3171):625–631PubMedCrossRefGoogle Scholar
  167. Setchell JM et al (2010) Stress, social behaviour, and secondary sexual traits in a male primate. Horm Behav 58(5):720–728PubMedCrossRefGoogle Scholar
  168. Sheldon C et al (1992) Chronic social stress, affiliation, and cellular immune response in nonhuman primates. Psychol Sci 3(5):301–304CrossRefGoogle Scholar
  169. Shively CA (1998) Behavioral and neurobiological effects of estrogen replacement therapy and a history of triphasic oral contraceptive exposure. Psychoneuroendocrinology 23(7):713–732PubMedCrossRefGoogle Scholar
  170. Shively CA, Kaplan JR, Adams MR (1986) Effects of ovariectomy, social instability and social status on female Macaca fascicularis social behavior. Physiol Behav 36(6):1147–1153PubMedCrossRefGoogle Scholar
  171. Shively CA, Laber-Laird K, Anton RF (1997) Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 41(8):871–882PubMedCrossRefGoogle Scholar
  172. Shively CA et al (2015) Effects of long-term sertraline treatment and depression on coronary artery atherosclerosis in premenopausal female primates. Psychosom Med 77(3):267–278PubMedPubMedCentralCrossRefGoogle Scholar
  173. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302(5648):1231–1234PubMedCrossRefGoogle Scholar
  174. Silk JB et al (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20(15):1359–1361PubMedCrossRefGoogle Scholar
  175. Silverman MN, Sternberg EM (2012) Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to glucocorticoid receptor dysfunction. Ann N Y Acad Sci 1261:55–63PubMedPubMedCentralCrossRefGoogle Scholar
  176. Silverman AJ, Hou-Yu A, Oldfield BJ (1983) Ultrastructural identification of noradrenergic nerve terminals and vasopressin-containing neurons of the paraventricular nucleus in the same thin section. J Histochem Cytochem 31(9):1151–1156PubMedCrossRefGoogle Scholar
  177. Silverman AJ, Hou-Yu A, Chen WP (1989) Corticotropin-releasing factor synapses within the paraventricular nucleus of the hypothalamus. Neuroendocrinology 49(3):291–299PubMedCrossRefGoogle Scholar
  178. Slavich GM, Irwin MR (2014) From stress to inflammation and major depressive disorder: a social signal transduction theory of depression. Psychol Bull 140(3):774–815PubMedPubMedCentralCrossRefGoogle Scholar
  179. Sloan EK et al (2007) Social stress enhances sympathetic innervation of primate lymph nodes: mechanisms and implications for viral pathogenesis. J Neurosci 27(33):8857–8865PubMedCrossRefGoogle Scholar
  180. Sloan EK, Capitanio JP, Cole SW (2008) Stress-induced remodeling of lymphoid innervation. Brain Behav Immun 22(1):15–21PubMedPubMedCentralCrossRefGoogle Scholar
  181. Smith SM, Vale WW (2006) The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci 8(4):383–395PubMedPubMedCentralGoogle Scholar
  182. Smith TE, McGreer-Whitworth B, French JA (1998) Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (Callithrix kuhli). Horm Behav 34(3):211–222PubMedCrossRefGoogle Scholar
  183. Snyder-Mackler N, Somel M, Tung J (2014) Shared signatures of social stress and aging in peripheral blood mononuclear cell gene expression profiles. Aging Cell 13(5):954–957PubMedPubMedCentralCrossRefGoogle Scholar
  184. Sousa MB et al (2005) Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups. Am J Primatol 67(1):37–50PubMedCrossRefGoogle Scholar
  185. Sperling M (ed) (2008) Pediatric endocrinology, vol xv, 3rd edn. Saunders/Elsevier, Philadelphia, PA, 889pGoogle Scholar
  186. Sundquist K et al (2006) Neighborhood violent crime and unemployment increase the risk of coronary heart disease: a multilevel study in an urban setting. Soc Sci Med 62(8):2061–2071PubMedCrossRefGoogle Scholar
  187. Thompson M Emery et al (2010) Dynamics of social and energetic stress in wild female chimpanzees. Horm Behav 58(3):440–449CrossRefGoogle Scholar
  188. Tonomura N et al (2003) Glucocorticoid-induced apoptosis of thymocytes: requirement of proteasome-dependent mitochondrial activity. J Immunol 170(5):2469–2478PubMedCrossRefGoogle Scholar
  189. Tung J, Gilad Y (2013) Social environmental effects on gene regulation. Cell Mol Life Sci 70(22):4323–4339PubMedPubMedCentralCrossRefGoogle Scholar
  190. Tung J et al (2012) Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proc Natl Acad Sci USA 109(17):6490–6495PubMedPubMedCentralCrossRefGoogle Scholar
  191. Unlap T, Jope RS (1995) Inhibition of NFkB DNA binding activity by glucocorticoids in rat brain. Neurosci Lett 198(1):41–44PubMedCrossRefGoogle Scholar
  192. Valentino RJ, Foote SL, Aston-Jones G (1983) Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Res 270(2):363–367PubMedCrossRefGoogle Scholar
  193. Veldhuis JD et al (1990) Amplitude, but not frequency, modulation of adrenocorticotropin secretory bursts gives rise to the nyctohemeral rhythm of the corticotropic axis in man. J Clin Endocrinol Metab 71(2):452–463PubMedCrossRefGoogle Scholar
  194. Vlahos R, Stewart AG (1999) Interleukin-1alpha and tumour necrosis factor-alpha modulate airway smooth muscle DNA synthesis by induction of cyclo-oxygenase-2: inhibition by dexamethasone and fluticasone propionate. Br J Pharmacol 126(6):1315–1324PubMedPubMedCentralCrossRefGoogle Scholar
  195. Vollmer RR (1996) Selective neural regulation of epinephrine and norepinephrine cells in the adrenal medulla—cardiovascular implications. Clin Exp Hypertens 18(6):731–751PubMedCrossRefGoogle Scholar
  196. Williams JM et al (1981) Sympathetic innervation of murine thymus and spleen: evidence for a functional link between the nervous and immune systems. Brain Res Bull 6(1):83–94PubMedCrossRefGoogle Scholar
  197. Wilson ME et al (2013) Social and emotional predictors of the tempo of puberty in female rhesus monkeys. Psychoneuroendocrinology 38(1):67–83PubMedPubMedCentralCrossRefGoogle Scholar
  198. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284(5756):555–556PubMedCrossRefGoogle Scholar
  199. Yee JR et al (2008) Reciprocal affiliation among adolescent rats during a mild group stressor predicts mammary tumors and lifespan. Psychosom Med 70(9):1050–1059PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Jordan Kohn
    • 1
  • Leonidas Panagiotakopoulos
    • 2
  • Gretchen N. Neigh
    • 3
    • 4
    Email author
  1. 1.Yerkes National Primate Research Center, Division of Developmental and Cognitive NeuroscienceEmory UniversityAtlantaUSA
  2. 2.Department of Pediatrics, Division of Pediatric EndocrinologyEmory UniversityAtlantaUSA
  3. 3.Department of PhysiologyEmory UniversityAtlantaUSA
  4. 4.Department of Psychiatry and Behavioral SciencesEmory UniversityAtlantaUSA

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