Epigenetic plasticity following early stress predicts long-term health outcomes in rhesus macaques

American Journal of Physical Anthropology

Volumn 155, Issue 2, 2014, Pages 192-199

  Kinnally, E L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Body condition; Development; Dna methylation; Inflammation; Maternal care; Rhesus macaque; Serotonin transporter

Indexed keywords

BIOLOGICAL MARKER; SEROTONIN TRANSPORTER;

5 HTT GENE; ADULT; ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; DIARRHEA; DNA METHYLATION; EARLY LIFE STRESS; EPIGENETICS; FACTORIAL ANALYSIS; FEMALE; GENE; GENETIC LINKAGE; INFANT; MALE; MATERNAL CARE; MOTHER CHILD RELATION; NONHUMAN; OUTCOME ASSESSMENT; RHESUS MONKEY; ANIMAL; GENETIC EPIGENESIS; GENETICS; MATERNAL BEHAVIOR; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REGRESSION ANALYSIS;

ANIMALS; BODY WEIGHT; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; MACACA MULATTA; MALE; MATERNAL BEHAVIOR; REGRESSION ANALYSIS; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84927911484     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22565     Document Type: Article

References (53)

1. Ainsworth MD. 1979. Infant-mother attachment. Am Psychologist 34:932-937.
2. Boyle WJ, Simonet WS, Lacey DL. 2003. Osteoclast differentiation and activation. Nature 423(6937):337-342.
3. Bardi M, Huffman MA. 2002. Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata). Develop Psychobiol 41:364-372.
4. Beach SR, Brody GH, Todorov AA, Gunter TD, Philibert RA. 2011. Methylation at 5HTT mediates the impact of child sex abuse on women's antisocial behavior: An examination of the Iowa adoptee sample. Psychosom Med 73:83-87.
5. Bird A. 1986. CpG-rich islands and the function of DNA methylation. Nature, 321:209-213.
6. Boyle WJ, Simonet WS, Lacey DL 2003. Osteoclast differentiation and activation. Nature 423:337-342.
7. Briggs AW, Stenzel U, Meyer M, Krause J, Kircher M, Pääbo S. 2010. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucl Acids Res 38(6): e87.
8. Brummett BH, Siegler IC, Ashley-Koch A, Williams RB. 2011. Effects of 5HTTLPR on cardiovascular response to an emotional stressor. Psychosomat Med 73:318-322.
9. Capitanio J, Mendoza S, Mason W, Maninger N. 2005. Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta). Develop Psychobiol 46:318-330.
10. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. 2006. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptoralpha expression in the medial preoptic area of female offspring. Endocrinology 147:2909-2915.
11. Chen X, Margolis KJ, Gershon MD, Schwartz GJ, Sze JY. 2012. Reduced serotonin reuptake transporter (SERT) function causes insulin resistance and hepatic steatosis independent of food intake. PLoS One 7(3):e32511.
12. Conti G, Hansman C, Heckman JJ, Novak MF, Ruggiero A, Suomi SJ. 2012. Primate evidence on the late health effects of early-life adversity. PNAS U S A 109(23):8866-8871.
13. Danese A, Moffitt TE, Harrington H, Milne BJ, Polanczyk G, Pariante CM, Poulton R, Caspi A. 2009. Adverse childhood experiences and adult risk factors for age-related disease: Depression, inflammation, and clustering of metabolic risk markers. Arch Pediatr Adolesc Med 163(12):1135-1143.
14. Essex MJ, Thomas Boyce W, Hertzman C, Lam LL, Armstrong JM, Neumann S, Kobor MS. 2013. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Develop 84:58-75.
15. Fairbanks L, McGuire M. 1988. Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Develop Psychobiol 21:711-724.
16. Fairbanks LA, McGuire MT.1995. Maternal condition and the quality of maternal care in vervet monkeys. Behaviour 132: 733-754.
17. Franklin TB, Russig H, Weiss IC, Gráff J, Linder N, Michalon A, Vizi S, Mansuy IM. 2010. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 68(5):408-415.
18. Giannaccini G, Betti L, Palego L, Marsili A, Santini F, Pelosini C, Lucacchini A. 2013. The expression of platelet serotonin transporter (SERT) in human obesity. BMC Neurosci 14:128.
19. Harlow H, Zimmerman RR. 1959. Affectional responses in the infant monkey; orphaned baby monkeys develop a strong and persistent attachment to inanimate surrogate mothers. Science 130:421-432.
20. Hofer MA. 1970. Environmental influences on the early development of autonomic cardiac regulation in the rat. Psychother Psychosomat Med 18:243-247.
21. Ichise M, Vines D, Gura T, Anderson G, Suomi S, Higley J, Innis RB. 2006. Effects of early life stress on [11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- And mother-reared rhesus monkeys. J Neurosci 26:4638-4643.
22. Jahng J, Kim J, Kim H, Kim B, Kang D, Lee J. 2007. Chronic food restriction in young rats results in depression- And anxiety-like behaviors with decreased expression of serotonin reuptake transporter. Brain Res 1150:100-107.
23. Kinnally E, Lyons L, Abel K, Mendoza S, Capitanio, J. 2008. Effects of early experience and genotype on serotonin transporter regulation in infant rhesus macaques. Genes Brain Behav 7:481-486.
24. Kinnally EL, Capitanio JP, Leibel R, Deng L, LeDuc C, Haghighi F, Mann JJ. 2010a. Epigenetic regulation of serotonin transporter expression and behavior in infant rhesus macaques. Genes Brain Behav 9:575-582.
25. Kinnally EL, Tarara ER, Abel K, Mendoza SP, Lyons LA, Mason WA, Capitanio JP. 2010b. Serotonin transporter expression is influenced by early life stress and predicts disinhibited behavior in infant rhesus macaques. Genes Brain Behav 9:45-52.
26. Klaus, HD, Tam ME. 2009. Contact in the Andes: bioarchaeology of systemic stress in Colonial Mórrope, Peru. Am J Phys Anthropol 138(3):356-368.
27. Larsen CS. 1987. Bioarchaeological interpretations of subsistence economy and behavior from human skeletal remains. Advances in archaeological method and theory 339-445.
28. Lee JH, Kim HJ, Kim JG, Ryu V, Kim, BT, Kang DW, Jahng JW. 2007. Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58:32-39.
29. Lyons D, Mendoza S, Mason W. 1992. Sexual segregation in squirrel monkeys (Saimiri sciureus): A transactional analysis of adult social dynamics. J Comparat Psychol 106:323-330.
30. Macchi F, Homberg JR, Calabrese F, Zecchillo C, Racagni G, Riva MA, Molteni R. 2013. Altered inflammatory responsiveness in serotonin transporter mutant rats. J Neuroinflammation 10:116.
31. Mason W, Mendoza S. 1998. Generic aspects of primate attachments: parents, offspring and mates. Psychoneuroendocrinology 23:765-778.
32. McCormack K, Sanchez M, Bardi M, Maestripieri D. 2006. Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Develop Psychobiol 48:537-550.
33. McDade TW, Hoke M, Borja JB, Adair LS, Kuzawa, C. 2013. Do environments in infancy moderate the association between stress and inflammation in adulthood? Initial evidence from a birth cohort in the Philippines. Brain Behav Immun 31:23- 30.
34. McGowan PO, Sasaki AC, D'Alessio A, Dymov S, Labonté B, Szyf M, Turecki G, Meaney MJ. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12(3):342-348.
35. Maestripieri D, Higley JD, Lindell S, Newman T, McCormack K, Sanchez M. 2006. Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta). Behav Neurosci 120:1017-1024.
36. Maestripieri D, Wallen K, Carroll K. 1997. Infant abuse runs in families of group-living pigtail macaques. Child Abuse Neglect 21:465-471.
37. Meaney MJ. 2010. Epigenetics and the biological definition of gene3 environment interactions. Child Develop 81:41-79.
38. Miller J, Kinnally E, Ogden R, Oquendo M, Mann JJ, Parsey R. 2009. Reported childhood abuse is associated with low serotonin transporter binding in vivo in major depressive disorder. Synapse 63:565-573.
39. Mulligan CJ. 2012. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 7:853-857.
40. Oberlander T, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin A. 2008. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3: 97-106.
41. Philibert RA, Sandhu H, Hollenbeck N, Gunter T, Adams W, Madan A. 2008. The relationship of 5HTT (SLC6A4) methylation and genotype on mRNA expression and liability to major depression and alcohol dependence in subjects from the Iowa Adoption Studies. Am J Med Genet B Neuropsychiatr Genetics 147:543-549.
42. Provençal N, Suderman MJ, Caramaschi D, Wang D, Hallett M, Vitaro F, Tremblay RE, Szyf M. 2013. Differential DNA methylation regions in cytokine and transcription factor genomic loci associate with childhood physical aggression. PLoS One 8(8):e71691.
43. Rosenblum L, Paully G. 1984. The effects of varying environmental demands on maternal and infant behavior. Child Develop 55:305-314.
44. Roth TL, Lubin FD, Funk AJ, Sweatt JD. 2009. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 65:760-769.
45. Shinozaki G, Romanowicz M, Kung S, Rundell J, Mrazek D. 2012. Investigation of serotonin transporter gene (SLC6A4) by child abuse history interaction with body mass index and diabetes mellitus of White female depressed psychiatric inpatients. Psychiatr Genet 22:109-114.
46. Stevenson-Hinde J, Simpson M. 1986. Mothers' characteristics, interactions, and infants' characteristics. Child Develop 52: 1246-1254.
47. Tost J, Gut I. 2007. DNA methylation analysis by pyrosequencing. Nature Protocols, 2(9), 2265-2275.
48. Unternaehrer E, Luers P, Mill J, Dempster E, Meyer AH, Staehli S, Meinlschmidt G. 2012. Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF) after acute psychosocial stress. Translational Psychiatry 2:e150.
49. Wang D, Szyf M, Benkelfat C, Provençal N, Turecki G, Caramaschi D, Booij L. 2012. Peripheral SLC6A4 DNA methylation is associated with in vivo measures of human brain serotonin synthesis and childhood physical aggression. PloS One 7:e39501.
50. Weaver I, Cervoni N, Champagne F, D'Alessio A, Sharma S, Seckl J, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
51. Wegman HL, Stetler C. 2009. A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosomat Med 71:805-812.
52. Wendelbo I, Mazzawi T, El-Salhy M. 2014. Increased serotonin transporter immunoreactivity intensity in the ileum of patients with irritable bowel disease. Mol Med Rep 9(1):180- 184.
53. Wheeler SM, Williams L, Beauchesne P, Dupras TL. 2013. Shattered lives and broken childhoods: evidence of physical child abuse in ancient Egypt. Int J Paleopathol 3:71-81.