Natural variation in maternal care and cross-tissue patterns of oxytocin receptor gene methylation in rats

Hormones and Behavior

Volumn 77, Issue , 2016, Pages 42-52

  Beery, Annaliese K ^a,b   McEwen, Lisa M ^c   MacIsaac, Julia L ^c   Francis, Darlene D ^b   Kobor, Michael S ^c  

^a SMITH COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Anxiety behavior; Concordance; Cross tissue; DNA methylation; Epigenetic; Maternal care; Natural variation; Oxtr; Oxytocin; Oxytocin receptor

Indexed keywords

CORTICOSTERONE; DNA; MESSENGER RNA; OXYTOCIN RECEPTOR; OXYTOCIN; OXYTOCIN RECEPTOR, RAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; BODY MASS; BRAIN; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOSTERONE RELEASE; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENETIC REGULATION; GENETIC VARIABILITY; GROOMING; HIPPOCAMPUS; HYPOTHALAMUS; LICKING; MALE; NATURAL VARIATION; NONHUMAN; OXTR GENE; PRIORITY JOURNAL; REARING; SIGNAL TRANSDUCTION; STRESS; ANIMAL; ANIMAL BEHAVIOR; GENETIC EPIGENESIS; GENETICS; LONG EVANS RAT; MATERNAL BEHAVIOR; METABOLISM; PHYSIOLOGY; RAT;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; MALE; MATERNAL BEHAVIOR; OXYTOCIN; RATS; RATS, LONG-EVANS; RECEPTORS, OXYTOCIN;

EID: 84956582102     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.05.022     Document Type: Article

References (105)

1. Anacker A.M.J., Beery A.K. Life in groups: the roles of oxytocin in mammalian sociality. Front. Behav. Neurosci. 2013, 7:185. 10.3389/fnbeh.2013.00185.
2. Aragona B.J., Wang Z. Dopamine regulation of social choice in a monogamous rodent species. Front. Behav. Neurosci. 2009, 3. 10.3389/neuro.08.015.2009.
3. Bachman M., Uribe-Lewis S., Yang X., Williams M., Murrell A., Balasubramanian S. 5-Hydroxymethylcytosine is a predominantly stable DNA modification. Nat. Chem. 2014, 6:1049-1055. 10.1038/nchem.2064.
4. Bale T.L., Davis A.M., Auger A.P., Dorsa D.M., McCarthy M.M. CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J. Neurosci. 2001, 21:2546-2552.
5. Bales K.L., Perkeybile A.M. Developmental experiences and the oxytocin receptor system. Horm. Behav. 2012, 61:313-319. 10.1016/j.yhbeh.2011.12.013.
6. Beery A.K., Francis D.D. Adaptive significance of natural variations in maternal care in rats: a translational perspective. Neurosci. Biobehav. Rev. 2011, 35:1552-1561. 10.1016/j.neubiorev.2011.03.012.
7. Beery A.K., Kaufer D. Stress, social behavior, and resilience: insights from rodents. Neurobiol. Stress 2015, 1:116-127. 10.1016/j.ynstr.2014.10.004.
8. Beery A.K., Zucker I. Oxytocin and same-sex social behavior in female meadow voles. Neuroscience 2010, 169:665-673. 10.1016/j.neuroscience.2010.05.023.
9. Beery A.K., Lacey E.A., Francis D.D. Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J. Comp. Neurol. 2008, 507:1847-1859. 10.1002/cne.21638.
10. Beery A.K., Lin J., Biddle J.S., Francis D.D., Blackburn E.H., Epel E.S. Chronic stress elevates telomerase activity in rats. Biol. Lett. 2012, 8:1063-1066. 10.1098/rsbl.2012.0747.
11. Beery A.K., Vahaba D.M., Grunberg D.M. Corticotropin-releasing factor receptor densities vary with photoperiod and sociality. Horm. Behav. 2014, 66:779-786. 10.1016/j.yhbeh.2014.08.014.
12. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 1995, 289-300.
13. Branco M.R., Ficz G., Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 2012, 13:7-13. 10.1038/nrg3080.
14. Burton C.L., Chatterjee D., Chatterjee-Chakraborty M., Lovic V., Grella S.L., Steiner M., Fleming A.S. Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats. Brain Res. 2007, 1158:28-38. 10.1016/j.brainres.2007.05.003.
15. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5335-5340.
16. Cameron N., Del Corpo A., Diorio J., McAllister K., Sharma S., Meaney M.J. Maternal programming of sexual behavior and hypothalamic-pituitary-gonadal function in the female rat. PLoS One 2008, 3:e2210. 10.1371/journal.pone.0002210.
17. Cameron N., Fish E.W., Meaney M.J. Maternal influences on the sexual behavior and reproductive success of the female rat. Horm. Behav. 2008, 54:178-184. 10.1016/j.yhbeh.2008.02.013.
18. Carter C.S., Grippo A.J., Pournajafi-Nazarloo H., Ruscio M.G., Porges S.W. Oxytocin, vasopressin and sociality. Prog. Brain Res. 2008, 170:331-336. 10.1016/S0079-6123(08)00427-5.
19. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T.C., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229. 10.1126/science.1153252.
20. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003, 79:359-371.
21. Christensen B.C., Houseman E.A., Marsit C.J., Zheng S., Wrensch M.R., Wiemels J.L., Nelson H.H., Karagas M.R., Padbury J.F., Bueno R., Sugarbaker D.J., Yeh R.-F., Wiencke J.K., Kelsey K.T. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet. 2009, 5:e1000602. 10.1371/journal.pgen.1000602.
22. Dadds M.R., Moul C., Cauchi A., Dobson-Stone C., Hawes D.J., Brennan J., Ebstein R.E. Methylation of the oxytocin receptor gene and oxytocin blood levels in the development of psychopathy. Dev. Psychopathol. 2014, 26:33-40. 10.1017/S0954579413000497.
23. Davies M.N., Volta M., Pidsley R., Lunnon K., Dixit A., Lovestone S., Coarfa C., Harris R.A., Milosavljevic A., Troakes C., others Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol. 2012, 13:R43.
24. Denenberg V.H., Whimbey A.E. Behavior of adult rats is modified by the experiences their mothers had as infants. Science 1963, 142:1192-1193.
25. Dölen G., Darvishzadeh A., Huang K.W., Malenka R.C. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013, 501:179-184. 10.1038/nature12518.
26. Donaldson Z.R., Young L.J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 2008, 322:900-904. 10.1126/science.1158668.
27. Dumais K.M., Bredewold R., Mayer T.E., Veenema A.H. Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region- and sex-specific ways. Horm. Behav. 2013, 64:693-701. 10.1016/j.yhbeh.2013.08.012.
28. Farré P., Jones M.J., Meaney M.J., Emberly E., Turecki G., Kobor M.S. Concordant and discordant DNA methylation signatures of aging in human blood and brain. Epigenetics Chromatin 2015, 8:19. 10.1186/s13072-015-0011-y.
29. Fraga M.F., Ballestar E., Paz M.F., Ropero S., Setien F., Ballestar M.L., Heine-Suñer D., Cigudosa J.C., Urioste M., Benitez J., Boix-Chornet M., Sanchez-Aguilera A., Ling C., Carlsson E., Poulsen P., Vaag A., Stephan Z., Spector T.D., Wu Y.-Z.Z., Plass C., Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10604-10609. 10.1073/pnas.0500398102.
30. Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 1999, 9:128-134.
31. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286:1155-1158.
32. Francis D.D., Young L.J., Meaney M.J., Insel T.R. Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J. Neuroendocrinol. 2002, 14:349-353.
33. Gonzalez A., Lovic V., Ward G.R., Wainwright P.E., Fleming A.S. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev. Psychobiol. 2001, 38:11-32.
34. Goodson J.L. The vertebrate social behavior network: evolutionary themes and variations. Horm. Behav. 2005, 48:11-22. 10.1016/j.yhbeh.2005.02.003.
35. Gregory S.G., Connelly J.J., Towers A.J., Johnson J., Biscocho D., Markunas C.A., Lintas C., Abramson R.K., Wright H.H., Ellis P., Langford C.F., Worley G., Delong G.R., Murphy S.K., Cuccaro M.L., Persico A., Pericak-Vance M.A. Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Med. 2009, 7:62. 10.1186/1741-7015-7-62.
36. Guastella A.J., Macleod C. A critical review of the influence of oxytocin nasal spray on social cognition in humans: evidence and future directions. Horm. Behav. 2012, 61:410-418. 10.1016/j.yhbeh.2012.01.002.
37. Guzmán Y.F., Tronson N.C., Jovasevic V., Sato K., Guedea A.L., Mizukami H., Nishimori K., Radulovic J. Fear-enhancing effects of septal oxytocin receptors. Nat. Neurosci. 2013, 16:1185-1187. 10.1038/nn.3465.
38. Hackett J.A., Sengupta R., Zylicz J.J., Murakami K., Lee C., Down T.A., Surani M.A. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 2013, 339:448-452. 10.1126/science.1229277.
39. Harony-Nicolas H., Mamrut S., Brodsky L., Shahar-Gold H., Barki-Harrington L., Wagner S. Brain region-specific methylation in the promoter of the murine oxytocin receptor gene is involved in its expression regulation. Psychoneuroendocrinology 2014, 39:121-131. 10.1016/j.psyneuen.2013.10.004.
40. Hertzman C., Boyce T. How experience gets under the skin to create gradients in developmental health. Annu. Rev. Public Health 2010, 31:329-347. 10.1146/annurev.publhealth.012809.103538.
41. Houde A.-A., Légaré C., Hould F.-S., Lebel S., Marceau P., Tchernof A., Vohl M.-C., Hivert M.-F., Bouchard L. Cross-tissue comparisons of leptin and adiponectin: DNA methylation profiles. Adipocytes 2014, 3:132-140. 10.4161/adip.28308.
42. Insel T.R., Young L.J. Neuropeptides and the evolution of social behavior. Curr. Opin. Neurobiol. 2000, 10:784-789.
43. Iwasaki S., Inoue K., Kiriike N., Hikiji K. Effect of maternal separation on feeding behavior of rats in later life. Physiol. Behav. 2000, 70:551-556.
44. Iyer P., Zekri A.-R., Hung C.-W., Schiefelbein E., Ismail K., Hablas A., Seifeldin I.A., Soliman A.S. Concordance of DNA methylation pattern in plasma and tumor DNA of Egyptian hepatocellular carcinoma patients. Exp. Mol. Pathol. 2010, 88:107-111. 10.1016/j.yexmp.2009.09.012.
45. Jack A., Connelly J.J., Morris J.P. DNA methylation of the oxytocin receptor gene predicts neural response to ambiguous social stimuli. Front. Hum. Neurosci. 2012, 6. 10.3389/fnhum.2012.00280.
46. Jiang R., Jones M.J., Chen E., Neumann S.M., Fraser H.B., Miller G.E., Kobor M.S. Discordance of DNA methylation variance between two accessible human tissues. Sci. Rep. 2015, 5:8257. 10.1038/srep08257.
47. Kimura T., Saji F., Nishimori K., Ogita K., Nakamura H., Koyama M., Murata Y. Molecular regulation of the oxytocin receptor in peripheral organs. J. Mol. Endocrinol. 2003, 30:109-115. 10.1677/jme.0.0300109.
48. Kirsch P., Esslinger C., Chen Q., Mier D., Lis S., Siddhanti S., Gruppe H., Mattay V.S., Gallhofer B., Meyer-Lindenberg A. Oxytocin modulates neural circuitry for social cognition and fear in humans. J. Neurosci. 2005, 25:11489-11493. 10.1523/JNEUROSCI.3984-05.2005.
49. Knobloch H.S., Charlet A., Hoffmann L.C., Eliava M., Khrulev S., Cetin A.H., Osten P., Schwarz M.K., Seeburg P.H., Stoop R., Grinevich V. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 2012, 73:553-566. 10.1016/j.neuron.2011.11.030.
50. Kumsta R., Hummel E., Chen F.S., Heinrichs M. Epigenetic regulation of the oxytocin receptor gene: implications for behavioral neuroscience. Front. Neurosci. 2013, 7:83. 10.3389/fnins.2013.00083.
51. Kurian J.R., Olesen K.M., Auger A.P. Sex differences in epigenetic regulation of the estrogen receptor-alpha promoter within the developing preoptic area. Endocrinology 2010, 151:2297-2305. 10.1210/en.2009-0649.
52. Kusui C., Kimura T., Ogita K., Nakamura H., Matsumura Y., Koyama M., Azuma C., Murata Y. DNA methylation of the human oxytocin receptor gene promoter regulates tissue-specific gene suppression. Biochem. Biophys. Res. Commun. 2001, 289:681-686. 10.1006/bbrc.2001.6024.
53. Lam L.L., Emberly E., Fraser H.B., Neumann S.M., Chen E., Miller G.E., Kobor M.S. Factors underlying variable DNA methylation in a human community cohort. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17253-17260. 10.1073/pnas.1121249109.
54. Langevin S.M., Koestler D.C., Christensen B.C., Butler R.A., Wiencke J.K., Nelson H.H., Houseman E.A., Marsit C.J., Kelsey K.T. Peripheral blood DNA methylation profiles are indicative of head and neck squamous cell carcinoma: an epigenome-wide association study. Epigenetics 2012, 7:291-299. 10.4161/epi.7.3.19134.
55. Lenz K.M., Sengelaub D.R. Maternal care effects on the development of a sexually dimorphic motor system: the role of spinal oxytocin. Horm. Behav. 2010, 58:575-581. 10.1016/j.yhbeh.2010.07.010.
56. Liberman S.A., Mashoodh R., Thompson R.C., Dolinoy D.C., Champagne F.A. Concordance in hippocampal and fecal Nr3c1 methylation is moderated by maternal behavior in the mouse. Ecol. Evol. 2012, 2:3123-3131. 10.1002/ece3.416.
57. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
58. Liu J., Morgan M., Hutchison K., Calhoun V.D. A study of the influence of sex on genome wide methylation. PLoS One 2010, 5:e10028. 10.1371/journal.pone.0010028.
59. Lukas M., Bredewold R., Neumann I.D., Veenema A.H. Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 2010, 58:78-87. 10.1016/j.neuropharm.2009.06.020.
60. Lukas M., Toth I., Veenema A.H., Neumann I.D. Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 2013, 38:916-926. 10.1016/j.psyneuen.2012.09.018.
61. Macciò A., Madeddu C., Chessa P., Panzone F., Lissoni P., Mantovani G. Oxytocin both increases proliferative response of peripheral blood lymphomonocytes to phytohemagglutinin and reverses immunosuppressive estrogen activity. In Vivo 2010, 24:157-163.
62. Mamrut S., Harony H., Sood R., Shahar-Gold H., Gainer H., Shi Y.-J.J., Barki-Harrington L., Wagner S. DNA methylation of specific CpG sites in the promoter region regulates the transcription of the mouse oxytocin receptor. PLoS One 2013, 8:e56869. 10.1371/journal.pone.0056869.
63. McCarthy N.S., Melton P.E., Cadby G., Yazar S., Franchina M., Moses E.K., Mackey D.A., Hewitt A.W. Meta-analysis of human methylation data for evidence of sex-specific autosomal patterns. BMC Genomics 2014, 15:981. 10.1186/1471-2164-15-981.
64. McEwen B.S. Brain on stress: how the social environment gets under the skin. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(Suppl. 2):17180-17185. 10.1073/pnas.1121254109.
65. McGowan P.O., Suderman M., Sasaki A., Huang T.C.T., Hallett M., Meaney M.J., Szyf M. Broad epigenetic signature of maternal care in the brain of adult rats. PLoS One 2011, 6:e14739. 10.1371/journal.pone.0014739.
66. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192. 10.1146/annurev.neuro.24.1.1161.
67. Miller C.A., Gavin C.F., White J.A., Parrish R.R., Honasoge A., Yancey C.R., Rivera I.M., Rubio M.D., Rumbaugh G., Sweatt J.D. Cortical DNA methylation maintains remote memory. Nat. Neurosci. 2010, 13:664-666. 10.1038/nn.2560.
68. Ndiaye K., Poole D.H., Pate J.L. Expression and regulation of functional oxytocin receptors in bovine T lymphocytes. Biol. Reprod. 2008, 78:786-793. 10.1095/biolreprod.107.065938.
69. Neumann I.D., Landgraf R. Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 2012, 35:649-659. 10.1016/j.tins.2012.08.004.
70. Neumann I., Wigger A., Abbott L., Holsboer F., Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J. Neuroendocrinol. 2000, 12:235-243. 10.1046/j.1365-2826.2000.00442.x.
71. Newman S.W. The medial extended amygdala in male reproductive behavior a node in the mammalian social behavior network. Ann. N. Y. Acad. Sci. 1999, 877:242-257.
72. Nicholson A.C., Unger E.R., Mangalathu R., Ojaniemi H., Vernon S.D. Exploration of neuroendocrine and immune gene expression in peripheral blood mononuclear cells. Mol. Brain Res. 2004, 129:193-197. 10.1016/j.molbrainres.2004.06.036.
73. O'Connell L.A., Hofmann H.A. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 2011, 519:3599-3639. 10.1002/cne.22735.
74. Olazábal D.E., Young L.J. Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 2006, 141:559-568. 10.1016/j.neuroscience.2006.04.017.
75. Ophir A.G., Gessel A., Zheng D.-J., Phelps S.M. Oxytocin receptor density is associated with male mating tactics and social monogamy. Horm. Behav. 2012, 61:445-453. 10.1016/j.yhbeh.2012.01.007.
76. Owen S.F., Tuncdemir S.N., Bader P.L., Tirko N.N., Fishell G., Tsien R.W. Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 2013, 500:458-462. 10.1038/nature12330.
77. 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. 2014, 128:736-748. 10.1037/bne0000014.
78. Parent C.I., Meaney M.J. The influence of natural variations in maternal care on play fighting in the rat. Dev. Psychobiol. 2008, 50:767-776. 10.1002/dev.20342.
79. Parent C.I., Del Corpo A., Cameron N.M., Meaney M.J. Maternal care associates with play dominance rank among adult female rats. Dev. Psychobiol. 2013, 55:745-756. 10.1002/dev.21070.
80. Phelps S.M., Campbell P., Zheng D.-J., Ophir A.G. Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharmacology 2010, 58:17-28. 10.1016/j.neuropharm.2009.06.043.
81. Puglia M.H., Lillard T.S., Morris J.P., Connelly J.J. Epigenetic modification of the oxytocin receptor gene influences the perception of anger and fear in the human brain. Proc. Natl. Acad. Sci. U. S. A. 2015, 10.1073/pnas.1422096112.
82. Reiner I., Van IJzendoorn M.H., Bakermans-Kranenburg M.J., Bleich S., Beutel M., Frieling H. Methylation of the oxytocin receptor gene in clinically depressed patients compared to controls: the role of OXTR rs53576 genotype. J. Psychiatr. Res. 2015, 10.1016/j.jpsychires.2015.03.012.
83. Reinius L.E., Acevedo N., Joerink M., Pershagen G., Dahlén S.-E.E., Greco D., Söderhäll C., Scheynius A., Kere J. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One 2012, 7:e41361. 10.1371/journal.pone.0041361.
84. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30:534-547. 10.1016/j.yfrne.2009.05.004.
85. Roth T.L., Lubin F.D., Funk A.J., Sweatt J.D. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol. Psychiatry 2009, 65:760-769. 10.1016/j.biopsych.2008.11.028.
86. Sakhai S.A., Kriegsfeld L.J., Francis D.D. Maternal programming of sexual attractivity in female Long Evans rats. Psychoneuroendocrinology 2011, 36:1217-1225. 10.1016/j.psyneuen.2011.02.016.
87. Shahrokh D.K., Zhang T.-Y.Y., Diorio J., Gratton A., Meaney M.J. Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 2010, 151:2276-2286. 10.1210/en.2009-1271.
88. Siegmund K.D., Connor C.M., Campan M., Long T.I., Weisenberger D.J., Biniszkiewicz D., Jaenisch R., Laird P.W., Akbarian S. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2007, 2:e895. 10.1371/journal.pone.0000895.
89. Smith A.S., Wang Z. Hypothalamic oxytocin mediates social buffering of the stress response. Biol. Psychiatry Neurobiol. Moderators Stress Response 2014, 76:281-288. 10.1016/j.biopsych.2013.09.017.
90. Starr-Phillips E.J., Beery A.K. Natural variation in maternal care shapes adult social behavior in rats. Dev. Psychobiol. 2014, 56:1017-1026. 10.1002/dev.21182.
91. Stenz L., Zewdie S., Laforge-Escarra T., Prados J., La Harpe R., Dayer A., Paoloni-Giacobino A., Perroud N., Aubry J.-M. BDNF promoter I methylation correlates between post-mortem human peripheral and brain tissues. Neurosci. Res. 2014, 10.1016/j.neures.2014.10.003.
92. Suomi S.J. Developmental trajectories, early experiences, and community consequences: lessons from studies with rhesus monkeys. Developmental Health and the Wealth of Nations: Social, Biological, and Educational Dynamics 1999, 185-200. Guilford Press, New York, NY, US. D.P. Keating, C. Hertzman (Eds.).
93. Tribollet E., Dubois-Dauphin M., Dreifuss J.J., Barberis C., Jard S. Oxytocin receptors in the central nervous system. Distribution, development, and species differences. Ann. N. Y. Acad. Sci. 1992, 652:29-38.
94. Unternaehrer E., Luers P., Mill J., Dempster E., Meyer A.H., Staehli S., Lieb R., Hellhammer D.H., Meinlschmidt G. Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF) after acute psychosocial stress. Transl. Psychiatry 2012, 2:e150. 10.1038/tp.2012.77.
95. Van Hasselt F.N., Cornelisse S., Zhang T.Y., Meaney M.J., Velzing E.H., Krugers H.J., Joëls M. Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus 2012, 22:255-266. 10.1002/hipo.20892.
96. Van Hasselt F.N., Tieskens J.M., Trezza V., Krugers H.J., Vanderschuren L.J.M.J., Joëls M. Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. Physiol. Behav. 2012, 106:701-706. 10.1016/j.physbeh.2011.12.007.
97. Veenema A.H. Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors. Horm. Behav. 2012, 61:304-312. 10.1016/j.yhbeh.2011.12.002.
98. Walker C.-D.D., Xu Z., Rochford J., Johnston C.C. Naturally occurring variations in maternal care modulate the effects of repeated neonatal pain on behavioral sensitivity to thermal pain in the adult offspring. Pain 2008, 140:167-176. 10.1016/j.pain.2008.08.004.
99. Weaver I.C., La Plante P., Weaver S., Parent A., Sharma S., Diorio J., Chapman K.E., Seckl J.R., Szyf M., Meaney M.J. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Mol. Cell. Endocrinol. 2001, 185:205-218.
100. Weaver I.C.G., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854. 10.1038/nn1276.
101. Young L.J. Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors. Horm. Behav. 1999, 36:212-221. 10.1006/hbeh.1999.1548.
102. Young L.J., Muns S., Wang Z., Insel T.R. Changes in oxytocin receptor mRNA in rat brain during pregnancy and the effects of estrogen and interleukin-6. J. Neuroendocrinol. 1997, 9:859-865.
103. Yu G.Z., Kaba H., Okutani F., Takahashi S., Higuchi T. The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience 1996, 72:1083-1088.
104. Zhang T.Y., Chrétien P., Meaney M.J., Gratton A. Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. J. Neurosci. 2005, 25:1493-1502. 10.1523/JNEUROSCI.3293-04.2005.
105. Ziegler C., Dannlowski U., Bräuer D., Stevens S., Laeger I., Wittmann H., Kugel H., Dobel C., Hurlemann R., Reif A., Lesch K.-P., Heindel W., Kirschbaum C., Arolt V., Gerlach A.L., Hoyer J., Deckert J., Zwanzger P., Domschke K. Oxytocin receptor gene methylation: converging multilevel evidence for a role in social anxiety. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 2015, 10.1038/npp.2015.2.