Litter and sex effects on maternal behavior and DNA methylation of the Nr3c1 exon 17 promoter gene in hippocampus and cerebellum

International Journal of Developmental Neuroscience

Volumn 36, Issue , 2014, Pages 5-12

  Kosten, Therese A ^a   Nielsen, David A ^a  

^a MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Epigenetics; Female; Glucocorticoid receptors; MRNA; Sex differences

Indexed keywords

GLUCOCORTICOID RECEPTOR; MESSENGER RNA; NR3C1 PROTEIN, RAT;

ADULT; ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; CEREBELLUM; DNA METHYLATION; EXON; FEMALE; HIPPOCAMPUS; JUVENILE ANIMAL; LICKING; MALE; MATERNAL BEHAVIOR; NONHUMAN; NR3C1 GENE; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; PYROSEQUENCING; RAT; SEX RATIO; AGE; ANIMAL; BODY SIZE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; MOTHER CHILD RELATION; NEWBORN; PHYSIOLOGY; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BODY SIZE; CEREBELLUM; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; MALE; MATERNAL BEHAVIOR; MOTHER-CHILD RELATIONS; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; SEX CHARACTERISTICS;

EID: 84900835030     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2014.03.010     Document Type: Article

References (79)

1. Ahima R.S., Harlan R.E. Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience 1990, 39:579-604.
2. Alleva E., Caprioli A., Laviola G. Litter gender composition affects maternal behavior of the primiparous mouse dam (Mus musculus). Journal of Comparative Psychology 1989, 103:83-87.
3. Alt S.R., Turner J.D., Klok M.D., Meijer O.C., Lakke E.A., Derijk R.H., Muller C.P. Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology 2010, 35:544-556.
4. Applied_Biosystems User Bulletin #2: ABI Prism 7700 sequence detection system, relative quantitation of gene expression 2001.
5. Avishai-Eliner S., Hatalski C.G., Tabachnik E., Eghbal-Ahmadi M., Baram T.Z. Differential regulation of glucocorticoid receptor messenger RNA (GR-mRNA) by maternal deprivation in immature rat hypothalamus and limbic regions. Brain Research Developmental Brain Research 1999, 114:265-268.
6. Baker-Andresen D., Ratnu V.S., Bredy T.W. Dynamic DNA methylation: a prime candidate for genomic metaplasticity and behavioral adaptation. Trends in Neurosciences 2013, 36:3-13.
7. Beatty W.W., Beatty P.A. Hormonal determinants of sex differences in avoidance behavior and reactivity to electric shock in the rat. Journal of Comparative and Physiological Psychology 1970, 73:446-455.
8. Champagne F., Meaney M.J. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Progress in Brain Research 2001, 133:287-302.
9. Champagne F.A., Curley J.P. Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neuroscience and Biobehavioral Reviews 2009, 33:593-600.
10. 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. Physiology & Behavior 2003, 79:359-371.
11. Champagne F.A., Weaver I.C.G., Diorio J., Dymov S., Szyf M., Meaney M.J. Maternal care associated with methylation of the estrogen receptor-a1b promoter and estrogen receptor-a expression in the medial preoptic area of female offspring. Endocrinology 2006, 147:2909-2915.
12. Chen J., Evans A.N., Liu Y., Honda M., Saavedra J.M., Aguilera G. Maternal deprivation in rats is associated with corticotrophin-releasing hormone (CRH) promoter hypomethylation and enhances CRH transcriptional responses to stress in adulthood. Journal of Neuroendocrinology 2012, 24:1055-1064.
13. Chen M., Xiong F., Zhang L. Promoter methylation of Egr-1 site contributes to fetal hypoxia-mediated PKCe{open} gene repression in the developing heart. American Journal of Physiology: Regul Inegr Comp Physiol 2013, 304:R683-R689.
14. Christian K.M., Thompson R.F. Neural substrates of eyeblink conditioning: acquisition and retention. Learning and Memory 2003, 11:427-455.
15. Cirulli F., Adriani W., Laviola G. Sexual segregation in infant mice: behavioural and neuroendocrine responses to d-amphetamine administration. Psychopharmacology 1997, 134:140-152.
16. Cordero M.I., Venero C., Kruyt N.D., Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats: evidence for a role of corticosterone. Hormones and Behavior 2003, 44:338-345.
17. 7 glucocorticoid receptor promotor region. Metabolic Brain Disease 2009, 24:615-627.
18. deJongh R., Geyer M.A., Olivier B., Groenink L. The effects of sex and neonatal maternal separation on fear-potentiated and light-enhanced startle. Behavioural Brain Research 2005, 161:190-196.
19. Dudley K.J., Li X., Kobor M.S., Kippin T.E., Bredy T.W. Epigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders. Neuroscience and Biobehavioral Reviews 2011, 35:1544-1551.
20. Edelmann M.N., Auger A.P. Epigenetic impact of simulated maternal grooming on estrogen receptor alpha within the developing amygdala. Brain, Behavior, and Immunity 2011, 25:1299-1304.
21. Fombonne E. Epidemiological surveys of autism and other pervasive developmental disorders: an update. Journal of Autism and Developmental Disorders 2003, 33:365-382.
22. Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Current Opinion in Neurobiology 1999, 9:128-134.
23. Francis D.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.
24. Goel N., Bale T.L. Examining the intersection of sex and stress in modelling neuropsychiatric disorders. Journal of Neuroendocrinology 2009, 21:415-420.
25. Gordon H.W. Early environmental stress and biological vulnerability to drug abuse. Psychoneuroendocrinology 2002, 27:115-126.
26. Grant B.F., Goldstein R.B., Chou S.P., Huang B., Stinson F.S., Dawson D.A., Saha T.D., Smith S.M., Pulay A.J., Pickering R.P., Ruan W.J., Compton W.M. Sociodemographic and psychopathologic predictors of first incidence of DSM-IV substance use, mood and anxiety disorders: results from the Wave 2 National Epidemiologic Survey on Alcohol and Related Conditions. Molecular Psychiatry 2009, 14:1051-1066.
27. Grota L.J., Ader R. Continuous recording of maternal behavior in Rattus norvegicus. Animal Behavior 1969, 17:722-729.
28. Hao Y., Huang W., Nielsen D.A., Kosten T.A. Litter gender composition and sex affect maternal behavior and DNA methylation levels of the Oprm1 gene in rat offspring. Frontiers in Child and Neurodevelopmental Psychiatry 2011, 2(Article 21):12-21.
29. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biological Psychiatry 2001, 49:1023-1039.
30. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamic-pituitary-adrenocortical axis. Trends in Neurosciences 1997, 20:78-84.
31. Howes O.D., McDonald C., Cannon M., Arseneault L., Boydell J., Murray R.M. Pathways to schizophrenia: the impact of environmental factors. International Journal of Neuropsychopharmacology 2004, 7:S7-S13.
32. Hwang C.K., Kim C.S., Kim K., Law P.Y., Wei L.N., Loh H.H. Up-regulation of the mu-opioid receptor gene is mediated through chromatin remodeling and transcriptional factors in differentiated neuronal cells. Molecular Pharmacology 2010, 78:58-68.
33. Jessen H.M., Auger A.P. Sex differences in epigenetic mechanisms may underlie risk and resilience for mental health disorders. Epigenetics 2011, 6:857-861.
34. Jones P.A., Taylor S.M. Cellular differentiation, cytidine analogs and DNA methylation. Cell 1980, 20:85-93.
35. Kim J.J., Song E.Y., Kosten T.A. Stress effects in the hippocampus: synaptic plasticity and memory. Stress 2006, 9:1-11.
36. Kitraki E., Karandrea D., Kittas C. Long-lasting effects of stress on glucocorticoid receptor gene expression in rat brain. Neuroendocrinology 1999, 69:331-338.
37. Kosten T.A., Kehoe P. The immediate and enduring effects of neonatal isolation on maternal behavior in rats. International Journal of Developmental Neuroscience 2010, 28:53-61.
38. Kosten T.A., Lee H.J., Kim J.J. Early life stress impairs fear conditioning in adult male and female rats. Brain Research 2006, 1087:142-150.
39. Kosten T.A., Huang W., Nielsen D.A. Sex and litter effects on anxiety and DNA methylation levels of stress and neurotrophin genes in adolescent rats. Developmental Psychobiology 2014, 56:392-406.
40. Kosten T.A., Miserendino M.J.D., Bombace J.C., Lee H.J., Kim J.J. Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity. Behavioural Brain Research 2005, 157:235-244.
41. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biological Psychiatry 2005, 69:113-132.
42. 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.
43. 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.
44. Marmendal M., Roman E., Eriksson C.J.P., Nylander I., Fahlke C. Maternal separation alters maternal care, but has minor effects on behavior and brain opioid peptides in adult offspring. Developmental Psychobiology 2004, 45:140-152.
45. McCormick J.A., Lyons V., Jacobson M.D., Nobe J., Biorio J., Nyirenda M., Weaver S., Ester W., Yau J.L., Meaney M.J., Seckl J.R., Chapman K.E. 5'-heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Molecular Endocrinology 2000, 14:506-517.
46. McEwen B.S. Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiology of Aging 2002, 23:921-939.
47. McGowan P.O., Suderman M., Sasaki A., Huang T.C. Broad epigenetic signature of maternal care in the brain of adult rats. PLoS 2011, 28:e14739.
48. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labone B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience 2009, 12:342-348.
49. McIntosh J., Anisman H., Merali Z. Short- and long-period of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Research Developmental Brain Research 1999, 113:91-106.
50. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 2001, 24:1161-1192.
51. Moore C.L., Morelli G.A. Mother rats interact differently with male and female offspring. Journal of Comparative and Physiological Psychology 1979, 93:667-684.
52. Moore C.L., Chadwick-Dias A.M. Behavioral responses of infant rats to maternal licking: variations with age and sex. Developmental Psychobiology 1986, 19:427-438.
53. Morimoto M., Morita N., Ozawa H., Yokoyama K. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neuroscience Research 1996, 26:235-269.
54. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience 2008, 28:9055-9065.
55. Nielsen D.A., Yuferov V., Hamon S., Jackson C., Ho A., Ott J., Kreek M.J. Increased OPRM1 DNA methylation in lymphocytes of methadone-maintained former heroin addicts. Neuropsychopharmacology 2009, 34:867-873.
56. Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
57. Pryce C.R., Bettschen D., Feldon J. Comparison of the effects of early handling and early deprivation on maternal care in the rat. Developmental Psychobiology 2001, 38:239-251.
58. Pryce C.R., Bettschen D., Nanz-Bahr N.I., Feldon J. Comparison of the effects of early handling and early deprivation on conditioned stimulus, context, and spatial learning and memory in adult rats. Behavioral Neuroscience 2003, 117:883-893.
59. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 1998, 17:4905-4908.
60. Reed K., Poulin M.L., Yan L., Parissenti A.M. Comparison of bisulfite sequencing PCR with pyrosequencing for measuring differences in DNA methylation. Analytical Biochemistry 2010, 397:96-106.
61. Richmond G., Sachs B.D. Maternal discrimination of pup sex in rats. Developmental Psychobiology 1984, 17:87-89.
62. Rivier C. Gender, sex steroids, corticotropin-releasing factor, nitric oxide, and the HPA response to stress. Pharmacology, Biochemistry and Behavior 1999, 64:739-751.
63. Roth T.L., Lubin F.D., Funk A.J., Sweatt J.D. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry 2009, 65:760-769.
64. Schug J., Overton G.C. TESS: Transcription Element Search Software on the http://www.cbil.upenn.edu/cgi-bin/tess/tess 1977, Computational Biology and Informatics Library, University of Pennsylvania.
65. Shiao Y.H., Crawford E.B., Anderson L.M., Patel P., Ko K. Allele-specific germ cell epimutation in the space promoter of the 45S ribosomal RNA gene after Cr(III) exposure. Toxicology and Applied Pharmacology 2005, 205. 209-209.
66. Shors T.J., Beylin A.V., Wood G.E., Gould E. The modulation of Pavlovian memory. Behavioural Brain Research 2000, 110:39-52.
67. Sousa R.J., Tannery N.H., Lafer E.M. In situ hybridization mapping of glucocorticoid receptor messenger ribonucleic acid in rat brain. Molecular Endocrinology 1989, 3:481-494.
68. Steinmetz J.E. Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behavioural Brain Research 2000, 110:13-24.
69. Sutanto W., Rosenfeld P., deKloet E.R., Levine S. Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors. Developmental Brain Research 1996, 92:156-164.
70. Thomassin H., Flavin M., Espinas M.L., Grange T. Glucocorticoid-induced DNA demethylation and gene memory during development. The EMBO Journal 2001, 20:1974-1983.
71. vanHasselt F.N., Cornelisse S., Zhang T.Y., Meaney M.J., Velzing E.H., Krugers H.J., Joels 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.
72. Vigod S.N., Stewart D.E. Emergent research in the cause of mental illness in women across the lifespan. Current Opinion in Psychiatry 2009, 22:396-400.
73. Vucetic Z., Kimmel J., Totoki K., Hollenbeck E., Reyes T.M. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 2010, 151:4756-4764.
74. Weaver I.C., Champagne F.A., Brown S.E., Dymov S., Sharma S., Meaney M.J., Szyf M. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. Journal of Neuroscience 2005, 25:11045-11054.
75. Weaver I.C., 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. Nature Neuroscience 2004, 7:847-854.
76. Wigger A., Neumann I.D. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiology & Behavior 1999, 66:293-302.
77. Wilber A.A., Southwood C.J., Sokoloff G., Steinmetz J.E., Wellman C.L. Neonatal maternal separation alters adult eyeblink conditioning and glucocorticoid receptor expression in the interpositus nucleus of the cerebellum. Developmental Neurobiology 2007, 67:1751-1764.
78. Wood G.E., Shors T.J. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proceedings of the National Academy of Science 1998, 95:4066-4071.
79. Yehuda R., Halligan S.L., Grossman R. Childhood trauma and risk for PTSD: relationship to intergenerational effects of trauma, parental PTSD, and cortisol excretion. Development & Psychopathology 2001, 13:733-753.