Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care

Journal of Neuroendocrinology

Volumn 20, Issue 6, 2008, Pages 795-801

  Cameron, N M ^a   Shahrokh, D ^a   Del Corpo, A ^a   Dhir, S K ^a   Szyf, M ^a   Champagne, F A ^b   Meaney, Michael J ^b,c  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Estrogen receptor alpha; Female; Gonadotropin releasing; Hormone; Medial preoptic area; Oxytocin

Indexed keywords

DOPAMINE; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; GONADORELIN; JANUS KINASE; OXYTOCIN; OXYTOCIN RECEPTOR; PROGESTERONE; TESTOSTERONE;

BEHAVIOR GENETICS; CHILD PARENT RELATION; ESTROGEN BLOOD LEVEL; FETUS DEVELOPMENT; GENE EXPRESSION; GENETIC EPIGENESIS; HUMAN; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LACTATION; MATERNAL BEHAVIOR; MATERNAL CARE; MEDIAL PREOPTIC AREA; NEUROENDOCRINE SYSTEM; NONHUMAN; PERINATAL PERIOD; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROTEIN EXPRESSION; REPRODUCTION; REVIEW; SEXUAL BEHAVIOR;

ANIMALS; EPIGENESIS, GENETIC; ESTROGEN RECEPTOR ALPHA; FEMALE; MATERNAL BEHAVIOR; NEUROSECRETORY SYSTEMS; PHENOTYPE; RATS; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL;

EID: 45549085392     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2008.01725.x     Document Type: Review

References (75)

1. Goy RW, McEwen BS. Sexual Differentiation of the Brain. Cambridge: MIT Press, 1980.
2. McCarthy MM. Molecular aspects of sexual differentiation of the rodent brain. Psychoneuroendocinology 1994; 19: 415-427.
3. Breedlove SM, Hampson E. Sexual differentiation of brain and behavior. In: Becker JB, Breedlove SM, Crews D, McCarthy MM, eds. Behavioral Endocrinology. 2nd Edition. Cambridge, MA: MIT Press, 2002: 75-114.
4. Arnold AP. Sex chromosomes and brain gender. Nat Rev Neurosci 2004; 5: 701-708.
5. Gross MR. Alternative reproductive strategies and tactics: Diversity within sexes. Trends Ecol Evol 1996; 11: 92-98.
6. Rhen T, Crews D. Variation in reproduction behaviour within a sex: neural systems and endocrine activation. J Neuroendocrinol 2002; 14: 507-513.
7. West-Eberhard M. Developmental Plasticity and Evolution. Oxford, England: Oxford University Press, 2003.
8. Agrawal AA. Phenotypic plasticity in the interactions and evolution of species. Science 2001; 294: 321-326.
9. Qvarnstrom A, Price TD. Maternal effects, paternal effects and sexual selection. Trends Ecol Evol 2001; 16: 95-100.
10. Rossiter MC. The role of environmental variation in parental effects expression. In: Mousseau TA, Fox CW, eds. Maternal Effects as Adaptations. London: Oxford University Press, 1998; pp 112-133.
11. Mousseau TA, Fox CW. The adaptive significance of maternal effects. Trends Ecol Evol 1998; 13: 403-407.
12. Groothuis TGG, Muller W, von Engelhardt N, Carere C, Eising C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 2005; 29: 329-352.
13. Cameron NM, Parent C, Champagne FA, Fish EW, Ozaki-Kuroda K, Meaney MJ. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev 2005; 29: 843-865.
14. Hinde RA. Some implications of evolutionary theory and comparative data for the study of human prosocial and aggressive behaviour. In: Olweus D, Block J, Radke-Yarrow M, eds. Development of Anti-Social and Prosocial Behaviour. Orlando: Academic Press, 1986: 13-32.
15. Danforth BN. The morphology and behavior of dimprhic males in Perdita portalis (Hymenoptera; Andrenidae). Behav Ecol Sociobiol 1991; 29: 235-247.
16. Schanberg SM, Evoniuk G, Kuhn CM. Tactile and nutritional aspects of maternal care: Specific regulators of neuroendocrine function and cellular development. Proc Soc Exp Biol Med 1984; 175: 135-146.
17. Levine S. Maternal behavior as a mediator of pup adrenocortical function. Ann NY Acad Sci 1994; 746: 260-275.
18. Myers MM, Brunelli SA, Squire JM, Shindeldecker RD, Hoffer MA. Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 1989; 22: 29-53.
19. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997; 277: 1659-1662.
20. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ. Maternal care during infancy regulates the development of neural systems mediating the expression of behavioral fearfulness in adulthood in the rat. Proc Natl Acad Sci U S A 1998; 95: 5335-5340.
21. Champagne FA, Francis DD, Mar A, Meaney MJ. Naturally-occurring variations in maternal care in the rat as a mediating influence for the effects of environment on the development of individual differences in stress reactivity. Physiol Behav 2003; 79: 359-371.
22. Meaney MJ. The development of individual differences in behavioral and endocrine responses to stress. Ann Rev Neurosci 2001; 24: 1161-1192.
23. Francis DD, Diorio J, Liu D, Meaney MJ. Nongenomic transmission across generations in maternal behavior and stress responses in the rat. Science 1999; 286: 1155-1158.
24. Champagne F, Diorio J, Sharma S, Meaney MJ. Variations in maternal care in the rat are associated with differences in estrogen-related changes in oxytocin receptor levels. Proc Natl Acad Sci U S A 2001; 98: 12736-12741.
25. Bridges RS. Biochemical basis of parental behavior in the rat. Adv Study Behav 1996; 25: 215-242.
26. Lovic V, Fleming AS. Artificially reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task - reversal of effects with maternal-like licking stimulation. Behav Brain Res 2004; 148: 209-219.
27. Melo AI, Lovic V, Gonzalez A, Madden M, Sinopoli K, Fleming AS. Maternal and littermate deprivation disrupts maternal behavior and social-learning of food preference in adulthood: Tactile stimulation, nest odor, and social rearing prevent these effects. Dev Psychobiology 2006; 48: 209-219.
28. Fleming AS, Kraemer GW, Gonzalez A, Lovic V, Rees S, Melo A. Mothering begets mothering: The transmission of behavior and its neurobiology across generations. Pharmacol Biochem Behav 2002; 73: 61-75.
29. Maestripieri D. Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc Natl Acad Sci U S A 2005; 102: 9726-9729.
30. Berman CM. Intergenerational transmission of maternal rejection rates among free-ranging rhesus monkeys on Cayo Santiago. Anim Behav 1990; 44: 247-258.
31. Fairbanks LM. Individual differences in maternal style. Adv Study Behav 1996; 25: 579-611.
32. Maestripieri D. The biology of human parenting: Insights from noonhuman primates. Neurosci Biobehav Rev 1999; 23: 411-422.
33. Krpan KM, Coombs R, Zinga D, Steiner M, Fleming AS. Experiential and hormonal correlates of maternal behavior in teen and adult mothers. Horm Behav 2005; 47: 112-122.
34. Miller L, Kramer R, Warner V, Wickramaratne P, Weissman M. Integenerational transmission of parental bonding among women. J Am Acad Child Adolesc Psychiatry 1997; 36: 1134-1139.
35. Smith JW, Seckl JR, Evans AT, Costall B, Smythe JW. Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 2004; 29: 227-244.
36. Champagne FA, Meaney MJ. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 2006; 59: 1227-1235.
37. Numan M, Sheehan TP. Neuroanatomical circuitry for mammalian maternal behavior. Ann N Y Acad Sci 1997; 807: 101-125.
38. Fleming AS, O'Day DH, Kraemer GW. Neurobiology of mother-infant interactions: Experience and central nervous system plasticity across development and generations. Neurosci Biobehav Rev 1999; 23: 673-685.
39. Pedersen CA. Oxytocin control of maternal behavior: Regulation by sex steriods and offspring stimuli. Ann N Y Acad Sci 1995; 807: 126-145.
40. Sawchenko PE, Swanson LW. Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 1982; 205: 260-272.
41. Bale TL, Pedersen CA, Dorsa DM. CNS oxytocin receptor mRNA expression and regulation by gonadal steroids. Adv Exp Med Biol 1995; 395: 269-280.
42. Fahrbach SE, Morrell JI, Pfaff DW. Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav 1984; 18: 267-286.
43. Champagne FA, Weaver ICG, Diorio J, Sharma S, Meaney MJ. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the MPOA. Endocrinology 2003; 144: 4720-4724.
44. Young LJ, Muns S, Wang Z, Insel TR. Changes in oxytocin receptor mRNA in rat brain during pregnancy and the effects of estrogen and interleukin-6. J Neuroendocrinology 1997; 9: 859-865.
45. Pedersen CA, Prange AJ Jr. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 1979; 76: 6661-6665.
46. Fahrbach SE, Morrell JI, Pfaff DW. Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 1985; 40: 526-532.
47. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr. Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 1985; 6: 175-182.
48. Francis DD, Champagne FA, Meaney MJ. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 2000; 12: 1145-1148.
49. Champagne FA, Weaver ICG, Diorio J, Dymov S, Szyf M, Meaney MJ. Maternal care regulates methylation of the estrogen receptor alpha 1b promoter and estrogen receptor alpha expression in the medial preoptic area of female offspring. Endocrinology 2006; 147: 2909-2915.
50. Kombian SB, Hirasawa M, Mouqinot D, Pittman QJ. Modulation of synaptic transmission by oxytocin and vasopressin in the supraoptic nucleus. Prog Brain Res 2002; 139: 235-246.
51. Wang YF, Ponzio TA, Hatton I. Autofeedback effects of progressively rising oxytocin concentrations on supraoptic oxytocin neuronal activity in slices from lactating rats. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1191-R1198.
52. Jirikowski GF, Caldwell JD, Pilgrim C, Stumpf WE, Pederson CA. Changes in immunostaining for oxytocin in the forebrain of the female rat during late pregnancy, parturition and early lactation. Cell Tissue Res 1989; 256: 144-417.
53. Numan M, Numan MJ, Schwarz JM, Neuner CM, Flood TF, Smith CD. Medial preoptic area interactions with the nucleus accumbens-ventral pallidum circuit and maternal behavior in rats. Behav Brain Res 2005; 158: 53-68.
54. Hansen S, Bergvall AH, Nyiredi S. Interaction with pups enhances dopamine release in the ventral striatum of maternal rats: A microdialysis study. Pharmacol Biochem Behav 1993; 45: 673-676.
55. Champagne FA, Stevenson C, Gratton A, Meaney MJ. Individual differences in maternal behavior are mediated by dopamine release in the nucleus accumbens. J Neurosci 2004; 24: 4113-4123.
56. Cameron NM, Del Corpo A, Diorio J, McAllister K, Sharma S, Meaney MJ. Maternal programming of sexual behavior and hypothalamic-pituitary-gonadal function in the female rat. Submitted.
57. Simerly RB. Wired for reproduction: Organization and development of sexually dimorphic circuits in the mammalian forebrain. Ann Rev Neurosci 2002; 25: 507-536.
58. Petersen SL, Ottem EN, Carpenter CD. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol Reprod 2003; 69: 1771-1778.
59. Petersen SL, McCrone S, Shores S. Localized changes in LHRH mRNA levels as cellular correlates of the positive feedback effects of estrogen on LHRH neurons. Am Zool 1993; 33: 255-265.
60. Herbison AE. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr Rev 1998; 19: 302-330.
61. Erskine MS. Solicitation behavior in the estrous female rat: A review. Horm Behav 1989; 23: 473-502.
62. Yang LY, Clemens LG. Relation of intromission to the female's postejaculatory refractory period in rats. Physiol Behav 1996; 60: 1505-1511.
63. Erskine MS, Lehmann ML, Cameron N, Polston E. Coregulation of female sexual behavior and pregnancy induction: An exploratory synthesis. Brain Res Rev 2004; 153: 295-315.
64. Blaustein JD, Erskine MS. Feminine sexual behavior: Cellular integration of hormonal and afferent information in the rodent forebrain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, Brain and Behavior. New York: Academic Press, 2002: 139-191.
65. Coopersmith C, Candurra C, Erskine M. Effects of paced mating and intromissive stimulation on feminine sexual behavior and estrus termination in the cycling rat. J Comp Psychol 1996; 110: 176-186.
66. Cameron NM, Fish EW, Meaney MJ. Maternal influences on the sexual behavior and reproductive success of the female rat. Horm Behav 2008; in press.
67. Foecking EM, Szabo M, Schwartz NB, Levine JE. Neuroendocrine consequences of prenatal androgen exposure in the female rat: Absence of luteinizing hormone surges, suppression of progesterone receptor gene expression, and acceleration of the gonadotropin-releasing hormone pulse generator. Biol Reprod 2005; 72: 1475-1483.
68. Weaver ICG, Cervoni N, D'Alessio AC, Champagne FA, Seckl JR, Szyf M, Meaney MJ. Epigenetic programming through maternal behavior. Nature (Neuroscience) 2004; 7: 847-854.
69. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, Szyf M. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. J Neurosci 2005; 25: 11045-11054.
70. Weaver ICG, D'Alessio AC, Brown SE, Hellstrom IC, Dymov S, Sharma S, Szyf M, Meaney MJ. The transcription factor nerve growth factor-inducible protein A mediates epigenetic programming: Altering epigenetic marks by immediate-early genes. J Neuroscience 2007; 27: 1756-1768.
71. Szyf M, Weaver IC, Champagne FA, Diorio J, Meaney MJ. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol, 2005; 26: 139-162.
72. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 1998; 17: 4905-4908.
73. Bird A, Wolffe AP. Methylation-induced repression - belts, braces, and chromatin. Cell 1999; 99: 451-454.
74. Bird AP. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16: 6-21.
75. Frasor J, Gibori G. Prolactin regulation of estrogen receptor expression. Trends Endocrinol Metabol 2003; 14: 118-123.