Maternal Influence on Offspring Reproductive Behavior: Implications for Transgenerational Effects

Neurobiology of the Parental Brain

Volumn , Issue , 2008, Pages 305-318

  Champagne, Frances A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882891333     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374285-8.00019-6     Document Type: Chapter

References (131)

1. Allegrucci C., Thurston A., Lucas E., Young L. Epigenetics and the germline. Reproduction 2005, 129:137-149.
2. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
3. Arling G.L., Harlow H.F. Effects of social deprivation on maternal behavior of rhesus monkeys. J. Comp. Physiol. Psychol. 1967, 64:371-377.
4. Bardi M., Huffman M.A. Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata). Dev. Psychobiol. 2002, 41:364-372.
5. Bardi M., Huffman M.A. Maternal behavior and maternal stress are associated with infant behavioral development in macaques. Dev Psychobiol. 2006, 48:1-9.
6. Barker D.J. The developmental origins of adult disease. J. Am. Coll. Nutr. 2004, 23:588S-595S.
7. Bayol S.A., Farrington S.J., Stickland N.C. A maternal "junk food" diet in pregnancy and lactation promotes an exacerbated taste for "junk food" and a greater propensity for obesity in rat offspring. Br. J. Nutr. 2007, 98:843-851.
8. Beckett C., Bredenkamp D., Castle J., Groothues C., O'Connor T.G., Rutter M. Behavior patterns associated with institutional deprivation: A study of children adopted from Romania. J. Dev. Behav. Pediatr. 2002, 23:297-303.
9. Benoit D., Parker K.C. Stability and transmission of attachment across three generations. Child Dev. 1994, 65:1444-1456.
10. Berman C. Intergenerational transmission of maternal rejection rates among free-ranging rheus monkeys on Cayo Santiago. Anim. Behav. 1990, 44:247-258.
11. Bernstein I.M., Mongeon J.A., Badger G.J., Solomon L., Heil S.H., Higgins S.T. Maternal smoking and its association with birth weight. Obstet. Gynecol. 2005, 106:986-991.
12. Blusztajn J.K., Wurtman R.J. Choline biosynthesis by a preparation enriched in synaptosomes from rat brain. Nature 1981, 290:417-418.
13. Boerke A., Dieleman S.J., Gadella B.M. A possible role for sperm RNA in early embryo development. Theriogenology 2007, 68(suppl 1):S147-S155.
14. Braadstad B.O. Effects of prenatal stress on behavior of offspring of laboratory and farmed mammals. Appl. Anim. Behav. Sci. 1998, 61:159-180.
15. Bredy T.W., Grant R.J., Champagne D.L., Meaney M.J. Maternal care influences neuronal survival in the hippocampus of the rat. Eur. J. Neurosci. 2003, 18:2903-2909.
16. Bukovsky A., Caudle M.R., Svetlikova M., Wimalasena J., Ayala M.E., Dominguez R. Oogenesis in adult mammals, including humans: A review. Endocrine 2005, 26:301-316.
17. 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. USA 1998, 95:5335-5340.
18. Cameron N.M., Meaney M.J. Effect of maternal care and ovariectomy on sexual behavior and c-Fos activity in the female rat. Front. Neuroendocrinol. 2006, 27:144.
19. Catalano R., Bruckner T., Hartig T., Ong M. Population stress and the Swedish sex ratio. Paediatr. Perinat. Epidemiol. 2005, 19:413-420.
20. Champagne F., Diorio J., Sharma S., Meaney M.J. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc. Natl Acad. Sci. USA 2001, 98:12736-12741.
21. Champagne F.A., Meaney M.J. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol. Psychiatr. 2006, 59:1227-1235.
22. 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.
23. Champagne F.A., Weaver I.C., Diorio J., Sharma S., Meaney M.J. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 2003, 144:4720-4724.
24. Champagne F.A., Chretien P., Stevenson C.W., Zhang T.Y., Gratton A., Meaney M.J. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J. Neurosci. 2004, 24:4113-4123.
25. Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M., Meaney M.J. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006, 147:2909-2915.
26. Champagne F.A., Curley J.P., Keverne E.B., Bateson P.P. Natural variations in postpartum maternal care in inbred and outbred mice. Physiol. Behav. 2007, 91:325-334.
27. Corcoran D., Fair T., Lonergan P. Predicting embryo quality: mRNA expression and the preimplantation embryo. Reprod. Biomed. Online 2005, 11:340-348.
28. Corcoran D., Rizos D., Fair T., Evans A.C., Lonergan P. Temporal expression of transcripts related to embryo quality in bovine embryos cultured from the two-cell to blastocyst stage in vitro or in vivo. Mol. Reprod. Dev. 2007, 74:972-977.
29. Cratty M.S., Ward H.E., Johnson E.A., Azzaro A.J., Birkle D.L. Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res. 1995, 675:297-302.
30. Crews D., Gore A.C., Hsu T.S., Dangleben N.L., Spinetta M., Schallert T., Anway M.D., Skinner M.K. Transgenerational epigenetic imprints on mate preference. Proc. Natl Acad. Sci. USA 2007, 104:5942-5946.
31. Curley J.P., Barton S., Surani A., Keverne E.B. Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proc. Biol. Sci. 2004, 271:1303-1309.
32. da Silva Faria T., da Fonte Ramos C., Sampaio F.J. Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation. J. Nutr. Biochem. 2004, 15:123-127.
33. Davis C.D., Uthus E.O. DNA methy-lation, cancer susceptibility, and nutrient interactions. Exp. Biol. Med. (Maywood) 2004, 229:988-995.
34. De Sousa P.A., Caveney A., Westhusin M.E., Watson A.J. Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology 1998, 49:115-128.
35. de Weerth C., Wied C.C., Jansen L.M., Buitelaar J.K. Cardiovascular and cortisol responses to a psychological stressor during pregnancy. Acta Obstet. Gynecol. Scand. 2007, 1181-1192.
36. Denenberg V.H., Rosenberg K.M. Nongenetic transmission of information. Nature 1967, 216:549-550.
37. Dolinoy D.C., Huang D., Jirtle R.L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl Acad. Sci. USA 2007, 104:13056-13061.
38. Edwards C.R., Benediktsson R., Lindsay R.S., Seckl J.R. 11 beta-Hydroxysteroid dehydrogenases: Key enzymes in determining tissue-specific glucocorticoid effects. Steroids 1996, 61:263-269.
39. Eichenlaub-Ritter U. Genetics of oocyte ageing. Maturitas 1998, 30:143-169.
40. Fairbanks L.A. Early experience and cross-generational continuity of mother-infant contact in vervet monkeys. Dev. Psychobiol. 1989, 22:669-681.
41. Fairbanks L.A., McGuire M.T. Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev. Psychobiol. 1988, 21:711-724.
42. Fernandez-Gonzalez R., Moreira P., Bilbao A., Jimenez A., Perez-Crespo M., Ramirez M.A., Rodriguez De Fonseca F., Pintado B., Gutierrez-Adan A. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc. Natl Acad. Sci. USA 2004, 101:5880-5885.
43. Fernandez-Gonzalez R., Ramirez M.A., Bilbao A., De Fonseca F.R., Gutierrez-Adan A. Suboptimal in vitro culture conditions: An epigenetic origin of long-term health effects. Mol. Reprod. Dev. 2007, 74:1149-1156.
44. 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.
45. Francis D.D., Champagne F.A., Liu D., Meaney M.J. Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann. NY Acad. Sci. 1999, 896:66-84.
46. Francis D.D., Champagne F.C., Meaney M.J. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J. Neuroendocrinol. 2000, 12:1145-1148.
47. Frye C.A., Orecki Z.A. Prenatal stress alters reproductive responses of rats in behavioral estrus and paced mating of hormone-primed rats. Horm. Behav. 2002, 42:472-483.
48. Fulroth R., Phillips B., Durand D.J. Perinatal outcome of infants exposed to cocaine and/or heroin in utero. Am. J. Dis. Child. 1989, 143:905-910.
49. Gavis E.R., Lehmann R. Localization of nanos RNA controls embryonic polarity. Cell 1992, 71:301-313.
50. Gluckman P.D., Hanson M.A., Pinal C. The developmental origins of adult disease. Matern. Child Nutr. 2005, 1:130-141.
51. 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.
52. Gosden R., Trasler J., Lucifero D., Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 2003, 361:1975-1977.
53. Gunnar M.R., van Dulmen M.H. Behavior problems in postinstitutionalized internationally adopted children. Dev. Psychopathol. 2007, 19:129-148.
54. Haig D. Genetic conflicts in human pregnancy. Q. Rev. Biol. 1993, 68:495-532.
55. Hall W.G. Weaning and growth of artificially reared rats. Science 1975, 190:1313-1315.
56. Hane A.A., Fox N.A. Ordinary variations in maternal caregiving influence human infants' stress reactivity. Psychol. Sci. 2006, 17:550-556.
57. Harlow H.F., Suomi S.J. Social r-ecovery by isolation-reared monkeys. Proc. Natl Acad. Sci. USA 1971, 68:1534-1538.
58. Harlow H.F., Suomi S.J. Induced depression in monkeys. Behav. Biol. 1974, 12:273-296.
59. Hertsgaard L., Gunnar M., Erickson M.F., Nachmias M. Adrenocortical responses to the strange situation in infants with disorganized/disoriented attachment relationships. Child Dev. 1995, 66:1100-1106.
60. Herrenkohl L.R. Prenatal stress reduces fertility and fecundity in female offspring. Science 1979, 208:1097-1099.
61. Higgins S. Smoking in pregnancy. Curr. Opin. Obstet. Gynecol. 2002, 14:145-151.
62. Hinde R.A., Simpson M.J. Qualities of mother-infant relationships in monkeys. Ciba Found. Symp. 1975, 39-67.
63. Hoyseth K.S., Jones P.J. Ethanol induced teratogenesis: Characterization, mechanisms and diagnostic approaches. Life Sci. 1989, 44:643-649.
64. Janny L., Menezo Y.J. Maternal age effect on early human embryonic development and blastocyst formation. Mol. Reprod. Dev. 1996, 45:31-37.
65. Kaaja R.J., Greer I.A. Manifestations of chronic disease during pregnancy. JAMA 2005, 294:2751-2757.
66. Kaiser S., Sachser N. The effects of prenatal social stress on behaviour: Mechanisms and function. Neurosci. Biobehav. Rev. 2005, 29:283-294.
67. Kaiser S., Kruijver F.P., Swaab D.F., Sachser N. Early social stress in female guinea pigs induces a masculinization of adult behavior and corresponding changes in brain and neuroendocrine function. Behav. Brain Res. 2003, 144:199-210.
68. Kinsley C.H., Bridges R.S. Prenatal stress and maternal behavior in intact virgin rats: Response latencies are decreased in males and increased in females. Horm. Behav. 1988, 22:76-89.
69. Kovacheva V.P., Mellott T.J., Davison J.M., Wagner N., Lopez-Coviella I., Schnitzler A.C., Blusztajn J.K. Gestational choline deficiency causes global- and Igf2 gene- DNA hypermethylation by upregulation of Dnmt1 expression. J. Biol. Chem. 2007.
70. Kruuk L.E., Hadfield J.D. How to separate genetic and environmental causes of similarity between relatives. J. Evol. Biol. 2007, 20:1890-1903.
71. Lee P.R., Brady D.L., Shapiro R.A., Dorsa D.M., Koenig J.I. Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin. Brain Res. 2007, 1156:152-167.
72. Lehmann J., Pryce C.R., Bettschen D., Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 1999, 64:705-715.
73. Lehmann J., Stohr T., Feldon J. Long-term effects of prenatal stress experiences and postnatal maternal separation on emotionality and attentional processes. Behav. Brain Res. 2000, 107:133-144.
74. Lesage J., Blondeau B., Grino M., Breant B., Dupouy J.P. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology 2001, 142:1692-1702.
75. Li T., Vu T.H., Ulaner G.A., Littman E., Ling J.Q., Chen H.L., Hu J.F., Behr B., Giudice L., Hoffman A.R. IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Mol. Hum. Reprod. 2005, 11:631-640.
76. Lippmann M., Bress A., Nemeroff C.B., Plotsky P.M., Monteggia L.M. Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci. 2007, 25:3091-3098.
77. 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.
78. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 2000, 3:799-806.
79. Lovic V., Fleming A.S. 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.
80. Maestripieri D. Parenting styles of abusive mothers in group-living rhesus macaques. Anim. Behav. 1998, 55:1-11.
81. Maestripieri D. Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc. Natl Acad. Sci. USA 2005, 102:9726-9729.
82. Maestripieri D., Wallen K., Carroll K.A. Infant abuse runs in families of group-living pigtail macaques. Child Abuse Neglect 1997, 21:465-471.
83. Maestripieri D., Tomaszycki M., Carroll K.A. Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants. Dev. Psychobiol. 1999, 34:29-35.
84. Maestripieri D., Lindell S.G., Ayala A., Gold P.W., Higley J.D. Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior. Neurosci. Biobehav. Rev. 2005, 29:51-57.
85. Maestripieri D., Higley J.D., Lindell S.G., Newman T.K., McCormack K.M., Sanchez M.M. Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta). Behav. Neurosci. 2006, 120:1017-1024.
86. Malcolm J.C., Lawson M.L., Gaboury I., Lough G., Keely E. Glucose tolerance of offspring of mother with gestational diabetes mellitus in a low-risk population. Diabet. Med. 2006, 23:565-570.
87. McCormack K., Sanchez M.M., Bardi M., Maestripieri D. Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev. Psychobiol. 2006, 48:537-550.
88. McLean M., Chipps D., Cheung N.W. Mother to child transmission of diabetes mellitus: Does gestational diabetes program Type 2 diabetes in the next generation?. Diabet. Med. 2006, 23:1213-1215.
89. McMillen I.C., Robinson J.S. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol. Rev. 2005, 85:571-633.
90. 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.
91. Moore C.L., Power K.L. Prenatal stress affects mother-infant interaction in Norway rats. Dev. Psychobiol. 1986, 19:235-245.
92. Mousseau T.A., Fox C.W. Maternal Effects as Adaptations 1998, Oxford University Press, New York.
93. Murphy L., Cherlet T., Lewis A., Banu Y., Watson P. New insights into estrogen receptor function in human breast cancer. Ann. Med. 2003, 35:614-631.
94. Nothias J.Y., Majumder S., Kaneko K.J., DePamphilis M.L. Regulation of gene expression at the beginning of mammalian development. J. Biol. Chem. 1995, 270:22077-22080.
95. Olegard R., Sabel K.G., Aronsson M., Sandin B., Johansson P.R., Carlsson C., Kyllerman M., Iversen K., Hrbek A. Effects on the child of alcohol abuse during pregnancy. Retrospective and prospective studies. Acta Paediatr. Scand. Suppl. 1979, 275:112-121.
96. Painter R.C., Roseboom T.J., Bleker O.P. Prenatal exposure to the Dutch famine and disease in later life: An overview. Reprod. Toxicol. 2005, 20:345-352.
97. Parker G. Parental "affectionless control" as an antecedent to adult depression. A risk factor delineated. Arch. Gen. Psychiatr. 1983, 40:956-960.
98. Parker G. The Parental Bonding Instrument: A decade of research. Soc. Psychiatr. Psychiatr. Epidemiol. 1990, 25:281-282.
99. Parker S.W., Nelson C.A. The impact of early institutional rearing on the ability to discriminate facial expressions of emotion: An event-related potential study. Child Dev. 2005, 76:54-72.
100. Peters D.A. Prenatal stress: Effects on brain biogenic amine and plasma corticosterone levels. Pharmacol. Biochem. Behav. 1982, 17:721-725.
101. 11C]raclopride. J. Neurosci. 2004, 24:2825-2831.
102. Razin A. CpG methylation, chromatin structure and gene silencing - a three-way connection. EMBO J. 1998, 17:4905-4908.
103. Rocha S.O., Gomes G.N., Forti A.L., do Carmo Pinho Franco M., Fortes Z.B., de Fatima Cavanal M., Gil F.Z. Long-term effects of maternal diabetes on vascular reactivity and renal function in rat male offspring. Pediatr. Res. 2005, 58:1274-1279.
104. Rondo P.H., Ferreira R.F., Nogueira F., Ribeiro M.C., Lobert H., Artes R. Maternal psychological stress and distress as predictors of low birth weight, prematurity and intrauterine growth retardation. Eur. J. Clin. Nutr. 2003, 57:266-272.
105. Roseboom T., de Rooij S., Painter R. The Dutch famine and its long-term consequences for adult health. Early Hum. Dev. 2006, 82:485-491.
106. Roseboom T.J., van der Meulen J.H., Osmond C., Barker D.J., Ravelli A.C., Schroeder-Tanka J.M., van Montfrans G.A., Michels R.P., Bleker O.P. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45. Heart 2000, 84:595-598.
107. Scott L.A. Oocyte and embryo polarity. Semin. Reprod. Med. 2000, 18:171-183.
108. Seckl J.R., Nyirenda M.J., Walker B.R., Chapman K.E. Glucocorticoids and fetal programming. Biochem. Soc. Trans. 1999, 27:74-78.
109. Sroufe L.A. Attachment and development: A prospective, longitudinal study from birth to adulthood. Attach. Hum. Dev. 2005, 7:349-567.
110. Stohr T., Schulte Wermeling D., Szuran T., Pliska V., Domeney A., Welzl H., Weiner I., Feldon J. Differential effects of prenatal stress in two inbred strains of rats. Pharmacol. Biochem. Behav. 1998, 59:799-805.
111. Strathdee G., Brown R. Aberrant DNA methylation in cancer: Potential clinical interventions. Expert Rev. Mol. Med. 2002, 4:1-17.
112. Symonds M.E., Budge H., Stephenson T., Gardner D.S. Experimental evidence for long-term programming effects of early diet. Adv. Exp. Med. Biol. 2005, 569:24-32.
113. Takahashi L.K., Turner J.G., Kalin N.H. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res. 1992, 574:131-137.
114. Tambyrajia R.L., Mongelli M. Sociobiological variables and pregnancy outcome. Int. J. Gynaecol. Obstet. 2000, 70:105-112.
115. Trottier G., Koski K.G., Brun T., Toufexis D.J., Richard D., Walker C.D. Increased fat intake during lactation modifies hypothalamic-pituitary-adrenal responsiveness in developing rat pups: A possible role for leptin. Endocrinology 1998, 139:3704-3711.
116. Turner B. Chromatin and Gene Regulation 2001, Blackwell Science Ltd, Oxford.
117. Uriarte N., Breigeiron M.K., Benetti F., Rosa X.F., Lucion A.B. Effects of maternal care on the development, emotionality, and reproductive functions in male and female rats. Dev. Psychobiol. 2007, 49:451-462.
118. Wagner C.L., Katikaneni L.D., Cox T.H., Ryan R.M. The impact of prenatal drug exposure on the neonate. Obstet. Gynecol. Clin. North Am. 1998, 25:169-194.
119. Wassarman P.M., Kinloch R.A. Gene expression during oogenesis in mice. Mutat. Res. 1992, 296:3-15.
120. Waterland R.A., Dolinoy D.C., Lin J.R., Smith C.A., Shi X., Tahiliani K.G. Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis 2006, 44:401-406.
121. Weaver I.C., Grant R.J., Meaney M.J. Maternal behavior regulates long-term hippocampal expression of BAX and apoptosis in the offspring. J. Neurochem. 2002, 82:998-1002.
122. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav. Immun. 2005, 19:296-308.
123. Weinstock M., Fride E., Hertzberg R. Prenatal stress effects on functional development of the offspring. Prog. Brain Res. 1988, 73:319-331.
124. West J.R. Use of pup in a cup model to study brain development. J. Nutr. 1993, 123:382-385.
125. Weissgerber T.L., Wolfe L.A. Physiological adaptation in early human pregnancy: adaptation to balance maternal-fetal demands. Appl. Physiol. Nutr. Metab. 2006, 31:1-11.
126. Wolff G.L., Kodell R.L., Moore S.R., Cooney C.A. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998, 12:949-957.
127. Yan L., Yang X., Davidson N.E. Role of DNA methylation and histone acetylation in steroid receptor expression in breast cancer. J. Mammary Gland Biol. Neoplasia 2001, 6:183-192.
128. Zambrano E., Martinez-Samayoa P.M., Bautista C.J., Deas M., Guillen L., Rodriguez-Gonzalez G.L., Guzman C., Larrea F., Nathanielsz P.W. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J. Physiol. 2005, 566:225-236.
129. Zhang T.Y., Chretien 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.
130. Zorn B., Sucur V., Stare J., Meden-Vrtovec H. Decline in sex ratio at birth after 10-day war in Slovenia: Brief communication. Hum. Reprod. 2002, 17:3173-3177.
131. Zubieta A.C., Lonnerdal B. Effect of suboptimal nutrition during lactation on milk protein gene expression in the rat. J. Nutr. Biochem. 2006, 17:604-610.