Mechanisms of non-genetic inheritance and psychiatric disorders

Neuropsychopharmacology

Volumn 40, Issue 1, 2015, Pages 129-140

  Toth, Miklos ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; GENETIC EPIGENESIS; GENETICS; HUMAN; INHERITANCE; MENTAL DISORDERS; PSYCHOLOGY; RISK FACTOR;

ANIMALS; EPIGENESIS, GENETIC; HUMANS; INHERITANCE PATTERNS; MENTAL DISORDERS; RISK FACTORS;

EID: 84926651422     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.127     Document Type: Review

References (135)

1. Abel EL, Moore C, Waselewsky D, Zajac C, Russell LD (1989). Effects of cocaine hydrochloride on reproductive function and sexual behavior of male rats and on the behavior of their offspring. J Androl 10: 17-27.
2. Agrawal AA, Laforsch C, Tollrian R (1999). Transgenerational induction of defences in animals and plants. Nature 401: 60-63.
3. Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S (2012). Gut microbial communities modulating brain development and function. Gut Microbes 3: 366-373.
4. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469.
5. Anway MD, Memon MA, Uzumcu M, Skinner MK (2006). Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl 27: 868-879.
6. Barbazanges A, Piazza PV, Le Moal M, Maccari S (1996). Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16: 3943-3949.
7. Bartel DP (2009). MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
8. Bergman K, Sarkar P, Glover V, O'Connor TG (2010). Maternal prenatal cortisol and infant cognitive development: moderation by infant-mother attachment. Biol Psychiatry 67: 1026-1032.
9. Bertram C, Khan O, Ohri S, Phillips DI, Matthews SG, Hanson MA (2008). Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic-pituitary-adrenal function. J Physiol 586: 2217-2229.
10. Bird A (2002). DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21.
11. Blewitt ME, Vickaryous NK, Paldi A, Koseki H, Whitelaw E (2006). Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet 2: e49.
12. Bohacek J, Gapp K, Saab BJ, Mansuy IM (2013). Transgenerational epigenetic effects on brain functions. Biol Psychiatry 73: 313-320.
13. Bonduriansky R (2012). Rethinking heredity, again. Trends Ecol Evol 27: 330-336.
14. Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H et al. (2010). Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 42: 1093-1100.
15. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG et al. (2011). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 108: 16050-16055.
16. Brown AS (2012). Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol 72: 1272-1276.
17. Brummelte S, Galea LA (2010). Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog Neuropsychopharmacol Biol Psychiatry 34: 766-776.
18. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC et al. (2010). Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 17: 679-687.
19. Byrnes EM (2005a). Transgenerational consequences of adolescent morphine exposure in female rats: effects on anxiety-like behaviors and morphine sensitization in adult offspring. Psychopharmacology (Berl) 182: 537-544.
20. Byrnes EM (2005b). Chronic morphine exposure during puberty decreases postpartum prolactin secretion in adult female rats. Pharmacol Biochem Behav 80: 445-451.
21. Byrnes EM (2008). Chronic morphine exposure during puberty induces long-lasting changes in opioid-related mRNA expression in the mediobasal hypothalamus. Brain Res 1190: 186-192.
22. Byrnes JJ, Babb JA, Scanlan VF, Byrnes EM (2011). Adolescent opioid exposure in female rats: transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav Brain Res 218: 200-205.
23. Byrnes JJ, Johnson NL, Carini LM, Byrnes EM (2013). Multigenerational effects of adolescent morphine exposure on dopamine D2 receptor function. Psychopharmacology (Berl) 227: 263-272.
24. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95: 5335-5340.
25. Cameron NM, Shahrokh D, Del Corpo A, Dhir SK, Szyf M, Champagne FA et al. (2008). Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 20: 795-801.
26. Champagne FA, Meaney MJ (2007). Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121: 1353-1363.
27. Chen GH, Wang H, Yang QG, Tao F, Wang C, Xu DX (2011). Acceleration of agerelated learning and memory decline in middle-aged CD-1 mice due to maternal exposure to lipopolysaccharide during late pregnancy. Behav Brain Res 218: 267-279.
28. Chong S, Vickaryous N, Ashe A, Zamudio N, Youngson N, Hemley S et al. (2007). Modifiers of epigenetic reprogramming show paternal effects in the mouse. Nat Genet 39: 614-622.
29. Cropley JE, Suter CM, Beckman KB, Martin DI (2006). Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation. Proc Natl Acad Sci USA 103: 17308-17312.
30. Curtis TP, Sloan WT (2004). Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr Opin Microbiol 7: 221-226.
31. Cuzin F, Rassoulzadegan M (2010). Non-Mendelian epigenetic heredity: gametic RNAs as epigenetic regulators and transgenerational signals. Essays Biochem 48: 101-106.
32. Danchin E, Charmantier A, Champagne FA, Mesoudi A, Pujol B, Blanchet S (2011). Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 12: 475-486.
33. Dantzer B, Newman AE, Boonstra R, Palme R, Boutin S, Humphries MM et al. (2013). Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340: 1215-1217.
34. Dave-Sharma S, Wilson RC, Harbison MD, Newfield R, Azar MR, Krozowski ZS et al. (1998). Examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J Clin Endocrinol Metab 83: 2244-2254.
35. Day T, Bonduriansky R (2011). A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178: E18-E36.
36. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG (2010). Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170: 1179-1188.
37. Dias BG, Ressler KJ (2013). Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17: 89-96.
38. Fernandez-Gonzalez R, Ramirez MA, Pericuesta E, Calle A, Gutierrez-Adan A (2010). Histone modifications at the blastocyst Axin1(Fu) locus mark the heritability of in vitro culture-induced epigenetic alterations in mice. Biol Reprod 83: 720-727.
39. Francis D, Diorio J, Liu D, Meaney MJ (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286: 1155-1158.
40. Francis DD, Szegda K, Campbell G, Martin WD, Insel TR (2003). Epigenetic sources of behavioral differences in mice. Nat Neurosci 6: 445-446.
41. Frankenhuis WE, Del Giudice M (2012). When do adaptive developmental mechanisms yield maladaptive outcomes? Dev Psychol 48: 628-642.
42. Franklin TB, Russig H, Weiss IC, Gräff J, Linder N, Michalon A et al. (2010). Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 68: 408-415.
43. French NP, Hagan R, Evans SF, Godfrey M, Newnham JP (1999). Repeated antenatal corticosteroids: size at birth and subsequent development. Am J Obstet Gynecol 180: 114-121.
44. Fride E, Dan Y, Feldon J, Halevy G, Weinstock M (1986). Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 37: 681-687.
45. Fak F, Ahrné S, Molin G, Jeppsson B, Weström B (2008). Microbial manipulation of the rat dam changes bacterial colonization and alters properties of the gut in her offspring. Am J Physiol Gastrointest Liver Physiol 294: G148-G154.
46. Gangi S, Talamo A, Ferracuti S (2009). The long-term effects of extreme warrelated trauma on the second generation of Holocaust survivors. Violence Vict 24: 687-700.
47. Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH (2007). Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56: 1522-1528.
48. Gitau R, Fisk NM, Glover V (2004). Human fetal and maternal corticotrophin releasing hormone responses to acute stress. Arch Dis Child Fetal Neonatal Ed 89: F29-F32.
49. Gleason G, Liu B, Bruening S, Zupan B, Auerbach A, Mark W et al. (2010). The serotonin1A receptor gene as a genetic and prenatal maternal environmental factor in anxiety. Proc Natl Acad Sci USA 107: 7592-7597.
50. Govorko D, Bekdash RA, Zhang C, Sarkar DK (2012). Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol Psychiatry 72: 378-388.
51. Grandjean V, Gounon P, Wagner N, Martin L, Wagner KD, Bernex F et al. (2009). The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136: 3647-3655.
52. Guibert S, Forné T, Weber M (2012). Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res 22: 633-641.
53. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, Down TA et al. (2013). Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339: 448-452.
54. Halligan SL, Herbert J, Goodyer IM, Murray L (2004). Exposure to postnatal depression predicts elevated cortisol in adolescent offspring. Biol Psychiatry 55: 376-381.
55. Halligan SL, Murray L, Martins C, Cooper PJ (2007). Maternal depression and psychiatric outcomes in adolescent offspring: a 13-year longitudinal study. J Affect Disord 97: 145-154.
56. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR (2009). Distinctive chromatin in human sperm packages genes for embryo development. Nature 460: 473-478.
57. Harper LV (2005). Epigenetic inheritance and the intergenerational transfer of experience. Psychol Bull 131: 340-360.
58. He F, Lidow IA, Lidow MS (2006). Consequences of paternal cocaine exposure in mice. Neurotoxicol Teratol 28: 198-209.
59. Henry C, Kabbaj M, Simon H, Le Moal M, Maccari S (1994). Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 6: 341-345.
60. Hoek HW, Brown AS, Susser E (1998). The Dutch famine and schizophrenia spectrum disorders. Soc Psychiatry Psychiatr Epidemiol 33: 373-379.
61. Hooper LV, Littman DR, Macpherson AJ (2012). Interactions between the microbiota and the immune system. Science 336: 1268-1273.
62. Howerton CL, Bale TL (2012). Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav 62: 237-242.
63. Huizink AC, Mulder EJ, Buitelaar JK (2004). Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility? Psychol Bull 130: 115-142.
64. Hunter B, Hollister JD, Bomblies K (2012). Epigenetic inheritance: what news for evolution? Curr Biol 22: R54-R56.
65. Iqbal M, Moisiadis VG, Kostaki A, Matthews SG (2012). Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamic-pituitary-adrenal function. Endocrinology 153: 3295-3307.
66. Ishiwata H, Shiga T, Okado N (2005). Selective serotonin reuptake inhibitor treatment of early postnatal mice reverses their prenatal stress-induced brain dysfunction. Neuroscience 133: 893-901.
67. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O et al. (2012). Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8: e1002440.
68. Koehl M, Darnaudéry M, Dulluc J, Van Reeth O, Le Moal M, Maccari S (1999). Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 40: 302-315.
69. Kostaki A, Owen D, Li D, Matthews SG (2005). Transgenerational effects of prenatal glucocorticoid exposure on growth, endocrine function and behaviour in the guinea pig. Pediatr Res 58: P1-052.
70. Ledig M, Misslin R, Vogel E, Holownia A, Copin JC, Tholey G (1998). Paternal alcohol exposure: developmental and behavioral effects on the offspring of rats. Neuropharmacology 37: 57-66.
71. Liu B, Zupan B, Laird E, Klein S, Gleason G, Bozinoski M et al. (2014). Maternal hematopoietic TNF, via milk chemokines, programs hippocampal development and memory. Nat Neurosci 17: 97-105.
72. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3: 799-806.
73. Lumey LH, Stein AD, Susser E (2011). Prenatal famine and adult health. Annu Rev Public Health 32: 237-262.
74. Luteijn MJ, Ketting RF (2013). PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat Rev Genet 14: 523-534.
75. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M (1995). Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15: 110-116.
76. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O (2003). Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27: 119-127.
77. Mairesse J, Lesage J, Breton C, Bréant B, Hahn T, Darnaudéry M et al. (2007). Maternal stress alters endocrine function of the fetoplacental unit in rats. Am J Physiol Endocrinol Metab 292: E1526-E1533.
78. Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH (2012). Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun 26: 607-616.
79. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ et al. (2009). Finding the missing heritability of complex diseases. Nature 461: 747-753.
80. Matthews SG, Phillips DI (2010). Minireview: transgenerational inheritance of the stress response: a new frontier in stress research. Endocrinology 151: 7-13.
81. McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ (2012). Sex differences in the brain: the not so inconvenient truth. J Neurosci 32: 2241-2247.
82. Meaney MJ (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24: 1161-1192.
83. Morgan CP, Bale TL (2011). Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 31: 11748-11755.
84. Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999). Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23: 314-318.
85. Mueller BR, Bale TL (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28: 9055-9065.
86. Murray L, Halligan SL, Goodyer I, Herbert J (2010). Disturbances in early parenting of depressed mothers and cortisol secretion in offspring: a preliminary study. J Affect Disord 122: 218-223.
87. Newbold RR, Padilla-Banks E, Jefferson WN (2006). Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147: S11-S17.
88. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W et al. (2012). Hostgut microbiota metabolic interactions. Science 336: 1262-1267.
89. O'Connor TG, Heron J, Golding J, Beveridge M, Glover V (2002). Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. Br J Psychiatry 180: 502-508.
90. Padmanabhan N, Jia D, Geary-Joo C, Wu X, Ferguson-Smith AC, Fung E et al. (2013). Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell 155: 81-93.
91. Painter RC, Roseboom TJ, Bleker OP (2005). Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 20: 345-352.
92. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ (2008). Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115: 1243-1249.
93. Patterson PH (2009). Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav Brain Res 204: 313-321.
94. Peters DA (1982). Prenatal stress: effects on brain biogenic amine and plasma corticosterone levels. Pharmacol Biochem Behav 17: 721-725.
95. Phillips DI, Walker BR, Reynolds RM, Flanagan DE, Wood PJ, Osmond C et al. (2000). Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension 35: 1301-1306.
96. Rakyan V, Whitelaw E (2003). Transgenerational epigenetic inheritance. Curr Biol 13: R6.
97. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV et al. (2003). Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci USA 100: 2538-2543.
98. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F (2006). RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441: 469-474.
99. Reynolds RM (2013). Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis-2012 Curt Richter Award Winner. Psychoneuroendocrinology 38: 1-11.
100. Roberts AL, Galea S, Austin SB, Cerda M, Wright RJ, Rich-Edwards JW et al. (2012). Posttraumatic stress disorder across two generations: concordance and mechanisms in a population-based sample. Biol Psychiatry 72: 505-511.
101. Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL (2013). Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 33: 9003-9012.
102. Rose CM, van den Driesche S, Meehan RR, Drake AJ (2013). Epigenetic reprogramming: preparing the epigenome for the next generation. Biochem Soc Trans 41: 809-814.
103. Räikkönen K, Pesonen AK, Heinonen K, Lahti J, Komsi N, Eriksson JG et al. (2009). Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am J Epidemiol 170: 1137-1146.
104. Saavedra-Rodriguez L, Feig LA (2012). Chronic social instability induces anxiety and defective social interactions across generations. Biol Psychiatry 73: 44-53.
105. Saavedra-Rodríguez L, Feig LA (2013). Chronic social instability induces anxiety and defective social interactions across generations. Biol Psychiatry 73: 44-53.
106. Scharf M (2007). Long-term effects of trauma: psychosocial functioning of the second and third generation of Holocaust survivors. Dev Psychopathol 19: 603-622.
107. Seisenberger S, Peat JR, Hore TA, Santos F, Dean W, Reik W (2013). Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos Trans R Soc Lond B Biol Sci 368: 20110330.
108. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F et al. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48: 849-862.
109. Sigal JJ, DiNicola VF, Buonvino M (1988). Grandchildren of survivors: can negative effects of prolonged exposure to excessive stress be observed two generations later? Can J Psychiatry 33: 207-212.
110. Skinner MK, Anway MD, Savenkova MI, Gore AC, Crews D (2008). Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS One 3: e3745.
111. Slatkin M (2009). Epigenetic inheritance and the missing heritability problem. Genetics 182: 845-850.
112. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A et al. (2011). Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet 43: 811-814.
113. Smith AK, Jeffrey Newport D, Ashe MP, Brennan PA, Laprairie JL, Calamaras M et al. (2011). Predictors of neonatal hypothalamic-pituitary-adrenal axis activity at delivery. Clin Endocrinol (Oxf) 75: 90-95.
114. Smith SE, Li J, Garbett K, Mirnics K, Patterson PH (2007). Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 27: 10695-10702.
115. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A et al. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484: 339-344.
116. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN et al. (2004). Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558: 263-275.
117. Szutorisz H, Dinieri JA, Sweet E, Egervari G, Michaelides M, Carter JM et al. (2014). Parental THC exposure leads to compulsive heroin-seeking and altered striatal synaptic plasticity in the subsequent generation. Neuropsychopharmacology 39: 1315-1323.
118. Tillfors M, Furmark T, Ekselius L, Fredrikson M (2001). Social phobia and avoidant personality disorder as related to parental history of social anxiety: a general population study. Behav Res Ther 39: 289-298.
119. Turner BM (2007). Defining an epigenetic code. Nat Cell Biol 9: 2-6.
120. Vallée M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S (1997). Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17: 2626-2636.
121. Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and selfreported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33: 536-545.
122. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC (2013). Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16: 42-47.
123. Veenema AH, Reber SO, Selch S, Obermeier F, Neumann ID (2008). Early life stress enhances the vulnerability to chronic psychosocial stress and experimental colitis in adult mice. Endocrinology 149: 2727-2736.
124. Wagner KD, Wagner N, Ghanbarian H, Grandjean V, Gounon P, Cuzin F et al. (2008). RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell 14: 962-969.
125. Waterland RA, Jirtle RL (2003). Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23: 5293-5300.
126. Waterland RA, Travisano M, Tahiliani KG (2007). Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J 21: 3380-3385.
127. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG (2006). Maternal methyl supplements increase offspring DNA methylation at Axin Fused. Genesis 44: 401-406.
128. Wehmer F, Porter RH, Scales B (1970). Pre-mating and pregnancy stress in rats affects behaviour of grandpups. Nature 227: 622.
129. Weiss IC, Franklin TB, Vizi S, Mansuy IM (2011). Inheritable effect of unpredictable maternal separation on behavioral responses in mice. Front Behav Neurosci 5: 3.
130. Weissman MM, Jensen P (2002). What research suggests for depressed women with children. J Clin Psychiatry 63: 641-647.
131. Whitelaw NC, Whitelaw E (2008). Transgenerational epigenetic inheritance in health and disease. Curr Opin Genet Dev 18: 273-279.
132. Wolff GL, Kodell RL, Moore SR, Cooney CA (1998). Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12: 949-957.
133. Yehuda R, Bell A, Bierer LM, Schmeidler J (2008). Maternal, not paternal, PTSD is related to increased risk for PTSD in offspring of Holocaust survivors. J Psychiatr Res 42: 1104-1111.
134. Zarrow MX, Philpott JE, Denenberg VH (1970). Passage of 14C-4-corticosterone from the rat mother to the foetus and neonate. Nature 226: 1058-1059.
135. Zerbo O, Qian Y, Yoshida C, Grether JK, Van de Water J, Croen LA (2013). Maternal Infection during pregnancy and autism spectrum disorders. J Autism Dev Disord (e-pub ahead of print).