Maternal prenatal depression is associated with decreased placental expression of the imprinted gene PEG3

Psychological Medicine

Volumn 46, Issue 14, 2016, Pages 2999-3011

  Janssen, A B ^a   Capron, L E ^b   O'Donnell, K ^c   Tunster, S J ^a   Ramchandani, P G ^b   Heazell, A E P ^d   Glover, V ^b   John, R M ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Human placental lactogen; PEG3; prenatal depression

Indexed keywords

KRUPPEL LIKE FACTOR; PEG3 PROTEIN, HUMAN; PLACENTA LACTOGEN;

ADULT; COHORT ANALYSIS; DEPRESSION; ENGLAND; FEMALE; GENE EXPRESSION; GENETICS; GENOME IMPRINTING; HUMAN; METABOLISM; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; SEX DIFFERENCE;

ADULT; COHORT STUDIES; DEPRESSION; ENGLAND; FEMALE; GENE EXPRESSION; GENOMIC IMPRINTING; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; PLACENTA; PLACENTAL LACTOGEN; PREGNANCY; PREGNANCY COMPLICATIONS; SEX FACTORS;

EID: 84982099163     PISSN: 00332917     EISSN: 14698978     Source Type: Journal    
DOI: 10.1017/S0033291716001598     Document Type: Article

References (69)

1. Abou-Saleh MT, Ghubash R, Karim L, Krymski M, Bhai I (1998). Hormonal aspects of postpartum depression. Psychoneuroendocrinology 23, 465-475.
2. Apostolidou S, Abu-Amero S, O'Donoghue K, Frost J, Olafsdottir O, Chavele K, Whittaker J, Loughna P, Stanier P, Moore G (2007). Elevated placental expression of the imprinted PHLDA2 gene is associated with low birth weight. Journal of Molecular Medicine 85, 379-387.
3. Asher I, Kaplan B, Modai I, Neri A, Valevski A,Weizman A (1995). Mood and hormonal changes during late pregnancy and puerperium. Clinical and Experimental Obstetrics and Gynecology 22, 321-325.
4. Blakeley PM, Capron LE, Jensen AB, O'Donnell KJ, Glover V (2013). Maternal prenatal symptoms of depression and down regulation of placental monoamine oxidase A expression. Journal of Psychosomatic Research 75, 341-345.
5. Bridges RS, DiBiase R, Loundes DD, Doherty PC (1985). Prolactin stimulation of maternal behavior in female rats. Science 227, 782-784.
6. Bridges RS, Freemark MS (1995). Human placental lactogen infusions into the medial preoptic area stimulate maternal behavior in steroid-primed, nulliparous female rats. Hormones and Behaviour 29, 216-226.
7. Bridges RS, Grattan DR (2003). Prolactin-induced neurogenesis in the maternal brain. Trends in Endocrinology and Metabolism 14, 199-201.
8. Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE (1990). Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proceedings of the National Academy of Sciences USA 87, 8003-8007.
9. Bridges RS, Robertson MC, Shiu RP, Sturgis JD, Henriquez BM, Mann PE (1997). Central lactogenic regulation of maternal behavior in rats: steroid dependence, hormone specificity, and behavioral potencies of rat prolactin and rat placental lactogen I. Endocrinology 138, 756-763.
10. Broad KD, Keverne EB (2011). Placental protection of the fetal brain during short-term food deprivation. Proceedings of the National Academy of Sciences USA 108, 15237-15241.
11. Champagne FA, Curley J, Swaney W, Hasen N, Keverne EB (2009). Paternal influence on female behavior: the role of Peg3 in exploration, olfaction, and neuroendocrine regulation of maternal behavior of female mice. Behavioral Neuroscience 123, 469-480.
12. Chiavegatto S, Sauce B, Ambar G, Cheverud JM, Peripato AC (2012). Hypothalamic expression of Peg3 gene is associated with maternal care differences between SM/J and LG/J mouse strains. Brain and Behavior 2, 365-376.
13. Cleal JK, Day P, Hanson MA, Lewis RM (2009). Measurement of housekeeping genes in human placenta. Placenta 30, 1002-1003.
14. Cleal JK, Day PL, Hanson MA, Lewis RM (2010). Sex differences in the mRNA levels of housekeeping genes in human placenta. Placenta 31, 556-557.
15. Clifton VL (2010). Review: Sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 31 (Suppl.), S33-S39.
16. Cox JL, Chapman G, Murray D, Jones P (1996). Validation of the Edinburgh Postnatal Depression Scale (EPDS) in non-postnatal women. Journal of Affective Disorders 39, 185-189.
17. Cox JL, Holden JM, Sagovsky R (1987). Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. British Journal of Psychiatry 150, 782-786.
18. Curley JP, Pinnock SB, Dickson SL, Thresher R, Miyoshi N, Surani MA, Keverne EB (2005). Increased body fat in mice with a targeted mutation of the paternally expressed imprinted gene Peg3. FASEB Journal 19, 1302-1304.
19. de Tychey C, Briancon S, Lighezzolo J, Spitz E, Kabuth B, de Luigi V, Messembourg C, Girvan F, Rosati A, Thockler A, Vincent S (2008). Quality of life, postnatal depression and baby gender. Journal of Clinical Nursing 17, 312-322.
20. Diplas AI, Lambertini L, Lee M-J, Sperling R, Lee YL, Wetmur JG, Chen J (2009). Differential expression of imprinted genes in normal and IUGR human placentas. Epigenetics 4, 235-240.
21. Dutton PJ, Warrander LK, Roberts SA, Bernatavicius G, Byrd LM, Gaze D, Kroll J, Jones RL, Sibley CP, Froen JF, Heazell AE (2012). Predictors of poor perinatal outcome following maternal perception of reduced fetal movements-a prospective cohort study. PLOS ONE 7, e39784.
22. Feng W, Marquez RT, Lu Z, Liu J, Lu KH, Issa JP, Fishman DM, Yu Y, Bast Jr. RC (2008). Imprinted tumor suppressor genes ARHI and PEG3 are the most frequently down-regulated in human ovarian cancers by loss of heterozygosity and promoter methylation. Cancer 112, 1489-1502.
23. Fritz MS, Mackinnon DP (2007). Required sample size to detect the mediated effect. Psychological Science 18, 233-239.
24. Gerardin P, Wendland J, Bodeau N, Galin A, Bialobos S, Tordjman S, Mazet P, Darbois Y, Nizard J, Dommergues M, Cohen D (2011). Depression during pregnancy: is the developmental impact earlier in boys? A prospective case-control study. Journal of Clinical Psychiatry 72, 378-387.
25. Glover V, Hill J (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: an evolutionary perspective. Physiology and Behavior 106, 736-740.
26. Glynn LM, Sandman CA (2011). Prenatal origins of neurological development: a critical period for fetus and mother. Current Directions in Psychological Science 20, 384-389.
27. Green BB, Kappil M, Lambertini L, Armstrong DA, Guerin DJ, Sharp AJ, Lester BM, Chen J, Marsit CJ (2015). Expression of imprinted genes in placenta is associated with infant neurobehavioral development. Epigenetics 10, 834-841.
28. Groer MW, Morgan K (2007). Immune, health and endocrine characteristics of depressed postpartum mothers. Psychoneuroendocrinology 32, 133-139.
29. Gude NM, Roberts CT, Kalionis B, King RG (2004). Growth and function of the normal human placenta. Thrombosis Research 114, 397-407.
30. Haig D (2008). Placental growth hormone-related proteins and prolactin-related proteins. Placenta 29 (Suppl. A), S36-S41.
31. Hayes A (2013). Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-based Approach. Guilford Press: New York.
32. Ingram J, Greenwood R, Woolridge M (2003). Hormonal predictors of postnatal depression at 6 months in breastfeeding women. Journal of Reproductive and Infant Psychology 21, 61-68.
33. Janssen AB, Kertes DA, McNamara GI, Braithwaite EC, Creeth HD, Glover VI, John RM (2016). A role for the placenta in programming maternal mood and childhood behavioural disorders. Journal of Neuroendocrinology. Published online 2 February 2016. doi:10.1111/jne.12373.
34. Janssen AB, Tunster SJ, Savory N, Holmes A, Beasley J, Parveen SA, Penketh RJ, John RM (2015). Placental expression of imprinted genes varies with sampling site and mode of delivery. Placenta 36, 790-795.
35. Jensen AB, Tunster SJ, John RM (2014). The significance of elevated placental PHLDA2 in human growth restricted pregnancies. Placenta 35, 528-532.
36. Jensen Pena C, Monk C, Champagne FA (2012). Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLOS ONE 7, e39791.
37. John RM (2013). Epigenetic regulation of placental endocrine lineages and complications of pregnancy. Biochemical Society Transactions 41, 701-709.
38. Khashan AS, McNamee R, Abel KM, Pedersen MG, Webb RT, Kenny LC, Mortensen PB, Baker PN (2008). Reduced infant birthweight consequent upon maternal exposure to severe life events. Psychosomatic Medicine 70, 688-694.
39. Kim J, Frey WD, He H, Kim H, Ekram MB, Bakshi A, Faisal M, Perera BP, Ye A, Teruyama R (2013). Peg3 mutational effects on reproduction and placenta-specific gene families. PLOS ONE 8, e83359.
40. Lagerberg D, Magnusson M (2012). Infant gender and postpartum sadness in the light of region of birth and some other factors: a contribution to the knowledge of postpartum depression. Archives of Women's Mental Health 15, 121-130.
41. Lefebvre L, Viville S, Barton SC, Ishino F, Keverne EB, Surani MA (1998). Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nature Genetics 20, 163-169.
42. Li J, Olsen J, Vestergaard M, Obel C (2010). Attention-deficit/ hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. European Child and Adolescent Psychiatry 19, 747-753.
43. Li LL, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA (1999). Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284, 330-334.
44. Liu Y, Murphy SK, Murtha AP, Fuemmeler BF, Schildkraut J, Huang Z, Overcash F, Kurtzberg J, Jirtle R, Iversen ES, Forman MR, Hoyo C (2012). Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements. Epigenetics 7, 735-746.
45. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-delta delta C(T)) method. Methods 25, 402-408.
46. Mairesse J, Lesage J, Breton C, Breant B, Hahn T, Darnaudery M, Dickson SL, Seckl J, Blondeau B, Vieau D, Maccari S, Viltart O (2007). Maternal stress alters endocrine function of the feto-placental unit in rats. American Journal of Physiology. Endocrinology and Metabolism 292, E1526-E1533.
47. McNamara GI, Isles AR (2014). Influencing the social group: the role of imprinted genes. Advances in Genetics 86, 107-134.
48. Meller M, Vadachkoria S, Luthy DA, Williams MA (2005). Evaluation of housekeeping genes in placental comparative expression studies. Placenta 26, 601-607.
49. Murthi P, Fitzpatrick E, Borg AJ, Donath S, Brennecke SP, Kalionis B (2008). GAPDH, 18S rRNA and YWHAZ are suitable endogenous reference genes for relative gene expression studies in placental tissues from human idiopathic fetal growth restriction. Placenta 29, 798-801.
50. Newbern D, Freemark M (2011). Placental hormones and the control of maternal metabolism and fetal growth. Current Opinion in Endocrinology, Diabetes and Obesity 18, 409-416.
51. O'Donnell K, O'Connor TG, Glover V (2009). Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Developmental Neuroscience 31, 285-292.
52. O'Donnell KJ, Bugge Jensen A, Freeman L, Khalife N, O'Connor TG, Glover V (2012). Maternal prenatal anxiety and downregulation of placental 11β-HSD2.1 Psychoneuroendocrinology 37, 818-826.
53. Pearson RM, Melotti R, Heron J, Joinson C, Stein A, Ramchandani PG, Evans J (2012). Disruption to the development of maternal responsiveness? The impact of prenatal depression on mother-infant interactions. Infant Behavior and Development 35, 613-626.
54. Radford EJ, Isganaitis E, Jimenez-Chillaron J, Schroeder J, Molla M, Andrews S, Didier N, Charalambous M, McEwen K, Marazzi G, Sassoon D, Patti ME, Ferguson-Smith AC (2012). An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genetics 8, e1002605.
55. Reynolds RM, Pesonen AK, O'Reilly JR, Tuovinen S, Lahti M, Kajantie E, Villa PM, Laivuori H, Hamalainen E, Seckl JR, Raikkonen K (2015). Maternal depressive symptoms throughout pregnancy are associated with increased placental glucocorticoid sensitivity. Psychological Medicine 45, 2023-2030.
56. Roh CR, Budhraja V, Kim HS, Nelson DM, Sadovsky Y (2005). Microarray-based identification of differentially expressed genes in hypoxic term human trophoblasts and in placental villi of pregnancies with growth restricted fetuses. Placenta 26, 319-328.
57. Rondo PHC, Ferreira RF, Nogueira F, Ribeiro MCN, Lobert H, Artes R (2003). Maternal psychological stress and distress as predictors of low birth weight, prematurity and intrauterine growth retardation. European Journal of Clinical Nutrition 57, 266-272.
58. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003). Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299, 117-120.
59. Smith FM, Garfield AS,Ward A (2006). Regulation of growth and metabolism by imprinted genes. Cytogenetic and Genome Research 113, 279-291.
60. Steer RA, Scholl TO, Hediger ML, Fischer RL (1992). Self-reported depression and negative pregnancy outcomes. Journal of Clinical Epidemiology 45, 1093-1099.
61. Surani MA (1998). Imprinting and the initiation of gene silencing in the germ line. Cell 93, 309-312.
62. Talge NM, Neal C, Glover V (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? Journal of Child Psychology and Psychiatry 48, 245-261.
63. Torner L, Toschi N, Pohlinger A, Landgraf R, Neumann ID (2001). Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. Journal of Neuroscience 21, 3207-3214.
64. Tunster SJ, Jensen AB, John RM (2013). Imprinted genes in mouse placental development and the regulation of fetal energy stores. Reproduction 145, R117-R137.
65. Van den Bergh BR, Mulder EJ, Mennes M, Glover V (2005). Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neuroscience and Biobehavioral Reviews 29, 237-258.
66. van Os J, Selten JP (1998). Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. British Journal of Psychiatry 172, 324-326.
67. Vidal AC, Benjamin Neelon SE, Liu Y, Tuli AM, Fuemmeler BF, Hoyo C, Murtha AP, Huang Z, Schildkraut J, Overcash F, Kurtzberg J, Jirtle RL, Iversen ES, Murphy SK (2014). Maternal stress, preterm birth, and DNA methylation at imprint regulatory sequences in humans. Genetics and Epigenetics 6, 37-44.
68. Walker TL, Vukovic J, Koudijs MM, Blackmore DG, Mackay EW, Sykes AM, Overall RW, Hamlin AS, Bartlett PF (2012). Prolactin stimulates precursor cells in the adult mouse hippocampus. PLOS ONE 7, e44371.
69. Warrander LK, Batra G, Bernatavicius G, Greenwood SL, Dutton P, Jones RL, Sibley CP, Heazell AE (2012). Maternal perception of reduced fetal movements is associated with altered placental structure and function. PLOS ONE 7, e34851.