The effect of antenatal depression and selective serotonin reuptake inhibitor treatment on nerve growth factor signaling in human placenta

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Kaihola, Helena ^a   Olivier, Jocelien ^a,b   Poromaa, Inger Sundström ^a   Åkerud, Helena ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR; PROTEIN TYROSINE KINASE A; RAF PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK1 SIGNAL PROTEIN; ROCK2 SIGNALING PROTEIN; SEROTONIN UPTAKE INHIBITOR; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; NGF PROTEIN, HUMAN; PLACENTA PROTEIN; RHO KINASE; ROCK2 PROTEIN, HUMAN; TRKA PROTEIN, E COLI;

ADULT; ANTENATAL DEPRESSION; ARTICLE; CELL LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN TISSUE; PLACENTA DISORDER; PLACENTA FUNCTION; PRENATAL DISORDER; PROTEIN DETERMINATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STROMA CELL; TROPHOBLAST; DRUG EFFECTS; METABOLISM; PREGNANCY; PREGNANCY COMPLICATIONS;

ADULT; DEPRESSION; ENDOTHELIAL CELLS; ESCHERICHIA COLI PROTEINS; FEMALE; HUMANS; NERVE GROWTH FACTOR; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY PROTEINS; PROTO-ONCOGENE PROTEINS C-RAF; RHO-ASSOCIATED KINASES; SEROTONIN UPTAKE INHIBITORS; SIGNAL TRANSDUCTION; TROPHOBLASTS;

EID: 84921791841     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116459     Document Type: Article

References (73)

1. Patkar AA, Bilal L, Masand PS (2004) Pharmacotherapy of depression in pregnancy. Ann Clin Psychiatry 16: 87-100.
2. Andersson L, Sundstrom-Poromaa I, Bixo M, Wulff M, Bondestam K, et al. (2003) Point prevalence of psychiatric disorders during the second trimester of pregnancy: a population-based study. Am J Obstet Gynecol 189: 148-154. PMID: 12861154
3. Gorman LL, O'Hara MW, Figueiredo B, Hayes S, Jacquemain F, et al. (2004) Adaptation of the structured clinical interview for DSM-IV disorders for assessing depression in women during pregnancy and post-partum across countries and cultures. Br J Psychiatry Suppl 46: s17-23. PMID: 14754814
4. Melville JL, Gavin A, Guo Y, Fan MY, Katon WJ (2010) Depressive disorders during pregnancy: prevalence and risk factors in a large urban sample. Obstet Gynecol 116: 1064-1070. doi: 10.1097/AOG. 0b013e3181f60b0a PMID: 20966690
5. Barbey JT, Roose SP (1998) SSRI safety in overdose. J Clin Psychiatry 59 Suppl 15: 42-48.
6. Gentile S (2005) SSRIs in pregnancy and lactation: emphasis on neurodevelopmental outcome. CNS Drugs 19: 623-633. PMID: 15984897
7. Oberlander TF, Warburton W, Misri S, Aghajanian J, Hertzman C (2006) Neonatal outcomes after prenatal exposure to selective serotonin reuptake inhibitor antidepressants and maternal depression using population-based linked health data. Arch Gen Psychiatry 63: 898-906. PMID: 16894066
8. Kieler H, Artama M, Engeland A, Ericsson O, Furu K, et al. (2012) Selective serotonin reuptake inhibitors during pregnancy and risk of persistent pulmonary hypertension in the newborn: population based cohort study from the five Nordic countries. BMJ 344: d8012. doi: 10.1136/bmj.d8012 PMID: 22240235
9. El Marroun H, Jaddoe VW, Hudziak JJ, Roza SJ, Steegers EA, et al. (2012) Maternal use of selective serotonin reuptake inhibitors, fetal growth, and risk of adverse birth outcomes. Arch Gen Psychiatry 69: 706-714. PMID: 22393202
10. Heikkinen T, Ekblad U, Palo P, Laine K (2003) Pharmacokinetics of fluoxetine and norfluoxetine in pregnancy and lactation. Clin Pharmacol Ther 73: 330-337. PMID: 12709723
11. Noorlander CW, Ververs FF, Nikkels PG, van Echteld CJ, Visser GH, et al. (2008) Modulation of serotonin transporter function during fetal development causes dilated heart cardiomyopathy and lifelong behavioral abnormalities. PLoS One 3: e2782. doi: 10.1371/journal.pone.0002782 PMID: 18716672
12. Hendrick V, Stowe ZN, Altshuler LL, Hwang S, Lee E, et al. (2003) Placental passage of antidepressant medications. Am J Psychiatry 160: 993-996.
13. Loughhead AM, Fisher AD, Newport DJ, Ritchie JC, Owens MJ, et al. (2006) Antidepressants in amniotic fluid: another route of fetal exposure. Am J Psychiatry 163: 145-147. PMID: 16390902
14. Olivier JD, Akerud H, Kaihola H, Pawluski JL, Skalkidou A, et al. (2013) The effects of maternal depression and maternal selective serotonin reuptake inhibitor exposure on offspring. Front Cell Neurosci 7: 73. PMID: 23734100
15. El Marroun H, White T, Verhulst FC, Tiemeier H (2014) Maternal use of antidepressant or anxiolytic medication during pregnancy and childhood neurodevelopmental outcomes: a systematic review. Eur Child Adolesc Psychiatry 23: 973-992. PMID: 24863148
16. Waters CS, Hay DF, Simmonds JR, van Goozen SH (2014) Antenatal depression and children's developmental outcomes: potential mechanisms and treatment options. Eur Child Adolesc Psychiatry 23: 957-971. doi: 10.1007/s00787-014-0582-3 PMID: 25037152
17. Olivier JD, Akerud H, Sundstrom Poromaa I (2014) Antenatal depression and antidepressants during pregnancy: Unraveling the complex interactions for the offspring. Eur J Pharmacol. doi: 10.1016/j. ejphar.2014.07.049 PMID: 25094036
18. Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4: 1002-1012. PMID: 14618156
19. Ansorge MS, Hen R, Gingrich JA (2007) Neurodevelopmental origins of depressive disorders. Curr Opin Pharmacol 7: 8-17.
20. Bonnin A, Goeden N, Chen K, Wilson ML, King J, et al. (2011) A transient placental source of serotonin for the fetal forebrain. Nature 472: 347-350. doi: 10.1038/nature09972 PMID: 21512572
21. Cikos S, Fabian D, Makarevich AV, Chrenek P, Koppel J (2011) Biogenic monoamines in preimplantation development. Hum Reprod 26: 2296-2305.
22. Oufkir T, Arseneault M, Sanderson JT, Vaillancourt C (2010) The 5-HT 2A serotonin receptor enhances cell viability, affects cell cycle progression and activates MEK-ERK1/2 and JAK2-STAT3 signalling pathways in human choriocarcinoma cell lines. Placenta 31: 439-447. doi: 10.1016/j.placenta.2010. 02.019 PMID: 20338635
23. Charnock-Jones DS, Burton GJ (2000) Placental vascular morphogenesis. Baillieres Best Pract Res Clin Obstet Gynaecol 14: 953-968.
24. Bottalico B, Larsson I, Brodszki J, Hernandez-Andrade E, Casslen B, et al. (2004) Norepinephrine transporter (NET), serotonin transporter (SERT), vesicular monoamine transporter (VMAT2) and organic cation transporters (OCT1, 2 and EMT) in human placenta from pre-eclamptic and normotensive pregnancies. Placenta 25: 518-529. PMID: 15135235
25. Viau M, Lafond J, Vaillancourt C (2009) Expression of placental serotonin transporter and 5-HT 2A receptor in normal and gestational diabetes mellitus pregnancies. Reprod Biomed Online 19: 207-215. PMID: 19712556
26. Bhuiyan M, Petropoulos S, Gibb W, Matthews SG (2012) Sertraline alters multidrug resistance phosphoglycoprotein activity in the mouse placenta and fetal blood-brain barrier. Reprod Sci 19: 407-415. doi: 10.1177/1933719111424438 PMID: 22510699
27. Ponder KL, Salisbury A, McGonnigal B, Laliberte A, Lester B, et al. (2011) Maternal depression and anxiety are associated with altered gene expression in the human placenta without modification by antidepressant use: implications for fetal programming. Dev Psychobiol 53: 711-723. doi: 10.1002/dev. 20549 PMID: 21547899
28. Tometten M, Blois S, Arck PC (2005) Nerve growth factor in reproductive biology: link between the immune, endocrine and nervous system? Chem Immunol Allergy 89: 135-148. PMID: 16129960
29. Cantarella G, Lempereur L, Presta M, Ribatti D, Lombardo G, et al. (2002) Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J 16: 1307-1309. PMID: 12154004
30. Chaves RN, Alves AM, Lima LF, Matos HM, Rodrigues AP, et al. (2013) Role of nerve growth factor (NGF) and its receptors in folliculogenesis. Zygote 21: 187-197. PMID: 22651979
31. Toti P, Ciarmela P, Florio P, Volpi N, Occhini R, et al. (2006) Human placenta and fetal membranes express nerve growth factor mRNA and protein. J Endocrinol Invest 29: 337-341. PMID: 16699300
32. Kanai-Azuma M, Kanai Y, Matsuda H, Kurohmaru M, Tachi C, et al. (1997) Nerve growth factor promotes giant-cell transformation of mouse trophoblast cells in vitro. Biochem Biophys Res Commun 231: 309-315. PMID: 9070269
33. Tometten M, Klapp BF, Joachim R, Fest S, Zenclussen AC, et al. (2004) Nerve growth factor and its functional receptor TrkA are up-regulated in murine decidual tissue of stress-triggered and substance P-mediated abortion. Am J Reprod Immunol 51: 86-93. PMID: 14725570
34. Dhobale MV, Pisal HR, Mehendale SS, Joshi SR (2013) Differential expression of human placental neurotrophic factors in preterm and term deliveries. Int J Dev Neurosci 31: 719-723. doi: 10.1016/j. ijdevneu.2013.09.006 PMID: 24076518
35. Dissen GA, Garcia-Rudaz C, Paredes A, Mayer C, Mayerhofer A, et al. (2009) Excessive ovarian production of nerve growth factor facilitates development of cystic ovarian morphology in mice and is a feature of polycystic ovarian syndrome in humans. Endocrinology 150: 2906-2914. doi: 10.1210/en.2008-1575 PMID: 19264868
36. Ross LE, Grigoriadis S, Mamisashvili L, Vonderporten EH, Roerecke M, et al. (2013) Selected Pregnancy and Delivery Outcomes After Exposure to Antidepressant Medication: A Systematic Review and Meta-analysis. JAMA Psychiatry 70: 436-443. doi: 10.1001/jamapsychiatry.2013.684 PMID: 23446732
37. Greene LA, Kaplan DR (1995) Early events in neurotrophin signalling via Trk and p75 receptors. Curr Opin Neurobiol 5: 579-587. PMID: 8580709
38. Fujisawa K, Fujita A, Ishizaki T, Saito Y, Narumiya S (1996) Identification of the Rho-binding domain of p160ROCK, a Rho-associated coiled-coil containing protein kinase. J Biol Chem 271: 23022-23028. PMID: 8798490
39. Sahai E, Ishizaki T, Narumiya S, Treisman R (1999) Transformation mediated by RhoA requires activity of ROCK kinases. Curr Biol 9: 136-145. PMID: 10021386
40. Sahai E, Olson MF, Marshall CJ (2001) Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility. EMBO J 20: 755-766. PMID: 11179220
41. Ehrenreiter K, Piazzolla D, Velamoor V, Sobczak I, Small JV, et al. (2005) Raf-1 regulates Rho signaling and cell migration. J Cell Biol 168: 955-964. PMID: 15753127
42. Gibson J, McKenzie-McHarg K, Shakespeare J, Price J, Gray R (2009) A systematic review of studies validating the Edinburgh Postnatal Depression Scale in antepartum and postpartum women. Acta Psychiatr Scand 119: 350-364. doi: 10.1111/j.1600-0447.2009.01363.x PMID: 19298573
43. Goldstein LD, Reynolds CP, Perez-Polo JR (1978) Isolation of human nerve growth factor from placental tissue. Neurochem Res 3: 175-183. PMID: 566860
44. Heinrich G, Meyer TE (1988) Nerve growth factor (NGF) is present in human placenta and semen, but undetectable in normal and Paget's disease blood: measurements with an anti-mouse-NGF enzyme immunoassay using a recombinant human NGF reference. Biochem Biophys Res Commun 155: 482-486. PMID: 3046616
45. Frank P, Barrientos G, Tirado-Gonzalez I, Cohen M, Moschansky P, et al. (2014) Balanced levels of nerve growth factor are required for normal pregnancy progression. Reproduction 148: 179-189. doi: 10.1530/REP-14-0112 PMID: 24825909
46. Nelissen EC, van Montfoort AP, Dumoulin JC, Evers JL (2011) Epigenetics and the placenta. Hum Reprod Update 17: 397-417.
47. Barker DJ, Bull AR, Osmond C, Simmonds SJ (1990) Fetal and placental size and risk of hypertension in adult life. BMJ 301: 259-262. PMID: 2390618
48. Barker DJ (1995) Intrauterine programming of adult disease. Mol Med Today 1: 418-423.
49. Leon DA (1998) Fetal growth and adult disease. Eur J Clin Nutr 52 Suppl 1: S72-78; discussion S78-82.
50. Forsen T, Osmond C, Eriksson JG, Barker DJ (2004) Growth of girls who later develop coronary heart disease. Heart 90: 20-24.
51. Forsen TJ, Eriksson JG, Osmond C, Barker DJ (2004) The infant growth of boys who later develop coronary heart disease. Ann Med 36: 389-392.
52. Stein C.E. , Fall C.H., Kumaran K., Osmond C., Cox V., et al. (1996) Fetal growth and coronary heart disease in south India. Lancet 348: 1269-1273. PMID: 8909379 53.
53. Masumoto A, Hirooka Y, Shimokawa H, Hironaga K, Setoguchi S, et al. (2001) Possible involvement of Rho-kinase in the pathogenesis of hypertension in humans. Hypertension 38: 1307-1310. PMID: 11751708
54. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, et al. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389: 990-994. PMID: 9353125
55. Mukai Y, Shimokawa H, Matoba T, Kandabashi T, Satoh S, et al. (2001) Involvement of Rho-kinase in hypertensive vascular disease: a novel therapeutic target in hypertension. FASEB J 15: 1062-1064. PMID: 12382411
56. Moriki N, Ito M, Seko T, Kureishi Y, Okamoto R, et al. (2004) RhoA activation in vascular smooth muscle cells from stroke-prone spontaneously hypertensive rats. Hypertens Res 27: 263-270. PMID: 15127884
57. Ark M, Yilmaz N, Yazici G, Kubat H, Aktas S (2005) Rho-associated protein kinase II (rock II) expression in normal and preeclamptic human placentas. Placenta 26: 81-84. PMID: 15664415
58. Toh S, Mitchell AA, Louik C, Werler MM, Chambers CD, et al. (2009) Selective serotonin reuptake inhibitor use and risk of gestational hypertension. Am J Psychiatry 166: 320-328. PMID: 19122006
59. Reis M, Kallen B (2010) Delivery outcome after maternal use of antidepressant drugs in pregnancy: an update using Swedish data. Psychol Med 40: 1723-1733. doi: 10.1017/S0033291709992194 PMID: 20047705
60. Qiu C, Williams MA, Calderon-Margalit R, Cripe SM, Sorensen TK (2009) Preeclampsia risk in relation to maternal mood and anxiety disorders diagnosed before or during early pregnancy. Am J Hypertens 22: 397-402. PMID: 19197246
61. Shimizu T, Fukumoto Y, Tanaka S, Satoh K, Ikeda S, et al. (2013) Crucial role of ROCK2 in vascular smooth muscle cells for hypoxia-induced pulmonary hypertension in mice. Arterioscler Thromb Vasc Biol 33: 2780-2791. doi: 10.1161/ATVBAHA.113.301357 PMID: 24135024
62. Bellissima V, Visser GH, Ververs TF, van Bel F, Termote JU, et al. (2011) Antenatal maternal antidepressants drugs affect Activin A concentrations in maternal blood, in amniotic fluid and in fetal cord blood. J Matern Fetal Neonatal Med 24 Suppl 2: 31-34. doi: 10.3109/14767058.2011.604931 PMID: 21767104
63. Florio P, Gazzolo D, Luisi S, Petraglia F (2007) Activin A in brain injury. Adv Clin Chem 43: 117-130.
64. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4: 496-505.
65. Fatemi SH, Kroll JL, Stary JM (2001) Altered levels of Reelin and its isoforms in schizophrenia and mood disorders. Neuroreport 12: 3209-3215. PMID: 11711858
66. Fatemi SH (2002) The role of Reelin in pathology of autism. Mol Psychiatry 7: 919-920. PMID: 12399938
67. Brummelte S, Galea LA, Devlin AM, Oberlander TF (2013) Antidepressant use during pregnancy and serotonin transporter genotype (SLC6A4) affect newborn serum reelin levels. Dev Psychobiol 55: 518-529. doi: 10.1002/dev.21056 PMID: 22692766
68. Matsui K, Furukawa S, Shibasaki H, Kikuchi T (1990) Reduction of nerve growth factor level in the brain of genetically ataxic mice (weaver, reeler). FEBS Lett 276: 78-80. PMID: 2265716
69. Larios JA, Jausoro I, Benitez ML, Bronfman FC, Marzolo MP (2014) Neurotrophins regulate ApoER2 proteolysis through activation of the Trk signaling pathway. BMC Neurosci 15: 108. doi: 10.1186/1471-2202-15-108 PMID: 25233900
70. Olivier JD, Blom T, Arentsen T, Homberg JR (2011) The age-dependent effects of selective serotonin reuptake inhibitors in humans and rodents: A review. Prog Neuropsychopharmacol Biol Psychiatry 35: 1400-1408. doi: 10.1016/j.pnpbp.2010.09.013 PMID: 20883714
71. Pawluski JL (2012) Perinatal selective serotonin reuptake inhibitor exposure: impact on brain development and neural plasticity. Neuroendocrinology 95: 39-46. doi: 10.1159/000329293 PMID: 21893935
72. Rayen I, Steinbusch HW, Charlier TD, Pawluski JL (2013) Developmental fluoxetine exposure and prenatal stress alter sexual differentiation of the brain and reproductive behavior in male rat offspring. Psychoneuroendocrinology 38: 1618-1629. doi: 10.1016/j.psyneuen.2013.01.007 PMID: 23399049
73. Knaepen L, Rayen I, Charlier TD, Fillet M, Houbart V, et al. (2013) Developmental fluoxetine exposure normalizes the long-term effects of maternal stress on post-operative pain in Sprague-Dawley rat offspring. PLoS One 8: e57608. doi: 10.1371/journal.pone.0057608 PMID: 23437400