Stimulation of serotonergic 5-HT 2A receptor signaling increases placental aromatase (CYP19) activity and expression in BeWo and JEG-3 human choriocarcinoma cells

Placenta

Volumn 32, Issue 9, 2011, Pages 651-656

  Klempan, T ^a   Hudon Thibeault, A A ^a   Oufkir, T ^a   Vaillancourt, C ^a   Sanderson, J T ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

5 HT 2A receptor; BeWo; Estrogens; Gene regulation; Human trophoblast; JEG 3; Placental aromatase (CYP19); Protein kinase C (PKC); Serotonin

Indexed keywords

AROMATASE; DEXAMETHASONE; JANUS KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; RITANSERIN; SEROTONIN; SEROTONIN ANTAGONIST; SEROTONIN RECEPTOR; STAT PROTEIN;

ARTICLE; CHORIOCARCINOMA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AROMATASE; CELL LINE, TUMOR; CHORIOCARCINOMA; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; PLACENTA; PREGNANCY; PROTEIN KINASE C; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN; SEROTONIN 5-HT2 RECEPTOR AGONISTS;

EID: 80052261101     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2011.06.003     Document Type: Article

References (49)

1. T.W. Bonagura, G.J. Pepe, A.C. Enders, and E.D. Albrecht Suppression of extravillous trophoblast vascular endothelial growth factor expression and uterine spiral artery invasion by estrogen during early baboon pregnancy Endocrinology 149 10 2008 5078 5087
2. R. Yashwanth, S. Rama, M. Anbalagan, and A.J. Rao Role of estrogen in regulation of cellular differentiation: a study using human placental and rat Leydig cells Mol Cell Endocrinol 246 1-2 2006 114 120 (Pubitemid 43238404)
3. A. Bukovsky, M. Cekanova, M.R. Caudle, J. Wimalasena, J.S. Foster, and D.C. Henley Expression and localization of estrogen receptor-alpha protein in normal and abnormal term placentae and stimulation of trophoblast differentiation by estradiol Reprod Biol Endocrinol 1 2003 13
4. D.R. Nelson, T. Kamataki, D.J. Waxman, F.P. Guengerich, R.W. Estabrook, and R. Feyereisen The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature DNA Cell Biol 12 1 1993 1 51 (Pubitemid 23064489)
5. N. Fournet-Dulguerov, N.J. MacLusky, C.Z. Leranth, R. Todd, C.R. Mendelson, and E.R. Simpson Immunohistochemical localization of aromatase cytochrome P-450 and estradiol dehydrogenase in the syncytiotrophoblast of the human placenta J Clin Endocrinol Metab 65 4 1987 757 764 (Pubitemid 17157398)
6. X. Wu, T. Iguchi, N. Itoh, K. Okamoto, T. Takagi, and K. Tanaka Ascorbic acid transported by sodium-dependent vitamin C transporter 2 stimulates steroidogenesis in human choriocarcinoma cells Endocrinology 149 1 2008 73 83
7. R.S. Bahn, A. Worsham, K.V. Speeg Jr., M. Ascoli, and D. Rabin Characterization of steroid production in cultured human choriocarcinoma cells J Clin Endocrinol Metab 52 3 1981 447 450 (Pubitemid 11136554)
8. E.R. Simpson, M.S. Mahendroo, G.D. Means, M.W. Kilgore, M.M. Hinshelwood, and S. Graham-Lorence Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis Endocr Rev 15 3 1994 342 355 (Pubitemid 24180792)
9. M. Demura, S. Reierstad, J.E. Innes, and S.E. Bulun Novel promoter I.8 and promoter usage in the CYP19 (aromatase) gene Reprod Sci 15 10 2008 1044 1053
10. C.R. Mendelson, and A. Kamat Mechanisms in the regulation of aromatase in developing ovary and placenta J Steroid Biochem Mol Biol 106 1-5 2007 62 70 (Pubitemid 47362643)
11. D. Barrera, E. Avila, G. Hernandez, A. Halhali, B. Biruete, and F. Larrea Estradiol and progesterone synthesis in human placenta is stimulated by calcitriol J Steroid Biochem Mol Biol 103 3-5 2007 529 532 (Pubitemid 46401361)
12. K. Yamada, H. Ogawa, S. Honda, N. Harada, and T. Okazaki A GCM motif protein is involved in placenta-specific expression of human aromatase gene J Biol Chem 274 45 1999 32279 32286
13. B. Jiang, A. Kamat, and C.R. Mendelson Hypoxia prevents induction of aromatase expression in human trophoblast cells in culture: potential inhibitory role of the hypoxia-inducible transcription factor Mash-2 (mammalian achaete-scute homologous protein-2) Mol Endocrinol 14 10 2000 1661 1673
14. O. Ritvos, and R. Voutilainen Regulation of aromatase cytochrome P-450 and 17 beta-hydroxysteroid dehydrogenase messenger ribonucleic acid levels in choriocarcinoma cells Endocrinology 130 1 1992 61 67
15. N. Harada, N. Yoshimura, and S. Honda Unique regulation of expression of human aromatase in the placenta J Steroid Biochem Mol Biol 86 3-5 2003 327 334 (Pubitemid 37412572)
16. Deroy K, St-Pierre J, Sanderson J, Vaillancourt C. Human placental trophoblasts produce serotonin de novo. In: International serotonin club conference, Serotonin: The New Wave New Developments in Serotonin Research; 2010.
17. T. Oufkir, M. Arseneault, J.T. Sanderson, and C. Vaillancourt 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 5 2010 439 447
18. S.L. Liang, and J.T. Pan An endogenous serotonergic rhythm acting on 5-HT(2A) receptors may be involved in the diurnal changes in tuberoinfundibular dopaminergic neuronal activity and prolactin secretion in female rats Neuroendocrinology 72 1 2000 11 19
19. H. Lefebvre, P. Compagnon, V. Contesse, C. Delarue, C. Thuillez, and H. Vaudry Production and metabolism of serotonin (5-HT) by the human adrenal cortex: paracrine stimulation of aldosterone secretion by 5-HT J Clin Endocrinol Metab 86 10 2001 5001 5007 (Pubitemid 33020556)
20. C.M. Foran, J. Weston, M. Slattery, B.W. Brooks, and D.B. Huggett Reproductive assessment of Japanese medaka (Oryzias latipes) following a four-week fluoxetine (SSRI) exposure Arch Environ Contam Toxicol 46 4 2004 511 517 (Pubitemid 38529646)
21. R. Yang, X. You, X. Tang, L. Gao, and X. Ni Corticotropin-releasing hormone inhibits progesterone production in cultured human placental trophoblasts J Mol Endocrinol 37 3 2006 533 540
22. T. Sanderson, M. Renaud, D. Scholten, S. Nijmeijer, M. van den Berg, and S. Cowell Effects of lactone derivatives on aromatase (CYP19) activity in H295R human adrenocortical and (anti)androgenicity in transfected LNCaP human prostate cancer cells Eur J Pharmacol 593 1-3 2008 92 98
23. J.T. Sanderson, W. Seinen, J.P. Giesy, and M. van den Berg 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 54 1 2000 121 127 (Pubitemid 30152463)
24. E.D. Lephart, and E.R. Simpson Assay of aromatase activity Meth Enzymol 206 1991 477 483
25. J.T. Sanderson, R.J. Letcher, M. Heneweer, J.P. Giesy, and M. van den Berg Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes Environ Health Perspect 109 10 2001 1027 1031 (Pubitemid 33100408)
26. A. Kamat, J.L. Alcorn, C. Kunczt, and C.R. Mendelson Characterization of the regulatory regions of the human aromatase (P450arom) gene involved in placenta-specific expression Mol Endocrinol 12 11 1998 1764 1777 (Pubitemid 28492452)
27. S.E. Bulun, S. Sebastian, K. Takayama, T. Suzuki, H. Sasano, and M. Shozu The human CYP19 (aromatase P450) gene: update on physiologic roles and genomic organization of promoters J Steroid Biochem Mol Biol 86 3-5 2003 219 224 (Pubitemid 37412560)
28. J.T. Sanderson, J. Hordijk, M.S. Denison, M.F. Springsteel, M.H. Nantz, and M. Van Den Berg Induction and inhibition of aromatase (CYP19) activity by natural and synthetic flavonoid compounds in H295R human adrenocortical carcinoma cells Toxicol Sci 82 2004 70 79 (Pubitemid 39485321)
29. G. Martiny-Baron, M.G. Kazanietz, H. Mischak, P.M. Blumberg, G. Kochs, and H. Hug Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976 J Biol Chem 268 13 1993 9194 9197 (Pubitemid 23145960)
30. S. Al-Nasiry, B. Spitz, M. Hanssens, C. Luyten, and R. Pijnenborg Differential effects of inducers of syncytialization and apoptosis on BeWo and JEG-3 choriocarcinoma cells Hum Reprod 21 1 2006 193 201 (Pubitemid 41794311)
31. M. Bilban, S. Barth, M. Cervar, R. Mauschitz, R.J. Schaur, and F. Zivkovic Differential regulation of endothelin secretion and endothelin receptor mRNA levels in JAR, JEG-3, and BeWo choriocarcinoma cell lines and in human trophoblasts, their nonmalignant counterpart Arch Biochem Biophys 382 2 2000 245 252
32. H.P. Hohn, M. Linke, B. Ugele, and H.W. Denker Differentiation markers and invasiveness: discordant regulation in normal trophoblast and choriocarcinoma cells Exp Cell Res 244 1 1998 249 258 (Pubitemid 28480872)
33. T. Nakanishi, J. Kohroki, S. Suzuki, J. Ishizaki, Y. Hiromori, and S. Takasuga Trialkyltin compounds enhance human CG secretion and aromatase activity in human placental choriocarcinoma cells J Clin Endocrinol Metab 87 6 2002 2830 2837 (Pubitemid 34655351)
34. D.W. Burleigh, C.M. Kendziorski, Y.J. Choi, K.M. Grindle, R.L. Grendell, and R.R. Magness Microarray analysis of BeWo and JEG3 trophoblast cell lines: identification of differentially expressed transcripts Placenta 28 5-6 2007 383 389 (Pubitemid 46593757)
35. A.G. Imir, Z. Lin, P. Yin, S. Deb, B. Yilmaz, and M. Cetin Aromatase expression in uterine leiomyomata is regulated primarily by proximal promoters I.3/II J Clin Endocrinol Metab 92 5 2007 1979 1982 (Pubitemid 46997221)
36. C.R. Mendelson, B. Jiang, J.M. Shelton, J.A. Richardson, and M.M. Hinshelwood Transcriptional regulation of aromatase in placenta and ovary J Steroid Biochem Mol Biol 95 1-5 2005 25 33 (Pubitemid 41137290)
37. A. Kamat, M.E. Smith, J.M. Shelton, J.A. Richardson, and C.R. Mendelson Genomic regions that mediate placental cell-specific and developmental regulation of human CYP19 (aromatase) gene expression in transgenic mice Endocrinology 146 5 2005 2481 2488 (Pubitemid 40577537)
38. S. Luo, H. Yu, D. Wu, and C. Peng Transforming growth factor-beta1 inhibits steroidogenesis in human trophoblast cells Mol Hum Reprod 8 4 2002 318 325 (Pubitemid 34303239)
39. K. Toda, L.X. Yang, and Y. Shizuta Transcriptional regulation of the human aromatase cytochrome P450 gene expression in human placental cells J Steroid Biochem Mol Biol 53 1-6 1995 181 190
40. J. Wang, and S. Chen Induction of aromatase gene expression in human placental choriocarcinoma (JAR) cells by phorbol esters Biochim Biophys Acta 1218 1994 48 54 (Pubitemid 24156190)
41. A.K. Banes, S.M. Shaw, A. Tawfik, B.P. Patel, S. Ogbi, and D. Fulton Activation of the JAK/STAT pathway in vascular smooth muscle by serotonin Am J Physiol Cell Physiol 288 4 2005 C805 C812
42. 2A receptor-stimulated phospholipase C signalling by olanzapine, clozapine and MDL 100907 Int J Neuropsychopharmacol 12 5 2009 651 665
43. Y. Zhao, J.E. Nichols, S.E. Bulun, C.R. Mendelson, and E.R. Simpson Aromatase P450 gene expression in human adipose tissue. Role of a Jak/STAT pathway in regulation of the adipose-specific promoter J Biol Chem 270 27 1995 16449 16457
44. A. Bonnin, N. Goeden, K. Chen, M.L. Wilson, J. King, and J.C. Shih A transient placental source of serotonin for the fetal forebrain Nature 472 7343 2011 347 350
45. B. Kallen The safety of antidepressant drugs during pregnancy Expert Opin Drug Saf 6 4 2007 357 370 (Pubitemid 351308164)
46. C.M. Way Safety of newer antidepressants in pregnancy Pharmacotherapy 27 4 2007 546 552 (Pubitemid 46536236)
47. K.L. Wisner, D.K. Sit, B.H. Hanusa, E.L. Moses-Kolko, D.L. Bogen, and D.F. Hunker Major depression and antidepressant treatment: impact on pregnancy and neonatal outcomes Am J Psychiatry 166 5 2009 557 566
48. A.C. Bolte, H.P. van Geijn, and G.A. Dekker Pathophysiology of preeclampsia and the role of serotonin Eur J Obstet Gynecol Reprod Biol 95 1 2001 12 21 (Pubitemid 32208665)
49. M. Viau, J. Lafond, and C. Vaillancourt Expression of placental serotonin transporter and 5-HT 2A receptor in normal and gestational diabetes mellitus pregnancies Reprod Biomed Online 19 2 2009 207 215