Folic acid uptake by the human syncytiotrophoblast: Interference by pharmacotherapy, drugs of abuse and pathological conditions

Reproductive Toxicology

Volumn 28, Issue 4, 2009, Pages 511-520

  Keating, Elisa ^a   Gonçalves, Pedro ^a   Campos, Isabel ^b   Costa, Fernanda ^b   Martel, Fátima ^a  

^a University of Porto   (Portugal)

^b HOSPITAL DE SÃO JOÃO   (Portugal)

Author keywords

Anti hypertensives; Drugs of abuse; Folate receptor ; Folic acid; Placenta; Proton coupled folate transporter; Reduced folate carrier; Xenobiotics

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; AMPHETAMINE; ATENOLOL; CLONIDINE; FOLIC ACID; LABETALOL; MESSENGER RNA; METHYLDOPA; TETRAHYDROCANNABINOL;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; CYTOTROPHOBLAST; FETOTOXICITY; GENE EXPRESSION; HUMAN; HUMAN CELL; PLACENTAL TRANSFER; SYNCYTIOTROPHOBLAST;

AMPHETAMINE; ANTIHYPERTENSIVE AGENTS; ATENOLOL; BIOLOGICAL TRANSPORT; CELL SURVIVAL; CELLS, CULTURED; DIABETES MELLITUS; DOSE-RESPONSE RELATIONSHIP, DRUG; ECLAMPSIA; ETHANOL; FEMALE; FOLIC ACID; GENE EXPRESSION; GLUCOSE; HUMANS; HYDROGEN-ION CONCENTRATION; HYPOGLYCEMIC AGENTS; INSULIN; KINETICS; LABETALOL; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NICOTINE; PREGNANCY; STREET DRUGS; TETRAHYDROCANNABINOL; TROPHOBLASTS;

EID: 70350228795     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2009.07.001     Document Type: Article

References (71)

1. Lucock M. Folic acid: nutritional biochemistry, molecular biology, and role in disease processes. Mol Genet Metab 71 1-2 (2000) 121-138
2. Pitkin R.M. Folate and neural tube defects. Am J Clin Nutr 85 1 (2007) 285S-288S
3. Herbert V. Folic acid. In: Shils M.E., Olson J.A., Shike M., and Ross A.H. (Eds). Modern nutrition in health and disease (1999), Lippincott, Williams & Wilkins, London
4. Worthington-Roberts B. Nutrition. In: Cohen W., Cherry S., and Merkatz I. (Eds). Cherry and Merkatz's complications of pregnancy (1999), Lippincott Williams & Wilkins, London
5. Picciano M.F. Pregnancy and lactation: physiological adjustments, nutritional requirements and the role of dietary supplements. J Nutr 133 (2003) 1997S-2002S
6. MRC Vitamin Study Research Group, Wald N., and Sneddon J. Prevention of neural tube defects: results of the Medical Research Council Vitamin Study. Lancet 338 8760 (1991) 131-137
7. Ganapathy V., Smith S.B., and Prasad P.D. SLC19: the folate/thiamine transporter family. Pflugers Arch 447 5 (2004) 641-646
8. Prasad P.D., Ramamoorthy S., Leibach F.H., and Ganapathy V. Molecular cloning of the human placental folate transporter. Biochem Biophys Res Commun 206 2 (1995) 681-687
9. Whetstine J.R., Flatley R.M., and Matherly L.H. The human reduced folate carrier gene is ubiquitously and differentially expressed in normal human tissues: identification of seven non-coding exons and characterization of a novel promoter. Biochem J 367 Pt 3 (2002) 629-640
10. Qiu A., Jansen M., Sakaris A., Min S.H., Chattopadhyay S., Tsai E., et al. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127 5 (2006) 917-928
11. Antony A.C., Utley C., Van Horne K.C., and Kolhouse J.F. Isolation and characterization of a folate receptor from human placenta. J Biol Chem 256 18 (1981) 9684-9692
12. Green T., and Ford H.C. Human placental microvilli contain high-affinity binding sites for folate. Biochem J 218 (1984) 75-80
13. Kamen B.A., and Smith A.K. A review of folate receptor alpha cycling and 5-methyltetrahydrofolate accumulation with an emphasis on cell models in vitro. Adv Drug Deliv Rev 56 (2004) 1085-1097
14. Elnakat H., and Ratnam M. Distribution, functionality and gene regulation of folate receptor isoforms: implications in targeted therapy. Adv Drug Deliv Rev 56 8 (2004) 1067-1084
15. Matherly L.H., and Goldman D.I. Membrane transport of folates. Vitam Horm 66 (2003) 403-456
16. Sabharanjak S., and Mayor S. Folate receptor endocytosis and trafficking. Adv Drug Deliv Rev 56 (2004) 1099-1109
17. Antony A.C. Folate receptors. Annu Rev Nutr 16 (1996) 501-521
18. Prasad P.D., Mahesh V.B., Leibach L.F.H., and Ganapathy V. Functional couploing between bafilomycin A1-sensitive proton pum and probenecid-sensitive folate transporter in human placental choriocarcinoma cells. Biochim Biophys Acta 1222 (1994) 309-314
19. Ratnam M., Marquardt H., Duhring J.L., and Freisheim J.H. Homologous membrane folate binding proteins in human placenta: cloning and sequence of a cDNA. Biochemistry 28 20 (1989) 8249-8254
20. Ganapathy V., Prasad P.D., Ganapathy M.E., and Leibach F.H. Placental transporters relevant to drug distribution across the maternal-fetal interface. J Pharmacol Exp Ther 294 2 (2000) 413-420
21. Bisseling T.M., Steegers E.A.P., vd Heuvel J.J.M., Siero H.L.M., vd Water F.M., Walker A.J., et al. Placental folate transport and binding are not impaired in pregnancies complicated by fetal growth restriction. Placenta 25 (2004) 588-593
22. Yasuda S., Hasui S., Yamamoto C., Yoshioka C., Kobayashi M., Itagaki S., et al. Placental folate transport during pregnancy. Biosci Biotechnol Biochem 72 9 (2008) 2277-2284
23. Verma R.S., Gullapalli S., and Antony A.C. Evidence that the hydrophobicity of isolated, in situ, and de novo-synthesized native human placental folate receptors is a function of glycosyl-phosphatidylinositol anchoring to membranes. J Biol Chem 267 6 (1992) 4119-4127
24. Zhao R., Matherly L.H., and Goldman I.D. Membrane transporters and folate homeostasis: intestinal absorption and transport into systemic compartments and tissues. Expert Rev Mol Med 11 (2009) e4
25. Keating E., Lemos C., Azevedo I., and Martel F. Comparison of folic acid uptake characteristics by human placental choriocarcinoma cells at acidic and physiological pH. Can J Physiol Pharmacol 84 2 (2006) 247-255
26. Kliman H.J., Nestler J.E., Sermasi E., Sanger J.M., and Strauss III J.F. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118 4 (1986) 1567-1582
27. Keating E., Goncalves P., Lemos C., Costa F., Campos I., Smith S.B., et al. Progesterone inhibits folic acid transport in human trophoblasts. J Membr Biol 216 2-3 (2007) 143-152
28. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65 1-2 (1983) 55-63
29. Chakrabarti R., Kundu S., Kumar S., and Chakrabarti R. Vitamin A as an enzyme that catalyzes the reduction of MTT to formazan by vitamin C. J Cell Biochem 80 1 (2000) 133-138
30. Bergmeyer H.U., and Bernt E. Lactate dehydrogenase. In: Bergmeyer H.U. (Ed). Methods in enzymatic analysis (1974), Academic Press, New York 574-579
31. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
32. Muzyka A., Tarkany O., Yelizanof V., Sergienko U., and Boichuk A. Non-linear regression (curve fit), in GraphPad Prism (version 4.03) for Windows (2005) San Diego, CA
33. Bloxam D.L., Bax C.M., and Bax B.E. Culture of syncytiotrophoblast for the study of human placental transfer. Part I. Isolation and purification of cytotrophoblast. Placenta 18 2-3 (1997) 93-98
34. Sastry B.V. Techniques to study human placental transport. Adv Drug Deliv Rev 38 1 (1999) 17-39
35. Bischof P., and Irminger-Finger I. The human cytotrophoblastic cell, a mononuclear chameleon. Int J Biochem Cell Biol 37 1 (2005) 1-16
36. Starreveld J.S., van Denderen J., Verrijt C.E., Kroos M.J., and van Dijk J.P. Morphological differentiation of cytotrophoblasts cultured in Medium 199 and in keratinocyte growth medium. Eur J Obstet Gynecol Reprod Biol 79 2 (1998) 205-210
37. Bax C.M., Ryder T.A., Mobberley M.A., Tyms A.S., Taylor D.L., and Bloxam D.L. Ultrastructural changes and immunocytochemical analysis of human placental trophoblast during short-term culture. Placenta 10 2 (1989) 179-194
38. Sirotnak F.M., and Tolner B. Carrier-mediated membrane transport of folates. Annu Rev Nutr 19 (1999) 91-122
39. Takahashi T., Utoguchi N., Takara A., Yamamoto N., Nakanishi T., Tanaka K., et al. Carrier-mediated transport of folic acid in BeWo cell monolayers as a model of the human trophoblast. Placenta 22 (2001) 863-869
40. Wang Y., Zhao R., and Goldman I.D. Characterization of a folate transporter in HeLa cells with a low pH optimum and high affinity for pemetrexed distinct from the reduced folate carrier. Clin Cancer Res 10 (2004) 6256-6264
41. Zhao R., Hanscom M., and Goldman I.D. The relationship between folate transport activity at low pH and reduced folate carrier function in human Huh7 hepatoma cells. Biochim Biophys Acta 1715 (2005) 57-64
42. Gregory J.F., and Quinlivan E.P. In vivo kinetics of folate metabolism. Annu Rev Nutr 22 (2002) 199-220
43. Magee L.A. Drugs in pregnancy. Antihypertensives. Best Pract Res Clin Obstet Gynaecol 15 6 (2001) 827-845
44. Kaaja R.J., and Greer I.A. Manifestations of chronic disease during pregnancy. JAMA 294 21 (2005) 2751-2757
45. Shankaran S., Lester B.M., Das A., Bauer C.R., Bada H.S., Lagasse L., et al. Impact of maternal substance use during pregnancy on childhood outcome. Semin Fetal Neonatal Med 12 2 (2007) 143-150
46. Glantz J.C., and Woods Jr. J.R. Obstetrical issues in substance abuse. Pediatr Ann 20 10 (1991) 531-539
47. Ganapathy V.V., Prasad P.D., Ganapathy M.E., and Leibach F.H. Drugs of abuse and placental transport. Adv Drug Deliv Rev 38 1 (1999) 99-110
48. Myllynen P., Pasanen M., and Pelkonen O. Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 26 5 (2005) 361-371
49. Gujrati V.R., Shanker K., Vrat S., Chandravati, and Parmar S.S. Novel appearance of placental nuclear monoamine oxidase: biochemical and histochemical evidence for hyperserotonomic state in preeclampsia-eclampsia. Am J Obstet Gynecol 175 6 (1996) 1543-1550
50. Weiner C.P. The role of serotonin in the genesis of hypertension in preeclampsia. Am J Obstet Gynecol 156 4 (1987) 885-888
51. Bolte A.C., van Geijn H.P., and Dekker G.A. Pathophysiology of preeclampsia and the role of serotonin. Eur J Obstet Gynecol Reprod Biol 95 1 (2001) 12-21
52. Keating E., Lemos C., Azevedo I., and Martel F. Characteristics of thiamine uptake by the BeWo human trophoblast cell line. J Biochem Mol Biol 39 4 (2006) 383-393
53. Keating E., Lemos C., Goncalves P., and Martel F. Acute and chronic effects of some dietary bioactive compounds on folic acid uptake and on the expression of folic acid transporters by the human trophoblast cell line BeWo. J Nutr Biochem (2007)
54. Eriksson U.J., Cederberg J., and Wentzel P. Congenital malformations in offspring of diabetic mothers-animal and human studies. Rev Endocr Metab Disord 4 1 (2003) 79-93
55. Hiden U., Maier A., Bilban M., Ghaffari-Tabrizi N., Wadsack C., Lang I., et al. Insulin control of placental gene expression shifts from mother to foetus over the course of pregnancy. Diabetologia 49 1 (2006) 123-131
56. Homko C., Sivan E., Chen X., Reece E.A., and Boden G. Insulin secretion during and after pregnancy in patients with gestational diabetes mellitus. J Clin Endocrinol Metab 86 2 (2001) 568-573
57. Pastrakuljic A., Derewlany L.O., Knie B., and Koren G. The effects of cocaine and nicotine on amino acid transport across the human placental cotyledon perfused in vitro. J Pharmacol Exp Ther 294 1 (2000) 141-146
58. Tabacova S.A., and Kimmel C.A. Atenolol: pharmacokinetic/dynamic aspects of comparative developmental toxicity. Reprod Toxicol 16 1 (2002) 1-7
59. Bayliss H., Churchill D., Beevers M., and Beevers D.G. Anti-hypertensive drugs in pregnancy and fetal growth: evidence for "pharmacological programming" in the first trimester?. Hypertens Pregnancy 21 2 (2002) 161-174
60. Lydakis C., Lip G.Y., Beevers M., and Beevers D.G. Atenolol and fetal growth in pregnancies complicated by hypertension. Am J Hypertens 12 6 (1999) 541-547
61. Slotkin T.A. Fetal nicotine or cocaine exposure: which one is worse?. J Pharmacol Exp Ther 285 3 (1998) 931-945
62. Rogers R.C., Sibai B.M., and Whybrew W.D. Labetalol pharmacokinetics in pregnancy-induced hypertension. Am J Obstet Gynecol 162 2 (1990) 362-366
63. Libiseller K., Pavlic M., Grubwieser P., and Rabl W. Ecstasy-deadly risk even outside rave parties. Forensic Sci Int 153 2-3 (2005) 227-230
64. Sanchez C., Velasco G., and Guzman M. Metabolic stimulation of mouse spleen lymphocytes by low doses of delta9-tetrahydrocannabinol. Life Sci 60 19 (1997) 1709-1717
65. Krulewitch C.J. Alcohol consumption during pregnancy. Annu Rev Nurs Res 23 (2005) 101-134
66. West J.R., and Blake C.A. Fetal alcohol syndrome: an assessment of the field. Exp Biol Med (Maywood) 230 6 (2005) 354-356
67. Redgrave G.W., Swartz K.L., and Romanoski A.J. Alcohol misuse by women. Int Rev Psychiatry 15 3 (2003) 256-268
68. Olney J.W. Fetal alcohol syndrome at the cellular level. Addict Biol 9 2 (2004) 137-49; discussion 151
69. Goodlett C.R., Horn K.H., and Zhou F.C. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp Biol Med (Maywood) 230 6 (2005) 394-406
70. DeYoung D.J., Bantle J.A., and Fort D.J. Assessment of the developmental toxicity of ascorbic acid, sodium selenate, coumarin, serotonin, and 13-cis retinoic acid using FETAX. Drug Chem Toxicol 14 1-2 (1991) 127-141
71. Jacqz-Aigrain E., and Koren G. Effects of drugs on the fetus. Semin Fetal Neonatal Med 10 2 (2005) 139-147