Chlorpyrifos modifies the expression of genes involved in human placental function

Reproductive Toxicology

Volumn 33, Issue 3, 2012, Pages 331-338

  Ridano, Magali E ^a   Racca, Ana C ^a   Flores Martín, Jésica ^a   Camolotto, Soledad A ^a   de Potas, Gladis Magnarelli ^b   Genti Raimondi, Susana ^a   Panzetta Dutari, Graciela M ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b UNIVERSIDAD NACIONAL DEL COMAHUE   (Argentina)

Author keywords

hCG; Gene expression; Organophosphate pesticide; Pregnancy; Trophoblast

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CHLORPYRIFOS; CHORIONIC GONADOTROPIN BETA SUBUNIT; HORMONE; MESSENGER RNA; PROTEIN;

ABCG2 GENE; ARTICLE; BETA HCG GENE; CELL STRUCTURE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEFENSE MECHANISM; GCM1 GENE; GENE; GENE TARGETING; HORMONE BLOOD LEVEL; HUMAN; HUMAN CELL; PLACENTA FUNCTION; POLYMERASE CHAIN REACTION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; TISSUE PRESERVATION; TROPHOBLAST;

ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; CELL SURVIVAL; CHLORPYRIFOS; CHORIONIC GONADOTROPIN, BETA SUBUNIT, HUMAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSECTICIDES; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PLACENTA; PREGNANCY; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84859737185     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.01.003     Document Type: Article

References (63)

1. Costa L.G. Current issues in organophosphate toxicology. Clin Chim Acta 2006, 366:1-13.
2. Slotkin T.A., Oliver C.A., Seidler F.J. Critical periods for the role of oxidative stress in the developmental neurotoxicity of chlorpyrifos and terbutaline, alone or in combination. Brain Res Dev Brain Res 2005, 157:172-180.
3. Eaton D.L., Daroff R.B., Autrup H., Bridges J., Buffler P., Costa L.G., et al. Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol 2008, 38(Suppl. 2):1-125.
4. Crumpton T.L., Seidler F.J., Slotkin T.A. Developmental neurotoxicity of chlorpyrifos in vivo and in vitro: effects on nuclear transcription factors involved in cell replication and differentiation. Brain Res 2000, 857:87-98.
5. Nakadai A., Li Q., Kawada T. Chlorpyrifos induces apoptosis in human monocyte cell line U937. Toxicology 2006, 224:202-209.
6. Mense S.M., Sengupta A., Lan C., Zhou M., Bentsman G., Volsky D.J., et al. The common insecticides cyfluthrin and chlorpyrifos alter the expression of a subset of genes with diverse functions in primary human astrocytes. Toxicol Sci 2006, 93:125-135.
7. Adigun A.A., Seidler F.J., Slotkin T.A. Disparate developmental neurotoxicants converge on the cyclic AMP signaling cascade, revealed by transcriptional profiles in vitro and in vivo. Brain Res 2010, 1316:1-16.
8. Perera F.P., Rauh V., Whyatt R.M., Tang D., Tsai W.Y., Bernert J.T., et al. A summary of recent findings on birth outcomes and developmental effects of prenatal ETS, PAH, and pesticide exposures. Neurotoxicology 2005, 26:573-587.
9. Eskenazi B., Harley K., Bradman A., Weltzien E., Jewell N.P., Barr D.B., et al. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect 2004, 112:1116-1124.
10. Levario-Carrillo M., Amato D., Ostrosky-Wegman P., Gonzalez-Horta C., Corona Y., Sanin L.H. Relation between pesticide exposure and intrauterine growth retardation. Chemosphere 2004, 55:1421-1427.
11. Dabrowski S., Hanke W., Polanska K., Makowiec-Dabrowska T., Sobala W. Pesticide exposure and birthweight: an epidemiological study in Central Poland. Int J Occup Med Environ Health 2003, 16:31-39.
12. Whyatt R.M., Camann D., Perera F.P., Rauh V.A., Tang D., Kinney P.L., et al. Biomarkers in assessing residential insecticide exposures during pregnancy and effects on fetal growth. Toxicol Appl Pharmacol 2005, 206:246-254.
13. Eskenazi B., Marks A.R., Bradman A., Harley K., Barr D.B., Johnson C., et al. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ Health Perspect 2007, 115:792-798.
14. Petit C., Chevrier C., Durand G., Monfort C., Rouget F., Garlantezec R., et al. Impact on fetal growth of prenatal exposure to pesticides due to agricultural activities: a prospective cohort study in Brittany, France. Environ Health 2010, 9:71.
15. Rauh V., Arunajadai S., Horton M., Perera F., Hoepner L., Barr D.B., et al. 7-Year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ Health Perspec 2011, 119:1196-1201.
16. Whyatt R.M., Rauh V., Barr D.B., Camann D.E., Andrews H.F., Garfinkel R., et al. Prenatal insecticide exposures and birth weight and length among an urban minority cohort. Environ Health Perspect 2004, 112:1125-1132.
17. Devlin R.B., Frampton M.L., Ghio A.J. In vitro studies: what is their role in toxicology?. Exp Toxicol Pathol 2005, 57(Suppl. 1):183-188.
18. Maltepe E., Bakardjiev A.I., Fisher S.J. The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 2010, 120:1016-1025.
19. Myatt L. Placental adaptive responses and fetal programming. J Physiol 2006, 572:25-30.
20. Joss-Moore L.A., Lane R.H. The developmental origins of adult disease. Curr Opin Pediatr 2009, 21:230-234.
21. Souza M.S., Magnarelli G.G., Rovedatti M.G., Cruz S.S., De D'Angelo A.M. Prenatal exposure to pesticides: analysis of human placental acetylcholinesterase, glutathione S-transferase and catalase as biomarkers of effect. Biomarkers 2005, 10:376-389.
22. Souza M.S., Magnarelli de Potas G., Pechen de D'Angelo A.M. Organophosphorous and organochlorine pesticides affect human placental phosphoinositides metabolism and PI-4 kinase activity. J Biochem Mol Toxicol 2004, 18:30-36.
23. Saulsbury M.D., Heyliger S.O., Wang K., Round D. Characterization of chlorpyrifos-induced apoptosis in placental cells. Toxicology 2008, 244:98-110.
24. Benachour N., Seralini G.E. Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells. Chem Res Toxicol 2009, 22:97-105.
25. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
26. Park P.H., Lim R.W., Shukla S.D. Involvement of histone acetyltransferase (HAT) in ethanol-induced acetylation of histone H3 in hepatocytes: potential mechanism for gene expression. Am J Physiol Gastrointest Liver Physiol 2005, 289:G1124-G1136.
27. Anson-Cartwright L., Dawson K., Holmyard D., Fisher S.J., Lazzarini R.A., Cross J.C. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 2000, 25:311-314.
28. Angeletti S., Rena V., Nores R., Fretes R., Panzetta-Dutari G.M., Genti-Raimondi S. Expression and localization of StarD7 in trophoblast cells. Placenta 2008, 29:396-404.
29. Mao Q. BCRP/ABCG2 in the placenta: expression, function and regulation. Pharm Res 2008, 25:1244-1255.
30. Koritschoner N.P., Bocco J.L., Panzetta-Dutari G.M., Dumur C.I., Flury A., Patrito L.C. A novel human zinc finger protein that interacts with the core promoter element of a TATA box-less gene. J Biol Chem 1997, 272:9573-9580.
31. Racca A.C., Camolotto S.A., Ridano M.E., Bocco J.L., Genti-Raimondi S., Panzetta-Dutari G.M. Krüppel-like factor 6 expression changes during trophoblast syncytialization and transactivates βhCG and PSG placental genes. PLoS ONE 2011, 6:e22438.
32. Cole L.A. New discoveries on the biology and detection of human chorionic gonadotropin. Reprod Biol Endocrinol 2009, 7:8.
33. Kalinderis M., Papanikolaou A., Kalinderi K., Ioannidou E., Giannoulis C., Karagiannis V., et al. Elevated serum levels of interleukin-6, interleukin-1beta and human chorionic gonadotropin in pre-eclampsia. Am J Reprod Immunol 2011, 66:468-475.
34. Fitzgerald B., Levytska K., Kingdom J., Walker M., Baczyk D., Keating S. Villous trophoblast abnormalities in extremely preterm deliveries with elevated second trimester maternal serum hCG or inhibin-A. Placenta 2011, 32:339-345.
35. Chattopadhyay S., Ghosh D. The involvement of hypophyseal-gonadal and hypophyseal-adrenal axes in arsenic-mediated ovarian and uterine toxicity: modulation by hCG. J Biochem Mol Toxicol 2010, 24:29-41.
36. Kajihara T., Uchino S., Suzuki M., Itakura A., Brosens J.J., Ishihara O. Human chorionic gonadotropin confers resistance to oxidative stress-induced apoptosis in decidualizing human endometrial stromal cells. Fertil Steril 2011, 95:1302-1307.
37. Cygalova L., Ceckova M., Pavek P., Staud F. Role of breast cancer resistance protein (Bcrp/Abcg2) in fetal protection during gestation in rat. Toxicol Lett 2008, 178:176-180.
38. Krishnamurthy P., Ross D.D., Nakanishi T., Bailey-Dell K., Zhou S., Mercer K.E., et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004, 279:24218-24225.
39. Baczyk D., Satkunaratnam A., Nait-Oumesmar B., Huppertz B., Cross J.C., Kingdom J.C. Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta. Placenta 2004, 25:553-559.
40. Lin F.Y., Chang C.W., Cheong M.L., Chen H.C., Lee D.Y., Chang G.D., et al. Dual-specificity phosphatase 23 mediates GCM1 dephosphorylation and activation. Nucleic Acids Res 2011, 39:848-861.
41. Morck T.J., Sorda G., Bechi N., Rasmussen B.S., Nielsen J.B., Ietta F., et al. Placental transport and in vitro effects of Bisphenol A. Reprod Toxicol 2010, 30:131-137.
42. Wojtowicz A.K., Augustowska K., Gregoraszczuk E.L. The short- and long-term effects of two isomers of DDT and their metabolite DDE on hormone secretion and survival of human choriocarcinoma JEG-3 cells. Pharmacol Rep 2007, 59:224-232.
43. Nakanishi T., Kohroki J., Suzuki S., Ishizaki J., Hiromori Y., Takasuga S., et al. Trialkyltin compounds enhance human CG secretion and aromatase activity in human placental choriocarcinoma cells. J Clin Endocrinol Metab 2002, 87:2830-2837.
44. Saulsbury M.D., Heyliger S.O., Wang K., Johnson D.J. Chlorpyrifos induces oxidative stress in oligodendrocyte progenitor cells. Toxicology 2009, 259:1-9.
45. Slotkin T.A., Seidler F.J. Oxidative stress from diverse developmental neurotoxicants: antioxidants protect against lipid peroxidation without preventing cell loss. Neurotoxicol Teratol 2010, 32:124-131.
46. Kharfi A., Giguere Y., De Grandpre P., Moutquin J.M., Forest J.C. Human chorionic gonadotropin (hCG) may be a marker of systemic oxidative stress in normotensive and preeclamptic term pregnancies. Clin Biochem 2005, 38:717-721.
47. Song X., Seidler F.J., Saleh J.L., Zhang J., Padilla S., Slotkin T.A. Cellular mechanisms for developmental toxicity of chlorpyrifos: targeting the adenylyl cyclase signaling cascade. Toxicol Appl Pharmacol 1997, 145:158-174.
48. 2+/cAMP response element binding protein in cultured neurons. Toxicol Appl Pharmacol 2002, 182:176-185.
49. Meyer A., Seidler F.J., Cousins M.M., Slotkin T.A. Developmental neurotoxicity elicited by gestational exposure to chlorpyrifos: when is adenylyl cyclase a target. Environ Health Perspect 2003, 111:1871-1876.
50. Delidaki M., Gu M., Hein A., Vatish M., Grammatopoulos D.K. Interplay of cAMP and MAPK pathways in hCG secretion and fusogenic gene expression in a trophoblast cell line. Mol Cell Endocrinol 2011, 332:213-220.
51. Natarajan K., Xie Y., Nakanishi T., Beck W.T., Bauer K.S., Ross D.D. Identification and characterization of the major alternative promoter regulating Bcrp1/Abcg2 expression in the mouse intestine. Biochim Biophys Acta 2011, 1809:295-305.
52. Al-Nasiry S., Spitz B., Hanssens M., Luyten C., Pijnenborg R. Differential effects of inducers of syncytialization and apoptosis on BeWo and JEG-3 choriocarcinoma cells. Hum Reprod 2006, 21:193-201.
53. Serrano M.A., Macias R.I., Briz O., Monte M.J., Blazquez A.G., Williamson C., et al. Expression in human trophoblast and choriocarcinoma cell lines, BeWo, Jeg-3 and JAr of genes involved in the hepatobiliary-like excretory function of the placenta. Placenta 2007, 28:107-117.
54. Slotkin T.A., MacKillop E.A., Ryde I.T., Seidler F.J. Ameliorating the developmental neurotoxicity of chlorpyrifos: a mechanisms-based approach in PC12 cells. Environ Health Perspect 2007, 115:1306-1313.
55. Karalliedde L.D., Edwards P., Marrs T.C. Variables influencing the toxic response to organophosphates in humans. Food Chem Toxicol 2003, 41:1-13.
56. Needham L.L. Assessing exposure to organophosphorus pesticides by biomonitoring in epidemiologic studies of birth outcomes. Environ Health Perspect 2005, 113:494-498.
57. Slotkin T.A., Seidler F.J. Developmental neurotoxicants target neurodifferentiation into the serotonin phenotype: chlorpyrifos, diazinon, dieldrin and divalent nickel. Toxicol Appl Pharmacol 2008, 233:211-219.
58. Li Q., Kobayashi M., Kawada T. Chlorpyrifos induces apoptosis in human T cells. Toxicology 2009, 255:53-57.
59. Oostingh G.J., Wichmann G., Schmittner M., Lehmann I., Duschl A. The cytotoxic effects of the organophosphates chlorpyrifos and diazinon differ from their immunomodulating effects. J Immunotoxicol 2009, 6:136-145.
60. Whyatt R.M., Barr D.B., Camann D.E., Kinney P.L., Barr J.R., Andrews H.F., et al. Contemporary-use pesticides in personal air samples during pregnancy and blood samples at delivery among urban minority mothers and newborns. Environ Health Perspect 2003, 111:749-756.
61. Tirelli V., Catone T., Turco L., Di Consiglio E., Testai E., De Angelis I. Effects of the pesticide clorpyrifos on an in vitro model of intestinal barrier. Toxicol In Vitro 2007, 21:308-313.
62. Barr D.B., Wang R.Y., Needham L.L. Biologic monitoring of exposure to environmental chemicals throughout the life stages: requirements and issues for consideration for the National Children's Study. Environ Health Perspect 2005, 113:1083-1091.
63. Ostrea E.M., Morales V., Ngoumgna E., Prescilla R., Tan E., Hernandez E., et al. Prevalence of fetal exposure to environmental toxins as determined by meconium analysis. Neurotoxicology 2002, 23:329-339.