Bisphenol A inhibits proliferation and induces apoptosis in micromass cultures of rat embryonic midbrain cells through the JNK, CREB and p53 signaling pathways

Food and Chemical Toxicology

Volumn 52, Issue , 2013, Pages 76-82

  Liu, Ran ^a   Xing, Lina ^a   Kong, Dan ^a   Jiang, Jianjun ^a   Shang, Lanqin ^a   Hao, Weidong ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Apoptosis; Bisphenol A; Cell cycle; Developmental toxicity; Micromass culture

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLINE; KI 67 ANTIGEN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BAX GENE; BCL 2 GENE; BRAIN CELL; CELL CULTURE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN GENE; CYCLINE GENE; DEVELOPMENTAL TOXICITY; EMBRYO; EMBRYO CELL; ENZYME PHOSPHORYLATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GROWTH INHIBITION; KI 67 ANTIGEN GENE; MALE; MESENCEPHALON; NONHUMAN; PROTEIN EXPRESSION; RAT; REGULATOR GENE; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; STRESS ACTIVATED PROTEIN KINASE GENE; TOXICITY TESTING; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BENZHYDRYL COMPOUNDS; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MAP KINASE KINASE 4; MESENCEPHALON; PHENOLS; PHOSPHORYLATION; PREGNANCY; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

RATTUS;

EID: 84870308188     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.10.033     Document Type: Article

References (39)

1. Amaral J.D., Xavier J.M., Steer C.J., Rodriques C.M. The role of p53 in apoptosis. Discov. Med. 2010, 9:145-152.
2. Autret A., Martin S.J. Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol. Cell 2009, 36:355-363.
3. Calafat A.M., Kuklenyik Z., Reidy J.A., Caudill S.P., Ekong J., Needham L.L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ. Health Perspect. 2005, 113:391-395.
4. Chan W.H. Embryonic toxicity of sanguinarine through apoptotic processes in mouse blastocysts. Toxicol. Lett. 2011, 205:285-292.
5. Chan W.H., Shiao N.H. Cytotoxic effect of CdSe quantum dots on mouse embryonic development. Acta Pharmacol. Sin. 2008, 29:259-266.
6. Chapin R.E., Adams J., Boekelheide K., Earl Gray L., Hayward S.W., Lees P.S.J., McIntyre B.S., Portier K.M., Schnorr T.M., Selevan S.G., Vandenbergh J.G., Woskie S.R. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res. Part B 2008, 83:157-395.
7. Chen L., Sokabe M. Perinatal BPA exposure influences synaptic functions in the dorsal striatum of offspring. J. Physiol. Sci. 2007, 58(Suppl. l):S84.
8. Dejean L.M., Martinez-Caballero S., Kinnally K.W. Is MAC the knife that cuts cytochrome c from mitochondria during apoptosis?. Cell Death Differ. 2006, 13:1387-1395.
9. Engel S.M., Levy B., Liu Z., Kaplan D., Wolff M.S. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod. Toxicol. 2006, 21:110-112.
10. Fernandez M.F., Arrebola J.P., Taoufiki J., Navalón A., Ballesteros O., Pulqar R., Vilchez J.L., Olea N. Bisphenol-A and chlorinated derivatives in adipose tissue of women. Reprod. Toxicol. 2007, 24:259-264.
11. Hardy K., Stark J., Winston R.M. Maintenance of the inner cell mass in human blastocysts from fragmented embryos. Biol. Reprod. 2003, 68:1165-1169.
12. INVITTOX Protocol No. 114, 1996. In vitro micromass teratogen assay. Available from: <> http://ecvam.jrc.it.
13. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
14. Kwak H.J., Park K.M., Choi H.E., Chung K.S., Lim H.J., Park H.Y. PDE4 inhibitor, roflumilast protects cardiomyocytes against NO-induced apoptosis via activation of PKA and Epac dual pathways. Cell. Signal. 2008, 20:803-814.
15. Lebesque D., Chevaleyre V., Zukin R.S., Etqen A.M. Estradiol rescues neuron from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids 2009, 74:555-561.
16. Lee S., Suk K., Kim I.K., Jang I.S., Johnson V.J., Kwon T.K., Choi B.J., Kim S.H. Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calcium-induced reactive oxygen species, mitogen-activated protein kinases, and nuclear factor-κB. J. Neurosci. Res. 2008, 86:2932-2942.
17. Li D., Zhou Z., Qing D., He Y., Wu T., Miao M., Wang J., Weng X., Ferber J.R., Herrinton L.J., Zhu Q., Gao E., Checkoway H., Yuan W. Occupational exposure to bisphenol-A (BPA) and the risk of self-reported male sexual dysfunction. Hum. Reprod. 2010, 25:519-527.
18. Lotz K., Proff P., Bienengraeber V., Fanghaenel J., Gedrange T., Weingaertner J. Apoptosis as a creative agent of embryonic development of bucca, mentum and nasolacrimal duct. An in vivo study in rats. J. Craniomaxillofac. Surg. 2006, 34(Suppl. 2):8-13.
19. Morice L., Benaîtreau D., Dieudonné M.N., Morvan C., Serazin V., de Mazancourt P., Pecquery R., Dos Santos E. Antiproliferative and proapoptotic effects of bisphenol A on human trophoblastic JEG-3 cells. Reprod. Toxicol. 2011, 32:69-76.
20. Nakagawa Y., Tayama S. Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes. Arch. Toxicol. 2000, 74:99-105.
21. Nakamura K., Itoh K., Yaoi T., Fujiwara Y., Sugimoto T., Fushiki S. Murine neocortical histogenesis is perturbed by prenatal exposure to low doses of bisphenol A. J. Neurosci. Res. 2006, 84:1197-1205.
22. Oka T., Adati N., Shinkai T., Sakuma K., Nishimura T., Kurose K. Bisphenol A induces apoptosis in central neural cells during early development of Xenopus laevis. Biochem. Biophys. Res. 2003, 312:877-882.
23. Padmanabhan V., Siefert K., Ransom S., Johnson T., Pinkerton J., Anderson L., Tao L., Kannan K. Maternal bisphenol-A levels at delivery: a looming problem?. J. Perinatol. 2008, 28:258-263.
24. Ranjit N., Siefert K., Padmanabhan V. Bisphenol-A and disparities in birth outcomes: a review and direction for future research. J. Perinatol. 2010, 30:2-9.
25. Seki S., Aoki M., Hosokawa T., Saito T., Masuma R., Komori M., Kurasaki M. Bisphenol-A suppresses neurite extension due to inhibition of phosphorylation of mitogen-activated protein kinase in PC12 cells. Chem. Biol. Interact. 2011, 11:23-30.
26. Tan B.L.L., Mohd M.A. Analysis of selected pesticides and alkylphenols in human cord blood by gas chromatograph-mass spectrometer. Talanta 2003, 61:385-391.
27. The National Toxicology Program-Center for the Evaluation of Risks to Human Reproduction (NTP-CERHR), 2007. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Available from: <> http://cerhr.niehs.nih.gov.
28. Tsutsui T., Tamura Y., Yagi E., Hasegawa K., Takahashi M., Maizumi N., Yamaguchi F., Barrett J.C. Bisphenol-A induces cellular transformation, aneuploidy and DNA adduct formation in cultured Syrian hamster embryo cells. Int. J. Cancer 1998, 75:290-294.
29. Vandenberg L.N., Hauser R., Marcus M., Olea N., Welshons W.V. Human exposure to bisphenol A (BPA). Reprod. Toxicol. 2007, 24:139-177.
30. Wang Q., Zhao X.F., Ji Y.L., Wang H., Liu P., Zhang C., Zhang Y., Xu D.X. Mitochondrial signaling pathways is also involved in bisphenol A induced germ cell apoptosis in testes. Toxicol. Lett. 2010, 199:129-135.
31. Wetherill Y.B., Akingbenmi B.T., Kanno J., McLachlan J.A., Nadal A., Sonnenschein C., Watson C.S. In vitro molecular mechanisms of bisphenol A action. Reprod. Toxicol. 2007, 24:178-198.
32. Wilk I., Minta M. Improvement of embryo midbrain cell cultures for testing developmental neurotoxicity in vitro. Reprod. Toxicol. 2008, 26:76-77.
33. Wilk I., Minta M., Zmudzki J. Evaluation of computer-based analysis for assessment of differentiation in embryo midbrain micromass culture. Toxicol. Lett. 2006, 164(Suppl.):S1-S324.
34. Xiao Y., Liu R., Xing L.N., Xu Y.J., Shang L.Q., Hao W.D. Combined developmental toxicity of bisphenol A and genistein in micromass cultures of rat embryonic limb bud and midbrain cells. Toxicol. In Vitro 2011, 25:153-159.
35. Xing L.N., Xu Y.J., Xiao Y., Shang L.Q., Liu R., Wei X.T., Jiang J.J., Hao W.D. Embryotoxic and teratogenic effects of the combination of bisphenol A and genistein on in vitro cultured postimplantation rat embryos. Toxicol. Sci. 2010, 115:577-588.
36. Xu J., Osuga Y., Yano T., Morita Y., Tang X., Fujiwara T., Takai Y., Matsumi H., Koga K., Taketani Y., Tsutsumi O. Bisphenol A induces apoptosis and G2- to-M arrest of ovarian granulosa cells. Biochem. Biophys. Res. 2002, 292:456-462.
37. Yokosuka M., Ohtani-Kaneko R., Yamashita K., Muraoka D., Kuroda Y., Watanabe C. Estrogen and environmental estrogenic chemicals exert developmental effects on rat hypothalamic neurons and glias. Toxicol. In Vitro 2008, 22:1-9.
38. Zalko D., Soto A.M., Dolo L., Dorio C., Rathahao E., Debrauwer L., Faure R., Cravedi J.P. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ. Health Perspect. 2003, 111:9-319.
39. Zhang W., Liu H.T. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 2002, 12:9-18.