Effects of uterine and lactational exposure to di-(2-ethylhexyl) phthalate on spatial memory and NMDA receptor of hippocampus in mice

Hormones and Behavior

Volumn 71, Issue , 2015, Pages 41-48

  Dai, Yuhua ^a   Yang, Yanling ^a   Xu, Xiaohong ^a   Hu, Yizhong ^a  

^a ZHEJIANG NORMAL UNIVERSITY   (China)

Author keywords

Behavior; Di (2 ethylhexyl) phthalate; NMDA receptor; Spatial learning and memory

Indexed keywords

DI (2 ETHYLHEXYL)PHTHALATE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHTHALIC ACID; UNCLASSIFIED DRUG; ENDOCRINE DISRUPTOR; NR2B NMDA RECEPTOR; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN REGION; CONTROLLED STUDY; FEMALE; FEMALE GENITAL SYSTEM FUNCTION; FUNCTIONAL ASSESSMENT; HIPPOCAMPUS; LACTATION; LOCOMOTION; MENTAL TASK; MORRIS WATER MAZE TEST; MOUSE; NONHUMAN; OPEN FIELD TEST; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; SEX DIFFERENCE; SPATIAL MEMORY; STIMULUS RESPONSE; TASK PERFORMANCE; UTERUS; WESTERN BLOTTING; ANIMAL; BODY WEIGHT; DRUG EFFECTS; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; MAZE TEST; METABOLISM; MOTOR ACTIVITY; ORGAN SIZE; PREGNANCY; PSYCHOLOGY;

ANIMALS; BODY WEIGHT; DIETHYLHEXYL PHTHALATE; ENDOCRINE DISRUPTORS; FEMALE; HIPPOCAMPUS; LACTATION; MALE; MAZE LEARNING; MICE; MICE, INBRED ICR; MOTOR ACTIVITY; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, N-METHYL-D-ASPARTATE; SPATIAL MEMORY;

EID: 84928250867     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.03.008     Document Type: Article

References (44)

1. Abdul-Ghani S., Yanai J., Abdul-Ghani R., Pinkas A., Abdeen Z. The teratogenicity and behavioral teratogenicity of di(2-ethylhexyl) phthalate (DEHP) and di-butyl phthalate (DBP) in a chick model. Neurotoxicol. Teratol. 2012, 34:56-62.
2. Adams M.M., Fink S.E., Janssen W.G., Shah R.A., Morrison J.H. Estrogen modulates synaptic N-methyl-d-aspartate receptor subunit distribution in the aged hippocampus. J. Comp. Neurol. 2004, 474:419-426.
3. Andrade A.J.M., Grande S.W., Talsness C.E., Grote K., Chahoud I. A dose-response study following in utero and lactational exposure to di-(2-ethylhexyl)-phthalate (DEHP): non-monotonic dose-response and low dose effects on rat brain aromatase activity. Toxicology 2006, 227:185-192.
4. Boberg J., Christiansen S., Axelstad M., Kledal T.S., Vinggaard A.M., Dalgaard M., Nellemann C., Hass U. Reproductive and behavioral effects of diisononyl phthalate (DINP) in perinatally exposed rats. Reprod. Toxicol. 2011, 31:200-209.
5. Boon W.C., Diepstraten J., van der Burg J., Jones M.E., Simpson E.R., van den Buuse M. Hippocampal NMDA receptor subunit expression and watermaze learning in estrogen deficient female mice. Brain Res. Mol. Brain Res. 2005, 140(1-2):127-132.
6. Borch J., Metzdorff S.B., Vinggaard A.M., Brokken L., Dalgaard M. Mechanisms underlying the anti-androgenic effects of diethylhexyl phthalate in fetal rat testis. Toxicology 2006, 223:144-155.
7. Carbone S., Ponzo O.J., Gobetto N., Samaniego Y.A., Reynoso R., Scacchi P., Moguilevsky J.A., Cutrera R. Antiandrogenic effect of perinatal exposure to the endocrine disruptor di-(2-ethylhexyl) phthalate increases anxiety-like behavior in male rats during sexual maturation. Horm. Behav. 2013, 63:692-699.
8. Cho S.C., Bhang S.Y., Hong Y.C., Shin M.S., Kim B.N., Kim J.W., Yoo H.J., Cho I.H., Kim H.W. Relationship between environmental phthalate exposure and the intelligence of school-age children. Environ. Health Perspect. 2010, 118:1027-1032.
9. Chopra V., Harley K., Lahiff M., Eskenazi B. Association between phthalates and attention deficit disorder and learning disability in U.S. children, 6-15years. Environ. Res. 2014, 128:64-69.
10. Cui Y., Jin J., Zhang X., Xu H., Yang L., Du D., Zeng Q., Tsien J.Z., Yu H., Cao X. Forebrain NR2B over expression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PLoS ONE 2011, 6:20312.
11. Culty M., Thuillier R., Li W., Wang Y., Martinez-Arguelles D.B., Benjamin C.G., Triantafilou K.M., Zirkin B.R., Papadopoulos V. In utero exposure to di-(2-ethylhexyl) phthalate exerts both short-term and long-lasting suppressive effects on testosterone production in the rat. Biol. Reprod. 2008, 78:1018-1028.
12. Do R.P., Stahlhut R.W., Ponzi D., Vom Saal F.S., Taylor J.A. Non-monotonic dose effects of in utero exposure to di(2-ethylhexyl) phthalate (DEHP) on testicular and serum testosterone and anogenital distance in male mouse fetuses. Reprod. Toxicol. 2012, 34(4):614-621.
13. Dorgan J.F., Stanczyk F.Z., Kahle L.L., Brinton L.A. Prospective case-control study of premenopausal serum estradiol and testosterone levels and breast cancer risk. Breast Cancer Res. 2010, 12:R98.
14. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., Berger T.W. 17β-Estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol. 1999, 81(2):925-929.
15. Hojo Y., Murakami G., Mukai H., Higo S., Hatanaka Y., Ogiue-Ikeda M., Ishii H., Kimoto T., Kawato S. Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol. Cell. Endocrinol. 2008, 290:31-43.
16. Huemmeke M., Eysel U.T., Mittmann T. Lesion-induced enhancement of LTP in rat visual cortexis mediated by NMDA receptors containing the NR2B subunit. J. Physiol. 2004, 559:875-882.
17. Ishido M., Morita M., Oka S., Masuo Y. Alteration of gene expression of G protein-coupled receptors in endocrine disruptors-caused hyperactive rats. Regul. Pept. 2005, 126:145-153.
18. Jelks K.B., Wylie R., Floyd C.L., McAllister A.K., Wise P. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha. J. Neurosci. 2007, 27:6903-6913.
19. Jordan C.L., Christensen S.E., Handa R.J., Anderson J.L., Pouliot W.A., Breedlove1 S.M. Evidence that androgen acts through NMDA receptors to affect motoneurons in the rat spinal nucleus of the bulbocavernosus. J. Neurosci. 2002, 22:9567-9572.
20. Kessler W., Numtip W., Grote K., Csanady G.A., Chahoud I., Filser J.G. Blood burden of di(2-ethylhexyl) phthalate and its primary metabolite mono (2-ethylhexyl) phthalate in pregnant and nonpregnant rats and marmosets. Toxicol. Appl. Pharmacol. 2004, 195:142-153.
21. Kim B.N., Cho S.C., Kim Y., Shin M.S., Yoo H.J., Kim J.W., Yang Y.H., Kim H.W., Bhang S.Y., Hong Y.C. Phthalates exposure and attention-deficit/hyperactivity disorder in school-age children. Biol. Psychiatry 2009, 66:958-963.
22. Konur S., Yuste R. Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition. Mol. Cell. Neurosci. 2004, 27:427-440.
23. Li Y., Zhuang M., Li T., Shi N. Neurobehavioral toxicity study of dibutyl phthalate on rats following in utero and lactational exposure. J. Appl. Toxicol. 2009, 29:603-611.
24. Li X.J., Jiang L., Chen L., Chen H.S., Li X. Neurotoxicity of dibutyl phthalate in brain development following perinatal exposure: a study in rats. Environ. Toxicol. Pharmacol. 2013, 36:392-402.
25. Lovekamp-Swan T., Davis B.J. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ. Health Perspect. 2003, 111(2):139-145.
26. McEwen B. Estrogen actions throughout the brain. Recent Prog. Horm. Res. 2002, 57:357-384.
27. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 1999, 20:279-307.
28. Meeker J.D., Calafat A.M., Hauser R. Urinary metabolites of di(2-ethylhexyl) phthalate are associated with decreased steroid hormone levels in adult men. J. Androl. 2009, 30(3):287-297.
29. Mukai H., Kimoto T., Hojo Y., Kawato S., Murakami G., Higo S., Hatanaka Y., Ogiue-Ikeda M. Modulation of synaptic plasticity by brain estrogen in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1030-1044.
30. Negishi T., Kawasaki K., Suzaki S., Maeda H., Ishii Y., Kyuwa S., Kuroda Y., Yoshikawa Y. Behavioral alterations in response to fear-provoking stimuli and tranylcypromine induced by perinatal exposure to bisphenol A and nonylphenol in male rats. Environ. Health Perspect. 2004, 112:1159-1164.
31. Ohtani-Kaneko R., Iwafuchi M., Iwakura T., Muraoka D., Yokosuka M., Shiga T., Watanabe C. Effects of estrogen on synapsin I distribution in developing hypothalamic neurons. Neurosci. Res. 2010, 66(2):180-188.
32. Patisaul H.B., Polston E.K. Influence of endocrine active compounds on the developing rodent brain. Brain Res. Rev. 2008, 57:352-362.
33. Singh S., Li S.S.-L. Bisphenol A and phthalates exhibit similar toxicogenomics and health effect. Gene 2012, 494:85-91.
34. Smith C.C., Vedder L.C., McMahon L.L. Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 2009, 34S:S130-S142.
35. Smith C.A., Macdonald A., Holahan M.R. Acute postnatal exposure to di (2-ethylhexyl) phthalate adversely impacts hippocampal development in the male rat. Neuroscience 2011, 193:100-108.
36. Stephenson F.A., Cousins S.L., Kenny A.V. Assembly and forward trafficking of NMDA receptors. Mol. Membr. Biol. 2008, 25:311-320.
37. Tanaka T. Reproductive and neurobehavioural effects of bis(2-ethylhexyl) phthalate (DEHP) in a cross-mating toxicity study of mice. Food Chem. Toxicol. 2005, 43:581-589.
38. Tando S., Itoh K., Yaoi T., Ikeda J., Fujiwara Y., Fushiki S. Effects of pre- and neonatal exposure to bisphenol A on murine brain development. Brain Dev. 2007, 29:352-356.
39. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Lett. Nature 1999, 401:63-69.
40. Vedder L.C., Smith C.C., Flannigan A.E., McMahon L.L. Estradiol-induced increase in novel object recognition requires hippocampal NR2B-containing NMDA receptors. Hippocampus 2013, 23:108-115.
41. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 1994, 14:7680-7687.
42. Xu Y., Agrawal S., Cook T.J., Knipp G.T. Di-(2-ethylhexyl)-phthalate affects lipid profiling in fetal rat brain upon maternal exposure. Arch. Toxicol. 2007, 1:57-62.
43. Xu X.H., Zhang J., Wang Y.M., Ye Y.P., Luo Q.Q. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice. Horm. Behav. 2010, 58:326-333.
44. Yolton K., Xu Y.Y., Strauss D., Altaye M., Calafat A.M., Khoury J. Prenatal exposure to bisphenol A and phthalates and infant neurobehavior. Neurotoxicol. Teratol. 2011, 33:558-566.