Different effects by sex on hypothalamic-pituitary axis of prepubertal offspring rats produced by in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP)

NeuroToxicology

Volumn 33, Issue 1, 2012, Pages 78-84

  Carbone, S ^a,b,c   Samaniego, Y A ^a   Cutrera, R ^a,b   Reynoso, R ^a   Cardoso, N ^a   Scacchi, P ^a,b,d   Moguilevsky, J A ^c   Ponzo, O J ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c FAVALORO UNIVERSITY   (Argentina)

^d PONTIFICIA UNIVERSIDAD CATÓLICA ARGENTINA   (Argentina)

Author keywords

Aspartate; GABA; Gestational; Gonadotropin; Lactational; Phthalate; Prepubertal; Rats

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; ASPARTIC ACID; FOLLITROPIN; GLUTAMIC ACID; GONADOTROPIN; PHTHALIC ACID 2 ETHYLHEXYL MONOESTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LACTATION; LITTER SIZE; MALE; NEUROTRANSMISSION; NONHUMAN; PERINATAL DRUG EXPOSURE; PREGNANCY; PREPUBERTY; PRIORITY JOURNAL; PROGENY; REPRODUCTIVE TOXICITY; UTERUS WEIGHT;

ANIMALS; ASPARTIC ACID; DIETHYLHEXYL PHTHALATE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FOLLICLE STIMULATING HORMONE; GAMMA-AMINOBUTYRIC ACID; GONADOTROPINS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LACTATION; LUTEINIZING HORMONE; MALE; MATERNAL EXPOSURE; ORGAN SIZE; PITUITARY-ADRENAL SYSTEM; PLASTICIZERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX CHARACTERISTICS; STATISTICS, NONPARAMETRIC; TESTIS; UTERUS;

ANIMALIA; RATTUS;

EID: 84455193602     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.11.009     Document Type: Article

References (61)

1. Adams M.N., Flagg R.A., Gore A.C. Perinatal changes in hypothalamic N-methyl-d-aspartate receptors and heir relationship to gonadotropin-releasing hormone neurons. Endocrinology 1999, 140:2288-2296.
2. Akingbemi B.T., Youker R.T., Sottas C.M., Ge R., Katz E., Klinefelter G.R., et al. Modulation of rat Leydig cell steroidogenic function by di (2-ethylhexyl) phthalate. Biol Reprod 2001, 65:1252-1259.
3. Akingbemi B.T., Hardy M.P. Oestrogenic and antiandrogenic chemicals in the environment: effects on male reproductive health. Ann Med 2001, 33:391-403.
4. Akingbemi B.T., Ge R., Klinefelter G.R., Zirkin B.R., Hardy M.P. Phthalate-induced Leydig cell hyperplasia is associated with multiple endocrine disturbances. Proc Natl Acad Sci USA 2004, 101:775-780.
5. Albro P.W. The biochemical toxicology of di-(2-ethylhexyl) and related phthalates: testicular atrophy and hepatocarcinogenesis. Rev Biochem Toxicol 1987, 8:73-119.
6. Andrade A.J., Grande S.W., Talsness C.E., Grote K., Golombiewski A., Sterner-Koch A., et al. A dose response study following in utero and lactational exposure to di-(2-ethylheyl) phatalate (DEHP): effects on androgenic status, developmental landmarks and testicular histology in male offspring rats. Toxicology 2006, 225:64-74.
7. Andrews W.W., Mizejewski G.J., Ojeda S.R. Development of estradiol positive feedback on LH release in the female rat: a quantitative study. Endocrinology 1981, 109:1404-1413.
8. Bonefeld-Jorgensen E.C., Andersen H.R., Rasmussen T.R., Vingaard A.M. Effects of highly bioaccumulated polychlorinated biphenyl congeners on estrogen and androgen receptor activity. Toxicology 2001, 158:141-153.
9. Borch J., Dalgaard M., Ladefoged O. Early testicular effects in rats perinatally exposed to DEHP in combination with DEHA - apoptosis assessment and immunohistochemical studies. Reprod Toxicol 2005, 19:517-525.
10. Borch J., Metzdorff S.B., Vinggaard A.M., Brokken L., Dalgaard M. Mechanisms underlying the anti-androgenic effect of diethylhexyl phthalate in fetal testis. Toxicology 2006, 223:144-155.
11. Brann W.D., Mahesh V.B. Excitatory amino acids: function and significance in reproduction and neuroendocrine regulation. Frontiers Neuroendocrinol 1994, 15:3-49.
12. Calafat A.M., Needham L.L., Silva M.J., Lambert G. Exposure to di-(2-ethylhexyl) phthalate among premature neonates in a neonatal intensive care unit. Pediatrics 2004, 113:429-431.
13. Calafat A.M., McKee R.H. Integrating biomonitoring exposure data into the risk assessment process: phthalates [diethyl phthalate and di(2-ethylhexyl) phthalate] as a case study. Environ Health Perspect 2006, 114:783-789.
14. Caligaris L., Astrada J., Taleisnik S. Influence of age on the release of luteinizing hormone induced by oestrogen-progesterone in immature rats. J Endocrinol 1972, 57:97-100.
15. Carbone S., Szwarcfarb B., Rondina D., Feleder C., Moguilevsky J.A. Differential effects of N-methyl-d-aspartate and non-N-metyl-d-aspartate receptors of the excitatory amino acids system on LH and FSH secretion. Its effects on the hypothalamic luteinizing hormone releasing during maturation in male rats. Brain Res 1996, 707:139-145.
16. Carbone S., Szwarcfarb B., Ponzo O., Reynoso R., Cardoso N., Dieguiz L., et al. Impact of gestational and lactational phthalate exposure on hypothalamic content of amino acid neurotransmitters and FSH secretion in peripubertal male rats. Neurotoxicology 2010, 31:747-751.
17. Dalsenter P.R., Santana G.M., Grande S.W., Andrade A.J., Araújo S.L. Phthalate affect the reproductive function and sexual behavior of male Wistar rats. Hum Exp Toxicol 2006, 25:297-303.
18. Davis B.J., Maronpot R.R., Heindel J.J. Di-(2-ethylhexyl) phthalate suppresses estradiol and ovulation in cycling rats. Toxicol Appl Pharmacol 1994, 128:216-223.
19. Doull J., Cattley R., Elcombe C., Lake B.G., Swenberg J., Wilkinson C., et al. A cancer risk assessment of di(2-ethylhexyl)phthalate: application of the new U.S. EPA Risk Assessment Guidelines. Regul Toxicol Pharmacol 1999, 29:27-57.
20. Engel S.M., Zhu C., Bekowitz G.S., Calafat A.M., Silva M.J., Miodovnik A., et al. Prenatal phthalate exposure and performance on the neonatal behavioral assessment scale in a multiethnic birth cohort. Neurotoxicology 2009, 30:522-528.
21. Engel S.M., Miodovnik A., Canfield R., Zhu C., Silva M.J., Calafat A.M., et al. Prenatal phthalate exposure is associated with childhood behavior and executive functioning. Environ Health Perspect 2010, 118:565-571.
22. Faouzi M.A., Dine T., Gressier B., Kambia K., Luyckx M., Pagniez D., et al. Exposure of hemodialysis patients to di-2-ethylhexyl phthalate. Int J Pharm 1999, 80:13-21.
23. Feleder C., Jarry H., Leonhart S., Wutke W., Moguilevsky J.A. The GABAergic control of gonadotropin-realising hormone secretion in male rats during sexual maturation involves effects on hypothalamic excitatory and inhibitory amino acids systems. Neuroendocrinology 1996, 64:305-312.
24. Foster P.M., Mylchreest E., Gaido K.W., Sar M. Effects of phthalate esters on the developing reproductive tract of male rats. Hum Reprod Update 2001, 7:231-235.
25. Gartner S., Balski M., Koch M., Nehls L. Analysis and migration of phtalates in infant food packed in recycled paperboard. J Agric Food Chem 2009, 57:10675-10681.
26. Ge R.S., Chen G.R., Tanrikut C., Hardy P. Phthalate ester toxicity in Leydig cells: developmental timing and dosage considerations. Reprod Toxicol 2007, 23:366-373.
27. Grande S.W., Andrade J.M., Talsness C.E., Grote K., Golombiewski A., Sterner-Kock A., et al. A dose-response study following in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP): reproductive effects on adult female offspring rats. Toxicology 2007, 229:114-122.
28. Gray L.E., Ostby J., Fur J., Price M., Veeramachanemi D.N., Parks L. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 2000, 58:350-365.
29. Gupta R.K., Singh J.M., Leslie T.C., Meachum S., Flaws J.A., Yao H.H. Di-(2-ethylhexyl) phthalate and mono-(2-ethylhexyl) phthalate inhibit growth and reduce estradiol levels of antral follicles in vitro. Toxicol Appl Pharmacol 2010, 242:224-230.
30. Heudorf J., Mersch-Sundermann J., Angerer J. Phthalates: toxicology and exposure. Int J Hyg Environ Health 2007, 210:623-634.
31. Howdeshell K.L., Furr J., Lambright C.R., Rider C.V., Wilson V.S., Gray L.E. Cumulative effects of dibutyl phthalate and diethylhexyl phthalate on male rat reproductive tract development: altered fetal steroid hormones and genes. Toxicol Sci 2007, 99:190-202.
32. Hu G.S., Lian Q.Q., Ge R.S., Hardy D.O., Li X.K. Phthalate-induced testicular dysgenesis syndrome: Leydig cell influence. Trends Endocrinol Metab 2009, 20:139-145.
33. Jarry H., Hirsch B., Leonhart S., Wutke W. Amino acid neurotransmitter release in the preoptic area of rats during the positive feedback actions of estradiol on LH release. Neuroendocrinology 1992, 56:133-140.
34. Joblin S. A variety of environmentally persistent chemicals, including some Phthalate plasticizers are weakly estrogenic. Environ Health Perspect 1995, 103:582-587.
35. Koch H.M., Preuss R., Angerer J. Di(2-ethylhexyl)phthalate (DEHP): human metabolism and internal exposure - an update and latest results. J Androl 2006, 29:155-165.
36. Latini G. Potential hazards of exposure to Di-(2-Ethylhexyl)-phthalate in babies. Biol Neonate 2000, 78:269-276.
37. Latini G., De Felice C., Presta G., Del Vecchio A., Paris I., Ruggieri F., et al. In utero exposure to di-(2-ethylhexyl) phthalate and duration of human pregnancy. Environ Health Perspect 2003, 111:1783-1785.
38. Lovekamp T.N., Davis B.J. Mono-(2-ethylhexyl) phthalate suppresses aromatase transcript levels and estradiol production in cultured rat garnulosa cells. Toxicol Appl Pharmacol 2001, 172:217-224.
39. Lovekamp-Swan T., Davis B.J. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ Health Perspect 2003, 111:139-145.
40. Main K.M., Mortensen G.K., Kaleva M.M., Boisen K.A., Damgaard I.N., Chellakooty M., et al. Human breast milk contamination with phthalates and alterations of endogenous reproductive hormones in infants three months of age. Environ Health Perspect 2006, 114:270-276.
41. Moguilevsky J.A., Carbone S., Szwarcfarb B., Rondina D. Sexual maturation modifies the GABAergic control of gonadotrophin secretion in female rats. Brain Res 1991, 563:12-16.
42. Moguilevsky J.A., Carbone S., Szwarcfarb B., Rondina D., Scacchi P. Hypothalamic excitatory amino acid system during sexual maturation in female rats. J Steroid Biochem Mol Biol 1995, 53:337-341.
43. Moguilevsky J.A., Wutke W. Changes in the control of gonadotrophin secretion by neurotransmitters during sexual development in rats. Exp Clin Endocrinol Diabetes 2001, 109:188-195.
44. Niswender G.H., Midgley A.T., Monroe S.E., Reichert L.E. Radioimmunoassay for rat luteinizing hormone with antiovine serum and ovine LH-1 311. Proc Soc Exp Biol Med 1968, 128:807-811.
45. NTP-CERHR NTP-CERHR Monograph on the Potential Human reproductive and Developmente Effects of di(2-ethylhexyl) phthalate (DEHP). National Toxicology Program Center for the Evaluation of Risks to Human Reproduction, NIH Publication No. 06-4476 2006, Available from: http://cerhr.niehs.nih.gov/chemicals/dehp/DEHP-Monograph.pdf.
46. Pak V.M.M., Nailon R.E., McCauley L.A. Controversy: neonatal exposure to plasticizers in the NICU. MCN Am J Matern Child Nurs 2007, 332:244-249.
47. Parks L.G., Ostby J.S., Lambright C.R., Abbott B.D., Klinefelter G.R., Barlow N.J., et al. The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicol Sci 2000, 58:339-349.
48. Scacchi P., Moguilevsky J.A. Effect of sexual hormones on gonadotropin secretion in prepubertal rats. Experientia 1973, 29:877-878.
49. Schettler T. Human exposure to phthalates via consumer products. Int J Androl 2006, 29:134-139.
50. Sharpe R.M. Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ Health Perspect 1995, 103:1136-1143.
51. Sharpe R.M. Hormones and testis development and the possible adverse effects of environmental chemicals. Toxicol Lett 2001, 120:221-232.
52. Shinji T., Mitsuru L., Satoshi K., Kazuo J., Tadashi M., Hiroyuki K. Differential effects of phthalate esters receptors α and β and androgen receptor. Toxicology 2005, 210:223-233.
53. Sjöberg P., Bondesson U., Hammarlund M. Non-linearities in the pharmacokinetics of di-(2-ethylhexyl) phthalate and metabolites in male rats. Arch Toxicol 1985, 58:72-77.
54. Sjöbergt P., Lindqvistt N.G., Ploen L. Age-dependent response of the rat testes to di(2-ethylhexyl) phthalate. Environ Health Perspect 1986, 65:237-242.
55. Skakkebaek N.E., Rajpert-De Meyts E., Main K.M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 2001, 16:972-978.
56. Stroheker T., Cabaton N., Nourdin G., Régnier J.F., Lhuguenot J.C., Chagnon C. Evaluation of anti-androgenic activity of di-(2-ethylhexyl)phthalate. Toxicology 2005, 208:115-121.
57. Svechnikova I., Svechnikov K., Soder O. The influence of di-(2-ethylhexyl) phthalate on steroidogenesis by the ovarian granulose cells of immature female rats. J Endocrinol 2007, 194:603-609.
58. Swan S., Main K.M., Liu F., Stewart S.L., Kruse R.L., Calafat A.M., et al. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 2005, 113:1056-1061.
59. Swan S. Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ Res 2008, 108:177-184.
60. Szwarcfarb B., Carbone S., Stein M., Medina J., Moguilevsky J.A. Sexual differences in the effect of the GABAergic system on LH secretion and in the hypothalamic ontogenesis of GABA-A receptors in peripubertal rats. Brain Res 1994, 646:351-356.
61. Wilson V.S., Blystone C.R., Hotchkiss A.K., Rider C.V., Gray L.E. Diverse mechanisms of anti-androgen action: impact on male rat reproductive tract development. Int J Androl 2008, 31:178-187.