Disruption of reproductive aging in female and male rats by gestational exposure to estrogenic endocrine disruptors

Endocrinology

Volumn 154, Issue 6, 2013, Pages 2129-2143

  Walker, Deena M ^a   Kermath, Bailey A ^a   Woller, Michael J ^b   Gore, Andrea C ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF WISCONSIN WHITEWATER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROCLOR; AROCLOR 1221; DIMETHYL SULFOXIDE; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTRADIOL BENZOATE; LUTEINIZING HORMONE; TESTOSTERONE; UNCLASSIFIED DRUG;

AGING; ARTICLE; ESTRUS CYCLE; FEMALE; GENE EXPRESSION; MALE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; SENESCENCE;

AGING; ANIMALS; ARCUATE NUCLEUS; AROCLORS; BODY WEIGHT; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; ESTRADIOL; ESTROUS CYCLE; FEMALE; GENE EXPRESSION; GESTATIONAL AGE; HYPOTHALAMUS; LUTEINIZING HORMONE; MALE; MEDIAN EMINENCE; MIDLINE THALAMIC NUCLEI; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX FACTORS;

EID: 84878425468     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2123     Document Type: Article

References (97)

1. Gore AC, Oung T, Woller MJ. Age-related changes in hypothalamic gonadotropin-releasing hormone and N-methyl-D-aspartate receptor gene expression, and their regulation by oestrogen, in the female rat. J Neuroendocrinol. 2002;14:300-309. (Pubitemid 34285299)
2. Chakraborty TR, Hof PR, Ng L, Gore AC. Stereologic analysis of estrogen receptor α (ER α) expression in rat hypothalamus and its regulation by aging and estrogen. J Comp Neurol. 2003;466:409-421. (Pubitemid 37296648)
3. Chakraborty TR, Ng L, Gore AC. Age-related changes in estrogen receptor beta in rat hypothalamus: a quantitative analysis. Endocrinology. 2003;144:4164-4171. (Pubitemid 37088772)
4. Lederman MA, Lebesgue D, Gonzalez VV, et al. Age-related LH surge dysfunction correlates with reduced responsiveness of hypothalamic anteroventral periventricular nucleus kisspeptin neurons to estradiol positive feedback in middle-aged rats. Neuropharmacology. 2010;58:314-320.
5. Sahu A, Kalra SP. Absence of increased neuropeptide Y neuronal activity before and during the luteinizing hormone (LH) surge may underlie the attenuated preovulatory LH surge in middle-aged rats. Endocrinology. 1998;139:696-702.
6. Zuo Z, Mahesh VB, Zamorano PL, Brann DW. Decreased gonadotropin-releasing hormone neurosecretory response to glutamate agonists in middle-aged female rats on proestrus afternoon: a possible role in reproductive aging? Endocrinology. 1996;137:2334-2338. (Pubitemid 26155766)
7. Yin W, Mendenhall JM, Monita M, Gore AC. Three-dimensional properties of GnRH neuroterminals in the median eminence of young and old rats. J Comp Neurol. 2009;517:284-295.
8. Kermath BA, Gore AC. Neuroendocrine control of the transition to reproductive senescence: lessons learned from the female rodent model. Neuroendocrinology. 2012;96:1-12.
9. Kok HS, van Asselt KM, van der Schouw YT, Peeters PH, Wijmenga C. Genetic studies to identify genes underlying menopausal age. Hum Reprod Update. 2005;11:483-493. (Pubitemid 41418803)
10. Dickerson SM, Gore AC. Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev Endocr Metab Disord. 2007;8:143-159. (Pubitemid 47434648)
11. Zoeller RT, Brown TR, Doan LL, et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology. 2012;153:4097-4110.
12. Barker DJ. The developmental origins of adult disease. Eur J Epidemiol. 2003;18:733-736. (Pubitemid 37039967)
13. Adewale HB, Jefferson WN, Newbold RR, Patisaul HB. Neonatal bisphenol-A exposure alters rat reproductive development and ovarian morphology without impairing activation of gonadotropin-releasing hormone neurons. Biol Reprod. 2009;81:690-699.
14. Armenti AE, Zama AM, Passantino L, Uzumcu M. Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian folliculogenesis and gene expression in adult rats. Toxicol Appl Pharmacol. 2008;233:286-296. (Pubitemid 50306578)
15. Gore AC, Walker DM, Zama AM, Armenti AE, Uzumcu M. Early life exposure to endocrine-disrupting chemicals causes lifelong molecular reprogramming of the hypothalamus and premature reproductive aging. Mol Endocrinol. 2011;25:2157-2168.
16. Shi Z, Valdez KE, Ting AY, Franczak A, Gum SL, Petroff BK. Ovarian endocrine disruption underlies premature reproductive senescence following environmentally relevant chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biol Reprod. 2007;76:198-202. (Pubitemid 46219333)
17. Gellert RJ. Kepone, mirex, dieldrin, and aldrin: estrogenic activity and the induction of persistent vaginal estrus and anovulation in rats following neonatal treatment. Environ Res. 1978;16:131-138. (Pubitemid 8369425)
18. Gellert RJ. Uterotrophic activity of polychlorinated biphenyls (PCB) and induction of precocious reproductive aging in neonatally treated female rats. Environ Res. 1978;16:123-130. (Pubitemid 8369424)
19. Faroon O, Olson J. Toxicological Profile for Polychlorinated biphenyls (PCBs). Atlanta: Agency for Toxic Substances and Disease Registry; 2000.
20. Hardy ML. Acomparison of the properties of the major commercial PBDPO/PBDE product to those of major PBB and PCB products. Chemosphere. 2002;46:717-728. (Pubitemid 34304092)
21. Haines DA, Murray J. Human biomonitoring of environmental chemicals-early results of the 2007-2009 Canadian Health Measures Survey for males and females. Int J Hygiene Environ Health. 2012;215:133-137.
22. Quinn CL, Wania F, Czub G, Breivik K. Investigating intergenerational differences in human PCB exposure due to variable emissions and reproductive behaviors. Envir Health Persp. 2011;119:641-646.
23. Layton AC, Sanseverino J, Gregory BW, Easter JP, Sayler GS, Schultz TW. In vitro estrogen receptor binding of PCBs: measured activity and detection of hydroxylated metabolites in a recombinant yeast assay. Toxicol Appl Pharmacol. 2002;180:157-163. (Pubitemid 34526456)
24. Shekhar PV, Werdell J, Basrur VS. Environmental estrogen stimulation of growth and estrogen receptor function in preneoplastic and cancerous human breast cell lines. J National Cancer Inst. 1997;89:1774-1782. (Pubitemid 27516231)
25. Kilic N, Sandal S, Colakoglu N, Kutlu S, Seyran A, Yilmaz B. Endocrine disruptive effects of polychlorinated biphenyls on the thyroid gland in female rats. The Tohoku J Exp Med. 2005;206:327-332. (Pubitemid 41195369)
26. Schrader TJ, Cooke GM. Effects of Aroclors and individual PCB congeners on activation of the human androgen receptor in vitro. Reprod Toxicol. 2003;17:15-23. (Pubitemid 36285758)
27. Woodhouse AJ, Cooke GM. Suppression of aromatase activity in vitro by PCBs 28 and 105 and Aroclor 1221. Toxicol Lett. 2004;152:91-100. (Pubitemid 39030791)
28. Van den Berg M, Birnbaum L, Bosveld AT, et al. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect. 1998;106:775-792. (Pubitemid 29073822)
29. Lutz RJ, Dedrick RL, Matthews HB, Eling TE, Anderson MW. A preliminary pharmacokinetic model for several chlorinated biphenyls in the rat. Drug Metab Dispos. 1977;5:386-396. (Pubitemid 8327318)
30. Tampal N, Lehmler HJ, Espandiari P, Malmberg T, Robertson LW. Glucuronidation of hydroxylated polychlorinated biphenyls (PCBs). Chem Res Toxicol. 2002;15:1259-1266. (Pubitemid 35222194)
31. Gellert RJ, Wilson C. Reproductive function in rats exposed prenatally to pesticides and polychlorinated biphenyls (PCB). Environ Res. 1979;18:437-443. (Pubitemid 9189664)
32. Dickerson SM, Cunningham SL, Gore AC. Prenatal PCBs disrupt early neuroendocrine development of the rat hypothalamus. Toxicol Appl Pharmacol. 2011;252:36-46.
33. Dickerson SM, Cunningham SL, Patisaul HB, Woller MJ, Gore AC. Endocrine disruption of brain sexual differentiation by developmental PCB exposure. Endocrinology. 2011;152:581-594.
34. Davis EC, Shryne JE, Gorski RA. Structural sexual dimorphisms in the anteroventral periventricular nucleus of the rat hypothalamus are sensitive to gonadal steroids perinatally, but develop peripubertally. Neuroendocrinology. 1996;63:142-148.
35. Jacobson CD, Shryne JE, Shapiro F, Gorski RA. Ontogeny of the sexually dimorphic nucleus of the preoptic area. J Comp Neurol. 1980;193:541-548. (Pubitemid 11233767)
36. Rhees RW, Shryne JE, Gorski RA. Onset of the hormone-sensitive perinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats. J Neurobiol. 1990;21:781-786. (Pubitemid 20241547)
37. Rhees RW, Shryne JE, Gorski RA. Termination of the hormone-sensitive period for differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats. Brain Res Dev Brain Res. 1990;52:17-23. (Pubitemid 20081059)
38. Steinberg RM, Juenger TE, Gore AC. The effects of prenatal PCBs on adult female paced mating reproductive behaviors in rats. Horm Behav. 2007;51:364-372. (Pubitemid 46365688)
39. Steinberg RM, Walker DM, Juenger TE, Woller MJ, Gore AC. Effects of perinatal polychlorinated biphenyls on adult female rat reproduction: development, reproductive physiology, and second generational effects. Biol Reprod. 2008;78:1091-1101. (Pubitemid 351749295)
40. Chung YW, Clemens LG. Effects of perinatal exposure to polychlorinated biphenyls on development of female sexual behavior. Bull Environ Contam Toxicol. 1999;62:664-670.
41. Gillette DM, Corey RD, Helferich WG, et al. Comparative toxicology of tetrachlorobiphenyls in mink and rats. I. Changes in hepatic enzyme activity and smooth endoplasmic reticulum volume. Fundam Appl Toxicol. 1987;8:5-14. (Pubitemid 17231786)
42. Gillette DM, Corey RD, Lowenstine LJ, Shull LR. Comparative toxicology of tetrachlorobiphenyls in mink and rats. II. Pathology. Fundam Appl Toxicol. 1987;8:15-22. (Pubitemid 17231787)
43. Murugesan P, Kanagaraj P, Yuvaraj S, Balasubramanian K, Aruldhas MM, Arunakaran J. The inhibitory effects of polychlorinated biphenyl Aroclor 1254 on Leydig cell LH receptors, steroidogenic enzymes and antioxidant enzymes in adult rats. Reprod Toxicol. 2005;20:117-126. (Pubitemid 40459660)
44. Murugesan P, Senthilkumar J, Balasubramanian K, Aruldhas MM, Arunakaran J. Impact of polychlorinated biphenyl Aroclor 1254 on testicular antioxidant system in adult rats. Hum Exp Toxicol. 2005;24:61-66. (Pubitemid 40523964)
45. 14C)polychlorinated biphenyls from maternal to fetal and suckling rats. Arch Environ Contam Toxicol. 1986;15:709-715.
46. Karmaus W, Zhu X. Maternal concentration of polychlorinated biphenyls and dichlorodiphenyl dichlorethylene and birth weight in Michigan fish eaters: a cohort study. Environ Health. 2004;3:1.
47. Law DC, Klebanoff MA, Brock JW, Dunson DB, Longnecker MP. Maternal serum levels of polychlorinated biphenyls and 1,1-di-chloro-2,2-bis(p-chlorophenyl) ethylene (DDE) and time to pregnancy. Am J Epidemiol. 2005;162:523-532. (Pubitemid 41253250)
48. Longnecker MP, Klebanoff MA, Brock JW, Guo X. Maternal levels of polychlorinated biphenyls in relation to preterm and small-for-gestational-age birth. Epidemiology. 2005;16:641-647. (Pubitemid 41233618)
49. Schantz SL. Developmental neurotoxicity of PCBs in humans: what do we know and where do we go from here? Neurotoxicol Teratol. 1996;18:217-227; discussion 229-276.
50. Lackmann GM. Polychlorinated biphenyls and hexachlorobenzene in full-term neonates. Reference values updated. Biol Neonate. 2002;81:82-85. (Pubitemid 34158314)
51. Eaton GG, Goy RW, Resko JA. Brain uptake and metabolism of estradiol benzoate and estrous behavior in ovariectomized guinea pigs. Horm Behav. 1975;6:81-97.
52. Landau IT. Effect of subcutaneous vs intraperitoneal administration of an anti-estrogen, CI-628, estradiol-and estradiol benzoate-stimulated lordosis in the ovariectomized rat. Pharmacol Biochem Behav. 1976;5:473-476. (Pubitemid 8011030)
53. Heinrich-Hirsch B, Beck H, Chahoud I, Grote K, Hartmann J, Mathar W. Tissue distribution, toxicokinetics and induction of hepatic drug metabolizing enzymes in male rats after a single s.c. dose of 3,4,3′,4′- tetrachlorobiphenyl (PCB-77). Chemosphere. 1997;34:1523-1534. (Pubitemid 27161628)
54. Lutz RJ, Dedrick RL, Tuey D, Sipes IG, Anderson MW, Matthews HB. Comparison of the pharmacokinetics of several polychlorinated biphenyls in mouse, rat, dog, and monkey by means of a physiological pharmacokinetic model. Drug Metab Dispos. 1984;12:527-535. (Pubitemid 14020821)
55. Mathews HB, Anderson MW. Effect of chlorination on the distribution and excretion of polychlorinated biphenyls. Drug Metab Dispos. 1975;3:371-380.
56. Matthews HB, Dedrick RL. Pharmacokinetics of PCBs. Annu Rev Pharmacol Toxicol. 1984;24:85-103. (Pubitemid 14129531)
57. Anderson MW, Eling TE, Lutz RJ, Dedrick RL, Matthews HB. The construction of a pharmacokinetic model for the disposition of polychlorinated biphenyls in the rat. Clin Pharmacol Ther. 1977;22:765-773. (Pubitemid 8227797)
58. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitativePCRand the 2[-δδ C(T)] method. Methods. 2001;25:402-408. (Pubitemid 34164012)
59. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.
60. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101-1108. (Pubitemid 351818697)
61. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B (Methodological). 1995;57:289-300.
62. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990;9:811-818. (Pubitemid 20343989)
63. Efron B, Tibshirani RJ. An introduction to the bootstrap. New York: Chapman and Hall; 1993.
64. Walker DM, Kirson D, Perez LF, Gore AC. Molecular profiling of postnatal development of the hypothalamus in female and male rats. Biol Reprod. 2012;87:1-12.
65. Kohl M. Standards, databases, and modeling tools in systems biology. Methods Mol Biol. 2011;696:413-427.
66. Kohl M, Wiese S, Warscheid B. Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol. 2011;696:291-303.
67. O'Connell LA, Hofmann HA. Social status predicts how sex steroid receptors regulate complex behavior across levels of biological organization. Endocrinology. 2012;153:1341-1351.
68. Akkina J, Reif J, Keefe T, Bachand A. Age at natural menopause and exposure to organochlorine pesticides in Hispanic women. J Toxicol Environ Health A. 2004;67:1407-1422. (Pubitemid 39180271)
69. Cooper GS, Savitz DA, Millikan R, Chiu Kit T. Organochlorine exposure and age at natural menopause. Epidemiology. 2002;13:729-733. (Pubitemid 44698481)
70. Hatch EE, Troisi R, Wise LA, et al. Age at natural menopause in women exposed to diethylstilbestrol in utero. Am J Epidemiol. 2006;164:682-688. (Pubitemid 44453497)
71. Knox SS, Jackson T, Javins B, Frisbee SJ, Shankar A, Ducatman AM. Implications of early menopause in women exposed to perfluorocarbons. J Clin Endocrinol Metab. 2011;96:1747-1753.
72. Farr SL, Cai J, Savitz DA, Sandler DP, Hoppin JA, Cooper GS. Pesticide exposure and timing of menopause: the Agricultural Health Study. Am J Epidemiol. 2006;163:731-742.
73. Yu ML, Guo YL, Hsu CC, Rogan WJ. Menstruation and reproduction in women with polychlorinated biphenyl (PCB) poisoning: long-term follow-up interviews of the women from the Taiwan Yucheng cohort. Int J Epidemiol. 2000;29:672-677. (Pubitemid 30612234)
74. Buck Louis GM, Rios LI, McLain A, Cooney MA, Kostyniak PJ, Sundaram R. Persistent organochlorine pollutants and menstrual cycle characteristics. Chemosphere. 2011;85:1742-1748.
75. Ojeda SR, Dubay C, Lomniczi A, et al. Gene networks and the neuroendocrine regulation of puberty. Mol Cell Endocrinol. 2010;324:3-11.
76. Lloyd JM, Hoffman GE, Wise PM. Decline in immediate early gene expression in gonadotropin-releasing hormone neurons during proestrus in regularly cycling, middle-aged rats. Endocrinology. 1994;134:1800-1805. (Pubitemid 24110740)
77. Navarro VM. New insights into the control of pulsatile GnRH release: the role of Kiss1/neurokinin B neurons. Front Endocrinol (Lausanne). 2012;3:48.
78. Weiss G, Skurnick JH, Goldsmith LT, Santoro NF, Park SJ. Menopause and hypothalamic-pituitary sensitivity to estrogen. JAMA. 2004;292:2991-2996. (Pubitemid 39665300)
79. Abel TW, Rance NE. Stereologic study of the hypothalamic infundibular nucleus in young and older women. J Comp Neurol. 2000;424:679-688. (Pubitemid 30643059)
80. Rometo AM, Krajewski SJ, Voytko ML, Rance NE. Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J Clin Endocrinol Metab. 2007;92:2744-2750. (Pubitemid 47037385)
81. Gore AC. Gonadotropin-releasing hormone neurons, NMDA receptors, and their regulation by steroid hormones across the reproductive life cycle. Brain Res Brain Res Rev. 2001;37:235-248. (Pubitemid 34020734)
82. Yosten GL, Samson WK. The melanocortins, not oxytocin, mediate the anorexigenic and antidipsogenic effects of neuronostatin. Peptides. 2010;31:1711-1714.
83. Yosten GL, Samson WK. The anorexigenic and hypertensive effects of nesfatin-1 are reversed by pretreatment with an oxytocin receptor antagonist. Am J Physiol Regul Integr Comp Physiol. 2010;298:R1642-R1647.
84. Onaka T, Takayanagi Y, Yoshida M. Roles of oxytocin neurones in the control of stress, energy metabolism, and social behaviour. J Neuroendocrinol. 2012;24:587-598.
85. Shimizu H, Inoue K, Mori M. The leptin-dependent and -independent melanocortin signaling system: regulation of feeding and energy expenditure. J Endocrinol. 2007;193:1-9. (Pubitemid 46638526)
86. Bowman RE, Maclusky NJ, Diaz SE, Zrull MC, Luine VN. Aged rats: sex differences and responses to chronic stress. Brain Res. 2006;1126:156-166. (Pubitemid 44880921)
87. Santollo J, Yao D, Neal-Perry G, Etgen AM. Middle-aged female rats retain sensitivity to the anorexigenic effect of exogenous estradiol. Behav Brain Res. 2012;232:159-164.
88. Appt SE, Ethun KF. Reproductive aging and risk for chronic disease: insights from studies of nonhuman primates. Maturitas. 2010;67:7-14.
89. Yin W, Gore AC. The hypothalamic median eminence and its role in reproductive aging. Ann NY Acad Sci. 2010;1204:113-122.
90. Jung H, Yoon BC, Holt CE. Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair. Nat Rev Neurosci. 2012;13:308-324.
91. Yin W, Wu D, Noel ML, Gore AC. Gonadotropin-releasing hormone neuroterminals and their microenvironment in the median eminence: effects of aging and estradiol treatment. Endocrinology. 2009;150:5498-5508.
92. Smith JT, Clifton DK, Steiner RA. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction. 2006;131:623-630.
93. Wiegand SJ, Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology. 1982;34:395-404. (Pubitemid 12100197)
94. Blaustein JD, King JC, Toft DO, Turcotte J. Immunocytochemical localization of estrogen-induced progestin receptors in guinea pig brain. Brain Res. 1988;474:1-15. (Pubitemid 19001179)
95. Blaustein JD, Turcotte JC. Estradiol-induced progestin receptor immunoreactivity is found only in estrogen receptor-immunoreactive cells in guinea pig brain. Neuroendocrinol. 1989;49:454-461. (Pubitemid 19119443)
96. Shughrue PJ, Lane MV, Merchenthaler I. Regulation of progesterone receptor messenger ribonucleic acid in the rat medial preoptic nucleus by estrogenic and antiestrogenic compounds: an in situ hybridization study. Endocrinology. 1997;138:5476-5484. (Pubitemid 27509711)
97. King JC, Tobet SA, Snavely FL, Arimura AA. LHRH immunopositive cells and their projections to the median eminence and organum vasculosum of the lamina terminalis. J Comp Neurol. 1982;209:287-300. (Pubitemid 12057155)