Atrazine-induced elevation or attenuation of the LH surge in the ovariectomized, estrogen-primed female rat: Role of adrenal progesterone

Reproduction

Volumn 146, Issue 4, 2013, Pages 305-314

  Goldman, Jerome M ^a   Davis, Lori K ^a,b   Murr, Ashley S ^a   Cooper, Ralph L ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b Pharmaceutical Development Services   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATRAZINE; ESTRADIOL; KISSPEPTIN; LUTEINIZING HORMONE; PROGESTERONE;

ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; ARTICLE; ATTENUATION; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; EXPOSURE; FEMALE; GENE EXPRESSION; LUTEINIZING HORMONE RELEASE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; RAT;

ADRENAL GLANDS; ANIMALS; ATRAZINE; ESTROGENS; FEMALE; HERBICIDES; KISSPEPTINS; LUTEINIZING HORMONE; OVARIECTOMY; OVARY; PROGESTERONE; RATS; RATS, LONG-EVANS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84885026206     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0011     Document Type: Article

References (52)

1. Balasubramanian B, Portillo W, Reyna A, Chen JZ, Moore AN, Dash PK & Mani SK 2008 Nonclassical mechanisms of progesterone action in the brain: I. Protein kinase C activation in the hypothalamus of female rats. Endocrinology 149 5509-5517. (doi:10.1210/en. 2008-0712)
2. Banks JA & Freeman ME 1978 The temporal requirement of progesterone on proestrus for extinction of the estrogen-induced daily signal controlling luteinizing hormone release in the rat. Endocrinology 102 426-432. (doi:10.1210/endo-102-2-426) (Pubitemid 8308349)
3. Barraclough CA, Camp P, Weiland N & Akabori A 1986 Stimulatory versus inhibitory effects of progesterone on estrogen-induced phasic LH and prolactin secretion correlated with estrogen nuclear and progestin cytosol receptor concentrations in brain and pituitary gland. Neuroendocrinology 42 6-14. (doi:10.1159/000124241) (Pubitemid 16211414)
4. Caligaris L, Astrada JJ & Taleisnik S 1971 Biphasic effect of progesterone on the release of gonadotropin in rats. Endocrinology 89 331-337. (doi:10.1210/endo-89-2-331)
5. Camp P & Barraclough CA 1985 Correlation of luteinizing hormone surges with estrogen nuclear and progestin cytosol receptors in the hypothalamus and pituitary gland. Neuroendocrinology 40 45-53. (doi:10.1159/000124050) (Pubitemid 15194790)
6. Clarke IJ 2011 Control of GnRH secretion: one step back. Frontiers in Neuroendocrinology 32 367-375. (doi:10.1016/j.yfrne.2011.01.001)
7. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, Colledge WH & Herbison AE 2008 Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. Journal of Neuroscience 28 8691-8697. (doi:10.1523/JNEUROSCI.1775-08. 2008)
8. Cooper RL, Stoker TE, Goldman JM, Parrish MB & Tyrey L 1996 Effect of atrazine on ovarian function in the rat. Reproductive Toxicology 10 257-264. (doi:10.1016/0890-6238 (96) 00054-8) (Pubitemid 26310254)
9. Cooper RL, Stoker TE, Tyrey L, Goldman JM & McElroy WK 2000 Atrazine disrupts the hypothalamic control of pituitary-ovarian function. Toxicological Sciences 53 297-307. (doi:10.1093/toxsci/53.2.297) (Pubitemid 30100147)
10. Cooper RL, Laws SC, Das PC, Narotsky MG, Goldman JM, Tyrey EL & Stoker TE 2007 Atrazine and reproductive function: mode and mechanism of action studies. Birth Defects Research. Part B: Developmental and Reproductive Toxicology 80 98-112. (doi:10.1002/bdrb.20110) (Pubitemid 46762319)
11. Couzinet B, Young J, Kujas M, Meduri G, Brailly S, Thomas JL, Chanson P & Schaison G 1999 The antigonadotropic activity of a 19-nor-progesterone derivative is exerted both at the hypothalamic and pituitary levels in women. Journal of Clinical Endocrinology and Metabolism 84 4191-4196. (doi:10.1210/jc.84.11.4191) (Pubitemid 30644216)
12. Cragin LA, Kesner JS, Bachand AM, Barr DB, Meadows JW, Krieg EF & Reif JS 2011 Menstrual cycle characteristics and reproductive hormone levels in women exposed to atrazine in the drinking water. Environmental Research 111 1293-1301. (doi:10.1016/j.envres.2011.09.009)
13. DePaolo LV & Barraclough CA 1979 Dose dependent effects of progesterone on the facilitation and inhibition of spontaneous gonadotropin surges in estrogen treated ovariectomized rats. Biology of Reproduction 21 1015-1023. (doi:10.1095/biolreprod21.4.1015) (Pubitemid 10216272)
14. Eldridge JC, Wetzel LT & Tyrey L 1999 Estrous cycle patterns of Sprague-Dawley rats during acute and chronic atrazine administration. Reproductive Toxicology 13 491-499. (doi:10.1016/S0890-6238 (99) 00056-8) (Pubitemid 30017326)
15. Everett JW & Sawyer CH 1950 A 24-hour periodicity in the "LH-release apparatus" of female rats, disclosed by barbiturate sedation. Endocrinology 47 198-218. (doi:10.1210/endo-47-3-198)
16. Fajer AB, Holzbauer M & Newport HM 1971 The contribution of the adrenal gland to the total amount of progesterone produced in the female rat. Journal of Physiology 214 115-126.
17. Faundes A, Brache V, Tejada AS, Cochon L & Alvarez-Sanchez F 1991 Ovulatory dysfunction during continuous administration of low-dose levonorgestrel by subdermal implants. Fertility and Sterility 56 27-31.
18. Foradori CD, Hinds LR, Hanneman WH & Handa RJ 2009 Effects of atrazine and its withdrawal on gonadotropin-releasing hormone neuroendocrine function in the adult female Wistar rat. Biology of Reproduction 81 1099-1105. (doi:10.1095/biolreprod.109.077453)
19. Fraites MJ, Cooper RL, Buckalew A, Jayaraman S, Mills L & Laws SC 2009 Characterization of the hypothalamic-pituitary-adrenal axis response to atrazine and metabolites in the female rat. Toxicological Sciences 112 88-99. (doi:10.1093/toxsci/kfp194)
20. Friedmann AS 2002 Atrazine inhibition of testosterone production in rat males following peripubertal exposure. Reproductive Toxicology 16 275-279. (doi:10.1016/S0890-6238 (02) 00019-9) (Pubitemid 34966266)
21. Goldman JM, Cooper RL, Edwards TL, Rehnberg GL, McElroy WK & Hein JF 1991 Suppression of the luteinizing hormone surge by chlordimeform in ovariectomized, steroid-primed female rats. Pharmacology & Toxicology 68 131-136. (doi:10.1111/j.1600-0773.1991.tb02050.x)
22. Goldman JM, Murr AS & Cooper RL 2007 The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Research. Part B, Developmental and Reproductive Toxicology 80 84-97. (doi:10.1002/bdrb.20106) (Pubitemid 46762318)
23. Goldman JM, Murr AS, Buckalew AR & Cooper RL 2008 Suppression of the steroid-primed luteinizing hormone surge in the female rat by sodium dimethyldithiocarbamate: relationship to hypothalamic catecholamines and GnRH neuronal activation. Toxicological Sciences 104 107-112. (doi:10.1093/toxsci/ kfn074) (Pubitemid 351859033)
24. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK & Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145 4073-4077. (doi:10.1210/en. 2004-0431) (Pubitemid 39120554)
25. Greig F & Weisz J 1973 Preovulatory levels of luteinizing hormone, the critical period and ovulation in rats. Journal of Endocrinology 57 235-245. (doi:10.1677/joe.0.0570235)
26. Gysin H & Knuesli E 1960 Chemistry and herbicidal properties of triazine derivatives. In Advances in Pest Control Research, vol 3, pp 289-358. Ed R Metcalf. New York: Wiley Interscience.
27. Intlekofer KA & Petersen SL 2011 17β-Estradiol and progesterone regulate multiple progestin signaling molecules in the anteroventral periventricular nucleus, ventromedial nucleus and sexually dimorphic nucleus of the preoptic area in female rats. Neuroscience 176 86-92. (doi:10.1016/j. neuroscience.2010.12.033)
28. Kam K, Park Y, Cheon M, Son GH, Kim K & Ryu K 2000 Effects of immobilization stress on estrogen-induced surges of luteinizing hormone and prolactin in ovariectomized rats. Endocrine 12 279-287. (doi:10.1385/ENDO:12:3: 279) (Pubitemid 30432245)
29. Laws SC, Hotchkiss M, Ferrell J, Jayaraman S, Mills L, Modic W, Tinfo N, Fraites M, Stoker T & Cooper R 2009 Chlorotriazine herbicides and metabolites activate an ACTH-dependent release of corticosterone in male Wistar rats. Toxicological Sciences 112 78-87. (doi:10.1093/toxsci/kfp190)
30. Legan SJ & Karsch FJ 1975 A daily signal for the LH surge in the rat. Endocrinology 96 57-62. (doi:10.1210/endo-96-1-57)
31. Legan SJ, Coon GA & Karsch FJ 1975 Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 96 50-56. (doi:10.1210/endo-96-1-50)
32. Livak KJ & Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2 (KDelta Delta C (T)) method. Methods 25 402-408. (doi:10.1006/meth.2001.1262) (Pubitemid 34164012)
33. Mahesh VB & Muldoon TG 1987 Integration of the effects of estradiol and progesterone in the modulation of gonadotropin secretion. Journal of Steroid Biochemistry 27 665-675. (doi:10.1016/0022-4731 (87) 90135-X) (Pubitemid 18020121)
34. McMullin TS, Andersen ME, Nagahara A, Lund TD, Pak T, Handa RJ & Hanneman WH 2004 Evidence that atrazine and diaminochlorotriazine inhibit the estrogen/progesterone induced surge of luteinizing hormone in female Sprague-Dawley rats without changing estrogen receptor action. Toxicological Sciences 79 278-286. (doi:10.1093/toxsci/kfh127) (Pubitemid 38786885)
35. Micevych P, Sinchak K, Mills RH, Tao L, LaPolt P & Lu J K H 2003 The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adrenalectomized rats. Neuroendocrinology 78 29-35. (doi:10.1159/000071703) (Pubitemid 36921032)
36. Navarro VM, Castellano JM, Fernández-Fernández R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P et al. 2005 Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146 156-163. (doi:10.1210/en. 2004-0836) (Pubitemid 40051735)
37. Pepe GJ & Rothchild I 1973 Metabolic clearance rate of progesterone: comparison between ovariectomized, pregnant, pseudopregnant and deciduoma-bearing pseudopregnant rats. Endocrinology 93 1200-1205. (doi:10.1210/endo-93-5-1200)
38. Pogrmic K, Fa S, Dakic V, Kaiserevic S & Kovacevic R 2009 Atrazine oral exposure of peripubertal male rats downregulates steroidogenesis gene expression in Leydig cells. Toxicological Sciences 111 189-197. (doi:10.1093/toxsci/kfp135)
39. Pogrmic-Majkic K, Fa S, Dakic V, Kaisarevic S & Kovacevic R 2010 Upregulation of peripubertal rat Leydig cell steroidogenesis following 24 h in vitro and in vivo exposure to atrazine. Toxicological Sciences 118 52-60. (doi:10.1093/toxsci/kfq227)
40. Rivest P, Devine PJ & Sanderson JT 2010 Evaluation of a bioluminescent mouse model expressing aromatase PII-promoter-controlled luciferase as a tool for the study of endocrine disrupting chemicals. Toxicology and Applied Pharmacology 249 33-40. (doi:10.1016/j.taap. 2010.08.011)
41. Roselli CE & Snipes CA 1983 Cytoplasmic progesterone receptors in the hypothalamus-preoptic area of the mouse: effect of estrogen priming. Journal of Steroid Biochemistry 19 1571-1575. (doi:10.1016/0022-4731-4731-4731 (83) 90372-2) (Pubitemid 14205828)
42. Sanderson JT, Seinen W, Giesy JP & van den Berg M 2000 2-Chloro-striazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicological Sciences 54 121-127. (doi:10.1093/toxsci/54.1.121) (Pubitemid 30152463)
43. Shaikh AA & Shaikh SA 1975 Adrenal and ovarian steroid secretion in the rat estrous cycle temporally related to gonadotropins and steroid levels found in peripheral plasma. Endocrinology 96 37-44. (doi:10.1210/endo-96-1-37)
44. Taketa Y, Yoshida M, Inoue K, Takahashi M, Sakamoto Y, Watanabe G, Taya K, Yamate J & Nishikawa A 2011 Differential stimulation pathways of progesterone secretion from newly formed corpora lutea in rats treated with ethylene glycol monomethyl ether, sulpiride, or atrazine. Toxicological Sciences 121 267-278. (doi:10.1093/toxsci/kfr062)
45. Tennant MK, Hill DS, Eldridge JC, Wetzel LT, Breckenridge CB & Stevens JT 1994 Possible antiestrogenic properties of chloro-s-triazines in rat uterus. Journal of Toxicology and Environmental Health 43 183-196. (doi:10.1080/15287399409531914) (Pubitemid 24332013)
46. Tinfo NS, Hotchkiss MG, Buckalew AR, Zorrilla LM, Cooper RL & Laws SC 2011 Understanding the effects of atrazine on steroidogenesis in rat granulosa and H295R adrenal cortical carcinoma cells. Reproductive Toxicology 31 184-193. (doi:10.1016/j.reprotox.2010.11.005)
47. Trentacoste SV, Friemann AS, Youker RT, Breckenridge CB & Zirkin BR 2001 Atrazine effects on testosterone levels and androgen-dependent reproductive organs in peripubertal male rats. Journal of Andrology 22 142-148. (Pubitemid 32012924)
48. Turgeon JL & Waring DW 2000 Progesterone regulation of the progesterone receptor in rat gonadotropes. Endocrinology 141 3422-3429. (doi:10.1210/en. 141.9.3422) (Pubitemid 32269032)
49. Turgeon JL, Van Patten SM, Shyamala G & Waring DW 1999 Steroid regulation of progesterone receptor expression in cultured rat gonadotropes. Endocrinology 140 2318-2325. (doi:10.1210/en. 140.5.2318) (Pubitemid 30636473)
50. Victor-Costa AB, Bandeira S M C, Oliveira AG, Mahecha G A B & Oliveira CA 2010 Changes in testicular morphology and steriodogenesis in adult rats exposed to atrazine. Reproductive Toxicology 29 323-331. (doi:10.1016/j.reprotox.2009.12.006)
51. Wetzel LT, Luempert LG III, Breckenridge CB, Tisdel MO, Stevens JT, Thakur AK, Extrom PJ & Eldridge JC 1994 Chronic effects of atrazine on estrus and mammary tumor formation in female Sprague-Dawley and Fischer 344 rats. Journal of Toxicology and Environmental Health 43 169-182. (doi:10.1080/15287399409531913) (Pubitemid 24332012)
52. Wetsel WC, Eraly SA, Whyte DB & Mellon PL 1993 Regulation of gonadotropin-releasing hormone by protein kinase-A and-C in immortalized hypothalamic neurons. Endocrinology 132 2360-2370. (doi:10.1210/en. 132.6.2360) (Pubitemid 23156883)