Scientific and Regulatory Policy Committee (SRPC) Paper: Assessment of Circulating Hormones in Nonclinical Toxicity Studies III. Female Reproductive Hormones

Toxicologic Pathology

Volumn 41, Issue 6, 2013, Pages 921-934

  Andersson, Håkan ^a   Stanislaus, Dinesh ^b   Wood, Charles E ^c  

^a ASTRAZENECA R AND D   (Sweden)

^b GLAXOSMITHKLINE   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

estradiol; follicle stimulating hormone; hormone measurement; luteinizing hormone; progesterone; prolactin; toxicology

Indexed keywords

GONADOTROPIN; HYPOPHYSIS HORMONE; PROLACTIN; SEX HORMONE; STEROID HORMONE;

ARTICLE; CIRCADIAN RHYTHM; DOG; ESTRUS CYCLE; FEMALE GENITAL SYSTEM; HORMONE DETERMINATION; HUMAN; MENSTRUAL CYCLE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; SEXUAL MATURITY; SPECIES DIFFERENCE;

ESTRADIOL; FOLLICLE-STIMULATING HORMONE; HORMONE MEASUREMENT; LUTEINIZING HORMONE; PROGESTERONE; PROLACTIN; TOXICOLOGY.;

ANIMALS; DOGS; ESTRADIOL; ESTROUS CYCLE; FEMALE; FOLLICLE STIMULATING HORMONE; GENITALIA, FEMALE; GONADAL HORMONES; GONADOTROPINS, PITUITARY; LUTEINIZING HORMONE; MACACA FASCICULARIS; MICE; PROGESTERONE; RATS; TOXICITY TESTS;

EID: 84880413159     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623312466959     Document Type: Article

References (109)

1. Abbott D. H. Bird I. M. (2009). Nonhuman primates as a model for human adrenal androgen production: Function and dysfunction. Rev Endocr Metab Disord 10, 33–42.
2. Alison R. H. Capen C. C. Prentice D. E. (1994). Neoplastic lesions of questionable significance to humans. Toxicol Pathol 22, 179–86.
3. Ankarberg-Lindgren C. Norjavaara E. (2008). A purification step prior to commercial sensitive immunoassay is necessary to achieve clinical usefulness when quantifying serum 17β-estradiol in prepubertal children. Eur J Endocrinol 158, 117–24.
4. Attia M. A. (1998). Cyclic changes in genital organs and vaginal cytology in cynomolgus monkeys (Macaca fascicularis). Dtsch Tierarztl Wochenschr 105, 399–404.
5. Beckman D. A. Feuston M. (2003). Landmarks in the development of the female reproductive system. Birth Defects Res (B) Dev Reprod Toxicol 68, 137–43.
6. Ben-Jonathan N. LaPensee C. R. LaPensee E. W. (2008). What can we learn from rodents about prolactin in humans. Endocrine Rev 29, 1–41.
7. Bianco A. R. De Placido S. Pagliarulo C. Fasano S. D’Istria M. De Sio L. Ricciardi I. Delrio G. (1985). Effect of adjuvant tamoxifen and CMF on endocrine function of patients with operable breast cancer. Chemioterapia 4, 252–55.
8. Bouilly J. Sonigo C. Auffret J. Gibori G. Binart N. (2012). Prolactin singnaling mechanisms in ovary. Mol Cell Endocr 356, 80–70.
9. Bowen J. M. Keyes P. L. Warren J. S. Townson D. H. (1996). Prolactin-induced regression of the rat corpus luteum: Expression of monocyte chemoattractant protein-1 and invasion of macrophages. Biol Reprod 54, 1120–27.
10. Brann D. W. Mahesh V. B. (2005). The aging reproductive neuroendocrine axis. Steroids 70, 273–83.
11. Brisken C. O’Malley B. (2010). Hormone action in the mammary gland. Cold Spring Harb Persect Biol 2, a003178.
12. Bronson F. H. Nguyen K. Q. De la Rosa J. (1996). Effect of anabolic steroids on behaviour and physiological characteristics of female mice. Physiol & Behav 59, 49–55.
13. Brott D. A. Werkheiser J. Campbell P Bentley P. Andersson H. Stewart J. Huby R. Altekar M. Kinter L. B. (2012). Inhibition of estradiol-induced prolactin release in a dual-cannulated ovariectomized rat model by Carmoxirole, a peripherally-restricted dopamine agonist. Basic & Clin Pharmacol & Toxicol 111, 411–6.
14. Capen C. C. (2004). Mechanisms of hormone-mediated carcinogenesis of the ovary. Toxicol Pathol 32, 1–5.
15. Chakravarty I. Shah P. G. Sheth A. R. Ghosh J. J. (1979). Mode of action of delta-9-tetrahydrocannabinol on hypothalamo-pituitary function in the adult female rats. J Reprod Fertil 57, 113–15.
16. Chandra S. A. Adler R. P. (2008). Frequency of different estroud stages in purpose-bred beagles: A retrospective study. Toxcol Pathol 36, 944–49.
17. Clark A. S. Kelton M. C. Whiteny A. C. (2003). Chronic administration of anabolic steroids disrupts pubertal onset and estrous cyclicity in rats. Biol Reprod 68, 465–71.
18. Cline J. M. (2007). Assessing the mammary gland of nonhuman primates: Effects of endogenous hormones and exogenous hormonal agents and growth factors. Birth Defects Res (B) Dev Reprod Toxicol 80, 126–46.
19. Cohen H. Guillaumot P. Sabbagh I. Bertrand J. (1983). A new hypoprolactinemic rat strain. Prolactin, luteinizing hormone, follicle-stimulating hormone, testosterone and corticosterone levels in males and effects of two anesthetics. Biol Reprod 28, 122–27.
20. Concannon P. W. (2011). Reproductive cycles of the domestic bitch. Anim Reprod Sci 124, 200–10.
21. Cooper R. L. Goldman J. M. Vandenbergh J. G. (1993). Monitoring of estrous cycle in the laboratory rodent by vaginal lavage. In Methods in Toxicology (Chapin R. E. Heindel J., eds.), Vol. 3, Part B. Female Reproductive Toxicology, pp. 45–56. Academic Press, Orlando, FL.
22. Döhler K. D. von zur Mühlen A. Gärtner K. Döhler U. (1977). Effect of various blood sampling techniques on serum levels of pituitary and thyroid hormones in the rat. J Endocrinol 74, 341–42.
23. Dudley S. D. (1982). Responsiveness to estradiol in central nervous system of aging female rats. Neurosci Biobehav Rev 6, 39–45.
24. Dupon C. Kim M. H. (1973). Peripheral plasma levels of testosterone, androstenedione, and oestradiol during the rat oestrus cycle. J Endocrinol 59, 653–54.
25. Esprey L. L. Adams R. R. Tanaka N. Okumura H. (1990). Effect of epostane on ovarian levels of progesterone, 17β-estradiol, prostaglandin E2, and prostaglandin F2α during ovulation in the gonadotropin-primed immature rat. Endocrinol 127, 259–63.
26. Esprey L. L. Tanaka N. Stacy S. Okumura H. (1992). Inhibition of ovulation in the gonadotropin-primed immature rat by exogenous prostaglandin E2. Prostaglandins 43, 67–74.
27. Ethun K. F. Wood C. E. Parker C. R. Jr Kaplan J. R. Chen H. Appt S. E. (2012). Effect of ovarian aging on androgen biosynthesis in a cynomolgus macaque model. Climacteric 15, 82–92.
28. Freeman M. E. Kanycska B. Lerant A. Nagy G. (2000). Prolactin: Structure, function and regulation of secretion. Physiol Rev 80, 1523–631.
29. Fuchs A. Weinbauer G. F. (2006). Feasibility of embryofetal development (EFD) studies in marmoset monkeys (Callithrix jacchus). Birth Defects Res B Dev Reprod Toxicol 76, 387.
30. Gambrell R. D. Bagnell C. A. Greenblatt R. B. (1983). Role of oestrogens and progesterone in the ethiology and prevention of endometrial cancer: Review. Am J Obstet Gynecol 146, 696–707.
31. Gala R. R. (1990). The physiology and mechanisms of the stress-induced changes in prolactin secretion in the rat. Life Sci 46, 1407–20.
32. Gilchrist R. B. Wicherek M. Heistermann M. Nayudu P. L. Hodges J. K. (2001). Changes in follicle-stimulating hormone and follicle populations during the ovarian cycle of the common marmoset. Biol Reprod 64, 127–35.
33. Goldman J. M. Murr A. S. Cooper R. L. (2007).The rodent estrous cycle: Characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol 80, 84–97.
34. Gobello C. (2006). Dopamine agonists, anti-progestins, anti-androgens, long-term-release GnRH agonists and anti-estrogens in canine reproduction: A review. Theriogenology 66, 1560–67.
35. Grattan D. R. Kokay I. C. (2008). Prolactin: A pleiotropic neuroendocrine hormone. J Neuroendocrinol 20, 752–63.
36. Haisenleder D. J. Schoenfelder A. H. Marcinko E. S. Geddis L. M. Marshall J. C. (2011). Estimation of estradiol in mouse serum samples: Evaluation of commercial estradiol immunoassays. Endocrinology 152, 4443–47.
37. Harleman J. H. Hargreaves A. Andersson H. Kirk S. (2012). Incidence and co-incidence of uterine tumours in Wistar and Sprague Dawley rats based on the RITA database—Evaluation of carcinogenicity results needs awareness of interdependency of tumour in pathogenesis. Toxicol Pathol 40, 926–30.
38. Harlow C. R. Hearn J. P. Hodges J. K. (1984). Ovulation in the marmoset monkey: Endocrinology, prediction and detection. J Endocrinol 103, 17–24.
39. Hart J. E. (1990). Endocrine pathology of estrogens: Species differences. Pharmacol Ther 7, 203–18.
40. Harvey P. W. (2011). Prolactin-induced mammary tumorigenesis is not a rodent-specific response. Toxicol Pathol 39, 1020–22.
41. Hoffmann B. Schneider S. (1993). Secretion and release of luteinizing hormone during the luteal phase of the oestrous cycle in the dog. J Reprod Fertil Suppl 47, 85–91.
42. Huang H. H. Meites J. (1975). Reproductive capacity of aging female rats. Neuroendocrinology 17, 289–95.
43. Jordan A. (1994). Toxicology of depot medroxyprogesterone acetate. Contraception 49, 189–201.
44. Kaplan J. R. Manuck S. B. (2004). Ovarian dysfunction, stress, and disease: A primate continuum. ILAR J 45, 89–115.
45. Kaplan J. R. Chen H. Appt S. E. Lees C. J. Franke A. A. Berga S. L. Wilson M. E. Manuck S. B. Clarkson T. B. (2010). Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflav,one soy diet. Hum Reprod 25, 3083–94.
46. Kavanagh M. Laursen E. (1984). Breeding seasonality among long-tailed macaques, Macaca fascicularis, in Peninsular Malaysia. Int J Primatol 5, 17–29.
47. Kawakami E. Hori T. Tsutsui T. (1997). Changes in plasma luteinizing hormone, testosterone and estradiol-17 β levels and semen quality after injections of gonadotropin releasing hormone agonist and human chorionic gonadotropin in three dogs with oligozoospermia and two dogs with azoospermia. Anim Reprod Sci 47, 157–67.
48. Kennedy T. G. Armstrong D. T. (1976). Induction of vaginal mucification in rats with testosterone and 17β-hydroxy-5α-androstan-3-one. Steroids 27, 423–30.
49. Kleinberg D. L. Ruan W. (2008). IGF-I, GH, and sex steroid effects in normal mammary gland development. J Mammary Gland Biol Neoplasia 13, 353–60.
50. Knuth U. A. Friesen H. G. (1983). Starvation induced anoestrus: Effect of chronic food restriction on body weight, its influence on oestrous cycle and gonadotrophin secretion in rats. Acta Endocrinol 104, 402–409.
51. Koizumi A. Masuda H. Wada Y. Tsukada M. Kawamura K. Kamiyama S. Walford R. L. (1989). Caloric restriction perturbs the pituitary-ovarian axis and inhibits mouse mammary tumor virus production in a high-spontaneous-mammary-tumor-incidence mouse strain (C3H/SHN). Mech Ageing Dev 49, 93–104.
52. Kooistra H. S. Okkens A. C. Bevers M. M. Popp-Snijders C. van Haaften B. Dieleman S. J. Schoemaker J. (1999). Concurrent pulsatile secretion of leuteinizing hormone and follicle-stimulating hormone during different phases of the estrous cycle and anestrus in beagle bitches. Biol Reprod 60, 65–71.
53. Labrie F. Luu-The V. Labrie C. Bélanger A. Simard J. Lin S. X. Pelletier G. (2003). Endocrine and intracrine sources of androgens in women: Inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone. Endocr Rev 24, 152–82.
54. Lawson D. M. Gala R. (1974). Influence of anaesthetics on basal, perphenazine-induced and thyrotrophin releasing hormone-induced prolactin secretion in ovariectomized, oestrogen-treated rats. J Endocrinol 66, 151–57.
55. J.A., Le, H.M., Wilson, A., Shehu, J., Mao, Y.S., Devi, J., Halperin, T., Aguilar, A., Seibold, E., Maizels, G., Gibori, Generation of mice expressing only the long form of the prolactin receptor reveals that both isoforms of the receptor are required for normal ovarian function, Biol Reprod, (2012), 86, 1-13
56. Li S. Davis B. (2007). Evaluating rodent vaginal and uterine histology in toxicity studies. Birth Defects Res B Dev Reprod Toxicol 80, 246–52.
57. Liehr J. G. (2000). Is estradiol a genotoxic mutagenic carcinogen? Endocr Rev 21, 40–54.
58. McRae G. I. Roberts B. B. Worden A. C. Bajka A. Vickery B. H. (1985). Long term reversible suppression of estrus in bitches with nafarelin acetate, a potent LHRH agonist. J Reprod Fertil 74, 389–97.
59. Milliken E. L. Ameduri R. K. Landis M. D. Behrooz A. Abdul-Karim F. W. Keri R. A. (2002). Ovarian hyperstimulation by LH leads to mammary gland hyperplasia and cancer predisposition in transgenic mice. Endocrinology 143, 3671–80.
60. Mirsky M. L. Sivaraman L. Houle C. Potter D. M. Chapin R. E. Cappon G. D. (2011). Histologic and cytologic detection of endocrine and reproductive tract effects of exemestane in female rats treated for up to twenty-eight days. Toxicol Pathol 11, 589–605.
61. Molon-Noblot S. Laroque P. Coleman J. B. Hoe C. M. Keenan K. P. (2003). The effects of ad libitum overfeeding and moderate and marked dietary restriction on age-related sponta0,neous pituitary gland pathology in Sprague-Dawley rats. Toxicol Pathol 1, 310–20.
62. Munson L. Moresco A. (2007). Comparative pathology of mammary gland cancers in domestic and wild animals. Breast Dis 28, 7–21.
63. Murai I. Ben-Jonathan N. (1990). Acute stimulation of prolactin release by estradiol: Mediation by the posterior pituitary. Endocrinology 126, 3179–84.
64. Murr S. M. Geschwind I. I. Bradford G. E. (1973). Plasma LH and FSH during different oestrous cycle conditions in mice. J Reprod Fertil 32, 221–30.
65. Nilson J. H. Abbud R. A. Keri R. A. Quirk C. C. (2000). Chronic hypersecretion of luteinizing hormone in transgenic mice disrupts both ovarian and pituitary function, with some effects modified by the genetic background. Recent Prog Horm Res 55, 69–89.
66. Nuttall M. E. Bradbeer J. N. Stroup G. B. Nadeau D. P. Hoffman S. J. Zhao H. Rehm S. Gowen M. (1998). Idoxifene — A novel selective estrogen receptor modulator prevents bone loss and lowers cholesterol levels in ovariectomized rats and decreases uterine weight in intact rats. Endocrinology 139, 5224–34.
67. O’Connor J. C. Cook J. C. Marty M. S. Davis L. G. Kaplan A. M. Carney E. W. (2002). Evaluation of Tier I screening approaches for detecting endocrine-active compounds (EACs). Crit Rev Toxicol 32, 521–49.
68. OECD (Organization for Economic Cooperation and Development). (2002). Appraisal of test methods for sex hormone disrupting chemicals. OECD Series on Testing and Assessment no. 21, Organisation for Economic Cooperation and Development, Paris, 313 pp.
69. OECD (Organization for Economic Cooperation and Development). (2009). Guidance document for histologic evaluation of endocrine and reproductive tests in rodents. OECD Series on Testing and Assessment no. 106, Organisation for Economic Cooperation and Development, Paris. 131 pp.
70. Okazaki K. Imazawa T. Nakamura H. Furukawa F. Nishikawa A. Hirose M. (2002). A repeated 28-day oral dose toxicity study of 17α-methyltestosterone in rats, based on the 'enhanced OECD Test Guideline 407' for screening the endocrine-disrupting chemicals. Arch Toxicol 75, 635–42.
71. Olson P. N. Bowen R. A. Behrendt M. D. Olson J. D. Nett T. M. (1984). Concentrations of testosterone in canine serum during late anestrus, proestrus, estrus, and early diestrus. Am J Vet Res 45, 145–48.
72. Owens W. Ashby J. Odum J. Onyon L. (2003). The OECD program to validate the rat uterotrophic bioassay. Phase 2: Dietary phytoestrogen analyses. Environ Health Perspect 111, 1559–67.
73. Pazol K. Kaplan J. R. Abbott D. Appt S. E. Wilson M. E. (2004). Practical measurement of total and bioavailable estradiol in female macaques. Clin Chim Acta 340, 117–26.
74. Quadri S. K. Spies H. G. (1976). Cyclic and diurnal patterns of serum prolactin in the Rhesus Monkey. Biol Reprod 14, 495–501.
75. Raskin R. E. Meyer D. J. (2001). Atlas of Canine and Feline Cytology. pp. 277–312, WB Saunders Co, Philadelphia, PA.
76. Rehm S. Dierksen D. Deerberg F. (1984). Spontaneous ovarian tumors in Han:NMRI mice: Histologic classification, incidence and influence of food restriction. J Natl Cancer Inst 72, 1383—95.
77. Rehm S. Solleveld H. A. Portelli S. T. Wier P. J. (2007). Histologic changes in ovary, uterus, vagina and mammary gland of mature Beagle dogs treated with the SERM Idoxifene. Birth Defects Res B Dev Reprod Toxicol 80, 225–32.
78. Rehm S. Stanislaus D. J. Wier P. J. (2007). Identification of drug-induced hyper- or hypoprolactinemia in the female rat based on general and reproductive toxicity study parameters. Birth Defects Res B Dev Reprod Toxicol 80, 253–57.
79. Rehm S. Stanislaus D. J. Williams A. (2007). Estrous cycle-dependent histology and review of sex steroid receptor expression in dog reproductive tissues and mammary gland and associated hormone levels. Birth Defects Res B Dev Reprod Toxicol 80, 233–45.
80. Rizvi S. S. Altaf S. Naseem A. A. Asif M. Rasul Z. Qayyum M. (2001). The effect of ketamine hydrochloride anesthesia on basal and N-methyl-D,L-aspartate induced plasma prolactin secretion in the adult male rhesus monkey. Life Sci 68, 1083–93.
81. Rossi E. Morabito A. Di Rella F. Esposito G. Gravina A. Labonia V. Landi G. Nuzzo F. Pacilio C. De Maio E. Di Maio M. Piccirillo M. C. De Feo G. D’Aiuto G. Botti G. Chiodini P. Gallo C. Perrone F. de Matteis A. (2009). Endocrine effects of adjuvant letrozole compared with tamoxifen in hormone-responsive postmenopausal patients with early breast cancer: The HOBOE trial. J Clin Oncol 27, 3192–97.
82. Rota A. Veronesi M. C. Volpe S. Riccardi A. Battocchio M. (2007). Estradiol-17β, progesterone and testosterone plasma concentrations during estrus in the bitch. Vet Res Commun 31 197–9.
83. Rush M. E. Blake C. A. (1982). Serum testosterone concentrations during the 4-day estrous cycle in normal and adrenalectomized rats. Proc Soc Exp Biol Med 169, 216–21.
84. Safranski T. J. Lamberson W. R. Keisler D. H. (1993). Correlations among three measures of puberty in mice and relationships with estradiol concentration and ovulation. Biol Reprod 48, 669–73.
85. Sajapitak S. Iwata K. Shahab M. Uenoyama Y. Yamada S. Kinoshita M. Bari F. Y. I'Anson H. Tsukamura H. Maeda K. (2008) Central lipoprivation-induced suppression of luteinizing hormone pulses is mediated by paraventricular catecholaminergic inputs in female rats. Endocrinology 149, 3016–24.
86. Sánchez H. L. Silva L. B. Portiansky E. L. Goys R. G. Zuccolilli G. O. (2003). Impact of very old age on hypothalamic dopaminergic neurons in the female rat: A morphometric study. J Comp Neurol 458, 319–25.
87. Sinkevicius K. W. Woloszyn K. Laine M. Jackson K. S. Greene G. L. Woodruff T. K. Burdette J. E. (2009). Characterization of the ovarian and reproductive abnormalities in prepubertal and adult estrogen non-responsive estrogen receptor α knock-in (ENERKI) mice. Steroids 74, 913–19.
88. Slayden O. D. Brenner R. M. (2004). Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: Effects of progesterone receptor antagonists. Arch Histol Cytol 67, 393–409.
89. Stanislaus D. Andersson H. Chapin R. Creasy D. Ferguson D. Gilbert M. O’Connor J. Rosol T. J. Waite Boyce R. Wood C. E. (2012). Assessment of circulating hormones in nonclinical toxicity studies. I. General concepts and consideration. Toxicol Pathol 40, 943–50.
90. Ström J. O. Theodorsson A. Theodorsson E. (2008). Substantial discrepancies in 17β-oestradiol concentrations obtained with three different commercial direct radioimmunoassay kits in rat sera. Scand J Clin Lab Invest 68, 806–13.
91. Stroud F. C. Appt S. E. Wilson M. E. Franke A. A. Adams M. R. Kaplan J. R. (2006). Concentrations of isoflavones in macaques consuming standard laboratory monkey diet. J Am Assoc Lab Anim Sci 45, 20–23.
92. Stute P. Wood C. E. Kaplan J. R. Cline J. M. (2004). Cyclic changes in the mammary gland of cynomolgus macaques. Fertil Steril 82, 1160–70.
93. Tardif S. D. Smucny D. A. Abbott D. H. Mansfield K. Schultz-Darken N. Yamamoto M. E. (2003). Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 53, 364–6 8.
94. Topaloglu A. K. Reimann F. Guclu M. Yalin A. S. Kotan L. D. Porter K. M. Serin A. Mungan N. O. Cook J. R. Ozbek M. N. Imamoglu S. Akalin N. S. Yuksel B. O'Rahilly S. Semple R. K. (2009). TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat Genet 41, 354–58.
95. USEPA (U.S. Environmental Protection Agency). (2009a). Endocrine Disruptor Screening Program (EDSP); Announcing the availability of the tier 1 screening battery and related test guidelines; notice (74 FR 54415). Accessed February 8, 2012. http:www.regulations.gov. Docket No. EPA-HQ-OPPT-2008-0521.
96. USEPA (U.S. Environmental Protection Agency). (2009b). Endocrine Disruptor Screening Program (EDSP); Announcing the availability of the tier 1 screening battery and related test guidelines; notice (74 FR 54415). Accessed February 8, 2012. http:www.regulations.gov. Docket ID No. EPA-HQ-OPPT-2009-0576.
97. Valiente C. Romero G. G. Corrada Y. de la Sota P. E. Hermo G. Gobello C. (2009). Interruption of the canine estrous cycle with a low and a high dose of the GnRH antagonist, acyline. Theriogenol 71, 408–11.
98. van Esch E. Cline J. M. Buse E. Weinbauer G. F. (2008). The Macaque endometrium, with special reference to the cynomolgus monkey (Macaca fascicularis). Toxicol Pathol 36, 67S–100.
99. Vo T. T. Jeung E. B. (2009). An evaluation of estrogenic activity of parabens using uterine calbindin-d9k gene in an immature rat model. Toxicol Sci 112, 68–77.
100. Wahab F. Aziz F. Zaman W. U. Shahab M. (2008). Short-term fasting attenuates the response of the HPG axis to kisspeptin challenge in the adult male rhesus monkey (Macaca mulatta). Life Sci 83, 633–37.
101. Walker R. F. (1983). Serotonin-reinstatement of luteinizing hormone surges after loss of positive feedback in ovariectomized rats bearing subcutaneous capsules containing oestrogen. J Endocrinol 98, 7–17.
102. Wanatabe D. Hishiya T. Sato J. Yamaguchi Y. Horiguchi K. Nagashima Y. Okaniwa A. Yoshikawa H. (2006). Changes in the reproductive organs depending on phases of reproductive cycle and aging in female cynomolgus monkeys. Toxicol Pathol 1, 169–77.
103. Weinbauer G. F. Niehoff M. Niehaus M. Srivastav S. Fuchs A. Van Esch E. Cline J. M. (2008). Physiology and endocrinology of the ovarian cycle in macaques. Toxicol Pathol 36, 7S–23S.
104. Westwood F. R. (2008). The female rat reproductive cycle: A practical histological guide to staging. Toxicol Pathol 36, 375–84.
105. WHO (World Health Organization). (2003). Global assessment of the state-of-the-science of endocrine disruptors (Damstra T. Barlow S. Bergman A. Kavlock R. Van der Kraak G., eds.), pp. 1–180. WHO/PCS/EDC/02.2, World Health Organisation, Geneva.
106. Wickings E. J. Nieschlag E. (1980). Seasonality in endocrine and exocrine testicular function of the adult rhesus monkey (Macaca mulatta). Int J Androl 3, 87–104.
107. Wilen M. E. Naftolin F. (1976). Age, weight and weight gain in the individual pubertal female rhesus monkey (Macaca mulatta). Biol Reprod 15, 356–60.
108. Xu X. Roman J. M. Issaq H. J. Keefer L. K. Veenstra T. D. Ziegler R. G. (2007). Quantitative measurement of endogenous estrogens and estrogen metabolites in human serum by liquid chromatography-tandem mass spectrometry. Anal Chem 79, 7813–21.
109. Yuan Y. D. Foley G. L. (2002). Female reproductive system. In Handbook of Toxicologic Pathology (Haschek W. M. Rousseaux C. G. Wallig M. A., eds.), 2nd ed., pp. 847–94. Academic Press, London, UK.