Regulation of baboon fetal ovarian development by placental estrogen: Onset of puberty is delayed in offspring deprived of estrogen in utero

Biology of Reproduction

Volumn 89, Issue 6, 2013, Pages

  Pepe, Gerald J ^a   Lynch, Terrie J ^a,b   Albrecht, Eugene D ^b  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Estradiol; Ovary; Pregnancy; Primate; Puberty

Indexed keywords

ESTRADIOL BENZOATE; ESTROGEN; FOLLITROPIN; LETROZOLE; PROGESTERONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD CHEMISTRY; BLOOD PRESSURE; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; ESTROGEN BLOOD LEVEL; FEMALE; FETUS; FETUS DEVELOPMENT; FOLLICULAR PHASE; LUTEAL PHASE; MENARCHE; MENSTRUAL CYCLE; NONHUMAN; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PAPIO ANUBIS; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROGESTERONE BLOOD LEVEL; PUBERTY; REGULATORY MECHANISM; REPRODUCTION; UTERUS;

ESTRADIOL; OVARY; PREGNANCY; PRIMATE; PUBERTY;

ANIMALS; ESTRADIOL; ESTROGENS; FEMALE; FETAL DEVELOPMENT; FETUS; MODELS, ANIMAL; NITRILES; OVARY; PAPIO; PLACENTA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PUBERTY; SEXUAL MATURATION; TRIAZOLES;

EID: 84901259651     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.107318     Document Type: Article

References (47)

1. Rabinovici J, Jaffe RB. Development and regulation of growth and differentiated function in human and subhuman primate fetal gonads. Endocr Rev 1990; 11:532-557.
2. Albrecht ED, Pepe GJ. Central integrative role of oestrogen in modulating the communication between the placenta and fetus that results in primate fetal-placental development. Placenta 1999; 20:129-139.
3. Pepe GJ, Albrecht ED. Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endocr Rev 1995; 16:608-648.
4. Albrecht ED, Pepe GJ. Endocrinology of pregnancy In: Brans YW, Kuehl TJ (eds.), Non-Human Primates in Perinatal Research. New York: John Wiley and Sons; 1988:13-78.
5. Pepe GJ, Billiar RB, Albrecht ED. Regulation of baboon fetal ovarian folliculogenesis by estrogen. Mol Cell Endocrinol 2006; 247:41-46.
6. Zachos NC, Billiar RB, Albrecht ED, Pepe GJ. Developmental regulation of baboon fetal ovarian maturation by estrogen. Biol Reprod 2002; 67: 1148-1156.
7. Zachos NC, Billiar RB, Albrecht ED, Pepe GJ. Regulation of oocyte microvilli development in the baboon fetal ovary by estrogen. Endocrinology 2004; 145:959-966.
8. Bocca SM, Billiar RB, Albrecht ED, Pepe GJ. Oocytes of baboon fetal primordial ovarian follicles express estrogen receptor b mRNA. Endocrine 2008; 33:254-260.
9. Pepe GJ, Billiar RB, Leavitt MG, Zachos NC, Gustafsson J-Å , Albrecht ED. Expression of estrogen receptors a and b in the baboon fetal ovary. Biol Reprod 2002; 66:1054-1060.
10. Zachos NC, Billiar RB, Albrecht ED, Pepe GJ. Developmental regulation of follicle-stimulating hormone receptor messenger RNA expression in the baboon fetal ovary. Biol Reprod 2003; 68:1911-1917.
11. Pepe GJ, Lynch TL, Davies WA Albrecht ED. Regulation of baboon fetal pituitary prolactin expression by estrogen. Biol Reprod 2009; 80: 1189-1195.
12. Bretherick KL, Hanna CW, Currie LM, Fluker MR, Hammond GL, Robinson WP. Estrogen receptor a gene polymorphisms are associated with idiopathic premature ovarian failure. Fertil Steril 2008; 89:318-324.
13. Swamy GK, Ostbye T, Skjaerven R. Association of preterm birth with long-term survival, reproduction, and next-generation preterm birth. JAMA 2008; 299:1429-1436.
14. Fowler PA, Anderson RA, Saunders PT, Kinnell H, Mason JI, Evans DB, Bhattacharya S, Flannigan S, Franks S, Monteiro A, O'Shaughnessy PJ. Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J Clin Endocrinol Metab 2011; 96: 1754-1762.
15. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009; 30:293-342.
16. Kulin HE, Grumbach MM, Kaplan SL. Changing sensitivity of the pubertal gonadal hypothalamic feedback mechanism in man. Science 1969; 166:1012-1013.
17. Steele RE, Weisz J. Changes in sensitivity of the estradiol-LH feedback system with puberty in the female rat. Endocrinology 1974; 95:513-520.
18. Ojeda SR, Skinner MK. Puberty in the rat. In: Neill JD (ed.), Knobil and Neill's Physiology of Reproduction, 3rd ed. Boston, MA: Elsevier; 2006:2061-2126.
19. Plant TM, Witchel SF. Puberty in nonhuman primates and humans. In: Neill JD (ed.), Knobil and Neill's Physiology of Reproduction, 3rd ed. Boston, MA: Elsevier; 2006:2177-2230.
20. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 2006; 26:6687-6694.
21. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A 2005; 102:1761-1766.
22. Mayer C, Costa-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine JE. Timing and completion of puberty in female mice depend on estrogen receptor a-signaling in kisspeptin neurons. Proc Natl Acad Sci U S A 2010; 107:22693-22698.
23. Roselli CE, Schrunk JM, Stadelman HL, Resko JA, Stormshak F. The effect of aromatase inhibition on the sexual differentiation of the sheep brain. Endocrine 2006; 29:501-511.
24. Britt KL, Saunders PK, McPherson SJ, Misso ML, Simpson ER, Findlay JK. Estrogen actions on follicle formation and early follicle development. Biol Reprod 2004; 71:1712-1723.
25. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007; 148:3580-3590.
26. Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP. Formation of ovarian follicles during fetal development in sheep. Biol Reprod 2002; 66:1134-1150.
27. Albrecht ED, Aberdeen GW, Pepe GJ. The role of estrogen in the maintenance of primate pregnancy. Am J Obstet Gynecol 2000; 182: 432-438.
28. Plant TM, Barker-Gibb ML. Neurobiological mechanisms of puberty in higher primates. Hum Reprod Update 2004; 10:67-77.
29. Watanabe G, Terasawa E. In vivo release of luteinizing hormone releasing hormone increases with puberty in the female rhesus monkey. Endocrinology 1989; 125:92-99.
30. Albrecht ED, Haskins AL, Hodgen GD, Pepe GJ. Luteal function in baboons with administration of the antiestrogen ethamoxytriphetol (MER-25) throughout the luteal phase of the menstrual cycle. Biol Reprod 1981; 25:451-457.
31. Albrecht ED, Aberdeen GW, Pepe GJ. Estrogen elicits cortical zonespecific effects on development of the primate fetal adrenal gland. Endocrinology 2005; 146:1737-1744.
32. Ramaswamy S, Pohl CR, McNeilly AS, Winters SJ, Plant TM. The timecourse of follicle-stimulating hormone suppression by recombinant human inhibin A in the adult male rhesus monkey (Macaca mulatta). Endocrinology 1998; 139:3409-3415.
33. Albrecht ED, Pepe GJ. Placental steroid hormone biosynthesis in primate pregnancy. Endocr Rev 1990; 11:124-150.
34. Kaplan SL, Grumbach MM. The ontogenesis of human foetal hormones. II. Luteinizing hormone (LH) and follicle stimulating hormone (FSH).Acta Endocrinol 1976; 81:808-829.
35. Ojeda SR, Roth C, Mungenast A, Heger S, Mastronardi C, Parent AS, Lomniczi A, Jung H. Neuroendocrine mechanisms controlling female puberty: new approaches, new concepts. Int J Androl 2006; 29:256-263.
36. Plant TM. Neurophysiology of puberty. J Adolesc Health 2002; 31: 185-191.
37. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005; 102: 2129-2134.
38. Terasawa E, Nass TE, Yeoman RR, Loose MD, Schultz NJ. Hypothalamic control of puberty in the female rhesus macaque. In: Norman RL (ed.), Neuroendocrine Aspects of Reproduction. New York: Academic Press; 1983:149.
39. Abbott DH, Padmanabhan V, Dumesic DA. Contributions of androgen and estrogen to fetal programming of ovarian dysfunction. Reprod Biol Endocrinol 2006; 4:17.
40. Steckler T, Wang J, Bartol FF, Roy SK, Padmanabhan V. Fetal programming: prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology 2005; 146:3185-3193.
41. Aberdeen GW, Baschat AA, Harman CR, Weiner CP, Langenberg PW, Pepe GJ, Albrecht ED. Uterine and fetal blood flow indexes and fetal growth assessment after chronic estrogen suppression in the second half of baboon pregnancy. Am J Physiol Heart Circ Physiol 2010; 298: H881-H889.
42. Aksglaede L, Juul A, Olsen LW, Sorensen TI. Age at puberty and the emerging obesity epidemic. PLoS One 2009; 4:e8450.
43. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 2003; 24:668-693.
44. Voelker R. US preterm births: "D" is for dismal. JAMA 2010; 303: 116-117.
45. Guzman C, Cabrera R, Cardenas M, Larrea F, Nathanielsz PW, Zambrano E. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol 2006; 572:97-108.
46. Leonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP. Effects of perinatal maternal food restriction on pituitarygonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 2003; 68:390-400.
47. Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci 2002; 72:63-71.