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Estrogen/Hypothalamus-Pituitary-Adrenal Axis Interactions in the Fetus: The Interplay Between Placenta and Fetal Brain

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Abstract

Objective

The hormonal interactions between the placenta and the fetal hypothalamus-pituitary-adrenal (HPA) axis are reviewed.

Methods

This review addresses data obtained from the chronically catheterized fetal sheep, drawing relevant comparisons to human fetuses.

Results

In the sheep, and perhaps in primate species, parturition is initiated by an increase in the activity of the HPA axis. The endogenous mechanisms underlying the increase in activity of the fetal HPA axis are incompletely understood but might involve an interplay between placenta and fetal hypothalamus and pituitary. Various hypotheses have been proposed, involving placental secretion of prostaglandins and various components of the fetal HPA axis. In the sheep, the influence of estradiol appears to be potent, and various experiments have suggested the possibility that, in late gestation, there exists a positive feedback relationship between placental estrogen secretion and pituitary adrenocorticotropin (ACTH) secretion. Estradiol circulates in concentrations known to stimulate fetal ACTH secretion. Additionally, estradiol circulates in the form of estradiol-3-sulfate, a molecular form that is taken up by the fetal brain and deconjugated by steroid sulfatase, which is expressed in the fetal brain. Recent evidence suggests that the interaction between estradiol and ACTH might involve production of paracrine or autocrine substances in the fetal brain. One candidate mediator is prostaglandin E2 (PGE2), highlighted by the action of estradiol on the expression of prostaglandin endoperoxide synthase-2 (PGHS-2 or COX-2) in brain regions known to be important for controlling HPA activity.

Conclusion

Estradiol, secreted by the placenta in increasing amounts in late gestation, is a potent stimulator of fetal ACTH secretion. The interactions between estradiol and the fetal HPA axis might function as a positive feedback loop that increases the concentrations of both hormones before birth.

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References

  1. Liggins GC, Kennedy PC, Holm LW. Failure of initiation of parturition after electrocoagulation of the pituitary of the fetal lamb. Am J Obstet Gynecol 1967;98:1080–6.

    Article  CAS  PubMed  Google Scholar 

  2. Bedford CA, Challis JRG, Harrison FA, Heap RB. The role of oestrogens and progesterone in the onset of parturition in several species. J Reprod Fertil 1972;16(Suppl): 1–23.

    Google Scholar 

  3. Thorburn GD, Nicol DH, Bassett JM, Shutt DA, Cox RI. Parturition in the goat and sheep: Changes in corticosteroids, progesterone, oestrogens and prostaglandin F. J Reprod Fertil 1972;16(Suppl):61–84.

    Google Scholar 

  4. Currie WB, Wong MF, Cox RI, Thorburn GD. Hormonal changes in ewes and their fetuses at parturition. J Reprod Fertil 1973;32:333–4.

    Article  CAS  PubMed  Google Scholar 

  5. Anderson ABM, Flint AP, Turnbull AC. Mechanism of activation of glucocorticoids in induction of ovine parturition: Effect on placental steroid metabolism. J Endocr 1975;66:61–70.

    Article  CAS  PubMed  Google Scholar 

  6. Thorburn GD, Hollingworth SA, Hooper SB. The trigger for parturition in sheep: Fetal hypothalamus or placenta? J Dev Physiol 1991;15:71–9.

    CAS  PubMed  Google Scholar 

  7. Challis JR, Sloboda DM, Alfaidy N, et al. Prostaglandins and mechanisms of preterm birth. Reproduction. 2002;124:1–17.

    Article  CAS  PubMed  Google Scholar 

  8. Rice GE, Wong MH, Hollingworth SA, Thorburn GD. Prostaglandin G/H synthase activity in ovine cotyledons: A gestational profile. Eicosanoids 1990;3:231–6.

    CAS  PubMed  Google Scholar 

  9. Challis JRG, Dilley SR, Robinson JS, Thorburn GD. Prostaglandins in the circulation of the fetal lamb. Prostaglandins 1976;11:1041–52.

    Article  CAS  PubMed  Google Scholar 

  10. Louis TM, Challis JRG, Robinson JS, Thorburn GD. Rapid increase in fetal corticosteroids after prostaglandin E2. Nature 1976;264:797–999.

    Article  CAS  PubMed  Google Scholar 

  11. Hedge GA, Hanson SD. The effects of prostaglandins on ACTH secretion. Endocrinology 1972;91:925–33.

    Article  CAS  PubMed  Google Scholar 

  12. Ratter S, Rees LH, Landon JR, et al. The effect of prostaglandin E2 infusion in the fetal lamb on fetal plasma ACTH, prolactin and Cortisol concentrations. Prostaglandins 1979;18:101–16.

    Article  CAS  PubMed  Google Scholar 

  13. Cudd TA, Wood CE. Does intracarotid PGE2 increase plasma ACTH concentration in concious adult ewes? Am J Physiol 1991;261:E395–401.

    CAS  PubMed  Google Scholar 

  14. Cudd TA, Wood CE. Prostaglandin E2 releases ovine fetal ACTH from a site not perfused by the carotid vasculature. Am J Physiol 1992;263:R136–40.

    CAS  PubMed  Google Scholar 

  15. Cudd TA, Castro MI, Wood CE. Content, in vivo release, and bioactivity of fetal pulmonary immunoreactive adrenocorticotropin. Am J Physiol 1993;265:E667–72.

    CAS  PubMed  Google Scholar 

  16. Cudd TA, Wood CE. Secretion and clearance of immunoreactive ACTH by fetal lung. Am J Physiol 1995;268:E845–8.

    CAS  PubMed  Google Scholar 

  17. Wood CE, Barkoe D, The A, et al. Fetal pulmonary immunoreactive adrenocorticotropin: Molecular weight and cellular localization. Regul Pept 1998;73:191–6.

    Article  CAS  PubMed  Google Scholar 

  18. Rudolph AM. Congenital Diseases of the Heart. Chicago: Year Book Medical, 1974:17–28.

    Google Scholar 

  19. Reimsnider SK, Wood CE. Colocalisation of prostaglandin en-doperoxide synthase and immunoreactive adrenocorticotropic hormone in ovine foetal pituitary. J Endocr 2004;180:303–10.

    Article  CAS  PubMed  Google Scholar 

  20. Tong H, Richards E, Wood CE. Prostaglandin endoperoxide synthase-2 abundance is increased in brain tissues of late-gestation fetal sheep in response to cerebral hypoperfusion. J Soc Gynecol Investig 1999;6:127–35.

    Article  CAS  PubMed  Google Scholar 

  21. Tong H, Dhillon H, Wood CE. Induction of PGHS-2 mRNA in response to cerebral hypoperfusion in late- gestation fetal sheep. Prostaglandins Other Lipid Mediat 2000;62:165–72.

    Article  CAS  PubMed  Google Scholar 

  22. Tong H, Gridley KE, Wood CE. Induction of immunoreactive prostaglandin H synthases 1 and 2 and fos in response to cerebral hypoperfusion in late-gestation fetal sheep. J Soc Gynecol Investig 2002;9:342–50.

    Article  CAS  PubMed  Google Scholar 

  23. Breder CD, Smith WL, Raz A, et al. Distribution and characterization of cyclooxygenase immunoreactivity in the ovine brain. J Comp Neurol 1992;322:409–38.

    Article  CAS  PubMed  Google Scholar 

  24. Breder CD, DeWitt DL, Kraig RP. Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 1995;355:296–315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chemtob S, Li DY, Varma DR. Deficiency in prostaglandin E2 (PGE2) receptors, mainly EP2 subtype, on brain synaptosomes in early development: Implications on cerebral metabolism. Semin Perinatol 1994;18:23–9.

    CAS  PubMed  Google Scholar 

  26. Pace-Asciak C, Nashat M. Catabolism of prostaglandin en-doperoxides into prostaglandin E2 and F2 by the rat brain. J Neurochem 1976;27:551–5.

    Article  CAS  PubMed  Google Scholar 

  27. Pace-Asciak CR, Rangaraj G. Prostaglandin biosynthesis and catabolism in the developing fetal sheep brain. J Biol Chem 1976;251:3381–5.

    CAS  Google Scholar 

  28. Tai TC, MacLusky NJ, Adamson SL. Ontogenesis of prostaglandin E2 binding sites in the brainstem of the sheep. Brain Res 1994;652:28–39.

    Article  CAS  PubMed  Google Scholar 

  29. Norton JL, Adamson SL, Bocking AD, Han VK. Prostaglandin-H synthase-1 (PGHS-1) gene is expressed in specific neurons of the brain of the late gestation ovine fetus. Brain Res Dev Brain Res 1996;95:79–96.

    Article  CAS  PubMed  Google Scholar 

  30. Walton M, Sirimanne E, Williams C, et al. Prostaglandin H synthase-2 and cytosolic phospholipase A2 in the hypoxicischemic brain: Role of neuronal death or survival? Brain Res Mol Brain Res 1997;50:165–70.

    Article  CAS  PubMed  Google Scholar 

  31. Li S, Wang Y, Matsumura K, et al. The febrile response to lipopolysaccharide is blocked in cyclooxygenase-2(-/-), but not in cyclooxygenase-1(-/-) mice. Brain Res 1999;825:86–94.

    Article  CAS  PubMed  Google Scholar 

  32. Nakamura K, Kaneko T, Yamashita Y, et al. Immunocyto-chemical localization of prostaglandin EP3 receptor in the rat hypothalamus. Neurosci Lett 1999;260:117–20.

    Article  CAS  PubMed  Google Scholar 

  33. Koistinaho J, Koponen S, Chan PH. Expression of cyclooxygen-ase-2 mRNA after global ischemia is regulated by AMPA receptors and glucocorticoids. Stroke 1999;30:1900–5.

    Article  CAS  PubMed  Google Scholar 

  34. Planas AM, Soriano MA, Justicia C, Rodriguez-Farre E. Induction of cyclooxygenase-2 in the rat brain after a mild episode of focal ischemia without tissue inflammation or neural cell damage. Neurosci Lett 1999;275:141–4.

    Article  CAS  PubMed  Google Scholar 

  35. Deauseault D, Giroux D, Wood CE. Ontogeny of immunoreactive prostaglandin endoperoxide synthase isoforms in ovine fetal pituitary, hypothalamus, and brainstem. Neuroendocrinology 2000;71:287–91.

    Article  CAS  PubMed  Google Scholar 

  36. Degi R, Thore C, Bari F, et al. Ischemia increases prostaglandin H synthase-2 levels in retina and visual cortex in piglets. Graefes Arch Clin Exp Ophthalmol 2001;239:59–65.

    Article  CAS  PubMed  Google Scholar 

  37. Nodwell A, Carmichael L, Fraser M, Challis J, Richardson B. Placental release of corticotrophin-releasing hormone across the umbilical circulation of the human newborn. Placenta 1999;20:197–202.

    Article  CAS  PubMed  Google Scholar 

  38. Okamoto E, Takagi T, Azuma C, et al. Expression of the corti-cotropin-releasing hormone (CRH) gene in human placenta and amniotic membrane. Horm Metabol Res 1990;22:394–7.

    Article  CAS  Google Scholar 

  39. McLean M, Bisits A, Davies J, Woods R, Lowry P, Smith R. A placental clock controlling the length of human pregnancy. Nat Med 1995;1:460–3.

    Article  CAS  PubMed  Google Scholar 

  40. Robinson BG, Emanuel RL, Frim DM, Majzoub JA. Glucocorticoid stimulates expression of corticotropin-releasing hormone gene in human placenta. Proc Natl Acad Sci USA 1988;85:5244–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Challis J, Sloboda D, Matthews S, et al. Fetal hypothalamic-pituitary adrenal (HPA) development and activation as a determinant of the timing of birth, and of postnatal disease. Endocr Res 2000;26:489–504.

    Article  CAS  PubMed  Google Scholar 

  42. Challis JRG, Matthews SG, Gibb W, Lye SJ. Endocrine and paracrine regulation of birth at term and preterm. Endocr Rev 2000;21:514–50.

    CAS  PubMed  Google Scholar 

  43. Smith R. Alterations in the hypothalamic pituitary adrenal axis during pregnancy and the placental clock that determines the length of parturition. J Reprod Immunol 1998;39:215–20.

    Article  CAS  PubMed  Google Scholar 

  44. Petraglia F, Florio P, Nappi C, Genazzani AR. Peptide signaling in human placenta and membranes: Autocrine, paracrine, and endocrine mechanisms. Endocr Rev 1996;17:156–86.

    CAS  PubMed  Google Scholar 

  45. Petraglia F, Aguzzoli L, Florio P, et al. Maternal plasma and placental immunoreactive corticotrophin-releasing factor concentrations in infection-associated term and pre-term delivery. Placenta 1995;16:157–64.

    Article  CAS  PubMed  Google Scholar 

  46. Keller-Wood M, Wood CE. Corticotropin-releasing factor in the ovine fetus and pregnant ewe: role of the placenta. Am J Physiol 1991;261:R995–1002.

    CAS  PubMed  Google Scholar 

  47. Frim DM, Emanuel RL, Robinson BG, et al. Characterization and gestational regulation of corticotropin-releasing hormone messenger RNA in human placenta. J Clin Invest 1988;82:287–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Jones CT, Gu W, Parer JT. Production of corticotrophin releasing hormone by the sheep placenta in vivo. J Dev Physiol 1989;11:97–101.

    CAS  PubMed  Google Scholar 

  49. Wood CE, Keller-Wood M. Induction of parturition by Cortisol: Effects on negative feedback sensitivity and plasma CRF. J Dev Physiol 1991;16:287–92.

    CAS  PubMed  Google Scholar 

  50. Laatikainen T, Saijonmaa O, Salminen K, Wahlstrom T. Localization and concentrations of B-endorphin and B-lipotropin in human placenta. Placenta 1987;8:381–7.

    Article  CAS  PubMed  Google Scholar 

  51. Waddell BJ, Burton PJ. Release of bioactive ACTH by perifused human placenta at early and late gestation. J Endocrinol 1993;136:345–53.

    Article  CAS  PubMed  Google Scholar 

  52. Liotta A, Osathanondh R, Ryan KJ, Krieger DT. Presence of corticotropin in human placenta: Demonstration of in vitro synthesis. Endocrinology 1977;101:1552–8.

    Article  CAS  PubMed  Google Scholar 

  53. Odagiri E, Sherrell BJ, Mount CD, Nicholson WE, Orth DN. Human placental immunoreactive corticotropin, lipotropin, and beta-endorphin: Evidence for a common precursor. Proc Natl Acad Sci USA 1979;76:2027–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Grigorakis SI, Anastasiou E, Dai K, Souvatzoglou A, Alevizaki M. Three mRNA transcripts of the proopiomelanocortin gene in human placenta at term. Eur J Endocrinol 2000;142:533–6.

    Article  CAS  PubMed  Google Scholar 

  55. Hodgen GD, Gulyas BJ, Tullner WW. Role of the primate placenta in Cortisol secretion by the maternal adrenals. Steroids 1975;26:233–40.

    Article  CAS  Google Scholar 

  56. Knobil E, Briggs FN. Fetal-maternal endocrine interrelations: The hypophyseal-adrenal system. Endocrinology 1955;57:147–52.

    Article  CAS  PubMed  Google Scholar 

  57. Keller-Wood M, Wood CE. Does the ovine placenta secrete ACTH under normoxic or hypoxic conditions? Am J Physiol 1991;260:R389–95.

    CAS  PubMed  Google Scholar 

  58. McDonald TJ, Rose JC, Figueroa JP, Gluckman PD, Nathanielsz PW. The effect of hypothalamic paraventricular nuclear lesions placed at 108–110 days gestational age on plasma ACTH concentrations in the fetal sheep. J Dev Physiol 1988;10:191–200.

    CAS  PubMed  Google Scholar 

  59. McDonald TJ, Nathanielsz PW. Bilateral destruction of the fetal paraventricular nuclei prolongs gestation in sheep. Am J Obstet Gynecol 1991;165:764–70.

    Article  CAS  PubMed  Google Scholar 

  60. Gluckman PD, Mallard C, Boshier DP. The effect of hypothalamic lesions on the length of gestation in fetal sheep. Am J Obstet Gynecol 1991;165:1464–8.

    Article  CAS  PubMed  Google Scholar 

  61. Liggins GC, Kennedy PC. Effects of electrocoagulation of the foetal lamb hypophysis on growth and development. J Endocrinol 1968;40:371–81.

    Article  CAS  PubMed  Google Scholar 

  62. Zakar T, Teixeira FJ, Hirst JJ, Guo F, MacLeod EA, Olson DM. Regulation of prostaglandin endoperoxide H synthase by glucocorticoids and activators of protein kinase C in the human amnion. J Reprod Fertil 1994;100:43–50.

    Article  CAS  PubMed  Google Scholar 

  63. Zakar T, Hirst JJ, Mijovic JE, Olson DM. Glucocorticoids stimulate the expression of prostaglandin endoperoxide H synthase-2 in amnion cells. Endocrinology 1995;136:1610–9.

    Article  CAS  PubMed  Google Scholar 

  64. Whittle WL, Holloway AC, Lye SJ, Gibb W, Challis JR. Prostaglandin production at the onset of ovine parturition is regulated by both estrogen-independent and estrogen-dependent pathways. Endocrinology 2000;141:3783–91.

    Article  CAS  PubMed  Google Scholar 

  65. Whittle WL, Gibb W, Challis JR. The characterization of human amnion epithelial and mesenchymal cells: The cellular expression, activity and glucocorticoid regulation of prostaglandin output. Placenta 2000;21:394–401.

    Article  CAS  PubMed  Google Scholar 

  66. Burgess LH, Handa RJ. Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated function in female rats. Endocrinology 1992;131:1261–9.

    Article  CAS  PubMed  Google Scholar 

  67. Viau V, Meaney MJ. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991;129:2503–11.

    Article  CAS  PubMed  Google Scholar 

  68. Viau V, Chu A, Soriano L, Dallman MF. Independent and overlapping effects of corticosterone and testosterone on corticotropin-releasing hormone and arginine vasopressin mRNA expression in the paraventricular nucleus of the hypothalamus and stress-induced adrenocorticotropic hormone release. J Neurosa 1999;19:6684–93.

    CAS  Google Scholar 

  69. Wood CE, Saoud CJ. Influence of estradiol and androstenedi-one on ACTH and Cortisol secretion in the ovine fetus. J Soc Gynecol Investig 1997;4:279–83.

    Article  CAS  PubMed  Google Scholar 

  70. Saoud CJ, Wood CE. Modulation of ovine fetal adrenocorti-cotropin secretion by androstenedione and 17beta-estradiol. Am J Physiol 1997;272:R1128–34.

    CAS  PubMed  Google Scholar 

  71. Purinton SC, Wood CE. Oestrogen augments the fetal ovine hypothalamus-pituitary-adrenal axis in response to hypotension. J Physiol 2002;544:919–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wood CE, Saoud CJ, Stoner TA, Keller-Wood M. Estrogen and androgen influence hypothalamic AVP and CRF concentrations in fetal and adult sheep. Regul Pept 2001;98:63–8.

    Article  CAS  PubMed  Google Scholar 

  73. Saoud CJ, Wood CE. Developmental changes and molecular weight of immunoreactive glucocorticoid receptor protein in the ovine fetal hypothalamus and pituitary. Biochem Biophys Res Commun 1996;229:916–21.

    Article  CAS  PubMed  Google Scholar 

  74. Pomerantz SM, Fox TO, Sholl SA, Vito CC, Goy RW. Androgen and estrogen receptors in fetal rhesus monkey brain and anterior pituitary. Endocrinology 1985;116:83–9.

    Article  CAS  PubMed  Google Scholar 

  75. Simerly RB, Chang C, Muramatsu M, Swanson LW. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. J Comp Neurol 1990;294:76–95.

    Article  CAS  PubMed  Google Scholar 

  76. Lisciotto CA, Morrell JI. Circulating gonadal steroid hormones regulate estrogen receptor mRNA in the male rat forebrain. Mol Brain Res 1993;20:79–90.

    Article  CAS  PubMed  Google Scholar 

  77. Lehman MN, Ebling FJP, Moenter SM, Karsch FJ. Distribution of estrogen receptor-immunoreactive cells in the sheep brain. Endocrinology 1993;133:876–86.

    Article  CAS  PubMed  Google Scholar 

  78. Mize AL, Poisner AM, Alper RH. Estrogens act in rat hippocampus and frontal cortex to produce rapid, receptor-mediated decreases in serotonin 5-HT(l A) receptor function. Neuroendocrinology 2001;73:166–74.

    Article  CAS  PubMed  Google Scholar 

  79. Wu WX, Ma XH, Zhang Q, Buchwalder L, Nathanielsz PW. Regulation of prostaglandin endoperoxide H synthase 1 and 2 by estradiol and progesterone in nonpregnant ovine myometrium and endometrium in vivo. Endocrinology 1997;138:4005–12.

    Article  CAS  PubMed  Google Scholar 

  80. Masferrer JL, Needleman P. Anti-inflammatories for cardiovascular disease. Proc Natl Acad Sci USA 2000;97:12400–1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Martinez RV, Reval M, Campos MD, Terron JA, Dominguez R, Lopez FJ. Involvement of peripheral cyclooxygenase-1 and cyclooxygenase-2 in inflammatory pain. J Pharm Pharmacol 2002;54:405–12.

    Article  CAS  PubMed  Google Scholar 

  82. Yamagata K, Matsumura K, Inoue W, et al. Coexpression of microsomal-type prostaglandin E synthase with cyclooxygenase-2 in brain endothelial cells of rats during endotoxin-induced fever. J Neurosci 2001;21:2669–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Li S, Bailou LR, Morham SG, Blatteis CM. Cyclooxygenase-2 mediates the febrile response of mice to interleukin-1beta. Brain Res 2001;910:163–73.

    Article  CAS  PubMed  Google Scholar 

  84. Chandrasekharan NV, Dai H, Roos KL, et al. COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: Cloning, structure, and expression. Proc Natl Acad Sci USA 2002;99:13926–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Wood CE, Giroux D. Central nervous system prostaglandin endoperoxide synthase-1 and -2 responses to oestradiol and cerebral hypoperfusion in late-gestation fetal sheep. J Physiol 2003;549:573–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Carnegie JA, Robertson HA. Conjugated and unconjugated estrogens in fetal and maternal fluids of the pregnant ewe: A possible role for estrone sulfate during early pregnancy. Biol Reprod 1978;19:202–11.

    Article  CAS  PubMed  Google Scholar 

  87. Payne AH, Lawrence CC, Foster DL, Jaffe RB. Intranuclear binding of 17ß-estradiol and estrone in female ovine pituitaries following incubation with estrone sulfate. J Biol Chem 1973;248:1598–602.

    CAS  PubMed  Google Scholar 

  88. Kuiper GG, Carlsson B, Grandien K, et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997;138:863–70.

    Article  CAS  PubMed  Google Scholar 

  89. Gips H, Bailer P, Korte K. Placental steroid metabolism in a case of placental sulfatase deficiency. J Endocrinol Invest 1980;3:51–8.

    Article  CAS  PubMed  Google Scholar 

  90. DiGiovanna JJ, Robinson-Bostom L. Ichthyosis: Etiology, diagnosis, and management. Am J Clin Dermatol 2003;4:81–95.

    Article  Google Scholar 

  91. Traupe H, Happle R. Clinical spectrum of steroid sulfatase deficiency: X-linked recessive ichthyosis, birth complications, and cryptorchidism. Eur J Pediatr 1983;140:19–21.

    Article  CAS  PubMed  Google Scholar 

  92. Shapiro LJ. Steroid sulfatase deficiency and X-linked ichthyosis. In: Scriver CR, Beaudet AL, Sly WS, Valle D, eds. The Metabolic Basis of Inherited Disease. New York: McGraw-Hill, 1998:1945–64.

    Google Scholar 

  93. Gurpide E, Marks C. Influence of endometrial 17 beta-hydroxysteroid dehydrogenase activity on the binding of estradiol to receptors. J Clin Endocrinol Metab 1981;52:252–5.

    Article  CAS  PubMed  Google Scholar 

  94. Martel C, Rheaume E, Takahashi M, et al. Distribution of 17 beta-hydroxysteroid dehydrogenase gene expression and activity in rat and human tissues. J Steroid Biochem Mol Biol 1992;41:597–603.

    Article  CAS  PubMed  Google Scholar 

  95. Lakshmi S, Balasubramanian AS. Studies on the chao tropic ally solubilized arylsulfatase C and estrone sulfatase of sheep brain. Biochem Biophys Acta 1979;567:184–95.

    CAS  PubMed  Google Scholar 

  96. Lakshmi S, Balasubramanian AS. The distribution of estrone sulphatase, dehydroepiandrosterone sulphatase, and arylsul-phatase C in the primate (Macaca radiata) brain and pituitary. J Neurochem 1981;37:358–62.

    Article  CAS  PubMed  Google Scholar 

  97. Mathew J, Balasubramanian AS. Arylsulphatase C and estrone sulphatase of sheep hypothalamus, preoptic area, and midbrain: Separation by hydrophobic interaction chromatography and evidence for differences in their lipid environment. J Neurochem 1982;39:1205–9.

    Article  CAS  PubMed  Google Scholar 

  98. Connolly PB, Resko JA. Estrone sulfatase activity in rat brain and pituitary: effects of gonadectomy and the estrous cycle. J Steroid Biochem 1989;33:1013–8.

    Article  CAS  PubMed  Google Scholar 

  99. Platia MP, Fencl MD, Elkind KE, Canick JA, Tushinsky D. Estrone sulfatase activity in the human brain and estrone sulfate levels in the normal menstrual cycle. J Steroid Biochem 1984;21:237–41.

    Article  CAS  PubMed  Google Scholar 

  100. Purinton SC, Newman H, Castro MI, Wood CE. Ontogeny of estrogen sulfatase activity in ovine fetal hypothalamus, hippocampus, and brain stem. Am J Physiol 1999;276:R1647–52.

    CAS  PubMed  Google Scholar 

  101. Purinton SC, Wood CE. Ovine fetal estrogen sulfotransferase in brain regions important for hypothalamus-pituitary-adrenal axis control. Neuroendocrinology 2000;71:237–42.

    Article  CAS  PubMed  Google Scholar 

  102. Sawchenko PE, Imaki T, Potter E, Kovacs K, Imaki J, Vale W. The functional neuroanatomy of corticotropin-releasing factor. Ciba Found Symp 1993;172:5–21 (abstr).

    CAS  PubMed  Google Scholar 

  103. Wood CE, Gridley KE, Keller-Wood M. Biological activity of 17beta-estradiol-3-sulfate in ovine fetal plasma and uptake in fetal brain. Endocrinology 2003;144:599–604.

    Article  CAS  PubMed  Google Scholar 

  104. Marselos M, Tomatis L. Diethylstilboestrol: II, pharmacology, toxicology and carcinogenicity in experimental animals. Eur J Cancer 1992;29A:149–55.

    CAS  PubMed  Google Scholar 

  105. Jaffe RB. Role of the human fetal adrenal gland in the initiation of parturition. Front Horm Res 2001;27:75–85.

    Article  CAS  PubMed  Google Scholar 

  106. Jaffe RB, Seron-Ferre M, Crickard K, Koritnik D, Mitchell BF, Huhtaniemi IT. Regulation and function of the primate fetal adrenal gland and gonad. Recent Prog Horm Res 1981;37:41–97.

    CAS  PubMed  Google Scholar 

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  1. Department of Physiology and Functional Genomics, University of Florida College of Medicine, P.O. Box 100274, Gainesville, FL, 32610-0274, USA

    Charles E. Wood PhD

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Wood, C.E. Estrogen/Hypothalamus-Pituitary-Adrenal Axis Interactions in the Fetus: The Interplay Between Placenta and Fetal Brain. Reprod. Sci. 12, 67–76 (2005). https://doi.org/10.1016/j.jsgi.2004.10.011

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