Skip to main content
SpringerLink
Log in

Prenatal and Postnatal Ovine Adrenal Cell responses to Prostaglandin E2

  • Original Article
  • Published:
The Journal of the Society for Gynecologic Investigation: JSGI Aims and scope Submit manuscript

Abstract

Objective

To examine the secretory effect of prostaglandin E2 (PGE2) and ACTH on the adrenal glands of prenatal and postnatal sheep.

Methods

Immunocytochemistry was used to examine the adrenal cortex and medulla for 17α-hydroxylase and tyrosine hydroxylase immunoreactivity. Microphysiometric technique was used to measure [H+] after exposure of whole dispersed prenatal and postnatal adrenal glands to PGE2, ACTH, or both.

Results

Immunocytochemistry showed many cortical-type cells in all adrenal medullae and many medullary-type cells in fetal adrenal cortices. Maximum H+ responsiveness to PGE2 deceased with increasing age. The developmental age-related pattern of maximum percentage change in [H+] during ACTH exposure was similar to previous findings with cortisol production as the endpoint. ACTH stimulated H+ production at 80 days’ gestation and at all ages greater than 125 days’ gestation (P <. 05). The molar concentration of ligand required to elicit a response that was 50% of maximum response (EC50) for the ACTH response was lower in fetuses than in newborn lambs (< 1 day and 3 days old), but there was no change in EC50 for PGE2 across the ages studied. Adrenal cell response to ACTH after prior ACTH and PGE2 exposure was higher (P <. 05) compared with ACTH after ACTH or ACTH alone at 110 days’ gestation only and was lower in 3-day-old lambs.

Conclusions

Based on the ACTH results, microphysiometry was a valid method for investigating dispresed adrenal cell physiology. Prostaglandin E2 stimulated dispersed adrenal cells during the mid-gestation ACTH refractory period, but this effect decreased with increasing age. Prostaglandin E2 sensitized adrenal cells to ACTH at 110 days’ gestation but inhibited ACTH effects at postnatal day 3.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Mann SE, Nijland MJ, Ross MG. Fetal absorption of intra-amniotic aldosterone: Effects on urine composition. J Soc Gynecol Investig 1999;6:252–7.

    CAS  PubMed  Google Scholar 

  2. Benson CA, Wintour EM. The effect of bilateral fetal adrenalectomy on fluid balance in the ovine fetus. J Physiol (Lond) 1995;489(Pt 1):235–41.

    Article  CAS  Google Scholar 

  3. Liggins GC. Adrenocortical-related maturational events in the fetus. Am J Obstet Gynecol 1976;126:931–41.

    Article  CAS  PubMed  Google Scholar 

  4. Liggins GC, Fairclough RJ, Grieves SA, Kendall JZ, Knox BS. The mechanism of initiation of parturition in the ewe. Rec Prog Horm Res 1973;29:111–59.

    CAS  PubMed  Google Scholar 

  5. Challis JRG, Brooks AN. Maturation and activation of hypotha-lamic-pituitary-adrenal function in fetal sheep. Endocrine Rev 1989;10:182–204.

    Article  CAS  Google Scholar 

  6. Lewis AB, Evans WN, Sischo W. Plasma catecholamine responses to hypoxemia in fetal lambs. Biol Neonate 1982;41:115–22.

    Article  CAS  PubMed  Google Scholar 

  7. Paulick R, Kastendieck E, Weth B, Wernze H. Metabolic, cardiovascular and sympathoadrenal reactions of the fetus to progressive hypoxia—animal experiment studies. Z Geburtshilfe Perinatol 1987;191:130–9.

    CAS  PubMed  Google Scholar 

  8. Cheung CY. Fetal adrenal medulla catecholamine response to hypoxia-direct and neural components. Am J Physiol 1990;258:R1340–6.

    CAS  PubMed  Google Scholar 

  9. Thorburn GD. The placenta, prostaglandins and parturition: A review. Reprod Fertil Dev 1991;3:277–94.

    Article  CAS  PubMed  Google Scholar 

  10. Liggins GC, Scroop GC, Haughey KG. Comparison of the effects of prostaglandin E2, prostacyclin and 1-24 adrenocorticotrophin on plasma Cortisol levels of fetal sheep. J Endocrinol 1982;95:153–62.

    Article  CAS  PubMed  Google Scholar 

  11. Comline RS, Silver M. Development of activity in the adrenal medulla of the foetus and new-born animal. Br Med Bull 1966;22:16–20.

    Article  CAS  PubMed  Google Scholar 

  12. Comline RS, Silver M. The release of adrenaline and noradrenaline from the adrenal glands of the foetal sheep. J Physiol 1961;156:424–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hooper SB, Coulter CL, Deayton JM, Harding R, Thorburn GD. Fetal endocrine responses to prolonged hypoxemia in sheep. Am J Physiol 1990;259:R703–8.

    CAS  PubMed  Google Scholar 

  14. Karaplis AC, Powell WS. Prostaglandin E-binding sites in the fetal adrenal. Endocrinology 1981;109:2124–8.

    Article  CAS  PubMed  Google Scholar 

  15. Ajilore O, Sapolsky RM. Application of silicon microphysiometry to tissue slices: Detection of metabolic correlates of selective vulnerability. Brain Research 1997;752:99–106.

    Article  CAS  PubMed  Google Scholar 

  16. Chio CL, Lajiness ME, Huff RM. Activation of heterologously expressed D3 dopamine receptors: Comparison with D2 dopamine receptors. Mol Pharmacol 1994;45:51–60.

    CAS  PubMed  Google Scholar 

  17. McConnell HM, Owicki JC, Parce JW, et al. The cytosensor microphysiometer: Biological applications of silicon technology. Science 1992;257:1906–12.

    Article  CAS  PubMed  Google Scholar 

  18. Owicki JC, Parce JW. Bioassays with a microphysiometer. Nature 1990;344:271

    Article  CAS  PubMed  Google Scholar 

  19. Owicki JC, Parce JW. Biosensors based on the energy metabolism of living cells: The physical chemistry and cell biology of extracellular acidification. Biosens Bioelectron 1992;7:255–72.

    Article  CAS  PubMed  Google Scholar 

  20. Owicki JC, Parce JW, Kercso KM, et al. Continuous monitoring of receptor-mediated changes in the metabolic rates of living cells. Proc Natl Acad Sci U S A 1990;87:4007–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Owicki JC, Bousse LJ, Hafeman DG, et al. The light-addressable potentiometric sensor: Principles and biological applications. Annu Rev Biophys Biomol Struct 1994;23:87–113.

    Article  CAS  PubMed  Google Scholar 

  22. Parce JW, Owicki JC, Kercso KM. Biosensors for directly measuring cell affecting agents. Ann Biol Clin (Paris) 1990;48:639–41.

    CAS  Google Scholar 

  23. Pitchford S, De Moor K, Glaeser BS. Nerve growth factor stimulates rapid metabolic responses in PC 12 cells. Am J Physiol 1995;268:C936–43.

    Article  CAS  PubMed  Google Scholar 

  24. Watson RE, Wiegand SJ, Clough RW, Hoffman GE. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 1986;7:155–9.

    Article  CAS  PubMed  Google Scholar 

  25. Hoffman GE, McDonald TJ, Figueroa JP, Nathanielsz PW. Neuropeptide cells and fibers in the hypothalamus and pituitary of the fetal Sheep: Comparison of oxytocin and arginine vasopressin. Neuroendocrinology 1989;50:633–43.

    Article  CAS  PubMed  Google Scholar 

  26. Bornstein SR, Ehrhart-Bornstein M, Scherbaum WA, Pfeiffer EF, Holst JJ. Effects of splanchnic nerve stimulation on the adrenal cortex may be mediated by chromaffin cells in a paracrine manner. Endocrinology 1990;127:900–6.

    Article  CAS  PubMed  Google Scholar 

  27. Walker SW, Lightly ERL, Milner SW, Williams BC. Catecholamine stimulation of Cortisol secretion by 3-day primary cultures of purified fasciculata/reticularis cells isolated from bovine adrenal cortex. Mol Cell Endocrinol 1988;57:139–47.

    Article  CAS  PubMed  Google Scholar 

  28. Pohorecky LA, Wurtman RJ. Adrenocortical control of epinephrine synthesis. Pharmacol Rev 1971;23:1–35.

    CAS  PubMed  Google Scholar 

  29. Walker SW, Lightly ER, Clyne C, Williams BC, Bird IM. Adrenergic and cholinergic regulation of Cortisol secretion from the zona fasciculata/reticularis of bovine adrenal cortex. Endocr Res 1991;17:237–65.

    Article  CAS  PubMed  Google Scholar 

  30. Haidan A, Bornstein SR, Glasow A, et al. Basal steroidogenic activity of adrenocortical cells is increased 10-fold by coculture with chromaffin cells. Endocrinology 1998;139:772–80.

    Article  CAS  PubMed  Google Scholar 

  31. Bornstein SR, Gonzalez-Hernandez JA, Ehrhart-Bornstein M, Alder G, Scherbaum WA. Intimate contact of chromaffin and cortical cells within the human adrenal gland forms the cellular basis for important intraadrenal interactions. J Clin Endocrinol Metab 1994;78:225–32.

    CAS  PubMed  Google Scholar 

  32. Bornstein SR, Ehrhart-Bornstein M. Ultrastructural evidence for a paracrine regulation of the rat adrenal cortex mediated by the local release of catecholamines from chromaffin cells. Endocrinology 1992;131:3126–8.

    Article  CAS  PubMed  Google Scholar 

  33. Gallo-Payet N, Pothier P, Isler H. On the presence of chromaffin cells in the adrenal cortex: Their possible role in adrenocortical function. Biochem Cell Biol 1987;65:588–92.

    Article  CAS  PubMed  Google Scholar 

  34. Cheung CY. Enhancement of adrenomedullary catecholamine release by adrenal cortex in fetus. Am J Physiol 1984;247:693–7.

    CAS  PubMed  Google Scholar 

  35. Graham ADM, Cheung L, Cheung CY. Catecholamine secretion from the adrenal medulla of the fetus, regulation by hormones. J Dev Physiol 1986;8:227–35.

    CAS  PubMed  Google Scholar 

  36. Hinson JP. Paracrine control of adrenocortical function: A new role for the medulla? J Endocrinol 1990;124:7–9.

    Article  CAS  PubMed  Google Scholar 

  37. Pohorecky LA, Wurtman RJ. Adrenocortical control of epinephrine synthesis. Pharmacological reviews 1971;23:1–35.

    CAS  PubMed  Google Scholar 

  38. Wintour EM, Brown EH, Denton DA, et al. The ontogeny and regulation of corticosteroid secretion by the ovine foetal adrenal. Acta Endocrinol 1975;79:301–16.

    Article  CAS  Google Scholar 

  39. Durand P. ACTH receptor levels in lamb adrenals at late gestation and early neonatal stages. Biol Reprod 1979;20:837–45.

    Article  CAS  PubMed  Google Scholar 

  40. Coulter CL, Myers DA, Nathanielsz PW, Bird IM. Ontogeny of angiotensin II type 1 receptor and cytochrome P450(cl1) in the sheep adrenal gland. Biol Reprod 2000;62:714–9.

    Article  CAS  PubMed  Google Scholar 

  41. Bird IM, Lightly ER, Nicol M, Williams BC, Walker SW. Dopaminergic stimulation of Cortisol secretion from bovine zfr cells occurs through nonspecific stimulation of adrenergic beta-receptors. Endocr Res 1998;24:769–72.

    Article  CAS  PubMed  Google Scholar 

  42. Roebuck MM, Jones CT, Holland D, Silman R. In vitro effects of high molecular weight forms of ACTH on the fetal sheep adrenal. Nature 1980;284:616–8.

    Article  CAS  PubMed  Google Scholar 

  43. Norman LJ, Lye SJ, Wlodek ME, Challis JRG. Changes in pituitary responses to synthetic ovine corticotrophin releasing factor in fetal sheep. Can J Physiol Pharmacol 1985;63:1398–403.

    Article  CAS  PubMed  Google Scholar 

  44. Krozowski Z. The 11 beta-hydroxysteroid dehydrogenases: Functions and physiological effects. Mol Cell Endocrinol 1999;151:121–7.

    Article  CAS  PubMed  Google Scholar 

  45. Berghorn KA, Li C, Nathanielsz PW, McDonald TJ. VIP innervation: Sharp contrast in fetal sheep and baboon adrenal glands suggests differences in developmental regulation. Brain Res 2000;877:271–80.

    Article  CAS  PubMed  Google Scholar 

  46. Ma XH, Wu WX, Nathanielsz P. Characterization of mRNA for prostaglandin (PG) E2 receptor subtypes in ovine fetal hippocampus (HC), hypothalamus (HT), pituitary (P) gland and adrenal. J Soc Gynecol Investig 1998;5:154A.

    Article  Google Scholar 

  47. Koyama Y, Kitayama S, Dohi T, Tsujimoto A. Evidence that prostaglandins activate calcium channels to enhance basal and stimulation-evoked catecholamine release from bovine adrenal chromaffin cells in culture. Biochem Pharmacol 1988;37:1725–30.

    Article  CAS  PubMed  Google Scholar 

  48. Gutman Y, Boonyaviroj P. Mechanism of PGE inhibition of catecholamine release from adrenal medulla. Eur J Pharmacol 1979;55:129–36.

    Article  CAS  PubMed  Google Scholar 

  49. Karaplis AC, Funk CD, Powell WS. Binding of prostaglandin E2 to cultured bovine adrenal chromaffin cells and its effect on catecholamine secretion. Biochim Biophys Acta 1989;1010:369–76.

    Article  CAS  PubMed  Google Scholar 

  50. Liggins GC. The role of Cortisol in preparing the fetus for birth. Reprod Fertil Dev 1994;6:141–50.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory for Pregnancy and Newborn Research, College of Veterinary Medicine, Dept. Biomedical Sciences, Box 16, Cornell University, 14853-6401, Ithaca, New York, USA

    E. Zambrano PhD, P. W. Nathanielsz MD, PhD & T. J. McDonald PhD

  2. Departamento de Biología de la Reproduccióon, Instituto Nacional de la Nutrición Salvador Zubirán, México D.F., México

    E. Zambrano PhD, P. W. Nathanielsz MD, PhD & T. J. McDonald PhD

Authors
  1. E. Zambrano PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. W. Nathanielsz MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. J. McDonald PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. J. McDonald PhD.

Additional information

Supported by National Institutes of Health grant HD 21350, DK51234-02 and Consejo Nacional de Ciencia y Tecnología (CONACyT) México Fellowship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zambrano, E., Nathanielsz, P.W. & McDonald, T.J. Prenatal and Postnatal Ovine Adrenal Cell responses to Prostaglandin E2. Reprod. Sci. 8, 149–157 (2001). https://doi.org/10.1177/107155760100800305

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/107155760100800305

Key words

Search

Navigation