Stress in pregnancy activates neurosteroid production in the fetal brain

Neuroendocrinology

Volumn 84, Issue 4, 2007, Pages 264-274

  Hirst, Jonathan J ^a   Yawno, Tamara ^b   Nguyen, Phuong ^c   Walker, David W ^b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c ALFRED HOSPITAL   (Australia)

Author keywords

Allopregnanolone; Fetus; Neuroprotection; Placenta; Placental steroidogenesis; Pregnane steroids; Progesterone

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID RECEPTOR; NEUROSTEROID;

BRAIN; BRAIN HYPOXIA; CONFERENCE PAPER; FETUS; FETUS BRAIN; GABAERGIC SYSTEM; GESTATIONAL AGE; HORMONE RECEPTOR INTERACTION; HORMONE RELEASE; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; ONTOGENY; PREGNANCY; PRIORITY JOURNAL; RECEPTOR DENSITY; RECEPTOR INTRINSIC ACTIVITY; RECEPTOR OCCUPANCY; SHEEP; STEROIDOGENESIS; STRESS;

ANIMALS; ASPHYXIA; BRAIN; FEMALE; FETUS; HYPOXIA, BRAIN; PREGNANCY; PREGNANOLONE; PRENATAL INJURIES; RECEPTORS, GABA-A; STRESS, PSYCHOLOGICAL;

EID: 33847789469     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000097990     Document Type: Conference Paper

References (68)

1. Corpechot C, Young J, Calvel M, Wehrey C, Veltz JN, Touyer G, Mouren M, Prasad VV, Banner C, Sjovall J, et al: Neurosteroids: 3-alpha-hydroxy-5 alpha-pregnan-20-one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology 1993;133:1003-1009.
2. Mellon SH, Griffin LD, Compagnone NA: Biosynthesis and action of neurosteroids. Brain Res Brain Res Rev 2001;37:3-12.
3. Dolling M, Seamark RF: Progestagen metabolites in fetal sheep plasma: the effect of fetal nephrectomy. J Dev Physiol 1979;1:399-413.
4. Bernardi F, Pluchino N, Begliuomini S, Lenzi E, Palumbo M, Luisi M, Genazzani AR: Disadaptive disorders in women: allopregnanolone, a sensitive steroid. Gynecol Endocrinol 2004;19:344-353.
5. Nguyen PN, Billiards SS, Walker DW, Hirst JJ: Changes in 5-alpha-pregnane steroids and neurosteroidogenic enzyme expression in the perinatal sheep. Pediatr Res 2003;53:956-964.
6. Billiards SS, Walker DW, Canny BJ, Hirst JJ: Endotoxin increases sleep and brain allopregnanolone concentrations in newborn lambs. Pediatr Res 2002;52:892-899.
7. Baulieu EE: Neurosteroids: a new function in the brain. Biol Cell 1991;71:3-10.
8. Lapchak PA: The neuroactive steroid 3-alpha-ol-5-beta-pregnan-20-one hemisuccinate, a selective NMDA receptor antagonist, improves behavioral performance following spinal cord ischemia. Brain Res 2004;997:152-158.
9. Nicol MB, Hirst JJ, Walker DW: Effects of pregnanolone on behavioural parameters and the responses to GABA A receptor antagonists in the late gestation fetal sheep. Neuropharmacology 1999;38:49-63.
10. Harrison NL, Majewska MD, Harrington JW, Barker JL: Structure-activity relationships for steroid interaction with the gamma-aminobutyric acid A receptor complex. J Pharmacol Exp Ther 1987;241:346-353.
11. A receptors. Brain Res Brain Res Rev 2001;37:91-97.
12. Harrison NL, Majewska MD, Harrington JW, Barker JL: Structure-activity relationships for steroid interaction with the gamma-aminobutyric acidA receptor complex. J Pharmacol Exp Ther 1987;241:346-353.
13. Seamark RF, Nancarrow CD, Gardiner J: Progesterone metabolism in ovine blood: the formation of 3α-hydroxy-pregn-4-en-20-one and other substances. Steroids 1970;15:589-604.
14. A receptors in fetal, neonatal and adult ovine brain: regionand age-related changes and the effects of allopregnanolone. Neuropharmacology 2000;39:1514-1522.
15. A receptors in the fetal sheep brain. Neuropharmacology 2003;45:461-472.
16. Frye CA, Duncan JE, Basham M, Erskine MS: Behavioral effects of 3-alpha-androstanediol. II. Hypothalamic and preoptic area actions via a GABAergic mechanism. Behav Brain Res 1996;79:119-130.
17. Stromberg J, Backstrom T, Lundgren P: Rapid non-genomic effect of glucocorticoid metabolites and neurosteroids on the gamma-aminobutyric acid-A receptor. Eur J Neurosci 2005;21:2083-2088.
18. Baulieu EE: Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 1998;23:963-987.
19. McKay SA: Mechanisms Involved in the Control of Steroidogenesis during the Oestrous Cycle and Pregnancy in Sheep; PhD thesis Monash University, Melbourne, 1987.
20. Saunders NR, Knott GW, Dziegielewska KM: Barriers in the immature brain. Cell Mol Neurobiol 2000;20:29-40.
21. Robel P, Bourreau E, Corpechot C, Dang DC, Halberg F, Clarke C, Haug M, Schlegel ML, Synguelakis M, Vourch C, et al: Neurosteroids: 3-beta-hydroxy- delta-5 derivatives in rat and monkey brain. J Steroid Biochem 1987;27:649-655.
22. Yan E, Castillo-Melendez M, Nicholls T, Hirst J, Walker D: Cerebrovascular responses in the fetal sheep brain to low-dose endotoxin. Pediatr Res 2004;55:855-863.
23. Herzog AG, Frye CA: Seizure exacerbation associated with inhibition of progesterone metabolism (see comment). Ann Neurol 2003;53:390-391.
24. Soderpalm AH, Lindsey S, Purdy RH, Hauger R, Wit de H: Administration of progesterone produces mild sedative-like effects in men and women. Psychoneuroendocrinology 2004;29:339-354.
25. Gilbert Evans SE, Ross LE, Sellers EM, Purdy RH, Romach MK: 3-Alpha-reduced neuroactive steroids and their precursors during pregnancy and the postpartum period. Gynecol Endocrinol 2005;21:268-279.
26. Dawes GS, Fox HE, Leduc BM, Liggins GC, Richards RT: Respiratory movements and rapid eye movement sleep in the foetal lamb. J Physiol 1972;220:119-143.
27. Crossley KJ, Nicol MB, Hirst JJ, Walker DW, Thorburn GD: Suppression of arousal by progesterone in fetal sheep. Reprod Fertil Dev 1997;9:767-773.
28. Nicol MB, Hirst JJ, Walker DW, Thorburn GD: Effect of alteration of maternal plasma progesterone concentrations on fetal behavioural state during late gestation. J Endocrinol 1997;152:379-386.
29. Nicol MB, Hirst JJ, Walker DW: Effect of finasteride on behavioural arousal and somatosensory evoked potentials in fetal sheep. Neurosci Lett 2001;306:13-16.
30. Brinton RD: The neurosteroid 3α-hydroxy-5α-pregnan-20-one induces cytoarchitectural regression in cultured fetal hippocampal neurons. J Neurosci 1994;14:2763-2774.
31. De Nicola AF, Labombarda F, Gonzalez SL, Gonzalez Deniselle MC, Guennoun R, Schumacher M: Steroid effects on glial cells: detrimental or protective for spinal cord function? Ann N Y Acad Sci 2003;1007:317-328.
32. Schumacher M, Guennoun R, Robert F, Carelli C, Gago N, Ghoumari A, Gonzalez Deniselle MC, Gonzalez SL, Ibanez C, Labombarda F, Coirini H, Baulieu EE, De Nicola AF: Local synthesis and dual actions of progesterone in the nervous system: neuroprotection and myelination. Growth Horm IGF Res 2004;14(Suppl A):S18-S33.
33. Mirmiran M: The function of fetal/neonatal rapid eye movement sleep. Behav Brain Res 1995;69:13-22.
34. Mellon SH, Deschepper CF: Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res 1993;629:283-292.
35. Zwain IH, Yen SS: Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 1999;140:3843-3852.
36. Guennoun R, Fiddes RJ, Gouezou M, Lombes M, Baulieu EE: A key enzyme in the biosynthesis of neurosteroids, 3-beta-hydroxysteroid dehydrogenase/delta 5-delta 4-isomerase (3 beta-HSD), is expressed in rat brain. Brain Res Mol Brain Res 1995;30:287-300.
37. Martini L, Celotti F, Melcangi RC: Testosterone and progesterone metabolism in the central nervous system: cellular localization and mechanism of control of the enzymes involved. Cell Mol Neurobiol 1996;16:271-282.
38. Wallace JM, Aitken RP, Cheyne MA, Humblot P: Pregnancy-specific protein B and progesterone concentrations in relation to nutritional regimen, placental mass and pregnancy outcome in growing adolescent ewes carrying singleton fetuses. J Reprod Fertil 1997;109:53-58.
39. A receptor. Nature Rev Neurosci 2005;6:565-575.
40. Rogawski MA, Reddy DS: Neurosteroids and infantile spasms: the deoxycorticosterone hypothesis. Int Rev Neurobiol 2002;49:199-219.
41. Kishimoto W, Hiroi T, Shiraishi M, Osada M, Imaoka S, Kominami S, Igarashi T, Funae Y: Cytochrome P450 2D catalyze steroid 21-hydroxylation in the brain. Endocrinology 2004;145:699-705.
42. Barbaccia ML, Roscetti G, Bolacchi F, Concas A, Mostallino MC, Purdy RH, Biggio G: Stress-induced increase in brain neuroactive steroids: antagonism by abecarnil. Pharmacol Biochem Behav 1996;54:205-210.
43. Nguyen PN, Yan EB, Castillo-Melendez M, Walker DW, Hirst JJ: Increased allopregnanolone levels in the fetal sheep brain following umbilical cord occlusion. J Physiol 2004;560:593-602.
44. Hirst JJ, Petratos S, Mendis S, Walker DW: Neuroactive steroid synthesis in the ovine fetal and newborn brain (abstract). FASEB Exp Biol 2000:C-493.
45. Petratos S, Hirst JJ, Mendis S, Anikijenko P, Walker DW: Localization of p450scc and 5alpha-reductase type-2 in the cerebellum of fetal and newborn sheep. Brain Res Dev Brain Res 2000;123:81-86.
46. Viscardi RM, Sun CC: Placental lesion multiplicity: risk factor for IUGR and neonatal cranial ultrasound abnormalities. Early Hum Dev 2001;62:1-10.
47. Mallard EC, Rees S, Stringer M, Cock ML, Harding R: Effects of chronic placental insufficiency on brain development in fetal sheep. Pediatr Res 1998;43:262-270.
48. Cock ML, McCrabb GJ, Wlodek ME, Harding R: Effects of prolonged hypoxemia on fetal renal function and amniotic fluid volume in sheep. Am J Obstet Gynecol 1997;176:320-326.
49. Nguyen PN, Billiards SS, Walker DW, Hirst JJ: Changes in 5alpha-pregnane steroids and neurosteroidogenic enzyme expression in fetal sheep with umbilicoplacental embolization. Pediatr Res 2003;54:840-847.
50. Gunn AJ, Quaedackers JS, Guan J, Heineman E, Bennet L: The premature fetus: not as defenseless as we thought, but still paradoxically vulnerable? Dev Neurosci 2001;23:175-179.
51. Dean J, George S, Wassink G, Gunn A, Bennet L: Suppression of post-hypoxic-ischemic EEG transients with dizocilpine is associated with partial striatal protection in the preterm fetal sheep. Neuropharmacology 2005;50:491-503.
52. A receptor in the developing guinea pig cerebral cortex. Brain Res Dev Brain Res 1999;113:21-28.
53. Reddy DS, Rogawski MA: Enhanced anticonvulsant activity of ganaxolone after neurosteroid withdrawal in a rat model of catamenial epilepsy. J Pharmacol Exp Ther 2000;294:909-915.
54. Barbaccia ML, Roscetti G, Trabucchi M, Cuccheddu T, Concas A, Biggio G: Neurosteroids in the brain of handling-habituated and naive rats: effect of CO 2 inhalation. Eur J Pharmacol 1994;261:317-320.
55. Billiards S, Nguyen PN, Canny BJ, Walker DW, Hirst JJ: Hypoxia and endotoxin interact to regulate sleep and allopregnanolone concentrations in the newborn lambs. Biol Neonate 2006;90:258-267.
56. Pratt L, Magness RR, Phernetton T, Hendricks SK, Abbott DH, Bird IM: Repeated use of betamethasone in rabbits: effects of treatment variation on adrenal suppression, pulmonary maturation, and pregnancy outcome (see comment). Am J Obstet Gynecol 1999;180:995-1005.
57. O'Shea TM, Doyle LW: Perinatal glucocorticoid therapy and neurodevelopmental outcome: an epidemiologic perspective. Semin Neonatol 2001;6:293-307.
58. di Michele F, Lekieffre D, Pasini A, Bernardi G, Benavides J, Romeo E: Increased neurosteroid synthesis after brain and spinal cord injury in rats. Neurosci Lett 2000;284:65-68.
59. Frank C, Sagratella S: Neuroprotective effects of allopregnenolone on hippocampal irreversible neurotoxicity in vitro. Prog Neuropsychopharmacol Biol Psychiatry 2000;24:1117-1126.
60. Bucolo C, Drago F: Effects of neurosteroids on ischemia-reperfusion injury in the rat retina: role of sigma1 recognition sites. Eur J Pharmacol 2004;498:111-114.
61. Djebaili M, Guo Q, Pettus EH, Hoffman SW, Stein DG: The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. J Neurotrauma 2005;22:106-118.
62. Gonzalez-Vital MD, Cervera-Gaviria M, Ruelas R, Escobar A, Cervantes M: Progesterone: protective effects on the cat hippocampal neuronal damage due to acute global cerebral ischemia. Arch Med Res 1998;29:117-124.
63. Bender AS, Norenberg MD: Effect of benzodiazepines and neurosteroids on ammonia-induced swelling in cultured astrocytes. J Neurosci Res 1998;54:673-680.
64. Ghoumari AM, Ibanez C, El-Etr M, Leclerc P, Eychenne B, O'Malley BW, Baulieu EE, Schumacher M: Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum. J Neurochem 2003;86:848-859.
65. Ibanez C, Shields SA, El-Etr M, Baulieu EE, Schumacher M, Franklin RJ: Systemic progesterone administration results in a partial reversal of the age-associated decline in CNS remyelination following toxin-induced demyelination in male rats. Neuropathol Appl Neurobiol 2004;30:80-89.
66. Martin LJ, Brambrink A, Koehler RC, Trays tman RJ: Primary sensory and forebrain motor systems in the newborn brain are preferentially damaged by hypoxia-ischemia. J Comp Neurol 1997;377:262-285.
67. Castillo-Melendez M, Chow JA, Walker DW: Lipid peroxidation, caspase-3 immunoreactivity, and pyknosis in late-gestation fetal sheep brain after umbilical cord occlusion. Pediatr Res 2004;55:864-871.
68. Yawno T, Walker D, Yan E, Hirst J: Inhibition of neurosteroid synthesis increases asphyxia-induced brain injury in the late gestation fetal sheep. Soc Gynecol Invest 2006;53:abstract 31.