Neonatal exposure to estradiol in rats influences neuroactive steroid concentrations, GABAA receptor expression, and behavioral sensitivity to anxiolytic drugs

Journal of Neurochemistry

Volumn 113, Issue 5, 2010, Pages 1285-1295

  Calza, Arianna ^a   Sogliano, Cristiana ^a   Santoru, Francesca ^a   Marra, Carla ^a   Angioni, Maria Maddalena ^a   Mostallino, Maria Cristina ^b   Biggio, Giovanni ^a,b   Concas, Alessandra ^a,b  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b CNR   (Italy)

Author keywords

Allopregnanolone; Cerebral cortex; Diazepam; Estradiol; GABAA receptor; Neuroactive steroid

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; DIAZEPAM; ESTRADIOL; ESTRADIOL BENZOATE; PRASTERONE; PROGESTERONE; TETRAHYDRODEOXYCORTICOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; GABAERGIC TRANSMISSION; HORMONE DETERMINATION; LOCOMOTION; MAZE TEST; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TRANQUILIZING ACTIVITY;

ANIMALS; ANIMALS, NEWBORN; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; CEREBRAL CORTEX; DIAZEPAM; ESTRADIOL; FEMALE; IMMUNOBLOTTING; MOTOR ACTIVITY; NEUROTRANSMITTER AGENTS; PREGNANCY; PREGNANOLONE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; STEROIDS;

RATTUS;

EID: 77951891267     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06696.x     Document Type: Article

References (55)

1. Amateau S. K., Alt J. J., Stamps C. L. McCarthy M. M. (2004) Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145, 2906 2917.
2. Barbaccia M. L., Roscetti G., Bolacchi F., Concas A., Mostallino M. C., Purdy R. H. Biggio G. (1996) Stress-induced increase in brain neuroactive steroids: antagonism by abecarnil. Pharmacol. Biochem. Behav. 54, 205 210. (Pubitemid 26146671)
3. Barbaccia M. L., Affricano D., Purdy R. H., Maciocco E., Spiga F. Biggio G. (2001) Clozapine, but not haloperidol, increases brain concentrations of neuroactive steroids in the rat. Neuropsychopharmacology 25, 489 497. (Pubitemid 32830953)
4. Biggio G., Concas A., Follesa P., Sanna E. Serra M. (2007) Stress, ethanol, and neuroactive steroids. Pharmacol. Ther. 116, 140 171. (Pubitemid 47391033)
5. Bitran D., Hilvers R. J. Kellogg C. K. (1991) Ovarian endocrine status modulates the anxiolytic potency of diazepam and the efficacy of γ-aminobutyric acid-benzodiazepine receptor-mediated chloride ion transport. Behav. Neurosci. 105, 653 662.
6. Chen G., Trombley P. Q. van den Pol A. N. (1996) Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol.(Lond.) 494, 451 464. (Pubitemid 26318783)
7. Concas A., Mostallino M. C., Porcu P., Follesa P., Barbaccia M. L., Trabucchi M., Purdy R. H., Grisenti P. Biggio G. (1998) Role of brain allopregnanolone in the plasticity of γ-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc. Natl Acad. Sci. USA 95, 13284 13289. (Pubitemid 28509563)
8. Concas A., Porcu P., Sogliano C., Serra M., Purdy R. H. Biggio G. (2000) Caffeine-induced increases in the brain and plasma concentrations of neuroactive steroids in the rat. Pharmacol. Biochem. Behav. 66, 39 45. (Pubitemid 30317516)
9. A-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat. Neurosci. 2, 833 839. (Pubitemid 30491177)
10. A receptor subunit mRNA expression by hypothalamic magnocellular neurons in the adult rat. J. Neurosci. 16, 4872 4880. (Pubitemid 26269649)
11. Fernández-Guasti A. Picazo O. (1997) Anxiolytic actions of diazepam, but not of buspirone, are influenced by gender and the endocrine stage. Behav. Brain Res. 88, 213 218. (Pubitemid 27496317)
12. Fernández-Guasti A. Picazo O. (1999) Sexual differentiation modifies the allopregnanolone anxiolytic actions in rats. Psychoneuroendocrinology 24, 251 267. (Pubitemid 29118374)
13. Finn D. A., Roberts A. J., Lotrich F. Gallaher E. J. (1997) Genetic differences in behavioral sensitivity to a neuroactive steroid. J. Pharmacol. Exp. Ther. 280, 820 828. (Pubitemid 27171345)
14. Foecking E. M., Szabo M., Schwartz N. B. Levine J. E. (2005) Neuroendocrine consequences of prenatal androgen exposure in the female rat: absence of luteinizing hormone surges, suppression of progesterone receptor gene expression, and acceleration of the gonadotropin-releasing hormone pulse generator. Biol. Reprod. 72, 1475 1483. (Pubitemid 40696090)
15. Foecking E. M., McDevitt M. A., Acosta-Martínez M., Horton T. H. Levine J. E. (2008) Neuroendocrine consequences of androgen excess in female rodents. Horm. Behav. 53, 673 692.
16. A receptor complex during pregnancy and after delivery in the rat brain. Eur. J. Neurosci. 10, 2905 2912. (Pubitemid 29073963)
17. A receptor expression and function during progesterone treatment and withdrawal. Mol. Pharmacol. 57, 1262 1270. (Pubitemid 30354400)
18. A receptor plasticity during long-term exposure to and withdrawal from progesterone. Brain Res. Brain Res. Rev. 37, 81 90. (Pubitemid 34020722)
19. A receptor γ2 subunit gene expression induced by long-term administration of oral contraceptives in rats. Neuropharmacology 42, 325 336. (Pubitemid 34230485)
20. A receptor subunits: plasticity of expression during the estrous cycle. Neuroscience 136, 457 466.
21. - flux across development in rat cerebral cortex. Brain Res. Dev. Brain Res. 131, 31 39.
22. Grobin A. C., Heenan E. J., Lieberman J. A. Morrow A. L. (2003) Perinatal neurosteroid levels influence GABAergic interneuron localization in adult rat prefrontal cortex. J. Neurosci. 23, 1832 1839.
23. A receptor in the amygdala after progesterone withdrawal. Eur. J. Neurosci. 17, 641 648. (Pubitemid 36255901)
24. Günther U., Benson J., Benke D. et al. (1995) Benzodiazepine- insensitive mice generated by targeted disruption of the γ2 subunit gene of γ-aminobutyric acid type A receptors. Proc. Natl Acad. Sci. USA 92, 7749 7753.
25. Handa R. J., Nass T. E. Gorski R. A. (1985) Proestrous hormonal changes preceding the onset of ovulatory failure in lightly androgenized female rats. Biol. Reprod. 32, 232 240.
26. Korenbrot C. C., Paup D. C. Gorski R. A. (1975) Effects of testosterone propionate or dihydrotestosterone propionate on plasma FSH and LH levels in neonatal rats and on sexual differentiation of the brain. Endocrinology 97, 709 717.
27. Laconi M. R., Casteller G., Gargiulo P. A., Bregonzio C. Cabrera R. J. (2001) The anxiolytic effect of allopregnanolone is associated with gonadal hormonal status in female rats. Eur. J. Pharmacol. 417, 111 116. (Pubitemid 32299873)
28. Löw K., Crestani F., Keist R. et al. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290, 131 134.
29. A receptors: relevance to the ovarian cycle and stress. J. Neurosci. 27, 2155 2162. (Pubitemid 46340948)
30. AR plasticity during pregnancy: relevance to postpartum depression. Neuron 59, 207 213. (Pubitemid 352033688)
31. A receptor. Mechanism of action and physiological significance. Prog. Neurobiol. 38, 379 395.
32. McCarthy M. M., Schwarz J. M., Wright C. L. Dean S. L. (2008) Mechanisms mediating oestradiol modulation of the developing brain. J. Neuroendocrinol. 20, 777 783.
33. McEwen B. S. (1983) Gonadal steroid influences on brain development and sexual differentiation. Int. Rev. Physiol. 27, 99 145.
34. Mellon S. H. Griffin L. D. (2002) Neurosteroids: biochemistry and clinical significance. Trends Endocrinol. Metab. 13, 35 43.
35. Mihalek R. M., Banerjee P. K., Korpi E. R. et al. (1999) Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor subunit knockout mice. Proc. Natl Acad. Sci. USA 96, 12905 12910.
36. Nuñez J. L., Bambrick L. L., Krueger B. K. McCarthy M. M. (2005) Prolongation and enhancement of γ-aminobutyric acid receptor mediated excitation by chronic treatment with estradiol in developing rat hippocampal neurons. Eur. J. Neurosci. 21, 3251 3261.
37. A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141 148.
38. Perrot-Sinal T. S., Davis A. M., Gregerson K. A., Kao J. P. McCarthy M. M. (2001) Estradiol enhances excitatory γ-aminobutyric acid-mediated calcium signaling in neonatal hypothalamic neurons. Endocrinology 142, 2238 2243. (Pubitemid 32473076)
39. Porcu P., Sogliano C., Cinus M., Purdy R. H., Biggio G. Concas A. (2003) Nicotine-induced changes in cerebrocortical neuroactive steroids and plasma corticosterone concentrations in the rat. Pharmacol. Biochem. Behav. 74, 683 690. (Pubitemid 36126547)
40. A receptor subunit for benzodiazepine pharmacology. Nature 338, 582 585. (Pubitemid 19102309)
41. Purdy R. H., Morrow A. L., Blinn J. R. Paul S. M. (1990) Synthesis, metabolism and pharmacological activity of 3α-hydroxy-steroids which potentiate GABA-receptor-mediated chloride ion uptake in rat cerebral cortical synaptoneurosomes. J. Med. Chem. 33, 1572 1581.
42. Pytel M., Wójtowicz T., Mercik K., Sarto-Jackson I., Sieghart W., Ikonomidou C. Mozrzymas J. W. (2007) 17β-Estradiol modulates GABAergic synaptic transmission and tonic currents during development in vitro. Neuropharmacology 52, 1342 1353. (Pubitemid 46601530)
43. Rapkin A. J., Morgan M., Sogliano C., Biggio G. Concas A. (2006) Decreased neuroactive steroids induced by combined oral contraceptive pills are not associated with mood changes. Fertil. Steril. 85, 1371 1378.
44. Robinson J. (2006) Prenatal programming of the female reproductive neuroendocrine system by androgens. Reproduction 132, 539 547. (Pubitemid 44660528)
45. Rodriguez P., Fernández-Galaz C. Tejero A. (1993) Controlled neonatal exposure to estrogens: a suitable tool for reproductive aging studies in the female rat. Biol. Reprod. 49, 387 392. (Pubitemid 23210262)
46. A receptor subtypes. Nature 401, 796 800. (Pubitemid 129515840)
47. A receptor activity in rat hippocampus. J. Neurosci. 24, 6521 6530. (Pubitemid 38971700)
48. A receptors in the rat hippocampus during pregnancy and after delivery. J. Neurosci. 29, 1755 1765.
49. Savić M. M., Milinković M. M., Rallapalli S., Clayton Sr. T., Joksimović S., Van Linn M. Cook J. M. (2009) The differential role of alpha1- and alpha5-containing GABA(A) receptors in mediating diazepam effects on spontaneous locomotor activity and water-maze learning and memory in rats. Int. J. Neuropsychopharmacol. 12, 1179 1193.
50. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392, 926 930. (Pubitemid 28232064)
51. A receptors: focus on the α4 and subunits. Pharmacol. Ther. 116, 58 76. (Pubitemid 47391031)
52. Solum D. T. Handa R. J. (2002) Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus. J. Neurosci. 22, 2650 2659.
53. Ströhle A., Pasini A., Romeo E., Hermann B., Spalletta G., di Michele F., Holsboer F. Rupprecht R. (2000) Fluoxetine decreases concentrations of 3α,5α-tetrahydrodeoxycorticosterone (THDOC) in major depression. J. Psychiatr. Res. 34, 183 186. (Pubitemid 30364917)
54. Wójtowicz T., Lebida K. Mozrzymas J. W. (2008) 17β-Estradiol affects GABAergic transmission in developing hippocampus. Brain Res. 1241, 7 17.
55. Yu R., Follesa P. Ticku M. K. (1996) Down-regulation of the GABA receptor subunits mRNA levels in mammalian cultured cortical neurons following chronic neurosteroid treatment. Brain Res. Mol. Brain Res. 41, 163 168. (Pubitemid 26288157)