Sex-specific effects of early neonatal progesterone treatment on dopamine and serotonin metabolism in rat striatum and frontal cortex

Life Sciences

Volumn 87, Issue 23-26, 2010, Pages 738-742

  Muneoka, Katsumasa ^a,c   Kuwagata, Makiko ^b   Ogawa, Tetsuo ^a   Shioda, Seiji ^a  

^a SHOWA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b HATANO RESEARCH INSTITUTE   (Japan)

^c CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Dopamine; Neonatal period; Neurosteroids; Progesterone; Serotonin; Sexual dimorphism

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; DOPAMINE; MONOAMINE; NEUROSTEROID; PREGNENOLONE; PROGESTERONE; SEROTONIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN TISSUE; CASTRATION; CONTROLLED STUDY; CORPUS STRIATUM; DEVELOPMENTAL STAGE; DOPAMINE METABOLISM; DOPAMINERGIC ACTIVITY; EARLY INTERVENTION; FEMALE; FRONTAL CORTEX; MALE; METABOLITE; MONOAMINE METABOLISM; NEWBORN; NEWBORN CARE; NEWBORN PERIOD; NONHUMAN; PERINATAL PERIOD; PREPUBERTY; RAT; SEROTONIN METABOLISM; SEROTONINERGIC SYSTEM; SEX DIFFERENCE; SHAM PROCEDURE; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; CORPUS STRIATUM; DOPAMINE; FEMALE; FRONTAL LOBE; HYDROXYINDOLEACETIC ACID; MALE; ORCHIECTOMY; PREGNENOLONE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SEX CHARACTERISTICS; TIME FACTORS;

RATTUS; RODENTIA;

EID: 78649450880     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2010.10.016     Document Type: Article

References (39)

1. Anderson L.I., Leipheimer R.E., Dluzen D.E. Effects of neonatal and prepubertal hormonal manipulations upon estrogen neuroprotection of the nigrostriatal dopaminergic system within female and male mice. Neuroscience 2005, 130:369-382.
2. Baulieu E., Schumacher M. Progesterone as a neuroactive neurosteroid, with special reference to the effect of progesterone on myelination. Steroids 2000, 65(10-11):605-612.
3. Bishop C.V., Filtz T., Zhang Y., Slayden O., Stormshak F. Progesterone suppresses an oxytocin-stimulated signal pathway in COS-7 cells transfected with the oxytocin receptor. Steroids 2008, 73(14):1367-1374.
4. Brake W.G., Zhang T.Y., Diorio J., Meaney M.J., Gratton A. Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur J Neurosci 2004, 19(7):1863-1874.
5. Concas A., Follesa P., Barbaccia M.L., Purdy R.H., Biggio G. Physiological modulation of GABAA receptor plasticity by progesterone metabolites. Eur J Pharmacol 1999, 375:225-235.
6. Gizerian S.S., Moy S.S., Lieberman J.A., Grobin A.C. Neonatal neurosteroid administration results in development-specific alterations in prepulse inhibition and locomotor activity. Neurosteroids alter prepulse inhibition and locomotor activity. Psychopharmacology (Berlin) 2006, 186:334-342.
7. Grobin A.C., Heenan E.J., Lieberman J.A., Morrow A.L. Perinatal neurosteroid levels influence GABAergic interneuron localization in adult rat prefrontal cortex. J Neurosci 2003, 23:1832-1839.
8. Grobin A.C., Morrow A.L. 3Alpha-hydroxy-5alpha-pregnan-20-one levels and GABA(A) receptor-mediated 36Cl(-) flux across development in rat cerebral cortex. Brain Res Dev Brain Res 2001, 131(1-2):31-39.
9. Jahagirdar V., Wagner C.K. Ontogeny of progesterone receptor expression in the subplate of fetal and neonatal rat cortex. Cereb Cortex 2010, 20(5):1046-1052.
10. Jorge J.C., González L., Fortis A., Cruz N.D. Sex-specific modulation of anxiety and locomotion after neonatal exposure to pregnenolone sulfate. Physiol Behav 2005, 83:779-786.
11. Kaur P., Jodhka P.K., Underwood W.A., Bowles C.A., de Fiebre N.C., de Fiebre C.M., et al. Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants. J Neurosci Res 2007, 85(11):2441-2449.
12. Knoll J., Miklya I., Knoll B., Dallo J. Sexual hormones terminate in the rat: the significantly enhanced catecholaminergic/serotoninergic tone in the brain characteristic to the post-weaning period. Life Sci 2000, 67(7):765-773.
13. Kuwagata M., Ogawa T., Shioda S., Nagata T. Observation of fetal brain in a rat valproate-induced autism model: a developmental neurotoxicity study. Int J Dev Neurosci 2009, 27(4):399-405.
14. Laborie C., Dutriez-Casteloot I., Montel V., Dickes-Coopman A., Lesage J., Vieau D. Prenatal morphine exposure affects sympathoadrenal axis activity and serotonin metabolism in adult male rats both under basal conditions and after an ether inhalation stress. Neurosci Lett 2005, 381(3):211-216.
15. Morita K., Gotohda T., Arimochi H., Lee M.S., Her S. Histone deacetylase inhibitors promote neurosteroid-mediated cell differentiation and enhance serotonin-stimulated brain-derived neurotrophic factor gene expression in rat C6 glioma cells. J Neurosci Res 2009, 87(11):2608-2614.
16. Muneoka K., Iwata M., Shirayama Y. Altered levels of synapsin I, dopamine transporter, dynorphin A, and neuropeptide Y in the nucleus accumbens and striatum at post-puberty in rats treated neonatally with pregnenolone or DHEA. Int J Dev Neurosci 2009, 27(6):575-581.
17. Muneoka K., Kuwagata M., Shirayama Y., Ogawa T., Shioda S. Biphasic effects of neonatal allopregnanolone on striatal dopamine metabolism. NeuroReport 2009, 20(9):860-863.
18. Muneoka K., Mikuni M., Ogawa T., Kitera K., Kamei K., Takigawa M., et al. Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am J Physiol 1997, 273(5 Pt 2):R1669-1675.
19. Muneoka K., Ogawa T., Kamei K., Muraoka S., Tomiyoshi R., Mimura Y., et al. Prenatal nicotine exposure affects the development of the central serotonergic system as well as the dopaminergic system in rat offspring: involvement of route of drug administrations. Brain Res Dev Brain Res 1997, 102(1):117-126.
20. 1 receptor, dopamine metabolites in the fronto-parietal cortex and behavioral response in the open field. Brain Res 2002, 956:332-338.
21. Muneoka K.T., Takigawa M. A neuroactive steroid, pregnenolone, alters the striatal dopaminergic tone before and after puberty. Neuroendocrinology 2002, 75:288-295.
22. Ness A., Dias T., Damus K., Burd I., Berghella V. Impact of the recent randomized trials on the use of progesterone to prevent preterm birth: a 2005 follow-up survey. Am J Obstet Gynecol 2006, 195(4):1174-1179.
23. Ogawa T., Mikuni M., Kuroda Y., Muneoka K., Mori K.J., Takahashi K. Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open field-induced behaviors. Pharmacol Biochem Behav 1994, 49(4):961-967.
24. Panagiotaropoulos T., Pondiki S., Papaioannou A., Alikaridis F., Stamatakis A., Gerozissis K., et al. Neonatal handling and gender modulate brain monoamines and plasma corticosterone levels following repeated stressors in adulthood. Neuroendocrinology 2004, 80(3):181-191.
25. Peters D.A. Prenatal stress: effect on development of rat brain serotonergic neurons. Pharmacol Biochem Behav 1986, 24(5):1377-1382.
26. Pomata P.E., Colman-Lerner A.A., Barañao J.L., Fiszman M.L. In vivo evidences of early neurosteroid synthesis in the developing rat central nervous system and placenta. Brain Res Dev Brain Res 2000, 120:83-86.
27. Russell J.A., Brunton P.J. Neuroactive steroids attenuate oxytocin stress responses in late pregnancy. Neuroscience 2006, 138(3):879-889.
28. 7 receptor in neonatally pregnenolone-treated rats. NeuroReport 2001, 12:3773-3776.
29. Slotkin T.A., Barnes G.A., McCook E.C., Seidler F.J. Programming of brainstem serotonin transporter development by prenatal glucocorticoids. Brain Res Dev Brain Res 1996, 93(1-2):155-161.
30. Slotkin T.A., Kreider M.L., Tate C.A., Seidler F.J. Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems. Neuropsychopharmacology 2006, 31(5):904-911.
31. Trotter A., Bokelmann B., Sorgo W., Bechinger-Kornhuber D., Heinemann H., Schmucker G., et al. Follow-up examination at the age of 15months of extremely preterm infants after postnatal estradiol and progesterone replacement. J Clin Endocrinol Metab 2001, 86(2):601-603.
32. Trotter A., Maier L., Kohn T., Bohm W., Pohlandt F. Growth of the uterus and mammary glands and vaginal cytologic features in extremely premature infants with postnatal replacement of estradiol and progesterone. Am J Obstet Gynecol 2002, 186(2):184-188.
33. Trotter A., Maier L., Kron M., Pohlandt F. Effect of oestradiol and progesterone replacement on bronchopulmonary dysplasia in extremely preterm infants. Fetal and Neonatal Edition 2007, vol. 92(2):F94-98.
34. Van den Hove D.L., Lauder J.M., Scheepens A., Prickaerts J., Blanco C.E., Steinbusch H.W. Prenatal stress in the rat alters 5-HT1A receptor binding in the ventral hippocampus. Brain Res 2006, 1090(1):29-34.
35. Wagner C.K. Progesterone receptors and neural development: a gap between bench and bedside?. Endocrinology 2008, 149(6):2743-2749.
36. Wakshlak A., Weinstock M. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 1990, 48(2):289-292.
37. Ward I.L., Weisz J. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology 1984, 114(5):1635-1644.
38. Zimmerberg B., Blaskey L.G. Prenatal stress effects are partially ameliorated by prenatal administration of the neurosteroid allopregnanolone. Pharmacol Biochem Behav 1998, 59(4):819-827.
39. Zimmerberg B., Kajunski E.W. Sexually dimorphic effects of postnatal allopregnanolone on the development of anxiety behavior after early deprivation. Pharmacol Biochem Behav 2004, 78:465-471.