Progestin receptor is transiently expressed perinatally in neurons of the rat isocortex

Journal of Comparative Neurology

Volumn 512, Issue 1, 2009, Pages 124-139

  Lopez, Verónica ^a   Wagner, Christine K ^b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Development; MAP 2; Neocortex; Pyramidal cells; Steroids; Subplate

Indexed keywords

MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; PROGESTERONE; PROGESTERONE RECEPTOR; BIOLOGICAL MARKER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL SUBPOPULATION; CONTROLLED STUDY; EMBRYO; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; NERVE CELL; NONHUMAN; OLFACTORY CORTEX; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; ANIMAL; CHEMISTRY; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

ANIMALS; BIOLOGICAL MARKERS; CEREBRAL CORTEX; FEMALE; MALE; NEURONS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PROGESTERONE;

EID: 58249086160     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21883     Document Type: Article

References (140)

1. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 17:185-218.
2. Amateau SK, Alt JJ, Stamps CL, McCarthy MM. 2004. Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145:2906-2917.
3. Arnold AP, Gorski RA. 1984. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 7:413-442.
4. Bennett-Clarke CA, Chiaia NL, Crissman RS, Rhoades RW. 1991. The source of the transient serotoninergic input to the developing visual and somatosensory cortices in rat. Neuroscience 43:163-183.
5. Berry M, Rogers AW. 1965. The migration of neuroblasts in the developing cerebral cortex. J Anat 99:691-709.
6. Binder LI, Frankfurter A, Kim H, Caceres A, Payne MR, Rebhun LI. 1984. Heterogeneity of microtubule-associated protein 2 during rat brain development. Proc Natl Acad Sci U S A 81:5613-5617.
7. Bogic L, Gerlach JL, McEwen BS. 1988. The ontogeny of sex differences in estrogen-induced progesterone receptors in rat brain. Endocrinology 122:2735-2741.
8. Caceres A, Binder LI, Payne MR, Bender P, Rebhun L, Steward O. 1984. Differential subcellular localization of tubulin and the microtubule-associated protein MAP2 in brain tissue as revealed by immunocytochemistry with monoclonal hybridoma antibodies. J Neurosci 4:394-410.
9. Carson R, Smith J. 1986. Development and steroidogenic activity of pre-antral follicles in the neonatal rat ovary. J Endocrinol 110:87-92.
10. Christensen K, Estes PA, Onate SA, Beck CA, DeMarzo A, Altmann M, Lieberman BA, St John J, Nordeen SK, Edwards DP. 1991. Characterization and functional properties of the A and B forms of human progesterone receptors synthesized in a baculovirus system. Mol Endocrinol 5:1755-1770.
11. Chung WC, Swaab DF, De Vries GJ. 2000. Apoptosis during sexual differentiation of the bed nucleus of the stria terminalis in the rat brain. J Neurobiol 43:234-243.
12. Clarke S, Innocenti GM. 1986. Organization of immature intrahemispheric connections. J Comp Neurol 251:1-22.
13. Conneely OM, Lydon JP. 2000. Progesterone receptors in reproduction: functional impact of the A and B isoforms. Steroids 65:571-577.
14. Coogan TA, Burkhalter A. 1988. Sequential development of connections between striate and extrastriate visual cortical areas in the rat. J Comp Neurol 278:242-252.
15. Cooke B, Hegstrom CD, Villeneuve LS, Breedlove SM. 1998. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 19:323-362.
16. De Vries GJ, Panzica GC. 2006. Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138:947-955.
17. De Vries GJ, Simerly RB. 2002. Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain. In: Hormones, brain, and behavior. Amsterdam: Elsevier Science. p 137-191.
18. DeCamilli P, Miller PE, Navone F, Theurkauf WE, Vallee RB. 1984. Distribution of microtubule-associated protein 2 in the nervous system of the rat studied by immunofluorescence. Neuroscience 11:817-846.
19. Derksen MJ, Ward NL, Hartle KD, Ivanco TL. 2007. MAP2 and synaptophysin protein expression following motor learning suggests dynamic regulation and distinct alterations coinciding with synaptogenesis. Neurobiol Learn Mem 87:404-415.
20. Devoto SH, Barnstable CJ. 1989. Expression of the growth cone specific epitope CDA 1 and the synaptic vesicle protein SVP38 in the developing mammalian cerebral cortex. J Comp Neurol 290:154-168.
21. DonCarlos LL, Nuñez JL, Huppenbauer C, McAbeel MD, Juraska JM. Androgen receptor expression in the developing male and female rat cerebral cortex. Soc Neurosci Abs 2000 (Abstract).
22. Feldman ML. 1984. Morphology of the neocortical pyramidal neuron. In: Peters A, Jones EG, editors. Cellular components of the cerebral cortex. New York: Plenum Press. p 123-200.
23. Ferreira A, Busciglio J, Caceres A. 1987. An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and Tau in the nervous system of the rat. Brain Res 431:9-31.
24. Finney EM, Stone JR, Shatz CJ. 1998. Major glutamatergic projection from subplate into visual cortex during development. J Comp Neurol 398: 105-118.
25. Forger NG. 2006. Cell death and sexual differentiation of the nervous system. Neuroscience 138:929-938.
26. Friedman WJ, McEwen BS, Toran-Allerand CD, Gerlach JL. 1983. Perinatal development of hypothalamic and cortical estrogen receptors in mouse brain: methodological aspects. Brain Res 313:19-27.
27. Gerlach JL, McEwen BS, Toran-Allerand CD, Friedman WJ. 1983. Perinatal development of estrogen receptors in mouse brain assessed by radio-autography, nuclear isolation and receptor assay. Brain Res 313:7-18.
28. Giangrande PH, McDonnell DP. 1999. The A and B isoforms of the human progesterone receptor: two functionally different transcription factors encoded by a single gene. Recent Prog Horm Res 54:291-313.
29. Giangrande PH, Pollio G, McDonnell DP. 1997. Mapping and characterization of the functional domains responsible for the differential activity of the A and B isoforms of the human progesterone receptor. J Biol Chem 272:32889-32900.
30. Giangrande PH, Kimbrel EA, Edwards DP, McDonnell DP. 2000. The opposing transcriptional activities of the two isoforms of the human progesterone receptor are due to differential cofactor binding. Mol Cell Biol 20:3102-3115.
31. Gollapudi L, Oblinger MM. 1999. Stable transfection of PC12 cells with estrogen receptor (ERalpha): protective effects of estrogen on cell survival after serum deprivation. J Neurosci Res 56:99-108.
32. Gritti I, Mainville L, Mancia M, Jones BE. 1997. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 383:163-177.
33. Grossberg S, Seitz A. 2003. Laminar development of receptive fields, maps and columns in visual cortex: the coordinating role of the subplate. Cereb Cortex 13:852-863.
34. Gu G, Cornea A, Simerly RB. 2003. Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J Comp Neurol 460:542-562.
35. Guo XZ, Su JD, Sun QW, Jiao BH. 2001. Expression of estrogen receptor (ER) -alpha and -beta transcripts in the neonatal and adult rat cerebral cortex, cerebellum, and olfactory bulb. Cell Res 11:321-324.
36. Hagihara K, Hirata S, Osada T, Hirai M, Kato J. 1992a. Distribution of cells containing progesterone receptor mRNA in the female rat di- and telencephalon: an in situ hybridization study. Brain Res Mol Brain Res 14:239-249.
37. Hagihara K, Hirata S, Osada T, Hirai M, Kato J. 1992b. Expression of progesterone receptor in the neonatal rat brain cortex: detection of its mRNA using reverse transcription-polymerase chain reaction. J Steroid Biochem Mol Biol 41:637-640.
38. Hamano K, Takeya T, Iwasaki N, Nakayama J, Ohto T, Okada Y. 1998. A quantitative study of the progress of myelination in the rat central nervous system, using the immunohistochemical method for proteolipid protein. Brain Res Dev Brain Res 108:287-293.
39. Hamre KM, Hyman BT, Goodlett CR, West JR, Van Hoesen GW. 1989. Alz-50 immunoreactivity in the neonatal rat: changes in development and co-distribution with MAP-2 immunoreactivity. Neurosci Lett 98: 264-271.
40. Hanganu IL, Kilb W, Luhmann HJ. 2002. Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci 22:7165-7176.
41. Hayashi S, Hayashi H, Ueda H, Papadopoulos GC. 2001. Analysis of transient expression of estrogen receptor-alpha in newborn rat primary auditory cortex. Horm Behav 40:191-195.
42. Henderson RG, Brown AE, Tobet SA. 1999. Sex differences in cell migration in the preoptic area/anterior hypothalamus of mice. J Neurobiol 41:252-266.
43. Hockfield S, McKay RD. 1985. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
44. Horner CH. 1993. Plasticity of the dendritic spine. Prog Neurobiol 41:281-321.
45. Hovland AR, Powell RL, Takimoto GS, Tung L, Horwitz KB. 1998. An N-terminal inhibitory function, IF, suppresses transcription by the A-isoform but not the B-isoform of human progesterone receptors. J Biol Chem 273:5455-5460.
46. Ibanez MA, Gu G, Simerly RB. 2001. Target-dependent sexual differentiation of a limbic-hypothalamic neural pathway. J Neurosci 21:5652-5659.
47. Ignacio MP, Kimm EJ, Kageyama GH, Yu J, Robertson RT. 1995. Postnatal migration of neurons and formation of laminae in rat cerebral cortex. Anat Embryol (Berl) 191:89-100.
48. Ilenchuk TT, Walters MR. 1987. Rat uterine progesterone receptor analyzed by [3H]R5020 photoaffinity labeling: evidence that the A and subunits are not equimolar. Endocrinology 120:1449-1456.
49. Ismail PM, Li J, DeMayo FJ, O'Malley BW, Lydon JP. 2002. A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol Endocrinol 16:2475-2489.
50. Izant JG, McIntosh JR. 1980. Microtubule-associated proteins: a monoclonal antibody to MAP2 binds to differentiated neurons. Proc Natl Acad Sci U S A 77:4741-4745.
51. Kalman M, Ajtai BM. 2001. A comparison of intermediate filament markers for presumptive astroglia in the developing rat neocortex: immunostaining against nestin reveals more detail, than GFAP or vimentin. Int J Dev Neurosci 19:101-108.
52. Kanold PO, Shatz CJ. 2006. Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 51:627-638.
53. Kanold PO, Kara P, Reid RC, Shatz CJ. 2003. Role of subplate neurons in functional maturation of visual cortical columns. Science 301:521-525.
54. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, Chambon P. 1990. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9:1603-1614.
55. Kato J, Onouchi T. 1981. Progesterone receptors in the cerebral cortex neonatal female rats. Dev Neurosci 4:427-432.
56. Kato J, Onouchi T. 1983. Progestin receptors in female rat brain and hypophysis in the development from fetal to postnatal stages. Endocrinology 113:29-36.
57. Kato J, Onouchi T, Okinaga S, Takamatsu M. 1984. The ontogeny cytosol and nuclear progestin receptors in male rat brain and its male-female differences. J Steroid Biochem 20:147-152.
58. Kato J, Hirata S, Nozawa A, Mouri N. 1993. The ontogeny of gene expression of progestin receptors in the female rat brain. J Steroid Biochem Mol Biol 47:173-182.
59. Kato J, Hirata S, Nozawa A, Yamada-Mouri N. 1994. Gene expression of progesterone receptor isoforms in the rat brain. Horm Behav 28:454-463.
60. Kohchi C, Ukena K, Tsutsui K. 1998. Age- and region-specific expressions of the messenger RNAs encoding for steroidogenic enzymes p450scc, P450c17 and 3beta-HSD in the postnatal rat brain. Brain Res 801:233-238.
61. Kraus WL, Montano MM, Katzenellenbogen BS. 1993. Cloning of the rat progesterone receptor gene 5′-region and identification of two functionally distinct promoters. Mol Endocrinol 7:1603-1616.
62. Kritzer MF. 1998. Perinatal gonadectomy exerts regionally selective, lateralized effects on the density of axons immunoreactive for tyrosine hydroxylase in the cerebral cortex of adult male rats. J Neurosci 18:10735-10748.
63. Lambert JJ, Belelli D, Sheperd SE, Pistis M, Peters JA. 1999. The selective interaction of neurosteroids with the GABAA Receptor. In: Baulieu EE, Robel P, Schumacher M, editors. Neurosteroids: a new regulatory function in the nervous system. Totowa, NJ: Humana Press. p 125-142.
64. Latsari M, Dori I, Antonopoulos J, Chiotelli M, Dinopoulos A. 2002. Noradrenergic innervation of the developing and mature visual and motor cortex of the rat brain: a light and electron microscopic immunocytochemical analysis. J Comp Neurol 445:145-158.
65. Lein ES, Finney EM, McQuillen PS, Shatz CJ. 1999. Subplate neuron ablation alters neurotrophin expression and ocular dominance column formation. Proc Natl Acad Sci U S A 96:13491-13495.
66. Liu XB, Murray KD, Jones EG. 2004. Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 24:8885-8895.
67. MacLusky NJ, McEwen BS. 1980. Progestin receptors in the developing rat brain and pituitary. Brain Res 189:262-268.
68. MacLusky NJ, Lieberburg I, McEwen BS. 1979. The development of estrogen receptor systems in the rat brain: perinatal development. Brain Res 178:129-142.
69. Mani SK, Allen JM, Clark JH, Blaustein JD, O'Malley BW. 1994. Convergent pathways for steroid hormone- and neurotransmitter-induced rat sexual behavior. Science 265:1246-1249.
70. Mani SK, Allen JM, Lydon JP, Mulac-Jericevic B, Blaustein JD, DeMayo FJ, Conneely O, O'Malley BW. 1996. Dopamine requires the unoccupied progesterone receptor to induce sexual behavior in mice. Mol Endocrinol 10:1728-1737.
71. Matus A, Bernhardt R, Hugh-Jones T. 1981. High molecular weight microtubule-associated proteins are preferentially associated with dendritic microtubules in brain. Proc Natl Acad Sci U S A 78:3010-3014.
72. McConnell SK, Ghosh A, Shatz CJ. 1989. Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245:978-982.
73. McConnell SK, Ghosh A, Shatz CJ. 1994. Subplate pioneers and the formation of descending connections from cerebral cortex. J Neurosci 14:1892-1907.
74. McEwen BS. 1981. Neural gonadal steroid actions. Science 211:1303-1311.
75. Mellon SH, Vaudry H. 2001. Biosynthesis of neurosteroids and regulation of their synthesis. Int Rev Neurobiol 46:33-78.
76. Meyer ME, Pornon A, Ji JW, Bocquel MT, Chambon P, Gronemeyer H. 1990. Agonistic and antagonistic activities of RU486 on the functions of the human progesterone receptor. EMBO J 9:3923-3932.
77. Meyer ME, Quirin-Stricker C, Lerouge T, Bocquel MT, Gronemeyer H. 1992. A limiting factor mediates the differential activation of promoters by the human progesterone receptor isoforms. J Biol Chem 267: 10882-10887.
78. Micheva KD, Beaulieu C. 1995. Postnatal development of GABA neurons in the rat somatosensory barrel cortex: a quantitative study. Eur J Neurosci 7:419-430.
79. Miller M. 1988. Development of projection and local circuit neurons in neocortex. In: Development and maturation of the cerebral cortex. New York: Plenum Press.
80. Miller MW, Robertson S. 1993. Prenatal exposure to ethanol alters the postnatal development and transformation of radial glia to astrocytes in the cortex. J Comp Neurol 337:253-266.
81. Minelli A, Edwards RH, Manzoni T, Conti F. 2003. Postnatal development of the glutamate vesicular transporter VGLUT1 in rat cerebral cortex. Brain Res Dev Brain Res 140:309-314.
82. Miranda RC, Toran-Allerand CD. 1992. Developmental expression of estrogen receptor mRNA in the rat cerebral cortex: a nonisotopic in situ hybridization histochemistry study. Cereb Cortex 2:1-15.
83. Mong JA, Roberts RC, Kelly JJ, McCarthy MM. 2001. Gonadal steroids reduce the density of axospinous synapses in the developing rat arcuate nucleus: an electron microscopy analysis. J Comp Neurol 432:259-267.
84. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM. 2000. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289:1751-1754.
85. Muñoz-Cueto JA, Ruiz-Marcos A. 1994. Sexual differences in the numerical density of synaptic profiles of developing rat visual cortex. J Neurobiol 25:50-58.
86. Muñoz-Cueto JA, Garcia-Segura LM, Ruiz-Marcos A. 1990. Developmental sex differences and effect of ovariectomy on the number of cortical pyramidal cell dendritic spines. Brain Res 515:64-68.
87. Muñoz-Cueto JA, Garcia-Segura LM, Ruiz-Marcos A. 1991. Regional sex differences in spine density along the apical shaft of visual cortex pyramids during postnatal development. Brain Res 540:41-47.
88. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714-720.
89. Northcutt RG, Kaas JH. 1995. The emergence and evolution of mammalian neocortex. Trends Neurosci 18:373-379.
90. Nuñez JL, Jurgens HA, Juraska JM. 2000. Androgens reduce cell death in the developing rat visual cortex. Brain Res Dev Brain Res 125:83-88.
91. Nuñez JL, Lauschke DM, Juraska JM. 2001. Cell death in the development of the posterior cortex in male and female rats. J Comp Neurol 436: 32-41.
92. Nuñez JL, Huppenbauer CB, McAbee MD, Juraska JM, DonCarlos LL. 2003. Androgen receptor expression in the developing male and female rat visual and prefrontal cortex. J Neurobiol 56:293-302.
93. Park OK, Mayo KE. 1991. Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol Endocrinol 5:967-978.
94. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
95. Paxinos G, Tork I, Tecott LH, Valentino KL. 1991. Atlas of the developing rat brain. San Diego: Academic Press.
96. Pepe GJ, Rothchild I. 1974. A comparative study of serum progesterone levels in pregnancy and in various types of pseudopregnancy in the rat. Endocrinology 95:275-279.
97. Perez SE, Chen EY, Mufson EJ. 2003. Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res Dev Brain Res 145:117-139.
98. Pfaff DW. 1966. Morphological changes in the brains of adult male rats after neonatal castration. J Endocrinol 36:415-416.
99. Pheonix CH, Goy RW, Gerall A, Young WC. 1959. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369-382.
100. Power RF, Mani SK, Codina J, Conneely OM, O'Malley BW. 1991. Dopaminergic and ligand-independent activation of steroid hormone receptors. Science 254:1636-1639.
101. Quadros PS, Lopez V, De Vries GJ, Chung WC, Wagner CK. 2002a. Progesterone receptors and the sexual differentiation of the medial preoptic nucleus. J Neurobiol 51:24-32.
102. Quadros PS, Pfau JL, Goldstein AY, De Vries GJ, Wagner CK. 2002b. Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology 143: 3727-3739.
103. Quadros PS, Pfau JL, Wagner CK. 2007. Distribution of progesterone receptor immunoreactivity in the fetal and neonatal rat forebrain. J Comp Neurol 504:42-56.
104. Reid SN, Juraska JM. 1992. Sex differences in the gross size of the rat neocortex. J Comp Neurol 321:442-447.
105. Richer JK, Jacobsen BM, Manning NG, Abel MG, Wolf DM, Horwitz KB. 2002. Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J Biol Chem 277:5209-5218.
106. Sakamoto H, Ukena K, Tsutsui K. 2001. Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis. J Neurosci 21:6221-6232.
107. Sakamoto H, Ukena K, Tsutsui K. 2002. Dendritic spine formation in response to progesterone synthesized de novo in the developing Purkinje cell in rats. Neurosci Lett 322:111-115.
108. Sartorius CA, Melville MY, Hovland AR, Tung L, Takimoto GS, Horwitz KB. 1994. A third transactivation function (AF3) of human progesterone receptors located in the unique N-terminal segment of the B-isoform. Mol Endocrinol 8:1347-1360.
109. Schneider W, Ramachandran C, Satyaswaroop PG, Shyamala G. 1991. Murine progesterone receptor exists predominantly as the 83-kilodalton 'A' form. J Steroid Biochem Mol Biol 38:285-291.
110. Scott HC, Sun GY, Zoeller RT. 1998. Prenatal ethanol exposure selectively reduces the mRNA encoding alpha-1 thyroid hormone receptor in fetal rat brain. Alcohol Clin Exp Res 22:2111-2117.
111. Seymoure P, Juraska JM. 1992. Sex differences in cortical thickness and the dendritic tree in the monocular and binocular subfields of the rat visual cortex at weaning age. Brain Res Dev Brain Res 69:185-189.
112. Seymoure P, Juraska JM. 1997. Vernier and grating actuity in adult hooded rats: the influence of sex. Behav Neurosci 111:792-800.
113. Shughrue PJ, Stumpf WE, MacLusky NJ, Zielinski JE, Hochberg RB. 1990. Developmental changes in estrogen receptors in mouse cerebral cortex between birth and postweaning: studied by autoradiography with 11 beta-methoxy-16 alpha-[125I]iodoestradiol. Endocrinology 126: 1112-1124.
114. Shughrue PJ, Stumpf WE, Elger W, Schulze PE, Sar M. 1991a. Progestin receptor cells in mouse cerebral cortex during early postnatal development: a comparison with preoptic area and central hypothalamus using autoradiography with [125I]progestin. Brain Res Dev Brain Res 59:143-155.
115. Shughrue PJ, Stumpf WE, Elger W, Schulze PE, Sar M. 1991b. Progestin receptor cells in the 8-day-old male and female mouse cerebral cortex: autoradiographic evidence for a sexual dimorphism in target cell number. Endocrinology 128:87-95.
116. Shughrue PJ, Sar M, Stumpf WE. 1992. Progestin target cell distribution in forebrain and midbrain regions of the 8-day postnatal mouse brain. Endocrinology 130:3650-3659.
117. Simerly RB. 2002. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507-536.
118. Stead JD, Neal C, Meng F, Wang Y, Evans S, Vazquez DM, Watson SJ, Akil H. 2006. Transcriptional profiling of the developing rat brain reveals that the most dramatic regional differentiation in gene expression occurs postpartum. J Neurosci 26:345-353.
119. Tetel MJ, Jung S, Carbajo P, Ladtkow T, Skafar DF, Edwards DP. 1997. Hinge and amino-terminal sequences contribute to solution dimerization of human progesterone receptor. Mol Endocrinol 11:1114-1128.
120. Toddywalla VS, Patel SB, Betrabet SS, Kulkarni RD, Saxena BN. 1995. Is time-interval between mini-pill ingestion and breastfeeding essential? Contraception 51:193-195.
121. Toran-Allerand CD. 1976. Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res 106:407-412.
122. Traish AM, Wotiz HH. 1990. Monoclonal and polyclonal antibodies to human progesterone receptor peptide-(533-547) recognize a specific site in unactivated (8S) and activated (4S) progesterone receptor and distinguish between intact and proteolyzed receptors. Endocrinology 127:1167-1175.
123. Tsai MJ, O'Malley BW. 1994. Molecular mechanisms of action of steroid/ thyroid receptor superfamily members. Annu Rev Biochem 63:451-486.
124. Tsutsui K, Sakamoto H, Shikimi H, Ukena K. 2004. Organizing actions of neurosteroids in the Purkinje neuron. Neurosci Res 49:273-279.
125. Tung L, Shen T, Abel MG, Powell RL, Takimoto GS, Sartorius CA, Horwitz KB. 2001. Mapping the unique activation function 3 in the progesterone B-receptor upstream segment. Two LXXLL motifs and a tryptophan residue are required for activity. J Biol Chem 276:39843-39851.
126. Uylings HBM, Van Eden CG, Parnavelas JG, Kalsbuk A. 1990. The prenatal and postnatal development of the rat cerebral cortex. In: Kolb B, Tees RC, editors. The cerebral cortex of the rat. Cambridge, MA: MIT Press. p 35-76.
127. Wagner CK, Nakayama AY, De Vries GJ. 1998. Potential role of maternal progesterone in the sexual differentiation of the brain. Endocrinology 139:3658-3661.
128. Wagner CK, Pfau JL, De Vries GJ, Merchenthaler IJ. 2001. Sex differences in progesterone receptor immunoreactivity in neonatal mouse brain depend on estrogen receptor alpha expression. J Neurobiol 47:176-182.
129. Wang L, Andersson S, Warner M, Gustafsson JA. 2001. Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc Natl Acad Sci U S A 98:2792-2796.
130. Wang L, Andersson S, Warner M, Gustafsson JA. 2003. Estrogen receptor (ER)beta knockout mice reveal a role for ERbeta in migration of cortical neurons in the developing brain. Proc Natl Acad Sci U S A 100:703-708.
131. Williams CL, Blaustein JD. 1988. Steroids induce hypothalamic progestin receptors and facilitate female sexual behavior in neonatal rats. Brain Res 449:403-407.
132. Wise SP, Jones EG. 1976. The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J Comp Neurol 168:313-343.
133. Wolfe CA, Van Doren M, Walker HJ, Seney ML, McClellan KM, Tobet SA. 2005. Sex differences in the location of immunochemically defined cell populations in the mouse preoptic area/anterior hypothalamus. Brain Res Dev Brain Res 157:34-41.
134. Wood JG, Martin S, Price DJ. 1992. Evidence that the earliest generated cells of the murine cerebral cortex form a transient population in the subplate and marginal zone. Brain Res Dev Brain Res 66:137-140.
135. Yokosuka M, Okamura H, Hayashi S. 1995. Transient expression of estrogen receptor-immunoreactivity (ER-IR) in the layer V of the developing rat cerebral cortex. Brain Res Dev Brain Res 84:99-108.
136. Zhang L, Chang YH, Feldman AN, Ma W, Lahjouji F, Barker JL, Hu Q, Maric D, Li BS, Li W, Rubinow DR. 1999. The expression of GABA(A) receptor alpha2 subunit is upregulated by testosterone in rat cerebral cortex. Neurosci Lett 265:25-28.
137. Zilles K. 1985. The cortex of the rat: a stereotaxic atlas. Berlin: Springer.
138. Zilles K. 1990. Anatomy of the neocortex: cytoarchitecture and myeloarchitecture. In: Kolb B, Tees RC, editors. The cerebral cortex of the rat. Cambridge, MA: MIT Press. p 77-112.
139. Zsarnovszky A, Belcher SM. 2001. Identification of a developmental gradient of estrogen receptor expression and cellular localization in the developing and adult female rat primary somatosensory cortex. Brain Res Dev Brain Res 129:39-46.
140. Zwain IH, Yen SS. 1999. Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140:3843-3852.