Glial-gonadotrophin hormone (GnRH) neurone interactions in the median eminence and the control of gnrh secretion

Journal of Neuroendocrinology

Volumn 20, Issue 6, 2008, Pages 732-742

  Ojeda, Sergio R ^a   Lomniczi, A ^a   Sandau, U S ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Astrocytes; Cell adhesion molecules; Female sexual development; Glial neuronal interactions; GnRH axons; Hypothalamus; Iintercellular signalling; Neuroendocrine neurones; Tanycytes

Indexed keywords

BETA SECRETASE; CELL ADHESION MOLECULE; CONTACTIN; CONTACTIN RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE BETA; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; ESTRADIOL; GLUTAMIC ACID; GONADORELIN; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; NEU DIFFERENTIATION FACTOR; PROSTAGLANDIN E2; PROTEIN TYROSINE KINASE; SEX HORMONE; SOMATOMEDIN C; SYNAPTIC CELL ADHESION MOLECULE 1; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

ASTROCYTE; CELL ADHESION; CELL FUNCTION; CELL INTERACTION; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; EPENDYMA CELL; GLIA CELL; GONADOTROPIN RELEASE; HORMONAL REGULATION; LIGAND BINDING; MEDIAN EMINENCE; NERVE ENDING; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SEXUAL DEVELOPMENT; SIGNAL PROCESSING; TANYCYTE;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL COMMUNICATION; CELL SHAPE; EPIDERMAL GROWTH FACTOR; GLUTAMIC ACID; GONADOTROPIN-RELEASING HORMONE; INSULIN-LIKE GROWTH FACTOR I; MEDIAN EMINENCE; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5;

EID: 45549107581     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2008.01712.x     Document Type: Review

References (94)

1. Kobayashi H, Wada M, Uemura H. The hypothalamic median eminence as a neuroendocrine organ. Med J Osaka Univ 1972; 23: 43-55.
2. Duvernoy H. The vascular architecture of the median eminence. In: Weindl A, Knigge KM, Scott DE, eds. Brain-Endocrine Interaction: Median Eminence-Structure and Function: Proceedings of the International Symposium, Munich, 1972. Basel: Karger, S. Inc., 1972; 79-108.
3. McKinley MJ, McAllen RM, Mendelsohn FAO, Allen AM, Chai SY, Oldfield BJ. Circumventricular organs: Neuroendocrine interfaces between the brain and the hemal milieu. Front Neuroendocrinol 1990; 11: 91-127.
4. Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 1999; 19: 4462-4471.
5. Rodriguez EM, Blazquez JL, Pastor FE, Pelaez B, Pena P, Peruzzo B, Amat P. Hypothalamic tanycytes: A key component of brain-endocrine interaction. Int Rev Cytol 2005; 247: 89-164.
6. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Varez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 2005; 25: 10-18.
7. Kozlowski GP, Coates PW. Ependymoneuronal specializations between LHRH fibers and cells of the cerebroventricular system. Cell Tissue Res 1985; 242: 301-311.
8. Liposits Z, Gores T, Setalo G, Lengvari I, Flerko B, Vigh S, Schally AV. Ultrastructural characteristics of immunolabelled, corticotropin releasing fractor (CRF)-synthesizing neurons in the rat brain. Cell Tissue Res 1983; 00: 229-191.
9. Jew J, Leranth C, Arimura A, Palkovits M. Preoptic LH-RH and somatostatin in the rat median eminence. An experimental light and electron microscopic immunocytochemical study. Neuroendocrinology 1984; 38: 169-175.
10. Hisano S, Ishizuka H, Nishiyama T, Tsuruo Y, Katoh S, Daikoku S. Immunoelectron microscopic observations of hypothalamic TRH-containing neurons in rats. Exp Brain Res 1986; 63: 495-504.
11. Ibata Y, Okamura H, Makino S, Kawakami F, Morimoto N, Chihara K. Light and electron microscopic immunocytochemistry of GRF-like immunoreactive neurons and terminals in the rat hypothalamic arcuate nucleus and median eminence. Brain Res 1986; 370: 136-143.
12. Prevot V, Dutoit S, Croix D, Tramu G, Beauvillain JC. Semi-quantitative ultrastructural analysis of the localization and neuropeptide content of gonadotropin releasing hormone nerve terminals in the median eminence throughout the estrous cycle of the rat. Neuroscience 1998; 84: 177-191.
13. Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, Beauvillain JC. Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience 1999; 94: 809-819.
14. Prevot V. Glial-neuronal-endothelial interactions are involved in the control of GnRH secretion. J Neuroendocrinol 2002; 14: 247-255.
15. Ojeda SR, Skinner MK. Puberty in the rat. In: Neill JD, ed. The Physiology of Reproduction, 3rd edn. San Diego, CA: Academic Press/ Elsevier, 2006; 2061-2126.
16. Mahesh VB, Dhandapani KM, Brann DW. Role of astrocytes in reproduction and neuroprotection. Mol Cell Endocrinol 2006; 246: 1-9.
17. Beattie EC, Stellwagen D, Morishita W, Bresnahan JC, Ha BK, von Zastrow ME, Beattie MS, Malenka RC. Control of synaptic strength by glial TNFα. Science 2002; 295: 2282-2285.
18. Blondel O, Collin C, McCarran WJ, Zhu S, Zamostiano R, Gozes I, Brenneman DE, McKay RD. A glia-derived signal regulating neuronal differentiation. J Neurosci 2000; 20: 8012-8020.
19. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G. Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci USA 2005; 102: 5606-5611.
20. Mauch DH, Nagler K, Schumacher S, Goritz C, Muller EC, Otto A, Pfrieger FW. CNS synaptogenesis promoted by glia-derived cholesterol. Science 2001; 294: 1354-1357.
21. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005; 120: 421-433.
22. Barres BA. New roles for glia. J Neurosci 1991; 11: 3685-3694.
23. Fields RD, Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 2006; 7: 423-436.
24. Martin DL. Synthesis and release of neuroactive substances by glial cells. Glia 1992; 5: 81-94.
25. Brann DW, Mahesh VB. Excitatory amino acids: Evidence for a role in the control of reproduction and anterior pituitary hormone secretion. Endocr Rev 1997; 18: 678-700.
26. Ojeda SR, Terasawa E. Neuroendocrine regulation of puberty. In: Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R, eds. Hormones, Brain and Behavior, Vol. 4. New York, NY: Elsevier, 2002: 589-659.
27. Fellin T, Sul JY, D'Ascenzo M, Takano H, Pascual O, Haydon PG. Bidirectional astrocyte-neuron communication: The many roles of glutamate and ATP. In: Purinergic signalling in Neuron-Glia Interactions (Norvartis Foundation Symposium 276), Chichester: Wiley, 2006: 208-221.
28. Blutstein T, Devidze N, Choleris E, Jasnow AM, Pfaff DW, Mong JA. Oestradiol up-regulates glutamine synthetase mRNA and protein expression in the hypothalamus and hippocampus: Implications for a role of hormonally responsive glia in amino acid neurotransmission. J Neuroendocrinol 2006; 18: 692-702.
29. Roth CL, McCormack AL, Lomniczi A, Mungenast AE, Ojeda SR. Quantitative proteomics identifies a major change in glial glutamate metabolism at the time of female puberty. Mol Cell Endocrinol 2006; 255: 51-59.
30. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 1998; 391: 281-285.
31. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG. Glutamate-mediated astrocyte-neuron signalling. Nature 1994; 369: 744-747.
32. Ojeda SR, Urbanski HF, Costa ME, Hill DF, Moholt-Siebert M. Involvement of transforming growth factor α in the release of luteinizing hormone-releasing hormone from the developing female hypothalamus. Proc Natl Acad Sci USA 1990; 87: 9698-9702.
33. Voigt P, Ma YJ, Gonzalez D, Fahrenbach WH, Wetsel WC, Berg-von der Emde K, Hill DF, Taylor KG, Costa ME, Seidah NG, Ojeda SR. Neural and glial-mediated effects of growth factors acting via tyrosine kinase receptors on LHRH neurons. Endocrinology 1996; 137: 2593-2605.
34. Tsai P-S, Werner S, Weiner RI. Basic fibroblast growth factor is a neurotropic factor in GT1 gonadotropin-releasing hormone neuronal cell lines. Endocrinology 1995; 136: 3831-3838.
35. Tsai PS, Moenter SM, Postigo HR, El Majdoubi M, Pak TR, Gill JC, Paruthiyil S, Werner S, Weiner RI. Targeted expression of a dominant-negative fibroblast growth factor (FGF) receptor in gonadotropin-releasing hormone (GnRH) neurons reduces FGF responsiveness and the size of GnRH neuronal population. Mol Endocrinol 2005; 19: 225-236.
36. Wetsel WC, Hill DF, Ojeda SR. Basic fibroblast growth factor regulates the conversion of pro-luteinizing hormone-releasing hormone (LHRH) to LHRH in immortalized hypothalamic neurons. Endocrinology 1996; 137: 2606-2616.
37. Gill JC, Tsai PS. Expression of a dominant negative FGF receptor in developing GnRH1 neurons disrupts axon outgrowth and targeting to the median eminence. Biol Reprod 2006; 74: 463-472.
38. 0Bouret S, De Seranno S, Beauvillain JC, Prevot V. Transforming growth factor β1 may directly influence gonadotropin-releasing hormone gene expression in the rat hypothalamus. Endocrinology 2004; 145: 1794-1801.
39. Galbiati M, Zanisi M, Messi E, Cavarretta I, Martini L, Melcangi RC. Transforming growth factor-β and astrocytic conditioned medium influence luteinizing hormone-releasing hormone gene expression in the hypothalamic cell line GT1. Endocrinology 1996; 137: 5605-5609.
40. Etgen AM, Gonzalez-Flores O, Todd BJ. The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Front Neuroendocrinol 2006; 27: 363-375.
41. Daftary SS, Gore AC. IGF-1 in the brain as a regulator of reproductive neuroendocrine function. Exp Biol Med (Maywood) 2005; 230: 292-306.
42. Hiney JK, Ojeda SR, Dees WL. Insulin-like growth factor-I: A possible metabolic signal involved in the regulation of female puberty. Neuroendocrinology 1991; 54: 420-423.
43. Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 1996; 137: 3717-3728.
44. Garcia-Segura LM, Naftolin F, Hutchison JB, Azcoitia I, Chowen JA. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J Neurobiol 1999; 40: 574-584.
45. Dueñas M, Luquin S, Chowen JA, Torres-Aleman I, Naftolin F, Garcia-Segura LM. Gonadal hormone regulation of insulin-like growth factor-I-like immunoreactivity in hypothalamic astroglia of developing and adult rats. Neuroendocrinology 1994; 59: 528-538.
46. Fernandez-Galaz MC, Naftolin F, Garcia-Segura LM. Phasic synaptic remodeling of the rat arcuate nucleus during the estrous cycle depends on insulin-like growth factor-I receptor activation. J Neurosci Res 1999; 55: 286-292.
47. Ojeda SR, Prevot V, Heger S, Lomniczi A, Dziedzic B, Mungenast A. Glia-to neuron signaling and the neuroendocrine control of female puberty. Ann Med 2003; 35: 244-255.
48. Ma YJ, Berg-von der Emde K, Rage F, Wetsel WC, Ojeda SR. Hypothalamic astrocytes respond to transforming growth factor alpha with secretion of neuroactive substances that stimulate the release of luteinizing hormone-releasing hormone. Endocrinology 1997; 138: 19-25.
49. Ma YJ, Hill DF, Creswick KE, Costa ME, Ojeda SR. Neuregulins signaling via a glial erbB2/erbB4 receptor complex contribute to the neuroendocrine control of mammalian sexual development. J Neurosci 1999; 19: 9913-9927.
50. Ma YJ, Junier M-P, Costa ME, Ojeda SR. Transforming growth factor alpha (TGFα) gene expression in the hypothalamus is developmentally regulated and linked to sexual maturation. Neuron 1992; 9: 657-670.
51. Prevot V, Cornea A, Mungenast A, Smiley G, Ojeda SR. Activation of erbB-1 signaling in tanycytes of the median eminence stimulates transforming growth factor β1 release via prostaglandin E2 production and induces cell plasticity. J Neurosci 2003; 23: 10622-10632.
52. Prevot V, Rio C, Cho GJ, Lomniczi A, Heger S, Neville CM, Rosenthal NA, Ojeda SR, Corfas G. Normal female sexual development requires neuregulin-erbB receptor signaling in hypothalamic astrocytes. J Neurosci 2003; 23: 230-239.
53. Ma YJ, Hill DF, Junier M-P, Costa ME, Felder SE, Ojeda SR. Expression of epidermal growth factor receptor changes in the hypothalamus during the onset of female puberty. Mol Cell Neurosci 1994; 5: 246-262.
54. 2 by activating a glia-to-neuron signaling pathway. J Neurosci 1997; 17: 9145-9156.
55. Jasoni CL, Todman MG, Han SK, Herbison AE. Expression of mRNAs encoding receptors that mediate stress signals in gonadotropin-releasing hormone neurons of the mouse. Neuroendocrinology 2005; 82: 320-328.
56. Rage F, Hill DF, Sena-Esteves M, Breakefield XO, Coffey RJ, Costa ME, McCann SM, Ojeda SR. Targeting transforming growth factor α expression to discrete loci of the neuroendocrine brain induces female sexual precocity. Proc Natl Acad Sci USA 1997; 94: 2735-2740.
57. Pinkas-Kramarski R, Shelly M, Guarino BC, Wang L-M, Lyass L, Alroy I, Alamandi M, Kuo A, Moyer JD, Lavi S, Eisenstein M, Ratzkin B, Seger R, Bacus SS, Pierce JH, Andrews GC, Yarden Y. ErbB tyrosine kinases and the two neuregulin families constitute a ligand-receptor network. Mol Cell Biol 1998; 18: 6090-6101.
58. Tzahar E, Pinkas-Kramarski R, Moyer JD, Klapper LN, Alroy I, Levkowitz G, Shelly M, Henis S, Eisenstein M, Ratzkin BJ, Sela M, Andrews GC, Yarden Y. Bivalence of EGF-like ligands drives the ErbB signaling network. EMBO J 1997; 16: 4938-4950.
59. Karunagaran D, Tsahar E, Beerli RR, Chen X, Graus-Porta D, Ratzkin BJ, Seger R, Hynes NE, Yarden Y. ErbB-2 is a common auxiliary subunit of NDF and EGF receptors: Implications for breast cancer. EMBO J 1996; 15: 254-264.
60. Garcia-Segura LM, McCarthy MM. Minireview: Role of glia in neuroendocrine function. Endocrinology 2004; 145: 1082-1086.
61. Mong JA, McCarthy MM. Steroid-induced developmental plasticity in hypothalamic astrocytes: Implications for synaptic patterning. J Neurobiol 1999; 40: 602-619.
62. King JC, Letourneau RL. Luteinizing hormone-releasing hormone terminals in the median eminence of rats undergo dramatic changes after gonadectomy, as revealed by electron microscopic image analysis. Endocrinology 1994; 134: 1340-1351.
63. Ojeda SR, Ma YJ, Lee BJ, Prevot V. Glia-to-neuron signaling and the neuroendocrine control of female puberty. Recent Prog Horm Res 2000; 55: 197-224.
64. Mong JA, Blutstein T. Estradiol modulation of astrocytic form and function: Implications for hormonal control of synaptic communication. Neuroscience 2006; 138: 967-975.
65. Garcia-Segura LM, Melcangi RC. Steroids and glial cell function. Glia 2006; 54: 485-498.
66. Zimmermann P. Estrogen-dependent changes in the functional interrelationships among neurons, ependymal cells and glial cells of the arcuate nucleus. Cytometric studies in the female albino mouse. Cell Tissue Res 1982; 227: 113-128.
67. King JC, Rubin BS. Recruitment of LHRH neurons and increased access of LHRH terminals to portal capillaries: Integral mechanisms for LH surge induction. Ann Endocrinol (Paris) 1996; 57(Suppl 4): 72.
68. Campbell RE. Defining the gonadotrophin-releasing hormone neuronal network: Transgenic approaches to understanding neurocircuitry. J Neuroendocrinol 2007; 19: 561-573.
69. De Seranno S, Estrella C, Loyens A, Cornea A, Ojeda SR, Beauvillain SC, Prevot V. Vascular endothelial cells promote acute ependymoglial cell plasticty. J Neurosci 2004; 24: 10353-10363.
70. Parkash J, Kaur G. Neuronal-glial plasticity in gonadotropin-releasing hormone release in adult female rats: Role of the polysialylated form of the neural cell adhesion molecule. J Endocrinol 2005; 186: 397-409.
71. Perera AD, Lagenaur CF, Plant TM. Postnatal expression of polysialic acid-neural cell adhesion molecule in the hypothalamus of the male rhesus monkey (Macaca mulatta). Endocrinology 1993; 133: 2729-2735.
72. Gascon E, Vutskits L, Kiss JZ. Polysialic acid-neural cell adhesion molecule in brain plasticity: From synapses to integration of new neurons. Brain Res Rev 2007; 56: 101-118.
73. Mungenast A, Ojeda SR. Expression of three gene families encoding cell-cell communication molecules in the prepubertal nonhuman primate hypothalamus. J Neuroendocrinol 2005; 17: 208-219.
74. Parent AS, Mungenast AE, Lomniczi A, Sandau US, Peles E, Bosch MA, Ronnekleiv OK, Ojeda SR. A contactin-receptor-like protein tyrosine phosphatase beta complex mediates adhesive communication between astroglial cells and gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2007; 19: 847-859.
75. Peles E, Nativ M, Campbell PL, Sakurai T, Martinez R, Lev S, Clary DO, Schilling J, Barnea G, Plowman GD, Grumet M, Schlessinger J. The carbonic anhydrase domain of receptor tyrosine phosphatase β is a functional ligand for the axonal cell recognition molecule contactin. Cell 1995; 82: 251-260.
76. Zisch AH, D'Alessandri L, Amrein K, Ranscht B, Winterhalter KH, Vaughan L. The glypiated neuronal cell adhesion molecule contactin/F11 complexes with src-family protein tyrosine kinase Fyn. Mol Cell Neurosci 1995; 6: 263-279.
77. Sakurai T, Lustig M, Nativ M, Hemperly JJ, Schlessinger J, Peles E, Grumet M. Induction of neurite outgrowth through contactin and Nr-CAM by extracellular regions of glial receptor tyrosine phosphatase beta. J Cell Biol 1997; 136: 907-918.
78. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Südhof TC. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 2002; 297: 1525-1531.
79. Mungenast AE, Parent A, Chen SS, Goodlett D, Aebersold R, Corfas G, Ojeda SR. The Synaptic Adhesion Molecule SynCAM is Associated with ERBB4 Dysregulation in the Hypothalamus of Mice with a Delayed Onset of Puberty. Program No 281 20, 2003 Abstract Viewer. Washington, DC: Society for Neuroscience, 2003 (Online).
80. Peles E, Nativ M, Lustig M, Grumet M, Schilling J, Martinez R, Plowman GD, Schlessinger J. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J 1997; 16: 978-988.
81. Lomniczi A, Ojeda SR. A role for glial cells of the neuroendocrine brain in the central control of female sexual development. In: Parpura V, Haydon P, eds. Astrocytes in (Patho)Physiology of the Nervous System, New York, NY: Springer, 2008.
82. Dziedzic B, Prevot V, Lomniczi A, Jung H, Cornea A, Ojeda SR. Neuron-to-glia signaling mediated by excitatory amino acid receptors regulates erbB receptor function in astroglial cells of the neuroendocrine brain. J Neurosci 2003; 23: 915-926.
83. Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, Russell WE, Castner BJ, Johnson RS, Fitzner JN, Boyce RW, Nelson N, Koslosky CJ, Wolfson MF, Rauch CT, Cerretti DP, Paxton RJ, March CJ, Black RA. An essential role for ectodomain shedding in mammalian development. Science 1998; 282: 1281-1284.
84. Horiuchi K, Zhou HM, Kelly K, Manova K, Blobel CP. Evaluation of the contributions of ADAMs 9, 12, 15, 17, and 19 to heart development and ectodomain shedding of neuregulins beta1 and beta2. Dev Biol 2005; 283: 459-471.
85. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S, Rittger A, DeStrooper B, Saftig P, Birchmeier C, Haass C. Control of peripheral nerve myelination by the beta-secretase BACE1. Science 2006; 314: 664-666.
86. Lomniczi A, Cornea A, Costa ME, Ojeda SR. Hypothalamic tumor necrosis factor-α converting enzyme (TACE) mediates excitatory amino acid-dependent neuron-to-glia signaling in the neuroendocrine brain. J Neurosci 2006; 26: 51-62.
87. Kalus I, Bormann U, Mzoughi M, Schachner M, Kleene R. Proteolytic cleavage of the neural cell adhesion molecule by ADAM17/TACE is involved in neurite outgrowth. J Neurochem 2006; 98: 78-88.
88. Perez J, Luquin S, Naftolin F, Garcia-Segura LM. The role of estradiol and progesterone in phased synaptic remodelling of the rat arcuate nucleus. Brain Res 1993; 608: 38-44.
89. Amateau SK, McCarthy MM. Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat Neurosci 2004; 7: 643-650.
90. Amateau SK, McCarthy MM. A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J Neurosci 2002; 22: 8586-8596.
91. Langub MC Jr, Watson RE Jr. Estrogen receptor-immunoreactive glia, endothelia, and ependyma in guinea pig preoptic area and median eminence: Electron microscopy. Endocrinology 1992; 130: 364-372.
92. Gudino-Cabrera G, Nieto-Sampedro M. Estrogen receptor immunoreactivity in Schwann-like brain macroglia. J Neurobiol 1999; 40: 458-470.
93. Fernandez-Galaz MC, Morschl E, Chowen JA, Torres-Aleman I, Naftolin F, Garcia-Segura LM. Role of astroglia and insulin-like growth factor-I in gonadal hormone-dependent synaptic plasticity. Brain Res Bull 1997; 44: 525-531.
94. Buchanan CD, Mahesh VB, Brann DW. Estrogen-astrocyte-luteinizing hormone-releasing hormone signaling: A role for transforming growth factor-β. Biol Reprod 2000; 62: 1710-1721.