A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2

Journal of Neuroscience

Volumn 22, Issue 19, 2002, Pages 8586-8596

  Amateau, Stuart K ^a   McCarthy, Margaret M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Cyclooxygenase 2; Dendritic spines; Estrogen; Preoptic area; Prostaglandin E2

Indexed keywords

AMPA RECEPTOR ANTAGONIST; CELL PROTEIN; CYCLOOXYGENASE 2; ESTRADIOL; KAINIC ACID RECEPTOR ANTAGONIST; PROSTAGLANDIN E2; SPINOPHILIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CENTRAL NERVOUS SYSTEM; DENDRITIC SPINE; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL PLASTICITY; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 0036813151     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-19-08586.2002     Document Type: Article

References (89)

1. Adair ER (1977) Skin, preoptic, and core temperatures influence behavioral thermoregulation. J Appl Physiol 42:559-564.
2. Allen PB, Ouimet CC, Greengard P (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci USA 941:9956-9961.
3. Altman J, Bayer SA (1995) Atlas of Prenatal Rat Brain Development. Boca Raton, FL: CRC.
4. Anderson CH (1982) Changes in dendritic spine density in the preoptic area of the female rat at puberty. Brain Res Bull 8:261-265.
5. Baloyannis SJ, Kim SU (1979) Experimental modification of cerebellar development in tissue culture: X-irradiation induces granular degeneration and unattached Purkinje cell dendritic spines. Neurosci Lett 12:283-288.
6. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285.
7. Bloch GJ, Gorski RA (1988) Estrogen/progesterone treatment in adulthood affects the size of several components of the medial preoptic area in the male rat. J Comp Neurol 4:613-622.
8. Brake WG, Alves SE, Dunlop JC, Lee SJ, Bulloch K, Allen PB, Greengard P, McEwen BS (2001) Novel target sites for estrogen action in the dorsal hippocampus: An examination of synaptic proteins. Endocrinology 142:1284-1289.
9. Breder CD, Dewitt D, Kraig RP (1995) Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 355:296-315.
10. Caggiano AO, Kraig RP (1998) Prostaglandin E2 and 4-aminopyridine prevent the lipopolysaccharide-induced outwardly rectifying potassium current and interleukin-1 beta production in cultured rat microglia. J Neurochem 70:2357-2368.
11. Calizo LH, Flanagan-Cato LM (2000) Estrogen selectively regulates spine density within the dendritic arbor of rat ventromedial hypothalamic neurons. J Neurosci 20:1589-1596.
12. Clemens LG, Gladue BA (1977) Effect of prostaglandin E2 on masculine sexual behaviour in the rat. J Endocrinol 75:383-389.
13. Colonnier M (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9:268-287.
14. Cordoba Montoya DA, Carrer HF (1997) Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778:430-438.
15. DonCarlos LL (1996) Developmental profile and regulation of estrogen receptor (ER) mRNA expression in the preoptic area of prenatal rats. Brain Res Dev Brain Res 94:224-233.
16. DonCarlos LL, Handa RJ (1994) Developmental profile of estrogen receptor mRNA in the preoptic area of male and female neonatal rats. Brain Res Dev Brain Res 79:283-289.
17. Feng J, Yan Z, Ferreira A, Tomizawa K, Liauw JA, Zhuo M, Allen PB, Ouimet CC, Greengard P (2000) Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad Sci USA 97:9287-9292.
18. Fifkova E (1985) A possible mechanism of morphometric changes in dendritic spines induced by stimulation. Cell Mol Neurobiol 5:47-63.
19. Fuxe K, Cintra A, Agnati LF, Harfstrand A, Wikstrom AC, Okret S, Zoli M, Miller LS, Greene JL, Gustafsson JA (1987) Studies on the cellular localization and distribution of glucocorticoid receptor and estrogen receptor immunoreactivity in the central nervous system of the rat and their relationship to the monoaminergic and peptidergic neurons of the brain. J Steroid Biochem 27:159-170.
20. Goldin M, Segal M, Avignone E (2001) Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. J Neurosci 21:186-193.
21. Gordon CJ, Heath JE (1980) Effects of prostaglandin E2 on the activity of thermosensitive and insensitive single units in the preoptic/anterior hypothalamus of unanesthetized rabbits. Brain Res 183:113-121.
22. Gupta RR, Sen S, Diepenhorst LL, Rudick CN, Maren S (2001) Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats(l). Brain Res 888:356-365.
23. Herrmann K (1996) Differential distribution of AMPA receptors and glutamate during pre- and postnatal development in the visual cortex of ferrets. J Comp Neurol 375:1-17.
24. Ito S, Okuda-Ashitaka E, Minami T (2001) Central and peripheral roles of prostaglandins in pain and their interactions with novel neuropeptides nociceptin and nocistatin. Neurosci Res 41:299-332.
25. Kaech S, Parmar H, Roelandse M, Bornmann C, Matus A (2001) Cytoskeletal microdifferentiation: A mechanism for organizing morphological plasticity in dendrites. Proc Natl Acad Sci USA 98:7086-7092.
26. Karmali RA, Welt S, Thaler HT, Lefevre F (1983) Prostaglandins in breast cancer: Relationship to disease stage and hormone status. Br J Cancer 48:689-696.
27. Katayama S, Lee JB (1985) Estradiol stimulates rat renopapillary prostaglandin E2 (PGE2), but not PGF2 alpha biosynthesis. Endocrinology 117:656-661.
28. Kaufmann WE, Worley PF, Pegg J, Bremer M, Isakson P (1996) COX-2, a synaptically induced enzyme, is expressed by excitatory neurons at postsynaptic sites in rat cerebral cortex. Proc Natl Acad Sci USA 93:2317-2321.
29. Kaufmann WE, Andreasson KI, Isakson PC, Worley PF (1997) Cyclooxygenases and the central nervous system. Prostaglandins 54:601624.
30. Kundu N, Yang Q, Dorsey R, Fulton AM (2001) Increased cyclooxygenase-2 (cox-2) expression and activity in a murine model of metastatic breast cancer. Int J Cancer 93:681-686.
31. Langub Jr MC, Watson Jr RE (1992) Estrogen receptor-immunoreactive glia, endothelia, and ependyma in guinea pig preoptic area and median eminence: Electron microscopy. Endocrinology 130:364-372.
32. Larkman AU (1991) Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J Comp Neurol 306:332-343.
33. Larriva-Sahd J (1991) Ultrastructural evidence of a sexual dimorphism in the neuropil of the medial preoptic nucleus of the rat: A quantitative study. Neuroendocrinology 54:416-419.
34. Luczak A, Szmigielski S, Gumulka SW (1979) Decreased myocardial and renal content of 3′, 5′-AMP in genetically hypertensive rats: Effects of PGE2 and PGF2 alpha. Pol J Pharmacol Pharm 31:589-594.
35. Luthi A, Schwyzer L, Mateos JM, Gahwiler BH, McKinney RA (2001) NMDA receptor activation limits the number of synaptic connections during hippocampal development. Nat Neurosci 4:1102-1107.
36. Ma YJ, Berg-von der Emde K, Rage F, Wetsel WC, Ojeda SR (1997) Hypothalamic astrocytes respond to transforming growth factor-alpha with the secretion of neuroactive substances that stimulate the release of luteinizing hormone-releasing hormone. Endocrinology 138:19-25.
37. MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 2114:1294-1302.
38. Matsumoto A, Arai Y (1980) Sexual dimorphism in 'wiring pattern' in the hypothalamic arcuate nucleus and its modification by neonatal hormonal environment. Brain Res 190:238-242.
39. Matsumoto A, Arai Y (1986) Male-female difference in synaptic organization of the ventromedial nucleus of the hypothalamus in the rat. Neuroendocrinology 42:232-236.
40. Matsumoto A, Murakami S, Arai Y (1988) Neurotropic effects of estrogen on the neonatal preoptic area grafted into the adult rat brain. Cell Tissue Res 252:33-37.
41. Mattson MP (1988) Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res 472:179-212.
42. Matus A (2000) Actin-based plasticity in dendritic spines. Science 290:754-758.
43. McEwen BS, Alves SE (1999) Estrogen actions in the central nervous system. Endocr Rev 20:279-307.
44. McKinney RA, Capogna M, Durr R, Gahwiler BH, Thompson SM (1999a) Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2:44-49.
45. McKinney RA, Luthi A, Bandtlow CE, Gahwiler BH, Thompson SM (1999b) Selective glutamate receptor antagonists can induce or prevent axonal sprouting in rat hippocampal slice cultures. Proc Natl Acad Sci USA 96:11631-11636.
46. Meisel RL, Sachs BD (1994) The physiology of male sexual behavior. In: The Physiology of Reproduction, Vol 2 (Knobil E, Neill JD), pp 3-107. New York: Raven.
47. Meshul CK, Seil FJ (1988) Transplanted astrocytes reduce synaptic density in the neuropil of cerebellar cultures. Brain Res 441:23-32.
48. Mong JA, Glaser E, McCarthy MM (1999) Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J Neurosci 19:1464-1472.
49. 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.
50. Montano MM, Welshons WV, vom Saal FS (1995) Free estradiol in serum and brain uptake of estradiol during fetal and neonatal sexual differentiation in female rats. Biol Reprod 53:1198-1207.
51. Morimoto A, Long NC, Nakamori T, Murakami N (1991) The effect of prostaglandin E2 on the body temperature of restrained rats. Physiol Behav 50:249-253.
52. Moser MB, Trommald M, Andersen P (1994) An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci USA 91:12673-12675.
53. Mouihate A, Lestage J (1995) Estrogen increases the release of epidermal growth factor from individual pituitary cells in female rats. J Endocrinol 146:495-500.
54. Munoz-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.
55. Murphy DD, Segal M (1996) Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059-4068.
56. Naftolin F, Ryan KJ, Petro Z (1971) Aromatization of androstenedione by the diencephalon. J Clin Endocrinol Metab 33:368-370.
57. Nakanishi H, Obaishi H, Satoh A, Wada M, Mandai K, Satoh K, Nishioka H, Matsuura Y, Mizoguchi A, Takai Y (1997) Neurabin: A novel neural tissue-specific actin filament-binding protein involved in neurite formation. J Cell Biol 139:951-961.
58. Nicol GD, Klingberg DK, Vasko MR (1992) Prostaglandin E2 increases calcium conductance and stimulates release of substance P in avian sensory neurons. J Neurosci 12:1917-1927.
59. Numan M (1994) Maternal behavior. In: The Physiology of Reproduction, Vol 2 (Knobil E, Neill JD), pp 221-302. New York: Raven.
60. O'Banion MK, Miller JC, Chang JW, Kaplan MD, Coleman PD (1996) Interleukin-1 beta induces prostaglandin G/H synthase-2 (cyclooxygenase-2) in primary murine astrocyte cultures. J Neurochem 66:2532-2540.
61. Ojeda SR, Ma YJ (1999) Glial-neuronal interactions in the neuroendocrine control of mammalian puberty: Facilitatory effects of gonadal steroids. J Neurobiol 40:528-540.
62. Perez J, Naftolin F, Garcia Segura LM (1990) Sexual differentiation of synaptic connectivity and neuronal plasma membrane in the arcuate nucleus of the rat hypothalamus. Brain Res 527:116-122.
63. Pfrieger FW, Barres BA (1997) Synaptic efficacy enhanced by glial cells in vitro. Science 277:1684-1687.
64. Pozzo Miller LD, Aoki A (1991) Stereological analysis of the hypothalamic ventromedial nucleus. II. Hormone-induced changes in the synaptogenic pattern. Brain Res Dev Brain Res 61:189-196.
65. Rage F, Lee BJ, Ma YJ, Ojeda SR (1997) Estradiol enhances prostaglandin E2 receptor gene expression in luteinizing hormone-releasing hormone (LHRH) neurons and facilitates the LHRH response to PGE2 by activating a glia-to-neuron signaling pathway. J Neurosci 17:9145-9156.
66. Raisman G, Field PM (1973) Sexual dimorphism in the neuropil of the preoptic area of the rat and its dependence on neonatal androgen. Brain Res 54:1-29.
67. Rhoda J, Corbier P, Roffi J (1984) Gonadal steroid concentrations in serum and hypothalamus of the rat at birth: Aromatization of testosterone to 17 beta-estradiol. Endocrinology 114:1754-1760.
68. Ruwe WD, Myers RD (1979) Fever produced by intrahypothalamic pyrogen: Effect of protein synthesis inhibition by anisomycin. Brain Res Bull 4:741-745.
69. Ryan KJ, Naftolin F, Reddy V, Flores F, Petro Z (1972) Estrogen formation in the brain. Am J Obstet Gynecol 114:454-460.
70. Sandstrom NJ, Williams CL (2001) Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115:384-393.
71. Sanzgiri RP, Araque A, Haydon PG (1999) Prostaglandin E(2) stimulates glutamate receptor-dependent astrocyte neuromodulation in cultured hippocampal cells. J Neurobiol 41:221-229.
72. Seil FJ (1997) Cerebellar culture models of dendritic spine proliferation after transplantation of glia. J Neural Transplant Plast 6:1-10.
73. Seil FJ, Eckenstein FP, Reier PJ (1992) Induction of dendritic spine proliferation by an astrocyte secreted factor. Exp Neurol 117:85-89.
74. Sorra KE, Harris KM (2000) Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10:501-511.
75. Southall MD, Vasko MR (2000) Prostaglandin E(2)-mediated sensitization of rat sensory neurons is not altered by nerve growth factor. Neurosci Lett 287:33-36.
76. Stephens DJ, Banting G (2000) In vivo dynamics of the F-actin-binding protein neurabin-II. Biochem J 345:185-194.
77. Takadera T, Yumoto H, Tozuka Y, Ohyashiki T (2002) Prostaglandin E(2) induces caspase-dependent apoptosis in rat cortical cells. Neurosci Lett 317:61-64.
78. Tremblay E, Roisin MP, Represa A, Charriaut-Marlangue C, Ben-Ari Y (1988) Transient increased density of NMDA binding sites in the developing rat hippocampus. Brain Res 461:393-396.
79. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657-661.
80. Villani F, Chiarra A, Cristalli S, Piccinini F (1974) Effect of PGE2 on the turnover of calcium in rat uterus. Experientia 30:532-534.
81. Warren SG, Humphreys AG, Juraska JM, Greenough WT (1995) LTP varies across the estrous cycle: Enhanced synaptic plasticity in proestrus rats. Brain Res 703:26-30.
82. Whalen RE, Nadler RD (1963) Suppression of the development of female behavior by estrogen administered in infancy. Science 141:273-274.
83. Woolley CS (1998) Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34:140-148.
84. Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
85. Woolley CS, McEwen BS (1994) Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687.
86. Woolley CS, Gould E, Frankfurt M, McEwen BS (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
87. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA (1997) Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: Correlation with dendritic spine density. J Neurosci 17:1848-1859.
88. Yuri K, Kawata M (1991) The effect of estrogen on the estrogen receptor-immunoreactive cells in the rat medial preoptic nucleus. Brain Res 548:50-54.
89. Zhang C, Hammassaki-Britto DE, Britto LR, Duvoisin RM (1996) Expression of glutamate receptor subunit genes during development of the mouse retina. NeuroReport 8:335-340.