Ovarian steroids increase PSD-95 expression and dendritic spines in the dorsal raphe of ovariectomized macaques

Synapse

Volumn 67, Issue 12, 2013, Pages 897-908

  Rivera, Heidi M ^a   Bethea, Cynthia L ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Dendritic spines; Estradiol; Golgi; Progesterone; Serotonin

Indexed keywords

ESTRADIOL; GLUTAMATE RECEPTOR; PLACEBO; POSTSYNAPTIC DENSITY PROTEIN 95; PROGESTERONE; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DENDRITIC SPINE; DORSAL RAPHE NUCLEUS; DRUG EFFECT; FEMALE; GENE EXPRESSION; GOLGI STAIN; IMMUNOGOLD STAINING; MACACA; NEUROTRANSMISSION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SEROTONINERGIC NERVE CELL; SILVER STAINING; STEREOLOGY; SYNAPSE;

DENDRITIC SPINES; ESTRADIOL; GOLGI; PROGESTERONE; SEROTONIN;

ANIMALS; DENDRITIC SPINES; ESTRADIOL; FEMALE; GOLGI APPARATUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACACA MULATTA; OVARIECTOMY; PROGESTERONE; RAPHE NUCLEI; SEROTONERGIC NEURONS;

EID: 84885863725     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21702     Document Type: Article

References (71)

1. Akama KT, McEwen BS. 2003. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 23:2333-2339.
2. Bethea CL. 1993. Colocalization of progestin receptors with serotonin in raphe neurons of macaque. Neuroendocrinology 57:1-6.
3. Bethea CL. 1994. Regulation of progestin receptors in raphe neurons of steroid-treated monkeys. Neuroendocrinology 60:50-61.
4. Bethea CL, Reddy AP. 2008. Effect of ovarian hormones on survival genes in laser captured serotonin neurons from macaques. J Neurochem 105:1129-1143.
5. Bethea CL, Reddy AP. 2010. Effect of ovarian hormones on genes promoting dendritic spines in laser-captured serotonin neurons from macaques. Mol Psychiatry 15:1034-1044.
6. Bethea CL, Reddy AP. 2012a. Effect of ovarian steroids on gene expression related to synapse assembly in serotonin neurons of macaques. J Neurosci Res 90:1324-1334.
7. Bethea CL, Reddy AP. 2012b. Ovarian steroids increase glutamatergic related gene expression in serotonin neurons of macaques. Mol Cell Neurosci 49:251-262.
8. Bethea CL, Lu NZ, Gundlah C, Streicher JM. 2002. Diverse actions of ovarian steroids in the serotonin neural system. Front Neuroendocrinol 23:41-100.
9. Bethea CL, Reddy AP, Smith LJ. 2006. Nuclear factor kappa B in the dorsal raphe of macaques: An anatomical link for steroids, cytokines and serotonin. J Psychiatry Neurosci 31:105-114.
10. Bethea CL, Streicher JM, Mirkes SJ, Sanchez RL, Reddy AP, Cameron JL. 2005. Serotonin-related gene expression in female monkeys with individual sensitivity to stress. Neuroscience 132:151-166.
11. Bethea CL, Reddy AP, Tokuyama Y, Henderson JA, Lima FB. 2009. Protective actions of ovarian hormones in the serotonin system of macaques. Front Neuroendocrinol 30:212-238.
12. Bethea CL, Smith AW, Centeno ML, Reddy AP. 2011. Long-term ovariectomy decreases serotonin neuron number and gene expression in free ranging macaques. Neuroscience 192:675-688.
13. 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.
14. Brenner RM, Slayden OD. 1994. Oestrogen action in the endometrium and oviduct of rhesus monkeys during RU486 treatment. Hum Reprod 9 (Suppl 1):82-97.
15. Butler AK, Uryu K, Chesselet MF. 1998. A role for N-methyl-d-aspartate receptors in the regulation of synaptogenesis and expression of the polysialylated form of the neural cell adhesion molecule in the developing striatum. Dev Neurosci 20:253-262.
16. Choi JM, Romeo RD, Brake WG, Bethea CL, Rosenwaks Z, McEwen BS. 2003. Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 144:4734-4738.
17. Coleman K, Robertson ND, Bethea CL. 2011. Long-term ovariectomy alters social and anxious behaviors in semi-free ranging Japanese macaques. Behav Brain Res 225:317-327.
18. de Castilhos J, Forti CD, Achaval M, Rasia-Filho AA. 2008. Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: A golgi study. Brain Res 1240:73-81.
19. De Roo M, Klauser P, Muller D. 2008. LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6:e219.
20. Dumitriu D, Rodriguez A, Morrison JH. 2011. High-throughput, detailed, cell-specific neuroanatomy of dendritic spines using microinjection and confocal microscopy. Nat Protocols 6:1391-1411.
21. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS. 2000. PSD-95 involvement in maturation of excitatory synapses. Science 290:1364-1368.
22. Epperson CN, Wisner KL, Yamamoto B. 1999. Gonadal steroids in the treatment of mood disorders. Psychosom Med 61:676-697.
23. Ethell IM, Pasquale EB. 2005. Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75:161-205.
24. Frankfurt M, Gould E, Woolley CS, McEwen BS. 1990. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: A golgi study in the adult rat. Neuroendocrinology 51:530-535.
25. Fukaya M, Watanabe M. 2000. Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment: A study in the adult mouse brain. J Comp Neurol 426:572-586.
26. Gould E, Woolley CS, Frankfurt M, McEwen BS. 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291.
27. Gundlah C, Lu NZ, Mirkes SJ, Bethea CL. 2001. Estrogen receptor beta (ERbeta) mRNA and protein in serotonin neurons of macaques. Brain Res Mol Brain Res 91:14-22.
28. Gundlah C, Lu NZ, Bethea CL. 2002. Ovarian steroid regulation of monoamine oxidase-A and -B mRNAs in the macaque dorsal raphe and hypothalamic nuclei. Psychopharmacology (Berlin) 160:271-282.
29. Hao J, Janssen WG, Tang Y, Roberts JA, McKay H, Lasley B, Allen PB, Greengard P, Rapp PR, Kordower JH, Hof PR, Morrison JH. 2003. Estrogen increases the number of spinophilin-immunoreactive spines in the hippocampus of young and aged female rhesus monkeys. J Comp Neurol 465:540-550.
30. Hao J, Rapp PR, Leffler AE, Leffler SR, Janssen WG, Lou W, McKay H, Roberts JA, Wearne SL, Hof PR, Morrison JH. 2006. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 26:2571-2578.
31. Hao J, Rapp PR, Janssen WG, Lou W, Lasley BL, Hof PR, Morrison JH. 2007. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci U S A 104:11465-11470.
32. Heikkinen J, Vaheri R, Timonen U. 2006. A 10-year follow-up of postmenopausal women on long-term continuous combined hormone replacement therapy: Update of safety and quality-of-life findings. J Br Menopause Soc 12:115-125.
33. Hotchkiss J, Dierschke DJ, Butler WR, Fritz GR, Knobil E. 1982. Relation between levels of circulating ovarian steroids and pituitary gonadotropin content during the menstrual cycle of the rhesus monkey. Biol Reprod 26:241-248.
34. Jacobs BL, Azmitia EC. 1992. Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
35. Joffe H, Cohen LS. 1998. Estrogen, serotonin, and mood disturbance: Where is the therapeutic bridge? Biol Psychiatry 44:798-811.
36. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH. 1995. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740.
37. Kramar EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G. 2009. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 29:12982-12993.
38. Kugaya A, Epperson CN, Zoghbi S, van Dyck CH, Hou Y, Fujita M, Staley JK, Garg PK, Seibyl JP, Innis RB. 2003. Increase in prefrontal cortex serotonin 2A receptors following estrogen treatment in postmenopausal women. Am J Psychiatry 160:1522-1524.
39. Leranth C, Shanabrough M, Redmond DE, Jr. 2002. Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J Comp Neurol 447:34-42.
40. Leuner B, Falduto J, Shors TJ. 2003. Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23:659-665.
41. Li C, Brake WG, Romeo RD, Dunlop JC, Gordon M, Buzescu R, Magarinos AM, Allen PB, Greengard P, Luine V, McEwen BS. 2004. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci U S A 101:2185-2190.
42. Lima FB, Bethea CL. 2010. Ovarian steroids decrease DNA fragmentation in the serotonin neurons of non-injured rhesus macaques. Mol Psychiatry 15:657-668.
43. Lin Y, Jover-Mengual T, Wong J, Bennett MV, Zukin RS. 2006. PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc Natl Acad Sci U S A 103:19902-19907.
44. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R, Grauer S, Zhang G, Kelley C, Pulito V, Sung A, Mervis RF, Navarra R, Hirst WD, Reinhart PH, Marquis KL, Moss SJ, Pangalos MN, Brandon NJ. 2008. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 11:334-343.
45. Lu NZ, Bethea CL. 2002. Ovarian steroid regulation of 5-HT1A receptor binding and G protein activation in female monkeys. Neuropsychopharmacology 27:12-24.
46. Lu NZ, Eshleman AJ, Janowsky A, Bethea CL. 2003. Ovarian steroid regulation of serotonin reuptake transporter (SERT) binding, distribution, and function in female macaques. Mol Psychiatry 8:353-360.
47. Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM. 1986. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232:1004-1007.
48. Manji HK, Quiroz JA, Sporn J, Payne JL, Denicoff K, Gray NA, Zarate CA, Jr, Charney DS. 2003. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 53:707-742.
49. McKinney RA, Capogna M, Durr R, Gahwiler BH, Thompson SM. 1999. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2:44-49.
50. Meyer C, Schmid R, Scriba PC, Wehling M. 1996. Purification and partial sequencing of high-affinity progesterone-binding site(s) from porcine liver membranes. Eur J Biochem 239:726-731.
51. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG. 1998. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439.
52. Murphy DD, Cole NB, Segal M. 1998. Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons. Proc Natl Acad Sci U S A 95:11412-11417.
53. Ranjan A, Mallick BN. 2012. Differential staining of glia and neurons by modified golgi-cox method. J Neurosci Methods 209:269-279.
54. Ressler KJ, Nemeroff CB. 2000. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12 (Suppl 1):2-19.
55. Rivera HM, Bethea CL. 2012. Ovarian steroids increase spinogenetic proteins in the macaque dorsal raphe. Neuroscience 208:27-40.
56. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL. 2008. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3:e1997.
57. Sanchez RL, Reddy AP, Centeno ML, Henderson JA, Bethea CL. 2005. A second tryptophan hydroxylase isoform, TPH-2 mRNA, is increased by ovarian steroids in the raphe region of macaques. Brain Res Mol Brain Res 135:194-203.
58. Sasahara K, Shikimi H, Haraguchi S, Sakamoto H, Honda S, Harada N, Tsutsui K. 2007. Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell. J Neurosci 27:7408-7417.
59. Schluter OM, Xu W, Malenka RC. 2006. Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51:99-111.
60. Schmidt PJ, Haq N, Rubinow DR. 2004. A longitudinal evaluation of the relationship between reproductive status and mood in perimenopausal women. Am J Psychiatry 161:2238-2244.
61. Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA. 2002. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci U S A 99:13902-13907.
62. Sherwin BB. 1991. The impact of different doses of estrogen and progestin on mood and sexual behavior in postmenopausal women. J Clin Endocrinol Metab 72:336-343.
63. Soares CN, Poitras JR, Prouty J. 2003. Effect of reproductive hormones and selective estrogen receptor modulators on mood during menopause. Drugs Aging 20:85-100.
64. Sorra KE, Harris KM. 2000. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10:501-511.
65. Spencer JL, Waters EM, Milner TA, McEwen BS. 2008. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155:1106-1119.
66. Stranahan AM, Khalil D, Gould E. 2007. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus 17:1017-1022.
67. Waters EM, Mitterling K, Spencer JL, Mazid S, McEwen BS, Milner TA. 2009. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 1290:1-11.
68. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
69. 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.
70. Yuste R, Bonhoeffer T. 2004. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24-34.
71. Zhu Y, Bond J, Thomas P. 2003. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc Natl Acad Sci U S A 100:2237-2242.