Ovarian steroids increase spinogenetic proteins in the macaque dorsal raphe

Neuroscience

Volumn 208, Issue , 2012, Pages 27-40

  Rivera, H M ^a   Bethea, C L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Estradiol; Immunocytochemistry; Progesterone; PSD 95; RhoGTPase; Serotonin

Indexed keywords

17ALPHA ESTRADIOL; 4 PREGNEN 3,20 DIONE; PLACEBO; POSTSYNAPTIC DENSITY PROTEIN 95; PROGESTERONE; PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DENDRITE; DORSAL RAPHE NUCLEUS; FEMALE; GENE EXPRESSION REGULATION; HORMONAL REGULATION; HORMONE ACTION; IMMUNOGOLD STAINING; IMMUNOHISTOCHEMISTRY; NERVE CELL PLASTICITY; NERVE FUNCTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RHESUS MONKEY; SEROTONINERGIC NERVE CELL; STEREOLOGY; TREATMENT DURATION;

ANIMALS; ANTIBODY SPECIFICITY; CDC42 GTP-BINDING PROTEIN; DENDRITIC SPINES; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; NERVE TISSUE PROTEINS; OVARIECTOMY; OVARY; PROGESTERONE; RAPHE NUCLEI; RHOA GTP-BINDING PROTEIN; STEROIDS;

EID: 84858624894     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.02.002     Document Type: Article

References (76)

1. Akama K.T., McEwen B.S. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 2003, 23:2333-2339.
2. Bethea C.L. Colocalization of progestin receptors with serotonin in raphe neurons of macaque. Neuroendocrinology 1993, 57:1-6.
3. Bethea C.L. Regulation of progestin receptors in raphe neurons of steroid-treated monkeys. Neuroendocrinology 1994, 60:50-61.
4. Bethea C.L., Lu N.Z., Gundlah C., Streicher J.M. Diverse actions of ovarian steroids in the serotonin neural system. Front Neuroendocrinol 2002, 23:41-100.
5. Bethea C.L., Reddy A.P. Effect of ovarian hormones on genes promoting dendritic spines in laser-captured serotonin neurons from macaques. Mol Psychiatry 2010, 15:1034-1044.
6. Bethea CL, Reddy AP (in press) Effect of ovarian steroids on gene expression related to synapse assembly in serotonin neurons of macaques. J Neurosci Res, in press.
7. Bethea C.L., Reddy A.P. Ovarian steroids increase glutamatergic related gene expression in serotonin neurons of macaques. Mol Cell Neurosci 2011, 49:251-262.
8. Bethea C.L., Reddy A.P., Tokuyama Y., Henderson J.A., Lima F.B. Protective actions of ovarian hormones in the serotonin system of macaques. Front Neuroendocrinol 2009, 30:212-238.
9. Bethea C.L., Smith A.W., Centeno M.L., Reddy A.P. Long-term ovariectomy decreases serotonin neuron number and gene expression in free ranging macaques. Neuroscience 2011, 192:675-688.
10. Bethea C.L., Streicher J.M., Mirkes S.J., Sanchez R.L., Reddy A.P., Cameron J.L. Serotonin-related gene expression in female monkeys with individual sensitivity to stress. Neuroscience 2005, 132:151-166.
11. Brabeck C., Beschorner R., Conrad S., Mittelbronn M., Bekure K., Meyermann R., Schluesener H.J., Schwab J.M. Lesional expression of RhoA and RhoB following traumatic brain injury in humans. J Neurotrauma 2004, 21:697-706.
12. Brake W.G., Alves S.E., Dunlop J.C., Lee S.J., Bulloch K., Allen P.B., Greengard P., McEwen B.S. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 2001, 142:1284-1289.
13. Brenner R.M., Slayden O.D. Oestrogen action in the endometrium and oviduct of rhesus monkeys during RU486 treatment. Hum Reprod 1994, 9(Suppl 1):82-97.
14. Butler A.K., Uryu K., Chesselet M.F. 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 1998, 20:253-262.
15. Choi J.M., Romeo R.D., Brake W.G., Bethea C.L., Rosenwaks Z., McEwen B.S. Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 2003, 144:4734-4738.
16. Coleman K., Robertson N.D., Bethea C.L. Long-term ovariectomy alters social and anxious behaviors in semi-free ranging Japanese macaques. Behav Brain Res 2011, 225:317-327.
17. Conde D.M., Pinto-Neto A.M., Santos-Sa D., Costa-Paiva L., Martinez E.Z. Factors associated with quality of life in a cohort of postmenopausal women. Gynecol Endocrinol 2006, 22:441-446.
18. de Castilhos J., Forti C.D., Achaval M., Rasia-Filho A.A. 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 2008, 1240:73-81.
19. de Roo M., Klauser P., Muller D. LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 2008, 6:e219.
20. Doyle M., Kiebler M.A. Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J 2011, 30:3540-3552.
21. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science 2000, 290:1364-1368.
22. Epperson C.N., Wisner K.L., Yamamoto B. Gonadal steroids in the treatment of mood disorders. Psychosom Med 1999, 61:676-697.
23. Ethell I.M., Pasquale E.B. Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 2005, 75:161-205.
24. Fischer M., Kaech S., Wagner U., Brinkhaus H., Matus A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci 2000, 3:887-894.
25. Frankfurt M., Gould E., Woolley C.S., McEwen B.S. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a Golgi study in the adult rat. Neuroendocrinology 1990, 51:530-535.
26. Fu X.D., Flamini M., Sanchez A.M., Goglia L., Giretti M.S., Genazzani A.R., Simoncini T. Progestogens regulate endothelial actin cytoskeleton and cell movement via the actin-binding protein moesin. Mol Hum Reprod 2008, 14:225-234.
27. Fu X.D., Giretti M.S., Baldacci C., Garibaldi S., Flamini M., Sanchez A.M., Gadducci A., Genazzani A.R., Simoncini T. Extra-nuclear signaling of progesterone receptor to breast cancer cell movement and invasion through the actin cytoskeleton. PLoS One 2008, 3:e2790.
28. Fukaya M., Watanabe M. 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 2000, 426:572-586.
29. Giretti M.S., Fu X.D., De Rosa G., Sarotto I., Baldacci C., Garibaldi S., Mannella P., Biglia N., Sismondi P., Genazzani A.R., Simoncini T. Extra-nuclear signalling of estrogen receptor to breast cancer cytoskeletal remodelling, migration and invasion. PLoS One 2008, 3:e2238.
30. Gould E., Woolley C.S., Frankfurt M., McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990, 10:1286-1291.
31. Gundlah C., Lu N.Z., Mirkes S.J., Bethea C.L. Estrogen receptor beta (ERbeta) mRNA and protein in serotonin neurons of macaques. Brain Res Mol Brain Res 2001, 91:14-22.
32. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
33. Hall A., Lalli G. Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb Perspect Biol 2010, 2. a001818.
34. Hao J., Janssen W.G., Tang Y., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen increases the number of spinophilin-immunoreactive spines in the hippocampus of young and aged female rhesus monkeys. J Comp Neurol 2003, 465:540-550.
35. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., McKay H., Roberts J.A., Wearne S.L., Hof P.R., Morrison J.H. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 2006, 26:2571-2578.
36. Heikkinen J., Vaheri R., Timonen U. 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 2006, 12:115-125.
37. Hoffman G.E., Le W.W., Sita L.V. The importance of titrating antibodies for immunocytochemical methods. Curr Protoc Neurosci Chapter 2 2008, Unit 2.12.
38. Hotchkiss J., Dierschke D.J., Butler W.R., Fritz G.R., Knobil E. Relation between levels of circulating ovarian steroids and pituitary gonadotropin content during the menstrual cycle of the rhesus monkey. Biol Reprod 1982, 26:241-248.
39. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-229.
40. Joffe H., Cohen L.S. Estrogen, serotonin, and mood disturbance: where is the therapeutic bridge?. Biol Psychiatry 1998, 44:798-811.
41. Kennedy M.J., Ehlers M.D. Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 2006, 29:325-362.
42. Kim E., Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci 2004, 5:771-781.
43. Kornau H.C., Schenker L.T., Kennedy M.B., Seeburg P.H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995, 269:1737-1740.
44. Kramar E.A., Chen L.Y., Brandon N.J., Rex C.S., Liu F., Gall C.M., Lynch G. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 2009, 29:12982-12993.
45. Kugaya A., Epperson C.N., Zoghbi S., van Dyck C.H., Hou Y., Fujita M., Staley J.K., Garg P.K., Seibyl J.P., Innis R.B. Increase in prefrontal cortex serotonin 2A receptors following estrogen treatment in postmenopausal women. Am J Psychiatry 2003, 160:1522-1524.
46. Lin Y., Jover-Mengual T., Wong J., Bennett M.V., Zukin R.S. PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc Natl Acad Sci U S A 2006, 103:19902-19907.
47. Liu F., Day M., Muniz L.C., Bitran D., Arias R., Revilla-Sanchez R., Grauer S., Zhang G., Kelley C., Pulito V., Sung A., Mervis R.F., Navarra R., Hirst W.D., Reinhart P.H., Marquis K.L., Moss S.J., Pangalos M.N., Brandon N.J. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 2008, 11:334-343.
48. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986, 232:1004-1007.
49. Maki P.M., Freeman E.W., Greendale G.A., Henderson V.W., Newhouse P.A., Schmidt P.J., Scott N.F., Shively C.A., Soares C.N. Summary of the National Institute on Aging-sponsored conference on depressive symptoms and cognitive complaints in the menopausal transition. Menopause 2010, 17:815-822.
50. Manji H.K., Quiroz J.A., Sporn J., Payne J.L., Denicoff K., Gray N.A., Zarate C.A., Charney D.S. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 2003, 53:707-742.
51. Matus A., Brinkhaus H., Wagner U. Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus 2000, 10:555-560.
52. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 1999, 2:44-49.
53. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G., Morrison J.H., O'Dell T.J., Grant S.G. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998, 396:433-439.
54. Murphy D.D., Cole N.B., Segal M. Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons. Proc Natl Acad Sci U S A 1998, 95:11412-11417.
55. Negishi M., Katoh H. Rho family GTPases and dendrite plasticity. Neuroscientist 2005, 11:187-191.
56. O'Kane E.M., Stone T.W., Morris B.J. Distribution of Rho family GTPases in the adult rat hippocampus and cerebellum. Brain Res Mol Brain Res 2003, 114:1-8.
57. Papa M., Segal M. Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience 1996, 71:1005-1011.
58. Ressler K.J., Nemeroff C.B. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 2000, 12(Suppl 1):2-19.
59. Sanchez A.M., Flamini M.I., Fu X.D., Mannella P., Giretti M.S., Goglia L., Genazzani A.R., Simoncini T. Rapid signaling of estrogen to WAVE1 and moesin controls neuronal spine formation via the actin cytoskeleton. Mol Endocrinol 2009, 23:1193-1202.
60. Sanchez R.L., Reddy A.P., Centeno M.L., Henderson J.A., Bethea C.L. A second tryptophan hydroxylase isoform, TPH-2 mRNA, is increased by ovarian steroids in the raphe region of macaques. Brain Res Mol Brain Res 2005, 135:194-203.
61. Santos Da Silva J., Schubert V., Dotti C.G. RhoA, Rac1, and cdc42 intracellular distribution shift during hippocampal neuron development. Mol Cell Neurosci 2004, 27:1-7.
62. Sasahara K., Shikimi H., Haraguchi S., Sakamoto H., Honda S., Harada N., Tsutsui K. Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell. J Neurosci 2007, 27:7408-7417.
63. Schluter O.M., Xu W., Malenka R.C. Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 2006, 51:99-111.
64. Schmidt P.J., Haq N., Rubinow D.R. A longitudinal evaluation of the relationship between reproductive status and mood in perimenopausal women. Am J Psychiatry 2004, 161:2238-2244.
65. Schnell E., Sizemore M., Karimzadegan S., Chen L., Bredt D.S., Nicoll R.A. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci U S A 2002, 99:13902-13907.
66. Sherwin B.B. The impact of different doses of estrogen and progestin on mood and sexual behavior in postmenopausal women. J Clin Endocrinol Metab 1991, 72:336-343.
67. Simoncini T., Scorticati C., Mannella P., Fadiel A., Giretti M.S., Fu X.D., Baldacci C., Garibaldi S., Caruso A., Fornari L., Naftolin F., Genazzani A.R. Estrogen receptor alpha interacts with Galpha13 to drive actin remodeling and endothelial cell migration via the RhoA/Rho kinase/moesin pathway. Mol Endocrinol 2006, 20:1756-1771.
68. Soares C.N., Poitras J.R., Prouty J. Effect of reproductive hormones and selective estrogen receptor modulators on mood during menopause. Drugs Aging 2003, 20:85-100.
69. Spencer J.L., Waters E.M., Milner T.A., McEwen B.S. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 2008, 155:1106-1119.
70. Tang Y., Janssen W.G., Hao J., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb Cortex 2004, 14:215-223.
71. Tangen T., Mykletun A. Depression and anxiety through the climacteric period: an epidemiological study (HUNT-II). J Psychosom Obstet Gynaecol 2008, 29:125-131.
72. Waters E.M., Mitterling K., Spencer J.L., Mazid S., McEwen B.S., Milner T.A. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 2009, 1290:1-11.
73. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991, 231:482-497.
74. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 1992, 12:2549-2554.
75. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 1993, 336:293-306.
76. Woolley C.S., Weiland N.G., McEwen B.S., Schwartzkroin P.A. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 1997, 17:1848-1859.