Membrane-initiated estradiol signaling regulating sexual receptivity

Frontiers in Endocrinology

Volumn 2, Issue SEP, 2011, Pages

  Micevych, Paul E ^a   Dewing, Phoebe ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell signaling; Estrogen receptor; Lordosis behavior; Neuroprogesterone; Neurosteroids; Stx

Indexed keywords

EID: 84861946274     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2011.00026     Document Type: Review

References (78)

1. Barfield, R. J., Glaser, J. H., Rubin, B. S., and Etgen, A. M. (1984). Behavioral effects of progestin in the brain. Psychoneuroendocrinology 9, 217-231.
2. Beach, F. A. (1948). Hormones and Behavior. New York: Paul B. Hoeber, Inc.
3. Beach, F. A., and LeBoeuf, B. J. (1967). Coital behaviour in dogs. I. Preferential mating in the bitch. Anim. Behav. 15, 546-558.
4. Berkley, K. J., McAllister, S. L., Accius, B. E., and Winnard, K. P. (2007). Endometriosis-induced vaginal hyperalgesia in the rat: effect of estropause, ovariectomy, and estradiol replacement. Pain 132(Suppl. 1), S150-S159.
5. Bermant, G., and Westbrook, W. H. (1966). Peripheral factors in the regulation of sexual contact by female rats. J. Comp. Physiol. Psychol. 61, 244-250.
6. Bloch, G. J., Babcock, A. M., Gorski, R. A., and Micevych, P. E. (1987). Cholecystokinin stimulates and inhibits lordosis behavior in female rats. Physiol. Behav. 39, 217-224.
7. Bondar, G., Kuo, J., Hamid, N., and Micevych, P. (2009). Estradiol-induced estrogen receptor-alpha trafficking. J. Neurosci. 29, 15323-15330.
8. Boulware, M. I., Weick, J. P., Becklund, B. R., Kuo, S. P., Groth, R. D., and Mermelstein, P. G. (2005). Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J. Neurosci. 25, 5066-5078.
9. Bradshaw, H. B., and Berkley, K. J. (2003). The influence of ovariectomy with or without estrogen replacement on responses of rat gracile nucleus neurons to stimulation of hindquarter skin and pelvic viscera. Brain Res. 986, 82-90.
10. Calizo, L. H., and Flanagan-Cato, L. M. (2003). Hormonal-neural integration in the female rat ventro-medial hypothalamus: triple labeling for estrogen receptoralpha, retrograde tract tracing from the periaqueductal gray, and mating-induced Fos expression. Endocrinology 144, 5430-5440.
11. Cardona-Gomez, G. P., DonCarlos, L., and Garcia-Segura, L. M. (2000). Insulin-like growth factor I receptors and estrogen receptors colocalize in female rat brain. Neuroscience 99, 751-760.
12. Carmeci, C., Thompson, D. A., Ring, H. Z., Francke, U., and Weigel, R. J. (1997). Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics 45, 607-617.
13. Cason, A. M., Samuelsen, C. L., and Berkley,K. J. (2003). Estrous changes in vaginal nociception in a rat model of endometriosis. Horm. Behav. 44, 123-131.
14. Chaban, V., Li, J., McDonald, J. S., Rapkin, A., and Micevych, P. (2011). Estradiol attenuates the adenosine triphosphate-induced increase of intracellular calcium through group ii metabotropic glutamate receptors in rat dorsal root ganglion neurons. J. Neurosci. Res. doi: 10.1002/jnr.22718. [Epub ahead of print].
15. Chaban, V. V., Lakhter, A. J., and Micevych, P. (2004). A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology 145, 3788-3795.
16. Chaban, V. V., Mayer, E. A., Ennes, H. S., and Micevych, P. E. (2003). Estradiol inhibits atp induced intracellular calcium concentration increase in dorsal root ganglia neurons. Neuroscience 118, 941-948.
17. 2+ signaling in mouse dorsal root ganglion neurons. J. Neurosci. Res. 81, 31-37.
18. Christensen, A., Dewing, P., and Micevych, P. (2011). "The STX-activated membrane estrogen receptor regulates female sexual receptivity through interaction with the metabotropic glutamate receptor," in Society for Neuroscience Annual Meeting, Washington, DC.
19. Cooke, B. M., and Woolley, C. S. (2005). Gonadal hormone modulation of dendrites in the mammalian CNS. J. Neurobiol. 64, 34-46.
20. Dewing, P., Boulware, M. I., Sinchak, K., Christensen, A., Mermelstein, P. G., and Micevych, P. (2007). Membrane estrogen receptor-alpha interactions with metabotropic glutamate receptor 1a modulate female sexual receptivity in rats. J. Neurosci. 27, 9294-9300.
21. Dewing, P., Christensen, A., Bondar, G., and Micevych, P. (2008). Protein kinase C signaling in the hypothalamic arcuate nucleus regulates sexual receptivity in female rats. Endocrinology 149, 5934-5942.
22. Dominguez, R., Hu, E., Zhou, M., and Baudry, M. (2009). 17beta-estradiol-mediated neuroprotection and ERK activation require a per-tussis toxin-sensitive mechanism involving GRK2 and beta-arrestin-1. J. Neurosci. 29, 4228-4238.
23. Dominguez, R., and Micevych, P. (2010). Estradiol rapidly regulates membrane estrogen receptor alpha levels in hypothalamic neurons. J. Neurosci. 30, 12589-12596.
24. Dubal, D. B., Rau, S. W., Shughrue, P. J., Zhu, H., Yu, J., Cashion, A. B., Suzuki, S., Gerhold, L. M., Bottner, M. B., Dubal, S. B., Merchanthaler, I., Kindy, M. S., and Wise, P. M. (2006). Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death. Endocrinology 147, 3076-3084.
25. Eckersell, C. B., Popper, P., and Micevych, P. E. (1998). Estrogen-induced alteration of muopioid receptor immunoreactivity in the medial preoptic nucleus and medial amygdala. J. Neurosci. 18, 3967-3976.
26. Erskine, M. S. (1985). Effects of paced coital stimulation on estrus duration in intact cycling rats and ovariectomized and ovariectomized-adrenalectomized hormone-primed rats. Behav. Neurosci. 99, 151-161.
27. Erskine, M. S. (1989). Solicitation behavior in the estrous female rat: a review. Horm. Behav. 23, 473-502.
28. Fernandez-Galaz, M. C., Naftolin, F., and Garcia-Segura, L. M. (1999). Phasic synaptic remodeling of the rat arcuate nucleus during the estrous cycle depends on insulin-like growth factor-I receptor activation. J. Neurosci. Res. 55, 286-292.
29. Garcia-Segura, L. M., Hernandez, P., Olmos, G., Tranque, P. A., and Naftolin, F. (1988). Neuronal membrane remodelling during the oestrus cycle: a freeze-fracture study in the arcuate nucleus of the rat hypothalamus. J. Neurocytol. 17, 377-383.
30. Gorosito, S. V., Lorenzo, A. G., and Cambiasso, M. J. (2008). Estrogen receptor alpha is expressed on the cell-surface of embryonic hypothalamic neurons. Neuroscience 154, 1173-1177.
31. Kuo, J., Hariri, O. R., Bondar, G., Ogi, J., and Micevych, P. (2009). Membrane estrogen receptor-alpha interacts with metabotropic glutamate receptor type 1a to mobilize intracellular calcium in hypothalamic astrocytes. Endocrinology 150, 1369-1376.
32. Loyd, D. R., and Murphy, A. Z. (2008). Androgen and estrogen (alpha) receptor localization on periaqueductal gray neurons projecting to the rostral ventrome-dial medulla in the male and female rat. J. Chem. Neuroanat. 36, 216-226.
33. Mamiya, N., Fukushima, H., Suzuki, A., Matsuyama, Z., Homma, S., Frankland,P.W.,and Kida,S. (2009). Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J. Neurosci. 29, 402-413.
34. McClintock, M. K., and Adler, N. T. (1978). The role of the female during copulation in wild and domestic Norway rats (Rattus norvegicus). Behaviour 67, 67-96.
35. Mendez, P., Azcoitia, I., and Garcia-Segura, L. M. (2003). Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Brain Res. Mol. Brain Res. 112, 170-176.
36. Mermelstein, P. G., and Micevych, P. E. (2008). Nervous system physiology regulated by membrane estrogen receptors. Rev. Neurosci. 19, 413-424.
37. Micevych, P., and Dominguez, R. (2009). Membrane estradiol signaling in the brain. Front. Neuroendocrinol. 30, 315-327. doi: 10.1016/j.yfrne.2009.04.011
38. Micevych, P., Kuo, J., and Christensen, A. (2009). Physiology of membrane oestrogen receptor signalling in reproduction. J. Neuroendocrinol. 21, 249-256.
39. Micevych, P., and Sinchak, K. (2007). "The neurochemistry of limbichypothalamic circuits regulating sexual receptivity," in Handbook of Neurochemistry and Molecular Neurobiology: Behavioral Neurochemistry, Neuroendocrinology and Molecular Neurobiology, eds A. Lajtha and J. Blaustein (New York: Springer), 154-193.
40. Micevych, P., and Sinchak, K. (2008). Estradiol regulation of progesterone synthesis in the brain. Mol. Cell. Endocrinol. 290, 44-50.
41. Micevych, P., Soma, K. K., and Sinchak, K. (2008). Neuroprogesterone: key to estrogen positive feedback? Brain Res. Rev. 57, 470-480.
42. Micevych, P. E., Chaban, V., Ogi, J., Dewing, P., Lu, J. K., and Sinchak, K. (2007). Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology 148, 782-789.
43. Micevych, P. E., and Mermelstein, P. G. (2008). Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol. Neurobiol. 38, 66-77.
44. Micevych, P. E., Rissman, E. F., Gustafsson, J. A., and Sinchak, K. (2003). Estrogen receptoralpha is required for estrogen-induced muopioid receptor internalization. J. Neurosci. Res. 71, 802-810.
45. Mills, R. H., Sohn, R. K., and Micevych, P. E. (2004). Estrogen-induced muopioid receptor internalization in the medial preoptic nucleus is mediated via neuropeptide Y-Y1 receptor activation in the arcuate nucleus of female rats. J. Neurosci. 24, 947-955.
46. Murphy, A. Z., Suckow, S. K., Johns, M., and Traub, R. J. (2009). Sex differences in the activation of the spinoparabrachial circuit by visceral pain. Physiol. Behav. 97, 205-212.
47. Olmos, G., Aguilera, P., Tranque, P., Naftolin, F., and Garcia-Segura, L. M. (1987). Estrogen-induced synaptic remodelling in adult rat brain is accompanied by the reorganization of neuronal membranes. Brain Res. 425, 57-64.
48. Pappas, T. C., Gametchu, B., and Watson, C. S. (1995). Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding. FASEB J. 9, 404-410.
49. Paredes, R. G., and Alonso, A. (1997). Sexual behavior regulated (paced) by the female induces conditioned place preference. Behav. Neurosci. 111, 123-128.
50. Pfaff, D. (1970). Nature of sex hormone effects on rat sex behavior: specificity of effects and individual patterns of response. J. Comp. Physiol. Psychol. 73, 349-358.
51. Pfaff, D. W., Kow, L. M., Loose, M. D., and Flanagan-Cato, L. M. (2008). Reverse engineering the lordosis behavior circuit. Horm. Behav. 54, 347-354.
52. Prossnitz, E. R., Oprea, T. I., Sklar, L. A., and Arterburn, J. B. (2008). The ins and outs of GPR30: a transmembrane estrogen receptor. J. Steroid Biochem. Mol. Biol. 109, 350-353.
53. Qiu, J., Bosch, M. A., Tobias, S. C., Grandy, D. K., Scanlan, T. S., Ronnekleiv,O. K.,and Kelly, M. J. (2003). Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 23, 9529-9540.
54. Qiu, J., Bosch, M. A., Tobias, S. C., Krust, A., Graham, S. M., Murphy, S. J., Korach, K. S., Chambon, P., Scanlan, T. S., Ronnekleiv, O. K., and Kelly, M. J. (2006). A G-protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J. Neurosci. 26, 5649-5655.
55. Quesada, A., and Etgen, A. M. (2002). Functional interactions between estrogen and insulin-like growth factor-I in the regulation of alpha 1B-adrenoceptors and female reproductive function. J. Neurosci. 22, 2401-2408.
56. Quesada, A., Lee, B. Y., and Micevych, P. E. (2008). PI3 kinase/Akt activation mediates estrogen and IGF-1 nigral DA neuronal neuroprotection against a unilateral rat model of Parkinson's disease. Dev. Neurobiol. 68, 632-644.
57. Quesada,A., and Micevych, P. E. (2004). Estrogen interacts with the IGF-1 system to protect nigrostriatal dopamine and maintain motoric behavior after 6-hydroxdopamine lesions. J. Neurosci. Res. 75, 107-116.
58. Quesada, A., Romeo, H. E., and Micevych, P. (2007). Distribution and localization patterns of estrogen receptorbeta and insulin-like growth factor-1 receptors in neurons and glial cells of the female rat substantia nigra: localization of ERbeta and IGF-1R in substantia nigra. J. Comp. Neurol. 503, 198-208.
59. Revankar, C. M., Cimino, D. F., Sklar, L. A., Arterburn, J. B., and Prossnitz, E. R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625-1630.
60. Rissman, E. F., Early, A. H., Taylor, J. A., Korach, K. S., and Lubahn, D. B. (1997). Estrogen receptors are essential for female sexual receptivity. Endocrinology 138, 507-510.
61. Ritter, S. L., and Hall, R. A. (2009). Fine-tuning of GPCR activity by receptor-interacting proteins. Nat. Rev. Mol. Cell Biol. 10, 819-830.
62. Roepke, T. A., Ronnekleiv, O. K., and Kelly, M. J. (2011). Physio-logical consequences of membrane-initiated estrogen signaling in the brain. Front. Biosci. 16, 1560-1573.
63. Sasahara, K., Shikimi, H., Haraguchi, S., Sakamoto, H., Honda, S., Harada, N., and 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.
64. Sinchak, K., Garcia, B. L., Bowlby, R., Charukulvanich, P., Garcia, M. P., and Sanathara, N. (2010). "Muopioid receptor neurons and opioid receptor-like receptor neurons in the medial preoptic nucleus project to the region of the ventrome-dial nucleus of the hypothalamus," in Society for Neuroscience Annual Meeting, San Diego, CA.
65. Sinchak, K., and Micevych, P. (2003). Visualizing activation of opioid circuits by internalization of G protein-coupled receptors. Mol. Neurobiol. 27, 197-222.
66. Sinchak, K., and Micevych, P. E. (2001). Progesterone blockade of estrogen activation of muopioid receptors regulates reproductive behavior. J. Neurosci. 21, 5723-5729.
67. Sodersten, P., and Eneroth, P. (1981). Serum levels of oestradiol-17 beta and progesterone in relation to sexual receptivity in intact and ovariectomized rats. J. Endocrinol. 89, 45-54.
68. Tennent, B. J., Smith, E. R., and Davidson, J. M. (1980). The effects of estrogen and progesterone on female ratproceptivebehavior.Horm. Behav. 14, 65-75.
69. Thomas, P., Pang, Y., Dong, J., Groenen, P., Kelder, J., de Vlieg, J., Zhu, Y., and Tubbs, C. (2007). Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor alpha subtypes and their evolutionary origins. Endocrinology 148, 705-718.
70. Toran-Allerand, C. D. (2005). Estrogen and the brain: beyond ER-alpha, ER-beta,and 17beta-estradiol. Ann. N.Y. Acad. Sci. 1052, 136-144.
71. Toran-Allerand, C. D., Ellis, L., and Pfenninger, K. H. (1988). Estrogen and insulin synergism in neurite growth enhancement in vitro: mediation of steroid effects by interactions with growth factors? Brain Res. 469, 87-100.
72. Toran-Allerand, C. D., Guan, X., MacLusky, N. J., Horvath, T. L., Diano, S., Singh, M., Connolly, E. S. Jr., Nethrapalli, I. S., and Tinnikov, A. A. (2002). ER-X: a novel, plasma membraneassociated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J. Neurosci. 22, 8391-8401.
73. Torii, M., Kubo, K., and Sasaki, T. (1996). Influence of opioid peptides on the priming action of estrogen on lordosis in ovariectomized rats. Neurosci. Lett. 212, 68-70.
74. Torii, M., Kubo, K., and Sasaki, T. (1999). Facilitatory and inhibitory effects of beta-endorphin on lordosis in female rats: relation to time of administration. Horm. Behav. 35, 271-278.
75. Wintermantel, T. M., Campbell, R. E., Porteous, R., Bock, D., Grone, H. J., Todman, M. G., Korach, K. S., Greiner, E., Perez, C. A., Schutz, G., and Herbison, A. E. (2006). Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52, 271-280.
76. Wise, P. M., Dubal, D. B., Rau, S. W., Brown, C. M., and Suzuki, S. (2005). Are estrogens protective or risk factors in brain injury and neuro degeneration? Reevaluation after the women's health initiative. Endocr. Rev. 26, 308-312.
77. Woolley, C. S., and McEwen, B. S. (1992). Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12, 2549-2554.
78. Yildirim, M., Janssen, W. G., Tabori, N. E., Adams, M. M., Yuen, G. S., Akama, K. T., McEwen, B. S., Milner, T. A., and Morrison, J. H. (2008). Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in CA1 region of female rat hippocampus. Neuroscience 152, 360-370.