Estrogen receptor α and G-protein coupled estrogen receptor 1 are localized to GABAergic neurons in the dorsal striatum

Neuroscience Letters

Volumn 622, Issue , 2016, Pages 118-123

  Almey, Anne ^a   Milner, Teresa A ^b,c   Brake, Wayne G ^a  

^a Concordia University ^*  (Canada)

^b FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Electron microscopy; GPR30; Membrane estrogen receptor alpha; Aminobutyric acid

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 30; G PROTEIN COUPLED RECEPTOR; GPR30 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AXON; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; DENDRITIC SPINE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; DORSAL STRIATUM; ELECTRON MICROSCOPY; FEMALE; GABAERGIC TRANSMISSION; GLIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; ANIMAL; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; CORPUS STRIATUM; ESTROGEN RECEPTOR ALPHA; FEMALE; GABAERGIC NEURONS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84979518714     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2016.04.023     Document Type: Article

References (40)

1. [1] Becker, J.B., Rudick, C.N., Rapid effects of estrogen or progesterone on the amphetamine-induced increase in striatal dopamine are enhanced by estrogen priming: a microdialysis study. Pharmacol. Biochem. Behav. 64 (1999), 53–57 http://www.ncbi.nlm.nih.gov/pubmed/10494997.
2. [2] Thompson, T.L., Attenuation of dopamine uptake in vivo following priming with estradiol benzoate. Brain Res. 834 (1999), 164–167.
3. [3] Becker, J.B., Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci. Lett. 118 (1990), 169–171 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/2125712.
4. [4] Watson, C.S., Alyea, R.A., Hawkins, B.E., Thomas, M.L., Cunningham, K.A., Jakubas, A.A., Estradiol effects on the dopamine transporter—protein levels, subcellular location, and function. J. Mol. Signal., 1, 2006, 5 http://www.ncbi.nlm.nih.gov/pubmed/17224081.
5. [5] Landry, M., Lévesque, D., Di Paolo, T., Estrogenic properties of raloxifene, but not tamoxifen, on D2 and D3 dopamine receptors in the rat forebrain. Neuroendocrinology 76 (2002), 214–222 http://www.karger.com/doi/10.1159/000065951.
6. [6] Becker, J.B., Direct effect of 17 beta-estradiol on striatum: sex differences in dopamine release. Synapse (New York, N. Y.) 5 (1990), 157–164 http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=2309159.
7. [7] Almey, A., Filardo, E.J., Milner, T.A., Brake, W.G., Estrogen receptors are found in glia and at extranuclear neuronal sites in the dorsal striatum of female rats: evidence for cholinergic but not dopaminergic colocalization. Endocrinology 153 (2012), 5373–5383, 10.1210/en.2012-1458.
8. [8] Blaustein, J.D., Lehman, M.N., Turcotte, J.C., Greene, G., Estrogen receptors in dendrites and axon terminals in the guinea pig hypothalamus. Endocrinology 131 (1992), 281–290, 10.1210/endo.131.1.1612006.
9. [9] Herbison, A.E., Estrogen regulation of GABA transmission in rat preoptic area. Brain Res. Bull. 44 (1997), 321–326 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/9370195.
10. [10] Milner, T.A., McEwen, B.S., Hayashi, S., Li, C.J., Reagan, L.P., Alves, S.E., Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 429 (2001), 355–371 http://www.ncbi.nlm.nih.gov/pubmed/11116225.
11. [11] Waters, E.M., Thompson, L.I., Patel, P., Gonzales, A.D., Ye, H.Z., Filardo, E.J., et al. G-protein-coupled estrogen receptor 1 is anatomically positioned to modulate synaptic plasticity in the mouse hippocampus. J. Neurosci. 35 (2015), 2384–2397, 10.1523/JNEUROSCI.1298-14.2015.
12. [12] Hu, M., Watson, C.J., Kennedy, R.T., Becker, J.B., Estradiol attenuates the K+-induced increase in extracellular GABA in rat striatum. Synapse 59 (2006), 122–124, 10.1002/syn.20221.
13. [13] Schultz, K.N., von Esenwein, S.A., Hu, M., Bennett, A.L., Kennedy, R.T., Musatov, S., et al. Viral vector-mediated overexpression of estrogen receptor-alpha in striatum enhances the estradiol-induced motor activity in female rats and estradiol-modulated GABA release. J. Neurosci. 29 (2009), 1897–1903, 10.1523/JNEUROSCI.4647-08.2009.
14. [14] Adermark, L., Subregion-specific modulation of excitatory input and dopaminergic output in the striatum by tonically activated glycine and GABAA receptors. Front. Syst. Neurosci., 5(85), 2011, 10.3389/fnsys.2011.00085.
15. [15] Williams, T.J., Torres-Reveron, A., Chapleau, J.D., Milner, T.A., Hormonal regulation of delta opioid receptor immunoreactivity in interneurons and pyramidal cells in the rat hippocampus. Neurobiol. Learn. Mem. 95 (2011), 206–220, 10.1016/j.nlm.2011.01.002.
16. [16] Okamura, H., Yamamoto, K., Hayashi, S., Kuroiwa, A., Muramatsu, M., A polyclonal antibody to the rat oestrogen receptor expressed in Escherichia coli: characterization and application to immunohistochemistry. J. Endocrinol. 135 (1992), 333–341 http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=1474341.
17. [17] Alves, S.E., Weiland, N.G., Hayashi, S., McEwen, B.S., Immunocytochemical localization of nuclear estrogen receptors and progestin receptors within the rat dorsal raphe nucleus. J. Comp. Neurol. 391 (1998), 322–334 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/9492203.
18. [18] Filardo, E.J., Quinn, J.A., Bland, K.I., Frackelton, A.R., Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. (Baltimore, Md.) 14 (2000), 1649–1660 http://www.ncbi.nlm.nih.gov/pubmed/11043579.
19. [19] Hammond, R., Gibbs, R.B., GPR30 is positioned to mediate estrogen effects on basal forebrain cholinergic neurons and cognitive performance. Brain Res. 1379 (2011), 53–60 http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3046317&tool=pmcentrez&rendertype=abstract.
20. [20] Lauder, J.M., Han, V.K., Henderson, P., Verdoorn, T., Towle, A.C., Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19 (1986), 465–493 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/3022187.
21. [21] Milner, T.A., Waters, E.M., Robinson, D.C., Pierce, J.P., Degenerating processes identified by electron microscopic immunocytochemical methods. Methods Mol. Biol. (Clifton, N. J.) 793 (2011), 23–59.
22. [22] Kritzer, M.F., Regional, laminar, and cellular distribution of immunoreactivity for ER alpha and ER beta in the cerebral cortex of hormonally intact, adult male and female rats. Cereb. Cortex., 2002 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/?term=Regional%2C+laminar%2C+and+cellular+distribution+of+immunoreactivity+for+ER+alpha+and+ER+beta+in+the+cerebral+cortex+of+hormonally+intact%2C+adult+male+and+female+rats.
23. [23] Milner, T.A., Waters, E.M., Robinson, D.C., Pierce, J.P., Degenerating processes identified by electron microscopic immunocytochemical methods. Methods Mol. Biol. 793 (2011), 23–59, 10.1007/978-1-61779-328-8_3.
24. [24] Peters, A., Palay, S.L., Webster, H.F., The Fine Structure of the Nervous System: Neurons and their Supporting Cells. 1991, Oxford University Press https://books.google.ca/books?id=eapqAAAAMAAJ.
25. [25] Delle Donne, K.T., Sesack, S.R., Pickel, V.M., Ultrastructural immunocytochemical localization of neurotensin and the dopamine D2 receptor in the rat nucleus accumbens. J. Comp. Neurol. 371 (1996), 552–566, 10.1002/(SICI)1096-9861(19960805)371:4<552::AID-CNE5>3.0.CO;2-3.
26. [26] Gundersen, V., Ottersen, O.P., Storm-Mathisen, J., Selective excitatory amino acid uptake in glutamatergic nerve terminals and in glia in the rat striatum: quantitative electron microscopic immunocytochemistry of exogenous (D)-aspartate and endogenous glutamate and GABA. Eur. J. Neurosci. 8 (1996), 758–765 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/9081627.
27. [27] Schultz, K.N., von Esenwein, S.A., Hu, M., Bennett, A.L., Kennedy, R.T., Musatov, S., et al. Viral vector-mediated overexpression of estrogen receptor- in striatum enhances the estradiol-induced motor activity in female rats and estradiol-modulated GABA release. J. Neurosci. 29 (2009), 1897–1903, 10.1523/JNEUROSCI.4647-08.2009.
28. [28] Pickel, V.M., Leranth, C., Electron Microscopic Preembedding Double-Immunostaining Methods in Neuroanatomical Tract-Tracing Methods 2. 1989, Springer, US, Boston, MA, 10.1007/978-1-4757-2055-6.
29. [29] Whitehead, K.J., Rose, S., Jenner, P., Involvement of intrinsic cholinergic and GABAergic innervation in the effect of NMDA on striatal dopamine efflux and metabolism as assessed by microdialysis studies in freely moving rats. Eur. J. Neurosci. 14 (2001), 851–860 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/11576189.
30. [30] Smolders, I., De Klippel, N., Sarre, S., Ebinger, G., Michotte, Y., Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat. Eur. J. Pharmacol. 284 (1995), 83–91 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/8549640.
31. [31] Gerfen, C.R., Bolam, J.P., Chapter 1—the neuroanatomical organization of the basal ganglia. Handb. Behav. Neurosci., 2010, 3–28 http://dx.doi.org/10.1016/B978-0-12-374767-9.00001-9.
32. [32] Hassler, R., Haug, P., Nitsch, C., Kim, J.S., Paik, K., Effect of motor and premotor cortex ablation on concentrations of amino acids, monoamines, and acetylcholine and on the ultrastructure in rat striatum. a confirmation of glutamate as the specific cortico-Striatal transmitter. J. Neurochem. 38 (1982), 1087–1098, 10.1111/j.1471-4159.1982.tb05352.x.
33. [33] Hart, S.A., Patton, J.D., Woolley, C.S., Quantitative analysis of ER alpha and GAD colocalization in the hippocampus of the adult female rat. J. Comp. Neurol. 440 (2001), 144–155 (accessed 29.01.16) http://www.ncbi.nlm.nih.gov/pubmed/11745614.
34. [34] Hart, S.A., Snyder, M.A., Smejkalova, T., Woolley, C.S., Estrogen mobilizes a subset of estrogen receptor-alpha-immunoreactive vesicles in inhibitory presynaptic boutons in hippocampal CA1. J. Neurosci. 27 (2007), 2102–2111, 10.1523/JNEUROSCI.5436-06.2007.
35. [35] Wagner, E.J., Ronnekleiv, O.K., Bosch, M.A., Kelly, M.J., Estrogen biphasically modifies hypothalamic GABAergic function concomitantly with negative and positive control of luteinizing hormone release. J. Neurosci. 21 (2001), 2085–2093 (accessed 27.01.16) http://www.ncbi.nlm.nih.gov/pubmed/11245692.
36. [36] Qiu, J., Bosch, M.A., Tobias, S.C., Grandy, D.K., Scanlan, T.S., Ronnekleiv, O.K., et al. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 23 (2003), 9529–9540 (accessed 27.01.16) http://www.jneurosci.org/content/23/29/9529.long.
37. [37] Wójtowicz, T., Mozrzymas, J.W., Estradiol and GABAergic transmission in the hippocampus. Vitam. Horm. 82 (2010), 279–300, 10.1016/S0083-6729(10)82015-1.
38. [38] Pickel, V.M., Towle, A.C., Joh, T.H., Chan, J., Gamma-aminobutyric acid in the medial rat nucleus accumbens: ultrastructural localization in neurons receiving monosynaptic input from catecholaminergic afferents. J. Comp. Neurol. 272 (1988), 1–14, 10.1002/cne.902720102.
39. [39] Pickel, V.M., Chan, J., Spiny neurons lacking choline acetyltransferase immunoreactivity are major targets of cholinergic and catecholaminergic terminals in rat striatum. J. Neurosci. Res. 25 (1990), 263–280.
40. [40] Vélez-Fort, M., Audinat, E., Angulo, M.C., Central role of GABA in neuron-glia interactions. Neuroscientist 18 (2012), 237–250, 10.1177/1073858411403317.