Medial prefrontal cortical estradiol rapidly alters memory system bias in female rats: Ultrastructural analysis reveals membrane-associated estrogen receptors as potential mediators

Endocrinology (United States)

Volumn 155, Issue 11, 2014, Pages 4422-4432

  Almey, Anne ^a   Cannell, Elizabeth ^a   Bertram, Kyla ^a   Filardo, Edward ^b   Milner, Teresa A ^c,d   Brake, Wayne G ^a  

^a Concordia University ^*  (Canada)

^b Radix Biosolutions ^*  (United States)

^c Department of Obstetrics Gynecology   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; G PROTEIN COUPLED RECEPTOR; GPR30 PROTEIN, RAT; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ANTIBODY LABELING; ARTICLE; ESTRADIOL BLOOD LEVEL; FEMALE; GLIA; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MEMORY; MITOCHONDRIAL MEMBRANE; NERVE ENDING; NONHUMAN; PREFRONTAL CORTEX; PROTEIN LOCALIZATION; RAT; SPRAGUE DAWLEY RAT; TISSUE FIXATION; TISSUE PREPARATION; ULTRASTRUCTURE ANALYSIS AND ELECTRON MICROSCOPY; ANIMAL; ANIMAL BEHAVIOR; CELL MEMBRANE; DRUG EFFECTS; MAZE TEST; METABOLISM; PHYSIOLOGY; TIME FACTOR; ULTRASTRUCTURE;

ANIMALS; BEHAVIOR, ANIMAL; CELL MEMBRANE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; TIME FACTORS;

EID: 84908043036     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1463     Document Type: Article

References (46)

1. Tolman EC, Ritchie BF, Kalish D. Studies in spatial learning: orientation and the short-cut. J Exp Psychol. 1946;36:13-24.
2. White NM, McDonald RJ. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem. 2002;77:125-184.
3. Korol DL. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol Learn Mem. 2004;82:309-323.
4. Hussain D, Hoehne A, Woodside B, Brake WG. Reproductive experience modifies the effects of estradiol on learning and memory bias in female rats. Horm Behav. 2013;63:418-423.
5. Korol DL, Kolo LL. Estrogen-induced changes in place and response learning in young adult female rats. Behav Neurosci. 2002;116:411-420.
6. Korol DL, Malin EL, Borden KA, Busby RA, Couper-Leo J. Shifts in preferred learning strategy across the estrous cycle in female rats. Horm Behav. 2004;45:330-338.
7. Quinlan MG, Almey A, Caissie M, LaChappelle I, Radiotis G, Brake WG. Estradiol and striatal dopamine receptor antagonism influence memory system bias in the female rat. Neurobiol Learn Mem. 2013;106:221-229.
8. Quinlan MG, Hussain D, Brake WG. Use of cognitive strategies in rats: the role of estradiol and its interaction with dopamine. Horm Behav. 2008;53:185-191.
9. Zurkovsky L, Serio SJ, Korol DL. Intra-striatal estradiol in female rats impairs response learning within two hours of treatment. Horm Behav. 2011;60:470-477.
10. Rich EL, Shapiro M. Rat prefrontal cortical neurons selectively code strategy switches. J Neurosci. 2009;29:7208-7219.
11. Funakoshi T, Yanai A, Shinoda K, Kawano MM, Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun. 2006;346:904-910.
12. Cardona-Gomez GP, DonCarlos L, Garcia-Segura LM. Insulin-like growth factor I receptors and estrogen receptors colocalize in female rat brain. Neuroscience. 2000;99:751-760.
13. Kritzer MF. Regional, laminar, and cellular distribution of immunoreactivity for ER α and ER β in the cerebral cortex of hormonally intact, adult male and female rats. Cereb Cortex. 2002;12:116-128.
14. Shughrue PJ, Merchenthaler I. Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J Comp Neurol. 2001;436:64-81.
15. Montague D, Weickert CS, Tomaskovic-Crook E, Rothmond DA, Kleinman JE, Rubinow DR. Oestrogen receptor α localisation in the prefrontal cortex of three mammalian species. J Neuroendocrinol. 2008;20:893-903.
16. Wang AC, Hara Y, Janssen WG, Rapp PR, Morrison JH. Synaptic estrogen receptor-α levels in prefrontal cortex in female rhesus monkeys and their correlation with cognitive performance. J Neurosci. 2010;30:12770-12776.
17. Mitra SW, Hoskin E, Yudkovitz J, et al. Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor α. Endocrinology. 2003;144:2055-2067.
18. Almey A, Filardo EJ, Milner TA, Brake WG. 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. 2012;153:5373-5383.
19. Zurkovsky L, Brown SL, Boyd SE, Fell JA, Korol DL. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience. 2007;144:26-37.
20. Klein R. Beyond Significance Testing: Reforming Data Analysis Methods in Behavioural Research. Washington DC: American Psychological Association; 2004.
21. Williams TJ, Torres-Reveron A, Chapleau JD, Milner TA. Hormonal regulation of delta opioid receptor immunoreactivity in interneurons and pyramidal cells in the rat hippocampus. Neurobiol Learn Mem. 2011;95:206-220.
22. 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. 1992;135:333-341.
23. Alves SE, Weiland NG, Hayashi S, McEwen BS. Immunocytochemical localization of nuclear estrogen receptors and progestin receptors within the rat dorsal raphe nucleus. J Comp Neurol. 1998;391:322-334.
24. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE. Ultrastructural evidence that hippocampal α estrogen receptors are located at extranuclear sites. J Comp Neurol. 2001;429:355-371.
25. Creutz LM, Kritzer MF. Estrogen receptor-β immunoreactivity in the midbrain of adult rats: regional, subregional, and cellular localization in the A10, A9, and A8 dopamine cell groups. J Comp Neurol. 2002;446:288-300.
26. Milner TA, Thompson LI, Wang G, et al. Distribution of estrogen receptor β containing cells in the brains of bacterial artificial chromosome transgenic mice. Brain Res. 2010;1351:74-96.
27. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005;307:1625-1630.
28. Hammond R, Gibbs RB. GPR30 is positioned to mediate estrogen effects on basal forebrain cholinergic neurons and cognitive performance. Brain Res. 2011;1379:53-60.
29. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr. 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. 2000;14:1649-1660.
30. Milner TA, Waters B, Robinson D, Pierce JP. Degenerating processes identified by electron microscopic immunocytochemical methods. Methods Mol Biol. 2011;793:23-59.
31. Peters A, Palay SL, Webster HD. The Fine Structure of the Nervous System. 3rd ed. New York: Oxford University Press; 1991.
32. Heidbreder CA, Groenewegen HJ. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev. 2003;27:555-579.
33. Dazzi L, Seu E, Cherchi G, Barbieri PP, Matzeu A, Biggio G. Estrous cycle-dependent changes in basal and ethanol-induced activity of cortical dopaminergic neurons in the rat. Neuropsychopharmacology. 2007;32:892-901.
34. Dupont A, Dussault JH, Rouleau D, et al. Effect of neonatal thyroid deficiency on the catecholamine, substance P, and thyrotropin-releasing hormone contents of discrete rat brain nuclei. Endocrinology. 1981;108:2039-2045.
35. Luine VN, Richards ST, Wu VY, Beck KD. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav. 1998;34:149-162.
36. Leranth C, Pickel VM. Electron microscopic preembedding double-immunostaining methods. In: Heimer I, Zaborsky I, eds. Neuroanatomical Tract Tracing Methods II: Recent Progress. New York: Plenum; 1989.
37. Matsuda K, Sakamoto H, Mori H, et al. Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci Lett. 2008;441:94-99.
38. Filardo EJ, Graeber CT, Quinn JA, et al. Distribution of GPR30, a seven membrane-spanning estrogen receptor, in primary breast cancer and its association with clinicopathologic determinants of tumor progression. Clin Cancer Res. 2006;12:6359-6366.
39. Filardo EJ, Thomas P. Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology. 2012;153:2953-2962.
40. Verdier D, Lund JP, Kolta A. GABAergic control of action potential propagation along axonal branches of mammalian sensory neurons. J Neurosci. 2003;23:2002-2007.
41. Cheung DW. Synaptic transmission in the guinea-pig vas deferens: the role of nerve action potentials. Neuroscience. 1990;37:127-134.
42. Arevalo MA, Santos-Galindo M, Bellini MJ, Azcoitia I, Garcia-Segura LM. Actions of estrogens on glial cells: implications for neuroprotection. Biochim Biophys Acta. 2010;1800:1106-1112.
43. Liu SB, Han J, Zhang N, Tian Z, Li XB, Zhao MG. Neuroprotective effects of oestrogen against oxidative toxicity through activation of G-protein-coupled receptor 30 receptor. Clin Exp Pharmacol Physiol. 2011;38:577-585.
44. Razmara A, Sunday L, Stirone C, et al. Mitochondrial effects of estrogen are mediated by estrogen receptor α in brain endothelial cells. J Pharmacol Exp Ther. 2008;325:782-790.
45. Araujo GW, Beyer C, Arnold S. Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J Neuroendocrinol. 2008;20:930-941.
46. Otto C, Rohde-Schulz B, Schwarz G, et al. G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology. 2008;149:4846-4856.