Corticosterone rapidly increases thorns of CA3 neurons via synaptic/extranuclear glucocorticoid receptor in rat hippocampus

Frontiers in Neural Circuits

Volumn 7, Issue NOV, 2013, Pages

  Yoshiya, Miyuki ^a   Komatsuzaki, Yoshimasa ^a,b   Hojo, Yasushi ^a   Ikeda, Muneki ^a   Mukai, Hideo ^a   Hatanaka, Yusuke ^a   Murakami, Gen ^a   Kawata, Mitsuhiro ^c   Kimoto, Tetsuya ^a   Kawato, Suguru ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Corticosterone; Hippocampus; Kinase; Spine; Stress; Thorn

Indexed keywords

AMPA RECEPTOR; CORTICOSTERONE; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOCORTICOID RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; LUCIFER YELLOW; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C; HORMONE ANTAGONIST; PHOSPHOTRANSFERASE;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CELL ACTIVATION; CELL DENSITY; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME INHIBITION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; HORMONE ACTION; INTRACELLULAR SIGNALING; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RECEPTOR BLOCKING; SYNAPSE; ANIMAL; DENDRITIC SPINE; DRUG ANTAGONISM; DRUG EFFECT; HIPPOCAMPUS; METABOLISM; NERVE CELL; SPINE; STRESS; THORN; WISTAR RAT; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS;

CORTICOSTERONE; HIPPOCAMPUS; KINASE; SPINE; STRESS; THORN;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CORTICOSTERONE; DENDRITIC SPINES; HORMONE ANTAGONISTS; MALE; MIFEPRISTONE; NEURONS; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; SYNAPSES;

EID: 84888613378     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00191     Document Type: Article

References (56)

1. Adams, J. P., Roberson, E. D., English, J. D., Selcher, J. C., and Sweatt, J. D. (2000). MAPK regulation of gene expression in the central nervous system. Acta Neurobiol. Exp. (Wars.) 60, 377-394.
2. Alfarez, D. N., De Simoni, A., Velzing, E. H., Bracey, E., Joels, M., Edwards, F. A., et al. (2009). Corticosterone reduces dendritic complexity in developing hippocampal CA1 neurons. Hippocampus 19, 828-836. doi: 10.1002/hipo.20566
3. Alonso, M., Medina, J. H., and Pozzo-Miller, L. (2004). ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn. Mem. 11,172-178. doi: 10.1101/lm.67804
4. Amaral, D. G., and Dent, J. A. (1981). Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 195, 51-86. doi: 10.1002/cne.901950106
5. Baude, A., Nusser, Z., Molnar, E., Mcilhinney, R. A., and Somogyi, P. (1995). High- resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69, 1031-1055. doi: 10.1016/0306-4522(95)00350-R
6. Bhat, R., Xue, Y., Berg, S., Hellberg, S., Ormo, M., Nilsson, Y., et al. (2003). Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem. 278,45937-45945. doi: 10.1074/jbc.M306268200
7. Birnbaum, S. G., Yuan, P. X., Wang, M., Vijayraghavan, S., Bloom, A. K., Davis, D. J., et al. (2004). Protein kinase C overactivity impairs prefrontal cortical regulation of working memory. Science 306, 882-884. doi: 10.1126/science.1100021
8. Breuner, C. W., and Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175, 99-112. doi: 10.1677/joe.0.1750099
9. Campbell, D. H., Sutherland, R. L., and Daly, R. J. (1999). Signaling pathways and structural domains required for phosphorylation of EMS1/cortactin. CancerRes. 59, 5376-5385.
10. Chen, Y., Dube, C. M., Rice, C. J., and Baram, T. Z. (2008). Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin- releasing hormone. J. Neurosci. 28, 2903-2911. doi: 10.1523/JNEUROSCI.0225- 08.2008
11. Chen, Q., Zhou, Z., Zhang, L., Wang, Y., Zhang, Y. W., Zhong, M., et al. (2012). Tau protein is involved in morphological plasticity in hippocampal neurons in response to BDNF. Neurochem. Int. 60, 233-242. doi: 10.1016/j.neuint.2011.12.013
12. Chicurel, M. E., and Harris, K. M. (1992). Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J. Comp. Neurol. 325, 169-182. doi: 10.1002/cne.903250204
13. Chijiwa, T., Mishima, A., Hagiwara, M., Sano, M., Hayashi, K., Inoue, T., et al. (1990). Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265, 5267-5272.
14. Daly, R. J. (2004). Cortactin signalling and dynamic actin networks. Biochem. J. 382, 13-25. doi: 10.1042/BJ20040737
15. Diamond, D. M., Bennett, M. C., Fleshner, M., and Rose, G. M. (1992). Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2, 421-430. doi: 10.1002/hipo.450020409
16. Duan, H., Wearne, S. L., Morrison, J. H., and Hof, P. R. (2002). Quantitative analysis of the dendritic morphology of corticocortical projection neurons in the macaque monkey association cortex. Neuroscience 114, 349-359. doi: 10.1016/S0306-4522(02)00305-6
17. Dudley, D. T., Pang, L., Decker, S. J., Bridges, A. J., and Saltiel, A. R. (1995). A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. U.S.A. 92,7686-7689. doi: 10.1073/pnas.92.17.7686
18. Fritschy, J. M., Meskenaite, V., Weinmann, O., Honer, M., Benke, D., and Mohler, H. (1999). GABAB-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization. Eur. J. Neurosci. 11, 761-768. doi: 10.1046/j.1460-9568.1999.00481.x
19. Gould, E., Woolley, C. S., Frankfurt, M., and Mcewen, B. S. (1990). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10, 1286-1291.
20. Hammond, R. S., Lin, L., Sidorov, M. S., Wikenheiser, A. M., and Hoffman, D. A. (2008). Protein kinaseamediates activity-dependent Kv4.2 channel trafficking. J. Neurosci. 28, 7513-7519. doi: 10.1523/JNEUROSCI.1951-08.2008
21. Hatanaka, Y., Mukai, H., Mitsuhashi, K., Hojo, Y., Murakami, G., Komatsuzaki, Y., et al. (2009). Androgen rapidly increases dendritic thorns of CA3 neurons in male rat hippocampus. Biochem. Biophys. Res. Commun. 381, 728-732. doi: 10.1016/j.bbrc.2009.02.130
22. Herbert, J. M., Augereau, J. M., Gleye, J., and Maffrand, J. P. (1990). Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 172,993-999. doi: 10.1016/0006-291X(90)91544-3
23. Hering, H., and Sheng, M. (2003). Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J. Neurosci. 23, 11759-11769.
24. Higo, S., Hojo, Y., Ishii, H., Komatsuzaki, Y., Ooishi, Y., Murakami, G., et al. (2011). Endogenous synthesis of corticosteroids in the hippocampus. PLoS ONE 6:e21631. doi: 10.1371/journal.pone.0021631
25. Hojo, Y., Hattori, T. A., Enami, T., Furukawa, A., Suzuki, K., Ishii, H. T., etal. (2004). Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. U.S.A. 101,865-870. doi: 10.1073/pnas.2630225100
26. Hojo, Y., Higo, S., Ishii, H., Ooishi, Y., Mukai, H., Murakami, G., et al. (2009). Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology 150, 5106-5112. doi: 10.1210/en.2009-0305
27. Hojo, Y., Higo, S., Kawato, S., Hatanaka, Y., Ooishi, Y., Murakami, G., et al. (2011). Hippocampal synthesis of sex steroids and corticosteroids: essential for modulation of synaptic plasticity. Front. Endocrinol. 2:43. doi: 10.3389/fendo.2011.00043
28. Karst, H., Karten, Y. J., Reichardt, H. M., De Kloet, E. R., Schutz, G., and Joels, M. (2000). Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers. Nat. Neurosci. 3, 977-978. doi: 10.1038/79910
29. Komatsuzaki, Y., Hatanaka, Y., Murakami, G., Mukai, H., Hojo, Y., Saito, M., et al. (2012). Corticosterone induces rapid spinogenesis via synaptic glucocorticoid receptors and kinase networks in hippocampus. PLoS ONE 7:e34124. doi: 10.1371/journal.pone.0034124
30. Komatsuzaki, Y., Murakami, G., Tsurugizawa, T., Mukai, H., Tanabe, N., Mitsuhashi, K., et al. (2005). Rapid spinogenesis of pyramidal neurons induced byactivation of glucocorticoid receptors in adult male rat hippocampus. Biochem. Biophys. Res. Commun. 335,1002-1007. doi: 10.1016/j.bbrc.2005.07.173
31. Lupien, S. J., and McEwen, B. S. (1997). The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res. Brain Res. Rev. 24, 1-27. doi: 10.1016/S0165-0173(97)00004-0
32. MacQueen, G. M., Campbell, S., Mcewen, B. S., Macdonald, K., Amano, S., Joffe, R. T., et al. (2003). Course of illness, hippocampal function, and hippocampal volume in major depression. Proc. Natl. Acad. Sci. U.S.A. 100, 1387-1392. doi: 10.1073/pnas.0337481100
33. McNaughton, B. L., and Morris, R. G. M. (1987). Hippocampal synaptic enhancement and information-storage within a distributed memory system. Trends Neurosci. 10, 408-415. doi: 10.1016/0166-2236(87)90011-7
34. Monaghan, D. T., Holets, V. R., Toy, D. W., and Cotman, C. W. (1983). Anatomical distributions of four pharmacologically distinct 3H-L-glutamate binding sites. Nature 306,176-179. doi: 10.1038/306176a0
35. Morimoto, M., Morita, N., Ozawa, H., Yokoyama, K., and Kawata, M. (1996). Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci. Res. 26, 235-269. doi: 10.1016/S0168-0102(96)01105-4
36. Morris, R. G., Garrud, P., Rawlins, J. N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683. doi: 10.1038/297681a0
37. Mukai, H., Hatanaka, Y., Mitsuhashi, K., Hojo, Y., Komatsuzaki, Y., Sato, R., et al. (2011). Automated analysis of spines from confocal laser microscopy images: application to the discrimination of androgen and estrogen effects on spinogenesis. Cereb. Cortex 21, 2704-2711. doi: 10.1093/cercor/ bhr059
38. Mukai, H., Tsurugizawa, T., Murakami, G., Kominami, S., Ishii, H., Ogiue-Ikeda, M., et al. (2007). Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J. Neurochem. 100, 950-967. doi: 10.1111/j.1471-4159.2006.04264.x
39. Ooishi, Y., Kawato, S., Hojo, Y., Hatanaka, Y., Higo, S., Mukai, H., et al. (2012a). Modulation of synaptic plasticityin the hippocampus byhippocampus- derived estrogen and androgen. J. Steroid Biochem. Mol. Biol. 131, 37-51. doi: 10.1016/j.jsbmb.2011.10.004
40. Ooishi, Y., Mukai, H., Hojo, Y., Murakami, G., Hasegawa, Y., Shindo, T., et al. (2012b). Estradiol rapidly rescues synaptic transmission from corticosterone- induced suppression via synaptic/extranuclear steroidreceptors in the hippocampus. Cereb. Cortex 22, 926-936. doi: 10.1093/cercor/bhr164
41. Pardridge, W. M., and Mietus, L. J. (1979). Transport of steroid hormones through the rat blood-brain barrier. Primary role of albumin-bound hormone. J. Clin. Invest. 64, 145-154. doi: 10.1172/JCI109433
42. Reagan, L. P., andMcEwen, B. S. (1997). Controversies surrounding glucocorticoid- mediated cell death in the hippocampus. J. Chem. Neuroanat. 13, 149-167. doi: 10.1016/S0891-0618(97)00031-8
43. Reid, C. A. (2002). The role of dendritic spines: comparing the complex with the simple. Eur. J. Pharmacol. 447, 173-176. doi: 10.1016/S0014-2999(02) 01841-1
44. Reid, C. A., Fabian-Fine, R., and Fine, A. (2001). Postsynaptic calcium transients evoked by activation of individual hippocampal mossy fiber synapses. J. Neurosci. 21,2206-2214.
45. Revest, J. M., Di Blasi, F., Kitchener, P., Rouge-Pont, F., Desmedt, A., Turiault, M., et al. (2005). The MAPK pathway and Egr-1 mediate stress-related behavioral effects of glucocorticoids. Nat. Neurosci. 8, 664-672. doi: 10.1038/nn1441
46. Roberson, E. D., English, J. D., Adams, J. P., Selcher, J. C., Kondratick, C., and Sweatt, J. D. (1999). The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci. 19, 4337-4348.
47. Roozendaal, B., Quirarte, G. L., and Mcgaugh, J. L. (2002). Glucocorticoids interact with the basolateral amygdala beta-adrenoceptor - cAMP/cAMP/PKA system in influencing memory consolidation. Eur. J. Neurosci. 15, 553-560. doi: 10.1046/j.0953-816x.2001.01876.x
48. Sato, S., Osanai, H., Monma, T., Harada, T., Hirano, A., Saito, M., et al. (2004). Acute effect of corticosterone on N-methyl-D-aspartate receptor-mediated Ca2+ elevation in mouse hippocampal slices. Biochem. Biophys. Res. Commun. 321, 510-513. doi: 10.1016/j.bbrc.2004.06.168
49. Shibuya, K., Takata, N., Hojo, Y., Furukawa, A., Yasumatsu, N., Kimoto, T., et al. (2003). Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim. Biophys. Acta 1619, 301-316. doi: 10.1016/S0304-4165(02)00489-0
50. Sorrells, S. F., Caso, J. R., Munhoz, C. D., and Sapolsky, R. M. (2009). The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64, 33-39. doi: 10.1016/j.neuron.2009.09.032
51. Stewart, M. G., Davies, H. A., Sandi, C., Kraev, I. V., Rogachevsky, V. V., Peddie, C. J., et al. (2005). Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 131, 43-54. doi: 10.1016/j.neuroscience.2004.10.031
52. Tsurugizawa, T., Mukai, H., Tanabe, N., Murakami, G., Hojo, Y., Kominami, S., et al. (2005). Estrogen induces rapid decrease in dendritic thorns of CA3 pyramidal neurons in adult male rat hippocampus. Biochem. Biophys. Res. Commun. 337, 1345-1352. doi: 10.1016/j.bbrc.2005.09.188
53. Watanabe, Y., Gould, E., and Mcewen, B. S. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588, 341-345. doi: 10.1016/0006-8993(92)91597-8
54. Weed, S. A., Du, Y., and Parsons, J. T. (1998). Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1. J. Cell Sci. 111(Pt 16), 2433-2443.
55. Woolley, C. S., Gould, E., Frankfurt, M., and McEwen, B. S. (1990a). Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10, 4035-4039.
56. Woolley, C. S., Gould, E., and McEwen, B. S. (1990b). Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531, 225-231. doi: 10.1016/0006-8993(90) 90778-A