Endogenous synthesis of corticosteroids in the Hippocampus

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Higo, Shimpei ^a   Hojo, Yasushi ^a   Ishii, Hirotaka ^a   Komatsuzaki, Yoshimasa ^a,b   Ooishi, Yuuki ^a   Murakami, Gen ^a   Mukai, Hideo ^a   Yamazaki, Takeshi ^c   Nakahara, Daiichiro ^d   Barron, Anna ^a   Kimoto, Tetsuya ^a   Kawato, Suguru ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

^d HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CORTICOSTEROID; CYTOCHROME P450; CYTOCHROME P450 11 BETA 1; CYTOCHROME P450 2D; CYTOCHROME P450 2D4; DEOXYCORTICOSTERONE; MESSENGER RNA; PROGESTERONE; STEROID 21 MONOOXYGENASE; UNCLASSIFIED DRUG; CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME METABOLISM; HIPPOCAMPUS; HORMONE SYNTHESIS; IMMUNOGOLD ELECTRON MICROSCOPY; IN SITU HYBRIDIZATION; LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; RNA ANALYSIS; TANDEM MASS SPECTROMETRY; ANIMAL; CYTOLOGY; GENETICS; IMMUNOELECTRON MICROSCOPY; MASS SPECTROMETRY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; WISTAR RAT;

RATTUS;

ANIMALS; BLOTTING, SOUTHERN; CHROMATOGRAPHY, LIQUID; CORTICOSTERONE; CYTOCHROME P-450 ENZYME SYSTEM; DESOXYCORTICOSTERONE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICROSCOPY, IMMUNOELECTRON; PROGESTERONE; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 79960884151     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021631     Document Type: Article

References (46)

1. McEwen BS, De Kloet ER, Rostene W, (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66: 1121-1188.
2. Reul JM, de Kloet ER, (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117: 2505-2511.
3. Gomez-Sanchez EP, Ahmad N, Romero DG, Gomez-Sanchez CE, (2005) Is aldosterone synthesized within the rat brain? Am J Physiol Endocrinol Metab 288: E342-346.
4. Furukawa A, Miyatake A, Ohnishi T, Ichikawa Y, (1998) Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of StAR, cytochrome P-450SCC (CYP XIA1), and 3beta-hydroxysteroid dehydrogenase in the rat brain. J Neurochem 71: 2231-2238.
5. Gomez-Sanchez CE, Zhou MY, Cozza EN, Morita H, Eddleman FC, et al. (1996) Corticosteroid synthesis in the central nervous system. Endocr Res 22: 463-470.
6. Gomez-Sanchez CE, Zhou MY, Cozza EN, Morita H, Foecking MF, et al. (1997) Aldosterone biosynthesis in the rat brain. Endocrinology 138: 3369-3373.
7. Ibanez C, Guennoun R, Liere P, Eychenne B, Pianos A, et al. (2003) Developmental expression of genes involved in neurosteroidogenesis: 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase in the rat brain. Endocrinology 144: 2902-2911.
8. Kawato S, Hojo Y, Kimoto T, (2002) Histological and metabolism analysis of P450 expression in the brain. Methods Enzymol 357: 241-249.
9. Kimoto T, Tsurugizawa T, Ohta Y, Makino J, Tamura H, et al. (2001) Neurosteroid synthesis by cytochrome p450-containing systems localized in the rat brain hippocampal neurons: N-methyl-D-aspartate and calcium-dependent synthesis. Endocrinology 142: 3578-3589.
10. MacKenzie SM, Clark CJ, Fraser R, Gomez-Sanchez CE, Connell JM, et al. (2000) Expression of 11beta-hydroxylase and aldosterone synthase genes in the rat brain. J Mol Endocrinol 24: 321-328.
11. Do Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, et al. (2009) Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol 30: 259-301.
12. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, et al. (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.
13. Kimoto T, Ishii H, Higo S, Hojo Y, Kawato S, (2010) Semicomprehensive analysis of the postnatal age-related changes in the mRNA expression of sex steroidogenic enzymes and sex steroid receptors in the male rat hippocampus. Endocrinology 151: 5795-5806.
14. Mukai H, Kimoto T, Hojo Y, Kawato S, Murakami G, et al. (2010) Modulation of synaptic plasticity by brain estrogen in the hippocampus. Biochim Biophys Acta 1800: 1030-1044.
15. Davies E, MacKenzie SM, (2003) Extra-adrenal production of corticosteroids. Clin Exp Pharmacol Physiol 30: 437-445.
16. Kishimoto W, Hiroi T, Shiraishi M, Osada M, Imaoka S, et al. (2004) Cytochrome P450 2D catalyze steroid 21-hydroxylation in the brain. Endocrinology 145: 699-705.
17. Hiroi T, Kishimoto W, Chow T, Imaoka S, Igarashi T, et al. (2001) Progesterone oxidation by cytochrome P450 2D isoforms in the brain. Endocrinology 142: 3901-3908.
18. Hojo Y, Higo S, Ishii H, Ooishi Y, Mukai H, et al. (2009) Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology 150: 5106-5112.
19. Stromstedt M, Waterman MR, (1995) Messenger RNAs encoding steroidogenic enzymes are expressed in rodent brain. Brain Res Mol Brain Res 34: 75-88.
20. Beyenburg S, Watzka M, Clusmann H, Blumcke I, Bidlingmaier F, et al. (2001) Messenger RNA of steroid 21-hydroxylase (CYP21) is expressed in the human hippocampus. Neurosci Lett 308: 111-114.
21. Ye P, Kenyon CJ, Mackenzie SM, Nichol K, Seckl JR, et al. (2008) Effects of ACTH, dexamethasone, and adrenalectomy on 11beta-hydroxylase (CYP11B1) and aldosterone synthase (CYP11B2) gene expression in the rat central nervous system. J Endocrinol 196: 305-311.
22. Sapolsky RM, Krey LC, McEwen BS, (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 5: 1222-1227.
23. Woolley CS, Gould E, McEwen BS, (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531: 225-231.
24. Revest JM, Di Blasi F, Kitchener P, Rouge-Pont F, Desmedt A, et al. (2005) The MAPK pathway and Egr-1 mediate stress-related behavioral effects of glucocorticoids. Nat Neurosci 8: 664-672.
25. Diamond DM, Bennett MC, Fleshner M, Rose GM, (1992) Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2: 421-430.
26. Reiheld CT, Teyler TJ, Vardaris RM, (1984) Effects of corticosterone on the electrophysiology of hippocampal CA1 pyramidal cells in vitro. Brain Res Bull 12: 349-353.
27. Hassan AH, von Rosenstiel P, Patchev VK, Holsboer F, Almeida OF, (1996) Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone. Exp Neurol 140: 43-52.
28. Breuner CW, Orchinik M, (2002) Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol 175: 99-112.
29. Windle RJ, Brady MM, Kunanandam T, Da Costa AP, Wilson BC, et al. (1997) Reduced response of the hypothalamo-pituitary-adrenal axis to alpha1-agonist stimulation during lactation. Endocrinology 138: 3741-3748.
30. Hojo Y, Murakami G, Mukai H, Higo S, Hatanaka Y, et al. (2008) Estrogen synthesis in the brain--role in synaptic plasticity and memory. Mol Cell Endocrinol 290: 31-43.
31. Higo S, Hojo Y, Ishii H, Kominami T, Nakajima K, et al. (2009) Comparison of sex-steroid synthesis between neonatal and adult rat hippocampus. Biochem Biophys Res Commun 385: 62-66.
32. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, et al. (2002) Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 22: 3608-3614.
33. Doody KM, Carr BR, Rainey WE, Byrd W, Murry BA, et al. (1990) 3 beta-hydroxysteroid dehydrogenase/isomerase in the fetal zone and neocortex of the human fetal adrenal gland. Endocrinology 126: 2487-2492.
34. Shinzawa K, Ishibashi S, Murakoshi M, Watanabe K, Kominami S, et al. (1988) Relationship between zonal distribution of microsomal cytochrome P-450s (P-450(17)alpha,lyase and P-450C21) and steroidogenic activities in guinea-pig adrenal cortex. J Endocrinol 119: 191-200.
35. Ogishima T, Suzuki H, Hata J, Mitani F, Ishimura Y, (1992) Zone-specific expression of aldosterone synthase cytochrome P-450 and cytochrome P-45011 beta in rat adrenal cortex: histochemical basis for the functional zonation. Endocrinology 130: 2971-2977.
36. Ishida A, Mutoh T, Ueyama T, Bando H, Masubuchi S, et al. (2005) Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab 2: 297-307.
37. Nakahara D, Nakamura M, Iigo M, Okamura H, (2003) Bimodal circadian secretion of melatonin from the pineal gland in a living CBA mouse. Proc Natl Acad Sci U S A 100: 9584-9589.
38. Komatsuzaki Y, Murakami G, Tsurugizawa T, Mukai H, Tanabe N, et al. (2005) Rapid spinogenesis of pyramidal neurons induced by activation of glucocorticoid receptors in adult male rat hippocampus. Biochem Biophys Res Commun 335: 1002-1007.
39. Mukai H, Tsurugizawa T, Ogiue-Ikeda M, Murakami G, Hojo Y, et al. (2006) Local neurosteroid production in the hippocampus: influence on synaptic plasticity of memory. Neuroendocrinology 84: 255-263.
40. Tsurugizawa T, Mukai H, Tanabe N, Murakami G, Hojo Y, 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.
41. Mukai H, Hatanaka Y, Mitsuhashi K, Hojo Y, Komatsuzaki Y, et al. (2011) Automated analysis of spines from confocal laser microscopy images: application to the discrimination of androgen and estrogen effects on spinogenesis. Cerebral Cortex in press.
42. Gago N, Akwa Y, Sananes N, Guennoun R, Baulieu EE, et al. (2001) Progesterone and the oligodendroglial lineage: stage-dependent biosynthesis and metabolism. Glia 36: 295-308.
43. Guennoun R, Schumacher M, Robert F, Delespierre B, Gouezou M, et al. (1997) Neurosteroids: expression of functional 3beta-hydroxysteroid dehydrogenase by rat sensory neurons and Schwann cells. Eur J Neurosci 9: 2236-2247.
44. Pelletier G, Luu-The V, Li S, Labrie F, (2004) Localization of 20alpha-hydroxysteroid dehydrogenase mRNA in mouse brain by in situ hybridization. Brain Res Mol Brain Res 125: 143-146.
45. Stapleton G, Steel M, Richardson M, Mason JO, Rose KA, et al. (1995) A novel cytochrome P450 expressed primarily in brain. J Biol Chem 270: 29739-29745.
46. Shinohara Y, Hirase H, Watanabe M, Itakura M, Takahashi M, et al. (2008) Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc Natl Acad Sci U S A 105: 19498-19503.