Biosynthesis, mode of action and functional significance of neurosteroids in the developing Purkinje cell

Journal of Steroid Biochemistry and Molecular Biology

Volumn 102, Issue 1-5 SPEC. ISS., 2006, Pages 187-194

  Tsutsui, Kazuyoshi ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Cerebellar development; Neuronal growth; Neurosteroids; Purkinje cell; Synaptogenesis

Indexed keywords

ANIMALS; HUMANS; NEURONS; PURKINJE CELLS; RECEPTORS, STEROID; STEROIDS;

MAMMALIA; VERTEBRATA;

EID: 33750987324     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2006.09.015     Document Type: Article

References (79)

1. Fuxe K., Gustafsson J.A., and Wetterberg L. Steroid Hormone Regulation of the Brain (1981), Pergamon Press, Oxford
2. Arnold A.P., and Gorski R.A. Gonadal steroid induction of structural sex differences in the CNS. Annu. Rev. Neurosci. 7 (1984) 413-442
3. McEwen B.S. Steroid hormones are multifunctional messengers in the brain. Trends Endocrinol. Metab. 2 (1991) 62-67
4. Baulieu E.E. Neurosteroids: of the nervous system, by the nervous system, for the nervous system (review). Rec. Progr. Hormone Res. 52 (1997) 1-32
5. Tsutsui K., Ukena K., Takase M., Kohchi C., and Lea R.W. Neurosteroid biosynthesis in vertebrate brains (review). Comp. Biochem. Physiol. C 124 (1999) 121-129
6. Tsutsui K., Ukena K., Usui M., Sakamoto H., and Takase M. Novel brain function: biosynthesis and actions of neurosteroids in neurons (review). Neurosci. Res. 36 (2000) 261-273
7. Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators (review). Front. Neuroendocrinol. 21 (2000) 1-56
8. Mellon S.H., and Vaudry H. Biosynthesis of neurosteroids and regulation of their synthesis (review). Int. Rev. Neurobiol. 46 (2001) 33-78
9. Corpéchot C., Robel P., Axelson M., Sjövall J., and Baulieu E.E. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 4704-4707
10. Corpéchot C., Synguelakis M., Talha S., Axelson M., Sjövall J., Vaihko R., Baulieu E.E., and Robel P. Pregnenolone and its sulfate ester in rat brain. Brain Res. 270 (1983) 119-125
11. 5-derivatives in the rodent brain. Neurochem. Int. 7 (1985) 953-958
12. Lanthier A., and Patwardhan V.V. Sex steroids and 5-en-3β-hydroxysteroids in specific regions of the human brain and cranial nerves. J. Steroid Biochem. 25 (1986) 445-449
13. 5-derivatives in the rat brain. In: Fink G., Harmar A.J., and McKerns K.W. (Eds). Neuroendocrine Molecular Biology (1986), Plenum Press, New York 367-377
14. 5-derivatives in rat and monkey brain. J. Steroid Biochem. 27 (1987) 649-655
15. Jo D.H., Abdallah M.A., Young J., Baulieu E.E., and Robel P. Pregnenolone, dehydroepiandrosterone, and their sulfate and fatty acid esters in the rat brain. Steroids 54 (1989) 287-297
16. Mathur C., Prasad V.V.K., Raju V.S., Welch M., and Lieberman S. Steroids and their conjugates in the mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 85-88
17. Mellon S.H., and Deschepper C.F. Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res. 629 (1993) 283-292
18. Compagnone N.A., Bulfone A., Rubenstein J.L.R., and Mellon S.H. Steroidogenic enzyme P450c17 is expressed in the embryonic central nervous system. Endocrinology 136 (1995) 5212-5223
19. Tsutsui K., and Yamazaki T. Avian neurosteroids. I. Pregnenolone biosynthesis in the quail brain. Brain Res. 678 (1995) 1-9
20. Usui M., Yamazaki T., Kominami S., and Tsutsui K. Avian neurosteroids. II. Localization of a cytochrome P450scc-like substance in the quail brain. Brain Res. 678 (1995) 10-20
21. Vanson A., Arnold A.P., and Schlinger B.A. 3β-Hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch telencephalon: dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen. Comp. Endocrinol. 102 (1996) 342-350
22. Tsutsui K., Yamazaki T., Usui M., Furukawa Y., Ukena K., Kohchi C., and Kominami S. P450scc activity in the brain. In: Harvey S., and Etches R.J. (Eds). Perspectives in Avian Endocrinology (1997), Journal of Endocrinol Ltd., Bristol 427-436
23. Tsutsui K., Usui M., Yamazaki T., Ukena K., and Kominami S. Neurosteroids in the avian brain. In: Maitra S.K. (Ed). Frontiers in Environmental and Metabolic Endocrinology (1997), Burdwan Press, Burdwan 151-159
24. 4-isomerase in different regions of the avian brain. Brain Res. 818 (1999) 536-542
25. Schlinger B.A., Lane N.I., Grisham W., and Thompson L. Androgen synthesis in a songbird: a study of cyp17 (17α-hydroxylase/c17,20-lyase) activity in the zebra finch. Gen. Comp. Endocrinol. 113 (1999) 46-58
26. Freking F., Nazairians T., and Schlinger B.A. The expression of the sex steroid-synthesizing enzymes CYP11A1, 3β-HSD, CYP17, and CYP 19 in gonads and adrenals of adult and developing zebra finches. Gen. Comp. Endocrinol. 119 (2000) 140-151
27. Ukena K., Honda Y., Lea R.W., and Tsutsui K. Developmental changes in progesterone biosynthesis and metabolism in the quail brain. Brain Res. 898 (2001) 190-194
28. Matsunaga M., Ukena K., and Tsutsui K. Expression and localization of cytochrome P450 17α-hydroxylase/c17, 20-lyase in the avian brain. Brain Res. 899 (2001) 112-122
29. Tsutsui K., and Schlinger B.A. Steroidogenesis in the avian brain. In: Dawson A., and Chaturvedi C.M. (Eds). Avian Endocrinology (2001), Narosa Publishing House, New Delhi 59-77
30. Matsunaga M., Ukena K., and Tsutsui K. Androgen biosynthesis in the quail brain. Brain Res. 948 (2002) 180-185
31. Soma K.K., Alday N.A., Hau M., and Schlinger B.A. DHEA metabolism by 3β-HSD in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145 (2003) 1668-1677
32. Tsutsui K., Matsunaga M., Ukena K., and Biosynthesis. biological actions of neurosteroids in the avian brain (review). Avian Poultry Biol. Rev. 14 (2003) 63-78
33. Mensah-Nyagan A.G., Feuilloley M., Dupont E., Do-Rego J.L., Leboulenger F., Pelletier G., and Vaudry H. Immunocytochemical localization and biological activity of 3β-hydroxysteroid dehydrogenase in the central nervous system of the frog. J. Neurosci. 14 (1994) 7306-7318
34. Mensah-Nyagan A.G., Feuilloley M., Do-Rego J.L., Marcual A., Lange C., Tonon M.C., Pelletier G., and Vaudry H. Localization of 17β-hydroxysteroid dehydrogenase and characterization of testosterone in the brain of the male frog. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 1423-1428
35. Mensah-Nyagan A.G., Do-Rego J.L., Feuilloley M., Marcual A., Lange C., Pelletier G., and Vaudry H. In vivo and in vitro evidence for the biosynthesis of testosterone in the telencephalon of the female frog. J. Neurochem. 67 (1996) 413-422
36. Takase M., Ukena K., Yamazaki T., Kominami S., and Tsutsui K. Pregnenolone, pregnenolone sulfate and cytochrome P450 side-chain cleavage enzyme in the amphibian brain and their seasonal changes. Endocrinology 140 (1999) 1936-1944
37. Inai Y., Nagai K., Ukena K., Oishi T., and Tsutsui K. Seasonal changes in neurosteroids in the urodele brain and environmental factors inducing their changes. Brain Res. 959 (2003) 214-225
38. Matsunaga M., Ukena K., Baulieu E.E., and Tsutsui K. 7α-Hydroxypregnenolone acts as a neuronal activator to stimulate locomotor activity of breeding newts by means of the dopaminergic system. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 17282-17287
39. Mensah-Nyagan A.G., Do-Rego J.L., Beaujean D., Luu-The V., Pelletier G., and Vaudry H. Neurosteroids: expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system (review). Pharmacol. Rev. 51 (1999) 63-81
40. Mensah-Nyagan A.G., Beaujean D., Luu-The V., Pelletier G., and Vaudry H. Anatomical and biochemical evidence for the synthesis of unconjugated and sulfated neurosteroids in amphibians (review). Brain Res. Rev. 37 (2001) 13-24
41. 4-isomerase in the zebrafish central nervous system. J. Comp. Neurol. 439 (2001) 291-305
42. Ukena K., Usui M., Kohchi C., and Tsutsui K. Cytochrome P450 side-chain cleavage enzyme in the cerebellar Purkinje neuron and its neonatal change in rats. Endocrinology 139 (1998) 137-147
43. 4-isomerase in the rat Purkinje neuron during neonatal life. Endocrinology 140 (1999) 805-813
44. Sakamoto H., Mezaki Y., Shikimi H., Ukena K., and Tsutsui K. Dendritic growth and spine formation in response to estrogen in the developing Purkinje cell. Endocrinology 144 (2003) 4466-4477
45. Furukawa A., Miyatake A., Ohnishi T., and Ichikawa Y. Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of StAR, cytochrome P-450scc (CYP XIA1), and 3β-hydroxysteroid dehydrogenase in the rat brain. J. Neurochem. 71 (1998) 2231-2238
46. Sierra A. Neurosteroids: the StAR protein in the brain. J. Neuroendocrinol. 16 (2004) 787-793
47. Lavaque E., Sierra A., Azcoitia I., and Garcia-Segura L.M. Steroidogenic acute regulatory protein in the brain. Neuroscience 138 (2006) 741-747
48. Tsutsui K., Sakamoto H., and Ukena K. Biosynthesis and action of neurosteroids in the cerebellar Purkinje neuron. J. Steroid Biochem. Mol. Biol. 85 (2003) 311-321
49. Clark B.J., Wells J., King S.R., and Stocco D.M. The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 269 (1994) 28314-28322
50. Stocco D.M., and Clark B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17 (1996) 221-244
51. Mason J.I. The 3β-hydroxysteroid dehydrogenase gene family of enzymes. Trends Endocrinol. Metab. 4 (1993) 199-203
52. Kohchi C., Ukena K., and Tsutsui K. Age- and region-specific expressions of the messenger RNAs encoding for steroidogenic enzymes P450scc, P450c17 and 3β-HSD in the postnatal rat brain. Brain Res. 801 (1998) 233-238
53. Tsutsui K., and Ukena K. Neurosteroids in the cerebellar Purkinje neuron and their actions (review). Int. J. Mol. Med. 4 (1999) 49-56
54. Tsutsui K., Ukena K., and Sakamoto H. A novel aspect of the cerebellum: biosynthesis of neurosteroids in the Purkinje cell (review). Cerebellum 2 (2003) 215-222
55. Tsutsui K., Sakamoto H., Shikimi H., and Ukena K. Organizing actions of neurosteroids in the Purkinje neuron (review). Neurosci. Res. 49 (2004) 273-279
56. Kimoto T., Tsurugizawa T., Ohta Y., Makino J., Tamura H., Hojo Y., Takata N., and Kawato S. Neurosteroid synthesis by cytochrome p450-containing systems localized in the rat brain hippocampal neurons: N-methyl-d-aspartate and calcium-dependent synthesis. Endocrinology 142 (2001) 3578-3589
57. Hojo Y., Hattori T.A., Enami T., Furukawa A., Suzuki K., Ishii H.T., Mukai H., Morrison J.H., Janssen W.G., Kominami S., Harada N., Kimoto T., and Kawato S. 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 (2004) 865-870
58. Guarneri P., Guarneri R., Cascio C., Pavasant P., Piccoli F., and Papadopoulos V. Neurosteroidogenesis in rat retinas. J. Neurochem. 63 (1994) 86-96
59. Altman J. Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J. Comp. Neurol. 145 (1972) 353-397
60. Altman J. Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol. 145 (1972) 399-463
61. Sakamoto H., Ukena K., and Tsutsui K. Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis. J. Neurosci. 21 (2001) 6221-6232
62. Sakamoto H., Ukena K., and Tsutsui K. Dendritic spine formation in response to progesterone synthesized de novo in the developing Purkinje cell in rats. Neurosci. Lett. 322 (2002) 111-115
63. Sakamoto H., Shikimi H., Ukena K., and Tsutsui K. Neonatal expression of progesterone receptor isoforms in the cerebellar Purkinje cell in rats. Neurosci. Lett. 343 (2003) 163-166
64. Sakamoto H., Ukena K., Takemori H., Okamoto M., Kawata M., and Tsutsui K. Expression and localization of 25-Dx, a membrane-associated putative progesterone-binding protein, in the developing Purkinje cell. Neuroscience 126 (2004) 325-334
65. Price R.H., and Handa R.J. Expression of estrogen receptor-β protein and mRNA in the cerebellum of the rat. Neurosci. Lett. 288 (2000) 115-118
66. Orikasa C., Kondo Y., Hayashi S., McEwen B.S., and Sakuma Y. Sexually dimorphic expression of estrogen receptor beta in the anteroventral periventricular nucleus of the rat preoptic area: implication in luteinizing hormone surge. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3306-3309
67. Ikeda Y., Nagai A., Ikeda M.A., and Hayashi S. Sexually dimorphic and estrogen-dependent expression of estrogen receptor beta in the ventromedial hypothalamus during rat postnatal development. Endocrinology 144 (2003) 5098-5115
68. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10 (1990) 1286-1291
69. Woolley C.S., Gould E., Frankfurt M., and McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10 (1990) 4035-4039
70. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12 (1992) 2549-2554
71. Woolley C.S., and McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 14 (1994) 7680-7687
72. McEwen B.S., Akama K., Alves S., Brake W.G., Bulloch K., Lee S., Li C., Yuen G., and Milner T.A. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation (review). Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 7093-7100
73. Murphy D.D., and Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J. Neurosci. 16 (1996) 4059-4068
74. Pérez J., Luquín S., Naftolin F., and García-Segura L.M. The role of estradiol and progesterone in phased synaptic remodelling of the rat arcuate nucleus. Brain Res. 608 (1993) 38-44
75. Langub M.C., Maley B.E., and Watson R.E. Estrous cycle-associated axosomatic synaptic plasticity upon estrogen receptive neurons in the rat preoptic area. Brain Res. 641 (1994) 303-310
76. Rocamora N., Garcia-Ladona F.J., Palacios J.M., and Mengod G. Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and low-affinity nerve growth factor receptor during the postnatal development of the rat cerebellar system. Mol. Brain. Res. 17 (1993) 1-8
77. Ernfors P., Lee K.F., and Jaenisch R. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368 (1994) 147-150
78. Schwartz P.M., Borghesani P.R., Levy R.L., Pomeroy S.L., and Segal R.A. Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning. Neuron 19 (1997) 269-281
79. Bates B., Rios M., Trumpp A., Chen C., Fan G., Bishop J.M., and Jaenisch R. Neurotrophin-3 is required for proper cerebellar development. Nat. Neurosci. 2 (1999) 115-117