Discovery of a novel avian neurosteroid, 7α-hydroxypregnenolone, and its role in the regulation of the diurnal rhythm of locomotor activity in Japanese quail

General and Comparative Endocrinology

Volumn 163, Issue 1-2, 2009, Pages 117-122

  Tsutsui, Kazuyoshi ^a   Inoue, Kazuhiko ^a,b   Miyabara, Hitomi ^b   Suzuki, Saori ^b   Ogura, Yuki ^a   Tobari, Yasuko ^a   Haraguchi, Shogo ^a  

^a WASEDA UNIVERSITY   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

7 Hydroxypregnenolone; Diurnal changes; Locomotor activity; Melatonin; Neurosteroids; Quail brain

Indexed keywords

7ALPHA HYDROXYPREGNENOLONE; 7BETA HYDROXYPREGNENOLONE; ESTRADIOL; MELATONIN; NEUROSTEROID; PREGNENOLONE; PROGESTERONE; TESTOSTERONE; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG;

ARTICLE; CIRCADIAN RHYTHM; DIENCEPHALON; HORMONE ACTION; HORMONE RELEASE; HORMONE SYNTHESIS; LOCOMOTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUAIL; STEROIDOGENESIS;

EID: 67649831421     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2009.04.005     Document Type: Article

References (64)

1. Akwa Y., Morfin R.F., Robel P., and Baulieu E.-E. Neurosteroid metabolism: 7α-hydroxylation of dehydroepiandrosterone and pregnenolone by rat brain microsomes. Biochem. J. 288 (1992) 959-964
2. Balthazart J., Foidart A., and Harada N. Immunocytochemical localization of aromatase in the brain. Brain Res. 514 (1990) 327-333
3. Balthazart J., Foidart A., Surlemont C., Vockel A., and Harada N. Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: an immunocytochemical study. J. Comp. Neurol. 301 (1990) 276-288
4. Baulieu E.-E. Neurosteroids: of the nervous system, by the nervous system, for the nervous system. Recent Prog. Horm. Res. 52 (1997) 1-32
5. Binkley S., Kluth E., and Menaker M. Pineal function in sparrows: circadian rhythms and body temperature. Science 174 (1971) 311-314
6. Cassone V.M., and Menaker M. Is the avian circadian system a neuroendocrine loop?. J. Exp. Zool. 232 (1984) 539-549
7. Chabot C.C., and Menaker M. Circadian feeding and locomotor rhythms in pigeons and house sparrows. J. Biol. Rhythms 7 (1992) 287-299
8. Cockrem J.F., and Follett B.K. Circadian rhythm of melatonin in the pineal gland of the Japanese quail (Coturnix coturnix japonica). J. Endocrinol. 107 (1985) 317-324
9. Compagnone N.A., Bulfone A., Rubenstein J.L., and Mellon S.H. Steroidogenic enzyme P450c17 is expressed in the embryonic central nervous system. Endocrinology 136 (1995) 5212-5223
10. Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21 (2000) 1-56
11. 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. USA 78 (1981) 4704-4707
12. Corpéchot C., Synguelakis M., Talha S., Axelson M., Sjövall J., Vihko R., Baulieu E.E., and Robel P. Pregnenolone and its sulfate ester in rat brain. Brain Res. 270 (1983) 119-125
13. Doostzadeh J., and Morfin R. Effects of cytochrome P450 inhibitors and of steroid hormones on the formation of 7-hydroxylated metabolites of pregnenolone in mouse brain microsomes. J. Endocrinol. 155 (1997) 343-350
14. Freking F., Nazairians T., and Schlinger B.A. The expression of the sex steroid-synthesizing enzymes CYP11A1, 3β-HSD, CYP17, and CYP19 in gonads and adrenals of adult and developing zebra finches. Gen. Comp. Endocrinol. 119 (2000) 140-151
15. Hau M., and Gwinner E. Melatonin facilitates synchronization of sparrow circadian rhythms to light. J. Comp. Physiol. A 175 (1994) 343-347
16. 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
17. Iwata T., Toyoda F., Yamamoto K., and Kikuyama S. Hormonal control of urodele reproductive behavior. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 126 (2000) 221-229
18. 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
19. John T.M., Itoh S., and George J.C. On the role of the pineal in thermoregulation in the pigeon. Horm. Res. 9 (1978) 41-56
20. Kumar V., and Follett B.K. The circadian nature of melatonin secretion in Japanese quail (Coturnix coturnix japonica). J. Pineal Res. 14 (1993) 192-200
21. 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
22. Lea R.W., Clark J.A., and Tsutsui K. Changes in central steroid receptor expression, steroid synthesis and dopaminergic activity related to the reproductive cycle of the ring dove (review). Microsc. Res. Tech. 55 (2001) 12-26
23. Mason J.I. The 3β-hydroxysteroid dehydrogenase gene family of enzymes. Trends Endocrinol. Metab. 4 (1993) 199-203
24. Massa R., and Sharp P.J. Conversion of testosterone to 5β-reduced metabolites in the neuroendocrine tissues of the maturing cockerel. J. Endocrinol. 88 (1981) 263-269
25. Mathur C., Prasad V.V., Raju V.S., Welch M., and Lieberman S. Steroids and their conjugates in the mammalian brain. Proc. Natl. Acad. Sci. USA 90 (1993) 85-88
26. 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. USA 101 (2004) 17282-17287
27. Matsunaga M., Ukena K., and Tsutsui K. Expression and localization of the cytochrome P450 17α-hydroxylase/c17, 20-lyase in the avian brain. Brain Res. 899 (2001) 112-122
28. Matsunaga M., Ukena K., and Tsutsui K. Androgen biosynthesis in the quail brain. Brain Res. 948 (2002) 180-185
29. 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
30. Mellon S.H., and Vaudry H. Biosynthesis of neurosteroids and regulation of their synthesis. Int. Rev. Neurobiol. 46 (2001) 33-78
31. 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
32. 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
33. 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. USA 93 (1996) 1423-1428
34. 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
35. Murakami N., Kawano T., Nakahara K., Nasu T., and Shiota K. Effect of melatonin on circadian rhythm, locomotor activity and body temperature in the intact house sparrow, Japanese quail and owl. Brain Res. 889 (2001) 220-224
36. Nakahara K., Kawano T., Shiota K., and Murakami N. Effects of microinjection of melatonin into various brain regions of Japanese quail on locomotor activity and body temperature. Neurosci. Lett. 345 (2003) 117-120
37. 5-derivatives in the rodent brain. Neurochem. Int. 7 (1985) 953-958
38. 5-derivatives in rat and monkey brain. J. Steroid Biochem. 27 (1987) 649-655
39. 4-isomerase in the zebrafish central nervous system. J. Comp. Neurol. 439 (2001) 291-305
40. Saper C.B., Lu J., Chou T.C., and Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci. 28 (2005) 152-157
41. Schlinger B.A., and Callard G.V. A comparison of aromatase, 5α, and 5β-reductase activities in the brain and pituitary of male and female quail (Coturnix coturnix japonica). J. Exp. Zool. 242 (1987) 171-180
42. Schlinger B.A., and Callard G.V. Aromatase activity in quail brain: correlation with aggressiveness. Endocrinology 124 (1989) 437-443
43. Schlinger B.A., and Callard G.V. Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49 (1989) 434-441
44. 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
45. 4-isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145 (2004) 1668-1677
46. 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
47. Tsutsui Y. Notes on the behavior of the common Japanese newt, Diemyctylus pyrrhogaster BOIE. I. Breeding habit. Mem. Col. Sci. Kyoto Imp. Univ. Ser. B7 (1931) 159-179
48. Tsutsui K., Inoue K., Miyabara H., Suzuki S., Ogura Y., and Haraguchi S. 7α-Hydroxypregnenolone mediates melatonin action underlying diurnal locomotor rhythms. J. Neurosci. 28 (2008) 2158-2167
49. Tsutsui K., Matsunaga M., and Ukena K. Review: biosynthesis and biological actions of neurosteroids in the avian brain. Avian Poult. Biol. Rev. 14 (2003) 63-78
50. Tsutsui K., Matsunaga M., Miyabara H., and Ukena K. Review: neurosteroid biosynthesis in the quail brain. J. Exp. Zool. 305A (2006) 733-742
51. 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
52. Tsutsui K., Ukena K., Takase M., Kohchi C., and Lea R.W. Review: neurosteroid biosynthesis in vertebrate brains. Comp. Biochem. Physiol. C 124 (1999) 121-129
53. 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
54. Tsutsui K., and Yamazaki T. Avian neurosteroids. I. Pregnenolone biosynthesis in the quail brain. Brain Res. 678 (1995) 1-9
55. 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
56. 4-isomerase in different regions of the avian brain. Brain Res. 818 (1999) 536-542
57. 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
58. 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
59. 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
60. Wada M. Photoperiodic control of LH secretion in Japanese quail with special reference to the photoinducible phase. Gen. Comp. Endocrinol. 39 (1979) 141-149
61. Warren W.S., and Cassone V.M. The pineal gland: photoreception and coupling of behavioral, metabolic, and cardiovascular circadian outputs. J. Biol. Rhythms 10 (1995) 64-79
62. 5-androstene-3β, 17β-diol in specific regions of the aging brain from Alzheimer's and non-demented patients. Brain Res. 969 (2003) 117-125
63. Wilson W.O. A review of the physiology of Coturnix (Japanese quail). World's Poult. Sci. J. 28 (1972) 413-429
64. Yau J.L., Rasmuson S., Andrew R., Graham M., Noble J., Olsson T., Fuchs E., Lathe R., and Seckl J.R. Dehydroepiandrosterone 7-hydroxylase CYP7B: predominant expression in primate hippocampus and reduced expression in Alzheimer's disease. Neuroscience 121 (2003) 307-314