Abstract
Regulation of ovarian activity is an integrated process encompassing both extraovarian signals and intrafollicular factors. The medaka, Oryzias latipes, has served as an excellent experimental model for studying the regulation of various processes of oogenesis such as oocyte growth, maturation, and ovulation. The advantage of the medaka model is the precise daily ovarian cyclicity and the ease of isolating large numbers of oocytes for in vitro studies. In addition, because of the identification of maturation-inducing hormones (steroids) in fish oocytes, the endocrine regulation of oocyte maturation has been investigated most extensively in fishes, including medaka. Here we provide a brief overview of the gene regulation of hormonally controlled processes of oocyte growth, maturation, and ovulation mainly in medaka, and present some novel data on the steroidogenic shift occurring in ovarian follicles during oocyte growth and maturation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364
Fukada S, Sakai N, Adachi S, Nagahama Y (1994) Steroidogenesis in the ovarian follicle of medaka (Oryzias latipes, a daily spanner) during oocyte maturation. Dev Growth Differ 36:81–88
Fukada S, Tanaka M, Matsuyama M, Kobayashi D, Nagahama Y (1996) Isolation, characterization, and expression of cDNAs encoding the medaka (Oryzias latipes) ovarian follicle P-450 aromatase. Mol Reprod Dev 45:285–290
Guan G, Tanaka M, Todo T, Young G, Yoshikuni M, Nagahama Y (1999) Cloning and expression of two carbonyl reductase-like 20β-hydroxysteroid dehydrogenase cDNAs in ovarian follicles of rainbow trout (Oncorhynchus mykiss). Biochem Biophys Res Commun 255:123–128
Hammes SR (2004) Steroids and oocyte maturation – a new look at an old story. Mol Endocrinol 18:769–775
Ito M, Yu R, Jameson JL (1997) DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol Cell Biol 17:1476–1483
Iwamatsu T (1980) Studies on oocyte maturation of the medaka Oryzias latipes. VIII. Role of follicular constituents in gonadotropin- and steroid-induced maturation of oocytes in vitro. J Exp Zool 211:231–239
Kagawa H, Young G, Adachi S, Nagahama Y (1982) Estradiol-17β production in amago salmon (Oncorhynchus rhodurus) ovarian follicles: role of the thecal and granulosa cells. Gen Comp Endocrinol 47:440–448
Kishimoto T (1999) Activation of MPF at meiosis reinitiation in starfish oocytes. Dev Biol 214:1–8
Kobayashi D, Tanaka M, Fukada S, Nagahama Y (1996) Steroidogenesis in the ovarian follicles of the medaka (Oryzias latipes) during vitellogenesis and oocyte maturation. Zool Sci 13:921–927
Lydon JP, DeMayo FJ, Funk CR et al (1995) Mice lacking progesterone receptors exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266–2278
Maller WL (2005) Minireview: regulation of steroidogenesis by electron transfer. Endocrinology 146:2544–2550
Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57:185–282
Mehlmann LM (2005) Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130:791–799
Nagahama Y (1983) The functional morphology of teleost gonads. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol IXA. Academic Press, New York, pp 223–275
Nagahama Y, Adachi S (1985) Identification of a maturation-inducing steroid in a teleost, the amago salmon (Oncorhynchus rhodurus). Dev Biol 109:428–435
Nagahama Y, Matsuhisa A, Iwamatsu T, Sakai N, Fukada S (1991) A mechanism for the action of pregnant mare serum gonadotropin on aromatase activity in the ovarian follicle of the medaka, Oryzias latipes. J Exp Zool 259:53–58
Nagahama Y, Yamashita, M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50:195–219
Nagahama Y, Yamashita M, Tokumoto T (1994) Regulation of oocyte maturation in fish. Curr Top Dev Biol 30:103–145
Nakamoto M, Wang DS, Suzuki A, Matsuda M, Nagahama Y, Shibata N (2007) Dax1 suppresses P450arom expression in medaka ovarian follicles. Mol Reprod Dev 74:1239–1246
Oba Y, Yoshikuni M, Tanaka M, Mita M, Nagahama Y (1997) Inhibitory guanine-nucleotide-binding regulatory protein α subunits in medaka (Oryzias latipes) oocytes. Eur J Biochem 249:846–853
Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T (2005) Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci USA 102:8442–8447
Onitake K, Iwamatsu T (1986) Immunocytochemical demonstration of steroid hormones in the granulosa cells of the medaka, Oryzias latipes. J Exp Zool 239:97–103
Sakai N, Iwamatsu T, Yamauchi K, Nagahama Y (1987) Development of the steroidogenetic capacity of medaka (Oryzias latipes) ovarian follicles during vitellogenesis and oocyte maturation. Gen Comp Endocrinol 66:333–342
Sakai N, Iwamatsu T, Yamauchi K, Suzuki N, Nagahama Y (1988) Influence of follicular development of steroid production in the medaka (Oryzias latipes) ovarian follicles in response to exogenous substances. Gen Comp Endocrinol 71:516–523
Senthilkumaran B, Sudhakumari CC, Chang XT, Kobayashi T, Oba Y, Guan GJ, Yoshiura Y, Yoshikuni M, Nagahama Y (2002) Ovarian carbonyl reductase-like 20β-hydroxysteroid dehydrogenase shows distinct surge in messenger RNA expression during natural and gonadotropin-induced meiotic maturation in Nile tilapia. Biol Reprod 67:1080–1086
Stocco DM (2000) The role of the StAR protein in steroidogenesis: challenges for the future. J Endocrinol 164:247–253
Tanaka M, Fukada S, Matsuyama M, Nagahama Y (1995) Structure and promoter analysis of the cytochrome P-450 aromatase gene of the teleost fish, medaka (Oryzias latipes). J Biochem (Tokyo) 117:719–725
Thomas P (2008) Characteristics of membrane progestin receptor alpha (mPRa) and progesterone membrane receptor component one (PGMRC1) and their roles in mediating rapid progestin actions. Front Neuroendocrinol 29:292–312
Thomas P, Trant JM (1989) Evidence that 17, 20β, 21-trihydroxy-4-pregnen-3-one is a maturation-inducing steroid in spotted seatrout. Fish Physiol Biochem 7:185–191
Tokumoto T, Yamashita M, Tokumoto M et al (1997) Initiation of cyclin B degradation by the 26S proteasome upon egg activation. J Cell Biol 138:1313–1322
Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, Nagahama Y (2007) Foxl2 up-regulates aromatase gene transcription female-specifically by binding to the promoter as well as interacting with Ad4BP/SF-1. Mol Endocrinol 21:712–725
Watanabe M, Tanaka M, Kobayashi D, Yoshiura Y, Oba Y, Nagahama Y (1999) Medaka (Oryzias latipes) FTZ-F1 potentially regulates the transcription of P450 aromatase in ovarian follicles: cDNA cloning and functional characterization. Mol Cell Endocrinol 149:221–228
Young G, Adachi S, Nagahama Y (1986) Role of ovarian thecal and granulosa layers in gonadotropin-induced synthesis of a salmonid maturation-inducing substance (17α, 20β-dihydroxy-4-pregnen-3-one). Dev Biol 118:1–8
Zazopoulos E, Lalli E, Stocco DM, Sassone-Corsi P (1997) DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature (Lond) 390:311–315
Zhou LY, Wang DS, Kobayashi T, Yano A, Paul-Prasanth B, Suzuki A, Sakai F, Nagahama Y (2007a) A novel type of P450c17 lacking the lyase activity is responsible for C21-steroid biosynthesis in the fish ovary and head kidney. Endocrinology 148:4288–4291
Zhou LY, Wang DS, Shibata Y, Paul-Prasanth B, Suzuki A, Nagahama Y (2007b) Characterization, expression and transcriptional regulation of P450c17-I and -II in the medaka, Oryzias latipes. Biochem Biophys Res Commun 362:619–624
Acknowledgments
Qurt strain medaka was provided by National BioResource Project Medaka (NBRP Medaka) of Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan. This work was supported in part by Grants-in-Aid for Scientific Research on Priority Areas from the Ministry of Education, Science and Culture of Japan and the SORST Research Project of Japan Science, and Technology Corporation.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer
About this chapter
Cite this chapter
Shibata, N., Nakamoto, M., Shibata, Y., Nagahama, Y. (2011). Endocrine Regulation of Oogenesis in the Medaka, Oryzias latipes . In: Naruse, K., Tanaka, M., Takeda, H. (eds) Medaka. Springer, Tokyo. https://doi.org/10.1007/978-4-431-92691-7_18
Download citation
DOI: https://doi.org/10.1007/978-4-431-92691-7_18
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-92690-0
Online ISBN: 978-4-431-92691-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)