Medaka pp 269-285 | Cite as

Endocrine Regulation of Oogenesis in the Medaka, Oryzias latipes

  • Naoki Shibata
  • Masatoshi Nakamoto
  • Yasushi Shibata
  • Yoshitaka Nagahama


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.


Luteinizing Hormone Granulosa Cell Oocyte Maturation Ovarian Follicle Germinal Vesicle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



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.


  1. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364CrossRefGoogle Scholar
  2. 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 36:81–88CrossRefGoogle Scholar
  3. 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 45:285–290CrossRefPubMedGoogle Scholar
  4. 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 255:123–128CrossRefPubMedGoogle Scholar
  5. Hammes SR (2004) Steroids and oocyte maturation – a new look at an old story. Mol Endocrinol 18:769–775CrossRefPubMedGoogle Scholar
  6. 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 17:1476–1483PubMedGoogle Scholar
  7. 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 211:231–239CrossRefGoogle Scholar
  8. 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 47:440–448CrossRefPubMedGoogle Scholar
  9. Kishimoto T (1999) Activation of MPF at meiosis reinitiation in starfish oocytes. Dev Biol 214:1–8CrossRefPubMedGoogle Scholar
  10. 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 13:921–927CrossRefGoogle Scholar
  11. Lydon JP, DeMayo FJ, Funk CR et al (1995) Mice lacking progesterone receptors exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266–2278CrossRefPubMedGoogle Scholar
  12. Maller WL (2005) Minireview: regulation of steroidogenesis by electron transfer. Endocrinology 146:2544–2550CrossRefGoogle Scholar
  13. Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57:185–282CrossRefPubMedGoogle Scholar
  14. Mehlmann LM (2005) Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130:791–799CrossRefPubMedGoogle Scholar
  15. 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 223–275Google Scholar
  16. Nagahama Y, Adachi S (1985) Identification of a maturation-inducing steroid in a teleost, the amago salmon (Oncorhynchus rhodurus). Dev Biol 109:428–435CrossRefPubMedGoogle Scholar
  17. 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 259:53–58CrossRefGoogle Scholar
  18. Nagahama Y, Yamashita, M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50:195–219Google Scholar
  19. Nagahama Y, Yamashita M, Tokumoto T (1994) Regulation of oocyte maturation in fish. Curr Top Dev Biol 30:103–145CrossRefGoogle Scholar
  20. Nakamoto M, Wang DS, Suzuki A, Matsuda M, Nagahama Y, Shibata N (2007) Dax1 suppresses P450arom expression in medaka ovarian follicles. Mol Reprod Dev 74:1239–1246CrossRefPubMedGoogle Scholar
  21. 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 249:846–853CrossRefPubMedGoogle Scholar
  22. 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 102:8442–8447CrossRefPubMedGoogle Scholar
  23. Onitake K, Iwamatsu T (1986) Immunocytochemical demonstration of steroid hormones in the granulosa cells of the medaka, Oryzias latipes. J Exp Zool 239:97–103CrossRefPubMedGoogle Scholar
  24. 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 66:333–342CrossRefPubMedGoogle Scholar
  25. 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 71:516–523CrossRefPubMedGoogle Scholar
  26. 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 67:1080–1086CrossRefPubMedGoogle Scholar
  27. Stocco DM (2000) The role of the StAR protein in steroidogenesis: challenges for the future. J Endocrinol 164:247–253CrossRefPubMedGoogle Scholar
  28. 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) 117:719–725Google Scholar
  29. 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 29:292–312CrossRefPubMedGoogle Scholar
  30. 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 7:185–191CrossRefGoogle Scholar
  31. Tokumoto T, Yamashita M, Tokumoto M et al (1997) Initiation of cyclin B degradation by the 26S proteasome upon egg activation. J Cell Biol 138:1313–1322CrossRefPubMedGoogle Scholar
  32. 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 21:712–725CrossRefPubMedGoogle Scholar
  33. 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 149:221–228CrossRefPubMedGoogle Scholar
  34. 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 118:1–8CrossRefGoogle Scholar
  35. Zazopoulos E, Lalli E, Stocco DM, Sassone-Corsi P (1997) DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature (Lond) 390:311–315CrossRefGoogle Scholar
  36. 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 148:4288–4291Google Scholar
  37. 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 362:619–624CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Naoki Shibata
    • 1
  • Masatoshi Nakamoto
    • 2
  • Yasushi Shibata
    • 3
  • Yoshitaka Nagahama
    • 4
  1. 1.Department of Biology, Faculty of ScienceShinshu UniversityMatsumotoJapan
  2. 2.Department of Biology, Faculty of ScienceShinshu UniversityMatsumotoJapan
  3. 3.Laboratory of Reproductive BiologyNational Institute for Basic BiologyOkazakiJapan
  4. 4.Laboratory of Reproductive BiologyNational Institute for Basic BiologyOkazakiJapan

Personalised recommendations