Recent advances in the understanding of teleost medaka ovulation: The roles of proteases and prostaglandins

Zoological Science

Volumn 30, Issue 4, 2013, Pages 239-247

  Takahashi, Takayuki ^a   Fujimori, Chika ^a   Hagiwara, Akane ^a   Ogiwara, Katsueki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

LH; Medaka; Ovary; Ovulation; Progesterone receptor; Prostaglandin E2

Indexed keywords

PEPTIDE HYDROLASE; PROSTAGLANDIN;

ANIMAL; FEMALE; METABOLISM; ORYZIAS; OVULATION; PHYSIOLOGY; REVIEW;

ANIMALS; FEMALE; ORYZIAS; OVULATION; PEPTIDE HYDROLASES; PROSTAGLANDINS;

ANIMALIA; MAMMALIA; ORYZIAS LATIPES; ORYZIINAE; TELEOSTEI; VERTEBRATA;

EID: 84875930016     PISSN: 02890003     EISSN: None     Source Type: Journal    
DOI: 10.2108/zsj.30.239     Document Type: Review

References (89)

1. Bahr JM (1978) Simultaneous measurement of steroids in follicular fluid and ovarian venous blood in the rabbit. Biol Reprod 18: 193-197
2. Berkholtz CB, Lai BE, Woodruff TK, Shea LD (2006) Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis. Histochem Cell Biol 126: 583-592
3. Berndtson AK, Goetz FW, Duman P (1989) In vitro ovulation, prostaglandin synthesis, and proteolysis in isolated ovarian components of yellow perch (Perca flavescens): Effects of 17?, 20?-dihydroxy-4-pregnen-3-one and phorbol ester. Gen Comp Endocrinol 75: 454-465
4. Bobe J, Nguyen T, Jalabert B (2004) Targeted gene expression profiling in the rainbow trout (Oncorhynchus mykiss) ovary during maturational competence acquisition and oocyte maturation. Biol Reprod 71: 73-82
5. Cetta F, Goetz FW (1982) Ovarian and plasma prostaglandin E and F levels in brook trout (Salvelinus fontinalis) during pituitaryinduced ovulation. Biol Reprod 27: 1216-1221
6. Chang KJ, Kim JW, Lee J, Im WB, Kwon HB, Schuetz AW (1995) Prostaglandin production and ovulation during exposure of amphibian ovarian follicles to gonadotropin or phorbol ester in vitro. Gen Comp Endocrinol 100: 257-266
7. Chang KJ, Kim JW, Im WB, Kang HM, Kwon HB (1997) Differential effects of gonadotropin and orthovanadate on oocyte maturation, ovulation, and prostaglandin synthesis by Rana ovarian follicles in vitro. J Exp Zool 277: 155-165
8. Crespo D, Bonnet E, Roher N, MacKenzie SA, Krasnov A, Goetz FW, et al. (2010) Cellular and molecular evidence for a role of tumor necrosis factor alpha in the ovulatory mechanism of trout. Reprod Biol Endocrinol 8: 34
9. Curry TE Jr, Osteen KG (2003) The matrix metalloproteinase system: Changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24: 428-465
10. Curry TE Jr, Smith MF (2006) Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin Reprod Med 24: 228-241
11. Epler P, Bieniarz K, Marosz E (1985) Effect of temperature, 17?-hydroxy-20 ?-dihydroprogesterone and prostaglandin F2 on carp oocyte maturation and ovulation in vitro. Gen Comp Endocrinol 58: 192-201
12. Espey LL (1967) Ultrastructure of the apex of the rabbit Graafian follicle during the ovulatory process. Endocrinology 81: 267-276
13. Espey LL, Lipner H (1994) Ovulation. In "The Physiology of Reproduction" Ed by E Knobil, JD Neill, Raven Press, New York, pp 725-780
14. Espey LL, Richards JS (2006) Ovulation. In "Physiology of Reproduction, Vol 1" 3rd ed, Ed by JD Neil et al., Academic Press, Amsterdam, pp 425-474
15. Fujimori C, Ogiwara K, Hagiwara A, Rajapakse S, Kimura A, Takahashi T (2011) Expression of cyclooxygenase-2 and prostaglandin receptor EP4b mRNA in the ovary of the medaka fish, Oryzias latipes: Possible involvement in ovulation. Mol Cell Endocrinol 332: 67-77
16. Fujimori C, Ogiwara K, Hagiwara A, Takahashi T (2012) New evidence for the involvement of prostaglandin receptor EP4b in ovulation of the medaka, Oryzias latipes. Mol Cell Endocrinol. 362: 76-84
17. Gazourian L, Deragon KL, Chase CF, Pati D, Habibi HR, Sower SA (1997) Characteristics of GnRH binding in the gonads and effects of lamprey GnRH-I and-III on reproduction in the adult sea lamprey. Gen Comp Endocrinol 108: 327-339
18. Goetz FW (1991) Compartmentalization of prostaglandin synthesis within the fish ovary. Am J Physiol 260: R862-R865
19. Goetz FW (1993) Involvement of protein kinase C in agoniststimulated goldfish ovulation. Biol Reprod 48: 846-850
20. Goetz FW (1997) Follicle and extrafollicular tissue interaction in 17?, 20?-dihydroxy-4-pregnen-3-one-stimulated ovulation and prostaglandin synthesis in the yellow perch (Perca flavescens) ovary. Gen Comp Endocrinol 105: 121-126
21. Goetz FW, Nagahama Y (1985) The in vitro effects of cyclic nucleotides on prostaglandin-induced ovulation of goldfish (Carassius auratus). Zool Sci 2: 225-228
22. Goetz FW, Theofan G (1979) In vitro stimulation of germinal vesicle breakdown and ovulation of yellow perch (Perca flavescens) oocytes. Effects of 17?-hydroxy-20?-dihydroprogesterone and prostaglandins. Gen Comp Endocrinol 37: 273-285
23. Goetz FW, Smith DC, Krickl SP (1982) The effects of prostaglandins, phosphodiesterase inhibitors, and cyclic AMP on ovulation of brook trout (Salvelinus fontinalis) oocytes. Gen Comp Endocrinol 48: 154-160
24. Goff AK, Henderson KM (1979) Changes in follicular fluid and serum concentrations of steroids in PMS treated immature rats following LH administration. Biol Reprod 20: 1153-1157
25. Grosser T, Yusuff S, Cheskis E, Pack MA, FitzGerald GA (2002) Developmental expression of functional cyclooxygenases in zebrafish. Proc Natl Acad Sci U S A 99: 8418-8423
26. Havird JC, Miyamoto MM, Choe KP, Evans DH (2008) Gene duplications and losses within the cyclooxygenase family of teleosts and other chordates. Mol Biol Evol 25: 2349-2359
27. Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, et al. (1999) Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc Natl Acad Sci U S A 96: 10501-10506
28. Horiguchi M, Fujimori C, Ogiwara K, Moriyama A, Takahashi T (2008) Collagen type-I ?1 chain mRNA is expressed in the follicle cells of the medaka ovary. Zool Sci 25: 937-945
29. Hubbard CJ, Greenwald GS (1982) Cyclic nucleotides, DNA, and steroid levels in ovarian follicles and corpora lutea of the cyclic hamster. Biol Reprod 26: 230-240
30. Ishikawa Y (2000) Medakafish as a model system for vertebrate developmental genetics. Bioessays 22: 487-495
31. Ishikawa TO, Herschman HR (2007) Two inducible, functional cyclooxygenase-2 genes are present in the rainbow trout genome. J Cell Biochem 102: 1486-1492
32. Ishikawa TO, Griffin KJ, Banerjee U, Herschman HR (2007) The zebrafish genome contains two inducible, functional cyclooxygenase-2 genes. Biochem Biophys Res Commun 352: 181-187
33. Iwamatsu T (1978) Studies on oocyte maturation of the medaka, Oryzias latipes. VI. Relationship between the circadian cycle of oocyte maturation and activity of the pituitary gland. J Exp Zool 206: 355-363
34. Iwamatsu T, Ohta T, Oshima E, Sakai N (1988) Oogenesis in the medaka Oryzias latipes. Stage of oocyte development. Zool Sci 5: 353-373
35. Jalabert B, Szollosi D (1975) In vitro ovulation of trout oocytes: Effect of prostaglandins on smooth muscle-like cells of the theca. Prostaglandins 9: 765-778
36. Jarving R, Jarving I, Kurg R, Brash AR, Samel N (2004) On the evolutionary origin of cyclooxygenase (COX) isozymes: Characterization of marine invertebrate COX genes points to independent duplication events in vertebrate and invertebrate lineages. J Biol Chem 279: 13624-13633
37. Joyce IM, Pendola FL, O'Brien M, Eppig JJ (2001) Regulation of prostaglandin-endoperoxide synthase 2 messenger ribonucleic acid expression in mouse granulosa cells during ovulation. Endocrinology 142: 3187-3197
38. Kagawa H, Nagahama Y (1981) In vitro effects of prostaglandins on ovulation in goldfish Carassius auratus. Bull Jap Soc Sci Fish 47: 1119-1121
39. Kagawa H, Tanaka H, Unuma T, Ohta H, Gen K, Kuzawa K (2003) Role of prostaglandin in the control of ovulation in the Japanese eel Anguilla japonica. Fisheries Sci 69: 234-241
40. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, et al. (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447: 714-719
41. Kato Y, Ogiwara K, Fujimori C, Kimura A, Takahashi T (2010) Expression and localization of collagen type IV ?1 chain in medaka ovary. Cell Tissue Res 340: 595-605
42. Kwok AH, Wang Y, Leung FC (2012) Molecular characterization of prostaglandin F receptor (FP) and E receptor subtype 1 (EP(1)) in zebrafish. Gen Comp Endocrinol 178: 216-226
43. Leonardsson G, Peng XR, Liu K, Nordstrom L, Carmeliet P, Mulligan R, et al. (1995) Ovulation efficiency is reduced in mice that lack plasminogen activator gene function: Functional redundancy among physiological plasminogen activators. Proc Natl Acad Sci USA 92: 12446-12450
44. Lessman CA (2009) Oocyte maturation: Converting the zebrafish oocyte to the fertilizable egg. Gen Comp Endocrinol 161: 53-57
45. Li X, O'Malley BW (2003) Unfolding the action of progesterone receptors. J Biol Chem 278: 39261-39264
46. Li S, Mao Z, Han W, Sun Z, Yan W, Chen H, Yan S (1993) In vitro oocyte maturation in the zebra fish, Brachydanio rerio, and the fertilization and development of the mature egg. Chin J Biotechnol 9: 247-255
47. Lind AK, Weijdegard B, Dahm-Kahler P, Molne J, Sundfeldt K, Brannstrom M (2006) Collagens in the human ovary and their changes in the perifollicular stroma during ovulation. Acta Obstet Gynecol Scand 85: 1476-1484
48. Lister AL, Van Der Kraak G (2008) An investigation into the role of prostaglandins in zebrafish oocyte maturation and ovulation. Gen Comp Endocrinol 159: 46-57
49. Lister AL, Van Der Kraak GJ (2009) Regulation of prostaglandin synthesis in ovaries of sexually-mature zebrafish (Danio rerio). Mol Reprod Dev 76: 1064-1075
50. Munakata A, Kobayashi M (2010) Endocrine control of sexual behavior in teleost fish. Gen Comp Endocrinol 165: 456-468
51. Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38: 217-229
52. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50 Suppl 1: S195-S219
53. Ny A, Nordstrom L, Carmeliet P, Ny T (1997) Studies of mice lacking plasminogen activator gene function suggest that plasmin production prior to ovulation exceeds the amount needed for optimal ovulation efficiency. Eur J Biochem 244: 487-493
54. Ny A, Leonardsson G, Hagglund AC, Hagglof P, Ploplis VA, Carmeliet P, Ny T (1999) Ovulation in plasminogen-deficient mice. Endocrinology 140: 5030-5035
55. 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
56. Ogiwara K, Ikeda T, Takahashi T (2010) A new in vitro ovulation model for medaka based on whole ovary culture. Zool Sci 27: 762-767
57. Ogiwara K, Minagawa K, Takano N, Kageyama T, Takahashi T (2012) Apparent involvement of plasmin in early-stage follicle rupture during ovulation in medaka. Biol Reprod 86: 113
58. Ogiwara K, Fujimori C, Rajapakse S, Takahashi T (2013) Characterization of luteinizing hormone and luteinizing hormone receptor and their indispensable role in the ovulatory process of the medaka. PLoS ONE 8(1): E54482. doi:10.1371/journal.pone. 0054482
59. Ohnishi J, Ohnishi E, Shibuya H, Takahashi T (2005) Functions for proteinases in the ovulatory process. Biochim Biophys Acta 1751: 95-109
60. Ozato K, Wakamatsu Y, Inoue K (1992) Medaka as a model of transgenic fish. Mol Mar Biol Biotechnol 1: 346-354
61. Pankhurst NW (1985) Final maturation and ovulation of oocytes of the goldeye, Hiodon alasoides (Rahubesque), in vitro. Can J Zool 63: 1003-1009
62. Patino R, Thomas P (1990) Effects of gonadotropin on ovarian intrafollicular processes during the development of oocyte maturational competence in a teleost, the Atlantic croaker: Evidence for two distinct stages of gonadotropin control of final oocyte maturation. Biol Reprod 43: 818-827
63. Patino R, Yoshizaki G, Bolamba D, Thomas P (2003) Role of arachidonic acid and protein kinase C during maturation-inducing hormone-dependent meiotic resumption and ovulation in ovarian follicles of Atlantic croaker. Biol Reprod 68: 516-523
64. Ramos I, Cisint SB, Crespo CA, Medina MF, Fernandez SN (2008) Modulators of Bufo arenarum ovulation. Zygote 16: 65-72
65. Richards JS, Russell DL, Robker RL, Dajee M, Alliston TN (1998) Molecular mechanisms of ovulation and luteinization. Mol Cell Endocrinol 145: 47-54
66. Richards JS, Russell DL, Ochsner S, Espey LL (2002) Ovulation: New dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 64: 69-92
67. Robker RL, Akison LK, Russell DL (2009) Control of oocyte release by progesterone receptor-regulated gene expression. Nucl Recept Signal 7: E012
68. Sakai N, Iwamatsu T, Yamauchi K, Nagahama Y (1987) Development of the steroidogenic capacity of medaka (Oryzias latipes) ovarian follicles during vitellogenesis and oocyte maturation. Gen Comp Endocrinol 66: 333-342
69. Sakai N, Iwamatsu T, Yamauchi K, Suzuki N, Nagahama Y (1988) Influence of follicular development on steroid production in the medaka (Oryzias latipes) ovarian follicle in response to exogenous substrates. Gen Comp Endocrinol 71: 516-523
70. Santos HB, Sato Y, Moro L, Bazzoli N, Rizzo E (2008) Relationship among follicular apoptosis, integrin beta1 and collagen type IV during early ovarian regression in the teleost Prochilodus argenteus after induced spawning. Cell Tissue Res 332: 159-170
71. Schochet SS (1916) A suggestion as to the process of ovulation and ovarian cyst formation. Anat Rec 10: 447-457
72. Schroeder PC, Pendergrass P (1976) The inhibition of in-Vitro ovulation from follicles of the teleost, Oryzias latipes, by cytochalasin B. J Reprod Fertil 48: 327-330
73. Schuetz AW (1986) Hormonal dissociation of ovulation and maturation of oocytes: Ovulation of immatureamphibian oocytes by prostaglandin. Gamete Res 15: 99-113
74. Sena J, Liu Z (2008) Expression of cyclooxygenase genes and production of prostaglandins during ovulation in the ovarian follicles of Xenopus laevis. Gen Comp Endocrinol 157: 165-173
75. Simmons DL, Botting RM, Hla T (2004) Cyclooxygenase isozymes: The biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56: 387-437
76. Sirois J, Sayasith K, Brown KA, Stock AE, Bouchard N, Dore M (2004) Cyclooxygenase-2 and its role in ovulation: A 2004 account. Hum Reprod Update 10: 373-385
77. Sorbera LA, Asturiano JF, Carrillo M, Zanuy S (2001) Effects of polyunsaturated fatty acids and prostaglandins on oocyte maturation in a marine teleost, the European sea bass (Dicentrarchus labrax). Biol Reprod 64: 382-389
78. Sorensen PW, Goetz FW (1993) Pheromonal and reproductive function of F prostaglandins and their metabolites in teleost fish. J Lipid Mediat 6: 385-393
79. Sorensen PW, Hara TJ, Stacey NE, Goetz FW (1988) F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol Reprod 39: 1039-1050
80. Sriraman V, Sinha M, Richards JS (2010) Progesterone receptorinduced gene expression in primary mouse granulosa cell cultures. Biol Reprod 82: 402-412
81. Stacey NE, Pandey S (1975) Effects of indomethacin and prostaglandins on ovulation of goldfish. Prostaglandins 9: 597-607
82. Sugimoto Y, Narumiya S (2007) Prostaglandin E receptors. J Biol Chem 282: 11613-11617
83. Thomas P (2012) Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen Comp Endocrinol 175: 367-383
84. Tsafriri A, Dekel N (1994) Molecular mechanisms in ovulation. In "Molecular Biology of the Female Reproductive System" Ed by JK Findley, New York, Academic press, pp 207-258
85. Tubbs C, Pace M, Thomas P (2010) Expression and gonadotropin regulation of membrane progestin receptor alpha in Atlantic croaker (Micropogonias undulatus) gonads: Role in gamete maturation. Gen Comp Endocrinol 165: 144-154
86. Villablanca EJ, Pistocchi A, Court FA, Cotelli F, Bordignon C, Allende ML, Traversari C, Russo V (2007) Abrogation of prostaglandin E2/EP4 signaling impairs the development of rag1+ lymphoid precursors in the thymus of zebrafish embryos. J Immunol 179: 357-364
87. Wittbrodt J, Shima A, Schartl M (2002) Medaka-A model organism from the far East. Nat Rev Genet 3: 53-64
88. Wong WY, DeWitt DL, Smith WL, Richards JS (1989) Rapid induction of prostaglandin endoperoxide synthase in rat preovulatory follicles by luteinizing hormone and cAMP is blocked by inhibitors of transcription and translation. Mol Endocrinol 3: 1714-1723
89. Zou J, Neumann NF, Holland JW, Belosevic M, Cunningham C, Secombes CJ, Rowley AF (1999) Fish macrophages express a cyclo-oxygenase-2 homologue after activation. Biochem J 340 (Pt 1): 153-159