Tide-related Changes in mRNA Abundance of Aromatases and Estrogen Receptors in the Ovary and Brain of the Threespot Wrasse Halichoeres trimaculatus

Abstract

The threespot wrasse (Halichoeres trimaculatus; Family Labridae) is a common coral reef species of the Indo-Pacific Ocean. Given that this species spawns daily at high tide (HT), we hypothesized that endocrine changes in relation to gonadal development are synchronized with the tidal cycle. To test this, we examined the transcript abundance of two cytochrome P450 aromatases (cyp19a and cyp19b) and two estrogen receptors (erα and erβ) in the ovary and brain of this species in response to tidal change. When fish were collected around four tidal points [low tide (LT), flood tide (FT), high tide (HT), and ebb tide (ET)], gonadosomatic index and oocyte diameter increased around HT and FT, respectively. Ovulatory follicles were observed in ovaries around HT. Real-time quantitative polymerase-chain reaction revealed that mRNA abundance of cyp19a and erα, but not erβ, in the ovary increased around ET and HT, respectively. On the other hand, mRNA levels of cyp19b in the forebrain were significantly higher around FT. Increases of erα and erβ mRNA abundance around FT were observed in all areas of the brain and the midbrain, respectively. The changes in mRNA abundance of key genes involved in reproduction at specific tidal cycles, along with the development of the vitellogenic oocytes in the ovary, support our hypothesis that synchronization of endocrine changes to the tidal periodicity plays a role in the gonadal development of this species. We hypothesize that conversion of testosterone to E2 in the brain may be associated with the spawning behavior given that the wrasse exhibits group spawning with a territory-holding male around HT.

This is a preview of subscription content, log in to check access.

References

  1. Afonso LOB, Iwama GK, Smith J, Donaldson EM (1999) Effects of the aromatase inhibitor Fadrozole on plasma sex steroid secretion and oocytematuration in female coho salmon (Oncorhynchus kisutch) during vitellogenesis. Fish Physiol Biochem 20:231–241

    Article  Google Scholar 

  2. Asahina K, Kambegawa A, Higashi T (1995) Development of a microtiter plate enzyme-linked immunosorbent assay for 17α,20β,21-trihydroxy-4-pregnen-3-one, a teleost gonadal steroid. Fish Sci 61:491–494

    Article  Google Scholar 

  3. Blázquez M, Piferrer F (2004) Cloning, sequence analysis, tissue distribution, and sex-specific expression of the neural form of P450 aromatase in juvenile sea bass (Dicentrarchus labrax). Mol Cell Endocrinol 219:83–94

    Article  Google Scholar 

  4. Chang XT, Kobayashi T, Kajiura H, Nakamura M, Nagahama Y (1997) Isolation and characterization of the cDNA encoding the tilapia (Oreochromis niloticus) cytochrome P450 aromatase (P450arom): changes in P450arom mRNA, protein, and enzyme activity in ovarian follicles during oogenesis. J Mol Endocrinol 18:57–66

    Article  Google Scholar 

  5. Chang X, Kobayashi T, Senthilkumaran B, Kobayashi-Kajura H, Sudhakumari CC, Nagahama Y (2005) Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen Comp Endocr 141:101–115

    Article  Google Scholar 

  6. Chaube R, Rawat A, Joy KP (2015) Molecular cloning and characterization of brain and ovarian cytochrome P450 aromatase genes in the catfish Heteropneustes fossilis: sex, tissue and seasonal variation in, and effects of gonadotropin on gene expression. Gen Comp Endocr 221:120–133

    Article  Google Scholar 

  7. Chen H, Zhang Y, Li S, Lin M, Shi Y, Sang Q, Liu M, Zhang H, Lu D, Meng Z, Liu X, Lin H (2011) Molecular cloning, characterization and expression profiles of three estrogen receptors in protogynous hermaphroditic orange-spotted grouper (Epinephelus coioides). Gen Comp Endocr 172:371–381

    Article  Google Scholar 

  8. Choi CY, Habibi HR (2003) Molecular cloning of estrogen receptor alpha and expression pattern of estrogen receptor subtypes in male and female goldfish. Mol Cell Endocr 204:169–177

    Article  Google Scholar 

  9. Colin PL, Bell LJ (1991) Aspects of the spawning of labrid and scarid fishes (Pisces: Labroidei) at Enewetak Atoll, Marshall Islands with notes on other families. Environ Biol Fish 31:229–260

    Article  Google Scholar 

  10. Filby AL, Thorpe KL, Tyler CR (2006) Multiple molecular effect pathways of an environmental oestrogen in fish. J Mol Endocrinol 37:121–134

    Article  Google Scholar 

  11. Halm S, Martínez-Rodrígueza G, Rodrígueza L, Prat F, Mylonas CC, Carrillo M, Zanuy S (2004) Cloning, characterisation, and expression of three oestrogen receptors (ERα, ERβ1 and ERβ2) in the European sea bass, Dicentrarchus labrax. Mol Cell Endocrinol 223:63–75

    Article  Google Scholar 

  12. Hawkins MB, Thornton JW, Crews D, Skipper JK, Dotte A, Thomas P (2000) Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. P Natl Acad Sci USA 97:10751–10756

    Article  Google Scholar 

  13. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S, Harada N, Kimoto T, Kawato S (2003) Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017? and P450 aromatase localized in neurons. P Natl Acad Sci USA 101:865–870

    Article  Google Scholar 

  14. Hoffman KS, Grau EG (1989) Daytime changes in oocyte development with relation to the tide for the Hawaiian saddleback wrasse, Thalassoma duperrey. J Fish Biol 34:529–546

    Article  Google Scholar 

  15. Holloway CC, Clayton DF (2001) Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci 4:170–175

    Article  Google Scholar 

  16. Hoque MM, Takemura A, Takano K (1998) Annual changes in oocyte development and serum vitellogenin level in the rabbitfish, Siganus canaliculatus (Park), in Okinawa, southern Japan. Fish Sci 64:44–52

    Article  Google Scholar 

  17. Huffman LS, O’Connell LA, Hofmann HA (2013) Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni. Physiol Behav 112–113:77–83

    Article  Google Scholar 

  18. Kazeto Y, Trant JM (2005) Molecular biology of channel catfish brain cytochrome P450 aromatase (CYP19A2): cloning, preovulatory induction of gene expression, hormonal gene regulation and analysis of promoter region. J Mol Endocrinol 35:571–583

    Article  Google Scholar 

  19. Li GL, Liu XC, Lin HR (2007) Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in red-spotted grouper (Epinephelus akaara). Anim Reprod Sci 99:156–166

    Article  Google Scholar 

  20. Ma CH, Dong KW, Yu KL (2000) CDNA cloning and expression of a novel estrogen receptor beta-subtype in goldfish (Carassius auratus). Biochim Biophys Acta 1490:145–152

    Article  Google Scholar 

  21. McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303–1311

    Article  Google Scholar 

  22. Matsuyama M, Adachi S, Nagahama Y, Maruyama K, Matsura S (1990) Diurnal rhythm of serum steroid hormone levels in the Japanese whiting, Sillago japonica, a daily-spawning teleost. Fish Physiol Biochem 8:329–338

    Article  Google Scholar 

  23. Matsuyama M, Morita S, Nasu T, Kashiwagi M (1998) Daily spawning and development of sensitivity to gonadotropin and maturation-inducing steroid in the oocytes of the bambooleaf wrasse, Pseudolabrus japonicas. Environ Biol Fish 52:281–290

    Article  Google Scholar 

  24. Matsuyama M, Onozato S, Kashiwagi M (2002) Endocrine control of diurnal oocyte maturation in the kyusen wrasse, Halichoeres poecilopterus. Zool Sci 19:1045–1053

    Article  Google Scholar 

  25. Menuet A, Pellegrini E, Anglade I, Blaise O, Laudet V, Kah O, Pakdel F (2002) Molecular characterization of three estrogen receptor forms in zebrafish: binding characteristics, transactivation properties, and tissue distributions. Biol Reprod 66:1881–1892

    Article  Google Scholar 

  26. Mu WJ, Wen HS, Shi D, Yang YP (2013) Molecular cloning and expression analysis of estrogen receptor betas (ERβ1 and ERβ2) during gonad development in the Korean rockfish, Sebastes schlegeli. Gene 523:39–49

    Article  Google Scholar 

  27. Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229

    Google Scholar 

  28. Nagler JJ, Cavileer T, Sullivan J, Cyr DG, Rexroad III C (2007) The complete nuclear estrogen receptor family in the rainbow trout: discovery of the novel ERα2 and both ERβ isoforms. Gene 392:164–173

    Article  Google Scholar 

  29. Nagler JJ, Cavileer TD, Verducci JS, Schultz IR, Hook SE, Hayton WL (2012) Estrogen receptor mRNA expression patterns in the liver and ovary of female rainbow trout over a complete reproductive cycle. Gen Comp Endocr 178:556–561

    Article  Google Scholar 

  30. Nelson ER, Habibi HR (2013) Estrogen receptor function and regulation in fish and other vertebrates. Gen Comp Endocr 192:15–24

    Article  Google Scholar 

  31. Nelson ER, Wiehler WB, Cole WC, Habibi HR (2007) Homologous regulation of estrogen receptor subtypes in goldfish (Carassius auratus). Mol Reprod Dev 74:1105–1112

    Article  Google Scholar 

  32. O’Connell LA, Hofmann HA (2012) Social status predicts how sex steroid receptors regulate complex behavior across levels of biological organization. Endocrinology 153:1341–1351

    Article  Google Scholar 

  33. Rasheeda MK, Sridevi P, Senthilkumaran B (2010) Cytochrome P450 aromatases: impact on gonadal development, recrudescence and effect of hCG in the catfish, Clarias gariepinus. Gen Comp Endocr 167:234–245

    Article  Google Scholar 

  34. Ross RM (1983) Annual, semilunar, and diel reproductive rhythms in the Hawaiian labrid Thalassoma duperrey. Mar Biol 72:311–318

    Article  Google Scholar 

  35. Sabo-Attwood T, Kroll KJ, Denslow ND (2004) Differential expression of largemouth bass (Micropterus salmoides) estrogen receptor isotypes alpha, beta, and gamma by estradiol. Mol Cell Endocrinol 218:107–118

    Article  Google Scholar 

  36. Suzuki S, Kuwamura T, Nakashima Y, Karino K, Kohda M (2010) Social factors of group spawning as an alternative mating tactic in the territorial males of the threespot wrasse Halichoeres trimaculatus. Environ Biol Fish 89:71–77

    Article  Google Scholar 

  37. Takemura A, Oya R, Shibata Y, Enomoto Y, Uchimura M, Nakamura S (2008) Role of the tidal cycle in the gonadal development and spawning of the tropical wrasse Halichoeres trimaculatus. Zool Sci 25:572–579

    Article  Google Scholar 

  38. Takemura A, Shibata Y, Takeuchi Y, Hur SP, Sugama N, Badruzzaman M (2012) Effects of hydrostatic pressure on monoaminergic activity in the brain of a tropical wrasse, Halicoeres trimaculatus: possible implication for controlling tidal-related reproductive activity. Gen Comp Endocr 175:173–179

    Article  Google Scholar 

  39. Tchoudakova A, Callard GV (1998) Identification of multiple cyp19 genes encoding different cytochrome p450 aromatase isozymes in brain and ovary. Endocrinology 139:2179–2189

    Article  Google Scholar 

  40. Tchoudakova A, Kishida M, Wood E, Callard GV (2001) Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J Steroid Biochem 78:427–439

    Article  Google Scholar 

  41. Villeneuve DL, Knoebl I, Kahl MD, Jensen KM, Hammermeister DE, Greene KJ, Blake LS, Ankley GT (2006) Relationship between brain and ovary aromatase activity and isoformspecific aromatase mRNA expression in the fathead minnow (Pimephales promelas). Aquat Toxicol 76:353–368

    Article  Google Scholar 

  42. Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleost. Amer Zool 21:325–343

    Article  Google Scholar 

  43. Warner RR (1982) Mating systems, sex change and sexual demography in the rainbow wrasse, Thalassoma lucasanum. Copeia 1982: 653–661

    Article  Google Scholar 

  44. Zwain IH, Yen SS (1999) Neurosteroidogenesis in astrocytes, oligo-dendrocytes, and neurons of the cerebral cortex of rat brain. Endocrinology 140:3843–3852

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sung-Pyo Hur.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Oh, D., Hur, S., Bouchekioua, S. et al. Tide-related Changes in mRNA Abundance of Aromatases and Estrogen Receptors in the Ovary and Brain of the Threespot Wrasse Halichoeres trimaculatus. Ocean Sci. J. 53, 239–249 (2018). https://doi.org/10.1007/s12601-018-0016-0

Download citation

Keywords

  • aromatase
  • brain
  • estrogen receptor
  • ovary
  • tide
  • wrasse