Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지

Sex- and Tissue-related Expression of Two Types of P450 Aromatase mRNA in the Protandrous Black Porgy, Acanthopagrus schlegeli, during Sex Reversal: Expression Profiles Following Exogenous Hormone Administration

  • Min, Tae-Sun (Division of Medical and Pharceutical Science, National Research Foundation of Korea) ;
  • An, Kwang-Wook (Division of Marine Environment & Bioscience, Korea Maritime University) ;
  • Kil, Gyung-Suk (Division of Electrical & Electronic Engineering, Korea Maritime University) ;
  • Choi, Cheol-Young (Division of Marine Environment & Bioscience, Korea Maritime University)
  • Published : 2009.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Cytochrome P450 aromatase (P450arom) catalyzes the conversion of androgens to estrogens and plays an important role in reproduction and development in vertebrates. We investigated the expression patterns of ovarian P450arom (P450aromA) and brain P450arom (P450aromB) mRNA during sex change in black porgy. Maturity was divided into seven stages from male to female (immature testis, mature testis, testicular portion of mostly testis, ovarian portion of mostly testis, testicular portion of mostly ovary, ovarian portion of mostly ovary, and mature ovary). P450aromA expression was significantly higher in the ovarian portion of mostly-ovarian stage fish, and P450aromB expression was highest in the brain of black porgy with mostly-ovarian gonads. Histology showed that testicular tissues were disintegrated with the development of ovarian tissue associated with an increase in the expression of the two P450arom mRNAs during sex change. Interestingly, among various tissues, P450aromA was only expressed in the ovary, and P450aromB was only expressed in the brain. To understand the role of gonadotropin-releasing hormone (GnRH) and estradiol ($E_2$), we injected exogenous hormone (GnRH analogue [GnRHa] and $E_2$) into immature black porgy. In the GnRHa group, expression of the two P450arom genes decreased 12 h after injection, and expression of the two P450arom genes were significantly higher at 6 dafter $E_2$ injection. These results provide useful baseline knowledge on the mechanism of natural sex change in black porgy.

Keywords

References

  1. An KW, Nelson ER, Habibi HR, and Choi CY (2008a) Molecular characterization and expression of three GnRH forms mRNA during gonad sex-change process, and effect of GnRHa on GTH subunits mRNA in the protandrous black porgy (Acanthopagrus schlegeli). Gen Comp Endocrinol 159: 38-45 https://doi.org/10.1016/j.ygcen.2008.07.012
  2. An KW, Nelson ER, Jo Po, Habibi HR, Shin HS, and Choi CY (2008b) Characterization of estrogen receptor ${\beta}2$ and expression of the estrogen receptor subtypes $\alpha$, ${\beta}1$ and ${\beta}2$ in the protandrous black porgy (Acanthopagrus schlegeli) during the sex change process. Comp Biochem Physiol B 150: 284-291 https://doi.org/10.1016/j.cbpb.2008.03.012
  3. Blazquez M and 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 https://doi.org/10.1016/j.mce.2004.01.006
  4. Chang CF, Lee MF, and Chen GR (1994) Estradiol-17${\beta}$ associated with the sex change in protandrous black porgy, Acanthopagrus schlegeli. J Exp Zool 268: 53-58 https://doi.org/10.1002/jez.1402680107
  5. Devlin H and Nagahama Y (2002) Sex determination and sex differentiation in fish; an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364 https://doi.org/10.1016/S0044-8486(02)00057-1
  6. Dubois EA, Slob S, Zandbergen MA, Peute J, and Goos HJTh (2001) Gonadal steroids and the maturation of the speciesspecific gonadotropin-releasinghormone system in brain and pituitary of the male African catfish (Clarias gariepinus). Comp Biochem Physiol B 129: 381-387 https://doi.org/10.1016/S1096-4959(01)00328-1
  7. Forlano PM, Deitcher DL, Myers DA, and Bass AH (2001) Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci 21: 8943-8955
  8. Fukada S, Tanaka M, Matsuyama M, Kobayashi D, and Nagahama Y (1996) Isolation, characterization and expression of cDNAs encoding the medaka (Oryzias latipes) ovarian follicle cytochrome P-450 aromatase. Mol Reprod Dev 45: 285-290 https://doi.org/10.1002/(SICI)1098-2795(199611)45:3<285::AID-MRD4>3.0.CO;2-O
  9. Gelinas D, Pitoc GA, and Callard GV (1998) Isolation of a goldfish brain cytochrome P450 aromatase cDNA: mRNA expression during the seasonal cycle and after steroid treatment. Mol Cell Endocrinol 138: 81-93 https://doi.org/10.1016/S0303-7207(98)00015-X
  10. Gen K, Okuzama K, Kumakura N, Yamaguchi S, and Kagawa H (2001) Correlation between messenger RNA expression of cytochrome P450 aromatase and its enzyme activity during oocyte development in the red seabream (Pagrus major). Biol Reprod 65: 1186-1194 https://doi.org/10.1095/biolreprod65.4.1186
  11. Godwin JR and Thomas P (1993) Sex change and steroid profiles in the protandrous anemone fish Amphiprion melanopus (Pomacentridae, Teleostei). Gen Comp Endocrinol 91: 144-157 https://doi.org/10.1006/gcen.1993.1114
  12. Greytak SR, Champlin D, and Callard GV (2005) Isolation and characterization of two cytochrome P450 aromatase forms in killifish (Fundulus heteroclitus): Differential expression in fish from polluted and unpolluted environments. Aquat Toxicol 71: 371-389 https://doi.org/10.1016/j.aquatox.2004.12.007
  13. Guiguen Y, Jalabert B, Thouard E, and Fostier A (1993) Changes in plasma and gonadal steroid hormones in relation to the reproductive cycle and the sex inversion process in the protandrous seabass, Lates calcarifer. Gen Comp Endocrinol 92: 327-338 https://doi.org/10.1006/gcen.1993.1170
  14. Holland MCH, Hassin S, and Zohar Y (2002) The effects of longterm testosterone, gonadotropin-releasing hormone agonist and pimozide treatments on testicular development and luteinizing hormone levels in juvenile and early maturing striped bass, Morone saxatilis. Gen Comp Endocrinol 129: 178-187 https://doi.org/10.1016/S0016-6480(02)00532-4
  15. Ijiri S, Kazeto Y, Lokman PK, Adachi S, and Yamauchi K (2003) Characterization of a cDNA encoding PA50 aromatase (CYP19) from Japanese eel ovary and its expression in ovarian follicles during induced ovarian development. Gen Comp Endocrinol 130: 193-203 https://doi.org/10.1016/S0016-6480(02)00589-0
  16. Kazeto Y, Goto-Kazeto R, Place AR, and Trant JM (2003) Aromatase expression in zebrafish and channel catfish brains: changes in transcript abundance associated with the reproductive cycle and exposure to endocrine disrupting chemicals. Fish Physiol Biochem 28: 29-32 https://doi.org/10.1023/B:FISH.0000030466.23085.94
  17. Kitano T, Takamune K, Kobayashi T, Nagahama Y, and Abe SI (1999) Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J Mol Endocrinol 23: 167-176 https://doi.org/10.1677/jme.0.0230167
  18. Kwon JY, Haghpanah V, Kogson-Hurtado LM, McAndrew BJ, and Penman DJ (2000) Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J Exp Zool 287: 46-53 https://doi.org/10.1002/1097-010X(20000615)287:1<46::AID-JEZ6>3.0.CO;2-X
  19. Kwon JY, McAndrew BJ, and Penman DJ (2001) Cloning of brain aromatase gene and expression of brain and ovarian aromatase genes during sexual differentiation in genetic male and female Nile tilapia, Oreochromis niloticus. Mol Reprod Dev 59: 359-370 https://doi.org/10.1002/mrd.1042
  20. Kwon JY, McAndrew BJ, and Penman DJ (2002) Treatment with an aromatase inhibitor suppresses high-temperature feminization of genetic male (YY) Nile tilapia. J Fish Biol 60: 625-636 https://doi.org/10.1111/j.1095-8649.2002.tb01689.x
  21. Lee YH, Du JL, Yueh WS, Lin BY, Huang JD, Lee CY, Lee MF, Lau EL, Lee FY, Morrey C, Nagahama Y, and Chang CF (2001) The sex change in the protandrous black porgy, Acanthopagrus schlegeli: goandal development, estradiol receptor, aromatase activity and gonadotropin. J Exp Zool 290: 715-726 https://doi.org/10.1002/jez.1122
  22. Lee YH, Lee FY, Yueh WS, Tacon P,Du JL, Chang CN, Jeng SR, Tanaka H, and Chang CF (2000) Profiles of gonadal development, sex steroids, aromatase activity, and gonadotropin II in the controlled sex change of protandrous black porgy, Acanthopagrus schlegeli Bleeker. Gen Comp Endocrinol 119: 111-120 https://doi.org/10.1006/gcen.2000.7499
  23. Lee YH, Wu GC, Du JL, and Chang CF (2004) Estradiol-17$\beta$ induced a reversible sex change in the fingerlings of protandrous black porgy, Acanthopagrus schlegeli bleeker: the possible roles of luteinizing hormone in sex change. Biol Reprod 71: 1270-1278 https://doi.org/10.1095/biolreprod.104.030221
  24. Lee YH, Yueh WS, Du JL, Sun LT, and Chang CF (2002) Aromatase inhibitors block natural sex change and induce male function in the protandrous black porgy, Acanthopagrus schlegeli Bleeker: possible mechanism of natural sex change. Biol Reprod 66: 251-257 https://doi.org/10.1095/biolreprod66.1.251
  25. Liu X, Liang B, and Shuyi Z (2004) Sequence and expression of cytochrome P450 aromatase and FTZ-FI genes in the protandrous black porgy (Acanthopagrus schlegeli). Gen Comp Endocrinol 138: 247-254 https://doi.org/10.1016/j.ygcen.2004.04.005
  26. Ohtani H, Miura I, and Ichikawa Y (2003) Role of aromatase and androgen receptor expression in gonadal sex differentiation of ZW/ZZ-type frogs, Rana rugosa. Comp Biochem Physiol C 134: 215-225 https://doi.org/10.1016/S1096-4959(02)00254-3
  27. Patil JG and Gunasekera RM (2008) Tissue and sexually dimorphic expression of ovarian and brain aromatase mRNA in the Japanese medaka (Oryzias latipesi: Implications for their preferential roles in ovarian and neural differentiation and development. Gen Comp Endocrinol 158: 131-137 https://doi.org/10.1016/j.ygcen.2008.05.016
  28. Sawyer SJ, Gerstner KA, and Callard GV (2006) Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: Gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen Comp Endocrinol 147: 108-117 https://doi.org/10.1016/j.ygcen.2005.12.010
  29. Simpson EK, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amameh B, Ito Y, Fisher CR, Michael MD, and Mendelson CR (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15: 342-355
  30. Strobl-Mazzulla PH, Moncaut NP, Lopez GC, Miranda LA, Canario AVM, and Somoza GM (2005) Brain aromatase from pejerrey fish (Odontesthes bonariensisy: cDNA cloning, tissue expression, and immunohistochemical localization. Gen Comp Endocrinol 143: 21-32 https://doi.org/10.1016/j.ygcen.2005.02.026