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Steroidogenesis and its regulation in teleost-a review

  • Anbazhagan Rajakumar
  • Balasubramanian SenthilkumaranEmail author
Article

Abstract

Steroid hormones modulate several important biological processes like metabolism, stress response, and reproduction. Steroidogenesis drives reproductive function wherein development and differentiation of undifferentiated gonads into testis or ovary, and their growth and maturation, are regulated. Steroidogenesis occurs in gonadal and non-gonadal tissues like head kidney, liver, intestine, and adipose tissue in teleosts. This process is regulated differently through multi-level modulation of promoter motif transcription factor regulation of steroidogenic enzyme genes to ultimately control enzyme activity and turnover. In view of this, understanding teleostean steroidogenesis provides major inputs for technological innovation of pisciculture. Unlike higher vertebrates, steroidal intermediates and shift in steroidogenesis is critical for gamete maturation in teleosts, more essentially oogenesis. Considering these characteristics, this review highlights the promoter regulation of steroidogenic enzyme genes by several transcription factors that are involved in teleostean steroidogenesis. It also addresses different methodologies involved in promoter regulation studies together with glucocorticoids and androgen relationship with reference to teleosts.

Keywords

Gonadal steroids Testosterone Estradiol Testis Ovary Promoter 

Notes

Acknowledgments

BS is a recipient of Department of Biotechnology-TATA innovation fellowship (BT/HRD/35/01/02/2013). AR is thankful to Council of Scientific and Industrial Research, India, for Junior and Senior Research Fellowships.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Adamski J, Jakob FJ (2001) A guide to 17β-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 171:1–4.  https://doi.org/10.1016/S0303-7207(00)00383-X CrossRefPubMedGoogle Scholar
  2. Baroiller JF, Guiguen Y, Fostier A (1999) Endocrine and environmental aspects of sex differentiation in fish. Cell Mol Life Sci 55:910–931.  https://doi.org/10.1007/s000180050344 CrossRefGoogle Scholar
  3. Baroiller J, D’Cotta H, Bezault E, Wessels S, Hoerstgen-Schwark G (2009) Tilapia sex determination: where temperature and genetics meet. Comp Biochem Physiol A 153:30–38.  https://doi.org/10.1016/j.cbpa.2008.11.018 CrossRefGoogle Scholar
  4. Blasco M, Fernandino JI, Guilgur LG, Strussmann CA, Somoza GM, Vizziano-Cantonnet D (2010) Molecular characterization of cyp11a1 and cyp11b1 and their gene expression profile in pejerrey (Odontesthes bonariensis) during early gonadal development. Comp Biochem Physiol A 156:110–118.  https://doi.org/10.1016/j.cbpa.2010.01.006 CrossRefGoogle Scholar
  5. Blazquez M, Somoza GM (2010) Fish with thermolabile sex determination (TSD) as models to study brain sex differentiation. Gen Comp Endocrinol 166:470–477.  https://doi.org/10.1016/j.ygcen.2009.10.004 CrossRefPubMedGoogle Scholar
  6. Blazquez M, Felip A, Zanuy S, Carrillo M, Piferrer F (2001) Critical period of androgen-inducible sex differentiation in a teleost fish, the European sea bass. J Fish Biol 58:342–358.  https://doi.org/10.1111/j.1095-8649.2001.tb02257.x CrossRefGoogle Scholar
  7. Bogerd J, Blomenrohr M, Andersson E, van der Putten HH, Tensen CP, Vischer HF, Granneman JC, Janssen-Dommerholt C, Goos HJ, Schulz RW (2001) Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish (Clarias gariepinus). Biol Reprod 64:1633–1643.  https://doi.org/10.1095/biolreprod64.6.1633 CrossRefPubMedGoogle Scholar
  8. Borg B (1994) Androgens in teleost fishes. Comp Biochem Physiol C 109:219–245.  https://doi.org/10.1016/0742-8413(94)00063-G CrossRefGoogle Scholar
  9. Cavaco JEB, Vischer HF, Lambert JGD, Goos HJT, Schulz RW (1997) Mismatch between patterns of circulating and testicular androgens in African catfish, Clarias gariepinus. Fish Physiol Biochem 17:155–162.  https://doi.org/10.1023/A:1007716514816 CrossRefGoogle Scholar
  10. Cheshenko K, Brion F, Le Page Y, Hinfray N, Pakdel F, Kah O, Segner H, Eggen R (2007) Expression of zebra fish aromatase cyp19a and cyp19b genes in response to the ligands of estrogen receptor and aryl hydrocarbon receptor. Toxicol Sci 96:255–267.  https://doi.org/10.1093/toxsci/kfm003 CrossRefPubMedGoogle Scholar
  11. Choi J, Smitz J (2014) Luteinizing hormone and human chorionic gonadotropin: origins of difference. Mol Cell Endocrinol 383:203–213.  https://doi.org/10.1016/j.mce.2013.12.009 CrossRefPubMedGoogle Scholar
  12. Chu L, Li J, Liu Y, Cheng CH (2015) Gonadotropin signaling in zebrafish ovary and testis development: insights from gene knockout study. Mol Endocrinol 29:1743–1758.  https://doi.org/10.1210/me.2015-1126 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Devlin RH, 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 CrossRefGoogle Scholar
  14. Diotel N, Page YL, Mouriec K, Tong S-K, Pellegrini E, Vaillant C, Anglade I, Brion F, Pakdel F, Chung BC et al (2010) Aromatase in the brain of teleost fish: expression, regulation and putative functions. F Neuroendocrinol 31:172–192.  https://doi.org/10.1016/j.yfrne.2010.01.003 CrossRefGoogle Scholar
  15. Fernandino JI, Hattori RS, Kishii A, Strussmann CA, Somoza GM (2012) The cortisol and androgen pathways cross talk in high temperature-induced masculinization: the 11β-hydroxysteroid dehydrogenase as a key enzyme. Endocrinology 153:6003–6011.  https://doi.org/10.1210/en.2012-1517 CrossRefPubMedGoogle Scholar
  16. Fernandino JI, Hattori RS, Moreno Acosta OD, Struessmann CA, Somoza GM (2013) Environmental stress-induced testis differentiation: androgen as a by-product of cortisol inactivation. Gen Comp Endocrinol 192:36–44.  https://doi.org/10.1016/j.ygcen.2013.05.024 CrossRefPubMedGoogle Scholar
  17. Francis RC (1992) Sexual lability in teleosts: developmental factors. Q Rev Biol 67:1–18.  https://doi.org/10.1086/417445 CrossRefGoogle Scholar
  18. Fuzzen MLM, Bernier NJ, Van Der Kraak G (2011) Differential effects of 17β-estradiol and 11-ketotestosterone on the endocrine stress response in zebrafish (Danio rerio). Gen Comp Endocrinol 170:365–373.  https://doi.org/10.1016/j.ygcen.2010.10.014 CrossRefPubMedGoogle Scholar
  19. Gade P, Kalvakolanu DV (2012) Chromatin immunoprecipitation assay as a tool for analyzing transcription factor activity. Methods Mol Biol 809:85–104.  https://doi.org/10.1007/978-1-61779-376-9_6 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ge W (2005) Intrafollicular paracrine communication in the zebrafish ovary: the state of the art of an emerging model for the study of vertebrate folliculogenesis. Mol Cell Endocrinol 237:1–10.  https://doi.org/10.1016/j.mce.2005.03.012 CrossRefPubMedGoogle Scholar
  21. Geertz M, Maerkl SJ (2010) Experimental strategies for studying transcription factor-DNA binding specificities. Brief Funct Genomics 9:362–373.  https://doi.org/10.1093/bfgp/elq023 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goos HJT, Senthilkumaran B, Joy KP (1999) Neuroendocrine integrative mechanisms in the control of gonadotropin secretion in teleosts. In: Joy KP, Krishna A, Haldar C (eds) Comparative endocrinology and reproduction. Narousa Publishing House, New Delhi, pp 113–136Google Scholar
  23. Govoroun MS, Pannetier M, Pailhoux E, Cocquet J, Brillard JP, Couty I, Batellier F, Cotinot C (2004) Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev Dyn 231:859–870.  https://doi.org/10.1002/dvdy.20189 CrossRefPubMedGoogle Scholar
  24. Guiguen Y (2000) Implication of steroids in fish gonadal sex differentiation and sex inversion. Curr Top Steroid Res 3:127–143Google Scholar
  25. Guiguen Y, Fostier A, Piferrer F, Chang CF (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352–366.  https://doi.org/10.1016/j.ygcen.2009.03.002 CrossRefPubMedGoogle Scholar
  26. Handa RJ, Pak TR, Kudwa AE, Lund TD, Hinds L (2008) An alternate pathway for androgen regulation of brain function: activation of estrogen receptor β by the metabolite of dihydrotestosterone, 5α-androstane-3β,17β-diol. Horm Behav 53:741–752.  https://doi.org/10.1016/j.yhbeh.2007.09.012 CrossRefPubMedGoogle Scholar
  27. Hattori RS, Fernandino JI, Kishii A, Kimura H, Kinno T, Oura M, Somoza GM, Yokota M, Strussmann CA, Watanabe S (2009) Cortisol induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination? PLoS One 4:e6548.  https://doi.org/10.1371/journal.pone.0006548 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Heckman CA, Boxer LM (2002) Allele-specific analysis of transcription factors binding to promoter regions. Methods 26:19–26.  https://doi.org/10.1016/S1046-2023(02)00004-X CrossRefPubMedGoogle Scholar
  29. Hellman LM, Fried MG (2007) Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nat Protoc 2:1849–1861.  https://doi.org/10.1038/nprot.2007.249 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hinfray N, Nobrega RH, Caulier M, Baudiffier D, Maillot-Marechal E, Chadili E, Palluel O, Porcher JM, Schulz R, Brion F (2013) Cyp17a1 and Cyp19a1 in the zebrafish testis are differentially affected by oestradiol. J Endocrinol 216:375–388.  https://doi.org/10.1530/JOE-12-0509 CrossRefPubMedGoogle Scholar
  31. Hsu HJ, Hsiao P, Kuo MW, Chung BC (2002) Expression of zebrafish cyp11a1 as a maternal transcript and in yolk syncytial layer. Gene Expr Patterns 2:219–222.  https://doi.org/10.1016/S1567-133X(02)00059-5 CrossRefPubMedGoogle Scholar
  32. Hu MC, Hsu HJ, Guo IC, Chung BC (2004) Function of Cyp11a1 in animal models. Mol Cell Endocrinol 215:95–100.  https://doi.org/10.1016/j.mce.2003.11.024 CrossRefPubMedGoogle Scholar
  33. Huang M, Chen J, Liu Y, Chen H, Yu Z, Ye Z, Peng C, Xiao L, Zhao M, Li S, Lin H, Zhang Y (2019) New insights into the role of follicle-stimulating hormone in sex differentiation of the protogynous orange-spotted grouper, Epinephelus coioides. Front Endocrinol (Lausanne) 10:304.  https://doi.org/10.3389/fendo.2019.00304 CrossRefGoogle Scholar
  34. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y (2008) Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78:333–341.  https://doi.org/10.1095/biolreprod.107.064246 CrossRefPubMedGoogle Scholar
  35. Ijiri S, Shibata Y, Takezawa N, Kazeto Y, Takatsuka N, Kato E, Hagihara S, Ozaki Y, Adachi S, Yamauchi K, Nagahama Y (2017) 17β-HSD type 12-like is responsible for maturation-inducing hormone synthesis during oocyte maturation in masu salmon. Endocrinology 158:627–639.  https://doi.org/10.1210/en.2016-1349
  36. Jiang JQ, Kobayashi T, Ge W, Kobayashi H, Tanaka M, Okamoto M, Nonaka Y, Nagahama Y (1996) Fish testicular 11β-hydroxylase: cDNA cloning and mRNA expression during spermatogenesis. FEBS Lett 397:250–252.  https://doi.org/10.1016/S0014-5793(96)01187-8 CrossRefPubMedGoogle Scholar
  37. Jiang JQ, Young G, Kobayashi T, Nagahama Y (1998) Eel (Anguilla japonica) testis 11β-hydroxylase gene is expressed in interrenal tissue and its product lacks aldosterone synthesizing activity. Mol Cell Endocrinol 146:207–211.  https://doi.org/10.1016/S0303-7207(98)00147-6 CrossRefPubMedGoogle Scholar
  38. Jiang JQ, Wang DS, Senthilkumaran B, Kobayashi T, Kobayashi HK, Yamaguchi A, Ge W, Young G, Nagahama Y (2003) Isolation, characterization and expression of 11β-hydroxsteroid dehydrogenase type 2 cDNAs from the testes of Japanese eel (Anguilla japonica) and Nile tilapia (Oreochromis niloticus). J Mol Endocrinol 31:305–315.  https://doi.org/10.1677/jme.0.0310305 CrossRefPubMedGoogle Scholar
  39. Kagawa H, Kasuga Y, Adachi J, Nishi A, Hashimoto H, Imaizumi H, Kaji S (2009) Effects of continuous administration of human chorionic gonadotropin, salmon pituitary extract, and gonadotropin-releasing hormone using osmotic pumps on induction of sexual maturation in male Japanese eel, Anguilla japonica. Aquaculture 296:117–122.  https://doi.org/10.1016/j.aquaculture.2009.07.023 CrossRefGoogle Scholar
  40. Kazeto Y, Ijiri S, Todo T, Adachi S, Yamauchi K (2000) Molecular cloning and characterization of Japanese eel ovarian P450c17 (CYP17) cDNA. Gen Comp Endocrinol 118:123–133.  https://doi.org/10.1006/gcen.1999.7449 CrossRefPubMedGoogle Scholar
  41. Kazeto Y, Ijiri S, Place AR, Zohar Y, Trant JM (2001) The 5′-flanking regions of CYP19A1 and CYP19A2 in zebrafish. Biochem Biophys Res Commun 288:503–508.  https://doi.org/10.1006/bbrc.2001.5796 CrossRefPubMedGoogle Scholar
  42. Kazeto Y, Ijiri S, Adachi S, Yamauchi K (2006) Cloning and characterization of a cDNA encoding cholesterol side-chain cleavage cytochrome P450 (CYP11A1): tissue distribution and changes in the transcript abundance in ovarian tissue of Japanese eel, Anguilla japonica, during artificially induced sexual development. J Steroid Biochem Mol Biol 99:121–128.  https://doi.org/10.1016/j.jsbmb.2005.12.004 CrossRefPubMedGoogle Scholar
  43. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (2003) Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet Genome Res 101:289–294.  https://doi.org/10.1159/000074351 CrossRefPubMedGoogle Scholar
  44. Kobayashi Y, Murata R, Nakamura M (2013) Physiological and endocrinological mechanisms of sex change in the grouper. In: Senthilkumaran B (ed) Sexual plasticity and gametogenesis in fishes. Nova Biomedical, Waltham, pp 221–234Google Scholar
  45. Kusakabe M, Nakamura I, Young G (2003) 11β-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. Endocrinology 144:2534–2545.  https://doi.org/10.1210/en.2002-220446 CrossRefPubMedGoogle Scholar
  46. Lau ES, Zhang Z, Qin M, Ge W (2016) Knockout of zebrafish ovarian aromatase gene (cyp19a1a) by TALEN and CRISPR/Cas9 leads to all-male offspring due to failed ovarian differentiation. Sci Rep 6:37357.  https://doi.org/10.1038/srep37357 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Levavi-Sivan B, Bogerd J, Mananos EL, Gomez A, Lareyre JJ (2009) Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol 165:412–437.  https://doi.org/10.1016/j.ygcen.2009.07.019 CrossRefPubMedGoogle Scholar
  48. Liu S, Govoroun M, D’Cotta H, Ricordel MJ, Lareyre JJ, McMeel OM, Smith T, Nagahama Y, Guiguen Y (2000) Expression of cytochrome P450 (11β) (11β-hydroxylase) gene during gonadal sex differentiation and spermatogenesis in rainbow trout, Oncorhynchus mykiss. J Steroid Biochem Mol Biol 75:291–298.  https://doi.org/10.1016/S0960-0760(00)00186-2 CrossRefPubMedGoogle Scholar
  49. Lokman PM, Harris B, Kusakabe M, Kime DE, Schulz RW, Adachi S, Young G (2002) 11-oxygenated androgens in female teleosts: prevalence, abundance, and life history implications. Gen Comp Endocrinol 129:1–12.  https://doi.org/10.1016/S0016-6480(02)00562-2 CrossRefPubMedGoogle Scholar
  50. Margiotta-Casaluci L, Sumpter JP (2011) 5α-Dihydrotestosterone is a potent androgen in the fathead minnow (Pimephales promelas). Gen Comp Endocrinol 171:309–318.  https://doi.org/10.1016/j.ygcen.2011.02.012 CrossRefPubMedGoogle Scholar
  51. Margiotta-Casaluci L, Courant F, Antignac JP, Le Bizec B, Sumpter JP (2013) Identification and quantification of 5α-dihydrotestosterone in the teleost fathead minnow (Pimephales promelas) by gas chromatography-tandem mass spectrometry. Gen Comp Endocrinol 191:202–209.  https://doi.org/10.1016/j.ygcen.2013.06.017 CrossRefPubMedGoogle Scholar
  52. Mayer I, Borg B, Schulz R (1990) Seasonal changes in and effect of castration/androgen replacement on the plasma levels of five androgens in the male three spined stickleback, Gasterosteus aculeatus L. Gen Comp Endocrinol 79:23–30.  https://doi.org/10.1016/0016-6480(90)90084-Y CrossRefPubMedGoogle Scholar
  53. Meyer A, Schartl M (1999) Gene and genome duplications in vertebrates: the one-to-four (-to eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11:699–704.  https://doi.org/10.1016/S0955-0674(99)00039-3 CrossRefPubMedGoogle Scholar
  54. Meyer A, Van De Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945.  https://doi.org/10.1002/bies.20293 CrossRefPubMedGoogle Scholar
  55. Mills LJ, Gutjahr-Gobell RE, Zaroogian GE, Horowitz DB, Laws SC (2014) Modulation of aromatase activity as a mode of action for endocrine disrupting chemicals in a marine fish. Aquat Toxicol 147:140–150.  https://doi.org/10.1016/j.aquatox.2013.12.023 CrossRefPubMedGoogle Scholar
  56. Mindnich R, Moller G, Adamski J (2004) The role of 17β-hydroxysteroid dehydrogenase. Mol Cell Endocrinol 218:7–20.  https://doi.org/10.1016/j.mce.2003.12.006 CrossRefPubMedGoogle Scholar
  57. Miura T, Yamauchi K, Takahashi H, Nagahama Y (1992) The role of hormones in the acquisition of sperm motility in salmonid fish. J Exp Zool 261:359–363.  https://doi.org/10.1002/jez.1402610316 CrossRefPubMedGoogle Scholar
  58. Moeller G, Adamski J (2009) Integrated view on 17β-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 301:7–19.  https://doi.org/10.1016/j.mce.2008.10.040 CrossRefPubMedGoogle Scholar
  59. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268.  https://doi.org/10.1023/A:1008924418720 CrossRefGoogle Scholar
  60. Murugananthkumar R, Senthilkumaran B (2016) Expression analysis and localization of wt1, ad4bp/sf-1 and gata4 in the testis of catfish, Clarias batrachus: impact of wt1-esiRNA silencing. Mol Cell Endocrinol 431:164–176.  https://doi.org/10.1016/j.mce.2016.05.006 CrossRefPubMedGoogle Scholar
  61. Murugananthkumar R, Prathibha Y, Senthilkumaran B, Rajakumar A, Kagawa H (2017) In vivo induction of human chorionic gonadotropin by osmotic pump advances sexual maturation during pre-spawning phase in adult catfish. Gen Comp Endocrinol 251:74–84.  https://doi.org/10.1016/j.ygcen.2016.09.015 CrossRefPubMedGoogle Scholar
  62. Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229PubMedGoogle Scholar
  63. Nagahama Y, Yoshikuni M, Yamashita M, Tukumono T, Katsu Y (1995) Regulation of oocyte growth and maturation in fish. Curr Top Dev Biol 30:103–145.  https://doi.org/10.1016/S0070-2153(08)60565-7 CrossRefPubMedGoogle Scholar
  64. Nakamura S, Kobayashi K, Nishimura T, Higashijima S, Tanaka M (2010) Identification of germline stem cells in the ovary of the teleost medaka. Science 328:1561–1563.  https://doi.org/10.1126/science.1185473 CrossRefPubMedGoogle Scholar
  65. Nakamura I, Kusakabe M, Swanson P, Young G (2016) Regulation of sex steroid production and mRNAs encoding gonadotropin receptors and steroidogenic proteins by gonadotropins, cyclic AMP and insulin-like growth factor-I in ovarian follicles of rainbow trout (Oncorhynchus mykiss) at two stages of vitellogenesis. Comp Biochem Physiol A Mol Integr Physiol 201:132–140.  https://doi.org/10.1016/j.cbpa.2016.06.035 CrossRefPubMedGoogle Scholar
  66. Navarro-Martin L, Vinas J, Ribas L, Diaz N, Gutierrez A, Di Croce L, Piferrer F (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet 7:1–15.  https://doi.org/10.1371/journal.pgen.1002447 CrossRefGoogle Scholar
  67. Nematollahi MA, van Pelt-Heerschap H, Komen J (2009) Transcript levels of five enzymes involved in cortisol synthesis and regulation during the stress response in common carp: relationship with cortisol. Gen Comp Endocrinol 164:85–90.  https://doi.org/10.1016/j.ygcen.2009.05.006 CrossRefPubMedGoogle Scholar
  68. Oppermann UC, Persson B, Filling C, Jornvall H (1997) Structure/function relationships of SDR hydroxysteroid dehydrogenases. Adv Exp Med Biol 414:403–415.  https://doi.org/10.1007/978-1-4615-4735-8_48 CrossRefPubMedGoogle Scholar
  69. Ozaki Y, Higuchi M, Miura C, Yamaguchi S, Tozawa Y, Miura T (2006) Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis. Endocrinology 147:5139–5146.  https://doi.org/10.1210/en.2006-0391 CrossRefPubMedGoogle Scholar
  70. Parajes S, Griffin A, Taylor AE, Rose IT, Miguel-Escalada I, Hadzhiev Y, Arlt W, Shackleton C, Müller F, Krone N (2013) Redefining the initiation and maintenance of zebrafish interrenal steroidogenesis by characterizing the key enzyme Cyp11a2. Endocrinology 154:2702–2711.  https://doi.org/10.1210/en.2013-1145 CrossRefPubMedGoogle Scholar
  71. Payne AH, Youngblood GL (1995) Regulation of expression of steroidogenic enzymes in Leydig cells. Biol Reprod 52:217–225.  https://doi.org/10.1095/biolreprod52.2.217 CrossRefPubMedGoogle Scholar
  72. Peter RE, Trudeau VL, Sloley BD (1991) Brain regulation of reproduction in teleosts. Bull Inst Zool Acad Sin Monogr 16:89–118Google Scholar
  73. Prisco M, Liguoro A, Ricchiari L, Del Giudice G, Angelini F, Andreuccetti P (2008) Immunolocalization of 3β-hsd and 17β-hsd in the testis of the spotted ray Torpedo marmorata. Gen Comp Endocrinol 155:157–163.  https://doi.org/10.1016/j.ygcen.2007.04.016 CrossRefPubMedGoogle Scholar
  74. Quek SI, Chan WK (2009) Transcriptional activation of zebrafish cyp11a1 promoter is dependent on the nuclear receptor Ff1b. J Mol Endocrinol 43:121–130.  https://doi.org/10.1677/JME-09-0029 CrossRefPubMedGoogle Scholar
  75. Raghuveer K, Senthilkumaran B (2009) Identification of multiple dmrt1s in catfish: localization, dimorphic expression pattern, changes during testicular cycle and after methyltestosterone treatment. J Mol Endocrinol 42:437–448.  https://doi.org/10.1677/JME-09-0011 CrossRefPubMedGoogle Scholar
  76. Raghuveer K, Senthilkumaran B, Sudhakumari CC, Sridevi P, Rajakumar A, Singh R, Murugananthkumar R, Majumdar KC (2011) Dimorphic expression of various transcription factor and steroidogenic enzyme genes during gonadal ontogeny in the air-breathing catfish, Clarias gariepinus. Sex Dev 5:213–223.  https://doi.org/10.1159/000328823 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Rajakumar A, Senthilkumaran B (2013) Sperm maturation in teleosts: role of androgens and progestins in our present understanding to emerging new concepts. In: Senthilkumaran B (ed) Sexual plasticity and gametogenesis in fishes. Nova Biomedical, Waltham, pp 377–400Google Scholar
  78. Rajakumar A, Senthilkumaran B (2014a) Expression analysis of cyp11a1 during gonadal development, recrudescence and after hCG induction and sex steroid analog treatment in the catfish, Clarias batrachus. Comp Biochem Physiol B 176:42–47.  https://doi.org/10.1016/j.cbpb.2014.07.007 CrossRefPubMedGoogle Scholar
  79. Rajakumar A, Senthilkumaran B (2014b) Molecular cloning and expression analysis of 17β-hydroxysteroid dehydrogenase 1 and 12 during gonadal development, recrudescence and after in vivo hCG induction in catfish, Clarias batrachus. Steroids 92:81–89.  https://doi.org/10.1016/j.steroids.2014.09.009 CrossRefPubMedGoogle Scholar
  80. Rajakumar A, Senthilkumaran B (2015) Dynamic expression of 11β-hydroxylase during testicular development, recrudescence and after in vivo and in vitro hCG induction in the catfish, Clarias batrachus. Gen Comp Endocrinol 211:69–80.  https://doi.org/10.1016/j.ygcen.2014.11.010 CrossRefPubMedGoogle Scholar
  81. Rajakumar A, Senthilkumaran B (2016) Sox3 binds to 11β-hydroxysteroid dehydrogenase gene promoter suggesting transcriptional interaction in catfish. J Steroid Biochem Mol Biol 158:90–103.  https://doi.org/10.1016/j.jsbmb.2016.01.003 CrossRefPubMedGoogle Scholar
  82. Rasheeda MK, Kagawa H, Kirubagaran R, Dutta-Gupta A, Senthilkumaran B (2010a) Cloning, expression and enzyme activity analysis of testicular 11β-hydroxysteroid dehydrogenase during seasonal cycle and after hCG induction in air-breathing catfish Clarias gariepinus. J Steroid Biochem Mol Biol 120:1–10.  https://doi.org/10.1016/j.jsbmb.2010.02.014 CrossRefPubMedGoogle Scholar
  83. Rasheeda MK, Sridevi P, Senthilkumaran B (2010b) Cytochrome P450 aromatases: impact on gonadal development, recrudescence and effect of hCG in the catfish, Clarias gariepinus. Gen Comp Endocrinol 167:234–245.  https://doi.org/10.1016/j.ygcen.2010.03.009 CrossRefPubMedGoogle Scholar
  84. Rashid H, Kitano H, Lee KH, Nii S, Shigematsu T, Kadomura K, Yamaguchi A, Matsuyama M (2007) Fugu (Takifugu rubripes) sexual differentiation: CYP19 regulation and aromatase inhibitor induced testicular development. Sex Dev 1:311–322.  https://doi.org/10.1159/000108935 CrossRefPubMedGoogle Scholar
  85. Rasmussen MK, Ekstrand B, Zamaratskaia G (2013) Regulation of 3β-hydroxysteroid dehydrogenase δ5-δ4 isomerase: a review. Int J Mol Sci 14:17926–17942.  https://doi.org/10.3390/ijms140917926 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Rege J, Garber S, Conley AJ, Elsey RM, Turcu AF, Auchus RJ, Rainey WE (2019) Circulating 11-oxygenated androgens across species. J Steroid Biochem Mol Biol 190:242–249.  https://doi.org/10.1016/j.jsbmb.2019.04.005 CrossRefPubMedGoogle Scholar
  87. Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556.  https://doi.org/10.1016/j.ygcen.2009.07.004 CrossRefPubMedGoogle Scholar
  88. Schreck CB, Contreras-Sanchez W, Fitzpatrick MS (2001) Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197:3–24.  https://doi.org/10.1016/S0044-8486(01)00580-4 CrossRefGoogle Scholar
  89. Schulz RW, França LR, Lareyre JJ, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411.  https://doi.org/10.1016/j.ygcen.2009.02.013 CrossRefPubMedGoogle Scholar
  90. Scott AP, Sumpter JP, Stacey N (2010) The role of the maturation-inducing steroid, 17,20β-dihydroxypregn-4-en-3- one, in male fishes: a review. J Fish Biol 76:183–224.  https://doi.org/10.1111/j.1095-8649.2009.02483.x CrossRefPubMedGoogle Scholar
  91. Senthilkumaran B (2011) Recent advances in meiotic maturation and ovulation: comparing mammals and pisces. Front Biosci 16:1898–1914.  https://doi.org/10.2741/3829 CrossRefGoogle Scholar
  92. Senthilkumaran B (2015) Pesticide- and sex steroid analogue-induced endocrine disruption differentially targets hypothalamo–hypophyseal–gonadal system during gametogenesis in teleosts – A review. General and Comparative Endocrinology 219:136–142.  https://doi.org/10.1016/j.ygcen.2015.01.010 CrossRefGoogle Scholar
  93. Senthilkumaran B, Joy KP (1996) Effects of administration of some monoamine synthesis blockers and precursors on ovariectomy-induced rise in plasma gonadotropin II in the catfish Heteropneustes fossilis. Gen Comp Endocrinol 101:220–226.  https://doi.org/10.1006/gcen.1996.0024 CrossRefPubMedGoogle Scholar
  94. Senthilkumaran B, Sudhakumari CC, Chang XT, Kobayashi T, Oba Y, Guan G, 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.  https://doi.org/10.1095/biolreprod67.4.1080 CrossRefPubMedGoogle Scholar
  95. Senthilkumaran B, Yoshikuni M, Nagahama Y (2004) A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol 215:11–18.  https://doi.org/10.1016/j.mce.2003.11.012 CrossRefPubMedGoogle Scholar
  96. Senthilkumaran B, Sudhakumari CC, Wang DS, Sreenivasulu G, Kobayashi T, Kobayashi HK, Yoshikuni M, Nagahama Y (2009) Novel 3β-hydroxysteroid dehydrogenases from gonads of the Nile tilapia: phylogenetic significance and expression during reproductive cycle. Mol Cell Endocrinol 299:146–152.  https://doi.org/10.1016/j.mce.2008.11.008 CrossRefPubMedGoogle Scholar
  97. Senthilkumaran B, Sreenivasulu G, Wang DS, Sudhakumari CC, Kobayashi T, Nagahama Y (2015) Expression patterns of CREBs in oocyte growth and maturation of fish. PLoS One 10:e0145182.  https://doi.org/10.1371/journal.pone.0145182 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Socorro S, Martins RS, Deloffre L, Mylonas CC, Canario AV (2007) A cDNA for European sea bass (Dicentrachus labrax) 11β-hydroxylase: gene expression during the thermosensitive period and gonadogenesis. Gen Comp Endocrinol 150:164–173.  https://doi.org/10.1016/j.ygcen.2006.07.018 CrossRefPubMedGoogle Scholar
  99. Sourdaine P, Garnier DH (1993) Stage-dependent modulation of Sertoli cell steroid production in dogfish (Scyliorhinus canicula). J Reprod Fertil 97:133–142.  https://doi.org/10.1530/jrf.0.0970133 CrossRefPubMedGoogle Scholar
  100. Sreenivasulu G, Senthilkumaran B (2009) A role for cytochrome P450 17alpha-hydroxylase and c17-20lyase during shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. J Steroid Biochem Mol Biol 115:77–85.  https://doi.org/10.1016/j.jsbmb.2009.03.004 CrossRefPubMedGoogle Scholar
  101. Sreenivasulu G, Senthilkumaran B, Sridevi P, Rajakumar A, Rasheeda MK (2012a) Expression and immunolocalization of 20β-hydroxysteroid dehydrogenase during testicular cycle and after hCG induction, in vivo in the catfish, Clarias gariepinus. Gen Comp Endocrinol 175:48–54.  https://doi.org/10.1016/j.ygcen.2011.09.002 CrossRefPubMedGoogle Scholar
  102. Sreenivasulu G, Senthilkumaran B, Sudhakumari CC, Guan G, Oba Y, Kagawa H, Nagahama Y (2012b) 20β-Hydroxysteroid dehydrogenase gene promoter: potential role for cyclic AMP and xenobiotic responsive elements. Gene 509:68–76.  https://doi.org/10.1016/j.gene.2012.07.017 CrossRefPubMedGoogle Scholar
  103. Sridevi P, Chaitanya RK, Dutta-Gupta A, Senthilkumaran B (2012) FTZ-F1 and FOXL2 up-regulate catfish brain aromatase gene by specific binding to promoter motifs. Biochim Biophys Acta 1819:57–66.  https://doi.org/10.1016/j.bbagrm.2011.10.003 CrossRefPubMedGoogle Scholar
  104. Stocco DM (2000) The role of the StAR protein in steroidogenesis: challenges for the future. J Endocrinol 164:247–253.  https://doi.org/10.1677/joe.0.1640247 CrossRefPubMedGoogle Scholar
  105. Su T, Ijiri S, Kanbara H, Hagihara S, Wang DS, Adachi S (2015) Characterization and expression of cDNAs encoding P450c17-II (cyp17a2) in Japanese eel during induced ovarian development. Gen Comp Endocrinol 221:134–143.  https://doi.org/10.1016/j.cbpa.2016.03.012 CrossRefPubMedGoogle Scholar
  106. Sudhakumari CC, Senthilkumaran B (2013) Expression profiling of various marker genes involved in gonadal differentiation of teleosts: molecular understanding of sexual plasticity. In: Senthilkumaran B (ed) Sexual plasticity and gametogenesis in fishes. Nova Biomedical, Waltham, pp 401–421Google Scholar
  107. Suzuki H, Kazeto Y, Gen K, Ozaki Y (2019) Functional analysis of recombinant single-chain Japanese eel Fsh and Lh produced in FreeStyle 293-F cell lines: binding specificities to their receptors and differential efficacy on testicular steroidogenesis. Gen Comp Endocrinol 285:113241.  https://doi.org/10.1016/j.ygcen.2019.113241 CrossRefPubMedGoogle Scholar
  108. Swart AC, Schloms L, Storbeck KH, Bloem LM, Toit TD, Quanson JL, Rainey WE, Swart P (2013) 11β-Hydroxyandrostenedione, the product of androstenedione metabolism in the adrenal, is metabolized in LNCaP cells by 5α-reductase yielding 11β-hydroxy-5α-androstanedione. J Steroid Biochem Mol Biol 138:132–142.  https://doi.org/10.1016/j.jsbmb.2013.04.010 CrossRefPubMedGoogle Scholar
  109. Tanaka SS, Nishinakamura R (2014) Regulation of male sex determination: genital ridge formation and Sry activation in mice. Cell Mol Life Sci 71:4781–4802.  https://doi.org/10.1007/s00018-014-1703-3 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Tanaka M, Telecky TM, Fukada S, Adachi S, Chen S, Nagahama Y (1992) Cloning and sequence analysis of the cDNA encoding P-450 aromatase (P450arom) from a rainbow trout (Oncorhynchus mykiss) ovary: relationship between the amount of P450arom mRNA and the production of oestradiol-17β in the ovary. J Mol Endocrinol 8:53–61.  https://doi.org/10.1677/jme.0.0080053 CrossRefPubMedGoogle Scholar
  111. 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 Mol Biol 78:427–439.  https://doi.org/10.1016/S0960-0760(01)00120-0 CrossRefPubMedGoogle Scholar
  112. Tokarz J, Mindnich R, Norton W, Möller G, Hrabé de Angelis M, Adamski J (2012) Discovery of a novel enzyme mediating glucocorticoid catabolismin fish: 20β-hydroxysteroid dehydrogenase type 2. Mol Cell Endocrinol 349:202–213.  https://doi.org/10.1016/j.mce.2011.10.022 CrossRefPubMedGoogle Scholar
  113. Tokarz J, Möller G, Hrabě de Angelis M, Adamski J (2015) Steroids in teleost fishes: a functional point of view. Steroids 103:123–144.  https://doi.org/10.1016/j.steroids.2015.06.011 CrossRefPubMedGoogle Scholar
  114. Trant JM, Thomas P (1989) Isolation of a novel maturation-inducing steroid produced in vitro by ovaries of Atlantic croaker. Gen Comp Endocrinol 75:397–404.  https://doi.org/10.1016/0016-6480(89)90174-3 CrossRefPubMedGoogle Scholar
  115. Valle LD, Lunardi L, Belvedere CP (2002) European sea bass (Dicentratus labrax L) cytochrome P450arom: cDNA cloning, expression and genomic organization. J Steroid Biochem Mol Biol 80:25–34.  https://doi.org/10.1016/S0960-0760(01)00170-4 CrossRefPubMedGoogle Scholar
  116. Vischer HF, Granneman JC, Noordam MJ, Mosselman S, Bogerd J (2003) Ligand selectivity of gonadotropin receptors role of the beta-strands of extracellular leucine-rich repeats 3 and 6 of the human luteinizing hormone receptor. J Biol Chem 278:15505–15513.  https://doi.org/10.1074/jbc.M300634200 CrossRefPubMedGoogle Scholar
  117. Vizziano D, Randuineau G, Baron D, Cauty C, Guiguen Y (2007) Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev Dyn 236:2198–2206.  https://doi.org/10.1002/dvdy.21212 CrossRefPubMedGoogle Scholar
  118. Wang XG, Orban L (2007) Anti-mullerian hormone and 11β-hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males. Dev Dyn 236:1329–1338.  https://doi.org/10.1002/dvdy.21129 CrossRefPubMedGoogle Scholar
  119. 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 in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 21:712–725.  https://doi.org/10.1210/me.2006-0248 CrossRefPubMedGoogle Scholar
  120. 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.  https://doi.org/10.1016/S0303-7207(99)00006-4 CrossRefPubMedGoogle Scholar
  121. Wilhelm D, Palmer S, Koopman P (2007) Sex determination and gonadal development in mammals. Physiol Rev 87:1–28.  https://doi.org/10.1152/physrev.00009.2006 CrossRefPubMedGoogle Scholar
  122. Yamaguchi T, Yoshinaga N, Yazawa T, Gen K, Kitano T (2010) Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 151:3900–3908.  https://doi.org/10.1210/en.2010-0228 CrossRefPubMedGoogle Scholar
  123. Yan Y, Chen H, Costa M (2004) Chromatin immunoprecipitation assays. Methods Mol Biol 287:9–19.  https://doi.org/10.1385/1-59259-828-5:009 CrossRefPubMedGoogle Scholar
  124. Yazawa T, Uesaka M, Inaoka Y, Mizutani T, Sekiguchi T, Kajitani T, Kitano T, Umezawa A, Miyamoto K (2008) Cyp11b1 is induced in the murine gonad by luteinizing hormone/human chorionic gonadotropin and involved in the production of 11-ketotestosterone, a major fish androgen: conservation and evolution of the androgen metabolic pathway. Endocrinology 149:1786–1792.  https://doi.org/10.1210/en.2007-1015 CrossRefPubMedGoogle Scholar
  125. Yoshiura Y, Senthilkumaran B, Watanabe M, Oba Y, Kobayashi T, Nagahama Y (2003) Synergistic expression of Ad4BP/SF-1 and cytochrome P- 450 aromatase (ovarian type) in the ovary of Nile tilapia, Oreochromis niloticus, during vitellogenesis suggests transcriptional interaction. Biol Reprod 68:1545–1553.  https://doi.org/10.1095/biolreprod.102.010843 CrossRefPubMedGoogle Scholar
  126. Young G, Kusakabe M, Nakamura I, Lokman PM, Goetz FW (2004) Gonadal steroidogenesis in teleost fish. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. World Scientific, New Jersey, pp 155–223Google Scholar
  127. Zhang WL, Zhou LY, Senthilkumaran B, Huang BF, Sudhakumari CC, Kobayashi T, Nagahama Y, Wang DS (2010) Molecular cloning of two isoforms of 11β-hydroxylase and their expressions in the Nile tilapia, Oreochromis niloticus. Gen Comp Endocrinol 165:34–41.  https://doi.org/10.1016/j.ygcen.2009.05.018 CrossRefPubMedGoogle Scholar
  128. Zhou LY, Wang DS, Senthilkumaran B, Yoshikuni M, Shibata Y, Kobayashi T, Sudhakumari CC, Nagahama Y (2005) Cloning, expression and characterization of three types of 17β-hydroxysteroid dehydrogenases from the Nile tilapia, Oreochromis niloticus. J Mol Endocrinol 35:103–116.  https://doi.org/10.1677/jme.1.01801 CrossRefPubMedGoogle Scholar
  129. 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 148:4282–4291.  https://doi.org/10.1210/en.2007-0487 CrossRefPubMedGoogle Scholar
  130. 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 362:619–625.  https://doi.org/10.1016/j.bbrc.2007.08.044 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  • Anbazhagan Rajakumar
    • 1
    • 2
  • Balasubramanian Senthilkumaran
    • 1
    Email author
  1. 1.Department of Animal BiologySchool of Life Sciences, University of Hyderabad, P.O. Central UniversityHyderabadIndia
  2. 2.Present Address: Section on Molecular Endocrinology, National Institute of Child Health and Human Development (NICHD)National Institutes of Health (NIH)BethesdaUSA

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