Abstract
The 17β-hydroxysteroid dehydrogenases (17β-HSDs) are key enzymes in the downstream process of steroid hormone biosynthesis. To date, relatively little is known about the role of 17β-HSDs in marine gastropods. In the present study, a putative cDNA sequence encoding type 12 17β-HSD (17β-HSD-12) was identified in abalone (Haliotis diversicolor supertexta). The full-length cDNA was 1,978 bp, including an open reading frame (ORF) of 963 bp that encoded a protein of 321 amino acids. Comparative structural analysis revealed that abalone 17β-HSD-12 shared 39.8–42.8% amino acid identity with other 17β-HSD-12 homologues and that the functional domains were well conserved. Phylogenetic analysis revealed that abalone 17β-HSD-12 belonged to the short-chain dehydrogenases/reductases (SDRs) family. Functional analysis following transient transfection of the ORF in human embryonic kidney-293 (HEK-293) cells indicated that abalone 17β-HSD-12 had the ability to convert estrone (E1) into estradiol (E2). Expression analysis in vivo demonstrated that abalone 17β-HSD-12 was differentially expressed during the three reproductive stages (pre-spawning, spawning, and post-spawning). These results indicate that abalone 17β-HSD-12 is an SDR family member with a key role in steroidogenesis during the reproductive period.
Similar content being viewed by others
Abbreviations
- 17β-HSD 12:
-
17β-Hydroxysteroid dehydrogenase 12
- SDRs:
-
Short-chain dehydrogenases/reductases
- E1:
-
Estrone
- E2:
-
Estradiol
- ORF:
-
Open reading frames
- HEK-293:
-
Human embryonic kidney-293 cells
References
Adamski J, Jakob FJ (2001) A guide to 17β-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 171:1–4
Persson B, Kallberg Y, Bray JE, Bruford E, Dellaporta SL, Favia AD, Duarte RG, Jornvall H, Kavanagh KL, Kedishvili N, Kisiela M, Maser E, Mindnich R, Orchard S, Penning TM, Thornton JM, Adamski J, Oppermann U (2009) The SDR (short-chain dehydrogenase/reductase and related enzymes) nomenclature initiative. Chem Biol Interact 178:94–98
Lefebvre YA, Schultz R, Groman EN, Watanabe M (1979) Localization of 3β- and 17β-hydroxysteroid dehydrogenases in Pseudomonas testosterone. J Steroid Biochem 10:523–528
Lanisnik RT, Adamski J, Zakelj-Mavric M (2001a) Expression of 17β-hydroxysteroid dehydrogenases in mesophilic and extremophilic yeast. Steroids 66:49–54
Lanisnik RT, Stojan J, Adamski J (2001b) 17β-Hydroxysteroid dehydrogenases from the fungus Cochilobolus lunatus: structure and functional aspects. Chem Biol Interact 130–132:793–803
Kristan K, Stojan J, Adamski J, Rizner TL (2007) Rational design of novel mutants of fungal 17β-hydroxysteroid dehydrogenase. J Biotechnol 129:123–130
Penning TM, Jin Y, Heredia VV, Lewis M (2003) Structure–function relationships in 3α-hrdroxysteroid dehydrogenases: a comparison of the rat and human isoforms. J Steroid Biochem Mol Biol 85:247–255
Mindnich R, Moller G, Adamski J (2004) The role of 17β-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 218:7–20
Lafont R, Mathieu M (2007) Steriods in aquatic invertebrates. Ecotoxicology 16:109–130
Nakamura Y, Hornsby PJ, Casson P, Morimoto R, Satoh F, Xing YW, Kennedy MR, Sasano H, Rainey WE (2009) Type 5 17β-hydroxysteroid dehydrogenase (AKR1C3) contributes to testosterone production in the adrenal reticularis. J Clin Endocrinol Metab 94:2192–2198
Moeller G, Adamski J (2009) Integrated view of 17beta-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 301:7–19
Wu X, Lukacik P, Kayanagh KL, Oppermann U (2007) SDR-type human hydroxysteroid dehydrogenases involved in steroid hormone activation. Mol Cell Endocrine 265–266:71–76
Moeller G, Adamski J (2006) Multifunctionality of human 17β-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 248:47–55
Pearce ST, Jordan VC (2004) The biological role of estrogen receptors α and β. Crit Rev Oncol Hematol 50:3–22
Castro LFC, Lima D, Machado A, Rocha E, Reis-Henriques MA, Santos MM (2010) Molecular characterization of 17β-hydroxysteroid dehydrogenase type 12 in the neogastropod Nucella lapillus. http://www.ciimar.up.pt/letox/images/CECE2008.pdf
Mindnich R, Adamski J (2009) Zebrafish 17beta-hydroxysteroid dehydrogenases: an evolutionary perspective. Mol Cell Endocrinol 301:20–26
Ings JS, Van DKGJ (2006) Characterization of the mRNA expression of StAR and steroidogenic enzymes in zebrafish ovarian follicles. Mol Reprod Dev 73:943–954
Kazeto Y, Ijiri S, Matsubara H, Adachi S, Yamauchi K (2000) Cloning of 17beta-hydroxysteroid dehydrogenase-I cDNAs from Japanese eel ovary. Biochem Biophys Res Commun 279:451–456
Wasson KM, Gower BA, Hines GA, Watts SA (2000) Levels of progesterone, testosterone, and estradiol, and androstenedione metabolism in the gonads of Lytechinus variegates (Echinodermata: echinoidea). Comp Biochem Physiol C 126:153–165
Kho KH, Inaba K (2004) Expression of 17 beta-hydroxysteroid dehydrogenease in testis of the ascidian Ciona intestinalis. Mol Cells 18:171–176
Ghosh D, Ray AK (1993) 17β-Hydroxysteroid dehydrogenease activity of ovary and hepatopancreas of freshwater prawn, Macrobrachium rosenbergii: relation to ovarian condition and estrogen treatment. Gen Comp Endocrinol 89:248–254
Le Curieux-Belfond O, Moslemi S, Mathieu M, Séralini GE (2001) Androgen metabolism in oyster Crassostrea gigas: evidence for 17beta-HSD activities and characterization of an aromatase-like activity inhibited by pharmacological compounds and a marine pollutant. J Steroid Biochem Mol Biol 78:359–366
Di Cristo C, Di Donato P, Palumbo A, d’Ischia M, Paolucci M, Di Cosmo A (2010) Steroidogenesis in the brain of Sepia officinalis and Octopus vulgaris. Front Biosci (Elite Ed). 2:673–683
Tarrant AM, Blomquist CH, Lima PH, Atkinson MJ, Atkinson S (2003) Metabolism of estrogens and androgens by scleractinian corals. Comp Biochem Physiol B 136:473–485
Twan WH, Hwang JS, Chang CF (2003) Sex steroids in scleractinian coral, Eupphyllia ancora: implication in mass spawning. Biol Reprod 68:2255–2260
Prehna C, Möllera G, Adamski J (2009) Recent advances in 17beta-hydroxysteroid dehydrogenases. J Steroid Biochem Mol Biol 114:72–77
Blanchard PG, Luu-The V (2007) Differential androgen and estrogen substances specificity in the mouse and primates type 12 17β-hrdroxysteroid dehydrogenase. J Endocrinol 194:449–455
Nagasaki S, Suzuki T, Miki Y, Akahira J, Kitada K, Ishida T, Handa H, Ohuchi N, Sasano H (2009) 17Beta-hydroxysteroid dehydrogenase type 12 in human breast carcinoma: a prognostic factor via potential regulation of fatty acid synthesis. Cancer Res 69:1392–1399
Zhou J, Cai ZH, Li L, Gao YF, Hutchinson TH (2010) A proteomics based approach to assessing the toxicity of bisphenol A and diallyl phthalate to the abalone (Haliotis diversicolor supertexta). Chemosphere 79:595–604
Zhou J, Cai ZH (2010) Molecular cloning and characterization of prohormone convertase 1 gene in abalone (Haliotis diversicolor supertexta). Comp Biochem Physiol B 155:331–339
Hartmann S, Steinhart H (1997) Simultaneous determination of anabolic and catabolic steroid hormones in meat by gas chromatography-mass spectrometry. J Chromatogr B 704:105–117
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta] [Delta] CT 319 method. Methods 25:402–408
Kallberg Y, Oppermann U, Jornvall H, Persson B (2002) Short-chain dehydrogenase/reductase (SDR) relationships: a large family with eight clusters common to human, animal, and plant genomes. Protein Sci 11:636–641
Baker ME (2001) Evolution of 17 beta-hydroxysteroid dehydrogeneases and their role in androgen, estrogen and retinoid action. Mol Cell Endocrinol 171:211–215
Breitling R, Krazeisen A, Moller G, Adamski J (2001) 17beta-hydroxysteroid dehydrogenease type 7—an ancient 3-kestosteroid reductase of cholesterogenesis. Mol Cell Endocrinol 171(172):199–204
Lukacik P, Kavanagh KL, Oppermann U (2006) Structure and function of human 17beta-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 248:61–71
Luu-The V, Tremblay P, Labrie F (2006) Characterization of type 12 17β-hydroxysteroid dehydrogenase, an isoform of type 3 17β-hydroxysteroid dehydrogenase responsible for estradiol formation in women. Mol Endocrinol 20:437–443
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 17beta-hydroxysteroid dehydrogenases from the Nile tilapia, Oreochromis niloticus. J Mol Endocrinol 35:103–116
Ni X, Tang XL (2009) The functional characterization of 17beta-hydroxysteroid dehydrogenase 12 in turbot (Scophthalmus maximus) (in Chinese). Prog Physiol Sci 33:173–177
Liu H, Zheng SF, Bellemare V, Pelletier G, Labrie F, Luu-The V (2007) Expression and localization of estrogenic type 12 17β-hydroxysteroid dehydrogenase in the cynomolgus monkey. BMC Biochem 8:2
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
Rantakari P, Lagerbohm H, Kaimainen M, Suomela JP, Strauss L, Sainio K, Pakarinen P, Poutanen M (2010) Hydroxysteroid (17{beta}) dehydrogenase 12 is essential for mouse organogenesis and embryonic survival. Endocrinology 151:1893–1901
Rasheeda MK, Kagawa H, Kirubagaran R, Dutta-Gupta A, Senthilkumaran B (2010) Cloning, expression and enzyme activity analysis of testicular 11beta-hydroxysteroid dehydrogenase during seasonal cycle and after hCG induction in air-breathing catfish Clarias gariepinus. J Steroid Biochem Mol Biol 120:1–10
Acknowledgment
This study was supported by International Cooperative Project of SZISTIC Committee of Shenzhen (ZYA200903260036A), the PhD Start-up Fund of Natural Science Foundation of Guangdong Province, China (10451805702004177), and the Seed Foundation of Graduate School at Shenzhen of Tsinghua University.
Author information
Authors and Affiliations
Corresponding author
Additional information
Jin Zhou and Yun-Feng Gao are contributed equally to this work.
Rights and permissions
About this article
Cite this article
Zhou, J., Gao, YF., Li, L. et al. Identification and functional characterization of a putative 17β-hydroxysteroid dehydrogenase 12 in abalone (Haliotis diversicolor supertexta). Mol Cell Biochem 354, 123–133 (2011). https://doi.org/10.1007/s11010-011-0811-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-011-0811-8