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RESEARCH ARTICLE

Molecular cloning, expression analysis and developmental changes in ovarian follicles of goose 3β-hydroxysteroid dehydrogenase 1

Yingying Zhang A , Hehe Liu A , Mingjun Yang A , Shengqiang Hu A , Liang Li A and Jiwen Wang A B
+ Author Affiliations
- Author Affiliations

A Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Ya’an 625014, Sichuan, People’s Republic of China.

B Corresponding author. Email: wjw2886166@163.com

Animal Production Science 54(8) 992-998 https://doi.org/10.1071/AN13315
Submitted: 21 March 2013  Accepted: 10 September 2013   Published: 26 November 2013

Abstract

The enzyme 3β-hydroxysteroid dehydrogenase/isomerase1 (3βHSD1) can catalyse the conversion of pregnenolone to progesterone in the 4-3-ketosteroid metabolic pathway. The aim of the present study was to clone 3βHSD1 and to determine whether this enzyme in the follicular wall has an effect on yolk progesterone in geese (Anser cygnoides). A putative coding sequence of 3βHSD1, which was 1134 nucleotides in length, was successfully obtained by using reverse transcription polymerase chain reaction (RT–PCR). A comparison of the deduced amino acid sequence with chicken, quail, zebra finch, cattle, horse, pig, human and mouse 3βHSD1 showed 89.7%, 88.4%, 87.3%, 55.6%, 54.0%, 53.5%, 55.3% and 52.9% similarity, respectively. The detection of 3βHSD1 mRNA levels in several tissues by quantitative real-time PCR showed that the highest level of 3βHSD1 was in the adrenal gland, followed by the ovary, which indicated that the gene we obtained was the adrenal gland/gonad-specific one. We measured the level of 3βHSD1 mRNA in the follicular wall and determined the concentration of progesterone in the yolk of these ovarian follicles; the concentration of progesterone in the yolk had a pattern of expression similar to that of 3βHSD1 in the follicular wall during follicular development. This result suggests that the expression of 3βHSD1 in the follicular wall may be a main factor that contributes to the accumulation of yolk progesterone.


References

Armstrong DG, Davidson MF, Gilbert AB, Wells JW (1977) Activity of 3beta-hydroxyteroiddehydrogenase in the postovulatory follicle of the domestic fowl (Gallus domesticus). Journal of Reproduction and Fertility 49, 253–259.
Activity of 3beta-hydroxyteroiddehydrogenase in the postovulatory follicle of the domestic fowl (Gallus domesticus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhvVKht74%3D&md5=12d73556f5a995ab4da0e71b58f36242CAS | 850216PubMed |

Bahr JM, Wang SC, Huang MY, Calvo FO (1983) Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biology of Reproduction 29, 326–334.
Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltlOjt7g%3D&md5=3d20a7f8b4c2740ba779a1ebc91bb6efCAS | 6640023PubMed |

Bain PA, Yoo M, Clarke T, Hammond SH, Payne AH (1991) Multiple forms of mouse 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4 isomerase and differential expression in gonads, adrenal glands, liver, and kidneys of both sexes. Proceedings of the National Academy, USA 88, 8870–8874.
Multiple forms of mouse 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4 isomerase and differential expression in gonads, adrenal glands, liver, and kidneys of both sexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVKgsg%3D%3D&md5=192d93036a9b08b4720282c5b5981db6CAS |

Gómez Y, Velazquez PN, Juarez-Oropeza MA, Pedernera E (1998) Steroid metabolism in granulosa and theca interna cells from preovulatory follicles of domestic hen (Gallus domesticus). Animal Reproduction Science 52, 81–91.
Steroid metabolism in granulosa and theca interna cells from preovulatory follicles of domestic hen (Gallus domesticus).Crossref | GoogleScholarGoogle Scholar | 9728817PubMed |

Groothuis TG, Muller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews 29, 329–352.
Maternal hormones as a tool to adjust offspring phenotype in avian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtlSqtLs%3D&md5=f47eedfbef728bc9a0a881f0f8c42aedCAS | 15811503PubMed |

Hackl R, Bromundt V, Daisley J, Kotrschal K, Mostl E (2003) Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 173, 327–331.
Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1OrsL4%3D&md5=0b4f66e0005868730d7becbef3dde354CAS | 12677460PubMed |

Hammond RW, Koelkebeck KW, Scanes CG, Biellier HV, Hertelendy F (1981) Plasma prostaglandin, LH, and progesterone level during the ovulation cycle of the turkey (Meleagris gallopauvo). General and Comparative Endocrinology 44, 400–403.
Plasma prostaglandin, LH, and progesterone level during the ovulation cycle of the turkey (Meleagris gallopauvo).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkt1WltL8%3D&md5=c7183b94ac08ece437be49a3c4fc7f61CAS | 7286623PubMed |

Hein J (1990) Unified approach to alignment and phylogenies. Methods in Enzymology 183, 626–645.
Unified approach to alignment and phylogenies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVOrs7Y%3D&md5=2a2462da5dadc2ef83a4ffe946dfd243CAS | 2314296PubMed |

Huang ES, Nalbandov AV (1979) Steroidogenesis of chicken granulosa and theca cells: in vitro incubation system. Biology of Reproduction 20, 442–453.
Steroidogenesis of chicken granulosa and theca cells: in vitro incubation system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktVarsr4%3D&md5=0869f53a6bb2ba3b5923c9b8fa0c2a6dCAS | 454747PubMed |

Johnson AL, Solovieva EV, Bridgham JT (2002) Relationship between steroidogenic acute regulatory protein expression and progesterone production in hen granulosa cells during follicle development. Biology of Reproduction 67, 1313–1320.
Relationship between steroidogenic acute regulatory protein expression and progesterone production in hen granulosa cells during follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2rtLg%3D&md5=f72ebd96d9444eecd8870a8d51051356CAS | 12297550PubMed |

Kowalski KI, Tilly JL, Johnson AL (1991) Cytochrome P450 side-chain cleavage (P450scc) in the hen ovary. I. Regulation of P450scc messenger RNA levels and steroidogenesis in theca cells of developing follicles. Biology of Reproduction 45, 955–966.
Cytochrome P450 side-chain cleavage (P450scc) in the hen ovary. I. Regulation of P450scc messenger RNA levels and steroidogenesis in theca cells of developing follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVCqsb0%3D&md5=57dd42547bc21dd2526ddd4f976175c6CAS | 1666852PubMed |

Lee KA, Volentine KK, Bahr JM (1998) Two steroidogenic pathways present in the chicken ovary: theca layer prefers delta 5 pathway and granulosa layer prefers delta 4 pathway. Domestic Animal Endocrinology 15, 1–8.
Two steroidogenic pathways present in the chicken ovary: theca layer prefers delta 5 pathway and granulosa layer prefers delta 4 pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktlSrsg%3D%3D&md5=9af7d464186f48858e1cf356b105987bCAS | 9437580PubMed |

Lipar JL, Ketterson ED, Nolan V, Casto JM (1999) Egg yolk layers vary in the concentration of steroid hormones in two avian species. General and Comparative Endocrinology 115, 220–227.
Egg yolk layers vary in the concentration of steroid hormones in two avian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksFChs7g%3D&md5=51a4092a5dc4ff0baedb683f7fecd35cCAS | 10417235PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=e7ddb0df18f96a9072b5ab8d1f12c74cCAS | 11846609PubMed |

Lorence MC, Corbin CJ, Kamimura N, Mahendroo MS, Mason JI (1990) Structural analysis of the gene encoding human 3 beta-hydroxysteroid dehydrogenase/delta 5-4-isomerase. Molecular Endocrinology 4, 1850–1855.
Structural analysis of the gene encoding human 3 beta-hydroxysteroid dehydrogenase/delta 5-4-isomerase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlslKhurw%3D&md5=a035bcf0bf9d74d21eaef4c181556a05CAS | 2082186PubMed |

Marrone BL, Sebring RJ (1989) Quantitative cytochemistry of 3 beta-hydroxysteroid dehydrogenase activity in avian granulosa cells during follicular maturation. Biology of Reproduction 40, 1007–1011.
Quantitative cytochemistry of 3 beta-hydroxysteroid dehydrogenase activity in avian granulosa cells during follicular maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltFamsL8%3D&md5=3fc1a30b3ad19cf57312c1a4a9333db9CAS | 2765605PubMed |

Mason JI, Howe BE, Howie AF, Morley SD, Nicol MR, Payne AH (2004) Promiscuous 3beta-hydroxysteroid dehydrogenases: testosterone 17beta-hydroxysteroid dehydrogenase activities of mouse type I and VI 3 beta-hydroxysteroid dehydrogenases. Endocrine Research 30, 709–714.
Promiscuous 3beta-hydroxysteroid dehydrogenases: testosterone 17beta-hydroxysteroid dehydrogenase activities of mouse type I and VI 3 beta-hydroxysteroid dehydrogenases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVGrsQ%3D%3D&md5=093fd9002d026ef12c290fc8964d222eCAS | 15666815PubMed |

Molho-Pessach V, Rios JJ, Xing C, Setchell KD, Cohen JC, Hobbs HH (2012) Homozygosity mapping identifies a bile acid biosynthetic defect in an adult with cirrhosis of unknown etiology. Hepatology 55, 1139–1145.
Homozygosity mapping identifies a bile acid biosynthetic defect in an adult with cirrhosis of unknown etiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xks1yjsLc%3D&md5=837df33936225798d5b23810028f3fbcCAS | 22095780PubMed |

Nakabayashi O, Nomura O, Nishimori K, Mizuno S (1995) The cDNA cloning and transient expression of a chicken gene encoding a 3 beta-hydroxysteroid dehydrogenase/delta 5→4 isomerase unique to major steroidogenic tissues. Gene 162, 261–265.
The cDNA cloning and transient expression of a chicken gene encoding a 3 beta-hydroxysteroid dehydrogenase/delta 5→4 isomerase unique to major steroidogenic tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnslyhurk%3D&md5=0bb7e95951f32af4f2ee9e60019de99fCAS | 7557440PubMed |

Nitta H, Osawa Y, Bahr JM (1991) Immunolocalization of steroidogenic cells in small follicles of the chicken ovary: anatomical arrangement and location of steroidogenic cells change during follicular development. Domestic Animal Endocrinology 8, 587–594.
Immunolocalization of steroidogenic cells in small follicles of the chicken ovary: anatomical arrangement and location of steroidogenic cells change during follicular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhtVejsbs%3D&md5=ae5164905dfd3b6f4bfeba68481bf104CAS | 1786705PubMed |

Nitta H, Mason JI, Bahr JM (1993) Localization of 3 beta-hydroxysteroid dehydrogenase in the chicken ovarian follicle shifts from the theca layer to granulosa layer with follicular maturation. Biology of Reproduction 48, 110–116.
Localization of 3 beta-hydroxysteroid dehydrogenase in the chicken ovarian follicle shifts from the theca layer to granulosa layer with follicular maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnslGjtg%3D%3D&md5=f724205cd05b6f3af1a255427bd11e72CAS | 8418898PubMed |

Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrine Reviews 25, 947–970.
Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslWntg%3D%3D&md5=c21396f6c19e37128b22314f487842ecCAS | 15583024PubMed |

Porter TE, Hargis BM, Silsby JL, el Halawani ME (1989) Differential steroid production between theca interna and theca externa cells: a three-cell model for follicular steroidogenesis in avian species. Endocrinology 125, 109–116.
Differential steroid production between theca interna and theca externa cells: a three-cell model for follicular steroidogenesis in avian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkslGjtL0%3D&md5=28f49f5b001028883a8dd9d39c27759dCAS | 2737138PubMed |

Rheaume E, Lachance Y, Zhao HF, Breton N, Dumont M, de Launoit Y, Trudel C, Luu-The V, Simard J, Labrie F (1991) Structure and expression of a new complementary DNA encoding the almost exclusive 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4-isomerase in human adrenals and gonads. Molecular Endocrinology 5, 1147–1157.
Structure and expression of a new complementary DNA encoding the almost exclusive 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4-isomerase in human adrenals and gonads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1GlsLY%3D&md5=ad06747b14031fad218857039454378aCAS | 1944309PubMed |

Rogerson FM, LeHoux JG, Mason JI (1995) Expression and characterization of isoforms of 3 beta-hydroxysteroid dehydrogenase/delta 5→4-isomerase in the hamster. The Journal of Steroid Biochemistry and Molecular Biology 55, 481–487.
Expression and characterization of isoforms of 3 beta-hydroxysteroid dehydrogenase/delta 5→4-isomerase in the hamster.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xkt1Sjsw%3D%3D&md5=1f38941829fb15a868e887a358349090CAS | 8547173PubMed |

Sechman A, Lakota P, Wojtysiak D, Hrabia A, Mika M, Lisowski M, Czekalski P, Rzasa J, Kapkowska E, Bednarczyk M (2006) Sex steroids level in blood plasma and ovarian follicles of the chimeric chicken. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 53, 501–508.
Sex steroids level in blood plasma and ovarian follicles of the chimeric chicken.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFCmsw%3D%3D&md5=ebbaa7dcccbe6ba7f2ab4b88dbb5f6faCAS | 17105570PubMed |

Sechman A, Pawlowska K, Hrabia A (2011) Effect of 3,3′,5-triiodothyronine and 3,5-diiodothyronine on progesterone production, cAMP synthesis, and mRNA expression of STAR, CYP11A1, and HSD3B genes in granulosa layer of chicken preovulatory follicles. Domestic Animal Endocrinology 41, 137–149.
Effect of 3,3′,5-triiodothyronine and 3,5-diiodothyronine on progesterone production, cAMP synthesis, and mRNA expression of STAR, CYP11A1, and HSD3B genes in granulosa layer of chicken preovulatory follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFaitL%2FO&md5=1ba03ec48454506d0aa0f3d510e326c9CAS | 21798688PubMed |

Simard J, Melner MH, Breton N, Low KG, Zhao HF, Periman LM, Labrie F (1991) Characterization of macaque 3 beta-hydroxy-5-ene steroid dehydrogenase/delta 5-delta 4 isomerase: structure and expression in steroidogenic and peripheral tissues in primate. Molecular and Cellular Endocrinology 75, 101–110.
Characterization of macaque 3 beta-hydroxy-5-ene steroid dehydrogenase/delta 5-delta 4 isomerase: structure and expression in steroidogenic and peripheral tissues in primate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltV2hur8%3D&md5=24df424f7515a56dc91d590a6520d752CAS | 2050270PubMed |

Simard J, Ricketts ML, Gingras S, Soucy P, Feltus FA, Melner MH (2005) Molecular biology of the 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene family. Endocrine Reviews 26, 525–582.
Molecular biology of the 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFejt7c%3D&md5=bb8678def9a907f6687b873c86bfce3dCAS | 15632317PubMed |

Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=390824119290d6292fa8e01ea5c11a32CAS | 17488738PubMed |