Aromatase is expressed and active in the rainbow trout oocyte during final oocyte maturation

While it is generally well accepted that the ovarian follicular sites of estradiol‐17β (E2) synthesis are restricted to somatic cells, the possible contribution of the germinal compartment has received little or no attention in teleosts. In order to demonstrate the expression of ovarian aromatase in the oocyte, cyp19a1a mRNA was studied in ovarian follicles by in situ hybridization. In addition, the expression of cyp19a1a was studied in both somatic and germinal compartments of the ovarian follicle in rainbow trout (Oncorhynchus mykiss) during final oocyte maturation (i.e., maturational competence acquisition and subsequent meiosis resumption) by real‐time PCR. The enzymatic activity of ovarian aromatase was also studied in both somatic and germinal compartments of the ovarian follicle. Finally, E2 levels were monitored in follicle‐enclosed oocytes throughout the pre‐ovulatory period. We were able to demonstrate a significant ovarian aromatase expression and activity in the late vitellogenic oocyte. Furthermore, a dramatic decrease in aromatase expression and activity occurs in the oocyte during late oogenesis, concomitantly with the trend observed in surrounding follicular layers. We also report an unexpected increase of E2 levels in the oocyte during the pre‐ovulatory period. To our knowledge, these observations are reported for the first time in any teleost species. Together, our data support the hypothesis of the participation of the germinal compartment in follicular estrogen synthesis and a biological role of E2 during oocyte and/or early embryo development. Mol. Reprod. Dev. 78:510–518, 2011. © 2011 Wiley‐Liss, Inc.

[1]  P. Thomas,et al.  Role of G protein-coupled estrogen receptor 1, GPER, in inhibition of oocyte maturation by endogenous estrogens in zebrafish. , 2010, Developmental biology.

[2]  Graham Young,et al.  Oogenesis in teleosts: how eggs are formed. , 2010, General and comparative endocrinology.

[3]  J. Bobe,et al.  Comparative transcriptomic analysis of follicle-enclosed oocyte maturational and developmental competence acquisition in two non-mammalian vertebrates , 2010, BMC Genomics.

[4]  P. Thomas,et al.  Involvement of estradiol-17beta and its membrane receptor, G protein coupled receptor 30 (GPR30) in regulation of oocyte maturation in zebrafish, Danio rario. , 2009, General and comparative endocrinology.

[5]  Paul D. Jones,et al.  Fluorescence in situ hybridization techniques (FISH) to detect changes in CYP19a gene expression of Japanese medaka (Oryzias latipes). , 2008, Toxicology and applied pharmacology.

[6]  Y. Guiguen,et al.  A novel, functional, and highly divergent sex hormone-binding globulin that may participate in the local control of ovarian functions in salmonids. , 2008, Endocrinology.

[7]  P. Thomas,et al.  Estrogen signaling characteristics of Atlantic croaker G protein-coupled receptor 30 (GPR30) and evidence it is involved in maintenance of oocyte meiotic arrest. , 2008, Endocrinology.

[8]  J. Montfort,et al.  Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays , 2006, Reproductive biology and endocrinology : RB&E.

[9]  S. Hammes,et al.  The physiology of the Xenopus laevis ovary. , 2006, Methods in molecular biology.

[10]  B. Jalabert,et al.  Steroidogenesis in rainbow trout (Salmo gairdneri) at various preovulatory stages: changes in plasma hormone levels andin vivo andin vitro responses of the ovary to salmon gonadotropin , 1986, Fish Physiology and Biochemistry.

[11]  N. Montserrat,et al.  Effects of follicle stimulating hormone on estradiol-17 beta production and P-450 aromatase (CYP19) activity and mRNA expression in brown trout vitellogenic ovarian follicles in vitro. , 2004, General and comparative endocrinology.

[12]  I. Helenowski,et al.  Variation in estradiol, estradiol precursors, and estrogen-related products in nipple aspirate fluid from normal premenopausal women. , 2004, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[13]  P. Thomas,et al.  Evidence that 17α,20β,21-trihydroxy-4-pregnen-3-one is a maturation-inducing steroid in spotted seatrout , 1989, Fish Physiology and Biochemistry.

[14]  R. Patiño,et al.  Ovarian follicle growth, maturation, and ovulation in teleost fish , 2004, Fish Physiology and Biochemistry.

[15]  J. Bobe,et al.  Rainbow trout follicular maturational competence acquisition is associated with an increased expression of follicle stimulating hormone receptor and insulin‐like growth factor 2 messenger RNAs , 2003, Molecular reproduction and development.

[16]  M. Kusakabe,et al.  11beta-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. , 2003, Endocrinology.

[17]  S. Hammes,et al.  Xenopus laevis Ovarian CYP17 Is a Highly Potent Enzyme Expressed Exclusively in Oocytes , 2003, The Journal of Biological Chemistry.

[18]  F. Piferrer,et al.  Characterization of aromatase activity in the sea bass: effects of temperature and different catalytic properties of brain and ovarian homogenates and microsomes. , 2002, The Journal of experimental zoology.

[19]  F. Goetz,et al.  Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. , 2002, Endocrinology.

[20]  G. Monod,et al.  Inhibition of ovarian microsomal aromatase and follicular oestradiol secretion by imidazole fungicides in Rainbow trout , 1993 .

[21]  Minoru Tanaka,et al.  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-17 beta in the ovary. , 1992, Journal of molecular endocrinology.

[22]  Y. Nagahama,et al.  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-17 beta in the ovary. , 1992, Journal of molecular endocrinology.

[23]  C. Schreck,et al.  Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation. , 1990, General and comparative endocrinology.

[24]  B. Moav,et al.  Changes in steroid concentrations during sexual ontogenesis in tilapia , 1987 .

[25]  B. Jalabert,et al.  The modulatory effect in vitro of oestradiol-17β, testosterone or cortisol on the output of 17α-hydroxy-20β-dihydroprogesterone by rainbow trout (Salmo gairdneri) ovarian follicles stimulated by the maturational gonadotropin s-GtH , 1984 .

[26]  J. E. Fortune Steroid production by Xenopus ovarian follicles at different developmental stages. , 1983, Developmental biology.

[27]  Y. Nagahama,et al.  Evidence for a decrease in aromatase activity in the ovarian granulosa cells of amago salmon (Oncorhynchus rhodurus) associated with final oocyte maturation. , 1983, Biology of reproduction.

[28]  J. Sumpter,et al.  Hormone changes during ovulation in the rainbow trout (Salmo gairdneri Richardson). , 1983, General and comparative endocrinology.

[29]  R. Gore-Langton,et al.  FSH induction of aromatase in cultured rat granulosa cells measured by a radiometric assay , 1981, Molecular and Cellular Endocrinology.

[30]  O. Sire,et al.  In vitro effect of a fish gonadotropin on aromatase and 17 beta-hydroxysteroid dehydrogenase activities in the ovary of the rainbow trout (Salmo gairdneri Rich.). , 1981, Reproduction, nutrition, developpement.

[31]  B. Jalabert,et al.  [Predominant action of a hydroxylated derivative of progesterone on the in vitro maturation of ovocytes of the rainbow trout (Salmo gairdnerii)]. , 1973, Comptes rendus hebdomadaires des seances de l'Academie des sciences. Serie D: Sciences naturelles.