Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles
Ovarian growth (vitellogenesis) in most lower vertebrates is mediated by estradiol-17beta (E2) secreted by the follicles in response to follicle-stimulating hormone (Fsh), whereas oocyte maturation and ovulation are mediated by progestins, such 17alpha,20beta-dihydroxypregn-4-en-3-one (17,20beta-P), produced in response to luteinizing hormone (Lh). In teleosts, follicular synthesis of 17,20beta-P at the time of maturation is due primarily to up-regulation of the enzymes P450c17-II (Cyp17a2) and 20beta-hydroxysteroid dehydrogenase (Cbr1). Here, we show that follicular cells associated with primary growth (previtellogenic) oocytes of the gilthead seabream also express cyp17a2 and cbr1, in addition to P450c17-I (cyp17a1) and aromatase (cyp19a1), enzymes required for E2 synthesis. Ovaries containing only oogonia and early primary ovarian follicles had a 60-fold higher concentration of 17,20beta-P than ovaries in the succeeding stages and had a higher expression of cbr1 and Fsh receptor (fshra). Stimulation of explants of primary follicles in vitro with recombinant piscine Fsh (rFsh), which specifically activates the seabream Fshra, promoted a rapid accumulation of 17,20beta-P, and synthesis was sustained by an external supply of 17alpha-hydroxyprogesterone. In the presence of Cbr1 inhibitors, rFsh-mediated 17,20beta-P production was reduced, with a concomitant increase in testosterone and E2 synthesis. In primary explants, rFsh up-regulated cyp17a2 and cbr1 transcription and simultaneously down-regulated cyp17a1 and cyp19a1 steady-state mRNA levels within 24 h. In contrast, in explants containing vitellogenic follicles, rFsh had no effect on cyp17a2 and cbr1 expression, but increased that of cyp17a1 and cyp19a1. These data suggest a functional Fshra-activated Cyp17a2/ Cbr1 steroidogenic pathway in gilthead seabream primary ovarian follicles triggering th production of 17,20beta-P. © 2012 by the Society for the Study of Reproduction, Inc.
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dig-icm-es-10261-648152021-10-22T11:54:06Z Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles Zapater, Cinta Chauvigné, François Scott, Alexander P. Gómez, Ana Katsiadaki, Ioanna Cerdà, Joan Ovarian growth (vitellogenesis) in most lower vertebrates is mediated by estradiol-17beta (E2) secreted by the follicles in response to follicle-stimulating hormone (Fsh), whereas oocyte maturation and ovulation are mediated by progestins, such 17alpha,20beta-dihydroxypregn-4-en-3-one (17,20beta-P), produced in response to luteinizing hormone (Lh). In teleosts, follicular synthesis of 17,20beta-P at the time of maturation is due primarily to up-regulation of the enzymes P450c17-II (Cyp17a2) and 20beta-hydroxysteroid dehydrogenase (Cbr1). Here, we show that follicular cells associated with primary growth (previtellogenic) oocytes of the gilthead seabream also express cyp17a2 and cbr1, in addition to P450c17-I (cyp17a1) and aromatase (cyp19a1), enzymes required for E2 synthesis. Ovaries containing only oogonia and early primary ovarian follicles had a 60-fold higher concentration of 17,20beta-P than ovaries in the succeeding stages and had a higher expression of cbr1 and Fsh receptor (fshra). Stimulation of explants of primary follicles in vitro with recombinant piscine Fsh (rFsh), which specifically activates the seabream Fshra, promoted a rapid accumulation of 17,20beta-P, and synthesis was sustained by an external supply of 17alpha-hydroxyprogesterone. In the presence of Cbr1 inhibitors, rFsh-mediated 17,20beta-P production was reduced, with a concomitant increase in testosterone and E2 synthesis. In primary explants, rFsh up-regulated cyp17a2 and cbr1 transcription and simultaneously down-regulated cyp17a1 and cyp19a1 steady-state mRNA levels within 24 h. In contrast, in explants containing vitellogenic follicles, rFsh had no effect on cyp17a2 and cbr1 expression, but increased that of cyp17a1 and cyp19a1. These data suggest a functional Fshra-activated Cyp17a2/ Cbr1 steroidogenic pathway in gilthead seabream primary ovarian follicles triggering th production of 17,20beta-P. © 2012 by the Society for the Study of Reproduction, Inc. Supported by the Spanish Ministry of Science and Innovation (MICINN; grant AGL2007-60261/ACU to J.C.), with additional financial support from the CEFAS Seedcorn fund. C.Z. and F.C. were supported by predoctoral (FPI) and postdoctoral (Juan de la Cierva Programme) fellowships, respectively, from MICINN. Peer Reviewed 2013-01-23T11:10:12Z 2013-01-23T11:10:12Z 2012 2013-01-23T11:10:12Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1095/biolreprod.112.102533 issn: 0006-3363 e-issn: 1529-7268 Biology of Reproduction 87(5): article 111 (2012) http://hdl.handle.net/10261/64815 10.1095/biolreprod.112.102533 en none Society for the Study of Reproduction |
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Ovarian growth (vitellogenesis) in most lower vertebrates is mediated by estradiol-17beta (E2) secreted by the follicles in response to follicle-stimulating hormone (Fsh), whereas oocyte maturation and ovulation are mediated by progestins, such 17alpha,20beta-dihydroxypregn-4-en-3-one (17,20beta-P), produced in response to luteinizing hormone (Lh). In teleosts, follicular synthesis of 17,20beta-P at the time of maturation is due primarily to up-regulation of the enzymes P450c17-II (Cyp17a2) and 20beta-hydroxysteroid dehydrogenase (Cbr1). Here, we show that follicular cells associated with primary growth (previtellogenic) oocytes of the gilthead seabream also express cyp17a2 and cbr1, in addition to P450c17-I (cyp17a1) and aromatase (cyp19a1), enzymes required for E2 synthesis. Ovaries containing only oogonia and early primary ovarian follicles had a 60-fold higher concentration of 17,20beta-P than ovaries in the succeeding stages and had a higher expression of cbr1 and Fsh receptor (fshra). Stimulation of explants of primary follicles in vitro with recombinant piscine Fsh (rFsh), which specifically activates the seabream Fshra, promoted a rapid accumulation of 17,20beta-P, and synthesis was sustained by an external supply of 17alpha-hydroxyprogesterone. In the presence of Cbr1 inhibitors, rFsh-mediated 17,20beta-P production was reduced, with a concomitant increase in testosterone and E2 synthesis. In primary explants, rFsh up-regulated cyp17a2 and cbr1 transcription and simultaneously down-regulated cyp17a1 and cyp19a1 steady-state mRNA levels within 24 h. In contrast, in explants containing vitellogenic follicles, rFsh had no effect on cyp17a2 and cbr1 expression, but increased that of cyp17a1 and cyp19a1. These data suggest a functional Fshra-activated Cyp17a2/ Cbr1 steroidogenic pathway in gilthead seabream primary ovarian follicles triggering th production of 17,20beta-P. © 2012 by the Society for the Study of Reproduction, Inc. |
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Zapater, Cinta Chauvigné, François Scott, Alexander P. Gómez, Ana Katsiadaki, Ioanna Cerdà, Joan |
spellingShingle |
Zapater, Cinta Chauvigné, François Scott, Alexander P. Gómez, Ana Katsiadaki, Ioanna Cerdà, Joan Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
author_facet |
Zapater, Cinta Chauvigné, François Scott, Alexander P. Gómez, Ana Katsiadaki, Ioanna Cerdà, Joan |
author_sort |
Zapater, Cinta |
title |
Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
title_short |
Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
title_full |
Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
title_fullStr |
Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
title_full_unstemmed |
Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
title_sort |
piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles |
publisher |
Society for the Study of Reproduction |
publishDate |
2012 |
url |
http://hdl.handle.net/10261/64815 |
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