The Prenatal Development of Bovine Freemartins

Jost, A; Perchellet, Jean‐Pierre; Prépin, J.; Vigier, B.

doi:10.1007/978-3-642-66069-6_36

Cited by 25 publications

(21 citation statements)

References 18 publications

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“…These ovarian changes closely resemble those observed by Jost and his coworkers in freemartins (22)(23)(24)(25), bovine females united in utero to male twins by placental anastomoses, which allows dissemination of testicular AMH in the female circulation (26). In the present study, related changes were observed in ovine fetal ovaries explanted at day 29 however, less conspicuous than in the rat; this could be due to the fact that ovine ovaries were explanted at a much earlier stage of development and differentiate at a much slower pace (27).…”

Section: Discussionsupporting

confidence: 86%

Anti-Müllerian hormone produces endocrine sex reversal of fetal ovaries.

Vigier

Forest

Eychenne

et al. 1989

Proc. Natl. Acad. Sci. U.S.A.

185

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We have previously reported that antiMullerian hormone (AMH), also known as Mfillerianinhibiting substance, the testicular glycoprotein involved in regression of the Mullerian ducts of the mnale fetus, induces the formation of seminiferous cord-like structures in fetal ovaries exposed to it in organ culture. We have now investigated the effect of bovine AMH, purified to homogeneity, on ovarian endocrine differentiation. Ovine fetal ovaries exposed to AMH release testosterone instead of estradiol, an endocrine sex reversal due to suppression of aromatase activity. AMH dramatically decreases the conversion rate of testosterone to estradiol and also decreases total aromatase activity, as measured by the tritiated water technique. AMH acts by decreasing aromatase biosynthesis rather than by blocking enzyme activity, as suggested by the relatively long period of AMH exposure required to produce an effect. In the rabbit fetal ovary, aromatase activity is AMH-responsive during the whole gestational period. The basal steroidogenic activity of rat fetal ovaries is extremely low but can be markedly increased by cAMP. AMH completely blocks the effect of cAMP. Taken together, our results suggest that AMH plays a pivotal role in both morphological and endocrine gonadal sex differentiation. New Zealand rabbits were sacrificed between day 16 and 28 of gestation. Prior to day 20, fetal sex was determined by a sex chromatin test performed on a fragment of the amniotic membrane (12); in older fetuses, sex was easily identified under the dissecting microscope. Wistar rat fetuses were used at 15 days postcoitum; sex was recognized macroscopically. Fetal age was counted from the day of mating, which was considered day 0.Reagents. Bovine AMH was purified by immunochromatography on a monoclonal antibody-conjugated matrix (3) and quantified by radioimmunoassay (13). Other unlabeled reagents were purchased from Sigma; [7-3H]testosterone (24.5 Ci/mmol; 1 Ci = 37 GBq) and [1,3,213-3H] Leshin et al. (14) to a specific activity of 23.2 Ci/mmol.Organ Culture. Fetal gonads were explanted in organ culture (7); they were separated from the mesonephros except in 29-day-old ovine fetal gonads, half of which were cultured together with the mesonephros. No difference was seen between gonads explanted with or without mesonephros, and the results were pooled. Culture medium was CMRL 1066 containing bovine serum albumin at 0.5 mg/ml and, for rat fetal gonads, 0.1 mM 3-isobutyl-1-methylxanthine; 1 mM N6,02'-dibutyryladenosine 3',5'-cyclic monophosphate (Bt2-cAMP) was added to culture medium in some cases. One gonad was placed in control medium, and the other one was placed in medium containing purified bovine AMH (2.25-3 Abbreviations: AMH, anti-Mullerian hormone; Bt2cAMP, N6,02'-dibutyryladenosine 3',5'-cyclic monophosphate. 3684The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

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Section: Discussionsupporting

confidence: 86%

Anti-Müllerian hormone produces endocrine sex reversal of fetal ovaries.

Vigier

Forest

Eychenne

et al. 1989

Proc. Natl. Acad. Sci. U.S.A.

185

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“…Ovarian stunting and loss of germ cells occur early in development, coincident with Millerian regression. Gonadal morphological virilization, characterized by the development of seminiferous tubules containing Sertoli cells capable of AMH production [26] occurs in approximately half of the freemartin gonads, but only during late pregnancy [27]. Altered steroidogenesis, characterized by abnormal testosterone production and loss of estrogen synthesis, has been documented in the fetal freemartin ovary [28] In rats, in vitro studies have shown that the primary biochemical defect elicited by AMH is a repression of aromatase biosynthesis [29,30].…”

Section: Discussionmentioning

confidence: 99%

Ontogeny of Reproductive Abnormalities Induced by Deregulation of Anti-Müllerian Hormone Expression in Transgenic Mice

Lyet

Louis

Forest

et al. 1995

Biology of Reproduction

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Anti-müllerian hormone, normally responsible for the regression of müllerian ducts in male fetuses, induces stunting, germ cell loss, and seminiferous tubule formation in ovaries of bovine freemartin fetuses and of transgenic mice, which express the human anti müllerian hormone gene under the control of the metallothionein promoter. Because the latter have been studied only after birth, we undertook a detailed chronological study of their reproductive organs. Müllerian ducts of transgenic female fetuses regressed at the same time as those of normal or transgenic males. Maximal reduction of germ cell number occurred between 16 days postcoitus and birth, when most transgenic oocytes were still in the leptotene stage of the meiotic prophase, whereas normal oocytes had already reached the pachytene phase. Interference with progression of the meiotic prophase and germ cell loss in the fetal ovary are probably responsible for subsequent ovarian regression and retardation of follicle growth. Seminiferous tubule formation was not detectable prior to birth and occurred only rarely in postnatal ovaries. Aromatase activity of fetal transgenic ovaries was decreased, as well as serum concentration of testosterone in adult transgenic males, suggesting that high levels of anti-müllerian hormone may impair Leydig cell steroidogenesis.

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“…At the time AMH secretion is initiated by the bovine testis of the male twin, germ cells in the prospective ovary of the fetal freemartins no longer multiply. Some of them fail to enter meiosis and none develop beyond the zygotene or, at best, pachytene stage (Jost et al, 1975 ;Prepin et al, 1979).…”

Section: Introductionmentioning

confidence: 99%

“…Fibronectin appeared very early around differentiating seminiferous tubules, and may play a role in the polarization of Sertoli cells (Paranko et al, 1983 . Seminiferous tubules containing immunoreactive AMH (Vigier et al, 1984b) develop only in approximately half the freemartin gonads after 90 days (Jost et al, 1973(Jost et al, , 1975, and their rate of AM H secretion is very low (Vigier et al, 1984b Vigier et al, 1987).…”

Section: Introductionmentioning

confidence: 99%

Anti-Müllerian hormone and freemartinism : inhibition of germ cell development and induction of seminiferous cord-like structures in rat fetal ovaries exposed in vitro to purified bovine AMH

Vigier¹,

Watrin²,

Magre³

et al. 1988

Reprod. Nutr. Dévelop.

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Summary. In 13 and 14-day old fetal rat ovaries maintained 3 to 10 days in organ culture, purified bovine anti-Mullerian hormone (AMH) (1.5 to 3 pg/ml) induced a characteristic freemartin effect. Gonadal volume and germ cell number were significantly reduced, compared to control ovaries cultured in anhormonal medium, and epithelial cells with large clear cytoplasm linked by interdigitations differentiated in the gonadal blastema. These cells resembling rat fetal Sertoli cells became polarized and formed seminiferous cord-like structures delineated by a basal membrane containing laminin and fibronectin as is the case of testicular seminiferous cords at the first step of their differentiation. These data indicate that AMH is probably the testicular factor responsible for the morphological modifications of bovine freemartin gonads and suggest that this hormone could also be involved in normal morphological differentiation of the testis. In contrast, in fetal rat ovaries, AMH did not trigger the testosterone production which occurs in freemartin gonads at an early stage of the gestation.Introduction.

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The Prenatal Development of Bovine Freemartins

Cited by 25 publications

References 18 publications

Anti-Müllerian hormone produces endocrine sex reversal of fetal ovaries.

Anti-Müllerian hormone produces endocrine sex reversal of fetal ovaries.

Ontogeny of Reproductive Abnormalities Induced by Deregulation of Anti-Müllerian Hormone Expression in Transgenic Mice

Anti-Müllerian hormone and freemartinism : inhibition of germ cell development and induction of seminiferous cord-like structures in rat fetal ovaries exposed in vitro to purified bovine AMH

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