Bashamboo Anu, Donohoue Patricia A, Vilain Eric, Rojo Sandra, Calvel Pierre, Seneviratne Sumudu N, Buonocore Federica, Barseghyan Hayk, Bingham Nathan, Rosenfeld Jill A, Mulukutla Surya Narayan, Jain Mahim, Burrage Lindsay, Dhar Shweta, Balasubramanyam Ashok, Lee Brendan, Dumargne Marie-Charlotte, Eozenou Caroline, Suntharalingham Jenifer P, de Silva Ksh, Lin Lin, Bignon-Topalovic Joelle, Poulat Francis, Lagos Carlos F, McElreavey Ken, Achermann John C
Human Developmental Genetics, Institut Pasteur, Paris, 75724 France.
Department of Pediatrics, Endocrinology & Diabetes, Medical college of Wisconsin, Milwaukee, WI, USA.
Hum Mol Genet. 2016 Aug 15;25(16):3446-3453. doi: 10.1093/hmg/ddw186. Epub 2016 Jul 4.
Cell lineages of the early human gonad commit to one of the two mutually antagonistic organogenetic fates, the testis or the ovary. Some individuals with a 46,XX karyotype develop testes or ovotestes (testicular or ovotesticular disorder of sex development; TDSD/OTDSD), due to the presence of the testis-determining gene, SRY Other rare complex syndromic forms of TDSD/OTDSD are associated with mutations in pro-ovarian genes that repress testis development (e.g. WNT4); however, the genetic cause of the more common non-syndromic forms is unknown. Steroidogenic factor-1 (known as NR5A1) is a key regulator of reproductive development and function. Loss-of-function changes in NR5A1 in 46,XY individuals are associated with a spectrum of phenotypes in humans ranging from a lack of testis formation to male infertility. Mutations in NR5A1 in 46,XX women are associated with primary ovarian insufficiency, which includes a lack of ovary formation, primary and secondary amenorrhoea as well as early menopause. Here, we show that a specific recurrent heterozygous missense mutation (p.Arg92Trp) in the accessory DNA-binding region of NR5A1 is associated with variable degree of testis development in 46,XX children and adults from four unrelated families. Remarkably, in one family a sibling raised as a girl and carrying this NR5A1 mutation was found to have a 46,XY karyotype with partial testicular dysgenesis. These unique findings highlight how a specific variant in a developmental transcription factor can switch organ fate from the ovary to testis in mammals and represents the first missense mutation causing isolated, non-syndromic 46,XX testicular/ovotesticular DSD in humans.
人类早期性腺的细胞谱系会走向两种相互拮抗的器官发生命运之一,即睾丸或卵巢。一些核型为46,XX的个体由于存在睾丸决定基因SRY,会发育出睾丸或卵睾(性发育的睾丸或卵睾障碍;TDSD/OTDSD)。其他罕见的复杂综合征形式的TDSD/OTDSD与抑制睾丸发育的促卵巢基因(如WNT4)突变有关;然而,更常见的非综合征形式的遗传原因尚不清楚。类固醇生成因子-1(又称NR5A1)是生殖发育和功能的关键调节因子。46,XY个体中NR5A1的功能丧失性变化与人类一系列表型相关,从睾丸形成缺失到男性不育。46,XX女性中NR5A1的突变与原发性卵巢功能不全有关,包括卵巢形成缺失、原发性和继发性闭经以及早绝经。在此,我们表明,NR5A1辅助DNA结合区域的一种特定复发性杂合错义突变(p.Arg92Trp)与来自四个无关家族的46,XX儿童和成人不同程度的睾丸发育有关。值得注意的是,在一个家族中,一名被当作女孩抚养且携带这种NR5A1突变的兄弟姐妹被发现核型为46,XY,伴有部分睾丸发育不全。这些独特的发现凸显了发育转录因子中的特定变异如何在哺乳动物中使器官命运从卵巢转变为睾丸,并且代表了人类中首个导致孤立的、非综合征性46,XX睾丸/卵睾性发育障碍的错义突变。