Department of Biology, Johns Hopkins University, Baltimore, MD 21218, USA.
Department of Genetics, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran; Univ. Grenoble Alpes, INSERM U1209, CNRS UMR 5309, Institute for Advanced Biosciences, Team Genetics Epigenetics and Therapies of Infertility, 38000 Grenoble, France.
Am J Hum Genet. 2018 Apr 5;102(4):636-648. doi: 10.1016/j.ajhg.2018.03.007.
The multiple morphological abnormalities of the flagella (MMAF) phenotype is among the most severe forms of sperm defects responsible for male infertility. The phenotype is characterized by the presence in the ejaculate of immotile spermatozoa with severe flagellar abnormalities including flagella being short, coiled, absent, and of irregular caliber. Recent studies have demonstrated that MMAF is genetically heterogeneous, and genes thus far associated with MMAF account for only one-third of cases. Here we report the identification of homozygous truncating mutations (one stop-gain and one splicing variant) in CFAP69 of two unrelated individuals by whole-exome sequencing of a cohort of 78 infertile men with MMAF. CFAP69 encodes an evolutionarily conserved protein found at high levels in the testis. Immunostaining experiments in sperm from fertile control individuals showed that CFAP69 localized to the midpiece of the flagellum, and the absence of CFAP69 was confirmed in both individuals carrying CFPA69 mutations. Additionally, we found that sperm from a Cfap69 knockout mouse model recapitulated the MMAF phenotype. Ultrastructural analysis of testicular sperm from the knockout mice showed severe disruption of flagellum structure, but histological analysis of testes from these mice revealed the presence of all stages of the seminiferous epithelium, indicating that the overall progression of spermatogenesis is preserved and that the sperm defects likely arise during spermiogenesis. Together, our data indicate that CFAP69 is necessary for flagellum assembly/stability and that in both humans and mice, biallelic truncating mutations in CFAP69 cause autosomal-recessive MMAF and primary male infertility.
多鞭毛形态异常(MMAF)表型是导致男性不育的最严重的精子缺陷之一。该表型的特征是精液中存在不动精子,其鞭毛严重异常,包括鞭毛短、卷曲、缺失和不规则口径。最近的研究表明,MMAF 是遗传异质性的,迄今为止与 MMAF 相关的基因仅占病例的三分之一。在这里,我们通过对 78 名患有 MMAF 的不育男性进行外显子组测序,发现了两名无关个体的 CFAP69 基因纯合截断突变(一个移码突变和一个剪接变异)。CFAP69 编码一种进化上保守的蛋白质,在睾丸中高水平表达。在正常生育控制个体的精子免疫染色实验中,CFAP69 定位于鞭毛的中段,在携带 CFPA69 突变的两个人中均证实 CFAP69 缺失。此外,我们发现 Cfap69 敲除小鼠模型的精子再现了 MMAF 表型。对敲除小鼠睾丸精子的超微结构分析显示鞭毛结构严重破坏,但这些小鼠睾丸的组织学分析显示存在生精上皮的所有阶段,表明精子发生的整体进展得到保留,并且精子缺陷可能发生在精子发生过程中。总之,我们的数据表明 CFAP69 对于鞭毛组装/稳定性是必要的,并且在人类和小鼠中,CFAP69 的双等位基因截断突变导致常染色体隐性 MMAF 和原发性男性不育。