Young Julia C, Whiley Penny A F, Sutherland Jessie M, Luu Michael, Garama Daniel J, Baker Mark A, Hogarth Cathryn A, Richards Elizabeth A, Jans David A, McLaughlin Eileen A, Loveland Kate L
Centre for Reproductive Health, Hudson Institute for Medical Research, Clayton, VIC, Australia.
Department of Anatomy and Developmental Biology, Monash University, Clayton, VIC, Australia.
Biol Reprod. 2025 Oct 14;113(4):917-933. doi: 10.1093/biolre/ioaf134.
The highly conserved nuclear transport protein importin 5 (IPO5) binds cargo implicated in fundamental processes including virus and chromatin assembly, germline development, and cell signaling. It also anchors cell-specific cargo for functional outcomes in development and immune responses. IPO5 displays both spatial and temporal regulation in the male germline, from fetal through to adult ages. Because it transports key early developmental/reproductive factors, including Stella and the BMP signaling SMADs 1/5/9, we hypothesized that targeted IPO5 deletion would impair germline development and viability at specific stages. Here, we demonstrate in vivo functional importance of IPO5 by generating global and conditional IPO5 knockout mice using an Ipo5FL/FL allele flanking exons 9 and 10. Global deletion using CMVCre produced no null embryos at embryonic day (E)12.5, while heterozygous embryo numbers were reduced to 50%, demonstrating it is essential for early embryogenesis. A sex-specific germline requirement for IPO5 was demonstrated following deletion using VasaCre (active from E15.5); adult testes lacked germ cells, while oocytes developed and female fertility was unaffected. Stra8Cre-directed IPO5 deletion (active from postnatal day (PND) 3) caused meiotic failure evident at PND 14; no IPO5-deficient germ cells were present in adults, although niche integrity and function supported emergence of rare IPO5-positive spermatozoa. Novel IPO5 binding proteins identified by immunoprecipitation and mass-spectrometry included SFPQ in fetal testes and XPO2 (exportin 2) in both isolated spermatocytes and spermatids. Remarkably, most IPO5 potential binding proteins are essential for male fertility. These results define IPO5 as crucial for in vivo embryonic development and male fertility.
高度保守的核转运蛋白输入蛋白5(IPO5)可结合参与病毒和染色质组装、生殖系发育及细胞信号传导等基本过程的货物分子。它还能锚定细胞特异性货物分子,以实现发育和免疫反应中的功能结果。从胎儿期到成年期,IPO5在雄性生殖系中呈现出空间和时间上的调控。由于它运输关键的早期发育/生殖因子,包括Stella和骨形态发生蛋白(BMP)信号传导的SMAD 1/5/9,我们推测靶向删除IPO5会在特定阶段损害生殖系发育和生存能力。在此,我们通过使用位于外显子9和10两侧的Ipo5FL/FL等位基因生成全局和条件性IPO5基因敲除小鼠,证明了IPO5在体内的功能重要性。使用CMVCre进行全局删除时,在胚胎第12.5天(E12.5)未产生无效胚胎,而异合子胚胎数量减少至50%,表明它对早期胚胎发育至关重要。使用VasaCre(从E15.5开始激活)删除后,证明了IPO5对生殖系存在性别特异性需求;成年睾丸缺乏生殖细胞,而卵母细胞发育正常且雌性生育能力未受影响。由Stra8Cre指导的IPO5删除(从出生后第3天(PND 3)开始激活)导致在PND 14时出现明显的减数分裂失败;尽管微环境的完整性和功能支持罕见的IPO5阳性精子出现,但成年动物中不存在IPO5缺陷的生殖细胞。通过免疫沉淀和质谱鉴定的新型IPO5结合蛋白包括胎儿睾丸中的SFPQ以及分离的精母细胞和精子细胞中的XPO2(输出蛋白2)。值得注意的是,大多数IPO5潜在结合蛋白对雄性生育能力至关重要。这些结果表明IPO5对体内胚胎发育和雄性生育能力至关重要。