Spermiogenesis is a highly orchestrated developmental process during which chromatin condensation decouples transcription from translation. Spermiogenic mRNAs are transcribed earlier and stored in a translationally inert state until needed for translation; however, it remains largely unclear how such repressed mRNAs become activated during spermiogenesis. We previously reported that the MIWI/piRNA machinery is responsible for mRNA elimination during late spermiogenesis in preparation for spermatozoa production. Here we unexpectedly discover that the same machinery is also responsible for activating translation of a subset of spermiogenic mRNAs to coordinate with morphological transformation into spermatozoa. Such action requires specific base-pairing interactions of piRNAs with target mRNAs in their 3' UTRs, which activates translation through coupling with cis-acting AU-rich elements to nucleate the formation of a MIWI/piRNA/eIF3f/HuR super-complex in a developmental stage-specific manner. These findings reveal a critical role of the piRNA system in translation activation, which we show is functionally required for spermatid development.

中文翻译：

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小鼠精子发生过程中 MIWI/piRNA 的翻译激活功能。

精子发生是一个高度协调的发育过程，在此过程中染色质浓缩使转录与翻译脱钩。生精子 mRNA 较早转录并以翻译惰性状态储存，直到需要翻译；然而，目前还不清楚这种被抑制的 mRNAs 在精子发生过程中是如何被激活的。我们之前曾报道过，MIWI/piRNA 机制负责精子发生晚期 mRNA 的消除，为精子的产生做准备。在这里，我们出乎意料地发现，同样的机制也负责激活精子生成 mRNA 子集的翻译，以协调精子的形态转化。这种作用需要 piRNA 与目标 mRNA 在其 3' UTR 中的特定碱基配对相互作用，它通过与顺式作用的富含 AU 的元素耦合来激活翻译，以发育阶段特定的方式成核 MIWI/piRNA/eIF3f/HuR 超复合物的形成。这些发现揭示了 piRNA 系统在翻译激活中的关键作用，我们表明这在功能上是精子细胞发育所必需的。