Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis

• DOI: 10.1038/cr.2014.41
• Publication Date: 2014-05-02T10:41:03Z
• Authors: Lan-Tao Gou; Peng Dai; Jian-Hua Yang; Yuanchao Xue; Yun-Ping Hu; Yu Zhou; Jun-Yan Kang; Xin Wang; Hairi Li; Min-Min Hua; Shuang Zhao; Si-Da Hu; Li-Gang Wu; Hui-Juan Shi; Yong Li; Xiang-Dong Fu; Liang-Hu Qu; En-Duo Wang; Mo-Fang Liu
• Keywords: Male; 0301 basic medicine; 570; MIWI; Messenger; Clinical Sciences; Inbred C57BL; Small Interfering; Mice; 03 medical and health sciences; Ribonucleases; Genetics; Animals; RNA, Messenger; RNA, Small Interfering; mRNA deadenylation; Spermatogenesis; 3' Untranslated Regions; Mice, Inbred ICR; 0303 health sciences; CAF1; Base Sequence; Proteins; pachytene piRNAs; pi-RISC; Stem Cell Research; Inbred ICR; Spermatids; Mice, Inbred C57BL; Repressor Proteins; ES; Exoribonucleases; RNA; Original Article; Biochemistry and Cell Biology; Sequence Alignment; Developmental Biology

Spermatogenesis in mammals is characterized by two waves of piRNA expression: one corresponds to classic piRNAs responsible for silencing retrotransponsons and the second wave is predominantly derived from nontransposon intergenic regions in pachytene spermatocytes, but the function of these pachytene piRNAs is largely unknown. Here, we report the involvement of pachytene piRNAs in instructing massive mRNA elimination in mouse elongating spermatids (ES). We demonstrate that a piRNA-induced silencing complex (pi-RISC) containing murine PIWI (MIWI) and deadenylase CAF1 is selectively assembled in ES, which is responsible for inducing mRNA deadenylation and decay via a mechanism that resembles the action of miRNAs in somatic cells. Such a highly orchestrated program appears to take full advantage of the enormous repertoire of diversified targeting capacity of pachytene piRNAs derived from nontransposon intergenic regions. These findings suggest that pachytene piRNAs are responsible for inactivating vast cellular programs in preparation for sperm production from ES.