2. Academic Validation
  3. A Translation-Activating Function of MIWI/piRNA during Mouse Spermiogenesis

A Translation-Activating Function of MIWI/piRNA during Mouse Spermiogenesis

  • Cell. 2019 Dec 12;179(7):1566-1581.e16. doi: 10.1016/j.cell.2019.11.022.
Peng Dai 1,  Xin Wang 1,  Lan-Tao Gou 2,  Zhi-Tong Li 1,  Ze Wen 1,  Zong-Gui Chen 3,  Min-Min Hua 4,  Ai Zhong 1,  Lingbo Wang 5,  Haiyang Su 6,  Huida Wan 7,  Kun Qian 6,  Lujian Liao 7,  Jinsong Li 8,  Bin Tian 9,  Dangsheng Li 1,  Xiang-Dong Fu 10,  Hui-Juan Shi 11,  Yu Zhou 12,  Mo-Fang Liu 13
Affiliations

Affiliations

  • 1 State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences-University of Chinese Academy of Sciences, Shanghai 200031, China.
  • 2 State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences-University of Chinese Academy of Sciences, Shanghai 200031, China; Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0651, USA.
  • 3 College of Life Sciences, Institute of Advanced Studies, Wuhan University, Wuhan, Hubei 430072, China.
  • 4 State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences-University of Chinese Academy of Sciences, Shanghai 200031, China; NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Pharmacy School, Fudan University, Shanghai, 200032, China.
  • 5 NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Pharmacy School, Fudan University, Shanghai, 200032, China; State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences-University of Chinese Academy of Sciences, Shanghai 200031, China.
  • 6 School of Biomedical Engineering, Med-X Research Institute, Shanghai Jiao Tong University, Shanghai 200030, China.
  • 7 Shanghai Key Laboratory of Regulatory Biology and Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai 200241, China.
  • 8 State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences-University of Chinese Academy of Sciences, Shanghai 200031, China; School of Life Science and Technology, Shanghai Tech University, Shanghai 201210, China.
  • 9 Department of Microbiology, Biochemistry and Molecular Genetics, Rutgers New Jersey Medical School, Newark, New Jersey 07103, USA.
  • 10 Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0651, USA.
  • 11 NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Pharmacy School, Fudan University, Shanghai, 200032, China. Electronic address: shihuijuan@sippr.stc.sh.cn.
  • 12 College of Life Sciences, Institute of Advanced Studies, Wuhan University, Wuhan, Hubei 430072, China. Electronic address: yu.zhou@whu.edu.cn.
  • 13 State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences-University of Chinese Academy of Sciences, Shanghai 200031, China; School of Life Science and Technology, Shanghai Tech University, Shanghai 201210, China. Electronic address: mfliu@sibcb.ac.cn.
PMID: 31835033 DOI: 10.1016/j.cell.2019.11.022
Abstract

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.

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