Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis.
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.
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Lan-Tao
LT
Gou
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Peng
P
Dai
Key Laboratory of Gene Engineering of the Ministry of Education, State Key Laboratory of Biocontrol, Sun Yat-sen University, Guangzhou, Guangzhou 510275, China.
Jian-Hua
JH
Yang
Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0651, USA.
Yuanchao
Y
Xue
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Yun-Ping
YP
Hu
Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0651, USA.
Yu
Y
Zhou
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Jun-Yan
JY
Kang
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Xin
X
Wang
Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0651, USA.
Hairi
H
Li
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Min-Min
MM
Hua
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Shuang
S
Zhao
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Si-Da
SD
Hu
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Li-Gang
LG
Wu
National Population and Family Planning Committee Key Laboratory of Contraceptive Drugs & Devices, Shanghai Institute of Planned Parenthood Research, Shanghai 200032, China.
Hui-Juan
HJ
Shi
Department of Biochemistry and Molecular Biology and Center for Genetics and Molecular Medicine, School of Medicine, University of Louisville, Louisville, KY 40202, US.
Yong
Y
Li
Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0651, USA.
Xiang-Dong
XD
Fu
Key Laboratory of Gene Engineering of the Ministry of Education, State Key Laboratory of Biocontrol, Sun Yat-sen University, Guangzhou, Guangzhou 510275, China.
Liang-Hu
LH
Qu
Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China.
En-Duo
ED
Wang
1] Center for RNA Research, State Key Laboratory of Molecular Biology-University of Chinese Academy of Sciences, Shanghai 200031, China [2] Shanghai Key Laboratory of Molecular Andrology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
Mo-Fang
MF
Liu
D020413:3' Untranslated Regions; D000818:Animals; D001483:Base Sequence; D005095:Exoribonucleases; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D008813:Mice, Inbred ICR; D011506:Proteins / Q000378:metabolism; D012333:RNA, Messenger / Q000378:metabolism*; D034741:RNA, Small Interfering / Q000378:metabolism*; D012097:Repressor Proteins; D012260:Ribonucleases; D016415:Sequence Alignment; D013087:Spermatids / Q000166:cytology / Q000378:metabolism; D013091:Spermatogenesis
D020413:3' Untranslated Regions; D011506:Proteins; D012333:RNA, Messenger; D034741:RNA, Small Interfering; D012097:Repressor Proteins; C489778:Cnot7 protein, mouse; D005095:Exoribonucleases; D012260:Ribonucleases