Literature DB >> 35588208

Uncoupling transcription and translation through miRNA-dependent poly(A) length control in haploid male germ cells.

Mei Guo1, Chunhai Luo2, Zhuqing Wang3,4, Sheng Chen4,5, Dayton Morris4, Fengying Ruan1, Zhichao Chen1, Linfeng Yang1, Xiongyi Wei2, Chuanwen Wu1, Bei Luo1, Zhou Lv1, Jin Huang1, Dong Zhang1, Cong Yu1, Qiang Gao1, Hongqi Wang1, Ying Zhang2, Fei Sun2, Wei Yan3,4,6, Chong Tang1,2.   

Abstract

As one of the post-transcriptional regulatory mechanisms, uncoupling of transcription and translation plays an essential role in development and adulthood physiology. However, it remains elusive how thousands of mRNAs get translationally silenced while stability is maintained for hours or even days before translation. In addition to oocytes and neurons, developing spermatids display significant uncoupling of transcription and translation for delayed translation. Therefore, spermiogenesis represents an excellent in vivo model for investigating the mechanism underlying uncoupled transcription and translation. Through full-length poly(A) deep sequencing, we discovered dynamic changes in poly(A) length through deadenylation and re-polyadenylation. Deadenylation appeared to be mediated by microRNAs (miRNAs), and transcripts with shorter poly(A) tails tend to be sequestered into ribonucleoprotein (RNP) granules for translational repression and stabilization. In contrast, re-polyadenylation might allow for translocation of the translationally repressed transcripts from RNP granules to polysomes. Overall, our data suggest that miRNA-dependent poly(A) length control represents a previously unreported mechanism underlying uncoupled translation and transcription in haploid male mouse germ cells.
© 2022. Published by The Company of Biologists Ltd.

Entities:  

Keywords:  Adenylation; Alternative splicing; Deadenylation; Infertility; MicroRNA; Mouse; Poly(A) tail; Polysome; RNP; Spermiogenesis; Uncoupling of transcription and translation

Mesh:

Substances:

Year:  2022        PMID: 35588208      PMCID: PMC9270972          DOI: 10.1242/dev.199573

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.862


  75 in total

1.  Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP.

Authors:  Shin-Ichi Kashiwabara; Junko Noguchi; Tiangang Zhuang; Ko Ohmura; Arata Honda; Shin Sugiura; Kiyoko Miyamoto; Satoru Takahashi; Kimiko Inoue; Atsuo Ogura; Tadashi Baba
Journal:  Science       Date:  2002-12-06       Impact factor: 47.728

2.  The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis.

Authors:  Qiuxia Wu; Rui Song; Nicole Ortogero; Huili Zheng; Ryan Evanoff; Chris L Small; Michael D Griswold; Satoshi H Namekawa; Helene Royo; James M Turner; Wei Yan
Journal:  J Biol Chem       Date:  2012-06-04       Impact factor: 5.157

Review 3.  Messenger RNA regulation: to translate or to degrade.

Authors:  Ann-Bin Shyu; Miles F Wilkinson; Ambro van Hoof
Journal:  EMBO J       Date:  2008-02-06       Impact factor: 11.598

Review 4.  Control of messenger RNA fate by RNA-binding proteins: an emphasis on mammalian spermatogenesis.

Authors:  R Keegan Idler; Wei Yan
Journal:  J Androl       Date:  2011-07-14

5.  A new G-tailing method for the determination of the poly(A) tail length applied to hepatitis A virus RNA.

Authors:  Y Y Kusov; G Shatirishvili; G Dzagurov; V Gauss-Müller
Journal:  Nucleic Acids Res       Date:  2001-06-15       Impact factor: 16.971

6.  mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos.

Authors:  Stephen W Eichhorn; Alexander O Subtelny; Iva Kronja; Jamie C Kwasnieski; Terry L Orr-Weaver; David P Bartel
Journal:  Elife       Date:  2016-07-30       Impact factor: 8.140

7.  m6A-dependent biogenesis of circular RNAs in male germ cells.

Authors:  Chong Tang; Yeming Xie; Tian Yu; Na Liu; Zhuqing Wang; Rebekah J Woolsey; Yunge Tang; Xinzong Zhang; Weibing Qin; Ying Zhang; Ge Song; Weiwei Zheng; Juan Wang; Weitian Chen; Xiongyi Wei; Zhe Xie; Rachel Klukovich; Huili Zheng; David R Quilici; Wei Yan
Journal:  Cell Res       Date:  2020-02-11       Impact factor: 25.617

8.  Spata6 is required for normal assembly of the sperm connecting piece and tight head-tail conjunction.

Authors:  Shuiqiao Yuan; Clifford J Stratton; Jianqiang Bao; Huili Zheng; Bhupal P Bhetwal; Ryuzo Yanagimachi; Wei Yan
Journal:  Proc Natl Acad Sci U S A       Date:  2015-01-20       Impact factor: 11.205

9.  Human MicroRNA targets.

Authors:  Bino John; Anton J Enright; Alexei Aravin; Thomas Tuschl; Chris Sander; Debora S Marks
Journal:  PLoS Biol       Date:  2004-10-05       Impact factor: 8.029

10.  mTAIL-seq reveals dynamic poly(A) tail regulation in oocyte-to-embryo development.

Authors:  Jaechul Lim; Mihye Lee; Ahyeon Son; Hyeshik Chang; V Narry Kim
Journal:  Genes Dev       Date:  2016-07-21       Impact factor: 11.361

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