Adenylation of Maternally Inherited MicroRNAs by Wispy

Overview

Journal Mol Cell

Publisher Cell Press

Specialty Cell Biology

Date 2014 Dec 3

PMID 25454948

Citations 54

Authors

Mihye Lee

Yeon Choi

Kijun Kim

Hua Jin

Jaechul Lim

Tuan Anh Nguyen

Jihye Yang

Minsun Jeong

Antonio J Giraldez

Hui Yang

Dinshaw J Patel

V Narry Kim

Affiliations

Soon will be listed here.

Abstract

Early development depends heavily on accurate control of maternally inherited mRNAs, and yet it remains unknown how maternal microRNAs are regulated during maternal-to-zygotic transition (MZT). We here find that maternal microRNAs are highly adenylated at their 3' ends in mature oocytes and early embryos. Maternal microRNA adenylation is widely conserved in fly, sea urchin, and mouse. We identify Wispy, a noncanonical poly(A) polymerase, as the enzyme responsible for microRNA adenylation in flies. Knockout of wispy abrogates adenylation and results in microRNA accumulation in eggs, whereas overexpression of Wispy increases adenylation and reduces microRNA levels in S2 cells. Wispy interacts with Ago1 through protein-protein interaction, which may allow the effective and selective adenylation of microRNAs. Thus, adenylation may contribute to the clearance of maternally deposited microRNAs during MZT. Our work provides mechanistic insights into the regulation of maternal microRNAs and illustrates the importance of RNA tailing in development.

Citing Articles

Analysis of somatic piRNAs in the malaria mosquito reveals atypical classes of genic small RNAs.

Funikov S, Rezvykh A, Akulenko N, Liang J, Sharakhov I, Kalmykova A RNA Biol. 2025; 22(1):1-16.

PMID: 39916410 PMC: 11834523. DOI: 10.1080/15476286.2025.2463812.

The biogenesis and regulation of animal microRNAs.

Kim H, Lee Y, Kim V Nat Rev Mol Cell Biol. 2024; .

PMID: 39702526 DOI: 10.1038/s41580-024-00805-0.

What goes up must come down: off switches for regulatory RNAs.

McJunkin K, Gottesman S Genes Dev. 2024; 38(13-14):597-613.

PMID: 39111824 PMC: 11368247. DOI: 10.1101/gad.351934.124.

Small RNAs: An expanding world with therapeutic promises.

Gou L, Zhu Q, Liu M Fundam Res. 2024; 3(5):676-682.

PMID: 38933305 PMC: 11197668. DOI: 10.1016/j.fmre.2023.03.003.

Target-directed microRNA degradation: Mechanisms, significance, and functional implications.

Hiers N, Li T, Traugot C, Xie M Wiley Interdiscip Rev RNA. 2024; 15(2):e1832.

PMID: 38448799 PMC: 11098282. DOI: 10.1002/wrna.1832.

References

Liu N, Abe M, Sabin L, Hendriks G, Naqvi A, Yu Z . The exoribonuclease Nibbler controls 3' end processing of microRNAs in Drosophila. Curr Biol. 2011; 21(22):1888-93. PMC: 3255556. DOI: 10.1016/j.cub.2011.10.006. View

Song J, Stoeckius M, Maaskola J, Friedlander M, Stepicheva N, Juliano C . Select microRNAs are essential for early development in the sea urchin. Dev Biol. 2011; 362(1):104-13. PMC: 3254792. DOI: 10.1016/j.ydbio.2011.11.015. View

Zhao Y, Yu Y, Zhai J, Ramachandran V, Dinh T, Meyers B . The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr Biol. 2012; 22(8):689-94. PMC: 3350747. DOI: 10.1016/j.cub.2012.02.051. View

Udagawa T, Swanger S, Takeuchi K, Kim J, Nalavadi V, Shin J . Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol Cell. 2012; 47(2):253-66. PMC: 3408552. DOI: 10.1016/j.molcel.2012.05.016. View

Backes S, Shapiro J, Sabin L, Pham A, Reyes I, Moss B . Degradation of host microRNAs by poxvirus poly(A) polymerase reveals terminal RNA methylation as a protective antiviral mechanism. Cell Host Microbe. 2012; 12(2):200-10. PMC: 3782087. DOI: 10.1016/j.chom.2012.05.019. View

Thornton J, Chang H, Piskounova E, Gregory R . Lin28-mediated control of let-7 microRNA expression by alternative TUTases Zcchc11 (TUT4) and Zcchc6 (TUT7). RNA. 2012; 18(10):1875-85. PMC: 3446710. DOI: 10.1261/rna.034538.112. View

Neilsen C, Goodall G, Bracken C . IsomiRs--the overlooked repertoire in the dynamic microRNAome. Trends Genet. 2012; 28(11):544-9. DOI: 10.1016/j.tig.2012.07.005. View

Heo I, Ha M, Lim J, Yoon M, Park J, Kwon S . Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell. 2012; 151(3):521-32. DOI: 10.1016/j.cell.2012.09.022. View

DAmbrogio A, Gu W, Udagawa T, Mello C, Richter J . Specific miRNA stabilization by Gld2-catalyzed monoadenylation. Cell Rep. 2012; 2(6):1537-45. PMC: 3534910. DOI: 10.1016/j.celrep.2012.10.023. View

10.

Chang H, Triboulet R, Thornton J, Gregory R . A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature. 2013; 497(7448):244-8. PMC: 3651781. DOI: 10.1038/nature12119. View

11.

Barckmann B, Simonelig M . Control of maternal mRNA stability in germ cells and early embryos. Biochim Biophys Acta. 2013; 1829(6-7):714-24. DOI: 10.1016/j.bbagrm.2012.12.011. View

12.

Cui J, Sartain C, Pleiss J, Wolfner M . Cytoplasmic polyadenylation is a major mRNA regulator during oogenesis and egg activation in Drosophila. Dev Biol. 2013; 383(1):121-31. PMC: 3821703. DOI: 10.1016/j.ydbio.2013.08.013. View

13.

Harding J, Horswell S, Heliot C, Armisen J, Zimmerman L, Luscombe N . Small RNA profiling of Xenopus embryos reveals novel miRNAs and a new class of small RNAs derived from intronic transposable elements. Genome Res. 2013; 24(1):96-106. PMC: 3875865. DOI: 10.1101/gr.144469.112. View

14.

Ha M, Kim V . Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014; 15(8):509-24. DOI: 10.1038/nrm3838. View

15.

Nakanishi T, Kubota H, Ishibashi N, Kumagai S, Watanabe H, Yamashita M . Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. Dev Biol. 2005; 289(1):115-26. DOI: 10.1016/j.ydbio.2005.10.017. View

16.

Bushati N, Cohen S . microRNA functions. Annu Rev Cell Dev Biol. 2007; 23:175-205. DOI: 10.1146/annurev.cellbio.23.090506.123406. View

17.

Pall G, Hamilton A . Improved northern blot method for enhanced detection of small RNA. Nat Protoc. 2008; 3(6):1077-84. DOI: 10.1038/nprot.2008.67. View

18.

Newman M, Thomson J, Hammond S . Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA. 2008; 14(8):1539-49. PMC: 2491462. DOI: 10.1261/rna.1155108. View

19.

Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl E, Nitsch R . A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol. 2008; 10(8):987-93. DOI: 10.1038/ncb1759. View

20.

Ramachandran V, Chen X . Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science. 2008; 321(5895):1490-2. PMC: 2570778. DOI: 10.1126/science.1163728. View