MicroRNA Transcriptomes Reveal Prevalence of Rare and Species-Specific Arm Switching Events During Zebrafish Ontogenesis

Overview

Journal Evol Bioinform Online

Publisher Sage Publications

Specialty Biology

Date 2024 Jul 26

PMID 39055772

Authors

Arthur Casulli de Oliveira

Luiz Augusto Bovolenta

Lucas Figueiredo

Amanda De Oliveira Ribeiro

Beatriz Jacinto Alves Pereira

Talita Roberto Aleixo de Almeida

Vinicius Farias Campos

James G Patton

Danillo Pinhal

Affiliations

Soon will be listed here.

Abstract

In metazoans, microRNAs (miRNAs) are essential regulators of gene expression, affecting critical cellular processes from differentiation and proliferation, to homeostasis. During miRNA biogenesis, the miRNA strand that loads onto the RNA-induced Silencing Complex (RISC) can vary, leading to changes in gene targeting and modulation of biological pathways. To investigate the impact of these "arm switching" events on gene regulation, we analyzed a diverse range of tissues and developmental stages in zebrafish by comparing 5p and 3p arms accumulation dynamics between embryonic developmental stages, adult tissues, and sexes. We also compared variable arm usage patterns observed in zebrafish to other vertebrates including arm switching data from fish, birds, and mammals. Our comprehensive analysis revealed that variable arm usage events predominantly take place during embryonic development. It is also noteworthy that isomiR occurrence correlates to changes in arm selection evidencing an important role of microRNA distinct isoforms in reinforcing and modifying gene regulation by promoting dynamics switches on miRNA 5p and 3p arms accumulation. Our results shed new light on the emergence and coordination of gene expression regulation and pave the way for future investigations in this field.

References

Watanabe Y, Yachie N, Numata K, Saito R, Kanai A, Tomita M . Computational analysis of microRNA targets in Caenorhabditis elegans. Gene. 2005; 365:2-10. DOI: 10.1016/j.gene.2005.09.035. View

Chen L, Sun H, Wang C, Yang Y, Zhang M, Wong G . miRNA arm switching identifies novel tumour biomarkers. EBioMedicine. 2018; 38:37-46. PMC: 6306400. DOI: 10.1016/j.ebiom.2018.11.003. View

Fan Y, Hu Y, Yang W . TGF-β superfamily: how does it regulate testis development. Mol Biol Rep. 2011; 39(4):4727-41. DOI: 10.1007/s11033-011-1265-5. View

Ruby J, Stark A, Johnston W, Kellis M, Bartel D, Lai E . Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 2007; 17(12):1850-64. PMC: 2099593. DOI: 10.1101/gr.6597907. View

Chen T, Chen J . Multifaceted roles of microRNAs: From motor neuron generation in embryos to degeneration in spinal muscular atrophy. Elife. 2019; 8. PMC: 6861003. DOI: 10.7554/eLife.50848. View

Wu H, Ye C, Ramirez D, Manjunath N . Alternative processing of primary microRNA transcripts by Drosha generates 5' end variation of mature microRNA. PLoS One. 2009; 4(10):e7566. PMC: 2762519. DOI: 10.1371/journal.pone.0007566. View

Chiang H, Schoenfeld L, Ruby J, Auyeung V, Spies N, Baek D . Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev. 2010; 24(10):992-1009. PMC: 2867214. DOI: 10.1101/gad.1884710. View

Oliveira A, Bovolenta L, Nachtigall P, Herkenhoff M, Lemke N, Pinhal D . Combining Results from Distinct MicroRNA Target Prediction Tools Enhances the Performance of Analyses. Front Genet. 2017; 8:59. PMC: 5432626. DOI: 10.3389/fgene.2017.00059. View

Stocks M, Moxon S, Mapleson D, Woolfenden H, Mohorianu I, Folkes L . The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets. Bioinformatics. 2012; 28(15):2059-61. PMC: 3400958. DOI: 10.1093/bioinformatics/bts311. View

10.

Qiu C, Chen G, Cui Q . Towards the understanding of microRNA and environmental factor interactions and their relationships to human diseases. Sci Rep. 2012; 2:318. PMC: 3306023. DOI: 10.1038/srep00318. View

11.

Berezikov E . Evolution of microRNA diversity and regulation in animals. Nat Rev Genet. 2011; 12(12):846-60. DOI: 10.1038/nrg3079. View

12.

Ma H, Wu Y, Choi J, Wu H . Lower and upper stem-single-stranded RNA junctions together determine the Drosha cleavage site. Proc Natl Acad Sci U S A. 2013; 110(51):20687-92. PMC: 3870748. DOI: 10.1073/pnas.1311639110. View

13.

Sharp P . The centrality of RNA. Cell. 2009; 136(4):577-80. DOI: 10.1016/j.cell.2009.02.007. View

14.

Harris M, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R . The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 2003; 32(Database issue):D258-61. PMC: 308770. DOI: 10.1093/nar/gkh036. View

15.

Glazov E, Cottee P, Barris W, Moore R, Dalrymple B, Tizard M . A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res. 2008; 18(6):957-64. PMC: 2413163. DOI: 10.1101/gr.074740.107. View

16.

Dexheimer P, Cochella L . MicroRNAs: From Mechanism to Organism. Front Cell Dev Biol. 2020; 8:409. PMC: 7283388. DOI: 10.3389/fcell.2020.00409. View

17.

Li S, Liao Y, Chan W, Ho M, Tsai K, Hu L . Interrogation of rabbit miRNAs and their isomiRs. Genomics. 2011; 98(6):453-9. DOI: 10.1016/j.ygeno.2011.08.008. View

18.

Wei C, Salichos L, Wittgrove C, Rokas A, Patton J . Transcriptome-wide analysis of small RNA expression in early zebrafish development. RNA. 2012; 18(5):915-29. PMC: 3334700. DOI: 10.1261/rna.029090.111. View

19.

Marco A, Macpherson J, Ronshaugen M, Griffiths-Jones S . MicroRNAs from the same precursor have different targeting properties. Silence. 2012; 3(1):8. PMC: 3503882. DOI: 10.1186/1758-907X-3-8. View

20.

Cutting A, Bannister S, Doran T, Sinclair A, Tizard M, Smith C . The potential role of microRNAs in regulating gonadal sex differentiation in the chicken embryo. Chromosome Res. 2011; 20(1):201-13. DOI: 10.1007/s10577-011-9263-y. View