miRCat2: accurate prediction of plant and animal microRNAs from next-generation sequencing datasets

Motivation: MicroRNAs are a class of ˜21‐22 nt small RNAs which are excised from a stable hairpin‐like secondary structure. They have important gene regulatory functions and are involved in many pathways including developmental timing, organogenesis and development in eukaryotes. There are several computational tools for miRNA detection from next‐generation sequencing datasets. However, many of these tools suffer from high false positive and false negative rates. Here we present a novel miRNA prediction algorithm, miRCat2. miRCat2 incorporates a new entropy‐based approach to detect miRNA loci, which is designed to cope with the high sequencing depth of current next‐generation sequencing datasets. It has a user‐friendly interface and produces graphical representations of the hairpin structure and plots depicting the alignment of sequences on the secondary structure. Results: We test miRCat2 on a number of animal and plant datasets and present a comparative analysis with miRCat, miRDeep2, miRPlant and miReap. We also use mutants in the miRNA biogenesis pathway to evaluate the predictions of these tools. Results indicate that miRCat2 has an improved accuracy compared with other methods tested. Moreover, miRCat2 predicts several new miRNAs that are differentially expressed in wild‐type versus mutants in the miRNA biogenesis pathway. Availability and Implementation: miRCat2 is part of the UEA small RNA Workbench and is freely available from http://srna‐workbench.cmp.uea.ac.uk/. Contact: v.moulton@uea.ac.uk or s.moxon@uea.ac.uk Supplementary information: Supplementary data are available at Bioinformatics online.

[1]  V. Kim,et al.  Re-evaluation of the roles of DROSHA, Exportin 5, and DICER in microRNA biogenesis , 2016, Proceedings of the National Academy of Sciences.

[2]  D. Voytas,et al.  MicroRNA Maturation and MicroRNA Target Gene Expression Regulation Are Severely Disrupted in Soybean dicer-like1 Double Mutants , 2015, G3: Genes, Genomes, Genetics.

[3]  C. Abreu-Goodger,et al.  High-Throughput Profiling of Caenorhabditis elegans Starvation-Responsive microRNAs , 2015, PloS one.

[4]  G. Meister,et al.  miRA: adaptable novel miRNA identification in plants using small RNA sequencing data , 2015, BMC Bioinformatics.

[5]  G. Wheeler,et al.  A Database of microRNA Expression Patterns in Xenopus laevis , 2015, PloS one.

[6]  J. Grenier,et al.  Dgcr8 and Dicer are essential for sex chromosome integrity during meiosis in males , 2015, Development.

[7]  J. Grenier,et al.  Dgcr8 and Dicer are essential for sex chromosome integrity during meiosis in males , 2015, Journal of Cell Science.

[8]  Marie-France Sagot,et al.  Mirinho: An efficient and general plant and animal pre-miRNA predictor for genomic and deep sequencing data , 2015, BMC Bioinformatics.

[9]  K. Thiel,et al.  Genetic Deficiency of Mtdh Gene in Mice Causes Male Infertility via Impaired Spermatogenesis and Alterations in the Expression of Small Non-coding RNAs* , 2015, The Journal of Biological Chemistry.

[10]  M. Friedländer,et al.  Bioengineering and Biotechnology Review Article Computational Prediction of Mirna Genes from Small Rna Sequencing Data , 2022 .

[11]  D. Patel,et al.  Adenylation of maternally inherited microRNAs by Wispy. , 2014, Molecular cell.

[12]  Lukasz Kurgan,et al.  Genome-wide analysis of thapsigargin-induced microRNAs and their targets in NIH3T3 cells , 2014, Genomics data.

[13]  Jikai Lei,et al.  miR-PREFeR: an accurate, fast and easy-to-use plant miRNA prediction tool using small RNA-Seq data , 2014, Bioinform..

[14]  Bin Yu,et al.  microRNA biogenesis, degradation and activity in plants , 2014, Cellular and Molecular Life Sciences.

[15]  Jiyuan An,et al.  miRPlant: an integrated tool for identification of plant miRNA from RNA sequencing data , 2014, BMC Bioinformatics.

[16]  S. Cho,et al.  Prediction of miRNA-mRNA associations in Alzheimer’s disease mice using network topology , 2014, BMC Genomics.

[17]  Lukasz Kurgan,et al.  P125Endoplasmic reticulum stress responses to disrupted endoplasmic reticulum ca2+ homeostasis , 2014 .

[18]  Phillip A Sharp,et al.  Endogenous miRNA and target concentrations determine susceptibility to potential ceRNA competition. , 2014, Molecular cell.

[19]  R. Sunkar,et al.  Global and local perturbation of the tomato microRNA pathway by a trans-activated DICER-LIKE 1 mutant , 2013, Journal of experimental botany.

[20]  Ana Kozomara,et al.  miRBase: annotating high confidence microRNAs using deep sequencing data , 2013, Nucleic Acids Res..

[21]  V. Kim,et al.  Regulation of microRNA biogenesis , 2014, Nature Reviews Molecular Cell Biology.

[22]  Xavier Estivill,et al.  Evidence for the biogenesis of more than 1,000 novel human microRNAs , 2014, Genome Biology.

[23]  Nicolas Servant,et al.  A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis , 2013, Briefings Bioinform..

[24]  Matthew B. Stocks,et al.  CoLIde: a bioinformatics tool for CO-expression-based small RNA Loci Identification using high-throughput sequencing data. , 2013, RNA biology.

[25]  Stefan L Ameres,et al.  Diversifying microRNA sequence and function , 2013, Nature Reviews Molecular Cell Biology.

[26]  C. Shin,et al.  miRAuto: An automated user-friendly MicroRNA prediction tool utilizing plant small RNA sequencing data , 2013, Molecules and cells.

[27]  Jens Allmer,et al.  Can MiRBase Provide Positive Data for Machine Learning for the Detection of MiRNA Hairpins? , 2013, J. Integr. Bioinform..

[28]  Sean R. Davis,et al.  NCBI GEO: archive for functional genomics data sets—update , 2012, Nucleic Acids Res..

[29]  C. Nelson,et al.  miRDeep*: an integrated application tool for miRNA identification from RNA sequencing data , 2012, Nucleic acids research.

[30]  Albert Kim,et al.  Detecting miRNAs in deep-sequencing data: a software performance comparison and evaluation , 2013, Briefings Bioinform..

[31]  V. Moulton,et al.  Diverse correlation patterns between microRNAs and their targets during tomato fruit development indicates different modes of microRNA actions , 2012, Planta.

[32]  Nahum Sonenberg,et al.  The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC , 2012, Nature Structural &Molecular Biology.

[33]  Vincent Moulton,et al.  The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets , 2012, Bioinform..

[34]  R. Green,et al.  miRNA-Mediated Gene Silencing by Translational Repression Followed by mRNA Deadenylation and Decay , 2012, Science.

[35]  A. Giraldez,et al.  Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish , 2012, Science.

[36]  Bairong Shen,et al.  Performance comparison and evaluation of software tools for microRNA deep-sequencing data analysis , 2012, Nucleic acids research.

[37]  Sebastian D. Mackowiak,et al.  miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades , 2011, Nucleic acids research.

[38]  Peter F. Stadler,et al.  ViennaRNA Package 2.0 , 2011, Algorithms for Molecular Biology.

[39]  Yufei Huang,et al.  MaturePred: Efficient Identification of MicroRNAs within Novel Plant Pre-miRNAs , 2011, PloS one.

[40]  Lei Li,et al.  miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants , 2011, Bioinform..

[41]  V. Moulton,et al.  Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns. , 2011, The Plant journal : for cell and molecular biology.

[42]  Jun Liu,et al.  Deep sequencing of small RNAs specifically associated with Arabidopsis AGO1 and AGO4 uncovers new AGO functions , 2011, The Plant journal : for cell and molecular biology.

[43]  B. Meyers,et al.  Experimental design, preprocessing, normalization and differential expression analysis of small RNA sequencing experiments , 2011, Silence.

[44]  Li Lin,et al.  Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. , 2011, Cancer cell.

[45]  Josh T. Cuperus,et al.  Evolution and Functional Diversification of MIRNA Genes , 2011, Plant Cell.

[46]  Hideaki Sugawara,et al.  The Sequence Read Archive , 2010, Nucleic Acids Res..

[47]  S. Moxon,et al.  Characterisation and expression of microRNAs in developing wings of the neotropical butterfly Heliconius melpomene , 2011, BMC Genomics.

[48]  Alessandra Carbone,et al.  MIReNA: finding microRNAs with high accuracy and no learning at genome scale and from deep sequencing data , 2010, Bioinform..

[49]  M. Lachmann,et al.  MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. , 2010, Genome research.

[50]  Monya Baker,et al.  Next-generation sequencing: adjusting to data overload , 2010, Nature Methods.

[51]  Álvaro L. Pérez-Quintero,et al.  Plant microRNAs and their role in defense against viruses: a bioinformatics approach , 2010, BMC Plant Biology.

[52]  David W. Taylor,et al.  A Novel miRNA Processing Pathway Independent of Dicer Requires Argonaute2 Catalytic Activity , 2010, Science.

[53]  Kyle Kai-How Farh,et al.  Expanding the microRNA targeting code: functional sites with centered pairing. , 2010, Molecular cell.

[54]  Alok Bhattacharya,et al.  Analysis of microRNA transcriptome by deep sequencing of small RNA libraries of peripheral blood , 2010, BMC Genomics.

[55]  P. Waterhouse,et al.  The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. , 2009, RNA.

[56]  M. Marra,et al.  Massively parallel sequencing: the next big thing in genetic medicine. , 2009, American journal of human genetics.

[57]  Ana M. Aransay,et al.  miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments , 2009, Nucleic Acids Res..

[58]  D. Bartel MicroRNAs: Target Recognition and Regulatory Functions , 2009, Cell.

[59]  Qingqing Zhang,et al.  Rice MicroRNA Effector Complexes and Targets , 2009 .

[60]  D. Bartel,et al.  Criteria for Annotation of Plant MicroRNAs , 2008, The Plant Cell Online.

[61]  Q. Cui,et al.  An Analysis of Human MicroRNA and Disease Associations , 2008, PloS one.

[62]  Vincent Moulton,et al.  A toolkit for analysing large-scale plant small RNA datasets , 2008, Bioinform..

[63]  B. Williams,et al.  Mapping and quantifying mammalian transcriptomes by RNA-Seq , 2008, Nature Methods.

[64]  Janet Kelso,et al.  PatMaN: rapid alignment of short sequences to large databases , 2008, Bioinform..

[65]  N. Rajewsky,et al.  Discovering microRNAs from deep sequencing data using miRDeep , 2008, Nature Biotechnology.

[66]  D. Bartel,et al.  MicroRNAS and their regulatory roles in plants. , 2006, Annual review of plant biology.

[67]  F. Slack,et al.  Oncomirs — microRNAs with a role in cancer , 2006, Nature Reviews Cancer.

[68]  Xuemei Chen,et al.  microRNA biogenesis and function in plants , 2005, FEBS letters.

[69]  C. Croce,et al.  MicroRNA gene expression deregulation in human breast cancer. , 2005, Cancer research.

[70]  V. Kim MicroRNA biogenesis: coordinated cropping and dicing , 2005, Nature Reviews Molecular Cell Biology.

[71]  M. Byrom,et al.  Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis , 2005, Nucleic acids research.

[72]  Xuemei Chen,et al.  Methylation as a Crucial Step in Plant microRNA Biogenesis , 2005, Science.

[73]  B. Cullen,et al.  Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha , 2005, The EMBO journal.

[74]  V. Kim,et al.  The Drosha-DGCR8 complex in primary microRNA processing. , 2004, Genes & development.

[75]  B. Cullen,et al.  Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. , 2004, RNA.

[76]  Yves Van de Peer,et al.  Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences , 2004, Bioinform..

[77]  R. Shiekhattar,et al.  The Microprocessor complex mediates the genesis of microRNAs , 2004, Nature.

[78]  G. Hannon,et al.  Processing of primary microRNAs by the Microprocessor complex , 2004, Nature.

[79]  Sanghyuk Lee,et al.  MicroRNA genes are transcribed by RNA polymerase II , 2004, The EMBO journal.

[80]  Yuichiro Watanabe,et al.  Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Adam M. Gustafson,et al.  Genetic and Functional Diversification of Small RNA Pathways in Plants , 2004, PLoS biology.

[82]  K. Czaplinski,et al.  Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. , 2004, RNA.

[83]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[84]  U. Kutay,et al.  Nuclear Export of MicroRNA Precursors , 2004, Science.

[85]  B. Cullen,et al.  Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. , 2003, Genes & development.

[86]  S. Jayasena,et al.  Functional siRNAs and miRNAs Exhibit Strand Bias , 2003, Cell.

[87]  V. Kim,et al.  The nuclear RNase III Drosha initiates microRNA processing , 2003, Nature.

[88]  Marjori Matzke,et al.  Evidence for Nuclear Processing of Plant Micro RNA and Short Interfering RNA Precursors1[w] , 2003, Plant Physiology.

[89]  J. Messing,et al.  CARPEL FACTORY, a Dicer Homolog, and HEN1, a Novel Protein, Act in microRNA Metabolism in Arabidopsis thaliana , 2002, Current Biology.

[90]  B. Reinhart,et al.  MicroRNAs in plants. , 2002, Genes & development.

[91]  L. Lim,et al.  An Abundant Class of Tiny RNAs with Probable Regulatory Roles in Caenorhabditis elegans , 2001, Science.

[92]  G. Hannon,et al.  C . elegans involved in developmental timing in Dicer functions in RNA interference and in synthesis of small RNA , 2001 .

[93]  A. Pasquinelli,et al.  Genes and Mechanisms Related to RNA Interference Regulate Expression of the Small Temporal RNAs that Control C. elegans Developmental Timing , 2001, Cell.

[94]  A. Pasquinelli,et al.  A Cellular Function for the RNA-Interference Enzyme Dicer in the Maturation of the let-7 Small Temporal RNA , 2001, Science.

[95]  A. Caudy,et al.  Role for a bidentate ribonuclease in the initiation step of RNA interference , 2001 .

[96]  Huaiyu Zhu On Information and Sufficiency , 1997 .