Cited by 11

Aberration-corrected ultrafine analysis of miRNA reads at single-base resolution: a k-mer lattice approach

Zhang, Xuan, Ping, Pengyao, Hutvagner, Gyorgy, Blumenstein, Michael, Li, Jinyan·2021·Nucleic Acids Research

Abstract

Raw sequencing reads of miRNAs contain machine-made substitution errors, or even insertions and deletions (indels). Although the error rate can be low at 0.1%, precise rectification of these errors is critically important because isoform variation analysis at single-base resolution such as novel isomiR discovery, editing events understanding, differential expression analysis, or tissue-specific isoform identification is very sensitive to base positions and copy counts of the reads. Existing error correction methods do not work for miRNA sequencing data attributed to miRNAs’ length and per-read-coverage properties distinct from DNA or mRNA sequencing reads. We present a novel lattice structure combining kmers, (k – 1)mers and (k + 1)mers to address this problem. The method is particularly effective for the correction of indel errors. Extensive tests on datasets having known ground truth of errors demonstrate that the method is able to remove almost all of the errors, without introducing any new error, to improve the data quality from every-50-reads containing one error to every-1300-reads containing one error. Studies on experimental miRNA sequencing datasets show that the errors are often rectified at the 5′ ends and the seed regions of the reads, and that there are remarkable changes after the correction in miRNA isoform abundance, volume of singleton reads, overall entropy, isomiR families, tissue-specific miRNAs, and rare-miRNA quantities.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/nar/gkab610

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • All runs were evaluated for adapter sequences, and any samples with barcodes, unique molecular identifiers (UMIs), or adapter sequences on both ends were not processed (n = 1,870 runs were removed).

    “All runs were evaluated for adapter sequences, and any samples with barcodes, unique molecular identifiers (UMIs), or adapter sequences on both ends were not processed (n = 1,870 runs were removed) due to the use of miREC in the processing [47].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 50

  1. [1]Goodwin S., McPherson J.D., McCombie W.R. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 2016; 17: 333. 27184599 PMC10373632
  2. [2]Yeung C.L.A., Co N.-N., Tsuruga T., Yeung T.-L., Kwan S.-Y., Leung C.S., Li Y., Lu E.S., Kwan K., Wong K.-K. et al. Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat. Commun. 2016; 7: 11150. 27021436 PMC4820618
  3. [3]Xiao Y., MacRae I.J. Toward a comprehensive view of microRNA biology. Mol. Cell. 2019; 75: 666– 668. 31442421
  4. [4]Tan G.C., Chan E., Molnar A., Sarkar R., Alexieva D., Isa I.M., Robinson S., Zhang S., Ellis P., Langford C.F. et al. 5 isomiR variation is of functional and evolutionary importance. Nucleic Acids Res. 2014; 42: 9424– 9435. 25056318 PMC4132760
  5. [5]Trontti K., Väänänen J., Sipilä T., Greco D., Hovatta I. Strong conservation of inbred mouse strain microRNA loci but broad variation in brain microRNAs due to RNA editing and isomiR expression. RNA. 2018; 24: 643– 655. 29445025 PMC5900563
  6. [6]Fernandez-Valverde S.L., Taft R.J., Mattick J.S. Dynamic isomiR regulation in Drosophila development. RNA. 2010; 16: 1881– 1888. 20805289 PMC2941097
  7. [7]Meng L., Liu C., Lü J., Zhao Q., Deng S., Wang G., Qiao J., Zhang C., Zhen L., Lu Y. et al. Small RNA zippers lock miRNA molecules and block miRNA function in mammalian cells. Nat. Commun. 2017; 8: 13964. 28045030 PMC5216115
  8. [8]Liu H., Lei C., He Q., Pan Z., Xiao D., Tao Y. Nuclear functions of mammalian MicroRNAs in gene regulation, immunity and cancer. Mol. Cancer. 2018; 17: 64. 29471827 PMC5822656
  9. [9]Telonis A.G., Magee R., Loher P., Chervoneva I., Londin E., Rigoutsos I. Knowledge about the presence or absence of miRNA isoforms (isomiRs) can successfully discriminate amongst 32 TCGA cancer types. Nucleic Acids Res. 2017; 45: 2973– 2985. 28206648 PMC5389567
  10. [10]Dutta R.K., Chinnapaiyan S., Unwalla H. Aberrant micrornaomics in pulmonary complications: Implications in lung health and diseases. Mol. Ther.-Nucl. Acids. 2019; 18: 413– 431. PMC6831837 31655261
  11. [11]Dai F.-Q., Li C.-R., Fan X.-Q., Tan L., Wang R.-T., Jin H. miR-150-5p inhibits non-small-cell lung cancer metastasis and recurrence by targeting HMGA2 and β-catenin signaling. Mol. Ther.-Nucl. Acids. 2019; 16: 675– 685. PMC6529773 31121479
  12. [12]Pisignano G., Napoli S., Magistri M., Mapelli S.N., Pastori C., Di Marco S., Civenni G., Albino D., Enriquez C., Allegrini S. et al. A promoter-proximal transcript targeted by genetic polymorphism controls E-cadherin silencing in human cancers. Nat. Commun. 2017; 8: 15622. 28555645 PMC5459991
  13. [13]Yang A., Shao T.-J., Bofill-De Ros X., Lian C., Villanueva P., Dai L., Gu S. AGO-bound mature miRNAs are oligouridylated by TUTs and subsequently degraded by DIS3L2. Nat. Commun. 2020; 11: 2765. 32488030 PMC7265490
  14. [14]Liu C.-H., Wang Z., Huang S., Sun Y., Chen J. MicroRNA-145 regulates pathological retinal angiogenesis by suppression of TMOD3. Mol. Ther.-Nucl. Acids. 2019; 16: 335– 347. PMC6460252 30981984
  15. [16]Liu H.-P., Lai H.-M., Guo Z. Prostate cancer early diagnosis: circulating microRNA pairs potentially beyond single microRNAs upon 1231 serum samples. Brief. Bioinform. 2021; 22: bbaa111. 32607548
  16. [17]Bilanges B., Posor Y., Vanhaesebroeck B. PI3K isoforms in cell signalling and vesicle trafficking. Nat. Rev. Mol. Cell. Biol. 2019; 20: 515– 534. 31110302
  17. [18]Sänger L., Bender J., Rostowski K., Golbik R., Lilie H., Schmidt C., Behrens S.-E., Friedrich S. Alternatively spliced isoforms of AUF1 regulate a miRNA-mRNA interaction differentially through their YGG motif. RNA Biol. 2021; 18: 843– 853. 32924750 PMC8163432
  18. [19]Pillman K.A., Goodall G.J., Bracken C.P., Gantier M.P. miRNA length variation during macrophage stimulation confounds the interpretation of results: implications for miRNA quantification by RT-qPCR. RNA. 2019; 25: 232– 238. 30487268 PMC6348984
  19. [20]Hoefer I.E. Isolating functional (iso) miRNA targets during ischemia. Mol. Ther. 2020; 28: 7– 8. 31870621 PMC6953964
  20. [21]Neilsen C.T., Goodall G.J., Bracken C.P. IsomiRs—the overlooked repertoire in the dynamic microRNAome. Trends Genet. 2012; 28: 544– 549. 22883467
  21. [22]Lan C., Peng H., McGowan E.M., Hutvagner G., Li J. An isomiR expression panel based novel breast cancer classification approach using improved mutual information. BMC Med. Genomics. 2018; 11: 118. 30598116 PMC6311920
  22. [23]Salk J.J., Schmitt M.W., Loeb L.A. Enhancing the accuracy of next-generation sequencing for detecting rare and subclonal mutations. Nat. Rev. Genet. 2018; 19: 269. 29576615 PMC6485430
  23. [24]Laehnemann D., Borkhardt A., McHardy A.C. Denoising DNA deep sequencing data—high-throughput sequencing errors and their correction. Brief. Bioinform. 2016; 17: 154– 179. 26026159 PMC4719071
  24. [25]Mardis E.R. Next-generation sequencing platforms. Annu. Rev. Anal. Chem. 2013; 6: 287– 303. 23560931
  25. [26]Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. cell. 2004; 116: 281– 297. 14744438
  26. [27]Chekulaeva M., Filipowicz W. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 2009; 21: 452– 460. 19450959
  27. [28]Yu F., Pillman K.A., Neilsen C.T., Toubia J., Lawrence D.M., Tsykin A., Gantier M.P., Callen D.F., Goodall G.J., Bracken C.P. Naturally existing isoforms of miR-222 have distinct functions. Nucleic Acids Res. 2017; 45: 11371– 11385. 28981911 PMC5737821
  28. [29]Telonis A.G., Rigoutsos I. Race disparities in the contribution of miRNA isoforms and tRNA-derived fragments to triple-negative breast cancer. Cancer Res. 2018; 78: 1140– 1154. 29229607 PMC5935570
  29. [30]van der Kwast R.V., Woudenberg T., Quax P.H., Nossent A.Y. MicroRNA-411 and Its 5-IsomiR have distinct targets and functions and are differentially regulated in the vasculature under ischemia. Mol. Ther. 2020; 28: 157– 170. 31636041 PMC6953895
  30. [32]Mullany L.E., Herrick J.S., Wolff R.K., Slattery M.L. MicroRNA seed region length impact on target messenger RNA expression and survival in colorectal cancer. PloS one. 2016; 11: e0154177. 27123865 PMC4849741
  31. [33]Guo L., Chen F. A challenge for miRNA: multiple isomiRs in miRNAomics. Gene. 2014; 544: 1– 7. 24768184
  32. [34]Ebhardt H.A., Tsang H.H., Dai D.C., Liu Y., Bostan B., Fahlman R.P. Meta-analysis of small RNA-sequencing errors reveals ubiquitous post-transcriptional RNA modifications. Nucleic Acids Res. 2009; 37: 2461– 2470. 19255090 PMC2677864
  33. [35]Limasset A., Flot J.-F., Peterlongo P. Toward perfect reads: self-correction of short reads via mapping on de Bruijn graphs. Bioinformatics. 2020; 36: 1374– 1381. 30785192
  34. [36]Li H. BFC: correcting Illumina sequencing errors. Bioinformatics. 2015; 31: 2885– 2887. 25953801 PMC4635656
  35. [37]Sheikhizadeh S., de Ridder D. ACE: accurate correction of errors using K-mer tries. Bioinformatics. 2015; 31: 3216– 3218. 26026137
  36. [38]Heo Y., Wu X.-L., Chen D., Ma J., Hwu W.-M. BLESS: bloom filter-based error correction solution for high-throughput sequencing reads. Bioinformatics. 2014; 30: 1354– 1362. 24451628 PMC6365934
  37. [39]Salmela L., Schröder J. Correcting errors in short reads by multiple alignments. Bioinformatics. 2011; 27: 1455– 1461. 21471014
  38. [40]Kao W.-C., Chan A.H., Song Y.S. ECHO: a reference-free short-read error correction algorithm. Genome Res. 2011; 21: 1181– 1192. 21482625 PMC3129260
  39. [41]Allam A., Kalnis P., Solovyev V. Karect: accurate correction of substitution, insertion and deletion errors for next-generation sequencing data. Bioinformatics. 2015; 31: 3421– 3428. 26177965
  40. [42]Le H.-S., Schulz M.H., McCauley B.M., Hinman V.F., Bar-Joseph Z. Probabilistic error correction for RNA sequencing. Nucleic Acids Res. 2013; 41: e109. 23558750 PMC3664804
  41. [43]Song L., Florea L. Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads. GigaScience. 2015; 4: 48. 26500767 PMC4615873
  42. [44]Kokot M., Długosz M., Deorowicz S. KMC 3: counting and manipulating k-mer statistics. Bioinformatics. 2017; 33: 2759– 2761. 28472236
  43. [45]Seppey M., Manni M., Zdobnov E.M. LEMMI: a continuous benchmarking platform for metagenomics classifiers. Genome Res. 2020; 30: 1208– 1216. 32616517 PMC7462069
  44. [46]Woldemariam N.T., Agafonov O., Høyheim B., Houston R.D., Taggart J.B., Andreassen R. Expanding the miRNA repertoire in Atlantic salmon; discovery of isomiRs and miRNAs highly expressed in different tissues and developmental stages. Cells. 2019; 8: 42. PMC6356880 30641951
  45. [47]Andreassen R., Worren M.M., Høyheim B. Discovery and characterization of miRNA genes in Atlantic salmon (Salmo salar) by use of a deep sequencing approach. BMC Genomics. 2013; 14: 482. 23865519 PMC3728263
  46. [48]Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal. 2011; 17: 10– 12.
  47. [49]Stelzer G., Rosen N., Plaschkes I., Zimmerman S., Twik M., Fishilevich S., Stein T.I., Nudel R., Lieder I., Mazor Y. et al. The GeneCards suite: from gene data mining to disease genome sequence analyses. Curr. Protoc. Bioinformatics. 2016; 54: 1.30.1– 1.30.33. 27322403
  48. [50]Martí E., Pantano L., Bañez-Coronel M., Llorens F., Miñones-Moyano E., Porta S., Sumoy L., Ferrer I., Estivill X. A myriad of miRNA variants in control and Huntington—s disease brain regions detected by massively parallel sequencing. Nucleic Acids Res. 2010; 38: 7219– 7235. 20591823 PMC2978354
  49. [51]Hu J.F., Yim D., Ma D., Huber S.M., Davis N., Bacusmo J.M., Vermeulen S., Zhou J., Begley T.J., DeMott M.S. et al. Quantitative mapping of the cellular small RNA landscape with AQRNA-seq. Nat. Biotechnol. 2021; 10.1038/s41587-021-00874-y. PMC8355021 33859402 · DOI
  50. [52]Hu J.F., Yim D., Huber S.M., Bacusmo J.M., Ma D., DeMott M.S., Levine S.S., de Crécy-Lagard V., Dedon P.C., Cao B. Sequencing-based quantitative mapping of the cellular small RNA landscape. 2019; bioRxiv doi: 26 November 2019, preprint: not peer reviewedhttps://doi.org/10.1101/841130. · DOI

Cited by

Sorted by citations

Authors
Zhang, X., Ping, P., Hutvagner, G., Blumenstein, M., & Li, J.
Affiliations
  • Data Science Institute, University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia
  • School of Biomedical Engineering, Faculty of Engineering and IT, University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia
  • Faculty of Engineering and IT, University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia
Venue
Nucleic Acids Research
Published
2021-07-21
Volume
49
Issue
18
Pages
e106-e106
ISSN
  • 0305-1048
  • 1362-4962
Cited by
11
References
2
Language
en
Funders
Australian Research Council (DP 180100120)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review