CoChat
Sign Up
Cited by 71MicroRNA in disease regulationGenomics and Phylogenetic StudiesPlant Molecular Biology Research

Parallel DNA pyrosequencing unveils new zebrafish microRNAs

Open access
Soares, Ana R, Pereira, Patrícia M, Santos, Bruno, Egas, Conceição, Gomes, Ana C, Arrais, Joel, Oliveira, José L, Moura, Gabriela R +1 more·2009·BMC Genomics
DOI 10.1186/1471-2164-10-195PMC PMC2684549
Open this paper in CoChat — free accountOpen PDF

Abstract

Background: MicroRNAs (miRNAs) are a new class of small RNAs of approximately 22 nucleotides in length that control eukaryotic gene expression by fine tuning mRNA translation. They regulate a wide variety of biological processes, namely developmental timing, cell differentiation, cell proliferation, immune response and infection. For this reason, their identification is essential to understand eukaryotic biology. Their small size, low abundance and high instability complicated early identification, however cloning/Sanger sequencing and new generation genome sequencing approaches overcame most technical hurdles and are being used for rapid miRNA identification in many eukaryotes. Results: We have applied 454 DNA pyrosequencing technology to miRNA discovery in zebrafish (Danio rerio). For this, a series of cDNA libraries were prepared from miRNAs isolated at different embryonic time points and from fully developed organs. Each cDNA library was tagged with specific sequences and was sequenced using the Roche FLX genome sequencer. This approach retrieved 90% of the 192 miRNAs previously identified by cloning/Sanger sequencing and bioinformatics. Twenty five novel miRNAs were predicted, 107 miRNA star sequences and also 41 candidate miRNA targets were identified. A miRNA expression profile built on the basis of pyrosequencing read numbers showed high expression of most miRNAs throughout zebrafish development and identified tissue specific miRNAs. Conclusion: This study increases the number of zebrafish miRNAs from 192 to 217 and demonstrates that a single DNA mini-chip pyrosequencing run is effective in miRNA identification in zebrafish. This methodology also produced sufficient information to elucidate miRNA expression patterns during development and in differentiated organs. Moreover, some zebrafish miRNA star sequences were more abundant than their corresponding miRNAs, suggesting a functional role for the former in gene expression control in this vertebrate model organism.

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 · 10.1186/1471-2164-10-195

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?

  • miR-96* has been experimentally detected in humans, mouse, platypus and zebrafish, suggesting that the miRNA* species has been maintained throughout vertebrate evolution, although its sequence is only partially conserved.

    “The miR-96* has been experimentally detected in humans, mouse, platypus and zebrafish (mirBase, http://www.mirbase.org/) (18), suggesting that also the miRNA* species has been maintained throughout vertebrate evolution, although its sequence is only partially conserved.”

    From A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing (2012) · cites this paper as [18]

    The Results section, “Star sequences of zebrafish microRNAs” (page unavailable), reports detection of zebrafish miRNA* sequences generally. Searches for miR-96*, miR-96, and the named vertebrate species found no passage establishing detection of miR-96* in those species or its partial sequence conservation. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

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: 67

  1. Filipowicz W Bhattacharyya SN Sonenberg N Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008 9 102 114 18197166 10.1038/nrg2290 · DOI
  2. Pillai RS MicroRNA function: multiple mechanisms for a tiny RNA? RNA 2005 11 1753 1761 16314451 10.1261/rna.2248605 PMC1370863 · DOI · Paper page
  3. Bartel DP MicroRNAs: genomics, biogenesis, mechanism, and function Cell 2004 116 281 297 14744438 10.1016/S0092-8674(04)00045-5 · DOI
  4. Nilsen TW Mechanisms of microRNA-mediated gene regulation in animal cells Trends Genet 2007 23 243 249 17368621 10.1016/j.tig.2007.02.011 · DOI
  5. Ambros V The functions of animal microRNAs Nature 2004 431 350 355 15372042 10.1038/nature02871 · DOI · Paper page
  6. Zamore PD Haley B Ribo-gnome: the big world of small RNAs Science 2005 309 1519 1524 16141061 10.1126/science.1111444 · DOI
  7. He L Hannon GJ MicroRNAs: small RNAs with a big role in gene regulation Nat Rev Genet 2004 5 522 531 15211354 10.1038/nrg1379 · DOI · Paper page
  8. Wu L Fan J Belasco JG MicroRNAs direct rapid deadenylation of mRNA Proc Natl Acad Sci USA 2006 103 4034 4039 16495412 10.1073/pnas.0510928103 PMC1449641 · DOI
  9. Lee RC Feinbaum RL Ambros V The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 Cell 1993 75 843 854 8252621 10.1016/0092-8674(93)90529-Y · DOI · Paper page
  10. Reinhart BJ Weinstein EG Rhoades MW Bartel B Bartel DP MicroRNAs in plants Genes & Development 2002 16 1616 1626 12101121 10.1101/gad.1004402 PMC186362 · DOI
  11. Sunkar R Zhou XF Zheng Y Zhang WX Zhu JK Identification of novel and candidate miRNAs in rice by high throughput sequencing Bmc Plant Biology 2008 8 25 18312648 10.1186/1471-2229-8-25 PMC2292181 · DOI
  12. Wang JF Zhou H Chen YQ Luo QJ Qu LH Identification of 20 microRNAs from Oryza sativa Nucleic Acids Research 2004 32 1688 1695 15020705 10.1093/nar/gkh332 PMC390330 · DOI
  13. Wang XJ Reyes JL Chua NH Gaasterland T Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets Genome Biol 2004 5 R65 15345049 10.1186/gb-2004-5-9-r65 PMC522872 · DOI
  14. Berezikov E Thuemmler F van Laake LW Kondova I Bontrop R Cuppen E Diversity of microRNAs in human and chimpanzee brain Nature Genetics 2006 38 1375 1377 17072315 10.1038/ng1914 · DOI · Paper page
  15. Morin RD O'Connor MD Griffith M Kuchenbauer F Delaney A Prabhu AL Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells Genome Research 2008 18 610 621 18285502 10.1101/gr.7179508 PMC2279248 · DOI · Paper page
  16. Burnside J Ouyang M Anderson A Bernberg E Lu C Meyers BC Deep sequencing of chicken microRNAs Bmc Genomics 2008 9 185 18430245 10.1186/1471-2164-9-185 PMC2375912 · DOI
  17. Xu HT Wang XB Du ZL Li N Identification of microRNAs from different tissues of chicken embryo and adult chicken Febs Letters 2006 580 3610 3616 16750530 10.1016/j.febslet.2006.05.044 · DOI
  18. Chen PY Manninga H Slanchev K Chien MC Russo JJ Ju JY The developmental miRNA profiles of zebrafish as determined by small RNA cloning Genes & Development 2005 19 1288 1293 15937218 10.1101/gad.1310605 PMC1142552 · DOI
  19. Kloosterman WP Steiner FA Berezikov E de Bruijn E Belt J van de Verheul M Cloning and expression of new microRNAs from zebrafish Nucleic Acids Research 2006 34 2558 2569 16698962 10.1093/nar/gkl278 PMC3303176 · DOI
  20. Ramachandra RK Salem M Gahr S Rexroad CE Yao J Cloning and characterization of microRNAs from rainbow trout (Oncorhynchus mykiss): Their expression during early embryonic development Bmc Developmental Biology 2008 8 41 18412968 10.1186/1471-213X-8-41 PMC2374770 · DOI
  21. Watanabe T Takeda A Mise K Okuno T Suzuki T Minami N Stage-specific expression of microRNAs during Xenopus development Febs Letters 2005 579 318 324 15642338 10.1016/j.febslet.2004.11.067 · DOI
  22. Lim LP Lau NC Weinstein EG Abdelhakim A Yekta S Rhoades MW The microRNAs of Caenorhabditis elegans Genes & Development 2003 17 991 1008 12672692 10.1101/gad.1074403 PMC196042 · DOI · Paper page
  23. Lu J Shen Y Wu Q Kumar S He B Shi S The birth and death of microRNA genes in Drosophila Nat Genet 2008 40 351 355 18278047 10.1038/ng.73 · DOI
  24. Zhao T Li GL Mi SJ Li S Hannon GJ Wang XJ A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii Genes & Development 2007 21 1190 1203 17470535 10.1101/gad.1543507 PMC1865491 · DOI
  25. Pfeffer S Zavolan M Grasser FA Chien MC Russo JJ Ju JY Identification of virus-encoded microRNAs Science 2004 304 734 736 15118162 10.1126/science.1096781 · DOI
  26. Lagos-Quintana M Rauhut R Lendeckel W Tuschl T Identification of novel genes coding for small expressed RNAs Science 2001 294 853 858 11679670 10.1126/science.1064921 · DOI · Paper page
  27. Lau NC Lim LP Weinstein EG Bartel DP An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans Science 2001 294 858 862 11679671 10.1126/science.1065062 · DOI · Paper page
  28. Lee RC Ambros V An extensive class of small RNAs in Caenorhabditis elegans Science 2001 294 862 864 11679672 10.1126/science.1065329 · DOI · Paper page
  29. Tay YMS Tam WL Ang YS Gaughwin PM Yang H Wang WJ MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1 Stem Cells 2008 26 17 29 17916804 10.1634/stemcells.2007-0295 · DOI
  30. Tili E Michaille JJ Cimino A Costinean S Dumitru CD Adair B Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock J Immunol 2007 179 5082 5089 17911593
  31. Gupta A Gartner JJ Sethupathy P Hatzigeorgiou AG Fraser NW Anti-apoptotic function of a microRNA encoded by the HSV-1 latency-associated transcript Nature 2006 442 82 85 16738545
  32. Jopling CL Yi MK Lancaster AM Lemon SM Sarnow P Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA Science 2005 309 1577 1581 16141076 10.1126/science.1113329 · DOI
  33. Huang QH Gumireddy K Schrier M Le Sage C Nagel R Nair S The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis Nature Cell Biology 2008 10 202 U83 18193036 10.1038/ncb1681 · DOI
  34. Silber J Lim DA Petritsch C Persson AI Maunakea AK Yu M miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells BMC Med 2008 6 14 18577219 10.1186/1741-7015-6-14 PMC2443372 · DOI · Paper page
  35. varez-Garcia I Miska EA MicroRNA functions in animal development and human disease Development 2005 132 4653 4662 16224045 10.1242/dev.02073 · DOI
  36. Hafner M Landgraf P Ludwig J Rice A Ojo T Lin C Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing Methods 2008 44 3 12 18158127 10.1016/j.ymeth.2007.09.009 PMC2847350 · DOI
  37. Griffiths-Jones S The microRNA Registry Nucleic Acids Research 2004 32 D109 D111 14681370 10.1093/nar/gkh023 PMC308757 · DOI
  38. Giraldez AJ Mishima Y Rihel J Grocock RJ van DS Inoue K Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs Science 2006 312 75 79 16484454 10.1126/science.1122689 · DOI · Paper page
  39. Wienholds E Kloosterman WP Miska E varez-Saavedra E Berezikov E de BE MicroRNA expression in zebrafish embryonic development Science 2005 309 310 311 15919954 10.1126/science.1114519 · DOI · Paper page
  40. Giraldez AJ Cinalli RM Glasner ME Enright AJ Thomson JM Baskerville S MicroRNAs regulate brain morphogenesis in zebrafish Science 2005 308 833 838 15774722 10.1126/science.1109020 · DOI · Paper page
  41. Droege M Hill B The Genome Sequencer FLX trade mark System-Longer reads, more applications, straight forward bioinformatics and more complete data sets J Biotechnol 2008 136 3 10 18616967 10.1016/j.jbiotec.2008.03.021 · DOI
  42. Friedlander MR Chen W Adamidi C Maaskola J Einspanier R Knespel S Discovering microRNAs from deep sequencing data using miRDeep Nature Biotechnology 2008 26 407 415 18392026 10.1038/nbt1394 · DOI
  43. Thatcher EJ Bond J Paydar I Patton JG Genomic organization of zebrafish microRNAs BMC Genomics 2008 9 253 18510755 10.1186/1471-2164-9-253 PMC2427041 · DOI
  44. Subramanian S Fu Y Sunkar R Barbazuk WB Zhu JK Yu O Novel and nodulation-regulated microRNAs in soybean roots BMC Genomics 2008 9 18402695 PMC2335117
  45. Schloss PD Handelsman J The last word: Books as a statistical metaphor for microbial communities Annual Review of Microbiology 2007 61 23 34 17439361 10.1146/annurev.micro.61.011507.151712 · DOI
  46. Sogin ML Morrison HG Huber JA Mark Welch D Huse SM Neal PR Microbial diversity in the deep sea and the underexplored "rare biosphere" Proceedings of the National Academy of Sciences of the United States of America 2006 103 12115 12120 16880384 10.1073/pnas.0605127103 PMC1524930 · DOI
  47. Colwell RK Coddington JA Estimating Terrestrial Biodiversity Through Extrapolation Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 1994 345 101 118 10.1098/rstb.1994.0091 7972351 · DOI
  48. Chao A Estimating the Population-Size for Capture Recapture Data with Unequal Catchability Biometrics 1987 43 783 791 3427163 10.2307/2531532 · DOI
  49. Reid JG Nagaraja AK Lynn FC Drabek RB Muzny DM Shaw CA Mouse let-7 miRNA populations exhibit RNA editing that is constrained in the 5'-seed/cleavage/anchor regions and stabilize predicted mmu-let-7a: mRNA duplexes Genome Research 2008 18 1571 1581 18614752 10.1101/gr.078246.108 PMC2556275 · DOI
  50. Thatcher EJ Flynt AS Li N Patton JR Patton JG miRNA expression analysis during normal zebrafish development and following inhibition of the hedgehog and notch signaling pathways Developmental Dynamics 2007 236 2172 2180 17584857 10.1002/dvdy.21211 · DOI
  51. Artzi S Kiezun A Shomron N miRNAminer: a tool for homologous microRNA gene search BMC Bioinformatics 2008 9 39 18215311 10.1186/1471-2105-9-39 PMC2258288 · DOI
  52. Lewis BP Burge CB Bartel DP Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets Cell 2005 120 15 20 15652477 10.1016/j.cell.2004.12.035 · DOI · Paper page
  53. Maziere P Enright AJ Prediction of microRNA targets Drug Discovery Today 2007 12 452 458 17532529 10.1016/j.drudis.2007.04.002 · DOI
  54. Saito R Tabata Y Muto A Arai K Watanabe S Melk-like kinase plays a role in hematopoiesis in the zebra fish Molecular and Cellular Biology 2005 25 6682 6693 16024803 10.1128/MCB.25.15.6682-6693.2005 PMC1190327 · DOI
  55. Okamura K Phillips MD Tyler DM Duan H Chou YT Lai EC The regulatory activity of microRNA* species has substantial influence on microRNA and 3' UTR evolution Nat Struct Mol Biol 2008 15 354 363 18376413 10.1038/nsmb.1409 PMC2698667 · DOI · Paper page
  56. Makeyev EV Zhang JW Carrasco MA Maniatis T The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative Pre-mRNA splicing Molecular Cell 2007 27 435 448 17679093 10.1016/j.molcel.2007.07.015 PMC3139456 · DOI · Paper page
  57. Sonkoly E Wei T Janson PC Saaf A Lundeberg L Tengvall-Linder M MicroRNAs: novel regulators involved in the pathogenesis of Psoriasis? PLoS ONE 2007 2 e610 17622355 10.1371/journal.pone.0000610 PMC1905940 · DOI · Paper page
  58. Care A Catalucci D Felicetti F Bonci D Addario A Gallo P MicroRNA-133 controls cardiac hypertrophy Nat Med 2007 13 613 618 17468766 10.1038/nm1582 · DOI
  59. Zhao Y Ransom JF Li A Vedantham V von Drehle M Muth AN Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2 Cell 2007 129 303 317 17397913 10.1016/j.cell.2007.03.030 · DOI
  60. Lagos-Quintana M Rauhut R Yalcin A Meyer J Lendeckel W Tuschl T Identification of tissue-specific microRNAs from mouse Current Biology 2002 12 735 739 12007417 10.1016/S0960-9822(02)00809-6 · DOI · Paper page
  61. Esau C Davis S Murray SF Yu XX Pandey SK Pear M miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting Cell Metabolism 2006 3 87 98 16459310 10.1016/j.cmet.2006.01.005 · DOI · Paper page
  62. Glazov EA Cottee PA Barris WC Moore RJ Dalrymple BP Tizard ML A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach Genome Research 2008 18 957 964 18469162 10.1101/gr.074740.107 PMC2413163 · DOI
  63. Yu HH Moens CB Semaphorin signaling guides cranial neural crest cell migration in zebrafish Developmental Biology 2005 280 373 385 15882579 10.1016/j.ydbio.2005.01.029 · DOI
  64. Martyn U Schulte-Merker S Zebrafish neuropilins are differentially expressed and interact with vascular endothelial growth factor during embryonic vascular development Developmental Dynamics 2004 231 33 42 15305285 10.1002/dvdy.20048 · DOI
  65. Wilm TP Solnica-Krezel L Essential roles of a zebrafish prdm1/blimp1 homolog in embryo patterning and organogenesis Development 2005 132 393 404 15623803 10.1242/dev.01572 · DOI
  66. Miller CT Maves L Kimmel CB moz regulates Hox expression and pharyngeal segmental identity in zebrafish Development 2004 131 2443 2461 15128673 10.1242/dev.01134 · DOI
  67. Kubista M Andrade J Bengtsson M Forootan A Jona J Lind K The real-time polymerase chain reaction Mol Aspects Med 2006 27 95 125 16460794 10.1016/j.mam.2005.12.007 · DOI · Paper page

Cited by

Sorted by citations

Authors
Soares, A. R., Pereira, P. M., Santos, B., Egas, C., Gomes, A. C., Arrais, J., Oliveira, J. L., Moura, G. R., & Santos, M. A.
Affiliations
  • Centro de Estudos do Ambiente e do Mar (PT)
  • University of Aveiro (PT)
  • Biocant – Associação de Transferência de Tecnologia (PT)
Corresponding author
Santos, Manuel AS
ORCID
Venue
BMC Genomics
Publisher
Springer Science and Business Media LLC
Published
2009-04-27
Volume
10
Issue
1
Pages
195-195
ISSN
1471-2164 (ISSN-L)
DOI
10.1186/1471-2164-10-195
PMC
PMC2684549
OpenAlex
W2033018990
Cited by
71
References
2
Citations by year
2024: 3 · 2023: 1 · 2021: 2 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 5 · 2015: 7 · 2014: 6 · 2013: 6 · 2012: 14
FWCI
4.03
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Genomics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by)
  • Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, other-oa)
Funders
  • Universidade de Coimbra
  • Fundação para a Ciência e a Tecnologia
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords
microRNA, zebrafish, microRNA discovery, 454 pyrosequencing, miRNA target prediction, miRNA expression profiling, embryonic development, gene expression regulation
MeSH terms
Animals, Base Sequence, Life Cycle Stages, Molecular Sequence Data, Nucleic Acid Conformation, Zebrafish, Gene Library, Sequence Analysis, DNA, Computational Biology, Gene Expression Profiling, MicroRNAs

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