IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0141351.html
   My bibliography  Save this article

Altered Gene Expression Associated with microRNA Binding Site Polymorphisms

Author

Listed:
  • Urmo Võsa
  • Tõnu Esko
  • Silva Kasela
  • Tarmo Annilo

Abstract

Allele-specific gene expression associated with genetic variation in regulatory regions can play an important role in the development of complex traits. We hypothesized that polymorphisms in microRNA (miRNA) response elements (MRE-SNPs) that either disrupt a miRNA binding site or create a new miRNA binding site can affect the allele-specific expression of target genes. By integrating public expression quantitative trait locus (eQTL) data, miRNA binding site predictions, small RNA sequencing, and Argonaute crosslinking immunoprecipitation (AGO-CLIP) datasets, we identified genetic variants that can affect gene expression by modulating miRNA binding efficiency. We also identified MRE-SNPs located in regions associated with complex traits, indicating possible causative mechanisms associated with these loci. The results of this study expand the current understanding of gene expression regulation and help to interpret the mechanisms underlying eQTL effects.

Suggested Citation

  • Urmo Võsa & Tõnu Esko & Silva Kasela & Tarmo Annilo, 2015. "Altered Gene Expression Associated with microRNA Binding Site Polymorphisms," PLOS ONE, Public Library of Science, vol. 10(10), pages 1-24, October.
    • Handle: RePEc:plo:pone00:0141351
    DOI: 10.1371/journal.pone.0141351
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0141351
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0141351&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0141351?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sohail F. Tavazoie & Claudio Alarcón & Thordur Oskarsson & David Padua & Qiongqing Wang & Paula D. Bos & William L. Gerald & Joan Massagué, 2008. "Endogenous human microRNAs that suppress breast cancer metastasis," Nature, Nature, vol. 451(7175), pages 147-152, January.
    2. Joseph K. Pickrell & John C. Marioni & Athma A. Pai & Jacob F. Degner & Barbara E. Engelhardt & Everlyne Nkadori & Jean-Baptiste Veyrieras & Matthew Stephens & Yoav Gilad & Jonathan K. Pritchard, 2010. "Understanding mechanisms underlying human gene expression variation with RNA sequencing," Nature, Nature, vol. 464(7289), pages 768-772, April.
    3. Lee P. Lim & Nelson C. Lau & Philip Garrett-Engele & Andrew Grimson & Janell M. Schelter & John Castle & David P. Bartel & Peter S. Linsley & Jason M. Johnson, 2005. "Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs," Nature, Nature, vol. 433(7027), pages 769-773, February.
    4. Matthias Selbach & Björn Schwanhäusser & Nadine Thierfelder & Zhuo Fang & Raya Khanin & Nikolaus Rajewsky, 2008. "Widespread changes in protein synthesis induced by microRNAs," Nature, Nature, vol. 455(7209), pages 58-63, September.
    5. Huili Guo & Nicholas T. Ingolia & Jonathan S. Weissman & David P. Bartel, 2010. "Mammalian microRNAs predominantly act to decrease target mRNA levels," Nature, Nature, vol. 466(7308), pages 835-840, August.
    6. Bryan N Howie & Peter Donnelly & Jonathan Marchini, 2009. "A Flexible and Accurate Genotype Imputation Method for the Next Generation of Genome-Wide Association Studies," PLOS Genetics, Public Library of Science, vol. 5(6), pages 1-15, June.
    7. Daria V Zhernakova & Eleonora de Klerk & Harm-Jan Westra & Anastasios Mastrokolias & Shoaib Amini & Yavuz Ariyurek & Rick Jansen & Brenda W Penninx & Jouke J Hottenga & Gonneke Willemsen & Eco J de Ge, 2013. "DeepSAGE Reveals Genetic Variants Associated with Alternative Polyadenylation and Expression of Coding and Non-coding Transcripts," PLOS Genetics, Public Library of Science, vol. 9(6), pages 1-15, June.
    8. Michael Morley & Cliona M. Molony & Teresa M. Weber & James L. Devlin & Kathryn G. Ewens & Richard S. Spielman & Vivian G. Cheung, 2004. "Genetic analysis of genome-wide variation in human gene expression," Nature, Nature, vol. 430(7001), pages 743-747, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Evelyn Zacharewicz & Paul Della Gatta & John Reynolds & Andrew Garnham & Tamsyn Crowley & Aaron P Russell & Séverine Lamon, 2014. "Identification of MicroRNAs Linked to Regulators of Muscle Protein Synthesis and Regeneration in Young and Old Skeletal Muscle," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-25, December.
    2. Bo Jiang & Jun S. Liu, 2015. "Bayesian Partition Models for Identifying Expression Quantitative Trait Loci," Journal of the American Statistical Association, Taylor & Francis Journals, vol. 110(512), pages 1350-1361, December.
    3. Xiaodong Cai & Juan Andrés Bazerque & Georgios B Giannakis, 2013. "Inference of Gene Regulatory Networks with Sparse Structural Equation Models Exploiting Genetic Perturbations," PLOS Computational Biology, Public Library of Science, vol. 9(5), pages 1-13, May.
    4. Panagiotis Alexiou & Manolis Maragkakis & Giorgio L Papadopoulos & Victor A Simmosis & Lin Zhang & Artemis G Hatzigeorgiou, 2010. "The DIANA-mirExTra Web Server: From Gene Expression Data to MicroRNA Function," PLOS ONE, Public Library of Science, vol. 5(2), pages 1-7, February.
    5. Jin Hyun Ju & Sushila A Shenoy & Ronald G Crystal & Jason G Mezey, 2017. "An independent component analysis confounding factor correction framework for identifying broad impact expression quantitative trait loci," PLOS Computational Biology, Public Library of Science, vol. 13(5), pages 1-26, May.
    6. Joel W Graff & Linda S Powers & Anne M Dickson & Jongkwang Kim & Anna C Reisetter & Ihab H Hassan & Karol Kremens & Thomas J Gross & Mary E Wilson & Martha M Monick, 2012. "Cigarette Smoking Decreases Global MicroRNA Expression in Human Alveolar Macrophages," PLOS ONE, Public Library of Science, vol. 7(8), pages 1-13, August.
    7. Ray M Marín & Jiří Vaníček, 2012. "Optimal Use of Conservation and Accessibility Filters in MicroRNA Target Prediction," PLOS ONE, Public Library of Science, vol. 7(2), pages 1-11, February.
    8. Youjia Hua & Shiwei Duan & Andrea E Murmann & Niels Larsen & Jørgen Kjems & Anders H Lund & Marcus E Peter, 2011. "miRConnect: Identifying Effector Genes of miRNAs and miRNA Families in Cancer Cells," PLOS ONE, Public Library of Science, vol. 6(10), pages 1-16, October.
    9. Yasemin Oztemur & Tufan Bekmez & Alp Aydos & Isik G Yulug & Betul Bozkurt & Bala Gur Dedeoglu, 2015. "A Ranking-Based Meta-Analysis Reveals Let-7 Family as a Meta-Signature for Grade Classification in Breast Cancer," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-16, May.
    10. Daniel Svensson & Matilda Rentoft & Anna M Dahlin & Emma Lundholm & Pall I Olason & Andreas Sjödin & Carin Nylander & Beatrice S Melin & Johan Trygg & Erik Johansson, 2020. "A whole-genome sequenced control population in northern Sweden reveals subregional genetic differences," PLOS ONE, Public Library of Science, vol. 15(9), pages 1-18, September.
    11. Chuan Gao & Nan Wang & Xiuqing Guo & Julie T Ziegler & Kent D Taylor & Anny H Xiang & Yang Hai & Steven J Kridel & Jerry L Nadler & Fouad Kandeel & Leslie J Raffel & Yii-Der I Chen & Jill M Norris & J, 2015. "A Comprehensive Analysis of Common and Rare Variants to Identify Adiposity Loci in Hispanic Americans: The IRAS Family Study (IRASFS)," PLOS ONE, Public Library of Science, vol. 10(11), pages 1-17, November.
    12. Julia Schröder & Vitalia Schüller & Andrea May & Christian Gerges & Mario Anders & Jessica Becker & Timo Hess & Nicole Kreuser & René Thieme & Kerstin U Ludwig & Tania Noder & Marino Venerito & Lothar, 2019. "Identification of loci of functional relevance to Barrett’s esophagus and esophageal adenocarcinoma: Cross-referencing of expression quantitative trait loci data from disease-relevant tissues with gen," PLOS ONE, Public Library of Science, vol. 14(12), pages 1-12, December.
    13. David Lyon & Maria Angeles Castillejo & Christiana Staudinger & Wolfram Weckwerth & Stefanie Wienkoop & Volker Egelhofer, 2014. "Automated Protein Turnover Calculations from 15N Partial Metabolic Labeling LC/MS Shotgun Proteomics Data," PLOS ONE, Public Library of Science, vol. 9(4), pages 1-10, April.
    14. Sora Yoon & Seon-Young Kim & Dougu Nam, 2016. "Improving Gene-Set Enrichment Analysis of RNA-Seq Data with Small Replicates," PLOS ONE, Public Library of Science, vol. 11(11), pages 1-16, November.
    15. Agius Phaedra & Ying Yiming & Campbell Colin, 2009. "Bayesian Unsupervised Learning with Multiple Data Types," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 8(1), pages 1-29, June.
    16. Paul S de Vries & Maria Sabater-Lleal & Daniel I Chasman & Stella Trompet & Tarunveer S Ahluwalia & Alexander Teumer & Marcus E Kleber & Ming-Huei Chen & Jie Jin Wang & John R Attia & Riccardo E Mario, 2017. "Comparison of HapMap and 1000 Genomes Reference Panels in a Large-Scale Genome-Wide Association Study," PLOS ONE, Public Library of Science, vol. 12(1), pages 1-22, January.
    17. Alicia Hurtado & Irene Mota-Gómez & Miguel Lao & Francisca M. Real & Johanna Jedamzick & Miguel Burgos & Darío G. Lupiáñez & Rafael Jiménez & Francisco J. Barrionuevo, 2024. "Complete male-to-female sex reversal in XY mice lacking the miR-17~92 cluster," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    18. Rakesh Chettier & Lesa Nelson & James W Ogilvie & Hans M Albertsen & Kenneth Ward, 2015. "Haplotypes at LBX1 Have Distinct Inheritance Patterns with Opposite Effects in Adolescent Idiopathic Scoliosis," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-11, February.
    19. Michel S. Naslavsky & Marilia O. Scliar & Guilherme L. Yamamoto & Jaqueline Yu Ting Wang & Stepanka Zverinova & Tatiana Karp & Kelly Nunes & José Ricardo Magliocco Ceroni & Diego Lima Carvalho & Carlo, 2022. "Whole-genome sequencing of 1,171 elderly admixed individuals from Brazil," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    20. Steinrücken, Matthias & Paul, Joshua S. & Song, Yun S., 2013. "A sequentially Markov conditional sampling distribution for structured populations with migration and recombination," Theoretical Population Biology, Elsevier, vol. 87(C), pages 51-61.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0141351. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.