[en] We herein describe the development of a biochemical method to evaluate the effect of single nucleotide polymorphisms (SNPs) in target genes on their regulation by microRNAs in vivo. The method is based on the detection of allelic imbalance in RNAs coimmunoprecipitated with AGO proteins from tissues of heterozygous individuals. We characterize the performances of our approach using a model system in a cell culture, and then apply it successfully to prove that the 3'UTR g+6223G-->A mutation operates by promoting RISC-dependent down-regulation of myostatin (MSTN) in skeletal muscle of Texel sheep.
Disciplines :
Genetics & genetic processes
Author, co-author :
Takeda, Haruko ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale
Charlier, Carole ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale
Farnir, Frédéric ; Université de Liège - ULiège > Département de productions animales > Biostatistiques et bioinformatique appliquées aux sc. vétér.
Abelson J, Kwan K, O'Roak B, Baek D, Stillman A, Morgan T, Mathews C, Pauls D, Rasin M, Gunel M, et al. 2005. Sequence variants in SLITRK1 are associated with Tourette's syndrome. Science 310: 317-320.
Adams B, Furneaux H, White B. 2007. The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-α (ERα) and represses ERα messenger RNA and protein expression in breast cancer cell lines. Mol Endocrinol 21: 1132-1147.
Beetz C, Schüle R, Deconinck T, Tran-Viet K, Zhu H, Kremer B, Frints S, van Zelst-Stams W, Byrne P, Otto S, et al. 2008. REEP1 mutation spectrum and genotype/phenotype correlation in hereditary spastic paraplegia type 31. Brain 131: 1078-1086.
Beitzinger M, Peters L, Zhu J, Kremmer E, Meister G. 2007. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol 4: 76-84.
Brendle A, Lei H, Brandt A, Johansson R, Enquist K, Henriksson R, Hemminki K, Lenner P, Forsti A. 2008. Polymorphisms in predicted microRNA-binding sites in integrin genes and breast cancer: ITGB4 as prognostic marker. Carcinogenesis 29: 1394-1399.
Chen K, Rajewsky N. 2007. The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8: 93-103. (Pubitemid 46122839)
Chi S, Zang J, Mele A, Darnell R. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
Chin LJ, Ratner E, Leng S, Zhai R, Nallur S, Babar I, Muller RU, Straka E, Su L, Burki EA, et al. 2008. A SNP in a let-7 microRNA complementary site in the KRAS 3′ untranslated region increases non-small cell lung cancer risk. Cancer Res 68: 8535-8540.
Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibé B, Bouix J, Caiment F, Elsen J, Eychenne F, et al. 2006. A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38: 813-818.
Easow G, Teleman A, Cohen S. 2007. Isolation of microRNA targets by miRNP immunopurification. RNA 13: 1198-1204.
Fasanaro P, Greco S, Lorenzi M, Pescatori M, Brioschi M, Kulshreshtha R, Banfi C, Stubbs A, Calin G, Ivan M, et al. 2009. An integrated approach for experimental target identification of hypoxia-induced miR-210. J Biol Chem 284: 35134-35143.
Friedman R, Farh K, Burge C, Bartel D. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
Ge B, Gurd S, Gaudin T, Dore C, Lepage P, Harmsen E, Hudson T, Pastinen T. 2005. Survey of allelic expression using EST mining. Genome Res 15: 1584-1591.
Hendrickson D, Hogan D, Herschlag D, Ferrell J, Brown P. 2008. Systematic identification of mRNAs recruited to argonaute 2 by specific microRNAs and corresponding changes in transcript abundance. PLoS ONE 3: e2126. doi: 10.1371/journal.pone.0002126.
Hiard S, Charlier C, Coppieters W, Georges M, Baurain D. 2010. Patrocles: A database of polymorphic miRNA-mediated gene regulation in vertebrates. Nucleic Acids Res 38: D640-D651.
Hong X, Hammell M, Ambros V, Cohen S. 2009. Immunopurification of Ago1 miRNPs selects for a distinct class of microRNA targets. Proc Natl Acad Sci 106: 15085-15090.
Jensen K, Covault J, Conner T, Tennen H, Kranzler H, Furneaux H. 2009. A common polymorphism in serotonin receptor 1B mRNA moderates regulation by miR-96 and associates with aggressive human behaviors. Mol Psychiatry 14: 381-389.
Kapeller J, Houghton L, Mönnikes H, Walstab J, Möller D, Bönisch H, Burwinkel B, Autschbach F, Funke B, Lasitschka F, et al. 2008. First evidence for an association of a functional variant in the microRNA-510 target site of the serotonin receptor-type 3E gene with diarrhea predominant irritable bowel syndrome. Hum Mol Genet 17: 2967-2977.
Karginov F, Conaco C, Xuan Z, Schmidt B, Parker J, Mandel G, Hannon G. 2007. A biochemical approach to identifying microRNA targets. Proc Natl Acad Sci 104: 19291-19296.
Kim J, Bartel D. 2009. Allelic imbalance sequencing reveals that single-nucleotide polymorphisms frequently alter microRNA-directed repression. Nat Biotechnol 27: 472-477.
Landi D, Gemignani F, Naccarati A, Pardini B, Vodicka P, Vodickova L, Novotny J, Försti A, Hemminki K, Canzian F, et al. 2008. Polymorphisms within micro-RNA-binding sites and risk of sporadic colorectal cancer. Carcinogenesis 29: 579-584.
Landthaler M, Gaidatzis D, Rothballer A, Chen P, Soll S, Dinic L, Ojo T, Hafner M, Zavolan M, Tuschl T. 2008. Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14: 2580-2596.
Lewis M, Quint E, Glazier A, Fuchs H, De Angelis M, Langford C, van Dongen S, Abreu-Goodger C, Piipari M, Redshaw N, et al. 2009. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat Genet 41: 614-618.
Lv K, Guo Y, Zhang Y, Wang K, Jia Y, Sun S. 2008. Allele-specific targeting of hsa-miR-657 to human IGF2R creates a potential mechanism underlying the association of ACAA-insertion/deletion polymorphism with type 2 diabetes. Biochem Biophys Res Commun 374: 101-105.
Masuda N, Ohnishi T, Kawamoto S, Monden M, Okubo K. 1999. Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples. Nucleic Acids Res 27: 4436-4443. (Pubitemid 29533185)
McPherron A, Lawler A, Lee S. 1997. Regulation of skeletal muscle mass in mice by a new TGF-b superfamily member. Nature 387: 83-90.
Mencía A, Modamio-Høybjør S, Redshaw N, Morín M, Mayo-Merino F, Olavarrieta L, Aguirre L, del Castillo I, Steel K, Dalmay T, et al. 2009. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat Genet 41: 609-613.
Mili S, Steitz J. 2004. Evidence for reassociation of RNA-binding proteins after cell lysis: Implications for the interpretation of immunoprecipitation analyses. RNA 10: 1692-1694.
Mishra P, Humeniuk R, Longo-Sorbello G, Banerjee D, Bertino J. 2007. A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci 104: 13513-13518.
Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L, Rappsilber J, Mann M, Dreyfuss G. 2002. miRNPs: A novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 16: 720-728.
Nelson P, Hatzigeorgiou A, Mourelatos Z. 2004. miRNP:mRNA association in polyribosomes in a human neuronal cell line. RNA 10: 387-394. (Pubitemid 38240999)
Nelson P, De Planell-Saguer M, Lamprinaki S, Kiriakidou M, Zhang P, O'Doherty U, Mourelatos Z. 2007. A novel monoclonal antibody against human Argonaute proteins reveals unexpected characteristics of miRNAs in human blood cells. RNA 13: 1787-1792.
Sethupathy P, Collins F. 2008. MicroRNA target site polymorphisms and human disease. Trends Genet 24: 489-497.
Sethupathy P, Borel C, Gagnebin M, Grant G, Deutsch S, Elton T, Hatzigeorgiou A, Antonarakis S. 2007. Human microRNA-155 on chromosome 21 differentially interacts with its polymorphic target in the AGTR1 3′ untranslated region: A mechanism for functional single-nucleotide polymorphisms related to phenotypes. Am J Hum Genet 81: 405-413.
Tan Z, Randall G, Fan J, Camoretti-Mercado B, Brockman-Schneider R, Pan L, Solway J, Gern J, Lemanske R, Nicolae D, et al 2007. Allele-specific targeting of microRNAs to HLA-G and risk of asthma. Am J Hum Genet 81: 829-834.
Tan L, Seinen E, Duns G, de Jong D, Sibon O, Poppema S, Kroesen B, Kok K, van den Berg A. 2009. A high throughput experimental approach to identify miRNA targets in human cells. Nucleic Acids Res 37: e137. doi: 10.1093/nar/gkp715.
Uejima H, Lee M, Cui H, Feinberg A. 2000. Hot-stop PCR: A simple and general assay for linear quantitation of allele ratios. Nat Genet 25: 375-376.
Vasudevan S, Steitz J. 2007. AU-rich-element-mediated up-regulation of translation by FXR1 and Argonaute 2. Cell 128: 1105-1118. (Pubitemid 46427873)
Verrier J, Lau P, Hudson L, Murashov A, Renne R, Notterpek L. 2009. Peripheral myelin protein 22 is regulated post-transcriptionally by miRNA-29a. Glia 57: 1265-1279.
Wang G, van der Walt J, Mayhew G, Li Y, Züchner S, Scott W, Martin E, Vance J. 2008. Variation in the miRNA-433 binding site of FGF20 confers risk for Parkinson disease by overexpression of α-synuclein. Am J Hum Genet 82: 283-289.
Wang W, Wilfred B, Hu Y, Stromberg A, Nelson P. 2010. Anti-Argonaute RIP-Chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 16: 394-404.
Zhang L, Ding L, Cheung TH, Dong M-Q, Chen J, Sewell AK, Liu X, Yates JR III, Han M. 2007. Systematic identification of C. elegans miRISC proteins, miRNAs, and mRNA targets by their interactions with GW182 proteins AIN-1 and AIN-2. Mol Cell 28: 598-613.
Zhang L, Hammell M, Kudlow B, Ambros V, Han M. 2009. Systematic analysis of dynamic miRNA-target interactions during C. elegans development. Development 136: 3043-3055.
Züchner S, Wang G, Tran-Viet K, Nance M, Gaskell P, Vance J, Ashley-Koch A, Pericak-Vance M. 2006. Mutations in the novel mitochondrial protein REEP1 cause hereditary spastic paraplegia type 31. Am J Hum Genet 79: 365-369.
