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Research Paper

Divergent effects of translation termination factor eRF3A and nonsense-mediated mRNA decay factor UPF1 on the expression of uORF carrying mRNAs and ribosome protein genes

, ORCID Icon, , , , , & ORCID Icon show all
Pages 227-239 | Received 18 Apr 2019, Accepted 26 Sep 2019, Published online: 17 Oct 2019

References

  • Jackson RJ, Hellen CUT, Pestova TV. Termination and post-termination events in eukaryotic translation. Adv Protein Chem Struct Biol. 2012;86:45–93.
  • Lejeune F. Nonsense-mediated mRNA decay at the crossroads of many cellular pathways. BMB Rep. 2017;50:175–185.
  • Kim YK, Maquat LE. UPFront and center in RNA decay: UPF1 in nonsense-mediated mRNA decay and beyond. RNA. 2019;25:407–422.
  • Raimondeau E, Bufton JC, Schaffitzel C. New insights into the interplay between the translation machinery and nonsense-mediated mRNA decay factors. Biochem Soc Trans. 2018;46:503–512.
  • Losson R, Lacroute F. Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc Natl Acad Sci USA. 1979;76:5134–5137.
  • Maquat LE, Kinniburgh AJ, Rachmilewitz EA, et al. Unstable β-globin mRNA in mRNA-deficient β0 thalassemia. Cell. 1981;27:543–553.
  • Leeds P, Peltz SW, Jacobson A, et al. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 1991;5:2303–2314.
  • Bühler M, Steiner S, Mohn F, et al. EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3ʹ UTR length. Nat Struct Mol Biol. 2006;13:462–464.
  • Hansen KD, Lareau LF, Blanchette M, et al. Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet. 2009;5:e1000525.
  • Mendell JT, Sharifi NA, Meyers JL, et al. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat Genet. 2004;36:1073–1078.
  • Singh G, Rebbapragada I, Lykke-Andersen J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 2008;6:e111.
  • Yepiskoposyan H, Aeschimann F, Nilsson D, et al. Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA. 2011;17:2108–2118.
  • Cosson B, Berkova N, Couturier A, et al. Poly(A)-binding protein and eRF3 are associated in vivo in human and Xenopus cells. Biol Cell. 2002;94:205–216.
  • Hoshino S, Imai M, Kobayashi T, et al. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3ʹ-Poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J Biol Chem. 1999;274:16677–16680.
  • Kashima I, Yamashita A, Izumi N, et al. Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev. 2006;20:355–367.
  • Neu‐Yilik G, Raimondeau E, Eliseev B, et al. Dual function of UPF3B in early and late translation termination. EMBO J. 2017;36:2968–2986.
  • Eberle AB, Stalder L, Mathys H, et al. Posttranscriptional gene regulation by spatial rearrangement of the 3ʹ untranslated region. PLoS Biol. 2008;6:e92.
  • Ivanov PV, Gehring NH, Kunz JB, et al. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 2008;27:736–747.
  • Celik A, Baker R, He F, et al. High-resolution profiling of NMD targets in yeast reveals translational fidelity as a basis for substrate selection. RNA. 2017;23:735–748.
  • Colombo M, Karousis ED, Bourquin J, et al. Transcriptome-wide identification of NMD-targeted human mRNAs reveals extensive redundancy between SMG6- and SMG7-mediated degradation pathways. RNA. 2017;23:189–201.
  • Hurt JA, Robertson AD, Burge CB. Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res. 2013;23:1636–1650.
  • Pan Q, Saltzman AL, Kim YK, et al. Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes Dev. 2006;20:153–158.
  • Tani H, Imamachi N, Salam KA, et al. Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol. 2012;9:1370–1379.
  • Wittmann J, Hol EM, Jäck H-M. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol. 2006;26:1272–1287.
  • Malabat C, Feuerbach F, Ma L, et al. Quality control of transcription start site selection by nonsense-mediated-mRNA decay. eLife. 2015;4:e06722.
  • Chapin A, Hu H, Rynearson SG, et al. In vivo determination of direct targets of the nonsense-mediated decay pathway in Drosophila. G3 Genes Genom Genet. 2014;4:485–496.
  • Huang L, Lou C-H, Chan W, et al. RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol Cell. 2011;43:950–961.
  • Lykke-Andersen S, Jensen TH. Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol. 2015;16:665–677.
  • Ait Ghezala H, Jolles B, Salhi S, et al. Translation termination efficiency modulates ATF4 response by regulating ATF4 mRNA translation at 5ʹ short ORFs. Nucleic Acids Res. 2012;40:9557–9570.
  • Hoshino S, Miyazawa H, Enomoto T, et al. A human homologue of the yeast GST1 gene codes for a GTP-binding protein and is expressed in a proliferation-dependent manner in mammalian cells. EMBO J. 1989;8:3807–3814.
  • Kikuchi Y, Shimatake H, Kikuchi A. A yeast gene required for the G1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. EMBO J. 1988;7:1175–1182.
  • Chauvin C, Salhi S, Jean-Jean O. Human eukaryotic release factor 3a depletion causes cell cycle arrest at G1 phase through inhibition of the mTOR pathway. Mol Cell Biol. 2007;27:5619–5629.
  • Hashimoto Y, Inagaki H, Hoshino S. Calpain mediates processing of the translation termination factor eRF3 into the IAP-binding isoform p-eRF3. FEBS Lett. 2015;589:2241–2247.
  • Hegde R, Srinivasula SM, Datta P, et al. The polypeptide chain-releasing factor GSPT1/eRF3 is proteolytically processed into an IAP-binding protein. J Biol Chem. 2003;278:38699–38706.
  • Jolles B, Aliouat A, Stierlé V, et al. Translation termination-dependent deadenylation of MYC mRNA in human cells. Oncotarget. 2018;9:26171–26182.
  • Osawa M, Hosoda N, Nakanishi T, et al. Biological role of the two overlapping poly(A)-binding protein interacting motifs 2 (PAM2) of eukaryotic releasing factor eRF3 in mRNA decay. RNA. 2012;18:1957–1967.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
  • Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1–13.
  • Azzalin CM, Reichenbach P, Khoriauli L, et al. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science. 2007;318:798–801.
  • Hong D, Park T, Jeong S. Nuclear UPF1 is associated with chromatin for transcription-coupled RNA surveillance. Mol Cells. 2019;42:523–529.
  • Mendell JT. ap Rhys CMJ, Dietz HC. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science. 2002;298:419–422.
  • Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci U S A. 2004;101:11269–11274.
  • Zhao C, Datta S, Mandal P, et al. Stress-sensitive regulation of IFRD1 mRNA decay is mediated by an upstream open reading frame. J Biol Chem. 2010;285:8552–8562.
  • Calkhoven CF, Müller C, Leutz A. Translational control of C/EBPalpha and C/EBPbeta isoform expression. Genes Dev. 2000;14:1920–1932.
  • Wethmar K, Bégay V, Smink JJ, et al. C/EBPbetaDeltauORF mice–a genetic model for uORF-mediated translational control in mammals. Genes Dev. 2010;24:15–20.
  • Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986;44:283–292.
  • Calvo SE, Pagliarini DJ, Mootha VK. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc Natl Acad Sci USA. 2009;106:7507–7512.
  • Johnstone TG, Bazzini AA, Giraldez AJ. Upstream ORFs are prevalent translational repressors in vertebrates. EMBO J. 2016;35:706–723.
  • Guo H, Ingolia NT, Weissman JS, et al. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466:835–840.
  • Ingolia NT, Ghaemmaghami S, Newman JRS, et al. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009;324:218–223.
  • Dey S, Baird TD, Zhou D, et al. Both transcriptional regulation and translational control of ATF4 are central to the integrated stress response. J Biol Chem. 2010;285:33165–33174.
  • Gardner LB. Hypoxic inhibition of nonsense-mediated RNA decay regulates gene expression and the integrated stress response. Mol Cell Biol. 2008;28:3729–3741.
  • Iacono M, Mignone F, Pesole G. uAUG and uORFs in human and rodent 5′untranslated mRNAs. Gene. 2005;349:97–105.
  • Brar GA, Yassour M, Friedman N, et al. High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science. 2012;335:552–557.
  • Ye Y, Liang Y, Yu Q, et al. Analysis of human upstream open reading frames and impact on gene expression. Hum Genet. 2015;134:605–612.
  • Wethmar K. The regulatory potential of upstream open reading frames in eukaryotic gene expression. Wiley Interdiscip Rev RNA. 2014;5:765–778.
  • Chauvin C, Salhi S, Le Goff C, et al. Involvement of human release factors eRF3a and eRF3b in translation termination and regulation of the termination complex formation. Mol Cell Biol. 2005;25:5801–5811.
  • Neu-Yilik G, Amthor B, Gehring NH, et al. Mechanism of escape from nonsense-mediated mRNA decay of human -globin transcripts with nonsense mutations in the first exon. RNA. 2011;17:843–854.
  • Pereira FJC, Teixeira A, Kong J, et al. Resistance of mRNAs with AUG-proximal nonsense mutations to nonsense-mediated decay reflects variables of mRNA structure and translational activity. Nucleic Acids Res. 2015;43:6528–6544.
  • Zhang J, Maquat LE. Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J. 1997;16:826–833.
  • Stockklausner C, Breit S, Neu-Yilik G, et al. The uORF-containing thrombopoietin mRNA escapes nonsense-mediated decay (NMD). Nucleic Acids Res. 2006;34:2355–2363.
  • Kozak M. The scanning model for translation: an update. J Cell Biol. 1989;108:229–241.
  • Wang J, Vock VM, Li S, et al. A quality control pathway that down-regulates aberrant T-cell receptor (TCR) transcripts by a mechanism requiring UPF2 and translation. J Biol Chem. 2002;277:18489–18493.
  • Hu H, Li X. Transcriptional regulation in eukaryotic ribosomal protein genes. Genomics. 2007;90:421–423.
  • Russo A, Russo G. Ribosomal proteins control or bypass p53 during nucleolar stress. Int J Mol Sci. 2017;18:140.
  • Li BB, Qian C, Gameiro PA, et al. Targeted profiling of RNA translation reveals mTOR-4EBP1/2-independent translation regulation of mRNAs encoding ribosomal proteins. Proc Natl Acad Sci USA. 2018;115:E9325–32.
  • Gupta V, Warner JR. Ribosome-omics of the human ribosome. RNA. 2014;20:1004–1013.
  • Warner JR, McIntosh KB. How common are extraribosomal functions of ribosomal proteins? Mol Cell. 2009;34:3–11.
  • Zhou X, Liao W-J, Liao J-M, et al. Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol. 2015;7:92–104.
  • Geng W, Qin F, Ren J, et al. Mini-peptide RPL41 attenuated retinal neovascularization by inducing degradation of ATF4 in oxygen-induced retinopathy mice. Exp Cell Res. 2018;369:243–250.
  • Wang A, Xu S, Zhang X, et al. Ribosomal protein RPL41 induces rapid degradation of ATF4, a transcription factor critical for tumour cell survival in stress. J Pathol. 2011;225:285–292.
  • Cai X, Gao L, Teng L, et al. Runx1 deficiency decreases ribosome biogenesis and confers stress resistance to hematopoietic stem and progenitor cells. Cell Stem Cell. 2015;17:165–177.
  • Ishii K, Washio T, Uechi T, et al. Characteristics and clustering of human ribosomal protein genes. BMC Genomics. 2006;7:37.
  • Li X, Zheng Y, Hu H, et al. Integrative analyses shed new light on human ribosomal protein gene regulation. Sci Rep. 2016;6:28619.
  • Paillusson A. A GFP-based reporter system to monitor nonsense-mediated mRNA decay. Nucleic Acids Res. 2005;33:e54–e54.
  • Baudin-Baillieu A, Hatin I, Legendre R, et al. Translation analysis at the genome scale by ribosome profiling. Methods Mol Biol. 2016;1361:105–124.
  • Martin F, Barends S, Jaeger S, et al. Cap-assisted internal initiation of translation of histone H4. Mol Cell. 2011;41:197–209.
  • Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
  • Kinsella RJ, Kähäri A, Haider S, et al. Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database. 2011;2011:bar030.
  • Kim D-Y, Kim W, Lee K-H, et al. hnRNP Q regulates translation of p53 in normal and stress conditions. Cell Death Differ. 2013;20:226–234.
  • Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–930.
  • Varet H, Brillet-Guéguen L, Coppée J-Y, et al. SARTools: a DESeq2- and EdgeR-based R pipeline for comprehensive differential analysis of RNA-seq data. PloS One. 2016;11:e0157022.
  • Schulze SK, Kanwar R, Gölzenleuchter M, et al. SERE: single-parameter quality control and sample comparison for RNA-Seq. BMC Genomics. 2012;13:524.
  • Rodriguez JM, Maietta P, Ezkurdia I, et al. APPRIS: annotation of principal and alternative splice isoforms. Nucleic Acids Res. 2013;41:D110–117.
  • Babicki S, Arndt D, Marcu A, et al. Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res. 2016;44:W147–153.
  • Descombes P, Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell. 1991;67:569–579.