1932

Abstract

Nonsense-mediated mRNA decay (NMD) is a eukaryotic surveillance mechanism that monitors cytoplasmic mRNA translation and targets mRNAs undergoing premature translation termination for rapid degradation. From yeasts to humans, activation of NMD requires the function of the three conserved Upf factors: Upf1, Upf2, and Upf3. Here, we summarize the progress in our understanding of the molecular mechanisms of NMD in several model systems and discuss recent experiments that address the roles of Upf1, the principal regulator of NMD, in the initial targeting and final degradation of NMD-susceptible mRNAs. We propose a unified model for NMD in which the Upf factors provide several functions during premature termination, including the stimulation of release factor activity and the dissociation and recycling of ribosomal subunits. In this model, the ultimate degradation of the mRNA is the last step in a complex premature termination process.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112414-054639
2015-11-23
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/genet/49/1/annurev-genet-112414-054639.html?itemId=/content/journals/10.1146/annurev-genet-112414-054639&mimeType=html&fmt=ahah

Literature Cited

  1. Ajamian L, Abrahamyan L, Milev M, Ivanov PV, Kulozik AE. 1.  et al. 2008. Unexpected roles for UPF1 in HIV-1 RNA metabolism and translation. RNA 14:914–27 [Google Scholar]
  2. Alkalaeva EZ, Pisarev AV, Frolova LY, Kisselev LL, Pestova TV. 2.  2006. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell 125:1125–36 [Google Scholar]
  3. Altamura N, Groudinsky O, Dujardin G, Slonimski PP. 3.  1992. NAM7 nuclear gene encodes a novel member of a family of helicases with a Zn-ligand motif and is involved in mitochondrial functions in Saccharomyces cerevisiae. J. Mol. Biol. 224:575–87 [Google Scholar]
  4. Amrani N, Ganesan R, Kervestin S, Mangus DA, Ghosh S, Jacobson A. 4.  2004. A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432:112–18 [Google Scholar]
  5. Amrani N, Ghosh S, Mangus DA, Jacobson A. 5.  2008. Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453:1276–80 [Google Scholar]
  6. Amrani N, Sachs MS, Jacobson A. 6.  2006. Early nonsense: mRNA decay solves a translational problem. Nat. Rev. Mol. Cell Biol. 7:415–25 [Google Scholar]
  7. Anders KR, Grimson A, Anderson P. 7.  2003. SMG-5, required for C. elegans nonsense-mediated mRNA decay, associates with SMG-2 and protein phosphatase 2A. EMBO J. 22:641–50 [Google Scholar]
  8. Applequist SE, Selg M, Raman C, Jack HM. 8.  1997. Cloning and characterization of HUPF1, a human homolog of the Saccharomyces cerevisiae nonsense mRNA-reducing UPF1 protein. Nucleic Acids Res. 25:814–21 [Google Scholar]
  9. Aravind L, Koonin EV. 9.  2000. Eukaryote-specific domains in translation initiation factors: implications for translation regulation and evolution of the translation system. Genome Res. 10:1172–84 [Google Scholar]
  10. Arribere JA, Gilbert WV. 10.  2013. Roles for transcript leaders in translation and mRNA decay revealed by transcript leader sequencing. Genome Res. 23:977–87 [Google Scholar]
  11. Atkin AL, Altamura N, Leeds P, Culbertson MR. 11.  1995. The majority of yeast UPF1 co-localizes with polyribosomes in the cytoplasm. Mol. Biol. Cell 6:611–25 [Google Scholar]
  12. Avery P, Vicente-Crespo M, Francis D, Nashchekina O, Alonso CR, Palacios IM. 12.  2011. Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf3-independent manner. RNA 17:624–38 [Google Scholar]
  13. Balistreri G, Horvath P, Schweingruber C, Zund D, McInerney G. 13.  et al. 2014. The host nonsense-mediated mRNA decay pathway restricts mammalian RNA virus replication. Cell Host Microbe 16:403–11 [Google Scholar]
  14. Barthelme D, Dinkelaker S, Albers SV, Londei P, Ermler U, Tampe R. 14.  2011. Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. PNAS 108:3228–33 [Google Scholar]
  15. Bashyam MD. 15.  2009. Nonsense-mediated decay: linking a basic cellular process to human disease. Expert Rev. Mol. Diagn. 9:299–303 [Google Scholar]
  16. Becker T, Franckenberg S, Wickles S, Shoemaker CJ, Anger AM. 16.  et al. 2012. Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature 482:501–6 [Google Scholar]
  17. Behm-Ansmant I, Gatfield D, Rehwinkel J, Hilgers V, Izaurralde E. 17.  2007. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J. 26:1591–601 [Google Scholar]
  18. Behm-Ansmant I, Kashima I, Rehwinkel J, Sauliere J, Wittkopp N, Izaurralde E. 18.  2007. mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 581:2845–53 [Google Scholar]
  19. Belgrader P, Cheng J, Maquat LE. 19.  1993. Evidence to implicate translation by ribosomes in the mechanism by which nonsense codons reduce the nuclear level of human triosephosphate isomerase mRNA. PNAS 90:482–86 [Google Scholar]
  20. Bhattacharya A, Czaplinski K, Trifillis P, He F, Jacobson A, Peltz SW. 20.  2000. Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA 6:1226–35 [Google Scholar]
  21. Bidou L, Allamand V, Rousset JP, Namy O. 21.  2012. Sense from nonsense: therapies for premature stop codon diseases. Trends Mol. Med. 18:679–88 [Google Scholar]
  22. Boehm V, Haberman N, Ottens F, Ule J, Gehring NH. 22.  2014. 3′ UTR length and messenger ribonucleoprotein composition determine endocleavage efficiencies at termination codons. Cell Rep. 9:555–68 [Google Scholar]
  23. Bono F, Gehring NH. 23.  2011. Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol. 8:24–29 [Google Scholar]
  24. Bruno IG, Karam R, Huang L, Bhardwaj A, Lou CH. 24.  et al. 2011. Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol. Cell 42:500–10 [Google Scholar]
  25. Buchwald G, Ebert J, Basquin C, Sauliere J, Jayachandran U. 25.  et al. 2010. Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. PNAS 107:10050–55 [Google Scholar]
  26. Cao D, Parker R. 26.  2001. Computational modeling of eukaryotic mRNA turnover. RNA 7:1192–212 [Google Scholar]
  27. Cao D, Parker R. 27.  2003. Computational modeling and experimental analysis of nonsense-mediated decay in yeast. Cell 113:533–45 [Google Scholar]
  28. Chakrabarti S, Bonneau F, Schussler S, Eppinger E, Conti E. 28.  2014. Phospho-dependent and phospho-independent interactions of the helicase UPF1 with the NMD factors SMG5-SMG7 and SMG6. Nucleic Acids Res. 42:9447–60 [Google Scholar]
  29. Chakrabarti S, Jayachandran U, Bonneau F, Fiorini F, Basquin C. 29.  et al. 2011. Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell 41:693–703 [Google Scholar]
  30. Chamieh H, Ballut L, Bonneau F, Le Hir H. 30.  2008. NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat. Struct. Mol. Biol. 15:85–93 [Google Scholar]
  31. Chan WK, Bhalla AD, Le Hir H, Nguyen LS, Huang L. 31.  et al. 2009. A UPF3-mediated regulatory switch that maintains RNA surveillance. Nat. Struct. Mol. Biol. 16:747–53 [Google Scholar]
  32. Chazal PE, Daguenet E, Wendling C, Ulryck N, Tomasetto C. 32.  et al. 2013. EJC core component MLN51 interacts with eIF3 and activates translation. PNAS 110:5903–8 [Google Scholar]
  33. Cheng Z, Saito K, Pisarev AV, Wada M, Pisareva VP. 33.  et al. 2009. Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev. 23:1106–18 [Google Scholar]
  34. Cho H, Han S, Choe J, Park SG, Choi SS, Kim YK. 34.  2013. SMG5-PNRC2 is functionally dominant compared with SMG5-SMG7 in mammalian nonsense-mediated mRNA decay. Nucleic Acids Res. 41:1319–28 [Google Scholar]
  35. Cho H, Kim KM, Han S, Choe J, Park SG. 35.  et al. 2012. Staufen1-mediated mRNA decay functions in adipogenesis. Mol. Cell 46:495–506 [Google Scholar]
  36. Cho H, Kim KM, Kim YK. 36.  2009. Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell 33:75–86 [Google Scholar]
  37. Clerici M, Deniaud A, Boehm V, Gehring NH, Schaffitzel C, Cusack S. 37.  2014. Structural and functional analysis of the three MIF4G domains of nonsense-mediated decay factor UPF2. Nucleic Acids Res. 42:2673–86 [Google Scholar]
  38. Clerici M, Mourao A, Gutsche I, Gehring NH, Hentze MW. 38.  et al. 2009. Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J. 28:2293–306 [Google Scholar]
  39. Colak D, Ji SJ, Porse BT, Jaffrey SR. 39.  2013. Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell 153:1252–65 [Google Scholar]
  40. Cosson B, Couturier A, Chabelskaya S, Kiktev D, Inge-Vechtomov S. 40.  et al. 2002. Poly(A)-binding protein acts in translation termination via eukaryotic release factor 3 interaction and does not influence [PSI+] propagation. Mol. Cell. Biol. 22:3301–15 [Google Scholar]
  41. Cui Y, Hagan KW, Zhang S, Peltz SW. 41.  1995. Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes Dev. 9:423–36 [Google Scholar]
  42. Culbertson MR. 42.  1999. RNA surveillance. Unforeseen consequences for gene expression, inherited genetic disorders and cancer. Trends Genet. 15:74–80 [Google Scholar]
  43. Czaplinski K, Ruiz-Echevarria MJ, Paushkin SV, Han X, Weng Y. 43.  et al. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12:1665–77 [Google Scholar]
  44. Czaplinski K, Weng Y, Hagan KW, Peltz SW. 44.  1995. Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA 1:610–23 [Google Scholar]
  45. Decourty L, Doyen A, Malabat C, Frachon E, Rispal D. 45.  et al. 2014. Long open reading frame transcripts escape nonsense-mediated mRNA decay in yeast. Cell Rep. 6:593–98 [Google Scholar]
  46. Denning G, Jamieson L, Maquat LE, Thompson EA, Fields AP. 46.  2001. Cloning of a novel phosphatidylinositol kinase-related kinase: characterization of the human SMG-1 RNA surveillance protein. J. Biol. Chem. 276:22709–14 [Google Scholar]
  47. de Pinto B, Lippolis R, Castaldo R, Altamura N. 47.  2004. Overexpression of Upf1p compensates for mitochondrial splicing deficiency independently of its role in mRNA surveillance. Mol. Microbiol. 51:1129–42 [Google Scholar]
  48. Drake KM, Dunmore BJ, McNelly LN, Morrell NW, Aldred MA. 48.  2013. Correction of nonsense BMPR2 and SMAD9 mutations by ataluren in pulmonary arterial hypertension. Am. J. Respir. Cell. Mol. Biol. 49:403–9 [Google Scholar]
  49. Dunn JG, Foo CK, Belletier NG, Gavis ER, Weissman JS. 49.  2013. Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster. eLife 2:e01179 [Google Scholar]
  50. Durand S, Lykke-Andersen J. 50.  2013. Nonsense-mediated mRNA decay occurs during eIF4F-dependent translation in human cells. Nat. Struct. Mol. Biol. 20:702–9 [Google Scholar]
  51. Eberle AB, Lykke-Andersen S, Muhlemann O, Jensen TH. 51.  2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16:49–55 [Google Scholar]
  52. Eberle AB, Stalder L, Mathys H, Orozco RZ, Muhlemann O. 52.  2008. Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLOS Biol. 6:e92 [Google Scholar]
  53. Fatscher T, Boehm V, Weiche B, Gehring NH. 53.  2014. The interaction of cytoplasmic poly(A)-binding protein with eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay. RNA 20:1579–92 [Google Scholar]
  54. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J. 54.  2005. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20:905–15 [Google Scholar]
  55. Fourati Z, Roy B, Millan C, Coureux P-D, Kervestin S. 55.  et al. 2014. A highly conserved region essential for NMD in the Upf2 N-terminal domain. J. Mol. Biol. 426:3689–702 [Google Scholar]
  56. Franks TM, Singh G, Lykke-Andersen J. 56.  2010. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143:938–50 [Google Scholar]
  57. Frischmeyer PA, Dietz HC. 57.  1999. Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8:1893–900 [Google Scholar]
  58. Fukuhara N, Ebert J, Unterholzner L, Lindner D, Izaurralde E, Conti E. 58.  2005. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell 17:537–47 [Google Scholar]
  59. Gaba A, Jacobson A, Sachs MS. 59.  2005. Ribosome occupancy of the yeast CPA1 upstream open reading frame termination codon modulates nonsense-mediated mRNA decay. Mol. Cell 20:449–60 [Google Scholar]
  60. Gardner LB. 60.  2010. Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol. Cancer Res. 8:295–308 [Google Scholar]
  61. Gatfield D, Unterholzner L, Ciccarelli FD, Bork P, Izaurralde E. 61.  2003. Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J. 22:3960–70 [Google Scholar]
  62. Ge Y, Porse BT. 62.  2014. The functional consequences of intron retention: alternative splicing coupled to NMD as a regulator of gene expression. BioEssays 36:236–43 [Google Scholar]
  63. Gehring NH, Kunz JB, Neu-Yilik G, Breit S, Viegas MH. 63.  et al. 2005. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell 20:65–75 [Google Scholar]
  64. Gehring NH, Neu-Yilik G, Schell T, Hentze MW, Kulozik AE. 64.  2003. Y14 and hUpf3b form an NMD-activating complex. Mol. Cell 11:939–49 [Google Scholar]
  65. Ghosh S, Ganesan R, Amrani N, Jacobson A. 65.  2010. Translational competence of ribosomes released from a premature termination codon is modulated by NMD factors. RNA 16:1832–47 [Google Scholar]
  66. Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C. 66.  et al. 2007. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179–91 [Google Scholar]
  67. Glavan F, Behm-Ansmant I, Izaurralde E, Conti E. 67.  2006. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25:5117–25 [Google Scholar]
  68. Gloggnitzer J, Akimcheva S, Srinivasan A, Kusenda B, Riehs N. 68.  et al. 2014. Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe 16:376–90 [Google Scholar]
  69. Goldmann T, Overlack N, Wolfrum U, Nagel-Wolfrum K. 69.  2011. PTC124-mediated translational readthrough of a nonsense mutation causing Usher syndrome type 1C. Hum. Gene Ther. 22:537–47 [Google Scholar]
  70. Gong C, Kim YK, Woeller CF, Tang Y, Maquat LE. 70.  2009. SMD and NMD are competitive pathways that contribute to myogenesis: effects on PAX3 and myogenin mRNAs. Genes Dev. 23:54–66 [Google Scholar]
  71. Gonzalez CI, Ruiz-Echevarria MJ, Vasudevan S, Henry MF, Peltz SW. 71.  2000. The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense-mediated mRNA decay. Mol. Cell 5:489–99 [Google Scholar]
  72. Goodenough E, Robinson TM, Zook MB, Flanigan KM, Atkins JF. 72.  et al. 2014. Cryptic MHC class I–binding peptides are revealed by aminoglycoside-induced stop codon read-through into the 3′ UTR. PNAS 111:5670–75 [Google Scholar]
  73. Gozalbo D, Hohmann S. 73.  1990. Nonsense suppressors partially revert the decrease of the mRNA level of a nonsense mutant allele in yeast. Curr. Genet. 17:77–79 [Google Scholar]
  74. Gregersen LH, Schueler M, Munschauer M, Mastrobuoni G, Chen W. 74.  et al. 2014. MOV10 is a 5′ to 3′ RNA helicase contributing to UPF1 mRNA target degradation by translocation along 3′ UTRs. Mol. Cell 54:573–85 [Google Scholar]
  75. Gregory-Evans CY, Wang X, Wasan KM, Zhao J, Metcalfe AL, Gregory-Evans K. 75.  2014. Postnatal manipulation of Pax6 dosage reverses congenital tissue malformation defects. J. Clin. Investig. 124:111–16 [Google Scholar]
  76. Grimson A, O'Connor S, Newman CL, Anderson P. 76.  2004. SMG-1 is a phosphatidylinositol kinase-related protein kinase required for nonsense-mediated mRNA decay in Caenorhabditis elegans. Mol. Cell. Biol. 24:7483–90 [Google Scholar]
  77. He F, Brown AH, Jacobson A. 77.  1996. Interaction between Nmd2p and Upf1p is required for activity but not for dominant-negative inhibition of the nonsense-mediated mRNA decay pathway in yeast. RNA 2:153–70 [Google Scholar]
  78. He F, Brown AH, Jacobson A. 78.  1997. Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 17:1580–94 [Google Scholar]
  79. He F, Ganesan R, Jacobson A. 79.  2013. Intra- and intermolecular regulatory interactions in Upf1, the RNA helicase central to nonsense-mediated mRNA decay in yeast. Mol. Cell. Biol. 33:4672–84 [Google Scholar]
  80. He F, Jacobson A. 80.  1995. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9:437–54 [Google Scholar]
  81. He F, Jacobson A. 81.  2001. Upf1p, Nmd2p, and Upf3p regulate the decapping and exonucleolytic degradation of both nonsense-containing mRNAs and wild-type mRNAs. Mol. Cell. Biol. 21:1515–30 [Google Scholar]
  82. He F, Jacobson A. 82.  2015. Control of mRNA decapping by positive and negative regulatory elements in the C-terminal domain of Dcp2. RNA 21:1633–47 [Google Scholar]
  83. He F, Li X, Spatrick P, Casillo R, Dong S, Jacobson A. 83.  2003. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol. Cell 12:1439–52 [Google Scholar]
  84. He F, Peltz SW, Donahue JL, Rosbash M, Jacobson A. 84.  1993. Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1-mutant. PNAS 90:7034–38 [Google Scholar]
  85. Hilleren P, Parker R. 85.  1999. mRNA surveillance in eukaryotes: kinetic proofreading of proper translation termination as assessed by mRNP domain organization?. RNA 5:711–19 [Google Scholar]
  86. Hogg JR, Goff SP. 86.  2010. Upf1 senses 3′UTR length to potentiate mRNA decay. Cell 143:379–89 [Google Scholar]
  87. Holbrook JA, Neu-Yilik G, Hentze MW, Kulozik AE. 87.  2004. Nonsense-mediated decay approaches the clinic. Nat. Genet. 36:801–8 [Google Scholar]
  88. Hoshino S, Imai M, Kobayashi T, Uchida N, Katada T. 88.  1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3′-poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J. Biol. Chem. 274:16677–80 [Google Scholar]
  89. Hu W, Petzold C, Coller J, Baker KE. 89.  2010. Nonsense-mediated mRNA decapping occurs on polyribosomes in Saccharomyces cerevisiae. Nat. Struct. Mol. Biol. 17:244–47 [Google Scholar]
  90. Huntzinger E, Kashima I, Fauser M, Sauliere J, Izaurralde E. 90.  2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14:2609–17 [Google Scholar]
  91. Hurt JA, Robertson AD, Burge CB. 91.  2013. Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res. 23:1636–50 [Google Scholar]
  92. Ingolia NT, Lareau LF, Weissman JS. 92.  2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147:789–802 [Google Scholar]
  93. Ishigaki Y, Li X, Serin G, Maquat LE. 93.  2001. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106:607–17 [Google Scholar]
  94. Isken O, Maquat LE. 94.  2007. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21:1833–56 [Google Scholar]
  95. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE. 95.  2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27:736–47 [Google Scholar]
  96. Jackson RJ, Hellen CU, Pestova TV. 96.  2012. Termination and post-termination events in eukaryotic translation. Adv. Protein Chem. Struct. Biol. 86:45–93 [Google Scholar]
  97. Jaillon O, Bouhouche K, Gout JF, Aury JM, Noel B. 97.  et al. 2008. Translational control of intron splicing in eukaryotes. Nature 451:359–62 [Google Scholar]
  98. Johansson MJ, He F, Spatrick P, Li C, Jacobson A. 98.  2007. Association of yeast Upf1p with direct substrates of the NMD pathway. PNAS 104:20872–77 [Google Scholar]
  99. Johansson MJ, Jacobson A. 99.  2010. Nonsense-mediated mRNA decay maintains translational fidelity by limiting magnesium uptake. Genes Dev. 24:1491–95 [Google Scholar]
  100. Johns L, Grimson A, Kuchma SL, Newman CL, Anderson P. 100.  2007. Caenorhabditis elegans SMG-2 selectively marks mRNAs containing premature translation termination codons. Mol. Cell. Biol. 27:5630–38 [Google Scholar]
  101. Jolly LA, Homan CC, Jacob R, Barry S, Gecz J. 101.  2013. The UPF3B gene, implicated in intellectual disability, autism, ADHD and childhood onset schizophrenia regulates neural progenitor cell behaviour and neuronal outgrowth. Hum. Mol. Genet. 22:4673–87 [Google Scholar]
  102. Jonas S, Weichenrieder O, Izaurralde E. 102.  2013. An unusual arrangement of two 14-3-3-like domains in the SMG5-SMG7 heterodimer is required for efficient nonsense-mediated mRNA decay. Genes Dev. 27:211–25 [Google Scholar]
  103. Kadlec J, Izaurralde E, Cusack S. 103.  2004. The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nat. Struct. Mol. Biol. 11:330–37 [Google Scholar]
  104. Kashima I, Yamashita A, Izumi N, Kataoka N, Morishita R. 104.  et al. 2006. 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. 20:355–67 [Google Scholar]
  105. Kaygun H, Marzluff WF. 105.  2005. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol. 12:794–800 [Google Scholar]
  106. Kebaara BW, Atkin AL. 106.  2009. Long 3′-UTRs target wild-type mRNAs for nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Nucleic Acids Res. 37:2771–78 [Google Scholar]
  107. Keeling KM, Xue X, Gunn G, Bedwell DM. 107.  2014. Therapeutics based on stop codon readthrough. Annu. Rev. Genomics Hum. Genet. 15:371–94 [Google Scholar]
  108. Kertesz S, Kerenyi Z, Merai Z, Bartos I, Palfy T. 108.  et al. 2006. Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Res. 34:6147–57 [Google Scholar]
  109. Kervestin S, Jacobson A. 109.  2012. NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol. 13:700–12 [Google Scholar]
  110. Kervestin S, Li C, Buckingham R, Jacobson A. 110.  2012. Testing the faux-UTR model for NMD: analysis of Upf1p and Pab1p competition for binding to eRF3/Sup35p. Biochimie 94:1560–71 [Google Scholar]
  111. Khajavi M, Inoue K, Lupski JR. 111.  2006. Nonsense-mediated mRNA decay modulates clinical outcome of genetic disease. Eur. J. Hum. Genet. 14:1074–81 [Google Scholar]
  112. Kim VN, Kataoka N, Dreyfuss G. 112.  2001. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293:1832–36 [Google Scholar]
  113. Kim YK, Furic L, Desgroseillers L, Maquat LE. 113.  2005. Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay. Cell 120:195–208 [Google Scholar]
  114. Koonin E. 114.  1992. A new group of putative RNA helicases. Trends Biochem. Sci. 17:495–97 [Google Scholar]
  115. Krawczak M, Ball EV, Cooper DN. 115.  1998. Neighboring-nucleotide effects on the rates of germ-line single-base-pair substitution in human genes. Am. J. Hum. Genet. 63:474–88 [Google Scholar]
  116. Kunz JB, Neu-Yilik G, Hentze MW, Kulozik AE, Gehring NH. 116.  2006. Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA 12:1015–22 [Google Scholar]
  117. Kurihara Y, Matsui A, Hanada K, Kawashima M, Ishida J. 117.  et al. 2009. Genome-wide suppression of aberrant mRNA-like noncoding RNAs by NMD in Arabidopsis. PNAS 106:2453–58 [Google Scholar]
  118. Kurosaki T, Li W, Hoque M, Popp MW, Ermolenko DN. 118.  et al. 2014. A post-translational regulatory switch on UPF1 controls targeted mRNA degradation. Genes Dev. 28:1900–16 [Google Scholar]
  119. Kurosaki T, Maquat LE. 119.  2013. Rules that govern UPF1 binding to mRNA 3′ UTRs. PNAS 110:3357–62 [Google Scholar]
  120. Kuschal C, DiGiovanna JJ, Khan SG, Gatti RA, Kraemer KH. 120.  2013. Repair of UV photolesions in xeroderma pigmentosum group C cells induced by translational readthrough of premature termination codons. PNAS 110:19483–88 [Google Scholar]
  121. Lai T, Cho H, Liu Z, Bowler MW, Piao S. 121.  et al. 2012. Structural basis of the PNRC2-mediated link between mRNA surveillance and decapping. Structure 20:2025–37 [Google Scholar]
  122. Lareau LF, Inada M, Green RE, Wengrod JC, Brenner SE. 122.  2007. Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446:926–29 [Google Scholar]
  123. Lasalde C, Rivera AV, Leon AJ, Gonzalez-Feliciano JA, Estrella LA. 123.  et al. 2014. Identification and functional analysis of novel phosphorylation sites in the RNA surveillance protein Upf1. Nucleic Acids Res. 42:1916–29 [Google Scholar]
  124. LeBlanc JJ, Beemon KL. 124.  2004. Unspliced Rous sarcoma virus genomic RNAs are translated and subjected to nonsense-mediated mRNA decay before packaging. J. Virol. 78:5139–46 [Google Scholar]
  125. Lee MH, Schedl T. 125.  2004. Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev. 18:1047–59 [Google Scholar]
  126. Leeds P, Peltz SW, Jacobson A, Culbertson MR. 126.  1991. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5:2303–14 [Google Scholar]
  127. Leeds P, Wood JM, Lee BS, Culbertson MR. 127.  1992. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2165–77 [Google Scholar]
  128. Le Hir H, Izaurralde E, Maquat LE, Moore MJ. 128.  2000. The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19:6860–69 [Google Scholar]
  129. Le Hir H, Seraphin B. 129.  2008. EJCs at the heart of translational control. Cell 133:213–16 [Google Scholar]
  130. Lejeune F, Li X, Maquat LE. 130.  2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12:675–87 [Google Scholar]
  131. Lelivelt MJ, Culbertson MR. 131.  1999. Yeast Upf proteins required for RNA surveillance affect global expression of the yeast transcriptome. Mol. Cell. Biol. 19:6710–19 [Google Scholar]
  132. Lentini L, Melfi R, Di Leonardo A, Spinello A, Barone G. 132.  et al. 2014. Toward a rationale for the PTC124 (ataluren) promoted readthrough of premature stop codons: a computational approach and GFP-reporter cell-based assay. Mol. Pharm. 11:653–64 [Google Scholar]
  133. Li M, Andersson-Lendahl M, Sejersen T, Arner A. 133.  2014. Muscle dysfunction and structural defects of dystrophin-null sapje mutant zebrafish larvae are rescued by ataluren treatment. FASEB J. 28:1593–99 [Google Scholar]
  134. Li S, Wilkinson MF. 134.  1998. Nonsense surveillance in lymphocytes?. Immunity 8:135–41 [Google Scholar]
  135. Liu C, Karam R, Zhou Y, Su F, Ji Y. 135.  et al. 2014. The UPF1 RNA surveillance gene is commonly mutated in pancreatic adenosquamous carcinoma. Nat. Med. 20:596–98 [Google Scholar]
  136. Loh B, Jonas S, Izaurralde E. 136.  2013. The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2. Genes Dev. 27:2125–38 [Google Scholar]
  137. Losson R, Lacroute F. 137.  1979. Interference of nonsense mutations with eukaryotic messenger RNA stability. PNAS 76:5134–37 [Google Scholar]
  138. Lou CH, Shao A, Shum EY, Espinoza JL, Huang L. 138.  et al. 2014. Posttranscriptional control of the stem cell and neurogenic programs by the nonsense-mediated RNA decay pathway. Cell Rep. 6:748–64 [Google Scholar]
  139. Lykke-Andersen J. 139.  2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22:8114–21 [Google Scholar]
  140. Lykke-Andersen J, Bennett EJ. 140.  2014. Protecting the proteome: eukaryotic cotranslational quality control pathways. J. Cell Biol. 204:467–76 [Google Scholar]
  141. Lykke-Andersen J, Shu MD, Steitz JA. 141.  2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103:1121–31 [Google Scholar]
  142. Lykke-Andersen J, Shu MD, Steitz JA. 142.  2001. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293:1836–39 [Google Scholar]
  143. Lykke-Andersen S, Chen Y, Ardal BR, Lilje B, Waage J. 143.  et al. 2014. Human nonsense-mediated RNA decay initiates widely by endonucleolysis and targets snoRNA host genes. Genes Dev. 28:2498–517 [Google Scholar]
  144. Ma XM, Yoon SO, Richardson CJ, Julich K, Blenis J. 144.  2008. SKAR links pre-mRNA splicing to mTOR/S6K1-mediated enhanced translation efficiency of spliced mRNAs. Cell 133:303–13 [Google Scholar]
  145. Maderazo AB, He F, Mangus DA, Jacobson A. 145.  2000. Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell. Biol. 20:4591–603 [Google Scholar]
  146. McGlincy NJ, Smith CW. 146.  2008. Alternative splicing resulting in nonsense-mediated mRNA decay: What is the meaning of nonsense?. Trends Biochem. Sci. 33:385–93 [Google Scholar]
  147. McIlwain DR, Pan Q, Reilly PT, Elia AJ, McCracken S. 147.  et al. 2010. Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. PNAS 107:12186–91 [Google Scholar]
  148. Medghalchi SM, Frischmeyer PA, Mendell JT, Kelly AG, Lawler AM, Dietz HC. 148.  2001. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10:99–105 [Google Scholar]
  149. Melero R, Buchwald G, Castano R, Raabe M, Gil D. 149.  et al. 2012. The cryo-EM structure of the UPF-EJC complex shows UPF1 poised toward the RNA 3′ end. Nat. Struct. Mol. Biol. 19:498–505, S1–2 [Google Scholar]
  150. Mendell JT, Sharifi NA, Meyers JL, Martinez-Murillo F, Dietz HC. 150.  2004. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36:1073–78 [Google Scholar]
  151. Metzstein MM, Krasnow MA. 151.  2006. Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLOS Genet. 2:e180 [Google Scholar]
  152. Miller JN, Pearce DA. 152.  2014. Nonsense-mediated decay in genetic disease: friend or foe?. Mutat. Res. 762:52–64 [Google Scholar]
  153. Min EE, Roy B, Amrani N, He F, Jacobson A. 153.  2013. Yeast Upf1 CH domain interacts with Rps26 of the 40S ribosomal subunit. RNA 19:1105–15 [Google Scholar]
  154. Mitchell P, Tollervey D. 154.  2003. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′→5′ degradation. Mol. Cell 11:1405–13 [Google Scholar]
  155. Moriarty PM, Reddy CC, Maquat LE. 155.  1998. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol. Cell. Biol. 18:2932–39 [Google Scholar]
  156. Mort M, Ivanov D, Cooper DN, Chuzhanova NA. 156.  2008. A meta-analysis of nonsense mutations causing human genetic disease. Hum. Mutat. 29:1037–47 [Google Scholar]
  157. Muhlrad D, Parker R. 157.  1994. Premature translational termination triggers mRNA decapping. Nature 370:578–81 [Google Scholar]
  158. Muhlrad D, Parker R. 158.  1999. Aberrant mRNAs with extended 3′ UTRs are substrates for rapid degradation by mRNA surveillance. RNA 5:1299–307 [Google Scholar]
  159. Nagy E, Maquat LE. 159.  1998. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23:198–99 [Google Scholar]
  160. Nguyen LS, Jolly L, Shoubridge C, Chan WK, Huang L. 160.  et al. 2012. Transcriptome profiling of UPF3B/NMD-deficient lymphoblastoid cells from patients with various forms of intellectual disability. Mol. Psychiatry 17:1103–15 [Google Scholar]
  161. Nguyen LS, Kim HG, Rosenfeld JA, Shen Y, Gusella JF. 161.  et al. 2013. Contribution of copy number variants involving nonsense-mediated mRNA decay pathway genes to neuro-developmental disorders. Hum. Mol. Genet. 22:1816–25 [Google Scholar]
  162. Ni J, Grate L, Donohue J, Preston C, Nobida N. 162.  et al. 2007. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev. 21:708–18 [Google Scholar]
  163. Nicholson P, Joncourt R, Muhlemann O. 163.  2012. Analysis of nonsense-mediated mRNA decay in mammalian cells. Curr. Protoc. Cell Biol. doi:10.1002/0471143030.cb2704s55
  164. Nicholson P, Josi C, Kurosawa H, Yamashita A, Muhlemann O. 164.  2014. A novel phosphorylation-independent interaction between SMG6 and UPF1 is essential for human NMD. Nucleic Acids Res. 42:9217–35 [Google Scholar]
  165. Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, Muhlemann O. 165.  2010. Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell Mol. Life Sci. 67:677–700 [Google Scholar]
  166. Nott A, Le Hir H, Moore MJ. 166.  2004. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev. 18:210–22 [Google Scholar]
  167. Nyiko T, Sonkoly B, Merai Z, Benkovics AH, Silhavy D. 167.  2009. Plant upstream ORFs can trigger nonsense-mediated mRNA decay in a size-dependent manner. Plant Mol. Biol. 71:367–78 [Google Scholar]
  168. Ohnishi T, Yamashita A, Kashima I, Schell T, Anders KR. 168.  et al. 2003. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell 12:1187–200 [Google Scholar]
  169. Okada-Katsuhata Y, Yamashita A, Kutsuzawa K, Izumi N, Hirahara F, Ohno S. 169.  2012. N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res. 40:1251–66 [Google Scholar]
  170. Page MF, Carr B, Anders KR, Grimson A, Anderson P. 170.  1999. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19:5943–51 [Google Scholar]
  171. Pal M, Ishigaki Y, Nagy E, Maquat LE. 171.  2001. Evidence that phosphorylation of human Upf1 protein varies with intracellular location and is mediated by a wortmannin-sensitive and rapamycin-sensitive PI 3-kinase-related kinase signaling pathway. RNA 7:5–15 [Google Scholar]
  172. Palacios IM, Gatfield D, St. Johnston D, Izaurralde E. 172.  2004. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427:753–57 [Google Scholar]
  173. Peixeiro I, Inacio A, Barbosa C, Silva AL, Liebhaber SA, Romao L. 173.  2012. Interaction of PABPC1 with the translation initiation complex is critical to the NMD resistance of AUG-proximal nonsense mutations. Nucleic Acids Res. 40:1160–73 [Google Scholar]
  174. Peltz SW, Brown AH, Jacobson A. 174.  1993. mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev. 7:1737–54 [Google Scholar]
  175. Peltz SW, Morsy M, Welch EM, Jacobson A. 175.  2013. Ataluren as an agent for therapeutic nonsense suppression. Annu. Rev. Med. 64:407–25 [Google Scholar]
  176. Perlick HA, Medghalchi SM, Spencer FA, Kendzior RJ Jr, Dietz HC. 176.  1996. Mammalian orthologues of a yeast regulator of nonsense transcript stability. PNAS 93:10928–32 [Google Scholar]
  177. Pisarev AV, Hellen CU, Pestova TV. 177.  2007. Recycling of eukaryotic posttermination ribosomal complexes. Cell 131:286–99 [Google Scholar]
  178. Pisarev AV, Skabkin MA, Pisareva VP, Skabkina OV, Rakotondrafara AM. 178.  et al. 2010. The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell 37:196–210 [Google Scholar]
  179. Ponting CP. 179.  2000. Novel eIF4G domain homologues linking mRNA translation with nonsense-mediated mRNA decay. Trends Biochem. Sci. 25:423–26 [Google Scholar]
  180. Pulak R, Anderson P. 180.  1993. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7:1885–97 [Google Scholar]
  181. Quek BL, Beemon K. 181.  2014. Retroviral strategy to stabilize viral RNA. Curr. Opin. Microbiol. 18:78–82 [Google Scholar]
  182. Rajavel KS, Neufeld EF. 182.  2001. Nonsense-mediated decay of human HEXA mRNA. Mol. Cell. Biol. 21:5512–19 [Google Scholar]
  183. Ramani AK, Nelson AC, Kapranov P, Bell I, Gingeras TR, Fraser AG. 183.  2009. High resolution transcriptome maps for wild-type and nonsense-mediated decay-defective Caenorhabditis elegans. Genome Biol. 10:R101 [Google Scholar]
  184. Rayson S, Arciga-Reyes L, Wootton L, De Torres Zabala M, Truman W. 184.  et al. 2012. A role for nonsense-mediated mRNA decay in plants: pathogen responses are induced in Arabidopsis thaliana NMD mutants. PLOS ONE 7:e31917 [Google Scholar]
  185. Rehwinkel J, Letunic I, Raes J, Bork P, Izaurralde E. 185.  2005. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11:1530–44 [Google Scholar]
  186. Rufener SC, Muhlemann O. 186.  2013. eIF4E-bound mRNPs are substrates for nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 20:710–17 [Google Scholar]
  187. Ruiz-Echevarria MJ, Peltz SW. 187.  1996. Utilizing the GCN4 leader region to investigate the role of the sequence determinants in nonsense-mediated mRNA decay. EMBO J. 15:2810–19 [Google Scholar]
  188. Ruiz-Echevarria MJ, Peltz SW. 188.  2000. The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101:741–51 [Google Scholar]
  189. Sakaki K, Yoshina S, Shen X, Han J, DeSantis MR. 189.  et al. 2012. RNA surveillance is required for endoplasmic reticulum homeostasis. PNAS 109:8079–84 [Google Scholar]
  190. Salas-Marco J, Bedwell DM. 190.  2004. GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination. Mol. Cell. Biol. 24:7769–78 [Google Scholar]
  191. Sauliere J, Murigneux V, Wang Z, Marquenet E, Barbosa I. 191.  et al. 2012. CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat. Struct. Mol. Biol. 19:1124–31 [Google Scholar]
  192. Schmidt SA, Foley PL, Jeong DH, Rymarquis LA, Doyle F. 192.  et al. 2014. Identification of SMG6 cleavage sites and a preferred RNA cleavage motif by global analysis of endogenous NMD targets in human cells. Nucleic Acids Res. 43:309–23 [Google Scholar]
  193. Schoenberg DR, Maquat LE. 193.  2012. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 13:246–59 [Google Scholar]
  194. Schweingruber C, Rufener SC, Zund D, Yamashita A, Muhlemann O. 194.  2013. Nonsense-mediated mRNA decay: mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim. Biophys. Acta 1829:612–23 [Google Scholar]
  195. Serin G, Gersappe A, Black JD, Aronoff R, Maquat LE. 195.  2001. Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell. Biol. 21:209–23 [Google Scholar]
  196. Seyedali A, Berry MJ. 196.  2014. Nonsense-mediated decay factors are involved in the regulation of selenoprotein mRNA levels during selenium deficiency. RNA 20:1248–56 [Google Scholar]
  197. Shen PS, Park J, Qin Y, Li X, Parsawar K. 197.  et al. 2015. Protein synthesis. Rqc2p and 60S ribosomal subunits mediate mRNA-independent elongation of nascent chains. Science 347:75–78 [Google Scholar]
  198. Shibuya T, Tange TO, Sonenberg N, Moore MJ. 198.  2004. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat. Struct. Mol. Biol. 11:346–51 [Google Scholar]
  199. Shigeoka T, Kato S, Kawaichi M, Ishida Y. 199.  2012. Evidence that the Upf1-related molecular motor scans the 3′-UTR to ensure mRNA integrity. Nucleic Acids Res. 40:6887–97 [Google Scholar]
  200. Shoemaker CJ, Green R. 200.  2011. Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. PNAS 108:E1392–98 [Google Scholar]
  201. Shoemaker CJ, Green R. 201.  2012. Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 19:594–601 [Google Scholar]
  202. Silva AL, Ribeiro P, Inacio A, Liebhaber SA, Romao L. 202.  2008. Proximity of the poly(A)-binding protein to a premature termination codon inhibits mammalian nonsense-mediated mRNA decay. RNA 14:563–76 [Google Scholar]
  203. Singh G, Kucukural A, Cenik C, Leszyk JD, Shaffer SA. 203.  et al. 2012. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151:750–64 [Google Scholar]
  204. Singh G, Rebbapragada I, Lykke-Andersen J. 204.  2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLOS Biol. 6:e111 [Google Scholar]
  205. Skabkin MA, Skabkina OV, Hellen CU, Pestova TV. 205.  2013. Reinitiation and other unconventional posttermination events during eukaryotic translation. Mol. Cell 51:249–64 [Google Scholar]
  206. Smith JE, Alvarez-Dominguez JR, Kline N, Huynh NJ, Geisler S. 206.  et al. 2014. Translation of small open reading frames within unannotated RNA transcripts in Saccharomyces cerevisiae. Cell Rep. 7:1858–66 [Google Scholar]
  207. Sonenberg N, Hinnebusch AG. 207.  2007. New modes of translational control in development, behavior, and disease. Mol. Cell 28:721–29 [Google Scholar]
  208. Song H, Mugnier P, Das AK, Webb HM, Evans DR. 208.  et al. 2000. The crystal structure of human eukaryotic release factor eRF1: mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100:311–21 [Google Scholar]
  209. Takahashi S, Araki Y, Sakuno T, Katada T. 209.  2003. Interaction between Ski7p and Upf1p is required for nonsense-mediated 3′-to-5′ mRNA decay in yeast. EMBO J. 22:3951–59 [Google Scholar]
  210. Tani H, Imamachi N, Salam KA, Mizutani R, Ijiri K. 210.  et al. 2012. Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol. 9:1370–79 [Google Scholar]
  211. Tani H, Torimura M, Akimitsu N. 211.  2013. The RNA degradation pathway regulates the function of GAS5 a non-coding RNA in mammalian cells. PLOS ONE 8:e55684 [Google Scholar]
  212. Tarpey PS, Raymond FL, Nguyen LS, Rodriguez J, Hackett A. 212.  et al. 2007. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat. Genet. 39:1127–33 [Google Scholar]
  213. Taylor MS, Lacava J, Mita P, Molloy KR, Huang CR. 213.  et al. 2013. Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 155:1034–48 [Google Scholar]
  214. Thermann R, Neu-Yilik G, Deters A, Frede U, Wehr K. 214.  et al. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17:3484–94 [Google Scholar]
  215. Thompson DM, Parker R. 215.  2007. Cytoplasmic decay of intergenic transcripts in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:92–101 [Google Scholar]
  216. Unterholzner L, Izaurralde E. 216.  2004. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16:587–96 [Google Scholar]
  217. Wang J, Gudikote JP, Olivas OR, Wilkinson MF. 217.  2002. Boundary-independent polar nonsense-mediated decay. EMBO Rep. 3:274–79 [Google Scholar]
  218. Wang W, Cajigas IJ, Peltz SW, Wilkinson MF, Gonzalez CI. 218.  2006. A role for Upf2p phosphorylation in Saccharomyces cerevisiae nonsense-mediated mRNA decay. Mol. Cell. Biol. 26:3390–4000 [Google Scholar]
  219. Wang W, Czaplinski K, Rao Y, Peltz SW. 219.  2001. The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J. 20:880–90 [Google Scholar]
  220. Weil JE, Beemon KL. 220.  2006. A 3′ UTR sequence stabilizes termination codons in the unspliced RNA of Rous sarcoma virus. RNA 12:102–10 [Google Scholar]
  221. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Monch K, Thoren LA. 221.  et al. 2008. NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev. 22:1381–96 [Google Scholar]
  222. Weischenfeldt J, Waage J, Tian G, Zhao J, Damgaard I. 222.  et al. 2012. Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns. Genome Biol. 13:R35 [Google Scholar]
  223. Welch EM, Barton ER, Zhuo J, Tomizawa Y, Friesen WJ. 223.  et al. 2007. PTC124 targets genetic disorders caused by nonsense mutations. Nature 447:87–91 [Google Scholar]
  224. Welch EM, Jacobson A. 224.  1999. An internal open reading frame triggers nonsense-mediated decay of the yeast SPT10 mRNA. EMBO J. 18:6134–45 [Google Scholar]
  225. Wen J, Brogna S. 225.  2010. Splicing-dependent NMD does not require the EJC in Schizosaccharomyces pombe. EMBO J. 29:1537–51 [Google Scholar]
  226. Weng Y, Czaplinski K, Peltz SW. 226.  1996. Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell. Biol. 16:5477–90 [Google Scholar]
  227. Weng Y, Czaplinski K, Peltz SW. 227.  1996. Identification and characterization of mutations in the UPF1 gene that affect nonsense suppression and the formation of the Upf protein complex but not mRNA turnover. Mol. Cell. Biol. 16:5491–506 [Google Scholar]
  228. Weng Y, Czaplinski K, Peltz SW. 228.  1998. ATP is a cofactor of the Upf1 protein that modulates its translation termination and RNA binding activities. RNA 4:205–14 [Google Scholar]
  229. Wilusz JE, JnBaptiste CK, Lu LY, Kuhn CD, Joshua-Tor L, Sharp PA. 229.  2012. A triple helix stabilizes the 3′ ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 26:2392–407 [Google Scholar]
  230. Withers JB, Beemon KL. 230.  2010. Structural features in the Rous sarcoma virus RNA stability element are necessary for sensing the correct termination codon. Retrovirology 7:65 [Google Scholar]
  231. Wittkopp N, Huntzinger E, Weiler C, Sauliere J, Schmidt S. 231.  et al. 2009. Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol. Cell. Biol. 29:3517–28 [Google Scholar]
  232. Xu X, Zhang L, Tong P, Xun G, Su W. 232.  et al. 2013. Exome sequencing identifies UPF3B as the causative gene for a Chinese non-syndrome mental retardation pedigree. Clin. Genet. 83:560–64 [Google Scholar]
  233. Yamashita A. 233.  2013. Role of SMG-1-mediated Upf1 phosphorylation in mammalian nonsense-mediated mRNA decay. Genes Cells 18:161–75 [Google Scholar]
  234. Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z. 234.  et al. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12:1054–63 [Google Scholar]
  235. Yamashita A, Izumi N, Kashima I, Ohnishi T, Saari B. 235.  et al. 2009. SMG-8 and SMG-9, two novel subunits of the SMG-1 complex, regulate remodeling of the mRNA surveillance complex during nonsense-mediated mRNA decay. Genes Dev. 23:1091–105 [Google Scholar]
  236. Yamashita A, Ohnishi T, Kashima I, Taya Y, Ohno S. 236.  2001. Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15:2215–28 [Google Scholar]
  237. Yepiskoposyan H, Aeschimann F, Nilsson D, Okoniewski M, Muhlemann O. 237.  2011. Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17:2108–18 [Google Scholar]
  238. Zaborske JM, Zeitler B, Culbertson MR. 238.  2013. Multiple transcripts from a 3′-UTR reporter vary in sensitivity to nonsense-mediated mRNA decay in Saccharomyces cerevisiae. PLOS ONE 8:e80981 [Google Scholar]
  239. Zhang J, Sun X, Qian Y, Maquat LE. 239.  1998. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 4:801–15 [Google Scholar]
  240. Zhang S, Welch EM, Hogan K, Brown AH, Peltz SW, Jacobson A. 240.  1997. Polysome-associated mRNAs are substrates for the nonsense-mediated mRNA decay pathway in Saccharomyces cerevisiae. RNA 3:234–44 [Google Scholar]
  241. Zhou Y, Jiang Q, Takahagi S, Shao C, Uitto J. 241.  2013. Premature termination codon read-through in the ABCC6 gene: potential treatment for pseudoxanthoma elasticum. J. Investig. Dermatol. 133:2672–77 [Google Scholar]
  242. Zünd D, Gruber AR, Zavolan M, Mühlemann O. 242.  2013. Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3′ UTRs. Nat. Struct. Mol. Biol. 20:936–43 [Google Scholar]
  243. Zünd D, Mühlemann O. 243.  2013. Recent transcriptome-wide mapping of UPF1 binding sites reveals evidence for its recruitment to mRNA before translation. Translation 1:e26977 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-054639
Loading
/content/journals/10.1146/annurev-genet-112414-054639
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error