Mechanism and regulation of the nonsense-mediated decay pathway

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1483-1495

  Hug, Nele ^a   Longman, Dasa ^a   Cáceres, Javier F ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; AZACITIDINE; CURCUMIN; CYTOKINE; MESSENGER RNA; NATURAL PRODUCT; PATEAMINE A; RNA HELICASE; UNCLASSIFIED DRUG; STOP CODON;

3' UNTRANSLATED REGION; CELL STRESS; CODON; CYTOKINE RESPONSE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXON; EXON JUNCTION COMPLEX; GENE EXPRESSION; GENE TARGETING; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PREMATURE TERMINATION CODON; PRIORITY JOURNAL; REVIEW; RNA DEGRADATION; RNA INTERFERENCE; RNA SPLICING; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UPREGULATION; VIRUS REPLICATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; RNA STABILITY; STOP CODON;

CODON, NONSENSE; GENE EXPRESSION REGULATION; HUMANS; METABOLIC NETWORKS AND PATHWAYS; NONSENSE MEDIATED MRNA DECAY; RNA HELICASES; RNA STABILITY; RNA, MESSENGER;

EID: 84960471570     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw010     Document Type: Review

References (165)

1. Isken, O. and Maquat, L.E. (2007) Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev., 21, 1833-1856.
2. Kervestin, S. and Jacobson, A. (2012) NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol., 13, 700-712.
3. Schweingruber, C., Rufener, S.C., Zünd, D., Yamashita, A. and Mühlemann, O. (2013) Nonsense-mediated mRNA decay - mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim. Biophys. Acta, 1829, 612-623.
4. Bhuvanagiri, M., Schlitter, A.M., Hentze, M.W. and Kulozik, A.E. (2010) NMD: RNA biology meets human genetic medicine. Biochem. J., 430, 365-377.
5. Miller, J.N. and Pearce, D.A. (2014) Nonsense-mediated decay in genetic disease: friend or foe? Mutat. Res. Rev. Mutat. Res., 762, 52-64.
6. Alonso, C.R. (2005) Nonsense-mediated RNA decay: a molecular system micromanaging individual gene activities and suppressing genomic noise. Bioessays, 27, 463-466.
7. Chang, Y.-F., Imam, J.S. and Wilkinson, M.F. (2007) The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem., 76, 51-74.
8. Palacios, I.M. (2013) Nonsense-mediated mRNA decay: from mechanistic insights to impacts on human health. Brief. Funct. Genomics, 12, 25-36.
9. Huang, L., Lou, C.-H., Chan, W., Shum, E.Y., Shao, A., Stone, E., Karam, R., Song, H.-W. and Wilkinson, M.F. (2011) RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol. Cell, 43, 950-961.
10. Yepiskoposyan, H., Aeschimann, F., Nilsson, D., Okoniewski, M. and Mühlemann, O. (2011) Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA, 17, 2108-2118.
11. Longman, D., Hug, N., Keith, M., Anastasaki, C., Patton, E.E., Grimes, G. and Cá;ceres, J.F. (2013) DHX34 and NBAS form part of an autoregulatory NMD circuit that regulates endogenous RNA targets in human cells, zebrafish and Caenorhabditis elegans. Nucleic Acids Res., 41, 8319-8331.
12. Degtiar, E., Fridman, A., Gottlieb, D., Vexler, K., Berezin, I., Farhi, R., Golani, L. and Shaul, O. (2015) The feedback control of UPF3 is crucial for RNA surveillance in plants. Nucleic Acids Res., 43, 4219-4235.
13. Nguyen, L.S., Wilkinson, M.F. and Gecz, J. (2014) Nonsense-mediated mRNA decay: inter-individual variability and human disease. Neurosci. Biobehav. Rev., 46 Pt 2, 175-186.
14. Hurt, J.A., Robertson, A.D. and Burge, C.B. (2013) Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res., 23, 1636-1650.
15. Kurihara, Y., Matsui, A., Hanada, K., Kawashima, M., Ishida, J., Morosawa, T., Tanaka, M., Kaminuma, E., Mochizuki, Y., Matsushima, A. et al. (2009) Genome-wide suppression of aberrant mRNA-like noncoding RNAs by NMD in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A., 106, 2453-2458.
16. Smith, J.E., Alvarez-Dominguez, J.R., Kline, N., Huynh, N.J., Geisler, S., Hu, W., Coller, J. and Baker, K.E. (2014) Translation of small open reading frames within unannotated RNA transcripts in Saccharomyces cerevisiae. Cell Rep., 7, 1858-1866.
17. Smith, J.E. and Baker, K.E. (2015) Nonsense-mediated RNA decay-a switch and dial for regulating gene expression. Bioessays, 37, 612-623.
18. Nagy, E. and Maquat, L.E. (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci., 23, 198-199.
19. Thermann, R., Neu-Yilik, G., Deters, A., Frede, U., Wehr, K., Hagemeier, C., Hentze, M.W. and Kulozik, A.E. (1998) Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J., 17, 3484-3494.
20. Zhang, J., Sun, X., Qian, Y., LaDuca, J.P. and Maquat, L.E. (1998) At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol., 18, 5272-5283.
21. Zhang, J., Sun, X., Qian, Y. and Maquat, L.E. (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, 801-815.
22. Le Hir, H., Gatfield, D., Izaurralde, E. and Moore, M.J. (2001) The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J., 20, 4987-4997.
23. Lykke-Andersen, J., Shu, M.D. and Steitz, J.A. (2001) Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science, 293, 1836-1839.
24. Gehring, N.H., Lamprinaki, S., Kulozik, A.E. and Hentze, M.W. (2009) Disassembly of exon junction complexes by PYM. Cell, 137, 536-548.
25. Le Hir, H. and Séraphin, B. (2008) EJCs at the heart of translational control. Cell, 133, 213-216.
26. Bono, F. and Gehring, N.H. (2011) Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol., 8, 24-29.
27. Singh, G., Kucukural, A., Cenik, C., Leszyk, J.D., Shaffer, S.A., Weng, Z. and Moore, M.J. (2012) The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell, 151, 750-764.
28. Saulière, J., Murigneux, V., Wang, Z., Marquenet, E., Barbosa, I., Le Tonquèze, O., Audic, Y., Paillard, L., Roest Crollius, H. and Le Hir, H. (2012) CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat. Struct. Mol. Biol., 19, 1124-1131.
29. Le Hir, H., Saulière, J. and Wang, Z. (2016) The exon junction complex as a node of post-transcriptional networks. Nat. Rev. Mol. Cell Biol., 17, 41-54.
30. Amrani, N., Ganesan, R., Kervestin, S., Mangus, D.A., Ghosh, S. and Jacobson, A. (2004) A faux 3'-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature, 432, 112-118.
31. Amrani, N., Sachs, M.S. and Jacobson, A. (2006) Early nonsense: mRNA decay solves a translational problem. Nat. Rev. Mol. Cell Biol., 7, 415-425.
32. Wen, J. and Brogna, S. (2010) Splicing-dependent NMD does not require the EJC in Schizosaccharomyces pombe. EMBO J., 29, 1537-1551.
33. Gatfield, D., Unterholzner, L., Ciccarelli, F.D., Bork, P. and Izaurralde, E. (2003) Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J., 22, 3960-3970.
34. Longman, D., Plasterk, R.H.A., Johnstone, I.L. and Cá;ceres, J.F. (2007) Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev., 21, 1075-1085.
35. Hodgkin, J., Papp, A., Pulak, R., Ambros, V. and Anderson, P. (1989) A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics, 123, 301-313.
36. Pulak, R. and Anderson, P. (1993) mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev., 7, 1885-1897.
37. Leeds, P., Peltz, S.W., Jacobson, A. and Culbertson, M.R. (1991) The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev., 5, 2303-2314.
38. Leeds, P., Wood, J.M., Lee, B.S. and Culbertson, M.R. (1992) Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol., 12, 2165-2177.
39. Mühlemann, O., Eberle, A.B., Stalder, L. and Zamudio Orozco, R. (2008) Recognition and elimination of nonsense mRNA. Biochim. Biophys. Acta, 1779, 538-549.
40. Cordin, O., Banroques, J., Tanner, N.K. and Linder, P. (2006) The DEAD-box protein family of RNA helicases. Gene, 367, 17-37.
41. Rajkowitsch, L., Chen, D., Stampfl, S., Semrad, K., Waldsich, C., Mayer, O., Jantsch, M.F., Konrat, R., Bläsi, U. and Schroeder, R. (2007) RNA chaperones, RNA annealers and RNA helicases. RNA Biol., 4, 118-130.
42. Denning, G., Jamieson, L., Maquat, L.E., Thompson, E.A. and Fields, A.P. (2001) Cloning of a novel phosphatidylinositol kinase-related kinase: characterization of the human SMG-1 RNA surveillance protein. J. Biol. Chem., 276, 22709-22714.
43. Grimson, A., O'Connor, S., Newman, C.L. and Anderson, P. (2004) SMG-1 is a phosphatidylinositol kinase-related protein kinase required for nonsense-mediated mRNA Decay in Caenorhabditis elegans. Mol. Cell. Biol., 24, 7483-7490.
44. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y. and Ohno, S. (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, 2215-2228.
45. Yamashita, A., Izumi, N., Kashima, I., Ohnishi, T., Saari, B., Katsuhata, Y., Muramatsu, R., Morita, T., Iwamatsu, A., Hachiya, T. 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, 1091-1105.
46. Ferná;ndez, I.S., Yamashita, A., Arias-Palomo, E., Bamba, Y., Bartolomé, R.A., Canales, M.A., Teixidó;, J., Ohno, S. and Llorca, O. (2011) Characterization of SMG-9, an essential component of the nonsense-mediated mRNA decay SMG1C complex. Nucleic Acids Res., 39, 347-358.
47. Arias-Palomo, E., Yamashita, A., Ferná;ndez, I.S., Nú;ñez-Ramírez, R., Bamba, Y., Izumi, N., Ohno, S. and Llorca, O. (2011) The nonsense-mediated mRNA decay SMG-1 kinase is regulated by large-scale conformational changes controlled by SMG-8. Genes Dev., 25, 153-164.
48. Kashima, I., Yamashita, A., Izumi, N., Kataoka, N., Morishita, R., Hoshino, S., Ohno, M., Dreyfuss, G. and Ohno, S. (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, 355-367.
49. Melero, R., Uchiyama, A., Casta ño, R., Kataoka, N., Kurosawa, H., Ohno, S., Yamashita, A. and Llorca, O. (2014) Structures of SMG1-UPFs complexes: SMG1 contributes to regulate UPF2-dependent activation of UPF1 in NMD. Structure, 22, 1105-1119.
50. Deniaud, A., Karuppasamy, M., Bock, T., Masiulis, S., Huard, K., Garzoni, F., Kerschgens, K., Hentze, M.W., Kulozik, A.E., Beck, M. et al. (2015) A network of SMG-8, SMG-9 and SMG-1 C-terminal insertion domain regulates UPF1 substrate recruitment and phosphorylation. Nucleic Acids Res., 43, 7600-7611.
51. Chakrabarti, S., Jayachandran, U., Bonneau, F., Fiorini, F., Basquin, C., Domcke, S., Le Hir, H. and Conti, E. (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell, 41, 693-703.
52. Chamieh, H., Ballut, L., Bonneau, F. and Le Hir, H. (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.
53. Fiorini, F., Boudvillain, M. and Le Hir, H. (2013) Tight intramolecular regulation of the human Upf1 helicase by its N- and C-terminal domains. Nucleic Acids Res., 41, 2404-2415.
54. Clerici, M., Mourão, A., Gutsche, I., Gehring, N.H., Hentze, M.W., Kulozik, A., Kadlec, J., Sattler, M. and Cusack, S. (2009) Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J., 28, 2293-22306.
55. Franks, T.M., Singh, G. and Lykke-Andersen, J. (2010) Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense- mediated mRNA decay. Cell, 143, 938-950.
56. Fiorini, F., Bagchi, D., Le Hir, H. and Croquette, V. (2015) Human Upf1 is a highly processive RNA helicase and translocase with RNP remodelling activities. Nat. Commun., 6, 7581.
57. Melero, R., Buchwald, G., Castaño, R., Raabe, M., Gil, D., Lá;zaro, M., Urlaub, H., Conti, E. and Llorca, O. (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.
58. Schoenberg, D.R. and Maquat, L.E. (2012) Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet., 13, 246-259.
59. Eberle, A.B., Lykke-Andersen, S., Mühlemann, O. and Jensen, T.H. (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol., 16, 49-55.
60. Okada-Katsuhata, Y., Yamashita, A., Kutsuzawa, K., Izumi, N., Hirahara, F. and Ohno, S. (2012) N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res., 40, 1251-1266.
61. Chakrabarti, S., Bonneau, F., Schüssler, S., Eppinger, E. and Conti, E. (2014) Phospho-dependent and phospho-independent interactions of the helicase UPF1 with the NMD factors SMG5-SMG7 and SMG6. Nucleic Acids Res., 42, 9447-9460.
62. Nicholson, P., Josi, C., Kurosawa, H., Yamashita, A. and Mühlemann, O. (2014) A novel phosphorylation-independent interaction between SMG6 and UPF1 is essential for human NMD. Nucleic Acids Res., 42, 9217-9235.
63. Huntzinger, E., Kashima, I., Fauser, M., Saulière, J. and Izaurralde, E. (2008) SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA, 14, 2609-2617.
64. Schmidt, S.A., Foley, P.L., Jeong, D.-H., Rymarquis, L.A., Doyle, F., Tenenbaum, S.A., Belasco, J.G. and Green, P.J. (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, 309-323.
65. Lykke-Andersen, S., Chen, Y., Ardal, B.R., Lilje, B., Waage, J., Sandelin, A. and Jensen, T.H. (2014) Human nonsense-mediated RNA decay initiates widely by endonucleolysis and targets snoRNA host genes. Genes Dev., 28, 2498-2517.
66. Lykke-Andersen, J. and Bennett, E.J. (2014) Protecting the proteome: eukaryotic cotranslational quality control pathways. J. Cell Biol., 204, 467-476.
67. Loh, B., Jonas, S. and Izaurralde, E. (2013) The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2. Genes Dev., 27, 2125-2138.
68. Unterholzner, L. and Izaurralde, E. (2004) SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell, 16, 587-596.
69. Gehring, N.H., Kunz, J.B., Neu-Yilik, G., Breit, S., Viegas, M.H., Hentze, M.W. and Kulozik, A.E. (2005) Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell, 20, 65-75.
70. Chan, W.-K., Huang, L., Gudikote, J.P., Chang, Y.-F., Imam, J.S., MacLean, J.A. and Wilkinson, M.F. (2007) An alternative branch of the nonsense-mediated decay pathway. EMBO J., 26, 1820-1830.
71. Ivanov, P. V, Gehring, N.H., Kunz, J.B., Hentze, M.W. and Kulozik, A.E. (2008) Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J., 27, 736-747.
72. Andersen, C.B.F., Ballut, L., Johansen, J.S., Chamieh, H., Nielsen, K.H., Oliveira, C.L.P., Pedersen, J.S., Séraphin, B., Le Hir, H. and Andersen, G.R. (2006) Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science, 313, 1968-1972.
73. Bono, F., Ebert, J., Lorentzen, E. and Conti, E. (2006) The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell, 126, 713-725.
74. Ballut, L., Marchadier, B., Baguet, A., Tomasetto, C., Séraphin, B. and Le Hir, H. (2005) The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol., 12, 861-869.
75. Noble, C.G. and Song, H. (2007) MLN51 stimulates the RNA-helicase activity of eIF4AIII. PLoS One, 2, e303.
76. Le Hir, H., Moore, M.J. and Maquat, L.E. (2000) Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev., 14, 1098-1108.
77. Gehring, N.H., Neu-Yilik, G., Schell, T., Hentze, M.W. and Kulozik, A.E. (2003) Y14 and hUpf3b form an NMD-activating complex. Mol. Cell, 11, 939-949.
78. Geißler, V., Altmeyer, S., Stein, B., Uhlmann-Schiffler, H. and Stahl, H. (2013) The RNA helicase Ddx5/p68 binds to hUpf3 and enhances NMD of Ddx17/p72 and Smg5 mRNA. Nucleic Acids Res., 41, 7875-7888.
79. Izumi, N., Yamashita, A., Iwamatsu, A., Kurata, R., Nakamura, H., Saari, B., Hirano, H., Anderson, P. and Ohno, S. (2010) AAA+ proteins RUVBL1 and RUVBL2 coordinate PIKK activity and function in nonsense-mediated mRNA decay. Sci. Signaling, 3, ra27.
80. Hug, N. and Cá;ceres, J.F. (2014) The RNA helicase DHX34 activates NMD by promoting a transition from the surveillance to the decay-inducing complex. Cell Rep., 8, 1845-1856.
81. Schwer, B. (2001) A new twist on RNA helicases: DExH/D box proteins as RNPases. Nat. Struct. Biol., 8, 113-116.
82. Jankowsky, E. and Bowers, H. (2006) Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res., 34, 4181-4188.
83. Hogg, J.R. and Goff, S.P. (2010) Upf1 senses 3' UTR length to potentiate mRNA decay. Cell, 143, 379-389.
84. Kurosaki, T. and Maquat, L.E. (2013) Rules that govern UPF1 binding to mRNA 3' UTRs. Proc. Natl. Acad. Sci. U.S.A., 110, 3357-3362.
85. Sievers, C., Schlumpf, T., Sawarkar, R., Comoglio, F. and Paro, R. (2012) Mixture models and wavelet transforms reveal high confidence RNA-protein interaction sites in MOV10 PAR-CLIP data. Nucleic Acids Res., 40, e160.
86. Gregersen, L.H., Schueler, M., Munschauer, M., Mastrobuoni, G., Chen, W., Kempa, S., Dieterich, C. and Landthaler, M. (2014) MOV10 is a 5' to 3' RNA helicase contributing to UPF1 mRNA target degradation by translocation along 3' UTRs. Mol. Cell, 54, 573-585.
87. Bühler, M., Steiner, S., Mohn, F., Paillusson, A. and Mühlemann, O. (2006) EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3' UTR length. Nat. Struct. Mol. Biol., 13, 462-464.
88. He, F. and Jacobson, A. (2015) Nonsense-mediated mRNA decay: degradation of defective transcripts is only part of the story. Annu. Rev. Genet., 49, 339-366.
89. Zünd, D., Gruber, A.R., Zavolan, M. and Mühlemann, O. (2013) Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3' UTRs. Nat. Struct. Mol. Biol., 20, 936-943.
90. Tani, H., Imamachi, N., Salam, K.A., Mizutani, R., Ijiri, K., Irie, T., Yada, T., Suzuki, Y. and Akimitsu, N. (2014) Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol., 6, 1370-1379.
91. Kurosaki, T., Li, W., Hoque, M., Popp, M.W.-L., Ermolenko, D.N., Tian, B. and Maquat, L.E. (2014) A post-translational regulatory switch on UPF1 controls targeted mRNA degradation. Genes Dev., 28, 1900-1916.
92. Lee, S.R., Pratt, G.A., Martinez, F.J., Yeo, G.W. and Lykke-Andersen, J. (2015) Target discrimination in nonsense-mediated mRNA decay requires Upf1 ATPase activity. Mol. Cell, 59, 413-425.
93. Fatscher, T., Boehm, V. and Gehring, N.H. (2015) Mechanism, factors, and physiological role of nonsense-mediated mRNA decay. Cell. Mol. Life Sci., 72, 4523-4544.
94. Eberle, A.B., Stalder, L., Mathys, H., Orozco, R.Z. and Mühlemann, O. (2008) Posttranscriptional gene regulation by spatial rearrangement of the 3' untranslated region. PLoS Biol., 6, e92.
95. Singh, G., Rebbapragada, I. and Lykke-Andersen, J. (2008) A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol., 6, e111.
96. Mendell, J.T., Sharifi, N.A., Meyers, J.L., Martinez-Murillo, F. and Dietz, H.C. (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet., 36, 1073-1078.
97. Wittmann, J., Hol, E.M. and Jäck, H.-M. (2006) hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol. Cell. Biol., 26, 1272-1287.
98. Weischenfeldt, J., Damgaard, I., Bryder, D., Theilgaard-Mönch, K., Thoren, L. a, Nielsen, F.C., Jacobsen, S.E.W., Nerlov, C. and Porse, B.T. (2008) NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev., 22, 1381-1396.
99. Nicholson, P., Yepiskoposyan, H., Metze, S., Zamudio Orozco, R., Kleinschmidt, N. and Mühlemann, O. (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.
100. Zarkower, D., De Bono, M., Aronoff, R. and Hodgkin, J. (1994) Regulatory rearrangements and smg-sensitive alleles of the C. elegans sex-determining gene tra-1. Dev. Genet., 15, 240-250.
101. Cho, H., Kim, K.M. and Kim, Y.K. (2009) Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell, 33, 75-86.
102. Lai, T., Cho, H., Liu, Z., Bowler, M.W., Piao, S., Parker, R., Kim, Y.K. and Song, H. (2012) Structural basis of the PNRC2-mediated link between mrna surveillance and decapping. Structure, 20, 2025-2037.
103. Flury, V., Restuccia, U., Bachi, A. and Mühlemann, O. (2014) Characterization of phosphorylation- and RNA-dependent UPF1 interactors by quantitative proteomics. J. Proteome Res., 13, 3038-3053.
104. Fairman-Williams, M.E., Guenther, U.-P. and Jankowsky, E. (2010) SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol., 20, 313-324.
105. Woychik, N.A., Liao, S.M., Kolodziej, P.A. and Young, R.A. (1990) Subunits shared by eukaryotic nuclear RNA polymerases. Genes Dev., 4, 313-323.
106. Anastasaki, C., Longman, D., Capper, A., Patton, E.E. and Cá;ceres, J.F. (2011) Dhx34 and Nbas function in the NMD pathway and are required for embryonic development in zebrafish. Nucleic Acids Res., 39, 3686-3694.
107. Wimmer, K., Zhu, X.X., Lamb, B.J., Kuick, R., Ambros, P.F., Kovar, H., Thoraval, D., Motyka, S., Alberts, J.R. and Hanash, S.M. (1999) Co-amplification of a novel gene, NAG, with the N-myc gene in neuroblastoma. Oncogene, 18, 233-238.
108. Scott, D.K., Board, J.R., Lu, X., Pearson, A.D., Kenyon, R.M. and Lunec, J. (2003) The neuroblastoma amplified gene, NAG: genomic structure and characterisation of the 7.3 kb transcript predominantly expressed in neuroblastoma. Gene, 307, 1-11.
109. Aoki, T., Ichimura, S., Itoh, A., Kuramoto, M., Shinkawa, T., Isobe, T. and Tagaya, M. (2009) Identification of the neuroblastoma-amplified gene product as a component of the syntaxin 18 complex implicated in Golgi-to-endoplasmic reticulum retrograde transport. Mol. Biol. Cell, 20, 2639-2649.
110. Maksimova, N., Hara, K., Nikolaeva, I., Chun-Feng, T., Usui, T., Takagi, M., Nishihira, Y., Miyashita, A., Fujiwara, H., Oyama, T. et al. (2010) Neuroblastoma amplified sequence gene is associated with a novel short stature syndrome characterised by optic nerve atrophy and Pelger-Huët anomaly. J. Med. Genet., 47, 538-548.
111. Garcia Segarra, N., Ballhausen, D., Crawford, H., Perreau, M., Campos-Xavier, B., van Spaendonck-Zwarts, K., Vermeer, C., Russo, M., Zambelli, P.-Y., Stevenson, B. et al. (2015) NBAS mutations cause a multisystem disorder involving bone, connective tissue, liver, immune system, and retina. Am. J. Med. Genet. A, 167A, 2902-2912.
112. Haack, T.B., Staufner, C., Köpke, M.G., Straub, B.K., Kölker, S., Thiel, C., Freisinger, P., Baric, I., McKiernan, P.J., Dikow, N. et al. (2015) Biallelic mutations in NBAS cause recurrent acute liver failure with onset in infancy. Am. J. Hum. Genet., 97, 163-169.
113. Kamath, R.S., Fraser, A.G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature, 421, 231-237.
114. Rual, J.-F., Ceron, J., Koreth, J., Hao, T., Nicot, A.-S., Hirozane-Kishikawa, T., Vandenhaute, J., Orkin, S.H., Hill, D.E., van den Heuvel, S. et al. (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res., 14, 2162-2168.
115. Casadio, A., Longman, D., Hug, N., Delavaine, L., Vallejos Baier, R., Alonso, C.R. and Cá;ceres, J.F. (2015) Identification and characterization of novel factors that act in the nonsense-mediated mRNA decay pathway in nematodes, flies and mammals. EMBO Rep., 16, 71-78.
116. Saveanu, C., Bienvenu, D., Namane, A., Gleizes, P.E., Gas, N., Jacquier, A. and Fromont-Racine, M. (2001) Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J., 20, 6475-6484.
117. Shaywitz, D.A., Orci, L., Ravazzola, M., Swaroop, A. and Kaiser, C.A. (1995) Human SEC13Rp functions in yeast and is located on transport vesicles budding from the endoplasmic reticulum. J. Cell Biol., 128, 769-777.
118. Huang, L. and Wilkinson, M.F. (2012) Regulation of nonsense-mediated mRNA decay. Wiley Interdiscip. Rev., 3, 807-828.
119. Lykke-Andersen, S. and Jensen, T.H. (2015) Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat. Rev. Mol. Cell Biol., 16, 665-677.
120. Viegas, M.H., Gehring, N.H., Breit, S., Hentze, M.W. and Kulozik, A.E. (2007) The abundance of RNPS1, a protein component of the exon junction complex, can determine the variability in efficiency of the Nonsense Mediated Decay pathway. Nucleic Acids Res., 35, 4542-4551.
121. Medghalchi, S.M., Frischmeyer, P.A., Mendell, J.T., Kelly, A.G., Lawler, A.M. and Dietz, H.C. (2001) Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet., 10, 99-105.
122. Li, T., Shi, Y., Wang, P., Guachalla, L.M., Sun, B., Joerss, T., Chen, Y.-S., Groth, M., Krueger, A., Platzer, M. et al., (2015) Smg6/Est1 licenses embryonic stem cell differentiation via nonsense-mediated mRNA decay. EMBO J., 34, 1630-1647.
123. McIlwain, D.R., Pan, Q., Reilly, P.T., Elia, A.J., McCracken, S., Wakeham, A.C., Itie-Youten, A., Blencowe, B.J. and Mak, T.W. (2010) Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc. Natl. Acad. Sci. U.S.A., 107, 12186-12191.
124. Varsally, W. and Brogna, S. (2012) UPF1 involvement in nuclear functions. Biochem. Soc. Trans., 40, 778-783.
125. Azzalin, C.M. and Lingner, J. (2006) The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol., 16, 433-439.
126. Kim, Y.K., Furic, L., Desgroseillers, L. and Maquat, L.E. (2005) Mammalian Staufen1 recruits Upf1 to specific mRNA 3' UTRs so as to elicit mRNA decay. Cell, 120, 195-208.
127. Park, E. and Maquat, L.E. (2013) Staufen-mediated mRNA decay. Wiley Interdiscip. Rev., 4, 423-435.
128. Kaygun, H. and Marzluff, W.F. (2005) Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol., 12, 794-800.
129. Brumbaugh, K.M., Otterness, D.M., Geisen, C., Oliveira, V., Brognard, J., Li, X., Lejeune, F., Tibbetts, R.S., Maquat, L.E. and Abraham, R.T. (2004) The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol. Cell, 14, 585-598.
130. Metzstein, M.M. and Krasnow, M.A. (2006) Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet., 2, e180.
131. Avery, P., Vicente-Crespo, M., Francis, D., Nashchekina, O., Alonso, C.R. and Palacios, I.M. (2011) Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf3-independent manner. RNA, 17, 624-638.
132. Gardner, L.B. (2010) Nonsense-mediated RNA decay regulation by cellular stress: implications for tumorigenesis. Mol. Cancer Res., 8, 295-308.
133. Karam, R., Wengrod, J., Gardner, L.B. and Wilkinson, M.F. (2013) Regulation of nonsense-mediated mRNA decay: implications for physiology and disease. Biochim. Biophys. Acta, 1829, 624-633.
134. Wang, D., Zavadil, J., Martin, L., Parisi, F., Friedman, E., Levy, D., Harding, H., Ron, D. and Gardner, L.B. (2011) Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol. Cell. Biol., 31, 3670-3680.
135. Gardner, L.B. (2008) Hypoxic inhibition of nonsense-mediated RNA decay regulates gene expression and the integrated stress response. Mol. Cell. Biol., 28, 3729-3741.
136. Karam, R., Lou, C.-H., Kroeger, H., Huang, L., Lin, J.H. and Wilkinson, M.F. (2015) The unfolded protein response is shaped by the NMD pathway. EMBO Rep., 16, 599-609.
137. Sakaki, K., Yoshina, S., Shen, X., Han, J., DeSantis, M.R., Xiong, M., Mitani, S. and Kaufman, R.J. (2012) RNA surveillance is required for endoplasmic reticulum homeostasis. Proc. Natl. Acad. Sci. U.S.A., 109, 8079-8084.
138. Oren, Y.S., McClure, M.L., Rowe, S.M., Sorscher, E.J., Bester, A.C., Manor, M., Kerem, E., Rivlin, J., Zahdeh, F., Mann, M. et al. (2014) The unfolded protein response affects readthrough of premature termination codons. EMBO Mol. Med., 6, 685-701.
139. Wengrod, J., Martin, L., Wang, D., Frischmeyer-Guerrerio, P., Dietz, H.C. and Gardner, L.B. (2013) Inhibition of nonsense-mediated RNA decay activates autophagy. Mol. Cell. Biol., 33, 2128-2135.
140. Mino, T., Murakawa, Y., Fukao, A., Vandenbon, A., Wessels, H.-H., Ori, D., Uehata, T., Tartey, S., Akira, S., Suzuki, Y. et al. (2015) Regnase-1 and Roquin regulate a common element in inflammatory mRNAs by spatiotemporally distinct mechanisms. Cell, 161, 1058-1073.
141. Belew, A.T., Meskauskas, A., Musalgaonkar, S., Advani, V.M., Sulima, S.O., Kasprzak, W.K., Shapiro, B.A. and Dinman, J.D. (2014) Ribosomal frameshifting in the CCR5 mRNA is regulated by miRNAs and the NMD pathway. Nature, 512, 265-269.
142. Pastor, F., Kolonias, D., Giangrande, P.H. and Gilboa, E. (2010) Induction of tumour immunity by targeted inhibition of nonsense-mediated mRNA decay. Nature, 465, 227-230.
143. Nickless, A., Jackson, E., Marasa, J., Nugent, P., Mercer, R.W., Piwnica-Worms, D. and You, Z. (2014) Intracellular calcium regulates nonsense-mediated mRNA decay. Nat. Med., 20, 961-966.
144. Riehs-Kearnan, N., Gloggnitzer, J., Dekrout, B., Jonak, C. and Riha, K. (2012) Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response. Nucleic Acids Res., 40, 5615-5624.
145. Gloggnitzer, J., Akimcheva, S., Srinivasan, A., Kusenda, B., Riehs, N., Stampfl, H., Bautor, J., Dekrout, B., Jonak, C., Jiménez-Gó;mez, J.M. et al. (2014) Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe, 16, 376-390.
146. Rigby, R.E. and Rehwinkel, J. (2015) RNA degradation in antiviral immunity and autoimmunity. Trends Immunol., 36, 179-188.
147. Balistreri, G., Horvath, P., Schweingruber, C., Zünd, D., McInerney, G., Merits, A., Mühlemann, O., Azzalin, C. and Helenius, A. (2014) The host nonsense-mediated mRNA decay pathway restricts mammalian RNA virus replication. Cell Host Microbe, 16, 403-411.
148. Weil, J.E. and Beemon, K.L. (2006) A 3' UTR sequence stabilizes termination codons in the unspliced RNA of Rous sarcoma virus. RNA, 12, 102-110.
149. Quek, B.L. and Beemon, K. (2014) Retroviral strategy to stabilize viral RNA. Curr. Opin. Microbiol., 18, 78-82.
150. Mocquet, V., Neusiedler, J., Rende, F., Cluet, D., Robin, J.-P., Terme, J.-M., Duc Dodon, M., Wittmann, J., Morris, C., Le Hir, H. et al., (2012) The human T-lymphotropic virus type 1 tax protein inhibits nonsense-mediated mRNA decay by interacting with INT6/EIF3E and UPF1. J. Virol., 86, 7530-7543.
151. Nakano, K., Ando, T., Yamagishi, M., Yokoyama, K., Ishida, T., Ohsugi, T., Tanaka, Y., Brighty, D.W. and Watanabe, T. (2013) Viral interference with host mRNA surveillance, the nonsense-mediated mRNA decay (NMD) pathway, through a new function of HTLV-1 Rex: implications for retroviral replication. Microbes Infect., 15, 491-505.
152. Garcia, D., Garcia, S. and Voinnet, O. (2014) Nonsense-mediated decay serves as a general viral restriction mechanism in plants. Cell Host Microbe, 16, 391-402.
153. Popp, M.W. and Maquat, L.E. (2015) Attenuation of nonsense-mediated mRNA decay facilitates the response to chemotherapeutics. Nat. Commun., 6, 6632.
154. Jia, J., Furlan, A., Gonzalez-Hilarion, S., Leroy, C., Gruenert, D.C., Tulasne, D. and Lejeune, F. (2015) Caspases shutdown nonsense-mediated mRNA decay during apoptosis. Cell Death Differ., 22, 1754-1763.
155. Feng, Q., Snider, L., Jagannathan, S., Tawil, R., van der Maarel, S.M., Tapscott, S.J. and Bradley, R.K. (2015) A feedback loop between nonsense-mediated decay and the retrogene DUX4 in facioscapulohumeral muscular dystrophy. Elife, 4, e04996.
156. Bhuvanagiri, M., Lewis, J., Putzker, K., Becker, J.P., Leicht, S., Krijgsveld, J., Batra, R., Turnwald, B., Jovanovic, B., Hauer, C. et al. (2014) 5-azacytidine inhibits nonsense-mediated decay in a MYC-dependent fashion. EMBO Mol. Med., 6, 1593-1609.
157. Wang, D., Wengrod, J. and Gardner, L.B. (2011) Overexpression of the c-myc oncogene inhibits nonsense-mediated RNA decay in B lymphocytes. J. Biol. Chem., 286, 40038-40043.
158. Durand, S., Cougot, N., Mahuteau-Betzer, F., Nguyen, C.-H., Grierson, D.S., Bertrand, E., Tazi, J. and Lejeune, F. (2007) Inhibition of nonsense-mediated mRNA decay (NMD) by a new chemical molecule reveals the dynamic of NMD factors in P-bodies. J. Cell Biol., 178, 1145-1160.
159. Martin, L., Grigoryan, A., Wang, D., Wang, J., Breda, L., Rivella, S., Cardozo, T. and Gardner, L.B. (2014) Identification and characterization of small molecules that inhibit nonsense-mediated RNA decay and suppress nonsense p53 mutations. Cancer Res., 74, 3104-3113.
160. Dang, Y., Low, W.-K., Xu, J., Gehring, N.H., Dietz, H.C., Romo, D. and Liu, J.O. (2009) Inhibition of nonsense-mediated mRNA decay by the natural product pateamine A through eukaryotic initiation factor 4AIII. J. Biol. Chem., 284, 23613-23621.
161. Feng, D., Su, R.-C., Zou, L., Triggs-Raine, B., Huang, S. and Xie, J. (2015) Increase of a group of PTC(+) transcripts by curcumin through inhibition of the NMD pathway. Biochim. Biophys. Acta, 1849, 1104-1115.
162. Gopalsamy, A., Bennett, E.M., Shi, M., Zhang, W.-G., Bard, J. and Yu, K. (2012) Identification of pyrimidine derivatives as hSMG-1 inhibitors. Bioorg. Med. Chem. Lett., 22, 6636-6641.
163. Keeling, K.M., Wang, D., Conard, S.E. and Bedwell, D.M. (2012) Suppression of premature termination codons as a therapeutic approach. Crit. Rev. Biochem. Mol. Biol., 47, 444-463.
164. Keeling, K.M., Xue, X., Gunn, G. and Bedwell, D.M. (2014) Therapeutics based on stop codon readthrough. Annu. Rev. Genomics Hum. Genet., 15, 371-394.
165. Nomakuchi, T.T., Rigo, F., Aznarez, I. and Krainer, A.R. (2015) Antisense oligonucleotide-directed inhibition of nonsense-mediated mRNA decay. Nat. Biotechnol., 10.1038/nbt.3427.