Binary specification of nonsense codons by splicing and cytoplasmic translation
Open accessAbstract
Premature translation termination codons resulting from nonsense or frameshift mutations are common causes of genetic disorders. Complications arising from the synthesis of C-terminally truncated polypeptides can be avoided by 'nonsense-mediated decay' of the mutant mRNAs. Premature termination codons in the beta-globin mRNA cause the common recessive form of beta-thalassemia when the affected mRNA is degraded, but the more severe dominant form when the mRNA escapes nonsense-mediated decay. We demonstrate that cells distinguish a premature termination codon within the beta-globin mRNA from the physiological translation termination codon by a two-step specification mechanism. According to the binary specification model proposed here, the positions of splice junctions are first tagged during splicing in the nucleus, defining a stop codon operationally as a premature termination codon by the presence of a 3' splicing tag. In the second step, cytoplasmic translation is required to validate the 3' splicing tag for decay of the mRNA. This model explains nonsense-mediated decay on the basis of conventional molecular mechanisms and allows us to propose a common principle for nonsense-mediated decay from yeast to man.
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The cfap20ua5025 frameshift mutation leads to an approximately 90% reduction in cfap20 transcript abundance.
“The frameshift mutation leads to an ~90% reduction in cfap20 transcript abundance (Fig. 2c), presumably due to nonsense-mediated decay24–26.”
From The inner junction protein CFAP20 functions in motile and non-motile cilia and is critical for vision (2022) · cites this paper as [26]
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Cites
Kozak, M. (1986) · Cell · doi:10.1016/0092-8674(86)90762-2 · Cited by 4,741 · see citing works
Hentze, M. W., & Kühn, L. C. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8175 · Cited by 1,292 · see citing works
Self-citationRegulating the fate of mRNA: the control of cellular iron metabolism
Klausner, R. D., Rouault, T. A., & Harford, J. B. (1993) · Cell · doi:10.1016/0092-8674(93)90046-s · Cited by 1,210 · see citing works
A versatilein vivoandin vitroeukaryotic expression vector for protein engineering
Green, S., Issemann, I., & Sheer, E. (1988) · Nucleic Acids Research · doi:10.1093/nar/16.1.369 · Cited by 659 · see citing works
When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells.
Maquat, L. E. (1995) · Europe PMC (PubMed Central) · Cited by 509 · see citing works
mRNA surveillance by the Caenorhabditis elegans smg genes.Preprint
Pulak, R., & Anderson, P. (1993) · Genes & Development · doi:10.1101/gad.7.10.1885 · Cited by 476 · see citing works
Nonsense Mutations in the Dihydrofolate Reductase Gene Affect RNA Processing
Urlaub, G., Mitchell, P. J., Ciudad, C. J., & Chasin, L. A. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.7.2868 · Cited by 354 · see citing works
Carter, M. S., Doskow, J., Morris, P., Li, S., Nhim, R. P., Sandstedt, S. A., & Wilkinson, M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.48.28995 · Cited by 330 · see citing works
The Skipping of Constitutive Exons in Vivo Induced by Nonsense Mutations
Dietz, H. C., Valle, D., Francomano, C. A., Kendzior, R. J., Pyeritz, R. E., & Cutting, G. A. (1993) · Science · doi:10.1126/science.8430317 · Cited by 289 · see citing works
Translational termination efficiency in mammals is influenced by the base following the stop codon
McCaughan, K. K., Brown, C. M., Dalphin, M. E., Berry, M. J., & Tate, W. P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5431 · Cited by 284 · see citing works
A splicing‐dependent regulatory mechanism that detects translation signals.
Carter, M. S., Li, S., & Wilkinson, M. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00983.x · Cited by 280 · see citing works
Gray, N. K., & Hentze, M. W. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06699.x · Cited by 276 · see citing works
Self-citationUnstable β-globin mRNA in mRNA-deficient β0 thalassemia
Maquat, L. E., Kinniburgh, A. J., Rachmilewitz, E. A., & Ross, J. (1981) · Cell · doi:10.1016/0092-8674(81)90396-2 · Cited by 271 · see citing works
Hentze, M. W., Rouault, T. A., Caughman, S. W., Dancis, A., Harford, J. B., & Klausner, R. D. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.19.6730 · Cited by 249 · see citing works
Self-citationNonsense mutations in the human beta-globin gene affect mRNA metabolism.
Baserga, S. J., & Benz, E. J. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.7.2056 · Cited by 235 · see citing works
Visa, N., Izaurralde, E., Ferreira, J. A., Daneholt, B., & Mattaj, I. W. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.133.1.5 · Cited by 232 · see citing works
Pantopoulos, K., & Hentze, M. W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.5.1267 · Cited by 220 · see citing works
Self-citationPremature translation termination mediates triosephosphate isomerase mRNA degradation.
Daar, I. O., & Maquat, L. E. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.2.802 · Cited by 214 · see citing works
Cheng, J., & Maquat, L. E. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.3.1892 · Cited by 200 · see citing works
Evidence that translation reinitiation abrogates nonsense‐mediated mRNA decay in mammalian cells
Zhang, J., & Maquat, L. E. (1997) · The EMBO Journal · doi:10.1093/emboj/16.4.826 · Cited by 194 · see citing works
Zillmann, M., Zapp, M. L., & Berget, S. M. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.2.814 · Cited by 191 · see citing works
Consequences of frameshift mutations at the immunoglobulin heavy chain locus of the mouse.
Baumann, B., Potash, M. J., & Köhler, G. (1985) · The EMBO Journal · doi:10.1002/j.1460-2075.1985.tb03636.x · Cited by 186 · see citing works
Belgrader, P., Cheng, J., & Maquat, L. E. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.2.482 · Cited by 185 · see citing works
Molecular basis for dominantly inherited inclusion body beta-thalassemia.
Thein, S. L., Hesketh, C., Taylor, P., Temperley, I. J., Hutchinson, R. M., Old, J. M., Wood, W. G., Clegg, J. B., & Weatherall, D. J. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.10.3924 · Cited by 183 · see citing works
Introns are cis Effectors of the Nonsense-Codon-Mediated Reduction in Nuclear mRNA Abundance
Cheng, J., Belgrader, P., Zhou, X., & Maquat, L. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.9.6317-6325.1994 · Cited by 159 · see citing works
Cheng, J., Fogel‐Petrovic, M., & Maquat, L. E. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.10.5215 · Cited by 158 · see citing works
Applequist, S. E., Selg, M., Raman, C., & Jäck, H. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.4.814 · Cited by 157 · see citing works
Goossen, B., & Hentze, M. W. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.5.1959-1966.1992 · Cited by 145 · see citing works
Self-citationMaintenance of an open reading frame as an additional level of scrutiny during splice site selection
Dietz, H. C., & Kendzior, R. J. (1994) · Nature Genetics · doi:10.1038/ng1094-183 · Cited by 140 · see citing works
Nonsense Mutations in the Dihydrofolate Reductase Gene Affect RNA Processing
Urlaub, G., Mitchell, P. J., Ciudad, C. J., et al. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.7.2868-2880.1989 · Cited by 139 · see citing works
Mammalian nonsense codons can be cis effectors of nuclear mRNA half-life.
Belgrader, P., Cheng, J., Zhou, X., Stephenson, L. S., & Maquat, L. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.8219 · Cited by 136 · see citing works
Aoufouchi, S., Yélamos, J., & Milstein, C. (1996) · Cell · doi:10.1016/s0092-8674(00)81119-8 · Cited by 132 · see citing works
In Vitro Recombination and Mutagenesis by Overlap Extension PCR
Pogulis, R. J., Vallejo, A. N., & Pease, L. R. (2003) · Humana Press eBooks · doi:10.1385/0-89603-332-5:167 · Cited by 129 · see citing works
Belgrader, P., & Maquat, L. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.9.6326 · Cited by 128 · see citing works
Ruiz-Echevarría, M. J., González, C. I., & Peltz, S. W. (1998) · The EMBO Journal · doi:10.1093/emboj/17.2.575 · Cited by 126 · see citing works
Naeger, L. K., Schoborg, R. V., Zhao, Q., Tullis, G. E., & Pintel, D. J. (1992) · Genes & Development · doi:10.1101/gad.6.6.1107 · Cited by 124 · see citing works
Baserga, S. J., & Benz, E. J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.7.2935 · Cited by 122 · see citing works
A model for the structure and functions of iron-responsive elements
Hentze, M. W., Caughman, S. W., Casey, J. L., Kodier, D. M., Rouault, T. A., Harford, J. B., & Klausner, R. D. (1988) · Gene · doi:10.1016/0378-1119(88)90145-x · Cited by 116 · see citing works
Self-citationNonsense Codons in Human β-Globin mRNA Result in the Production of mRNA Degradation Products
Lim, S. K., Sigmund, C. D., Gross, K. W., & Maquat, L. E. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.3.1149-1161.1992 · Cited by 114 · see citing works
Humphries, R. K., Ley, T. J., Anagnou, N., Baur, A., & Nienhuis, A. (1984) · Blood · doi:10.1182/blood.v64.1.23.bloodjournal64123 · Cited by 107 · see citing works
Kessler, O., Jiang, Y., & Chasin, L. A. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.10.6211 · Cited by 105 · see citing works
Making sense of nonsense in yeast
Ruiz-Echevarría, M. J., Czaplinski, K., & Peltz, S. W. (1996) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)10055-4 · Cited by 96 · see citing works
Zillmann, M., Zapp, M. L., & Berget, S. M. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.2.814-821.1988 · Cited by 95 · see citing works
Lozano, F., Maertzdorf, B., Pannell, R., & Milstein, C. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06783.x · Cited by 94 · see citing works
Takeshita, K., Forget, B. G., Scarpa, A. L., & Benz, E. J. (1984) · Blood · doi:10.1182/blood.v64.1.13.13 · Cited by 93 · see citing works
Lim, S. K., & Maquat, L. E. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05405.x · Cited by 89 · see citing works
Premature Translation Termination Mediates Triosephosphate Isomerase mRNA Degradation
Daar, I. O., & Maquat, L. E. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.2.802-813.1988 · Cited by 84 · see citing works
Cheng, J., & Maquat, L. E. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.3.1892-1902.1993 · Cited by 81 · see citing works
Li, S., Leonard, D., & Wilkinson, M. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.6.985 · Cited by 77 · see citing works
Differential regulation of two related RNA-binding proteins, iron regulatory protein (IRP) and IRPB.
Pantopoulos, K., Gray, N. K., & Hentze, M. W. (1995) · PubMed · Cited by 70 · see citing works
Self-citationKugler, W., Enssle, J., Hentze, M. W., & Kulozik, A. E. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.3.413 · Cited by 69 · see citing works
Self-citationEffects of Nonsense Mutations on Nuclear and Cytoplasmic Adenine Phosphoribosyltransferase RNA
Kessler, O., & Chasin, L. A. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.8.4426 · Cited by 65 · see citing works
Determination of mRNA fate by different RNA polymerase II promoters.
Enssle, J., Kugler, W., Hentze, M. W., & Kulozik, A. E. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.21.10091 · Cited by 64 · see citing works
Self-citationMashima, Y., Murakami, A., Weleber, R. G., Kennaway, N. G., Clarke, L. A., Shiono, T., & Inana, G. (1992) · PubMed · Cited by 61 · see citing works
Cheng, J., Fogel‐Petrovic, M., & Maquat, L. E. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.10.5215-5225.1990 · Cited by 55 · see citing works
Belgrader, P., & Maquat, L. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.9.6326-6336.1994 · Cited by 50 · see citing works
Beta‐thalassaemia in the immigrant and non‐immigrant German populations
Vetter, B., Schwarz, C., KOHNE, E., & Kulozik, A. E. (1997) · British Journal of Haematology · doi:10.1046/j.1365-2141.1997.342674.x · Cited by 48 · see citing works
Self-citationT Cell Receptor-β mRNA Splicing: Regulation of Unusual Splicing Intermediates
Qian, L., Theodor, L., Carter, M., Vu, M. N., Sasaki, A. W., & Wilkinson, M. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.3.1686-1696.1993 · Cited by 45 · see citing works
Mammalian Nonsense Codons Can Be cis Effectors of Nuclear mRNA Half-Life
Belgrader, P., Cheng, J., Zhou, X., Stephenson, L. S., & Maquat, L. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.8219-8228.1994 · Cited by 45 · see citing works
Simpson, S. B., & Stoltzfus, C. M. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.3.1835-1844.1994 · Cited by 36 · see citing works
Nonsense mutations and altered splice-site selection.
Dietz, H. C. (1997) · PubMed · Cited by 35 · see citing works
Menon, K. P., & Neufeld, E. F. (1994) · PubMed · Cited by 35 · see citing works
Liu, X., & Mei, J. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.9.1765 · Cited by 25 · see citing works
Site-Directed Mutagenesis Using a Uracil-Containing Phagemid Template
Hagemeier, C. (2003) · Humana Press eBooks · doi:10.1385/0-89603-332-5:45 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- Ausubel,F.M., Brent,R., Kingston,R.I., Moore,D.D., Seidman,J.G., Smith,J.A. and Struhl,K. (1994) Current Protocols in Molecular Biology. Vol. 1. John Wiley, New York.
- Konat,G.W., Laszkiewicz,I., Grubinska,B. and Wiggins,R.C. (1994) Generation of labelled DNA probes by PCR. In Griffin,H.G. and Griffin,A.M. (eds), PCR Technology. Current Innovations. CRC Press, London, pp. 37-42.
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Messenger-RNA-binding proteins and the messages they carry
Dreyfuss, G., Kim, V. N., & Kataoka, N. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm760 · Cited by 1,469 · see citing works
Telomeric Repeat–Containing RNA and RNA Surveillance Factors at Mammalian Chromosome Ends
Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E., & Lingner, J. (2007) · Science · doi:10.1126/science.1147182 · Cited by 1,318 · see citing works
The Nonsense-Mediated Decay RNA Surveillance Pathway
Chang, Y.-F., Imam, J. S., & Wilkinson, M. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.050106.093909 · Cited by 1,283 · see citing works
Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics
Maquat, L. E. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1310 · Cited by 1,214 · see citing works
Nonsense-mediated mRNA decayin health and disease
Frischmeyer, P. A. (1999) · Human Molecular Genetics · doi:10.1093/hmg/8.10.1893 · Cited by 991 · see citing works
The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon–exon junctions
Hir, H. L., Izaurralde, E., Maquat, L. E., & Moore, M. J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.24.6860 · Cited by 970 · see citing works
Pre-mRNA Processing Reaches Back toTranscription and Ahead to Translation
Moore, M. J., & Proudfoot, N. J. (2009) · Cell · doi:10.1016/j.cell.2009.02.001 · Cited by 835 · see citing works
Hir, H. L., Gatfield, D., Izaurralde, E., & Moore, M. J. (2001) · The EMBO Journal · doi:10.1093/emboj/20.17.4987 · Cited by 842 · see citing works
Quality and quantity control of gene expression by nonsense-mediated mRNA decay
Kurosaki, T., Popp, M. W., & Maquat, L. E. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0126-2 · Cited by 834 · see citing works
Hentze, M. W., & Kulozik, A. E. (1999) · Cell · doi:10.1016/s0092-8674(00)80542-5 · Cited by 809 · see citing works
Self-citationKönig, J., Nies, A. T., Cui, Y., Leier, I., & KEPPLER, D. O. R. (1999) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(99)00169-8 · Cited by 786 · see citing works
hERG K + Channels: Structure, Function, and Clinical Significance
Vandenberg, J. I., Perry, M., Perrin, M. J., Mann, S. A., Ke, Y., & Hill, A. P. (2012) · Physiological Reviews · doi:10.1152/physrev.00036.2011 · Cited by 698 · see citing works
Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias
Weatherall, D. J. (2001) · Nature Reviews Genetics · doi:10.1038/35066048 · Cited by 692 · see citing works
Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases
Löscher, W., & Potschka, H. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.04.006 · Cited by 617 · see citing works
Nonsense-mediated mRNA decay (NMD) mechanisms
Brogna, S., & Wen, J. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1550 · Cited by 593 · see citing works
Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA functionPreprint
Isken, O., & Maquat, L. E. (2007) · Genes & Development · doi:10.1101/gad.1566807 · Cited by 584 · see citing works
Evidence for a Pioneer Round of mRNA Translation
Ishigaki, Y., Li, X., Serin, G., & Maquat, L. E. (2001) · Cell · doi:10.1016/s0092-8674(01)00475-5 · Cited by 583 · see citing works
Lykke‐Andersen, J., Shu, M.-D., & STEITZ, J. A. (2000) · Cell · doi:10.1016/s0092-8674(00)00214-2 · Cited by 579 · see citing works
NMD: a multifaceted response to premature translational termination
Kervestin, S., & Jacobson, A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3454 · Cited by 572 · see citing works
The rules and impact of nonsense-mediated mRNA decay in human cancers
Lindeboom, R. G. H., Supek, F., & Lehner, B. (2016) · Nature Genetics · doi:10.1038/ng.3664 · Cited by 549 · see citing works
Mechanism and regulation of the nonsense-mediated decay pathway
Hug, N., Longman, D., & Cáceres, J. F. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw010 · Cited by 535 · see citing works
Nonsense-mediated mRNA decay: terminating erroneous gene expression
Baker, K. E., & Parker, R. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.03.003 · Cited by 455 · see citing works
SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells
Eberle, A. B., Lykke‐Andersen, S., Mühlemann, O., & Jensen, T. H. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1530 · Cited by 430 · see citing works
Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y., & Ohno, S. (2001) · Genes & Development · doi:10.1101/gad.913001 · Cited by 420 · see citing works
The apical conjugate efflux pump ABCC2 (MRP2)
Nies, A. T., & KEPPLER, D. O. R. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0109-y · Cited by 394 · see citing works
Lejeune, F., Li, X., & Maquat, L. E. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00349-6 · Cited by 389 · see citing works
Organizing Principles of Mammalian Nonsense-Mediated mRNA Decay
Popp, M. W., & Maquat, L. E. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133424 · Cited by 371 · see citing works
Schweingruber, C., Rufener, S. C., Zünd, D., Yamashita, A., & Mühlemann, O. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.02.005 · Cited by 356 · see citing works
An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay
Palacios, I. M., Gatfield, D., Johnston, D. S., & Izaurralde, E. (2004) · Nature · doi:10.1038/nature02351 · Cited by 362 · see citing works
Ohnishi, T., Yamashita, A., Kashima, I., Schell, T., Anders, K. R., Grimson, A., Hachiya, T., Hentze, M. W., Anderson, P., & Ohno, S. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00443-x · Cited by 346 · see citing works
Self-citationSMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan
Huntzinger, E., Kashima, I., Fauser, M., Saulière, J., & Izaurralde, E. (2008) · RNA · doi:10.1261/rna.1386208 · Cited by 343 · see citing works
Singh, G., Rebbapragada, I., & Lykke‐Andersen, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060111 · Cited by 342 · see citing works
Hir, H. L., Moore, M. J., & Maquat, L. E. (2000) · Genes & Development · doi:10.1101/gad.14.9.1098 · Cited by 337 · see citing works
Nicholson, P., Yepiskoposyan, H., Metze, S., Orozco, R. Z., Kleinschmidt, N., & Mühlemann, O. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0177-1 · Cited by 336 · see citing works
Mechanisms of deadenylation‐dependent decay
Chen, C. A., & Shyu, A. (2010) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.40 · Cited by 330 · see citing works
Ivanov, P. V., Gehring, N. H., Kunz, J. B., Hentze, M. W., & Kulozik, A. E. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.17 · Cited by 331 · see citing works
Self-citationNonsense-Mediated mRNA Decay: Degradation of Defective Transcripts Is Only Part of the Story
He, F., & Jacobson, A. (2015) · Annual Review of Genetics · doi:10.1146/annurev-genet-112414-054639 · Cited by 303 · see citing works
Nonsense‐mediated mRNA decay in Drosophila:at the intersection of the yeast and mammalian pathways
Gatfield, D., Unterholzner, L., Ciccarelli, F. D., Peer Bork, B., & Izaurralde, E. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg371 · Cited by 303 · see citing works
Posttranscriptional Gene Regulation by Spatial Rearrangement of the 3′ Untranslated Region
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Kim, V. N., Kataoka, N., & Dreyfuss, G. (2001) · Science · doi:10.1126/science.1062829 · Cited by 299 · see citing works
Y14 and hUpf3b Form an NMD-Activating Complex
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Self-citationThe exon junction complex as a node of post-transcriptional networks
Hir, H. L., Saulière, J., & Wang, Z. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2015.7 · Cited by 280 · see citing works
Gehring, N. H., Frede, U., Neu‐Yilik, G., Hundsdoerfer, P., Vetter, B., Hentze, M. W., & Kulozik, A. E. (2001) · Nature Genetics · doi:10.1038/ng578 · Cited by 277 · see citing works
Self-citationThe ever-increasing complexities of the exon junction complex
Tange, T. Ø., Nott, A., & Moore, M. J. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.03.012 · Cited by 274 · see citing works
Execution of nonsense-mediated mRNA decay: what defines a substrate?
Rebbapragada, I., & Lykke‐Andersen, J. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.02.007 · Cited by 269 · see citing works
Katsuhata, Y., Yamashita, A., Kutsuzawa, K., Izumi, N., Hirahara, F., & Ohno, S. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr791 · Cited by 255 · see citing works
Serin, G., Gersappe, A., Black, J. D., Aronoff, R., & Maquat, L. E. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.1.209-223.2001 · Cited by 253 · see citing works
Perrin-Vidoz, L. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.23.2805 · Cited by 245 · see citing works
To NMD or Not To NMD: Nonsense-Mediated mRNA Decay in Cancer and Other Genetic Diseases
Supek, F., Lehner, B., & Lindeboom, R. G. H. (2020) · Trends in Genetics · doi:10.1016/j.tig.2020.11.002 · Cited by 246 · see citing works
hUPF2 Silencing Identifies Physiologic Substrates of Mammalian Nonsense-Mediated mRNA Decay
Wittmann, J., Hol, E. M., & Jäck, H. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.4.1272-1287.2006 · Cited by 240 · see citing works
mRNA surveillance: the perfect persist
Wagner, E., & Lykke‐Andersen, J. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.15.3033 · Cited by 238 · see citing works
Involvement of SR Proteins in mRNA Surveillance
Zhang, Z., & Krainer, A. R. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.10.031 · Cited by 232 · see citing works
Page, M. F., Carr, B., Anders, K. R., Grimson, A., & Anderson, P. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.9.5943 · Cited by 230 · see citing works
A GFP-based reporter system to monitor nonsense-mediated mRNA decay
Paillusson, A. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni052 · Cited by 224 · see citing works
An NMD Pathway in Yeast Involving Accelerated Deadenylation and Exosome-Mediated 3′→5′ Degradation
Mitchell, P., & Tollervey, D. W. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00190-4 · Cited by 222 · see citing works
An alternative branch of the nonsense‐mediated decay pathway
Chan, W.-K., Huang, L., Gudikote, J. P., Chang, Y.-F., Imam, J. S., MacLean, J. A., & Wilkinson, M. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601628 · Cited by 222 · see citing works
Loh, B., Jonas, S., & Izaurralde, E. (2013) · Genes & Development · doi:10.1101/gad.226951.113 · Cited by 212 · see citing works
Colombo, M., Karousis, E. D., Bourquin, J., Bruggmann, R., & Mühlemann, O. (2016) · RNA · doi:10.1261/rna.059055.116 · Cited by 201 · see citing works
NMD: RNA biology meets human genetic medicine
Bhuvanagiri, M., Schlitter, A. M., Hentze, M. W., & Kulozik, A. E. (2010) · Biochemical Journal · doi:10.1042/bj20100699 · Cited by 216 · see citing works
Self-citationNonsense-Mediated mRNA Decay Begins Where Translation EndsPreprint
Karousis, E. D., & Mühlemann, O. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032862 · Cited by 212 · see citing works
The Human RNA Surveillance Factor UPF1 Is Required for S Phase Progression and Genome Stability
Azzalin, C. M., & Lingner, J. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.018 · Cited by 210 · see citing works
Mechanisms of mRNA Surveillance in Eukaryotes
Hilleren, P. J., & Parker, R. (1999) · Annual Review of Genetics · doi:10.1146/annurev.genet.33.1.229 · Cited by 209 · see citing works
Pesch, U. E. A. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.13.1359 · Cited by 197 · see citing works
Nonsense‐mediated mRNA decay: novel mechanistic insights and biological impact
Karousis, E. D., Nasif, S., & Mühlemann, O. (2016) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1357 · Cited by 195 · see citing works
Disassembly of Exon Junction Complexes by PYM
Gehring, N. H., Lamprinaki, S., Kulozik, A. E., & Hentze, M. W. (2009) · Cell · doi:10.1016/j.cell.2009.02.042 · Cited by 194 · see citing works
Self-citationRobinson, P. N., Booms, P., Katzke, S., Ladewig, M. S., Neumann, L. M., Palz, M., Pregla, R., Tiecke, F., & Rosenberg, T. (2002) · Human Mutation · doi:10.1002/humu.10113 · Cited by 194 · see citing works
Durand, S., Cougot, N., Mahuteau‐Betzer, F., Nguyen, C.-H., Grierson, D. S., Bertrand, É., Tazi, J., & Lejeune, F. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200611086 · Cited by 189 · see citing works
Distinct Mutations in the Receptor Tyrosine Kinase Gene ROR2 Cause Brachydactyly Type B
Schwabe, G. C., Tinschert, S., Buschow, C., Meinecke, P., Wolff, G., Gillessen‐Kaesbach, G., Oldridge, M., Wilkie, A. O. M., Kömec, R., & Mundlos, S. (2000) · The American Journal of Human Genetics · doi:10.1086/303084 · Cited by 189 · see citing works
Thyroglobulin From Molecular and Cellular Biology to Clinical Endocrinology
Di Jeso, B., & Arvan, P. (2016) · Endocrine Reviews · doi:10.1210/er.2015-1090 · Cited by 184 · see citing works
The Y14 protein communicates to the cytoplasm the position of exon–exon junctions
Kim, V. N., Yong, J., Kataoka, N., Abel, L., Diem, M. D., & Dreyfuss, G. (2001) · The EMBO Journal · doi:10.1093/emboj/20.8.2062 · Cited by 181 · see citing works
A post-translational regulatory switch on UPF1 controls targeted mRNA degradationPreprint
Kurosaki, T., Li, W., Hoque, M., Popp, M. W., Ermolenko, D. N., Tian, B., & Maquat, L. E. (2014) · Genes & Development · doi:10.1101/gad.245506.114 · Cited by 175 · see citing works
SECIS–SBP2 interactions dictate selenocysteine incorporation efficiency and selenoprotein hierarchy
Low, S. C., Grundner‐Culemann, E., Harney, J. W., & Berry, M. J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.24.6882 · Cited by 171 · see citing works
Single-Molecule Imaging Uncovers Rules Governing Nonsense-Mediated mRNA Decay
Hoek, T. A., Khuperkar, D., Lindeboom, R., Sonneveld, S., Verhagen, B. M. P., Boersma, S., Vermeulen, M., & Tanenbaum, M. (2019) · Molecules and Cells · doi:10.1016/j.molcel.2019.05.008 · Cited by 143 · see citing works
Schrijver, I., Liu, W., Odom, R. S., Brenn, T., Oefner, P. J., Furthmayr, H., & Francke, U. (2002) · The American Journal of Human Genetics · doi:10.1086/341581 · Cited by 165 · see citing works
Chiu, S.-Y., Serin, G., Ohara, O., & Maquat, L. E. (2003) · RNA · doi:10.1261/rna.2137903 · Cited by 161 · see citing works
The Yeast hnRNP-like Protein Hrp1/Nab4 Marks a Transcript for Nonsense-Mediated mRNA Decay
Gonzalez, C. I., Ruiz-Echevarría, M. J., Vasudevan, S., Henry, M. F., & Peltz, S. W. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80443-8 · Cited by 155 · see citing works
Silva, A. L., & Romão, L. (2009) · FEBS Letters · doi:10.1016/j.febslet.2008.12.058 · Cited by 154 · see citing works
Tsujii, H., König, J., Rost, D., Stöckel, B., Leuschner, U., & KEPPLER, D. O. R. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70459-2 · Cited by 152 · see citing works
Looking at mRNA decay pathways through the window of molecular evolution
Culbertson, M. R., & Leeds, P. (2003) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(03)00014-5 · Cited by 147 · see citing works
Inácio, Â., Silva, A. L., Pinto, J. B. S. A., Ji, X., Morgado, A., Almeida, F., Faustino, P., Lavinha, J., Liebhaber, S. A., & Romão, L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405024200 · Cited by 147 · see citing works
Keitel, V., Kartenbeck, J., Nies, A. T., Spring, H., Brom, M., & KEPPLER, D. O. R. (2000) · Hepatology · doi:10.1053/jhep.2000.19791 · Cited by 145 · see citing works
Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation
Kunz, J. B., Neu‐Yilik, G., Hentze, M. W., Kulozik, A. E., & Gehring, N. H. (2006) · RNA · doi:10.1261/rna.12506 · Cited by 142 · see citing works
Self-citationMetze, S., Herzog, V. A., Ruepp, M., & Mühlemann, O. (2013) · RNA · doi:10.1261/rna.038893.113 · Cited by 141 · see citing works
Neu-Yilik, G., Amthor, B., Gehring, N. H., Bahri, S., Paidassi, H., Hentze, M. W., & Kulozik, A. E. (2011) · RNA · doi:10.1261/rna.2401811 · Cited by 140 · see citing works
Self-citationBaek, D., & Green, P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506139102 · Cited by 138 · see citing works
Linde, L., Boelz, S., Neu‐Yilik, G., Kulozik, A. E., & Kerem, B. (2007) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201889 · Cited by 139 · see citing works
Self-citationRules that govern UPF1 binding to mRNA 3′ UTRs
Kurosaki, T., & Maquat, L. E. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219908110 · Cited by 138 · see citing works
Chen, C. A., & Shyu, A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.14.4805-4813.2003 · Cited by 137 · see citing works
Gehring, N. H., Lamprinaki, S., Hentze, M. W., & Kulozik, A. E. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000120 · Cited by 136 · see citing works
Self-citationNonsense-mediated mRNA decay in Saccharomyces cerevisiae
Gonzalez, C. I., Bhattacharya, A., Wang, W., & Peltz, S. W. (2001) · Gene · doi:10.1016/s0378-1119(01)00552-2 · Cited by 135 · see citing works
Andersen, P. S., Havndrup, O., Hougs, L., Sorensen, K. M., Jensen, M. K., Larsen, L. A., Hedley, P. L., Thomsen, A. R. B., Moolman‐Smook, J. C., Christiansen, M., et al. (2008) · Human Mutation · doi:10.1002/humu.20862 · Cited by 133 · see citing works
Gijselinck, I., Broeckhoven, C. V., & Cruts, M. (2008) · Human Mutation · doi:10.1002/humu.20785 · Cited by 131 · see citing works
Precursor RNAs Harboring Nonsense Codons Accumulate Near the Site of Transcription
Mühlemann, O., Mock-Casagrande, C. S., Wang, J., Li, S., Custódio, N., Carmo‐Fonseca, M., Wilkinson, M., & Moore, M. J. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00288-x · Cited by 132 · see citing works
Normalized long read RNA sequencing in chicken reveals transcriptome complexity similar to human
Kuo, R. I., Tseng, E., Eöry, L., Paton, I. R., Archibald, A. L., & Burt, D. W. (2017) · BMC Genomics · doi:10.1186/s12864-017-3691-9 · Cited by 126 · see citing works
Dyle, M. C., Kolakada, D., Cortázar, M. A., & Jagannathan, S. (2019) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1560 · Cited by 124 · see citing works
Viegas, M. H., Gehring, N. H., Breit, S., Hentze, M. W., & Kulozik, A. E. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm461 · Cited by 124 · see citing works
Self-citationKeitel, V., Nies, A. T., Brom, M., Hummel-Eisenbeiss, J., Spring, H., & KEPPLER, D. O. R. (2003) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00362.2002 · Cited by 122 · see citing works
Temporal and spatial characterization of nonsense-mediated mRNA decayPreprint
Trcek, T., Sato, H., Singer, R. H., & Maquat, L. E. (2013) · Genes & Development · doi:10.1101/gad.209635.112 · Cited by 120 · see citing works
Exon Junction Complexes: Supervising the Gene Expression Assembly Line
Boehm, V., & Gehring, N. H. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.09.003 · Cited by 121 · see citing works
Chester, A., Somasekaram, A., Tzimina, M., Jarmuz, A., Gisbourne, J., O’Keefe, R. T., Scott, J., & Navaratnam, N. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg369 · Cited by 121 · see citing works
- Authors
- Thermann, R., Neu‐Yilik, G., Deters, A., Frede, U., Wehr, K., Hagemeier, C., Hentze, M. W., & Kulozik, A. E.
- Affiliations
- Humboldt-Universität zu Berlin (DE)
- European Molecular Biology Laboratory (DE)
- Corresponding author
- Hentze, Matthias W.
- Kulozik, Andreas E.
- Venue
- The EMBO Journal
- Published
- 1998-06-15
- Volume
- 17
- Issue
- 12
- Pages
- 3484-3494
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1170685
- OpenAlex
- W2036625038
- Cited by
- 406
- References
- 59
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 3 · 2023: 12 · 2022: 15 · 2021: 17 · 2020: 15 · 2019: 14 · 2018: 15 · 2017: 12 · 2016: 15 · 2015: 15 · 2014: 8 · 2013: 19 · 2012: 8
- FWCI
- 7.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Chinese Academy of Agricultural Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
- Keywords
- nonsense-mediated mRNA decay, stop codon, premature stop codon, beta-globin mRNA, beta-thalassemia, splicing, splice junctions, cytoplasmic translation, mRNA degradation, frameshift mutation
- MeSH terms
- HeLa Cells, Humans, RNA, Messenger, Protein Biosynthesis, Codon, Terminator, Codon, Nonsense, Fluorescent Antibody Technique, Indirect
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