Nonsense-mediated decay approaches the clinic

Nature Genetics

Volumn 36, Issue 8, 2004, Pages 801-808

  Holbrook, Jill A ^a,b   Neu Yilik, Gabriele ^a,b   Hentze, Matthias W ^b,c   Kulozik, Andreas E ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Molecular Medicine Partnership Unit   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BETA GLOBIN; BLOOD CLOTTING FACTOR 10; BRCA1 PROTEIN; CALPAIN; FERROCHELATASE; FIBRILLARIN; GAMMA INTERFERON; GLUTATHIONE PEROXIDASE; HOMEODOMAIN PROTEIN; IMMUNOGLOBULIN; MESSENGER RNA; PROTEIN P53; PROTEIN TYROSINE KINASE; RHODOPSIN; T LYMPHOCYTE RECEPTOR; TELOMERASE; VON WILLEBRAND FACTOR; WT1 PROTEIN;

ALTERNATIVE RNA SPLICING; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENETIC DISORDER; HETEROZYGOTE; NONHUMAN; NONSENSE MUTATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SACCHAROMYCES CEREVISIAE; SRY GENE; STOP CODON; TELOMERE; TUMOR SUPPRESSOR GENE; WILD TYPE;

ALTERNATIVE SPLICING; CODON, NONSENSE; GENE EXPRESSION REGULATION; GENES, TUMOR SUPPRESSOR; GENETIC DISEASES, INBORN; HUMANS; MODELS, GENETIC; RNA, MESSENGER;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; MELANOGASTER; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 3542995089     PISSN: 10614036     EISSN: None     Source Type: Journal    
DOI: 10.1038/ng1403     Document Type: Review

References (100)

1. Chang, J.C. & Kan, Y.W. Beta-thalassemia, a nonsense mutation in man. Proc. Natl. Acad. Sci. USA 76, 2886-2889 (1979).
2. Losson, R. & Lacroute, F. Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc. Natl. Acad. Sci. USA 76, 5134-5137 (1979).
3. Brogna, S. Nonsense mutations in the alcohol dehydrogenase gene of Drosophila melanogaster correlate with an abnormal 3′ end processing of the corresponding pre-mRNA. RNA 5, 562-573 (1999).
4. Pulak, R. & Anderson, P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7, 1885-1897 (1993).
5. Maquat, L.E. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat. Rev. Mol. Cell Biol. 5, 89-99 (2004).
6. Brocke, K.S., Neu-Yilik, G., Gehring, N.H., Hentze, M.W. & Kulozik, A.E. The human intronless melanocortin 4-receptor gene is NMD insensitive. Hum. Mol. Genet. 11, 331-335 (2002).
7. Maquat, L.E. & Li, X. Mammalian heat shock p70 and histone H4 transcripts, which derive from naturally intronless genes, are immune to nonsense-mediated decay. RNA 7, 445-456 (2001).
8. Neu-Yilik, G. et al. Splicing and 3′ end formation in the definition of nonsense-mediated decay-competent human beta-globin mRNPs. EMBO J. 20, 532-540 (2001).
9. Le Hir, H., Izaurralde, E., Maquat, L.E. & Moore, M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19, 6860-6869 (2000).
10. Kim, V.N. et al. The Y14 protein communicates to the cytoplasm the position of exon-exon junctions. EMBO J. 20, 2062-2068 (2001).
11. Lykke-Andersen, J., Shu, M.D. & Steitz, J.A. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293, 1836-1839 (2001).
12. Atkin, A.L. et al. Relationship between yeast polyribosomes and Upf proteins required for nonsense mRNA decay. J. Biol. Chem. 272, 22163-22172 (1997).
13. Czaplinski, K. et al. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12, 1665-1677. (1998).
14. Pal, M., Ishigaki, Y., Nagy, E. & Maquat, L.E. Evidence that phosphorylation of human Upfl 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 (2001).
15. Ohnishi, T. et al. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell 12, 1187-1200 (2003).
16. Chiu, S.Y., Serin, G., Ohara, O. & Maquat, L.E. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 9, 77-87 (2003).
17. Page, M.F., Carr, B., Anders, K.R., Grimson, A. & Anderson, P. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19, 5943-5951 (1999).
18. Schell, T., Kulozik, A.E. & Hentze, M.W. Integration of splicing, transport and translation to achieve mRNA quality control by the nonsense-mediated decay pathway. Genome Biol. 3, Reviews 1006.1-1006.6 (2002).
19. Singh, G. & Lykke-Andersen, J. New insights into the formation of active nonsense-mediated decay complexes. Trends Biochem. Sci. 28, 464-466 (2003).
20. Wilkinson, M.F. The cycle of nonsense. Mol. Cell 12, 1059-1061 (2003).
21. Nagy, E. & Maquat, L.E. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23, 198-199 (1998).
22. Wang, J., Gudikote, J.P., Olivas, O.R. & Wilkinson, M.F. Boundary-independent polar nonsense-mediated decay. EMBO Rep. 3, 274-279 (2002).
23. Chan, D., Weng, Y.M., Graham, H.K., Sillence, D.O. & Bateman, J.F. A nonsense mutation in the carboxyl-terminal domain of type X collagen causes haploinsufficiency in schmid metaphyseal chondrodysplasia. J. Clin. Invest. 101, 1490-1499. (1998).
24. Asselta, R. et al. Congenital afibrinogenemia: mutations leading to premature termination codons in fibrinogen A alpha-chain gene are not associated with the decay of the mutant mRNAs. Blood 98, 3685-3692. (2001).
25. Danckwardt, S. et al. Abnormally spliced beta-globin mRNAs: a single point mutation generates transcripts sensitive and insensitive to nonsense-mediated mRNA decay. Blood 99, 1811-1816 (2002).
26. Romao, L. et al. Nonsense mutations in the human beta-globin gene lead to unexpected levels of cytoplasmic mRNA accumulation. Blood 96, 2895-2901 (2000).
27. Mango, S.E. Stop making nonSense: the C. elegans smg genes. Trends Genet. 17, 646-653 (2001).
28. Bamber, B.A., Beg, A.A., Twyman, R.E. & Jorgensen, E.M. The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J. Neurosci. 19, 5348-5359 (1999).
29. Chester, A. et al. The apolipoprotein B mRNA editing complex performs a multifunctional cycle and suppresses nonsense-mediated decay. EMBO J. 22, 3971-3982 (2003).
30. Bateman, J.F., Freddi, S., Nattrass, G. & Savarirayan, R. Tissue-specific RNA surveillance? Nonsense-mediated mRNA decay causes collagen X haploinsufficiency in Schmid metaphyseal chondrodysplasia cartilage. Hum. Mol. Genet. 12, 217-225 (2003).
31. Kerr, T.P., Sewry, C.A., Robb, S.A. & Roberts, R.G. Long mutant dystrophins and variable phenotypes: evasion of nonsense-mediated decay? Hum. Genet. 109, 402-407 (2001).
32. Donnadieu, E. et al. Competing functions encoded in the allergy-associated F(c)epsilonRIbeta gene. Immunity 18, 665-674 (2003).
33. Li, S. & Wilkinson, M.F. Nonsense surveillance in lymphocytes? Immunity 8, 135-141 (1998).
34. Frischmeyer, P.A. & Dietz, H.C. Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8, 1893-1900 (1999).
35. Blaschke, R.J. et al. Transcriptional and translational regulation of the Leri-Weill and Turner syndrome homeobox gene SHOX. J. Biol. Chem. 278, 47820-47826 (2003).
36. Moriarty, P.M., Reddy, C.C. & Maquat, L.E. 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, 2932-2939 (1998).
37. Sun, X. et al. Nonsense-mediated decay of mRNA for the selenoprotein phospholipid hydroperoxide glutathione peroxidase is detectable in cultured cells but masked or inhibited in rat tissues. Mol. Biol. Cell 12, 1009-1017 (2001).
38. Lewis, B.P., Green, R.E. & Brenner, S.E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. USA 100, 189-192 (2003).
39. Green, R.E. et al. Widespread predicted nonsense-mediated mRNA decay of alternatively-spliced transcripts of human normal and disease genes. Bioinformatics 19 Suppl 1, 1118-1121 (2003).
40. Lamba, J.K. et al. Nonsense mediated decay downregulates conserved alternatively spliced ABCC4 transcripts bearing nonsense codons. Hum. Mol. Genet. 12, 99-109 (2003).
41. Gouya, L. et al. The penetrance of dominant erythropoietic protoporphyria is modulated by expression of wildtype FECH. Nat. Genet. 30, 27-28 (2002).
42. Sureau, A., Gattoni, R., Dooghe, Y., Stevenin, J. & Soret, J. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J. 20, 1785-1796 (2001).
43. Wollerton, M.C., Gooding, C., Wagner, E.J., Garcia-Blanco, M.A. & Smith, C.W. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell 13, 91-100 (2004).
44. Snow, B.E. et al. Functional conservation of the telomerase protein EST1p in humans. Curr. Biol. 13, 698-704 (2003).
45. Reichenbach, P. et al. A human homolog of yeast Est1 associates with telomerase and uncaps chromosome ends when overexpressed. Curr. Biol. 13, 568-574 (2003).
46. Neu-Yilik, G., Gehring, N.H., Hentze, M.W. & Kulozik, A.E. Nonsense-mediated mRNA decay: from vacuum cleaner to Swiss army knife. Genome Biol. 5, 218.1-218.4 (2004).
47. Medghalchi, S.M. et al. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10, 99-105 (2001).
48. Pelczar, P. & Filipowicz, W. The host gene for intronic U17 small nucleolar RNAs in mammals has no protein-coding potential and is a member of the 5′-terminal oligopyrimidine gene family. Mol. Cell. Biol. 18, 4509-4518 (1998).
49. Tycowski, K.T., Shu, M.D. & Steitz, J.A. A mammalian gene with introns instead of exons generating stable RNA products. Nature 379, 464-466 (1996).
50. Ruiz-Echevarria, M.J., Czaplinski, K. & Peltz, S.W. Making sense of nonsense in yeast. Trends Biochem. Sci. 21, 433-438 (1996).
51. Hall, G.W. & Thein, S. Nonsense codon mutations in the terminal exon of the betaglobin gene are not associated with a reduction in beta-mRNA accumulation: a mechanism for the phenotype of dominant beta-thalassemia. Blood 83, 2031-2037 (1994).
52. Thein, S.L. et al. Molecular basis for dominantly inherited inclusion body beta-thalassemia. Proc. Natl. Acad. Sci. USA 87, 3924-3928 (1990).
53. Kugler, W., Enssle, J., Hentze, M.W. & Kulozik, A.E. Nuclear degradation of nonsense mutated beta-globin mRNA: a post-transcriptional mechanism to protect heterozygotes from severe clinical manifestations of beta-thalassemia? Nucleic Acids Res. 23, 413-418 (1995).
54. Jouanguy, E. et al. Interferon-gamma-receptor deficiency in an infant with fatal bacille Calmette-Guerin infection. N. Engl. J. Med. 335, 1956-1961 (1996).
55. Jouanguy, E. et al. A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection, Nat. Genet. 21, 370-378 (1999).
56. Schwabe, G.C. et al. Distinct mutations in the receptor tyrosine kinase gene ROR2 cause brachydactyly type B. Am. J. Hum. Genet. 67, 822-831. (2000).
57. Schneppenheim, R. et al. Expression and characterization of von Willebrand factor dimerization defects in different types of von Willebrand disease. Blood 97, 2059-2066 (2001).
58. Millar, D.S. et al. Molecular analysis of the genotype-phenotype relationship in factor X deficiency. Hum. Genet. 106, 249-257 (2000).
59. Rivolta, C., Berson, E.L. & Dryja, T.P. Dominant Leber congenital amaurosis, conerod degeneration, and retinitis pigmentosa caused by mutant versions of the transcription factor CRX. Hum. Mutat. 18, 488-498 (2001).
60. Rosenfeld, P.J. et al. A null mutation in the rhodopsin gene causes rod photoreceptor dysfunction and autosomal recessive retinitis pigmentosa. Nat. Genet. 1, 209-213 (1992).
61. Sung, C.H. et al. Rhodopsin mutations in autosomal dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. USA 88, 6481-6485 (1991).
62. Inoue, K. et al. Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat. Genet. 36, 361-369 (2004).
63. Perrin-Vidoz, L., Sinilnikova, O.M., Stoppa-Lyonnet, D., Lenoir, G.M. & Mazoyer, S. The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Hum. Mol. Genet. 11, 2805-2814 (2002).
64. Kawasaki, T. et al. mRNA and protein expression of p53 mutations in human bladder cancer cell lines. Cancer Lett. 82, 113-121 (1994).
65. Williams, C. et al. Assessment of sequence-based p53 gene analysis in human breast cancer: messenger RNA in comparison with genomic DNA targets. Clin. Chem. 44, 455-462 (1998).
66. Magnusson, K.P. et al. p53 splice acceptor site mutation and increased HsRAD51 protein expression in Bloom's syndrome GM1492 fibroblasts. Gene 246, 247-254 (2000).
67. Usuda, J. et al. Restoration of p53 gene function in 12-O- tetradecanoylphorbor 13-acetate-resistant human leukemia K562/TPA cells. Int. J. Oncol. 22, 81-86 (2003).
68. King-Underwood, L. & Pritchard-Jones, K. Wilms' tumor (WT1) gene mutations occur mainly in acute myeloid leukemia and may confer drug resistance. Blood 91, 2961-2981 (1998).
69. Fan, S. et al. Mutant BRCA1 genes antagonize phenotype of wild-type BRCA1. Oncogene 20, 8215-8235 (2001).
70. Sylvain, V., Lafarge, S. & Bignon, Y.J. Dominant-negative activity of a Brca1 truncation mutant: effects on proliferation, tumorigenicity in vivo, and chemosensitivity in a mouse ovarian cancer cell line. Int. J. Oncol. 20, 845-853 (2002).
71. Cardinali, M., Kratochvil, F.J., Ensley, J.F., Robbins, K.C. & Yeudall, W.A. Functional characterization in vivo of mutant p53 molecules derived from squamous cell carcinomas of the head and neck. Mol. Carcinog. 18, 78-88 (1997).
72. Reddy, J.C. et al. WT1-mediated transcriptional activation is inhibited by dominant negative mutant proteins. J. Biol. Chem. 270, 10878-10884 (1995).
73. Englert, C. et al. Truncated WT1 mutants alter the subnuclear localization of the wild-type protein. Proc. Natl. Acad. Sci. USA 92, 11960-11964 (1995).
74. Flaman, J.M. et al. The human tumour suppressor gene p53 is alternatively spliced in normal cells. Oncogene 12, 813-818 (1996).
75. Chow, V.T., Quek, H.H. & Tock, E.P. Alternative splicing of the p53 tumor suppressor gene in the Molt-4 T-lymphoblastic leukemia cell line. Cancer Lett. 73, 141-148 (1993).
76. King-Underwood, L., Renshaw, J. & Pritchard-Jones, K. Mutations in the Wilms' tumor gene WT1 in leukemias. Blood 87, 2171-2179 (1996).
77. Little, M.H. et al. Zinc finger point mutations within the WT1 gene in Wilms tumor patients. Proc. Natl. Acad. Sci. USA 89, 4791-4795 (1992).
78. Kohsaka, T. et al. Exon 9 mutations in the WT1 gene, without influencing KTS splice isoforms, are also responsible for Frasier syndrome. Hum. Mutat. 14, 466-470 (1999).
79. Barbaux, S. et al. Donor splice-site mutations in WT1 are responsible for Frasier syndrome. Nat. Genet. 17, 467-470 (1997).
80. Klamt, B. et al. Frasier syndrome is caused by defective alternative splicing of WT1 leading to an altered ratio of WT1 +/-KTS splice isoforms. Hum. Mol. Genet. 7, 709-714 (1998).
81. Eustice, D.C. & Wilhelm, J.M. Fidelity of the eukaryotic codon-anticodon interaction: interference by aminoglycoside antibiotics. Biochemistry 23, 1462-1467 (1984).
82. Zsembery, A. et al. Correction of CFTR malfunction and stimulation of Ca-activated CI channels restore HCO3- secretion in cystic fibrosis bile ductular cells. Hepatology 35, 95-104 (2002).
83. Bedwell, D.M. et al. Suppression of a CFTR premature stop mutation in a bronchial epithelial cell line. Nat. Med. 3, 1280-1284 (1997).
84. Keeling, K.M. et al. Gentamicin-mediated suppression of Hurler syndrome stop mutations restores a low level of alpha-L-iduronidase activity and reduces lysosomal glycosaminoglycan accumulation. Hum. Mol. Genet 10, 291-299 (2001).
85. Barton-Davis, E.R., Cordier, L., Shoturma, D.I., Leland, S.E. & Sweeney, H.L. Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J. Clin. Invest. 104, 375-381 (1999).
86. Du, M. et al. Aminoglycoside suppression of a premature stop mutation in a Cftr-/-mouse carrying a human CFTR-G542X transgene. J. Mol. Med. 80, 595-604 (2002).
87. Sangkuhl, K. et al. Aminoglycoside-mediated rescue of a disease-causing nonsense mutation in the V2 vasopressin receptor gene in vitro and in vivo. Hum. Mol. Genet. 13,893-903 (2004).
88. Dunant, P., Walter, M.C., Karpati, G. & Lochmuller, H. Gentamicin fails to increase dystrophin expression in dystrophin-deficient muscle. Muscle Nerve 27, 624-627 (2003).
89. Wilschanski, M. et al. Gentamicin-induced correction of CFTR function in patients with cystic fibrosis and CFTR stop mutations. N. Engl. J. Med. 349, 1433-1441 (2003).
90. Wilschanski, M. et al. A pilot study of the effect of gentamicin on nasal potential difference measurements in cystic fibrosis patients carrying stop mutations. Am. J. Respir. Crit. Care Med. 161, 860-865 (2000).
91. Clancy, J.P. et al. Evidence that systemic gentamicin suppresses premature stop mutations in patients with cystic fibrosis. Am. J. Respir. Crit. Care Med. 163, 1683-1692 (2001).
92. Wagner, K.R. et al. Gentamicin treatment of Duchenne and Becker muscular dystrophy due to nonsense mutations. Ann. Neurol. 49, 706-711 (2001).
93. Politano, L. et al. Gentamicin administration in Duchenne patients with premature stop codon. Preliminary results. Acta Myol. 22, 15-21 (2003).
94. Dominski, Z. & Kole, R. Restoration of correct splicing in thalassemic pre-mRNA by antisense oligonucleotides. Proc. Natl. Acad. Sci. USA 90, 8673-8677 (1993).
95. Mann, C.J. et al. Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse. Proc. Natl. Acad. Sci. USA 98, 42-47 (2001).
96. Lu, Q.L. et al. Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nat. Med. 9, 1009-1014 (2003).
97. Shibuya, T., Tange, T.O., Sonenberg, N. & Moore, M.J. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat. Struct. Mol. Biol. 11, 346-351 (2004).
98. Palacios, I.M., Gatfield, D., St Johnston, D. & Izaurralde, E. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427, 753-757 (2004).
99. Ferraiuolo, M.A. et al. A nuclear translation-like factor eIF4AIII is recruited to the mRNA during splicing and functions in nonsense-mediated decay. Proc. Natl. Acad. Sci. USA 101, 4118-4123 (2004).
100. Bono, F. et al. Molecular insights into the interaction of PYM with the Mago-Y14 core of the exon junction complex. EMBO Rep. 5, 304-310 (2004).