Nonsense-Mediated mRNA Decay Effectors Are Essential for Zebrafish Embryonic Development and Survival

REFERENCES

• Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402.
   PubMed Web of Science ®Google Scholar
• Amrani, N., R. Ganesan, S. Kervestin, D. A. Mangus, S. Ghosh, and A. Jacobson. 2004. A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432:112–118.
   PubMed Web of Science ®Google Scholar
• Amrani, N., M. S. Sachs, and A. Jacobson. 2006. Early nonsense: mRNA decay solves a translational problem. Nat. Rev. Mol. Cell Biol. 7:415–425.
   PubMed Web of Science ®Google Scholar
• Anders, K. R., A. Grimson, and P. Anderson. 2003. SMG-5, required for C. elegans nonsense-mediated mRNA decay, associates with SMG-2 and protein phosphatase 2A. EMBO J. 22:641–650.
   PubMedGoogle Scholar
• Arciga-Reyes, L., L. Wootton, M. Kieffer, and B. Davies. 2006. UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J. 47:480–489.
   PubMedGoogle Scholar
• Azzalin, C. M., and J. Lingner. 2006. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol. 16:433–439.
   PubMedGoogle Scholar
• Behm-Ansmant, I., D. Gatfield, J. Rehwinkel, V. Hilgers, and E. Izaurralde. 2007. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J. 26:1591–1601.
   PubMed Web of Science ®Google Scholar
• Behm-Ansmant, I., and E. Izaurralde. 2006. Quality control of gene expression, a stepwise assembly pathway for the surveillance complex that triggers nonsense-mediated mRNA decay. Genes Dev. 20:391–398.
   PubMed Web of Science ®Google Scholar
• Carter, M. S., J. Doskow, P. Morris, S. Li, R. P. Nhim, S. Sandstedt, and M. F. Wilkinson. 1995. A regulatory mechanism that detects premature nonsense codons in T-cell receptor transcripts in vivo is reversed by protein synthesis inhibitors in vitro. J. Biol. Chem. 270:28995–29003.
   PubMed Web of Science ®Google Scholar
• Chan, W. K., L. Huang, J. P. Gudikote, Y. F. Chang, J. S. Imam, J. A. MacLean, and M. F. Wilkinson. 2007. An alternative branch of the nonsense-mediated decay pathway. EMBO J. 26:1820–1830.
   PubMed Web of Science ®Google Scholar
• Chiu, S. Y., G. Serin, O. Ohara, and L. E. Maquat. 2003. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 1:77–87.
   Google Scholar
• Conti, E., and E. Izaurralde. 2005. Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species. Curr. Opin. Cell Biol. 17:316–325.
   PubMedGoogle Scholar
• Denning, G., L. Jamieson, L. E. Maquat, E. A. Thompson, and A. P. Fields. 2001. Cloning of a novel phosphatidylinositol kinase-related kinase: characterization of the human SMG-1 RNA surveillance protein. J. Biol. Chem. 276:22709–22714.
   PubMed Web of Science ®Google Scholar
• Eberle, A. B., S. Lykke-Andersen, O. Mühlemann, and T. H. Jensen. 2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16:49–55.
   PubMed Web of Science ®Google Scholar
• Eberle, A. B., L. Stalder, H. Mathys, R. Z. Orozco, and O. Mühlemann. 2008. Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol. 6:e92.
   PubMed Web of Science ®Google Scholar
• Fukuhara, N., J. Ebert, L. Unterholzner, D. Lindner, E. Izaurralde, and E. Conti. 2005. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell 18:537–547.
   Google Scholar
• Gatfield, D., L. Unterholzner, F. D. Ciccarelli, P. Bork, and E. Izaurralde. 2003. Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J. 22:3960–3970.
   PubMed Web of Science ®Google Scholar
• Gehring, N. H., J. B. Kunz, G. Neu-Yilik, S. Breit, M. H. Viegas, M. W. Hentze, and A. E. Kulozik. 2005. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell 20:65–75.
   PubMed Web of Science ®Google Scholar
• Glavan, F., I. Behm-Ansmant, E. Izaurralde, and E. Conti. 2006. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25:5117–5125.
   PubMedGoogle Scholar
• Grimson, A., S. O'Connor, C. L. Newman, and P. Anderson. 2004. SMG-1 is a phosphatidylinositol kinase-related protein kinase required for nonsense-mediated mRNA decay in Caenorhabditis elegans. Mol. Cell. Biol. 17:7483–7490.
   Google Scholar
• Hodgkin, J., A. Papp, R. Pulak, V. Ambros, and P. Anderson. 1989. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123:301–313.
   PubMed Web of Science ®Google Scholar
• Hori, K., and Y. Watanabe. 2007. Context analysis of termination codons in mRNA that are recognized by plant NMD. Plant Cell Physiol. 48:1072–1078.
   PubMedGoogle Scholar
• Hori, K., and Y. Watanabe. 2005. UPF3 suppresses aberrant spliced mRNA in Arabidopsis. Plant J. 43:530–540.
   PubMedGoogle Scholar
• Huntzinger, E., I. Kashima, M. Fauser, J. Saulière, and E. Izaurralde. 2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoa. RNA 14:2609–2617.
   PubMed Web of Science ®Google Scholar
• Isken, O., and L. E. Maquat. 5 August 2008. The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat. Rev. Genet. 9:699–712.
   PubMed Web of Science ®Google Scholar
• Kashima, I., A. Yamashita, N. Izumi, N. Kataoka, R. Morishita, S. Hoshino, M. Ohno, G. Dreyfuss, and S. Ohno. 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.
   PubMed Web of Science ®Google Scholar
• Kerényi, Z., Z. Mérai, L. Hiripi, A. Benkovics, P Gyula, C. Lacomme, E. Barta, F. Nagy, and D. Silhavy. 2008. Inter-kingdom conservation of mechanism of nonsense-mediated mRNA decay. EMBO J. 27:1585–1595.
   PubMed Web of Science ®Google Scholar
• Kertesz, S., Z. Kerenyi, Z. Merai, I. Bartos, T. Palfy, E. Barta, and D. Silhavy. 2006. Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Res. 34:6147–6157.
   PubMedGoogle Scholar
• Kimmel, C. B., W. W. Ballard, S. R. Kimmel, R. Ullmann, and T. F. Schilling. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:253–310.
   PubMed Web of Science ®Google Scholar
• Kunz, J. B., G. Neu-Yilik, M. W. Hentze, A. E. Kulozik, and N. H. Gehring. 2006. Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA 12:1015–1022.
   PubMed Web of Science ®Google Scholar
• Lamason, R. L., M. A. Mohideen, J. R. Mest, A. C. Wong, H. L. Norton, M. C. Aros, M. J. Jurynec, X. Mao, V. R. Humphreville, J. E. Humbert, et al. 2005. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310:1782–1786.
   PubMed Web of Science ®Google Scholar
• Le Hir, H., E. Izaurralde, L. E. Maquat, and M. J. Moore. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19:6860–6869.
   PubMed Web of Science ®Google Scholar
• Lejeune, F., and L. E. Maquat. 2005. Mechanistic links between nonsense-mediated mRNA decay and pre-mRNA splicing in mammalian cells. Curr. Opin. Cell Biol. 17:309–315.
   PubMed Web of Science ®Google Scholar
• Li, S., and M. F. Wilkinson. 1998. Nonsense surveillance in lymphocytes? Immunity 8:135–141.
   PubMedGoogle Scholar
• Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408.
   PubMed Web of Science ®Google Scholar
• Longman, D., R. H. Plasterk, I. L. Johnstone, and J. F. Caceres. 2007. Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev. 21:1075–1085.
   PubMed Web of Science ®Google Scholar
• Medghalchi, S. M., P. A. Frischmeyer, J. T. Mendell, A. G. Kelly, A. M. Lawler, and H. C. Dietz. 2001. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10:99–105.
   PubMedGoogle Scholar
• Metzstein, M. M., and M. A. Krasnow. 2006. Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet. 2:e180.
   PubMed Web of Science ®Google Scholar
• Nagy, E., and L. E. Maquat. 1998. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23:198–199.
   PubMed Web of Science ®Google Scholar
• Ohnishi, T., A. Yamashita, I. Kashima, T. Schell, K. R. Anders, A. Grimson, T. Hachiya, M. W. Hentze, P. Anderson, and S. Ohno. 2003. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell 12:1187–1200.
   PubMed Web of Science ®Google Scholar
• Page, M. F., B. Carr, K. R. Anders, A. Grimson, and P. Anderson. 1999. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19:5943–5951.
   PubMed Web of Science ®Google Scholar
• Pal, M., Y. Ishigaki, E. Nagy, and L. E. Maquat. 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.
   PubMedGoogle Scholar
• Rehwinkel, J., I. Letunic, J. Raes, P. Bork, and E. Izaurralde. 2005. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11:1530–1544.
   PubMed Web of Science ®Google Scholar
• Rehwinkel, J., J. Raes, and E. Izaurralde. 2006. Nonsense-mediated mRNA decay: target genes and functional diversification of effectors. Trends Biochem. Sci. 31:639–646.
   PubMedGoogle Scholar
• Riehs, N., S. Akimcheva, J. Puizina, P. Bulankova, R. A. Idol, J. Siroky, A. Schleiffer, D. Schweizer, D. E. Shippen, and K. Riha. 2008. Arabidopsis SMG7 protein is required for exit from meiosis. J. Cell Sci. 121:2208–2216.
   PubMedGoogle Scholar
• Robu, M. E., J. D. Larson, A. Nasevicius, S. Beiraghi, C. Brenner, S. A. Farber, and S. C. Ekker. 2007. p53 activation by knockdown technologies. PLoS Genet. 3:c78.
   PubMed Web of Science ®Google Scholar
• Schulte-Merker, S., R. K. Ho, B. G. Herrmann, and C. Nüsslein-Volhard. 1992. The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116:1021–1032.
   PubMedGoogle Scholar
• Schwartz, A. M., T. V. Komarova, M. V. Skulachev, A. S. Zvereva, I. L. Dorokhov, and J. G. Atabekov. 2006. Stability of plant mRNAs depends on the length of the 3′-untranslated region. Biochemistry (Moscow) 71:1377–1384.
   PubMedGoogle Scholar
• Singh, G., I. Rebbapragada, and J. Lykke-Andersen. 2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6:e111.
   PubMed Web of Science ®Google Scholar
• Unterholzner, L., and E. Izaurralde. 2004. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16:587–596.
   PubMed Web of Science ®Google Scholar
• Weischenfeldt, J., I. Damgaard, D. Bryder, K. Theilgaard-Mönch, L. A. Thoren, F. C. Nielsen, S. E. Jacobsen, C. Nerlov, and B. T. Porse. 2008. NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev. 22:1381–1396.
   PubMedGoogle Scholar
• Wu, J., J. H. Kang, C. Hettenhausen, and I. T. Baldwin. 2007. Nonsense-mediated mRNA decay (NMD) silences the accumulation of aberrant trypsin proteinase inhibitor mRNA in Nicotiana attenuata. Plant J. 51:693–706.
   PubMedGoogle Scholar
• Yamashita, A., T. Ohnishi, I. Kashima, Y. Taya, and S. Ohno. 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.
   PubMed Web of Science ®Google Scholar
• Yoine, M., T. Nishii, and K. Nakamura. 2006. Arabidopsis UPF1 RNA helicase for nonsense-mediated mRNA decay is involved in seed size control and is essential for growth. Plant Cell Physiol. 47:572–580.
   PubMedGoogle Scholar