SMG6 interacts with the exon junction complex via two conserved EJC-binding motifs (EBMs) required for nonsense-mediated mRNA decay

Genes and Development

Volumn 24, Issue 21, 2010, Pages 2440-2450

  Kashima, Isao ^a   Jonas, Stefanie ^a   Jayachandran, Uma ^b   Buchwald, Gretel ^b   Conti, Elena ^b   Lupas, Andrei N ^a   Izaurralde, Elisa ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Exon junction complex; MRNA decay; NMD; UPF1

Indexed keywords

CELL PROTEIN; ENDONUCLEASE; MESSENGER RNA; PROTEIN SMG6; PROTEIN UPF3B; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EXON; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; STOP CODON;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CODON, NONSENSE; EXONS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RNA INTERFERENCE; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TELOMERASE;

VERTEBRATA;

EID: 78049447110     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.604610     Document Type: Article

References (38)

1. Anders KR, Grimson A, Anderson P. 2003. SMG-5, required for C. elegans nonsense-mediated mRNA decay, associates with SMG-2 and protein phosphatase 2A. EMBO J 22: 641-650.
2. Ballut L, Marchadier B, Baguet A, Tomasetto C, Séraphin B, 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. (Pubitemid 41486709)
3. Biegert A, Mayer C, Remmert M, Söding J, Lupas AN. 2006. The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34: W335-W339. doi: 10.1093/nar/gkl217.
4. Bono F, Ebert J, Lorentzen E, Conti E. 2006. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126: 713-725. (Pubitemid 44233638)
5. Buchwald G, Ebert J, Basquin C, Sauliere J, Jayachandran U, Bono F, Le Hir H, Conti E. 2010. Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC- UPF3b complex. Proc Natl Acad Sci 107: 10050-10055.
6. Cali BM, Kuchma SL, Latham J, Anderson P. 1999. smg-7 is required for mRNA surveillance in Caenorhabditis elegans. Genetics 151: 605-616. (Pubitemid 29082930)
7. Chan WK, Huang L, Gudikote JP, Chang YF, Imam JS, MacLean JA II, Wilkinson MF. 2007. An alternative branch of the nonsense-mediated decay pathway. EMBO J 26: 1820-1830. (Pubitemid 46624044)
8. Chang Y, Imam JS, Wilkinson MF. 2007. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76: 51-74.
9. Chiu SY, Serin G, Ohara O, Maquat LE. 2003. 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.
10. Czaplinski K, Ruiz-Echevarria MJ, Paushkin SV, Han X, Weng Y, Perlick HA, Dietz HC, Ter-Avanesyan MD, Peltz SW. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes & Dev 12: 1665-1677. (Pubitemid 28299517)
11. Denning G, Jamieson L, Maquat LE, Thompson EA, Fields AP. 2001. Cloning of a novel phosphatidylinositol kinase-related kinase: Characterization of the human SMG-1 RNA surveillance protein. J Biol Chem 276: 22709-22714.
12. Eberle AB, Lykke-Andersen S, Mühlemann O, Jensen TH. 2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16: 49-55.
13. Fukuhara N, Ebert J, Unterholzner L, Lindner D, Izaurralde E, Conti E. 2005. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol Cell 18: 537-547. (Pubitemid 40269118)
14. Gatfield D, Izaurralde E. 2004. Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429: 575-578. (Pubitemid 38737663)
15. Gehring NH, Neu-Yilik G, Schell T, Hentze MW, Kulozik AE. 2003. Y14 and hUpf3b form an NMD-activating complex. Mol Cell 11: 939-949. (Pubitemid 36566316)
16. Glavan F, Behm-Ansmant I, Izaurralde E, Conti E. 2006. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 25: 5117-5125.
17. Goulet I, Boisvenue S, Mokas S, Mazroui R, Côté J. 2008. TDRD3, a novel Tudor domain-containing protein, localizes to cytoplasmic stress granules. Hum Mol Genet 17: 3055-3074.
18. Huntzinger E, Kashima I, Fauser M, Saulière J, Izaurralde E. 2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoa. RNA 14: 2609-2617.
19. Isken O, Maquat LE. 2007. Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function. Genes & Dev 21: 1833-1856.
20. Kashima I, Yamashita A, Izumi N, Kataoka N, Morishita R, Hoshino S, Ohno M, Dreyfuss G, 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.
21. Kunz JB, Neu-Yilik G, Hentze MW, Kulozik AE, Gehring NH. 2006. Functions of hUpf3a and hUpf3b in nonsense-mediated mRNA decay and translation. RNA 12: 1015-1022. (Pubitemid 43788120)
22. Le Hir H, Izaurralde E, Maquat LE, Moore MJ. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 19: 6860-6869. (Pubitemid 32011679)
23. Linder B, Plöttner O, Kroiss M, Hartmann E, Laggerbauer B, Meister G, Keidel E, Fischer U. 2008. Tdrd3 is a novel stress granule-associated protein interacting with the Fragile-X syndrome protein FMRP. Hum Mol Genet 17: 3236-3246.
24. Nagy E, Maquat LE. 1998. A rule for termination-codon position within intron-containing genes: When nonsense affects RNA abundance. Trends Biochem Sci 23: 198-199. (Pubitemid 28302613)
25. Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, 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.
26. Oeffinger M, Dlakic M, Tollervey D. 2004. A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes & Dev 18: 196-209. (Pubitemid 38141787)
27. Ohnishi T, Yamashita A, Kashima I, Schell T, Anders KR, Grimson A, Hachiya T, Hentze MW, Anderson P, Ohno S. 2003. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol Cell 12: 1187-1200.
28. Page MF, Carr B, Anders KR, Grimson A, Anderson P. 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. (Pubitemid 29399299)
29. Pal M, Ishigaki Y, Nagy E, Maquat LE. 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. (Pubitemid 32381924)
30. Rebbapragada I, Lykke-Andersen J. 2009. Execution of nonsense-mediated mRNA decay: What defines a substrate. Curr Opin Cell Biol 21: 394-402.
31. Schuler GD, Altschul SF, Lipman DJ. 1991. A workbench for multiple alignment construction and analysis. Proteins 9: 180-190.
32. Studier WF. 2005. Protein production by auto-induction in high-density shaking cultures. Protein Expr Purif 1: 207-234.
33. Thermann R, Neu-Yilik G, Deters A, Frede U, Wehr K, Hagemeier C, Hentze MW, Kulozik AE. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J 17: 3484-3494. (Pubitemid 28279521)
34. Unterholzner L, Izaurralde E. 2004. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol Cell 16: 587-596.
35. Wang J, Vock VM, Li S, Olivas OR, Wilkinson MF. 2002. A quality control pathway that down-regulates aberrant T-cell receptor (TCR) transcripts by a mechanism requiring UPF2 and translation. J Biol Chem 277: 18489-18493.
36. Wittkopp N, Huntzinger E, Weiler C, Saulière J, Schmidt S, Sonawane M, Izaurralde E. 2009. Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol Cell Biol 29: 3517-3528.
37. Wittmann J, Hol EM, Jäck H-M. 2006. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 26: 1272-1287.
38. Yamashita A, Ohnishi T, Kashima I, Taya Y, 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.