The RNA-binding protein Y14 inhibits mRNA decapping and modulates processing body formation

Molecular Biology of the Cell

Volumn 24, Issue 1, 2013, Pages 1-13

  Chuang, Tzu Wei ^a   Chang, Wei Lun ^a   Lee, Kuo Ming ^a   Tarn, Woan Yuh ^a  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

EXORIBONUCLEASE; HETERODIMER; INITIATION FACTOR 4A; MESSENGER RNA; PROTEIN; PROTEIN DCP2; RNA BINDING PROTEIN; RNA BINDING PROTEIN Y14; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; GENE OVEREXPRESSION; HALF LIFE TIME; MESSENGER RNA DECAPPING; PRIORITY JOURNAL; PROCESSING BODY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA CAPPING; RNA DEGRADATION; RNA METABOLISM; RNA SPLICING; RNA STRUCTURE;

BINDING SITES; ENDORIBONUCLEASES; EUKARYOTIC INITIATION FACTOR-4A; EXONS; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RNA CAPS; RNA INTERFERENCE; RNA SPLICING; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84871898471     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-03-0217     Document Type: Article

References (53)

1. Brengues M, Teixeira D, Parker R (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310, 486-489. (Pubitemid 41507961)
2. Chamieh H, Ballut L, Bonneau F, 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.
3. Chang WL, Tarn WY (2009). A role for transportin in deposition of TTP to cytoplasmic RNA granules and mRNA decay. Nucleic Acids Res 37, 6600-6612.
4. Cheng Z, Muhlrad D, Lim MK, Parker R, Song H (2007). Structural and functional insights into the human Upf1 helicase core. EMBO J 26, 253-264. (Pubitemid 46094716)
5. Chuang TW, Peng PJ, Tarn WY (2011). The exon junction complex component Y14 modulates the activity of the methylosome in biogenesis of spliceosomal small nuclear ribonucleoproteins. J Biol Chem 286, 8722-8728.
6. Coller J, Parker R (2005). General translational repression by activators of mRNA decapping. Cell 122, 875-886. (Pubitemid 41345205)
7. Cougot N, Babajko S, Seraphin B (2004). Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165, 31-40. (Pubitemid 38649174)
8. Dostie J, Dreyfuss G (2002). Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr Biol 12, 1060-1067. (Pubitemid 34766927)
9. Durand S, Cougot N, Mahuteau-Betzer F, Nguyen CH, Grierson DS, Bertrand E, Tazi J, 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. (Pubitemid 47480223)
10. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J (2005). Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell 20, 905-915. (Pubitemid 41814879)
11. Fischer N, Weis K (2002). The DEAD box protein Dhh1 stimulates the decapping enzyme Dcp1. EMBO J 21, 2788-2797. (Pubitemid 34619394)
12. Franks TM, Lykke-Andersen J (2007). TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev 21, 719-735. (Pubitemid 46440293)
13. Franks TM, Singh G, Lykke-Andersen J (2010). Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143, 938-950.
14. Fribourg S, Gatfield D, Izaurralde E, Conti E (2003). A novel mode of RBD-proGatfield D, Izaurralde E (2002). REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J Cell Biol 159, 579-588.
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. Harigaya Y, Jones BN, Muhlrad D, Gross JD, Parker R (2010). Identification and analysis of the interaction between Edc3 and Dcp2 in Saccharomyces cerevisiae. Mol Cell Biol 30, 1446-1456.
17. Hsu CL, Stevens A (1993). Yeast cells lacking 5′→3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 52 cap structure. Mol Cell Biol 13, 4826-4835. (Pubitemid 23220388)
18. Hsu IW, Hsu M, Li C, Chuang TW, Lin RI, Tarn WY (2005). Phosphorylation of Y14 modulates its interaction with proteins involved in mRNA metabolism and influences its methylation. J Biol Chem 280, 34507-34512. (Pubitemid 41504580)
19. Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW, Maquat LE (2008). Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133, 314-327. (Pubitemid 351508299)
20. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE (2008). Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J 27, 736-747. (Pubitemid 351506680)
21. Jiao X, Wang Z, Kiledjian M (2006). Identification of an mRNA-decapping regulator implicated in X-linked mental retardation. Mol Cell 24, 713-722. (Pubitemid 44839209)
22. 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. (Pubitemid 43200289)
23. Khanna R, Kiledjian M (2004). Poly(A)-binding-protein-mediated regulation of hDcp2 decapping in vitro. EMBO J 23, 1968-1976. (Pubitemid 38902075)
24. Kiriakidou M, Tan GS, Lamprinaki S, De Planell-Saguer M, Nelson PT, Mourelatos Z (2007). An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 129, 1141-1151. (Pubitemid 46891041)
25. Kshirsagar M, Parker R (2004). Identification of Edc3p as an enhancer of mRNA decapping in Saccharomyces cerevisiae. Genetics 166, 729-739. (Pubitemid 38391738)
26. Lai MC, Lee YH, Tarn WY (2008). The DEAD-box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well as tip-associated protein and participates in translational control. Mol Biol Cell 19, 3847-3858.
27. Larimer FW, Hsu CL, Maupin MK, Stevens A (1992). Characterization of the XRN1 gene encoding a 5′→3′ exoribonuclease: sequence data and analysis of disparate protein and mRNA levels of gene-disrupted yeast cells. Gene 120, 51-57.
28. Le Hir H, Gatfield D, Izaurralde E, Moore MJ (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. (Pubitemid 32848650)
29. 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)
30. Lee HC, Choe J, Chi SG, Kim YK (2009). Exon junction complex enhances translation of spliced mRNAs at multiple steps. Biochem Biophys Res Commun 384, 334-340.
31. Lee KM, Hsu W, Tarn WY (2010). TRAP150 activates pre-mRNA splicing and promotes nuclear mRNA degradation. Nucleic Acids Res 38, 3340-3350.
32. Li C, Lin RI, Lai MC, Ouyang P, Tarn WY (2003). Nuclear Pnn/DRS protein binds to spliced mRNPs and participates in mRNA processing and export via interaction with RNPS1. Mol Cell Biol 23, 7363-7376. (Pubitemid 37211015)
33. Li Y, Song MG, Kiledjian M (2008). Transcript-specific decapping and regulated stability by the human Dcp2 decapping protein. Mol Cell Biol 28, 939-948. (Pubitemid 351160050)
34. Lykke-Andersen J (2002). Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 22, 8114-8121.
35. Piccirillo C, Khanna R, Kiledjian M (2003). Functional characterization of the mammalian mRNA decapping enzyme hDcp2. RNA 9, 1138-1147. (Pubitemid 37093622)
36. Schwartz DC, Parker R (1999). Mutations in translation initiation factors lead to increased rates of deadenylation and decapping of mRNAs in Saccharomyces cerevisiae. Mol Cell Biol 19, 5247-5256. (Pubitemid 29339884)
37. Schwartz DC, Parker R (2000). mRNA decapping in yeast requires dissociation of the cap binding protein, eukaryotic translation initiation factor 4E. Mol Cell Biol 20, 7933-7942.
38. She M, Decker CJ, Sundramurthy K, Liu Y, Chen N, Parker R, Song H (2004). Crystal structure of Dcp1p and its functional implications in mRNA decapping. Nat Struct Mol Biol 11, 249-256. (Pubitemid 38282770)
39. She M, Decker CJ, Svergun DI, Round A, Chen N, Muhlrad D, Parker R, Song H (2008). Structural basis of dcp2 recognition and activation by dcp1. Mol Cell 29, 337-349. (Pubitemid 351222722)
40. Sheth U, Parker R (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300, 805-808. (Pubitemid 36532117)
41. Sheth U, Parker R (2006). Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125, 1095-1109. (Pubitemid 43866203)
42. Singh G, Jakob S, Kleedehn MG, Lykke-Andersen J (2007). Communication with the exon-junction complex and activation of nonsense-mediated decay by human Upf proteins occur in the cytoplasm. Mol Cell 27, 780-792. (Pubitemid 47333219)
43. Tange TO, Shibuya T, Jurica MS, Moore MJ (2005). Biochemical analysis of the EJC reveals two new factors and a stable tetrameric protein core. RNA 11, 1869-1883. (Pubitemid 41720036)
44. Teixeira D, Parker R (2007). Analysis of P-body assembly in Saccharomyces cerevisiae. Mol Biol Cell 18, 2274-2287. (Pubitemid 46911377)
45. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11, 371-382. (Pubitemid 40397171)
46. Tritschler F, Braun JE, Eulalio A, Truffault V, Izaurralde E, Weichenrieder O (2009). Structural basis for the mutually exclusive anchoring of P body components EDC3 and Tral to the DEAD box protein DDX6/Me31B. Mol Cell 33, 661-668.
47. Tritschler F, Eulalio A, Helms S, Schmidt S, Coles M, Weichenrieder O, Izaurralde E, Truffault V (2008). Similar modes of interaction enable Trailer Hitch and EDC3 to associate with DCP1 and Me31B in distinct protein complexes. Mol Cell Biol 28, 6695-6708.
48. Tritschler F, Eulalio A, Truffault V, Hartmann MD, Helms S, Schmidt S, Coles M, Izaurralde E, Weichenrieder O (2007). A divergent Sm fold in EDC3 proteins mediates DCP1 binding and P-body targeting. Mol Cell Biol 27, 8600-8611.
49. van Dijk E, Cougot N, Meyer S, Babajko S, Wahle E, Seraphin B (2002). Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 21, 6915-6924. (Pubitemid 36014563)
50. Vilela C, Velasco C, Ptushkina M, McCarthy JE (2000). The eukaryotic mRNA decapping protein Dcp1 interacts physically and functionally with the eIF4F translation initiation complex. EMBO J 19, 4372-4382. (Pubitemid 30623748)
51. Wang Z, Jiao X, Carr-Schmid A, Kiledjian M (2002). The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc Natl Acad Sci USA 99, 12663-12668.
52. Yu JH, Yang WH, Gulick T, Bloch KD, Bloch DB (2005). Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA 11, 1795-1802. (Pubitemid 41720029)
53. Zhang S, Williams CJ, Wormington M, Stevens A, Peltz SW (1999). Monitoring mRNA decapping activity. Methods 17, 46-51. (Pubitemid 29440546)