The interaction of cytoplasmic poly(A)-binding protein with eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay

RNA

Volumn 20, Issue 10, 2014, Pages 1579-1592

  Fatscher, Tobias ^a   Boehm, Volker ^a   Weiche, Benjamin ^a   Gehring, Niels H ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

EIF4G; NMD; PABPC1; Ribosome recycling; Translation termination

Indexed keywords

CYTOPLASM PROTEIN; INITIATION FACTOR 4G; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; EIF4G1 PROTEIN, HUMAN; PEPTIDE-CHAIN-RELEASE FACTOR 3; POLYADENYLIC ACID; STOP CODON; TRANSLATION TERMINATION FACTOR;

3' UNTRANSLATED REGION; ARTICLE; CODON; EXON; GENE EXPRESSION; NONSENSE MEDIATED MRNA DECAY; PROTEIN PROTEIN INTERACTION; RNA DEGRADATION; CHEMISTRY; CYTOPLASM; GENETICS; HELA CELL LINE; HUMAN; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; NORTHERN BLOTTING; PROTEIN SYNTHESIS; RIBOSOME; STOP CODON;

BLOTTING, NORTHERN; CODON, NONSENSE; CYTOPLASM; EUKARYOTIC INITIATION FACTOR-4G; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NONSENSE MEDIATED MRNA DECAY; PEPTIDE TERMINATION FACTORS; POLY A; POLY(A)-BINDING PROTEIN I; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER;

EID: 84907189359     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.044933.114     Document Type: Article

References (50)

1. Amrani N, Ganesan R, Kervestin S, Mangus DA, Ghosh S, Jacobson A. 2004. A faux 3'-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432: 112-118.
2. Amrani N, Ghosh S, Mangus DA, Jacobson A. 2008. Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453: 1276-1280.
3. Behm-Ansmant I, Gatfield D, Rehwinkel J, Hilgers V, Izaurralde E. 2007. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J 26: 1591-1601.
4. Bhuvanagiri M, Schlitter AM, Hentze MW, Kulozik AE. 2010. NMD: RNA biology meets human genetic medicine. Biochem J 430: 365-377.
5. Burgess HM, Richardson WA, Anderson RC, Salaun C, Graham SV, Gray NK. 2011. Nuclear relocalisation of cytoplasmic poly(A)-binding proteins PABP1 and PABP4 in response to UV irradiation reveals mRNA-dependent export of metazoan PABPs. J Cell Sci 124: 3344-3355.
6. Chang YF, Imam JS, Wilkinson MF. 2007. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76: 51-74.
7. Chauvin C, Salhi S, Le Goff C, Viranaicken W, Diop D, Jean-Jean O. 2005. Involvement of human release factors eRF3a and eRF3b in translation termination and regulation of the termination complex formation. Mol Cell Biol 25: 5801-5811.
8. Clerici M, Deniaud A, Boehm V, Gehring NH, Schaffitzel C, Cusack S. 2013. Structural and functional analysis of the three MIF4G domains of nonsense-mediated decay factor UPF2. Nucleic Acids Res 42: 2673-2686.
9. Durand S, Lykke-Andersen J. 2013. Nonsense-mediated mRNA decay occurs during eIF4F-dependent translation in human cells. Nat Struct Mol Biol 20: 702-709.
10. Eberle AB, Stalder L, Mathys H, Orozco RZ, Muhlemann O. 2008. Posttranscriptional gene regulation by spatial rearrangement of the 3' untranslated region. PLoS Biol 6: e92.
11. Eberle AB, Lykke-Andersen S, Muhlemann O, Jensen TH. 2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16: 49-55.
12. Gatfield D, Unterholzner L, Ciccarelli FD, Bork P, Izaurralde E. 2003. Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J 22: 3960-3970.
13. Gehring NH, Kunz JB, Neu-Yilik G, Breit S, Viegas MH, Hentze MW, Kulozik AE. 2005. Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol Cell 20: 65-75.
14. Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW. 2009. Disassembly of exon junction complexes by PYM. Cell 137: 536-548.
15. 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.
16. Hoshino S, Imai M, Kobayashi T, Uchida N, Katada T. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3'-poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J Biol Chem 274: 16677-16680.
17. Hundsdoerfer P, Thoma C, Hentze MW. 2005. Eukaryotic translation initiation factor 4GI and p97 promote cellular internal ribosome entry sequence-driven translation. Proc Natl Acad Sci 102: 13421-13426.
18. Huntzinger E, Kashima I, Fauser M, Sauliere J, Izaurralde E. 2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14: 2609-2617.
19. Hwang J, Maquat LE. 2011. Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: To die or not to die, that is the question. Curr Opin Genet Dev 21: 422-430.
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.
21. Jackson RJ, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
22. Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN, Sonenberg N. 2005. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev 19: 104-113.
23. 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.
24. Kervestin S, Jacobson A. 2012. NMD: a multifaceted response to premature translational termination. Nat Rev Mol Cell Biol 13: 700-712.
25. Kononenko AV, Mitkevich VA, Atkinson GC, Tenson T, Dubovaya VI, Frolova LY, Makarov AA, Hauryliuk V. 2010. GTP-dependent structural rearrangement of the eRF1:eRF3 complex and eRF3 sequence motifs essential for PABP binding. Nucleic Acids Res 38: 548-558.
26. Kozlov G, Gehring K. 2010. Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein. PLoS One 5: e10169.
27. Kozlov G, De Crescenzo G, Lim NS, Siddiqui N, Fantus D, Kahvejian A, Trempe JF, Elias D, Ekiel I, Sonenberg N, et al. 2004. Structural basis of ligand recognition by PABC, a highly specific peptide-binding domain found in poly(A)-binding protein and a HECT ubiquitin ligase. EMBO J 23: 272-281.
28. Loh B, Jonas S, Izaurralde E. 2013. The SMG5-SMG7 heterodimer directly recruits the CCR4-NOT deadenylase complex to mRNAs containing nonsense codons via interaction with POP2. Genes Dev 27: 2125-2138.
29. Mendell JT, ap Rhys CM, Dietz HC. 2002. Separable roles for rent1/ hUpf1 in altered splicing and decay of nonsense transcripts. Science 298: 419-422.
30. Min EE, Roy B, Amrani N, He F, Jacobson A. 2013. Yeast Upf1 CH domain interacts with Rps26 of the 40S ribosomal subunit. RNA 19: 1105-1115.
31. Nicholson P, Muhlemann O. 2010. Cutting the nonsense: the degradation of PTC-containing mRNAs. Biochem Soc Trans 38: 1615-1620.
32. Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, Muhlemann 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.
33. Okada-Katsuhata Y, Yamashita A, Kutsuzawa K, Izumi N, Hirahara F, Ohno S. 2012. N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res 40: 1251-1266.
34. Osawa M, Hosoda N, Nakanishi T, Uchida N, Kimura T, Imai S, Machiyama A, Katada T, Hoshino S, Shimada I. 2012. Biological role of the two overlapping poly(A)-binding protein interacting motifs 2 (PAM2) of eukaryotic releasing factor eRF3 in mRNA decay. RNA 18: 1957-1967.
35. Rebbapragada I, Lykke-Andersen J. 2009. Execution of nonsense-mediated mRNA decay: What defines a substrate? Curr Opin Cell Biol 21: 394-402.
36. Rufener SC, Muhlemann O. 2013. eIF4E-bound mRNPs are substrates for nonsense-mediated mRNA decay in mammalian cells. Nat Struct Mol Biol 20: 710-717.
37. Safaee N, Kozlov G, Noronha AM, Xie J, Wilds CJ, Gehring K. 2012. Interdomain allostery promotes assembly of the poly(A) mRNA complex with PABP and eIF4G. Mol Cell 48: 375-386.
38. Sauliere J, Murigneux V, Wang Z, Marquenet E, Barbosa I, Le Tonqueze O, Audic Y, Paillard L, Roest Crollius H, Le Hir H. 2012. CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat Struct Mol Biol 19: 1124-1131.
39. Schweingruber C, Rufener SC, Zund D, Yamashita A, Muhlemann O. 2013. Nonsense-mediated mRNA decay-mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 1829: 612-623.
40. Silva AL, Ribeiro P, Inacio A, Liebhaber SA, Romao L. 2008. Proximity of the poly(A)-binding protein to a premature termination codon inhibits mammalian nonsense-mediated mRNA decay. RNA 14: 563-576.
41. Singh G, Rebbapragada I, Lykke-Andersen J. 2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 6: e111.
42. Singh G, Kucukural A, Cenik C, Leszyk JD, Shaffer SA, Weng Z, Moore MJ. 2012. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151: 750-764.
43. Steckelberg AL, Boehm V, Gromadzka AM, Gehring NH. 2012. CWC22 connects pre-mRNA splicing and exon junction complex assembly. Cell Rep 2: 454-461.
44. Tani H, Imamachi N, Salam KA, Mizutani R, Ijiri K, Irie T, Yada T, Suzuki Y, Akimitsu N. 2012. Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol 9: 1370-1379.
45. Thermann R, Neu-Yilik G, Deters A, Frede U, Wehr K, Hagemeier C, HentzeMW, Kulozik AE. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J 17: 3484-3494.
46. Uchida N, Hoshino S, Imataka H, Sonenberg N, Katada T. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in cap/poly(A)-dependent translation. J Biol Chem 277: 50286-50292.
47. Wakiyama M, Imataka H, Sonenberg N. 2000. Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr Biol 10: 1147-1150.
48. Wells SE, Hillner PE, Vale RD, Sachs AB. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2: 135-140.
49. Yepiskoposyan H, Aeschimann F, Nilsson D, Okoniewski M, Muhlemann O. 2011. Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17: 2108-2118.
50. Zhang J, Sun X, Qian Y, Maquat LE. 1998. Intron function in the nonsense- mediated decay of β-globin mRNA: indications that premRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 4: 801-815.