Eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay by two genetically separable mechanisms

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Joncourt, Raphael ^a   Eberle, Andrea B ^a,b   Rufener, Simone C ^a   Mühlemann, Oliver ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4G; POLYADENYLIC ACID BINDING PROTEIN; DNA BINDING PROTEIN; ELF3 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN SUBUNIT; RIBONUCLEOSIDE DIPHOSPHATE REDUCTASE; RIBONUCLEOTIDE REDUCTASE M2; RRM1 PROTEIN, HUMAN; STOP CODON; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS; TUMOR SUPPRESSOR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME MECHANISM; HUMAN; HUMAN CELL; NONSENSE MEDIATED MRNA DECAY; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION; TRANSLATION INITIATION; TRANSLATION TERMINATION; CHEMISTRY; GENE EXPRESSION REGULATION; METABOLISM; PROTEIN DOMAIN; PROTEIN SUBUNIT; STOP CODON;

CODON, NONSENSE; DNA-BINDING PROTEINS; EUKARYOTIC INITIATION FACTOR-4G; GENE EXPRESSION REGULATION; HUMANS; NONSENSE MEDIATED MRNA DECAY; POLY(A)-BINDING PROTEIN I; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-ETS; RIBONUCLEOSIDE DIPHOSPHATE REDUCTASE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84929054432     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104391     Document Type: Article

References (80)

1. He F, Li X, Spatrick P, Casillo R, Dong S, et al. (2003) Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol Cell 12: 1439-1452. (Pubitemid 38037013)
2. Hurt JA, Robertson AD, Burge CB (2013) Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res 23: 1636-1650.
3. Mendell JT, Sharifi NA, Meyers JL, Martinez-Murillo F, Dietz HC (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat Genet 36: 1073-1078. (Pubitemid 41184468)
4. Tani H, Imamachi N, Salam KA, Mizutani R, Ijiri K, et al. (2012) Identification of hundreds of novel UPF1 target transcripts by direct determination of whole transcriptome stability. RNA Biol 9: 1370-1379.
5. Rehwinkel J, Letunic I, Raes J, Bork P, Izaurralde E (2005) Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11: 1530-1544. (Pubitemid 41396923)
6. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Monch K, Thoren LA, et al. (2008) NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev 22: 1381-1396. (Pubitemid 351717528)
7. Wittmann J, Hol EM, Jack HM (2006) hUPF2 Silencing Identifies Physiologic Substrates of Mammalian Nonsense-Mediated mRNA Decay. Mol Cell Biol 26: 1272-1287. (Pubitemid 43202555)
8. Zund D, Gruber AR, Zavolan M, Muhlemann O (2013) Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3′ UTRs. Nat Struct Mol Biol 20: 936-943.
9. 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.
10. McIlwain DR, Pan Q, Reilly PT, Elia AJ, McCracken S, et al. (2010) Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc Natl Acad Sci U S A 107: 12186-12191.
11. Medghalchi SM, Frischmeyer PA, Mendell JT, Kelly AG, Lawler AM, et al. (2001) Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum Mol Genet 10: 99-105. (Pubitemid 32098119)
12. Frischmeyer PA, Dietz HC (1999) Nonsense-mediated mRNA decay in health and disease. Hum Mol Genet 8: 1893-1900. (Pubitemid 29458667)
13. Khajavi M, Inoue K, Lupski JR (2006) Nonsense-mediated mRNA decay modulates clinical outcome of genetic disease. Eur J Hum Genet 14: 1074-1081. (Pubitemid 44463965)
14. Peixeiro I, Inacio A, Barbosa C, Silva AL, Liebhaber SA, et al. (2011) Interaction of PABPC1 with the translation initiation complex is critical to the NMD resistance of AUG-proximal nonsense mutations. Nucleic Acids Res 40: 1160-1173.
15. Amrani N, Ganesan R, Kervestin S, Mangus DA, Ghosh S, et al. (2004) A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432: 112-118. (Pubitemid 39490837)
16. 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.
17. 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.
18. 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.
19. 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.
20. Cho H, Kim KM, Kim YK (2009) Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol Cell 33: 75-86.
21. 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. (Pubitemid 46480926)
22. 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.
23. 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)
24. 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. (Pubitemid 351397821)
25. 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.
26. Cosson B, Berkova N, Couturier A, Chabelskaya S, Philippe M, et al. (2002) Poly(A)-binding protein and eRF3 are associated in vivo in human and Xenopus cells. Biol Cell 94: 205-216. (Pubitemid 35363818)
27. 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.
28. Kozlov G, Gehring K (2010) Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein. PLoS One 5: e10169.
29. Czaplinski K, Ruiz-Echevarria MJ, Paushkin SV, Han X, Weng Y, et al. (1998) The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev 12: 1665-1677. (Pubitemid 28299517)
30. Kashima I, Yamashita A, Izumi N, Kataoka N, Morishita R, et al. (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)
31. Muhlemann O, Jensen TH (2012) mRNP quality control goes regulatory. Trends Genet 28: 70-77.
32. Kervestin S, Li C, Buckingham R, Jacobson A (2012) Testing the faux-UTR model for NMD: Analysis of Upf1p and Pab1p competition for binding to eRF3/Sup35p. Biochimie 94: 1560-1571.
33. Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272: 2118-2131. (Pubitemid 40655326)
34. Kuhn U, Pieler T (1996) Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction. J Mol Biol 256: 20-30. (Pubitemid 26104207)
35. Deo RC, Bonanno JB, Sonenberg N, Burley SK (1999) Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98: 835-845. (Pubitemid 29446900)
36. Karim MM, Svitkin YV, Kahvejian A, De Crescenzo G, Costa-Mattioli M, et al. (2006) A mechanism of translational repression by competition of Paip2 with eIF4G for poly(A) binding protein (PABP) binding. Proc Natl Acad Sci U S A 103: 9494-9499. (Pubitemid 43955853)
37. Imataka H, Gradi A, Sonenberg N (1998) A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J 17: 7480-7489. (Pubitemid 29002714)
38. Roy G, De Crescenzo G, Khaleghpour K, Kahvejian A, O'Connor-McCourt M, et al. (2002) Paip1 interacts with poly(A) binding protein through two independent binding motifs. Mol Cell Biol 22: 3769-3782. (Pubitemid 34525219)
39. Wells SE, Hillner PE, Vale RD, Sachs AB (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2: 135-140. (Pubitemid 128378975)
40. Bernstein P, Peltz SW, Ross J (1989) The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol Cell Biol 9: 659-670. (Pubitemid 19038869)
41. 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. (Pubitemid 40095820)
42. Munroe D, Jacobson A (1990) mRNA poly(A) tail, a 3′ enhancer of translational initiation. Mol Cell Biol 10: 3441-3455.
43. Roy B, Jacobson A (2013) The intimate relationships of mRNA decay and translation. Trends Genet 29: 691-699.
44. 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. (Pubitemid 36042176)
45. Kozlov G, Trempe JF, Khaleghpour K, Kahvejian A, Ekiel I, et al. (2001) Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc Natl Acad Sci U S A 98: 4409-4413. (Pubitemid 32294990)
46. Bushell M, Wood W, Carpenter G, Pain VM, Morley SJ, et al. (2001) Disruption of the interaction of mammalian protein synthesis eukaryotic initiation factor 4B with the poly(A)-binding protein by caspase- and viral protease-mediated cleavages. J Biol Chem 276: 23922-23928.
47. Craig AW, Haghighat A, Yu AT, Sonenberg N (1998) Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392: 520-523. (Pubitemid 28168986)
48. Khaleghpour K, Svitkin YV, Craig AW, DeMaria CT, Deo RC, et al. (2001) Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol Cell 7: 205-216. (Pubitemid 32162913)
49. Uchida N, Hoshino S, Katada T (2004) Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J Biol Chem 279: 1383-1391. (Pubitemid 38082665)
50. Melo EO, Dhalia R, Martins de Sa C, Standart N, de Melo Neto OP (2003) Identification of a C-terminal poly(A)-binding protein (PABP)-PABP interaction domain: role in cooperative binding to poly (A) and efficient cap distal translational repression. J Biol Chem 278: 46357-46368. (Pubitemid 37452206)
51. Tarun SZ Jr, Sachs AB (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J 15: 7168-7177.
52. Groft CM, Burley SK (2002) Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol Cell 9: 1273-1283. (Pubitemid 34722306)
53. Coldwell MJ, Morley SJ (2006) Specific isoforms of translation initiation factor 4GI show differences in translational activity. Mol Cell Biol 26: 8448-8460. (Pubitemid 44748578)
54. De Gregorio E, Preiss T, Hentze MW (1999) Translation driven by an eIF4G core domain in vivo. EMBO J 18: 4865-4874. (Pubitemid 29415539)
55. Poyry TA, Kaminski A, Jackson RJ (2004) What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev 18: 62-75. (Pubitemid 38090688)
56. Zhang J, Maquat LE (1997) Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J 16: 826-833. (Pubitemid 27089529)
57. Kim KM, Cho H, Choi K, Kim J, Kim BW, et al. (2009) A new MIF4G domain-containing protein, CTIF, directs nuclear cap-binding protein CBP80/20-dependent translation. Genes Dev 23: 2033-2045.
58. 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.
59. Hwang J, Sato H, Tang Y, Matsuda D, Maquat LE (2010) UPF1 association with the cap-binding protein, CBP80, promotes nonsense-mediated mRNA decay at two distinct steps. Mol Cell 39: 396-409.
60. Ishigaki Y, Li X, Serin G, Maquat LE (2001) Evidence for a Pioneer Round of mRNA Translation. mRNAs Subject to Nonsense-Mediated Decay in Mammalian Cells Are Bound by CBP80 and CBP20. Cell 106: 607-617. (Pubitemid 32879322)
61. 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.
62. Imataka H, Sonenberg N (1997) Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Mol Cell Biol 17: 6940-6947. (Pubitemid 27505924)
63. Morino S, Imataka H, Svitkin YV, Pestova TV, Sonenberg N (2000) Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol Cell Biol 20: 468-477. (Pubitemid 30023088)
64. LeFebvre AK, Korneeva NL, Trutschl M, Cvek U, Duzan RD, et al. (2006) Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J Biol Chem 281: 22917-22932.
65. Morris C, Wittmann J, Jack HM, Jalinot P (2007) Human INT6/eIF3e is required for nonsense-mediated mRNA decay. EMBO Rep 8: 596-602. (Pubitemid 47214715)
66. Pisarev AV, Hellen CU, Pestova TV (2007) Recycling of eukaryotic posttermination ribosomal complexes. Cell 131: 286-299. (Pubitemid 47576139)
67. Beznoskova P, Cuchalova L, Wagner S, Shoemaker CJ, Gunisova S, et al. (2013) Translation Initiation Factors eIF3 and HCR1 Control Translation Termination and Stop Codon Read-Through in Yeast Cells. PLoS Genet 9: e1003962.
68. Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW, et al. (2008) Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133: 314-327. (Pubitemid 351508299)
69. Choe J, Oh N, Park S, Lee YK, Song OK, et al. (2012) Translation initiation on mRNAs bound by nuclear cap-binding protein complex CBP80/20 requires interaction between CBP80/20-dependent translation initiation factor and eukaryotic translation initiation factor 3g. J Biol Chem 287: 18500-18509.
70. Coldwell MJ, Hashemzadeh-Bonehi L, Hinton TM, Morley SJ, Pain VM (2004) Expression of fragments of translation initiation factor eIF4GI reveals a nuclear localisation signal within the N-terminal apoptotic cleavage fragment N-FAG. J Cell Sci 117: 2545-2555. (Pubitemid 38877850)
71. Moriarty PM, Reddy CC, Maquat LE (1997) The presence of an intron within the rat gene for selenium-dependent glutathione peroxidase 1 is not required to protect nuclear RNA from UGA-mediated decay. RNA 3: 1369-1373. (Pubitemid 128633478)
72. Pillai RS, Grimmler M, Meister G, Will CL, Luhrmann R, et al. (2003) Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev 17: 2321-2333. (Pubitemid 37128646)
73. Paillusson A, Hirschi N, Vallan C, Azzalin CM, Muhlemann O (2005) A GFP-based reporter system to monitor nonsense-mediated mRNA decay. Nucleic Acids Res 33: e54.
74. Welnowska E, Castello A, Moral P, Carrasco L (2009) Translation of mRNAs from vesicular stomatitis virus and vaccinia virus is differentially blocked in cells with depletion of eIF4GI and/or eIF4GII. J Mol Biol 394: 506-521.
75. Buhler M, Steiner S, Mohn F, Paillusson A, Muhlemann O (2006) EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3′ UTR length. Nat Struct Mol Biol 13: 462-464. (Pubitemid 43881589)
76. Nicholson P, Joncourt R, Muhlemann O (2012) Analysis of nonsense-mediated mRNA decay in mammalian cells. Curr Protoc Cell Biol Chapter 27: Unit27 24.
77. Lerner EA, Lerner MR, Janeway CA Jr, Steitz JA (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci U S A 78: 2737-2741.
78. Jenny A, Hauri HP, Keller W (1994) Characterization of cleavage and polyadenylation specificity factor and cloning of its 100-kilodalton subunit. Mol Cell Biol 14: 8183-8190. (Pubitemid 24373567)
79. Jenny A, Minvielle-Sebastia L, Preker PJ, Keller W (1996) Sequence similarity between the 73-kilodalton protein of mammalian CPSF and a subunit of yeast polyadenylation factor I. Science 274: 1514-1517. (Pubitemid 26403924)
80. Marintchev A, Edmonds KA, Marintcheva B, Hendrickson E, Oberer M, et al. (2009) Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136: 447-460.