Browse > Article
http://dx.doi.org/10.5483/BMBRep.2017.50.4.007

Translation initiation mediated by nuclear cap-binding protein complex  

Ryu, Incheol (Creative Research Initiatives Center for Molecular Biology of Translation, Korea University)
Kim, Yoon Ki (Creative Research Initiatives Center for Molecular Biology of Translation, Korea University)
Publication Information
BMB Reports / v.50, no.4, 2017 , pp. 186-193 More about this Journal
Abstract
In mammals, cap-dependent translation of mRNAs is initiated by two distinct mechanisms: cap-binding complex (CBC; a heterodimer of CBP80 and 20)-dependent translation (CT) and eIF4E-dependent translation (ET). Both translation initiation mechanisms share common features in driving cap- dependent translation; nevertheless, they can be distinguished from each other based on their molecular features and biological roles. CT is largely associated with mRNA surveillance such as nonsense-mediated mRNA decay (NMD), whereas ET is predominantly involved in the bulk of protein synthesis. However, several recent studies have demonstrated that CT and ET have similar roles in protein synthesis and mRNA surveillance. In a subset of mRNAs, CT preferentially drives the cap-dependent translation, as ET does, and ET is responsible for mRNA surveillance, as CT does. In this review, we summarize and compare the molecular features of CT and ET with a focus on the emerging roles of CT in translation.
Keywords
CBC; eIF4E; NMD; Translation;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Oh N, Kim KM, Choe J and Kim YK (2007) Pioneer round of translation mediated by nuclear cap-binding proteins CBP80/20 occurs during prolonged hypoxia. FEBS Lett 581, 5158-5164   DOI
2 Oh N, Kim KM, Cho H, Choe J and Kim YK (2007) Pioneer round of translation occurs during serum starvation. Biochem Bioph Res Co 362, 145-151   DOI
3 Apcher S, Daskalogianni C, Lejeune F et al (2011) Major source of antigenic peptides for the MHC class I pathway is produced during the pioneer round of mRNA translation. Proc Natl Acad Sci U S A 108, 11572-11577   DOI
4 Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW and Maquat LE (2008) Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133, 314-327   DOI
5 Sharma A, Yilmaz A, Marsh K, Cochrane A and Boris-Lawrie K (2012) Thriving under Stress: Selective Translation of HIV-1 Structural Protein mRNA during Vpr-Mediated Impairment of eIF4E Translation Activity. PLoS Pathog 8, e1002612   DOI
6 Ma XM and Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10, 307-318   DOI
7 Martinez-Nunez RT, Wallace A, Coyne D et al (2016) Modulation of nonsense mediated decay by rapamycin. Nucleic Acids Res [Epub ahead of print]
8 Park J, Ahn S, Jayabalan AK, Ohn T, Koh HC and Hwang J (2016) Insulin Signaling Augments eIF4E-Dependent Nonsense-Mediated mRNA Decay in Mammalian Cells. Biochim Biophys Acta 1859, 896-905   DOI
9 Rattray AM and Muller B (2012) The control of histone gene expression. Biochem Soc T 40, 880-885   DOI
10 Cowling VH (2010) Regulation of mRNA cap methylation. Biochem J 425, 295-302   DOI
11 Le Hir H, Sauliere J and Wang Z (2016) The exon junction complex as a node of post-transcriptional networks. Nat Rev Mol Cell Biol 17, 41-54   DOI
12 Woodward LA, Mabin JW, Gangras P and Singh G (2016) The exon junction complex: a lifelong guardian of mRNA fate. Wiley Interdiscip Rev RNA e1411
13 Banerjee A, Apponi LH, Pavlath GK and Corbett AH (2013) PABPN1: molecular function and muscle disease. FEBS J 280, 4230-4250   DOI
14 Maquat LE, Tarn WY and Isken O (2010) The pioneer round of translation: features and functions. Cell 142, 368-374   DOI
15 Lejeune F, Ishigaki Y, Li X and Maquat LE (2002) The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling. EMBO J 21, 3536-3545   DOI
16 Jackson RJ, Hellen CU and Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11, 113-127   DOI
17 Hinnebusch AG (2014) The scanning mechanism of eukaryotic translation initiation. Ann Rev Biochem 83, 779-812   DOI
18 Marintchev A and Wagner G (2004) Translation initiation: structures, mechanisms and evolution. Q Rev Biophys 37, 197-284
19 McKendrick L, Thompson E, Ferreira J, Morley SJ and Lewis JD (2001) Interaction of eukaryotic translation initiation factor 4G with the nuclear cap-binding complex provides a link between nuclear and cytoplasmic functions of the m(7) guanosine cap. Mol Cell Biol 21, 3632-3641   DOI
20 von Moeller H, Lerner R, Ricciardi A, Basquin C, Marzluff WF and Conti E (2013) Structural and biochemical studies of SLIP1-SLBP identify DBP5 and eIF3g as SLIP1-binding proteins. Nucleic Acids Res 41, 7960-7971   DOI
21 Masutani M, Sonenberg N, Yokoyama S and Imataka H (2007) Reconstitution reveals the functional core of mammalian eIF3. EMBO J 26, 3373-3383   DOI
22 Zhou M, Sandercock AM, Fraser CS et al (2008) Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc Natl Acad Sci U S A 105, 18139-18144   DOI
23 Fraser CS, Berry KE, Hershey JW and Doudna JA (2007) eIF3j is located in the decoding center of the human 40S ribosomal subunit. Mol Cell 26, 811-819   DOI
24 Romeo V and Schumperli D (2016) Cycling in the nucleus: regulation of RNA 3' processing and nuclear organization of replication-dependent histone genes. Curr Opin Cell Biol 40, 23-31   DOI
25 Marzluff WF, Wagner EJ and Duronio RJ (2008) Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9, 843-854   DOI
26 Simonetti A, Brito Querido J, Myasnikov AG et al (2016) eIF3 Peripheral Subunits Rearrangement after mRNA Binding and Start-Codon Recognition. Mol Cell 63, 206-217   DOI
27 Parsyan A, Svitkin Y, Shahbazian D et al (2011) mRNA helicases: the tacticians of translational control. Nat Rev Mol Cell Biol 12, 235-245   DOI
28 Pestova TV and Kolupaeva VG (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16, 2906-2922   DOI
29 Marintchev A, Edmonds KA, Marintcheva B et al (2009) Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136, 447-460   DOI
30 Harris ME, Bohni R, Schneiderman MH, Ramamurthy L, Schumperli D and Marzluff WF (1991) Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol 11, 2416-2424   DOI
31 Hoefig KP and Heissmeyer V (2014) Degradation of oligouridylated histone mRNAs: see UUUUU and goodbye. Wiley Interdiscip Rev RNA 5, 577-589   DOI
32 Kaygun H and Marzluff WF (2005) Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol 12, 794-800   DOI
33 Choe J, Ahn SH and Kim YK (2014) The mRNP remodeling mediated by UPF1 promotes rapid degradation of replication-dependent histone mRNA. Nucleic Acids Res 42, 9334-9349   DOI
34 Proud CG (2005) eIF2 and the control of cell physiology. Semin Cell Dev Biol 16, 3-12   DOI
35 Hinnebusch AG (2006) eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci 31, 553-562   DOI
36 Majumdar R, Bandyopadhyay A and Maitra U (2003) Mammalian translation initiation factor eIF1 functions with eIF1A and eIF3 in the formation of a stable 40 S preinitiation complex. J Biol Chem 278, 6580-6587   DOI
37 Pestova TV, Borukhov SI and Hellen CU (1998) Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394, 854-859   DOI
38 Villa N, Do A, Hershey JW and Fraser CS (2013) Human eukaryotic initiation factor 4G (eIF4G) protein binds to eIF3c, -d, and -e to promote mRNA recruitment to the ribosome. J Biol Chem 288, 32932-32940   DOI
39 LeFebvre AK, Korneeva NL, Trutschl M et al (2006) Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J Biol Chem 281, 22917-22932   DOI
40 Kim KM, Cho H, Choi K et al (2009) A new MIF4G domain-containing protein, CTIF, directs nuclear capbinding protein CBP80/20-dependent translation. Genes Dev 23, 2033-2045   DOI
41 Choe J, Oh N, Park S 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   DOI
42 Lejeune F, Ranganathan AC and Maquat LE (2004) eIF4G is required for the pioneer round of translation in mammalian cells. Nat Struct Mol Biol 11, 992-1000   DOI
43 Li Q, Imataka H, Morino S et al (1999) Eukaryotic translation initiation factor 4AIII (eIF4AIII) is functionally distinct from eIF4AI and eIF4AII. Mol Cell Biol 19, 7336-7346   DOI
44 Oberer M, Marintchev A and Wagner G (2005) Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev 19, 2212-2223   DOI
45 Choe J, Ryu I, Park OH et al (2014) eIF4AIII enhances translation of nuclear cap-binding complex-bound mRNAs by promoting disruption of secondary structures in 5'UTR. Proc Natl Acad Sci U S A 111, E4577-4586   DOI
46 Rogers GW Jr, Richter NJ and Merrick WC (1999) Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J Biol Chem 274, 12236-12244   DOI
47 Graves RA, Pandey NB, Chodchoy N and Marzluff WF (1987) Translation is required for regulation of histone mRNA degradation. Cell 48, 615-626   DOI
48 Cakmakci NG, Lerner RS, Wagner EJ, Zheng L and Marzluff WF (2008) SLIP1, a factor required for activation of histone mRNA translation by the stem-loop binding protein. Mol Cell Biol 28, 1182-1194   DOI
49 Choe J, Kim KM, Park S et al (2013) Rapid degradation of replication-dependent histone mRNAs largely occurs on mRNAs bound by nuclear cap-binding proteins 80 and 20. Nucleic Acids Res 41, 1307-1318   DOI
50 Stimac E, Groppi VE Jr and Coffino P (1984) Inhibition of protein synthesis stabilizes histone mRNA. Mol Cell Biol 4, 2082-2090   DOI
51 Holcik M and Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6, 318-327   DOI
52 Gebauer F and Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5, 827-835
53 Ballut L, Marchadier B, Baguet A, Tomasetto C, Seraphin B and 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   DOI
54 Ishigaki Y, Li X, Serin G and 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   DOI
55 Yamasaki S and Anderson P (2008) Reprogramming mRNA translation during stress. Curr Opin Cell Biol 20, 222-226   DOI
56 Koritzinsky M, Magagnin MG, van den Beucken T et al (2006) Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J 25, 1114-1125   DOI
57 Singh G, Pratt G, Yeo GW and Moore MJ (2015) The Clothes Make the mRNA: Past and Present Trends in mRNP Fashion. Ann Rev Biochem 84, 325-354   DOI
58 Shatkin AJ and Manley JL (2000) The ends of the affair: capping and polyadenylation. Nat Struct Biol 7, 838-842   DOI
59 Kashima I, Yamashita A, Izumi N 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   DOI
60 Lu WT, Wilczynska A, Smith E and Bushell M (2014) The diverse roles of the eIF4A family: you are the company you keep. Biochem Soc T 42, 166-172   DOI
61 Noble CG and Song H (2007) MLN51 stimulates the RNA-helicase activity of eIF4AIII. PLoS One 2, e303   DOI
62 Unbehaun A, Borukhov SI, Hellen CU and Pestova TV (2004) Release of initiation factors from 48S complexes during ribosomal subunit joining and the link between establishment of codon-anticodon base-pairing and hydrolysis of eIF2-bound GTP. Genes Dev 18, 3078-3093   DOI
63 Lee JH, Pestova TV, Shin BS, Cao C, Choi SK and Dever TE (2002) Initiation factor eIF5B catalyzes second GTPdependent step in eukaryotic translation initiation. Proc Natl Acad Sci U S A 99, 16689-16694   DOI
64 Pestova TV, Lomakin IB, Lee JH, Choi SK, Dever TE and Hellen CU (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403, 332-335   DOI
65 Wells SE, Hillner PE, Vale RD and Sachs AB (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2, 135-140   DOI
66 Mokas S, Mills JR, Garreau C et al (2009) Uncoupling stress granule assembly and translation initiation inhibition. Mol Biol Cell 20, 2673-2683   DOI
67 Weill L, Belloc E, Bava FA and Mendez R (2012) Translational control by changes in poly(A) tail length: recycling mRNAs. Nat Struct Mol Biol 19, 577-585   DOI
68 Imataka H, Gradi A and 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   DOI
69 von Der Haar T, Ball PD and McCarthy JE (2000) Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5'-Cap by domains of eIF4G. J Biol Chem 275, 30551-30555   DOI
70 Borman AM, Michel YM and Kean KM (2000) Biochemical characterisation of cap-poly(A) synergy in rabbit reticulocyte lysates: the eIF4G-PABP interaction increases the functional affinity of eIF4E for the capped mRNA 5'-end. Nucleic Acids Res 28, 4068-4075   DOI
71 Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN and Sonenberg N (2005) Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev 19, 104-113   DOI
72 Hoshino S, Imai M, Kobayashi T, Uchida N and 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   DOI
73 Jackson RJ, Hellen CU and Pestova TV (2012) Termination and post-termination events in eukaryotic translation. Adv Protein Chem Str 86, 45-93
74 Chiu SY, Lejeune F, Ranganathan AC and Maquat LE (2004) The pioneer translation initiation complex is functionally distinct from but structurally overlaps with the steady-state translation initiation complex. Genes Dev 18, 745-754   DOI
75 Fatscher T, Boehm V and Gehring NH (2015) Mechanism, factors, and physiological role of nonsense-mediated mRNA decay. Cell Mol Life Sci 72, 4523-4544   DOI
76 Koumenis C, Naczki C, Koritzinsky M et al (2002) Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22, 7405-7416   DOI
77 Arsham AM, Howell JJ and Simon MC (2003) A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J Biol Chem 278, 29655-29660   DOI
78 Dostie J, Ferraiuolo M, Pause A, Adam SA and Sonenberg N (2000) A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5' cap-binding protein, eIF4E. EMBO J 19, 3142-3156   DOI
79 Gardner LB (2008) Hypoxic inhibition of nonsensemediated RNA decay regulates gene expression and the integrated stress response. Mol Cell Biol 28, 3729-3741   DOI
80 He F and Jacobson A (2015) Nonsense-Mediated mRNA Decay: Degradation of Defective Transcripts Is Only Part of the Story. Ann Rev Gene 49, 339-366   DOI
81 Karousis ED, Nasif S and Muhlemann O (2016) Nonsensemediated mRNA decay: novel mechanistic insights and biological impact. Wiley Interdiscip Rev RNA 7, 661-682   DOI
82 Hwang J and Kim YK (2013) When a ribosome encounters a premature termination codon. BMB Rep 46, 9-16   DOI
83 Kurosaki T and Maquat LE (2016) Nonsense-mediated mRNA decay in humans at a glance. J Cell Sci 129, 461-467   DOI
84 Sato H and Maquat LE (2009) Remodeling of the pioneer translation initiation complex involves translation and the karyopherin importin beta. Genes Dev 23, 2537-2550   DOI
85 Durand S and Lykke-Andersen J (2013) Nonsensemediated mRNA decay occurs during eIF4F-dependent translation in human cells. Nat Struct Mol Biol 20, 702-709   DOI
86 Rufener SC and Muhlemann O (2013) eIF4E-bound mRNPs are substrates for nonsense-mediated mRNA decay in mammalian cells. Nat Struct Mol Biol 20, 710-717   DOI
87 McMahon R, Zaborowska I and Walsh D (2011) Noncytotoxic inhibition of viral infection through eIF4F-independent suppression of translation by 4EGi-1. J Virol 85, 853-864   DOI
88 Moerke NJ, Aktas H, Chen H et al (2007) Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128, 257-267   DOI
89 Qin X, Jiang B and Zhang Y (2016) 4E-BP1, a multifactor regulated multifunctional protein. Cell cycle 15, 781-786   DOI