DOI QR코드

DOI QR Code

Translation initiation mediated by nuclear cap-binding protein complex

Ryu, Incheol;Kim, Yoon Ki

  • Received : 2017.01.13
  • Published : 2017.04.30

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

References

  1. 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 https://doi.org/10.1128/MCB.22.21.7405-7416.2002
  2. 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 https://doi.org/10.1074/jbc.M212770200
  3. 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 https://doi.org/10.1093/emboj/19.12.3142
  4. Gardner LB (2008) Hypoxic inhibition of nonsensemediated RNA decay regulates gene expression and the integrated stress response. Mol Cell Biol 28, 3729-3741 https://doi.org/10.1128/MCB.02284-07
  5. 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 https://doi.org/10.1016/j.febslet.2007.10.002
  6. 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 https://doi.org/10.1016/j.bbrc.2007.07.169
  7. 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 https://doi.org/10.1073/pnas.1104104108
  8. 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 https://doi.org/10.1016/j.cell.2008.02.030
  9. 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 https://doi.org/10.1371/journal.ppat.1002612
  10. Ma XM and Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10, 307-318 https://doi.org/10.1038/nrm2672
  11. Martinez-Nunez RT, Wallace A, Coyne D et al (2016) Modulation of nonsense mediated decay by rapamycin. Nucleic Acids Res [Epub ahead of print]
  12. 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 https://doi.org/10.1016/j.bbagrm.2015.12.006
  13. Rattray AM and Muller B (2012) The control of histone gene expression. Biochem Soc T 40, 880-885 https://doi.org/10.1042/BST20120065
  14. 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 https://doi.org/10.1038/nrg2438
  15. 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 https://doi.org/10.1128/MCB.11.5.2416
  16. 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 https://doi.org/10.1016/j.ceb.2016.01.015
  17. Hoefig KP and Heissmeyer V (2014) Degradation of oligouridylated histone mRNAs: see UUUUU and goodbye. Wiley Interdiscip Rev RNA 5, 577-589 https://doi.org/10.1002/wrna.1232
  18. 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 https://doi.org/10.1038/nsmb972
  19. 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 https://doi.org/10.1093/nar/gku610
  20. 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 https://doi.org/10.1128/MCB.01500-07
  21. 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 https://doi.org/10.1093/nar/gks1196
  22. Stimac E, Groppi VE Jr and Coffino P (1984) Inhibition of protein synthesis stabilizes histone mRNA. Mol Cell Biol 4, 2082-2090 https://doi.org/10.1128/MCB.4.10.2082
  23. Graves RA, Pandey NB, Chodchoy N and Marzluff WF (1987) Translation is required for regulation of histone mRNA degradation. Cell 48, 615-626 https://doi.org/10.1016/0092-8674(87)90240-6
  24. Holcik M and Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6, 318-327 https://doi.org/10.1038/nrm1618
  25. Gebauer F and Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5, 827-835
  26. Yamasaki S and Anderson P (2008) Reprogramming mRNA translation during stress. Curr Opin Cell Biol 20, 222-226 https://doi.org/10.1016/j.ceb.2008.01.013
  27. 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 https://doi.org/10.1038/sj.emboj.7600998
  28. 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 https://doi.org/10.1146/annurev-biochem-080111-092106
  29. Shatkin AJ and Manley JL (2000) The ends of the affair: capping and polyadenylation. Nat Struct Biol 7, 838-842 https://doi.org/10.1038/79583
  30. Cowling VH (2010) Regulation of mRNA cap methylation. Biochem J 425, 295-302 https://doi.org/10.1042/BJ20091352
  31. 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 https://doi.org/10.1038/nrm.2015.7
  32. 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
  33. Banerjee A, Apponi LH, Pavlath GK and Corbett AH (2013) PABPN1: molecular function and muscle disease. FEBS J 280, 4230-4250 https://doi.org/10.1111/febs.12294
  34. Maquat LE, Tarn WY and Isken O (2010) The pioneer round of translation: features and functions. Cell 142, 368-374 https://doi.org/10.1016/j.cell.2010.07.022
  35. 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 https://doi.org/10.1093/emboj/cdf345
  36. 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 https://doi.org/10.1038/nrm2838
  37. Hinnebusch AG (2014) The scanning mechanism of eukaryotic translation initiation. Ann Rev Biochem 83, 779-812 https://doi.org/10.1146/annurev-biochem-060713-035802
  38. Hinnebusch AG (2006) eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci 31, 553-562 https://doi.org/10.1016/j.tibs.2006.08.005
  39. 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 https://doi.org/10.1074/jbc.M210357200
  40. Pestova TV, Borukhov SI and Hellen CU (1998) Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394, 854-859 https://doi.org/10.1038/29703
  41. Proud CG (2005) eIF2 and the control of cell physiology. Semin Cell Dev Biol 16, 3-12 https://doi.org/10.1016/j.semcdb.2004.11.004
  42. 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 https://doi.org/10.1074/jbc.M113.517011
  43. 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 https://doi.org/10.1074/jbc.M605418200
  44. 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 https://doi.org/10.1101/gad.1823409
  45. 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 https://doi.org/10.1074/jbc.M111.327528
  46. 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 https://doi.org/10.1038/nsmb824
  47. 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 https://doi.org/10.1016/S0092-8674(01)00475-5
  48. 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 https://doi.org/10.1128/MCB.21.11.3632-3641.2001
  49. 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 https://doi.org/10.1093/nar/gkt558
  50. Marintchev A and Wagner G (2004) Translation initiation: structures, mechanisms and evolution. Q Rev Biophys 37, 197-284
  51. Masutani M, Sonenberg N, Yokoyama S and Imataka H (2007) Reconstitution reveals the functional core of mammalian eIF3. EMBO J 26, 3373-3383 https://doi.org/10.1038/sj.emboj.7601765
  52. 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 https://doi.org/10.1073/pnas.0801313105
  53. 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 https://doi.org/10.1016/j.molcel.2007.05.019
  54. 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 https://doi.org/10.1016/j.molcel.2016.05.033
  55. Parsyan A, Svitkin Y, Shahbazian D et al (2011) mRNA helicases: the tacticians of translational control. Nat Rev Mol Cell Biol 12, 235-245 https://doi.org/10.1038/nrm3083
  56. 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 https://doi.org/10.1101/gad.1020902
  57. 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 https://doi.org/10.1016/j.cell.2009.01.014
  58. Oberer M, Marintchev A and Wagner G (2005) Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev 19, 2212-2223 https://doi.org/10.1101/gad.1335305
  59. 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 https://doi.org/10.1073/pnas.1409695111
  60. 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 https://doi.org/10.1074/jbc.274.18.12236
  61. 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 https://doi.org/10.1128/MCB.19.11.7336
  62. 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 https://doi.org/10.1042/BST20130161
  63. 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 https://doi.org/10.1038/nsmb990
  64. Noble CG and Song H (2007) MLN51 stimulates the RNA-helicase activity of eIF4AIII. PLoS One 2, e303 https://doi.org/10.1371/journal.pone.0000303
  65. 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 https://doi.org/10.1101/gad.1255704
  66. 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 https://doi.org/10.1073/pnas.262569399
  67. 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 https://doi.org/10.1038/35002118
  68. 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 https://doi.org/10.1038/nsmb.2311
  69. 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 https://doi.org/10.1093/emboj/17.24.7480
  70. 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 https://doi.org/10.1074/jbc.M004565200
  71. 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 https://doi.org/10.1093/nar/28.21.4068
  72. Wells SE, Hillner PE, Vale RD and Sachs AB (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2, 135-140 https://doi.org/10.1016/S1097-2765(00)80122-7
  73. 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 https://doi.org/10.1101/gad.1262905
  74. 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 https://doi.org/10.1074/jbc.274.24.16677
  75. Jackson RJ, Hellen CU and Pestova TV (2012) Termination and post-termination events in eukaryotic translation. Adv Protein Chem Str 86, 45-93
  76. 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 https://doi.org/10.1101/gad.1170204
  77. 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 https://doi.org/10.1146/annurev-genet-112414-054639
  78. 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 https://doi.org/10.1007/s00018-015-2017-9
  79. Karousis ED, Nasif S and Muhlemann O (2016) Nonsensemediated mRNA decay: novel mechanistic insights and biological impact. Wiley Interdiscip Rev RNA 7, 661-682 https://doi.org/10.1002/wrna.1357
  80. Hwang J and Kim YK (2013) When a ribosome encounters a premature termination codon. BMB Rep 46, 9-16 https://doi.org/10.5483/BMBRep.2013.46.1.002
  81. Kurosaki T and Maquat LE (2016) Nonsense-mediated mRNA decay in humans at a glance. J Cell Sci 129, 461-467 https://doi.org/10.1242/jcs.181008
  82. 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 https://doi.org/10.1101/gad.1817109
  83. 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 https://doi.org/10.1038/nsmb.2575
  84. 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 https://doi.org/10.1038/nsmb.2576
  85. 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 https://doi.org/10.1016/j.cell.2006.11.046
  86. Qin X, Jiang B and Zhang Y (2016) 4E-BP1, a multifactor regulated multifunctional protein. Cell cycle 15, 781-786 https://doi.org/10.1080/15384101.2016.1151581
  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 https://doi.org/10.1128/JVI.01873-10
  88. Mokas S, Mills JR, Garreau C et al (2009) Uncoupling stress granule assembly and translation initiation inhibition. Mol Biol Cell 20, 2673-2683 https://doi.org/10.1091/mbc.E08-10-1061
  89. 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 https://doi.org/10.1101/gad.1389006

Cited by

  1. Misfolded polypeptides are selectively recognized and transported toward aggresomes by a CED complex vol.8, 2017, https://doi.org/10.1038/ncomms15730

Acknowledgement

Supported by : National Research Foundation (NRF), Korea University