3,133
Views
22
CrossRef citations to date
0
Altmetric
Research Paper

Cellular mRNA recruits the ribosome via eIF3-PABP bridge to initiate internal translation

, , , , , , & show all
Pages 553-567 | Received 28 Aug 2015, Accepted 23 Dec 2015, Published online: 21 Feb 2016

References

  • Spriggs KA, Stoneley M, Bushell M, Willis AE. Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol Cell 2008; 100:27-38; PMID:18072942; http://dx.doi.org/10.1042/BC20070098
  • Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell 2010; 40:228-37; PMID:20965418; http://dx.doi.org/10.1016/j.molcel.2010.09.028
  • Holcik M, Sonenberg N. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 2005; 6:318-27; PMID:15803138; http://dx.doi.org/10.1038/nrm1618
  • Silvera D, Formenti SC, Schneider RJ. Translational control in cancer. Nat Rev Cancer 2010; 10:254-66; PMID:20332778; http://dx.doi.org/10.1038/nrc2824
  • Ruggero D. Translational control in cancer etiology. Cold Spring Harb Perspect Biol 2013; 1:5-2. pii: a012336; PMID: 22767671; http://dx.doi/ 0.1101/cshperspect.a012336.
  • Pelletier J, Sonenberg N. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 1988; 334:320-5; PMID:2839775; http://dx.doi.org/10.1038/334320a0
  • Jackson RJ. The current status of vertebrate cellular mRNA IRESs. Cold Spring Harb Perspect Biol. 2013; 1:5-2; PMID:23378589; http://dx.doi/10.1101/cshperspect.a011569.
  • Holcik M, Lefebvre C, Yeh C, Chow T, Korneluk RG. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat Cell Biol 1999; 1:190-2; PMID:10559907; http://dx.doi.org/10.1038/11109
  • Baird SD, Lewis SM, Turcotte M, Holcik M. A search for structurally similar cellular internal ribosome entry sites. Nucleic Acids Res 2007; 35:4664-77; PMID:17591613; http://dx.doi.org/10.1093/nar/gkm483
  • Liwak U, Thakor N, Jordan LE, Roy R, Lewis SM, Pardo OE, Seckl M, Holcik M. Tumor suppressor PDCD4 represses internal ribosome entry site-mediated translation of antiapoptotic proteins and is regulated by S6 kinase 2. Mol Cell Biol 2012; 32:1818-29; PMID:22431522; http://dx.doi.org/10.1128/MCB.06317-11
  • Holcik M, Korneluk RG. Functional characterization of the X-linked inhibitor of apoptosis (XIAP) internal ribosome entry site element: role of La autoantigen in XIAP translation. Mol Cell Biol 2000; 20:4648-57; PMID:10848591; http://dx.doi.org/10.1128/MCB.20.13.4648-4657.2000
  • Holcik M, Gordon BW, Korneluk RG. The internal ribosome entry site-mediated translation of antiapoptotic protein XIAP is modulated by the heterogeneous nuclear ribonucleoproteins C1 and C2. Mol Cell Biol 2003; 23:280-8; PMID:12482981; http://dx.doi.org/10.1128/MCB.23.1.280-288.2003
  • Lewis SM, Veyrier A, Hosszu Ungureanu N, Bonnal S, Vagner S, Holcik M. Subcellular relocalization of a trans-acting factor regulates XIAP IRES-dependent translation. Mol Biol Cell 2007; 18:1302-11; PMID:17287399; http://dx.doi.org/10.1091/mbc.E06-06-0515
  • Hundsdoerfer P, Thoma C, Hentze MW Eukaryotic translation initiation factor 4GI and p97 promote cellular internal ribosome entry sequence-driven translation. Proc Natl Acad Sci U S A 2005; 102:13421-6; Epub 12005 Sep 13427; PMID:16174738; http://dx.doi.org/10.1073/pnas.0506536102
  • Thakor N, Holcik M. IRES-mediated translation of cellular messenger RNA operates in eIF2alpha- independent manner during stress. Nucleic Acids Res 2012; 40:541-52; PMID:21917851; http://dx.doi.org/10.1093/nar/gkr701
  • Locker N, Lukavsky PJ. A practical approach to isolate 48S complexes: affinity purification and analyses. Methods Enzymol 2007; 429:83-104; PMID:17913620; http://dx.doi.org/10.1016/S0076-6879(07)29005-6
  • Graber TE, Baird SD, Kao PN, Mathews MB, Holcik M. NF45 functions as an IRES trans-acting factor that is required for translation of cIAP1 during the unfolded protein response. Cell Death Differ 2010; 17:719-29; PMID:19893574; http://dx.doi.org/10.1038/cdd.2009.164
  • Faye MD, Graber TE, Liu P, Thakor N, Baird SD, Durie D, Holcik M. Nucleotide composition of cellular internal ribosome entry sites defines dependence on NF45 and predicts a posttranscriptional mitotic regulon. Mol Cell Biol 2013; 33:307-18; PMID:23129811; http://dx.doi.org/10.1128/MCB.00546-12
  • Wilkinson KA, Merino EJ, Weeks KM. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat Protoc 2006; 1:1610-6; PMID:17406453; http://dx.doi.org/10.1038/nprot.2006.249
  • Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A 2004; 101:7287-92; Epub 2004 May 7283; PMID:15123812; http://dx.doi.org/10.1073/pnas.0401799101
  • Svitkin YV, Sonenberg N. An efficient system for cap- and poly(A)-dependent translation in vitro. Methods Mol Biol 2004; 257:155-70; PMID:14770004
  • Sun C, Todorovic A, Querol-Audi J, Bai Y, Villa N, Snyder M, Ashchyan J, Lewis CS, Hartland A, Gradia S, et al. Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3). Proc Natl Acad Sci U S A 2011; 108:20473-8; Epub 1116822011 Dec 1116821101; PMID:22135459; http://dx.doi.org/10.1073/pnas.1116821108
  • Jan E, Sarnow P. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J Mol Biol 2002; 324:889-902; PMID:12470947; http://dx.doi.org/10.1016/S0022-2836(02)01099-9
  • Jang CJ, Lo MC, Jan E. Conserved element of the dicistrovirus IGR IRES that mimics an E-site tRNA/ribosome interaction mediates multiple functions. J Mol Biol 2009; 387:42-58; Epub 2009 Jan 1029; PMID:19361441; http://dx.doi.org/10.1016/j.jmb.2009.01.042
  • Riley A, Jordan LE, Holcik M. Distinct 5′ UTRs regulate XIAP expression under normal growth conditions and during cellular stress. Nucleic Acids Res 2010; 38:4665-74; PMID:20385593; http://dx.doi.org/10.1093/nar/gkq241
  • Shirokikh NE, Alkalaeva EZ, Vassilenko KS, Afonina ZA, Alekhina OM, Kisselev LL, Spirin AS. Quantitative analysis of ribosome-mRNA complexes at different translation stages. Nucleic Acids Res 2010; 38:e15; Epub 2009 Nov 1012; PMID:19910372; http://dx.doi.org/10.1093/nar/gkp1025
  • Holcik M, Graber T, Lewis SM, Lefebvre CA, Lacasse E, Baird S. Spurious splicing within the XIAP 5′ UTR occurs in the Rluc/Fluc but not the {beta}gal/CAT bicistronic reporter system. RNA 2005; 11:1605-9; PMID:16177136; http://dx.doi.org/10.1261/rna.2158605
  • Hellen CU, Sarnow P. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev 2001; 15:1593-612; PMID:11445534; http://dx.doi.org/10.1101/gad.891101
  • Berry KE, Waghray S, Mortimer SA, Bai Y, Doudna JA. Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure 2011; 19:1456-66; PMID:22000514; http://dx.doi.org/10.1016/j.str.2011.08.002
  • Berry KE, Waghray S, Doudna JA. The HCV IRES pseudoknot positions the initiation codon on the 40S ribosomal subunit. RNA 2010; 16:1559-69; Epub 2192010 Jun 2197228; PMID:20584896; http://dx.doi.org/10.1261/rna.2197210
  • Thoma C, Bergamini G, Galy B, Hundsdoerfer P, Hentze MW. Enhancement of IRES-mediated translation of the c-myc and BiP mRNAs by the Poly(A) tail is independent of intact eIF4G and PABP. Mol Cell 2004; 15:925-35; PMID:15383282; http://dx.doi.org/10.1016/j.molcel.2004.08.021
  • Pestova TV, Lorsch JR, Hellen CU. In Mathews, M. B., Sonenberg, N. and Hershey, J. W. B. (eds.), Translational Control in Biology and Medicine. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press 2007; pp. 87-128.
  • Lewis SM, Cerquozzi S, Graber TE, Ungureanu NH, Andrews M, Holcik M. The eIF4G homolog DAP5/p97 supports the translation of select mRNAs during endoplasmic reticulum stress. Nucleic Acids Res 2008; 36:168-78; PMID:18003655; http://dx.doi.org/10.1093/nar/gkm1007
  • Lopez de Quinto S, Martinez-Salas E. Interaction of the eIF4G initiation factor with the aphthovirus IRES is essential for internal translation initiation in vivo. RNA 2000; 6:1380-92; PMID:11073214; http://dx.doi.org/10.1017/S1355838200000753
  • Silvera D, Arju R, Darvishian F, Levine PH, Zolfaghari L, Goldberg J, Hochman T, Formenti SC, Schneider RJ. Essential role for eIF4GI overexpression in the pathogenesis of inflammatory breast cancer. Nat Cell Biol 2009; 11:903-8; PMID:19525934; http://dx.doi.org/10.1038/ncb1900
  • Braunstein S, Karpisheva K, Pola C, Goldberg J, Hochman T, Yee H, Cangiarella J, Arju R, Formenti SC, Schneider RJ. A hypoxia-controlled cap-dependent to cap-independent translation switch in breast cancer. Mol Cell 2007; 28:501-12; PMID:17996713; http://dx.doi.org/10.1016/j.molcel.2007.10.019
  • Svitkin YV, Evdokimova VM, Brasey A, Pestova TV, Fantus D, Yanagiya A, Imataka H, Skabkin MA, Ovchinnikov LP, Merrick WC, et al. General RNA-binding proteins have a function in poly(A)-binding protein-dependent translation. EMBO J 2009; 28:58-68; Epub 2008 Dec 1011; PMID:19078965; http://dx.doi.org/10.1038/emboj.2008.259
  • Holcik M, Korneluk RG. XIAP, the guardian angel. Nat Rev Mol Cell Biol 2001; 2:550-6; PMID:11433370; http://dx.doi.org/10.1038/35080103
  • Holcik M, Yeh C, Korneluk RG, Chow T. Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death. Oncogene 2000; 19:4174-7; PMID:10962579; http://dx.doi.org/10.1038/sj.onc.1203765
  • Durie D, Lewis SM, Liwak U, Kisilewicz M, Gorospe M, Holcik M. RNA-binding protein HuR mediates cytoprotection through stimulation of XIAP translation. Oncogene 2011; 30:1460-9; PMID:21102524; http://dx.doi.org/10.1038/onc.2010.527
  • Bevilacqua E, Wang X, Majumder M, Gaccioli F, Yuan CL, Wang C, Zhu X, Jordan LE, Scheuner D, Kaufman RJ, et al. eIF2alpha phosphorylation tips the balance to apoptosis during osmotic stress. J Biol Chem 2010; 285:17098-111; PMID:20338999; http://dx.doi.org/10.1074/jbc.M110.109439
  • Yoon A, Peng G, Brandenburg Y, Zollo O, Xu W, Rego E, Ruggero D. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 2006; 312:902-6; PMID:16690864; http://dx.doi.org/10.1126/science.1123835
  • Gu L, Zhu N, Zhang H, Durden DL, Feng Y, Zhou M. Regulation of XIAP translation and induction by MDM2 following irradiation. Cancer Cell 2009; 15:363-75; PMID:19411066; http://dx.doi.org/10.1016/j.ccr.2009.03.002
  • Filbin ME, Kieft JS Toward a structural understanding of IRES RNA function. Curr Opin Struct Biol 2009; 19:267-76; Epub 2009 Apr 1019; PMID:19362464; http://dx.doi.org/10.1016/j.sbi.2009.03.005
  • Kieft JS, Zhou K, Jubin R, Murray MG, Lau JY, Doudna JA. The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J Mol Biol 1999; 292:513-29; PMID:10497018; http://dx.doi.org/10.1006/jmbi.1999.3095
  • Odreman-Macchioli F, Baralle FE, Buratti E. Mutational analysis of the different bulge regions of the HCV domain II and their influence on IRES translational ability. J Biol Chem 2001; 276:41648-55; PMID:11498532; http://dx.doi.org/10.1074/jbc.M104128200
  • Brown EA, Day SP, Jansen RW, Lemon SM. The 5′ nontranslated region of hepatitis A virus RNA: secondary structure and elements required for translation in vitro. J Virol 1991; 65:5828-38; PMID:1656072
  • Kolupaeva VG, Hellen CU, Shatsky IN. Structural analysis of the interaction of the pyrimidine tract-binding protein with the internal ribosomal entry site of encephalomyocarditis virus and foot-and-mouth disease virus RNAs. RNA 1996; 2:1199-212; PMID:8972770
  • Hoffman MA, Palmenberg AC. Mutational analysis of the J-K stem-loop region of the encephalomyocarditis virus IRES. J Virol 1995; 69:4399-406; PMID:7769702
  • Yaman I, Fernandez J, Liu H, Caprara M, Komar AA, Koromilas AE, Zhou L, Snider MD, Scheuner D, Kaufman RJ, et al. The zipper model of translational control. A small upstream ORF is the switch that controls structural remodeling of an mRNA leader. Cell 2003; 113:519-31; PMID:12757712; http://dx.doi.org/10.1016/S0092-8674(03)00345-3
  • Mitchell SA, Spriggs KA, Coldwell MJ, Jackson RJ, Willis AE. The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr. Mol Cell 2003; 11:757-71; PMID:12667457; http://dx.doi.org/10.1016/S1097-2765(03)00093-5
  • Jopling CL, Spriggs KA, Mitchell SA, Stoneley M, Willis AE. L-Myc protein synthesis is initiated by internal ribosome entry. RNA 2004; 10:287-98; PMID:14730027; http://dx.doi.org/10.1261/rna.5138804
  • Bonnal S, Schaeffer C, Creancier L, Clamens S, Moine H, Prats AC, Vagner S. A single internal ribosome entry site containing a G quartet RNA structure drives fibroblast growth factor 2 gene expression at four alternative translation initiation codons. J Biol Chem 2003; 278:39330-6; Epub 32003 Jul 39311; PMID:12857733; http://dx.doi.org/10.1074/jbc.M305580200
  • Martineau Y, Le Bec C, Monbrun L, Allo V, Chiu IM, Danos O, Moine H, Prats H, Prats AC. Internal ribosome entry site structural motifs conserved among mammalian fibroblast growth factor 1 alternatively spliced mRNAs. Mol Cell Biol 2004; 24:7622-35; PMID:15314170; http://dx.doi.org/10.1128/MCB.24.17.7622-7635.2004
  • Le Quesne JP, Stoneley M, Fraser GA, Willis AE. Derivation of a structural model for the c-myc IRES. J Mol Biol 2001; 310:111-26; PMID:11419940; http://dx.doi.org/10.1006/jmbi.2001.4745
  • Pickering BM, Mitchell SA, Spriggs KA, Stoneley M, Willis AE. Bag-1 internal ribosome entry segment activity is promoted by structural changes mediated by Poly(rC) binding protein 1 and recruitment of polypyrimidine tract binding protein 1. Mol Cell Biol 2004; 24:5595-605; PMID:15169918; http://dx.doi.org/10.1128/MCB.24.12.5595-5605.2004
  • Willcocks MM, Locker N, Gomwalk Z, Royall E, Bakhshesh M, Belsham GJ, Idamakanti N, Burroughs KD, Reddy PS, Hallenbeck PL. et al. Structural features of the Seneca Valley virus internal ribosome entry site (IRES) element: a picornavirus with a pestivirus-like IRES. J Virol 2011; 85:4452-61; Epub 02011 Feb 01116; PMID:21325406; http://dx.doi.org/10.1128/JVI.01107-10
  • Sizova DV, Kolupaeva VG, Pestova TV, Shatsky IN, Hellen CU. Specific interaction of eukaryotic translation initiation factor 3 with the 5′ nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J Virol 1998; 72:4775-82; PMID:9573242
  • Balvay L, Soto Rifo R, Ricci EP, Decimo D, Ohlmann T. Structural and functional diversity of viral IRESes. Biochim Biophys Acta 2009; 1789:542-57; Epub 2009 Jul 1024; PMID:19632368; http://dx.doi.org/10.1016/j.bbagrm.2009.07.005
  • Fletcher SP, Ali IK, Kaminski A, Digard P, Jackson RJ. The influence of viral coding sequences on pestivirus IRES activity reveals further parallels with translation initiation in prokaryotes. RNA 2002; 8:1558-71; PMID:12515388 http://dx.doi.org/10-1017/S135583820202303
  • Jubin R, Vantuno NE, Kieft JS, Murray MG, Doudna JA, Lau JY, Baroudy BM. Hepatitis C virus internal ribosome entry site (IRES) stem loop IIId contains a phylogenetically conserved GGG triplet essential for translation and IRES folding. J Virol 2000; 74:10430-7; PMID:11044087; http://dx.doi.org/10.1128/JVI.74.22.10430-10437.2000
  • Koh DC, Edelman GM, Mauro VP. Physical evidence supporting a ribosomal shunting mechanism of translation initiation for BACE1 mRNA. Translation 2013; 1, e24400; http://dx.doi.org/10.4161/trla.24400
  • Ding Y, Tang Y, Kwok CK, Zhang Y, Bevilacqua PC, Assmann SM. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 2014; 505:696-700; Epub 12013 Nov 12724; PMID:24270811; http://dx.doi.org/10.1038/nature12756
  • Komar AA, Mazumder B, Merrick WC. A new framework for understanding IRES-mediated translation. Gene 2012; 502:75-86; PMID:22555019; http://dx.doi.org/10.1016/j.gene.2012.04.039
  • Komar AA, Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 2011; 10:229-40; PMID:21220943; http://dx.doi.org/10.4161/cc.10.2.14472
  • Hashem Y, des Georges A, Dhote V, Langlois R, Liao HY, Grassucci RA, Pestova TV, Hellen CU, Frank J. Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 2013; 503:539-43; Epub 12013 Nov 12653; PMID:24185006; http://dx.doi.org/10.1038/nature12658
  • Collier AJ, Gallego J, Klinck R, Cole PT, Harris SJ, Harrison GP, Aboul-Ela F, Varani G, Walker S. A conserved RNA structure within the HCV IRES eIF3-binding site. Nat Struct Biol 2002; 9:375-80; PMID:11927954
  • Derry MC, Yanagiya A, Martineau Y, Sonenberg N. Regulation of poly(A)-binding protein through PABP-interacting proteins. Cold Spring Harb Symp Quant Biol 2006; 71:537-43; PMID:17381337; http://dx.doi.org/10.1101/sqb.2006.71.061
  • Martineau Y, Derry MC, Wang X, Yanagiya A, Berlanga JJ, Shyu AB, Imataka H, Gehring K, Sonenberg N. Poly(A)-binding protein-interacting protein 1 binds to eukaryotic translation initiation factor 3 to stimulate translation. Mol Cell Biol 2008; 28:6658-67; Epub 02008 Aug 00725; PMID:18725400; http://dx.doi.org/10.1128/MCB.00738-08
  • Martineau Y, Wang X, Alain T, Petroulakis E, Shahbazian D, Fabre B, Bousquet-Dubouch MP, Monsarrat B, Pyronnet S, Sonenberg N. Control of Paip1-eukayrotic translation initiation factor 3 interaction by amino acids through S6 kinase. Mol Cell Biol 2014; 34:1046-53; Epub 02014 Jan 01076; PMID:24396066; http://dx.doi.org/10.1128/MCB.01079-13