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Research Papers

Two related trypanosomatid eIF4G homologues have functional differences compatible with distinct roles during translation initiation

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Pages 305-319 | Received 30 Oct 2014, Accepted 09 Jan 2015, Published online: 31 Mar 2015

References

  • Stuart K, Brun R, Croft S, Fairlamb A, Gurtler RE, McKerrow J, Reed S, Tarleton R. Kinetoplastids: related protozoan pathogens, different diseases. J Clin Invest 2008; 118: 1301–10; PMID:18382742; http://dx.doi.org/10.1172/JCI33945
  • Daniels JP, Gull K, Wickstead B. Cell biology of the trypanosome genome. Microbiol Mol Biol Rev 2010; 74: 552–69; PMID:21119017; http://dx.doi.org/10.1128/MMBR.00024-10
  • Gunzl A. The pre-mRNA splicing machinery of trypanosomes: complex or simplified? Eukaryot Cell 2010; 9: 1159–70; PMID:20581293; http://dx.doi.org/10.1128/EC.00113-10
  • Martinez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martinez LE, Manning-Cela RG, Figueroa-Angulo EE. Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010; 2010: 525241; PMID:20169133; http://dx.doi.org/10.1155/2010/525241
  • Alsford S, duBois K, Horn D, Field MC. Epigenetic mechanisms, nuclear architecture and the control of gene expression in trypanosomes. Expert Rev Mol Med 2012; 14: e13; PMID:22640744
  • Schwede A, Kramer S, Carrington M. How do trypanosomes change gene expression in response to the environment? Protoplasma 2012; 249: 223–38; PMID: 21594757; http://dx.doi.org/10.1007/s00709-011-0282-5
  • Ouellette M, Papadopoulou B. Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J Biol 2009; 8: 100; PMID:20017896; http://dx.doi.org/10.1186/jbiol203
  • Kramer S. Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol BiochemParasitol 2012; 181: 61–72; PMID:22019385; http://dx.doi.org/10.1016/j.molbiopara.2011.10.002
  • Clayton CE. Networks of gene expression regulation in Trypanosoma brucei. Mol Biochem Parasitol 2014; 195:96-106.
  • Mayho M, Fenn K, Craddy P, Crosthwaite S, Matthews K. Post-transcriptional control of nuclear-encoded cytochrome oxidase subunits in Trypanosoma brucei: evidence for genome-wide conservation of life-cycle stage-specific regulatory elements. Nucleic Acids Res. 2006; 34: 5312–24; PMID:17012283
  • Abanades DR, Ramirez L, Iborra S, Soteriadou K, Gonzalez VM, Bonay P, Alonso C, Soto M. Key role of the 3' untranslated region in the cell cycle regulated expression of the Leishmania infantum histone H2A genes: minor synergistic effect of the 5' untranslated region. BMC Mol Biol 2009; 10: 48; PMID:19460148
  • Walrad P, Paterou A, Costa-Serrano A, Matthews KR. Differential trypanosome surface coat regulation by a CCCH protein that co-associates with procyclin mRNA cis-elements. PLoS Pathog 2009; 5: e1000317; PMID:19247446
  • David M, Gabdank I, Ben-David M, Zilka A, Orr I, Barash D, Shapira M. Preferential translation of Hsp83 in Leishmania requires a thermosensitive polypyrimidine-rich element in the 3' UTR and involves scanning of the 5' UTR. RNA 2010; 16: 364–74; PMID:20040590
  • MacGregor P, Matthews KR. Identification of the regulatory elements controlling the transmission stage-specific gene expression of PAD1 in Trypanosoma brucei. Nucleic Acids Res. 2012; 40: 7705–17; PMID:22684509
  • Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010; 11: 113–27; PMID:20094052; http://dx.doi.org/10.1038/nrm2838
  • Aitken CE, Lorsch JR. A mechanistic overview of translation initiation in eukaryotes. Nat Struct Mol Biol 2012; 19: 568–76; PMID:22664984; http://dx.doi.org/10.1038/nsmb.2303
  • Valasek LS. 'Ribozoomin'–translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs). Curr Protein Pept Sci 2012; 13: 305–30; PMID:22708493; http://dx.doi.org/10.2174/138920312801619385
  • Hinnebusch AG. The scanning mechanism of eukaryotic translation initiation. Annu RevBiochem 2014; 83: 779–812; http://dx.doi.org/10.1146/annurev-biochem-060713-035802
  • von der Haar T, Gross JD, Wagner G, McCarthy JE. The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat Struct Mol Biol 2004; 11: 503–11; PMID:15164008; http://dx.doi.org/10.1038/nsmb779
  • Prevot D, Darlix JL, Ohlmann T. Conducting the initiation of protein synthesis: the role of eIF4G. Biol Cell 2003; 95: 141–56; PMID:12867079
  • Gallie DR. A tale of two termini: a functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation. Gene 1998; 216: 1–11; PMID:9714706; http://dx.doi.org/10.1016/S0378-1119(98)00318-7
  • Svitkin YV, Sonenberg N. Translational control by the poly(A) binding protein: a check for mRNA integrity. Mol Biol(Mosk) 2006; 40: 684–93; PMID:16913227
  • Gross JD, Moerke NJ, von der HT, Lugovskoy AA, Sachs AB, McCarthy JE, Wagner G. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 2003; 115: 739–50; PMID:14675538; http://dx.doi.org/10.1016/S0092-8674(03)00975-9
  • Marcotrigiano J, Lomakin IB, Sonenberg N, Pestova TV, Hellen CU, Burley SK. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol Cell 2001; 7: 193–203; PMID:11172724
  • Bellsolell L, Cho-Park PF, Poulin F, Sonenberg N, Burley SK. Two structurally atypical HEAT domains in the C-terminal portion of human eIF4G support binding to eIF4A and Mnk1. Structure 2006; 14: 913–23; PMID:16698552; http://dx.doi.org/10.1016/j.str.2006.03.012
  • Marintchev A, Wagner G. Translation initiation: structures, mechanisms and evolution. Q Rev Biophys 2004; 37: 197–284; PMID:16194295; http://dx.doi.org/10.1017/S0033583505004026
  • Dobrikov MI, Dobrikova EY, Gromeier M. Dynamic regulation of the translation initiation helicase complex by mitogenic signal transduction to eukaryotic translation initiation factor 4G. Mol Cell Biol 2013; 33: 937–46; PMID:23263986
  • Villa N, Do A, Hershey JW, Fraser CS. Human Eukaryotic Initiation Factor 4G (eIF4G) Protein Binds to eIF3c, -d, and -e to Promote mRNA Recruitment to the Ribosome. J Biol Chem 2013; 288: 32932–40; PMID:24092755; http://dx.doi.org/10.1074/jbc.M113.517011
  • Yanagiya A, Svitkin YV, Shibata S, Mikami S, Imataka H, Sonenberg N. Requirement of RNA binding of mammalian eukaryotic translation initiation factor 4GI (eIF4GI) for efficient interaction of eIF4E with the mRNA cap. Mol Cell Biol 2009; 29: 1661–9; PMID:19114555; http://dx.doi.org/10.1128/MCB.01187-08
  • Schutz P, Bumann M, Oberholzer AE, Bieniossek C, Trachsel H, Altmann M, Baumann U. Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc Natl Acad Sci U S A 2008; 105: 9564–9; PMID:18606994;http://dx.doi.org/10.1073/pnas.0800418105
  • Marintchev A, Edmonds KA, Marintcheva B, Hendrickson E, Oberer M, Suzuki C, Herdy B, Sonenberg N, Wagner G. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 2009; 136: 447–60; PMID:19203580; http://dx.doi.org/10.1016/j.cell.2009.01.014
  • Marintchev A, Wagner G. eIF4G and CBP80 share a common origin and similar domain organization: implications for the structure and function of eIF4G. Biochemistry 2005; 44: 12265–72; PMID:16156639; http://dx.doi.org/10.1021/bi051271v
  • Hernandez G, Vazquez-Pianzola P. Functional diversity of the eukaryotic translation initiation factors belonging to eIF4 families. Mech Dev 2005; 122: 865–76; PMID:15922571
  • Dhalia R, Reis CR, Freire ER, Rocha PO, Katz R, Muniz JR, Standart N, de Melo Neto OP. Translation initiation in Leishmania major: characterisation of multiple eIF4F subunit homologues. Mol Biochem Parasitol 2005; 140: 23–41; PMID:15694484
  • Yoffe Y, Leger M, Zinoviev A, Zuberek J, Darzynkiewicz E, Wagner G, Shapira M. Evolutionary changes in the Leishmania eIF4F complex involve variations in the eIF4E-eIF4G interactions. Nucleic Acids Res 2009; 37: 3243–53; PMID:19321500; http://dx.doi.org/10.1093/nar/gkp190
  • Freire ER, Dhalia R, Moura DM, da Costa Lima TD, Lima RP, Reis CR, Hughes K, Figueiredo RC, Standart N, Carrington M, et al. The four trypanosomatid eIF4E homologues fall into two separate groups, with distinct features in primary sequence and biological properties. Mol Biochem Parasitol 2011; 176: 25–36; PMID:21111007; http://dx.doi.org/10.1016/j.molbiopara.2010.11.011
  • Zinoviev A, Manor S, Shapira M. Nutritional stress affects an atypical cap-binding protein in Leishmania. RNA Biol 2012; 9:1450-60.
  • Jagus R, Bachvaroff TR, Joshi B, Place AR. Diversity of eukaryotic translational initiation factor eIF4E in protists. Comp Funct Genomics 2012; 2012: 134839; PMID:22778692
  • Zinoviev A, Shapira M. Evolutionary conservation and diversification of the translation initiation apparatus in trypanosomatids. Comp Funct Genomics 2012; 2012: 813718; PMID:22829751
  • Freire ER, Malvezzi AM, Vashisht AA, Zuberek J, Saada EA, Langousis G, Nascimento JD, Moura D, Darzynkiewicz E, Hill K, et al. Trypanosoma brucei translation initiation factor homolog EIF4E6 forms a tripartite cytosolic complex with EIF4G5 and a capping enzyme homolog. Eukaryot Cell 2014; 13: 896–908; PMID:24839125; http://dx.doi.org/10.1128/EC.00071-14
  • Freire ER, Vashisht AA, Malvezzi AM, Zuberek J, Langousis G, Saada EA, Nascimento Jde F, Stepinski J, Darzynkiewicz E, Hill K, et al. eIF4F-like complexes formed by cap-binding homolog TbEIF4E5 with TbEIF4G1 or TbEIF4G2 are implicated in post-transcriptional regulation in Trypanosoma brucei. RNA 2014; 20: 1272–86; PMID:24962368
  • Chang JH, Cho YH, Sohn SY, Choi JM, Kim A, Kim YC, Jang SK, Cho Y. Crystal structure of the eIF4A-PDCD4 complex. Proc Natl Acad Sci U S A 2009; 106: 3148–53; PMID:19204291; http://dx.doi.org/10.1073/pnas.0808275106
  • Liberman N, Dym O, Unger T, Albeck S, Peleg Y, Jacobovitch Y, Branzburg A, Eisenstein M, Marash L, Kimchi A. The crystal structure of the C-terminal DAP5/p97 domain sheds light on the molecular basis for its processing by caspase cleavage. J Mol Biol 2008; 383: 539–48; PMID:18722383; http://dx.doi.org/10.1016/j.jmb.2008.08.013
  • Mader S, Lee H, Pause A, Sonenberg N. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol 1995; 15: 4990–7; PMID:7651417
  • Tarun SZ, Jr., Wells SE, Deardorff JA, Sachs AB. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc NatlAcad Sci U S A 1997; 94: 9046–51; PMID:9256432
  • Imataka H, Gradi A, Sonenberg N. 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. 1998; 17: 7480–9; PMID:9857202
  • da Costa Lima TD, Moura DM, Reis CR, Vasconcelos JR, Ellis L, Carrington M, Figueiredo RC, de Melo Neto OP. Functional characterization of three leishmania poly(a) binding protein homologues with distinct binding properties to RNA and protein partners. Eukaryot.Cell 2010; 9: 1484–94; PMID:20675580
  • Dhalia R, Marinsek N, Reis CR, Katz R, Muniz JR, Standart N, Carrington M, de Melo Neto OP. The two eIF4A helicases in Trypanosoma brucei are functionally distinct. Nucleic Acids Res 2006; 34: 2495–507; PMID:16687655
  • Zinoviev A, Leger M, Wagner G, Shapira M. A novel 4E-interacting protein in Leishmania is involved in stage-specific translation pathways. Nucleic Acids Res 2011; 39: 8404–15; PMID:21764780
  • Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol.Cell 1999; 3: 707–16; PMID:10394359
  • Fraser CS, Pain VM, Morley SJ. The association of initiation factor 4F with poly(A)-binding protein is enhanced in serum-stimulated Xenopus kidney cells. J Biol Chem 1999; 274: 196–204; PMID:9867830
  • Contreras V, Richardson MA, Hao E, Keiper BD. Depletion of the cap-associated isoform of translation factor eIF4G induces germline apoptosis in C. elegans. Cell Death Differ 2008; 15: 1232–42; PMID:18451872
  • Hernandez G, Altmann M, Lasko P. Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci. 2010; 35: 63–73
  • Clarkson BK, Gilbert WV, Doudna JA. Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae. PLoSOne 2010; 5: e9114; PMID:20161741
  • Castello A, Alvarez E, Carrasco L. Differential cleavage of eIF4GI and eIF4GII in mammalian cells. Effects on translation. J Biol Chem 2006; 281: 33206–16; PMID:16959778; http://dx.doi.org/10.1074/jbc.M604340200
  • Gallie DR, Browning KS. eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J Biol Chem 2001; 276: 36951–60; PMID:11483601; http://dx.doi.org/10.1074/jbc.M103869200
  • Lee SH, McCormick F. p97/DAP5 is a ribosome-associated factor that facilitates protein synthesis and cell proliferation by modulating the synthesis of cell cycle proteins. EMBO J 2006; 25: 4008–19; PMID:16932749; http://dx.doi.org/10.1038/sj.emboj.7601268
  • Baker CC, Fuller MT. Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog. Development 2007; 134: 2863–9; PMID:17611220
  • Pereira MM, Malvezzi AM, Nascimento LM, da Costa Lima TD, Alves VS, Palma ML, Freire ER, Moura DM, Reis CR, de Melo Neto OP. The eIF4E subunits of two distinct trypanosomatid eIF4F complexes are subjected to differential post-translational modifications associated to distinct growth phases in culture. Mol Biochem Parasitol 2013; 190: 82–6; PMID:23867205; http://dx.doi.org/10.1016/j.molbiopara.2013.06.008
  • Urbaniak MD, Martin DM, Ferguson MA. Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res 2013; 12: 2233–44; PMID:23485197; http://dx.doi.org/10.1021/pr400086y
  • Cho PF, Poulin F, Cho-Park YA, Cho-Park IB, Chicoine JD, Lasko P, Sonenberg N. A new paradigm for translational control: inhibition via 5'-3' mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 2005; 121: 411–23; PMID:15882623; http://dx.doi.org/10.1016/j.cell.2005.02.024
  • Villaescusa JC, Buratti C, Penkov D, Mathiasen L, Planaguma J, Ferretti E, Blasi F. Cytoplasmic Prep1 interacts with 4EHP inhibiting Hoxb4 translation. PLoS One 2009; 4: e5213; PMID:19365557
  • Morales J, Mulner-Lorillon O, Cosson B, Morin E, Belle R, Bradham CA, Beane WS, Cormier P. Translational control genes in the sea urchin genome. Dev Biol 2006; 300: 293–307; PMID:16959243
  • Cheng S, Gallie DR. Competitive and noncompetitive binding of eIF4B, eIF4A, and the poly(A) binding protein to wheat translation initiation factor eIFiso4G. Biochemistry 2010; 49: 8251–65; PMID:20795652; http://dx.doi.org/10.1021/bi1008529
  • Kelley LA, Sternberg MJ. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009; 4: 363–71; PMID:19247286; http://dx.doi.org/10.1038/nprot.2009.2
  • Kelly S, Reed J, Kramer S, Ellis L, Webb H, Sunter J, Salje J, Marinsek N, Gull K, Wickstead B, et al. Functional genomics in Trypanosoma brucei: a collection of vectors for the expression of tagged proteins from endogenous and ectopic gene loci. Mol Biochem Parasitol 2007; 154: 103–9; PMID:17512617
  • Wickstead B, Ersfeld K, Gull K. Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol Biochem Parasitol 2002; 125: 211–6; PMID:12467990
  • Sunter J, Wickstead B, Gull K, Carrington M. A new generation of T7 RNA polymerase-independent inducible expression plasmids for Trypanosoma brucei. PLoS One 2012; 7: e35167; PMID:22511983
  • Tan R, Frankel AD. Structural variety of arginine-rich RNA-binding peptides. Proc Natl Acad Sci USA 1995; 92: 5282–6; PMID:7777498
  • Bastin P, Bagherzadeh Z, Matthews KR, Gull K. A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol Biochem Parasitol 1996; 77: 235–9; PMID:8813669
  • Wirtz E, Leal S, Ochatt C, Cross GA. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 1999; 99: 89–101
  • Poon SK, Peacock L, Gibson W, Gull K, Kelly S. A modular and optimized single marker system for generating Trypanosoma brucei cell lines expressing T7 RNA polymerase and the tetracycline repressor. Open Biol 2012; 2: 110037
  • Bangs JD, Uyetake L, Brickman MJ, Balber AE, Boothroyd JC. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei. Divergent ER retention signals in a lower eukaryote. J Cell Sci 1993; 105( Pt 4): 1101–13

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