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On the Origin and Early Evolution of Translation in Eukaryotes

  • Greco HernándezEmail author
  • Vincent G. Osnaya
  • Alejandra García
  • Mitzli X. Velasco
Chapter

Abstract

Eukaryotes emerged as a result of profound changes in the global biology of ancestral prokaryotes, being the outcome of large-scale evolutionary innovations at the morphological, metabolic and molecular levels. During these changes, fundamental processes sustaining life also evolved. One of them is translation, which is crucial for gene expression in all forms of life. While both mechanisms and components of the translation machinery are well known, how they evolved still remains poorly understood. In this chapter, we review recent advances in the understanding of how translation might have evolved during the origin and early evolution of eukaryotes from archaeal ancestors. The emerging view suggests that, while the fundamental process of translation remained well conserved across all forms of life, the initiation step underwent a substantial increase in evolution. This was probably due to the emergence of the nuclear membrane and split genes as well as the lack of both Shine-Dalgarno-like sequences in eukaryotic mRNAs and ribosomal protein S1. We discuss the possible evolutionary scenario where, during eukaryogenesis, mRNAs were perhaps translated in an IRES-dependent manner. It was only after IRES-dependent initiation was already established that capped and polyadenylated mRNAs, as well as novel initiation factors, were gradually and sequentially incorporated into protein synthesis, perhaps recruited from diverse cellular processes other than translation. Thus, this cap-independent initiation was later superseded in evolution by the cap-dependent mechanism.

Keywords

Translation evolution Translation initiation Shine-Dalgarno eIF4E eIF4G eIF3 eIF4A PABP Cap-dependent IRES 

Notes

Acknowledgments

This work was supported by the National Institute of Cancer (INCan), Mexico, and by the National Council of Science and Technology (CONACyT, grant no. 168154 to G.H.), Mexico.

References

  1. 1.
    Mathews MB, Sonenberg N, Hershey JWB. Origins and principles of translational control. In: Sonenberg N, Hershey JWB, Mathews MB, editors. Translational control of gene expression. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2000. p. 1–31.Google Scholar
  2. 2.
    Mathews MB, Sonenberg N, Hershey JWB. Origins and principles of translational control. In: Mathews MB, Sonenberg N, Hershey JWB, editors. Translational control in biology and medicine. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2007. p. 1–40.Google Scholar
  3. 3.
    Hernández G. Was the initiation of translation in early eukaryotes IRES-driven? Trends Biochem Sci. 2008;33:58–64.CrossRefPubMedGoogle Scholar
  4. 4.
    Hernández G. On the origin of the cap-dependent initiation of translation in eukaryotes. Trends Biochem Sci. 2009;34:166–75.CrossRefPubMedGoogle Scholar
  5. 5.
    Hernández G. On the emergence and evolution of the eukaryotic translation apparatus. In: Biyani M, editor. Cell-free protein synthesis. Rijekra, Croatia: InTech; 2012. p. 31–50.Google Scholar
  6. 6.
    Hernández G, Altmann M, Lasko P. Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci. 2010;35:63–73.CrossRefPubMedGoogle Scholar
  7. 7.
    Hernández G, Proud CG, Preiss T, Parsyan A. On the diversification of the translation apparatus across eukaryotes. Comp Funct Genom. 2012;2012:256848.Google Scholar
  8. 8.
    Benelli D, Londei P. Translation initiation in Archaea: conserved and domain-specific features. Biochem Soc Trans. 2011;19:89–93.CrossRefGoogle Scholar
  9. 9.
    Londei P. Evolution of translational initiation: news insights from the archaea. FEMS Microbiol Rev. 2005;29:185–200.CrossRefPubMedGoogle Scholar
  10. 10.
    Laursen BS, Sørensen HP, Mortensen KK, Sperling-Petersen HU. Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev. 2005;69:101–23.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Shine J, Dalgarno L. The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA. 1974;71:1342–6.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Shine J, Dalgarno L. Determinant of cistron specificity in bacterial ribosomes. Nature. 1975;254:34–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Jacob WF, Santer M, Dahlberg AE. A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins. Proc Natl Acad Sci USA. 1987;84:4757–61.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Dennis PP. Ancient ciphers: translation in archaea. Cell. 1997;89:1007–10.Google Scholar
  15. 15.
    Band L, Henner DJ. Bacillus subtilis requires a “stringent” Shine-Dalgarno region for gene expression. DNA. 1984;3:17–21.CrossRefPubMedGoogle Scholar
  16. 16.
    Steitz JA, Jakes K. How ribosomes select initiator regions in mRNA: base-pair formation between the 3’ terminus of 16 s rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc Natl Acad Sci USA. 1975;72:4734–8.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Jackson RJ. A comparative view of initiation site selection mechanisms. In: Sonenberg N, Hershey JWB, Mathews MB, editors. Translational control of gene expression. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory press; 2000. p. 127–83.Google Scholar
  18. 18.
    Wilson DN, Nierhaus KH. Ribosomal proteins in the spotlight. Crit Rev Biochem Mol Biol. 2005;40:243–67.CrossRefPubMedGoogle Scholar
  19. 19.
    Moll I, Grill S, Gründling A, Bläsi U. Effects of ribosomal proteins S1, S2 and the DeaD/CsdA DEAD-box helicase on translation of leaderless and canonical mRNAs in Escherichia coli. Mol Microbiol. 2002;44:1387–96.CrossRefPubMedGoogle Scholar
  20. 20.
    Delvillani F, Papiani G, Dehò G, Briani F. S1 ribosomal protein and the interplay between translation and mRNA decay. Nucleic Acid Res. 2011;39:7702–15.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Sengupta J, Agrawal RK, Frank J. Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc Natl Acad Sci USA. 2001;98:11991–6.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Kaberdin VR, Bläsi U. Translation initiation and the fate of bacterial mRNAs. FEMS Microbiol Rev. 2006;30:967–79.CrossRefPubMedGoogle Scholar
  23. 23.
    Komarova AV, Tchufistova LS, Supina EV, Boni IV. Protein S1 counteracts the inhibitory effect of the extended Shine-Dalgarno sequence on translation. RNA. 2002;8:1137–47.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Shell SS, Wang J, Lapierre P, Mir M, Chase MR, Pyle MM, Gawande R, Ahmad R, Sarracino DA, Ioerger TR, Fortune SM, Derbyshire KM, Wade JT, Gray T. Leaderless transcripts and small proteins are common features of the mycobacterial translational landscape. PLoS Genet. 2015;11:e1005641.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ma J, Campbell A, Karlin S. Correlation between Shine-Dalgarno sequence and gene features such as predicted expression levels and operon structure. J Bacteriol. 2002;184:5733–45.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Torarinsson E, Klenk HP, Garret RA. Divergent transcriptional and translational signals in Archaea. Environ Microbiol. 2005;7:45–54.CrossRefGoogle Scholar
  27. 27.
    Sensen CW. Organizational characteristics and information content of an archaeal genome: 156 kb of sequence from Sulfolobus solfataricus P2. Mol Microbiol. 1996;22:175–91.CrossRefPubMedGoogle Scholar
  28. 28.
    Weiner J, Herrmann R, Browning GF. Transcription in Mycoplasma pneumoniae. Nucleic Acid Res. 2000;28:4488–96.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Chang B, Halgamuge S, Tang SL. Analysis of SD sequences in completed microbial genomes: non-SD-led genes are as common as SD-led genes. Gene. 2006;373:90–9.CrossRefPubMedGoogle Scholar
  30. 30.
    Nakagawa S, Niimura Y, Miura KI, Gojobori T. Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc Natl Acad Sci USA. 2010;107:6382–7.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Benelli D, Londei P. Begin at the beginning: evolution of translational initiation. Res Microbiol. 2009;160:493–501.CrossRefPubMedGoogle Scholar
  32. 32.
    Brenneis M, Hering O, Lange C, Soppa J. Experimental characterization of Cis-acting elements important for translation and transcription in halophilic archaea. PLoS Genet. 2007;3:e229.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Zheng X, Hu GQ, She ZS, Zhu H. Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes. BMC Genom. 2011;12:361–70.CrossRefGoogle Scholar
  34. 34.
    Slupska MM, King AG, Fitz-Gibbon S, Besemer J, Borodovsky M, Miller JH. Leaderless transcripts of the crenarchaeal hyperthermophile Pyrobaculum aerophilum. J Mol Biol. 2001;309:347–60.CrossRefPubMedGoogle Scholar
  35. 35.
    Tolstrup N, Sensen CW, Garrett RA, Clausen IG. Two different and highly organized mechanisms of translation initiation in the archaeon Sulfolobus solfataricus. Extremophiles. 2000;4:175–9.CrossRefPubMedGoogle Scholar
  36. 36.
    Jäger D, Förstner KU, Sharma CM, Santangelo TJ, Reeve J. Primary transcriptome map of the hyperthermophilic archaeon Thermococcus kodakarensis. BMC Genom. 2014;15:684.CrossRefGoogle Scholar
  37. 37.
    Cortes T, Schubert OT, Rose G, Arnvig KB, Comas I, Aebersold R, Young DB. Genome-wide mapping of transcriptional start sites defines an extensive leaderless transcriptome in Mycobacterium tuberculosis. Cell Rep. 2013;5:1121–31.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Kramer P, Gäbel K, Pfeiffer F, Soppa J. Haloferax volcanii, a prokaryotic species that does not use the Shine Dalgarno mechanism for translation initiation at 5’-UTRs. PLoS ONE. 2014;9:e94979.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Sullivan MJ, Curson AR, Shearer N, Todd JD, Green RT, Johnston AW. Unusual regulation of a leaderless operon involved in the catabolism of dimethylsulfoniopropionate in Rhodobacter sphaeroides. PLoS ONE. 2011;6:e15972.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Krishnan KM, Van Etten WJ, Janssen GR. Proximity of the start codon to a leaderless mRNA’s 5’ terminus is a strong positive determinant of ribosome binding and expression in Escherichia coli. J Bacteriol. 2010;192:6482–5.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina AC, Engelberg-Kulka H, Moll I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell. 2011;147:147–57.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    La Teana A, Benelli D, Londei P, Bläsi U. Translation initiation in the crenarchaeon Sulfolobus solfataricus: eukaryotic features but bacterial route. Biochem Soc Trans. 2013;41:350–5.CrossRefPubMedGoogle Scholar
  43. 43.
    Hering O, Brenneis M, Beer J, Suess B, Soppa J. A novel mechanism for translation initiation operates in haloarchaea. Mol Microbiol. 2009;71:1451–63.CrossRefPubMedGoogle Scholar
  44. 44.
    Omotajo D, Tate T, Cho H, Choudhary M. Distribution and diversity of ribosome binding sites in prokaryotic genomes. BMC Genom. 2015;16:e604.CrossRefGoogle Scholar
  45. 45.
    Balakin AG, Skripkin EA, Shatsky IN, Bogdanov AA. Unusual ribosome binding properties of mRNA encoding bacteriophage lambda repressor. Nucleic Acid Res. 1992;20:563–71.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Brock JE, Pourshahian S, Giliberti J, Limbach PA, Janssen G. Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5′-terminal AUG. RNA. 2008;14:2159–69.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Van Etten WJ, Janssen GR. An AUG initiation codon, not codon-anticodon complementarity, is required for the translation of unleadered mRNA in Escherichia coli. Mol Microbiol. 1998;27:987–1001.CrossRefPubMedGoogle Scholar
  48. 48.
    Grill S, Gualerzi CO, Londei P, Bläsi U. Selective stimulation of translation of leaderless mRNA by initiation factor 2: evolutionary implications for translation. EMBO J. 2000;19:4101–10.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    O’Donnell SM, Janssen GR. The initiation codon affects ribosome binding and translational efficiency in Escherichia coli of cI mRNA with or without the 5’ untranslated leader. J Bacteriol. 2001;183:1277–83.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    O’Donnell SM, Janssen GR. Leaderless mRNAs bind 70S ribosomes more strongly than 30S ribosomal subunits in Escherichia coli. J Bacteriol. 2002;184:6730–3.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Moll I, Grill S, Gualerzi CO, Bläsi U. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol. 2002;43:239–46.CrossRefPubMedGoogle Scholar
  52. 52.
    Moll I, Hirokawa G, Kiel MC, Kaji A, Bläsi U. Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acid Res. 2004;32:3354–63.Google Scholar
  53. 53.
    Kudla G, Murray AW, Tollervey D, Plotkin JB. Coding-sequence determinants of gene expression in Escherichia coli. Science. 2009;324:255–8.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Scharff LB, Childs L, Walther D, Bock R. Local absence of secondary structure permits translation of mRNAs that lack ribosome-binding site. PLoS Genet. 2011;7:e1002155.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Fox GE. Origin and evolution of the ribosome. Cold Spring Harb Perspect Biol. 2012;2:e003483.Google Scholar
  56. 56.
    Golshani A, Krogan NJ, Xu J, Pacal M, Yang XC, Ivanov I, Providenti MA, Ganoza MC, Ivanov IG. Abou Haidar MG. Escherichia coli mRNAs with strong Shine/Dalgarno sequences also contain 5’ end sequences complementary to domain #17 on the 16S ribosomal RNA. Biochem Biophys Res Commun. 2004;316:978–83.CrossRefPubMedGoogle Scholar
  57. 57.
    Loechel S, Inamine JM, Hu PC. A novel translation initiation region from Mycoplasma genitalium that functions in Escherichia coli. Nucleic Acids Res. 1991;19:6905–11.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Jenner L, Romby P, Rees B, Schulze-Briese C, Springer M, Ehresmann C, Ehresmann B, Moras D, Yusupova G, Yusupov M. Translational operator of mRNA on the ribosome: how repressor proteins exclude ribosome binding. Science. 2005;308:120–3.CrossRefPubMedGoogle Scholar
  59. 59.
    Kyrpides NC, Woese CR. Universally conserved translation initiation factors. Proc Natl Acad Sci USA. 1998;95:224–8.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Koonin EV. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 2010;11:209.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Koumandou VL, Wickstead B, Ginger ML, van der Giezen M, Dacks JB, Field MC. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit Rev Biochem Mol Biol. 2013;48:373–96.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Woese CR. On the evolution of cells. Proc Natl Acad Sci USA. 2002;99:8742–7.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Wu CJ, Janssen GR. Translation of vph mRNA in Streptomyces lividans and Escherichia coli after removal of the 5’ untranslated leader. Mol Microbiol. 1996;22:339–55.CrossRefPubMedGoogle Scholar
  64. 64.
    Sonenberg N, Hinnebusch A. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009;136:731–45.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Hinnebusch AG. Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol Mol Biol Rev. 2011;75:434–67.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Pelletier J. Sonenberg N Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature. 1988;334:320–5.CrossRefPubMedGoogle Scholar
  68. 68.
    Jang SK, Kräusslich HG, Nicklin MJ, Duke GM, Palmenberg AC, Wimmer E. A segment of the 5’ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol. 1988;62:2636–43.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Macejak DG, Sarnow P. Internal initiation of translation mediated the 5’UTR leader of a cellular mRNA. Nature. 1991;353:90–4.CrossRefPubMedGoogle Scholar
  70. 70.
    Martínez-Salas E, Piñeiro D, Fernández N. Alternative mechanisms to initiate translation in eukaryotic mRNAs. Comp Funct Genom. 2012;2012:391546.CrossRefGoogle Scholar
  71. 71.
    Elroy-Stein O, Merrick WC. Translation initiation via cellular internal ribosome entry sites. In: Mathews MB, Sonenberg N, Hershey JWB, editors. Translational control in biology and medicine. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2007. p. 155–72.Google Scholar
  72. 72.
    Stoneley M, Willis AE. Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene. 2004;23:3200–7.CrossRefPubMedGoogle Scholar
  73. 73.
    Dounda JA, Sarnow P. Translation initiation by viral internal ribosome entry sites. In: Mathews MB, Sonenberg N, Hershey JWB, editors. Translational control in biology and medicine. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2007. p. 129–53.Google Scholar
  74. 74.
    Guy L, Saw JH, Ettema TJG. The archaeal legacy of eukaryotes: a phylogenomic perspective. In: Keeling PJ, Koonin EV, editors. The origin and evolution of eukaryotes. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2014. p. 97–128.Google Scholar
  75. 75.
    Poole AM, Gribaldo S. Eukaryotic origins: how and when was the mitochondrion acquired? In: Keeling PJ, Koonin EV, editors. The origin and evolution of eukaryotes. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2014. p. 129–40.Google Scholar
  76. 76.
    McFadden GI. Origin and evolution of plastids and photosynthesis in eukaryotes. In: Keeling PJ, Koonin EV, editors. The origin and evolution of eukaryotes. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2014. p. 263–70.Google Scholar
  77. 77.
    Williams TA, Foster PG, Cox CJ, Embley M. An archaeal origin of eukaryotes supports only two primary domains of life. Nature. 2013;504:231–6.CrossRefPubMedGoogle Scholar
  78. 78.
    Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA. 1977;74:5088–90.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Woese CR, Fox GE. The concept of cellular evolution. J Mol Evol. 1977;10:1–6.CrossRefPubMedGoogle Scholar
  80. 80.
    Woese CR. Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA. 2000;97:8392–6.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM. The archaebacterial origin of eukaryotes. Proc Natl Acad Sci USA. 2008;105:20356–61.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Williams TA, Foster PG, Nye TM, Cox CJ, Embley TM. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Sci. 2012;279:4870–9.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Guy L, Ettema TJG. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 2011;19:580–7.CrossRefPubMedGoogle Scholar
  84. 84.
    Pedulla N, Palermo R, Hasenöhr D, Bläsi U, Cammarano P, Londei P. The archaeal eIF2 homologue: functional properties of an ancient translation initiation factor. Nucleic Acid Res. 2005;33:1804–12.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Aravind L, Koonin EV. Eukaryotic-specific domains in translation initiation factors: implications for translation regulation and evolution of the translation system. Genome Res. 2000;10:1172–84.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Lecompte O, Ripp R, Thierry JC, Moras D, Poch O. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acid Res. 2002;30:5382–90.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Wilson DN, Cate JHD. The structure and function of the eukaryotic ribosome. In: Hershey JWB, Sonenberg N, Mathews MB, editors. Protein synthesis and translational control. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2012. p. 11–27.Google Scholar
  88. 88.
    Dresios J, Panopoulos P, Synetos D. Eukaryotic ribosomal proteins lacking a eubacterial counterpart: important players in ribosomal function. Mol Microbiol. 2006;59:1651–63.CrossRefPubMedGoogle Scholar
  89. 89.
    Wolf YI, Aravind L, Grishin N, Koonin EV. Evolution of aminoacyl-tRNA synthetases-analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 1999;9:689–710.PubMedGoogle Scholar
  90. 90.
    O’Donoghue P, Luthey-Schulten Z. On the Evolution of Structure in Aminoacyl-tRNA Synthetases. Microbiol Mol Biol Rev. 2003;67:550–3.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Petrov AS, Bernier CR, Hsiao C, Norris AM, Kovacs NA, Waterbury CC, Stepanov VG, Harvey SC, Fox GE, Wartell RM, Hud NV, Williams LD. Evolution of the ribosome at atomic resolution. Proc Natl Acad Sci USA. 2014;111:10251–6.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Roberts E, Sethi A, Montoya J, Woese CR, Luthey-Schulten Z. Molecular signatures of ribosomal evolution. Proc Natl Acad Sci USA. 2008;105:13953–8.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Lynch M. The origins of genome architecture. Sunderland, Massachusetts: Sinauer Associates, Inc., Publishers; 2007.Google Scholar
  94. 94.
    Martin W, Koonin EV. Introns and the origin of nucleus-cytosol compartmentalization. Nature. 2006;440:41–5.CrossRefPubMedGoogle Scholar
  95. 95.
    Taylor DJ, Frank J, Kinzy TG. Structure and function of the eukaryotic ribosome and elongation factors. In: Mathews MB, Sonenberg N, Hershey JWB, editors. Translational control in biology and medicine. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2007. p. 59–85.Google Scholar
  96. 96.
    Yokoyama T, Suzuki T. Ribosomal RNAs are tolerant toward genetic insetions: evolutionary origin of the expansion segments. Nucleic Acid Res. 2008;36:3539–51.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Hartman H, Favaretto P, Smith TF. The archaeal origins of the eukaryotic translational system. Archaea. 2006;2:1–9.CrossRefPubMedGoogle Scholar
  98. 98.
    Klinge S, Voigst-Hoffmann F, Leibundgut M, Ban N. Atomic structures of the eukaryotic ribosome. Trends Biochem. 2012;37:189–98.CrossRefGoogle Scholar
  99. 99.
    Kozak M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene. 2005;361:13–37.CrossRefPubMedGoogle Scholar
  100. 100.
    Lukaszewicz M. M. F, Jerouville B, Stas A, Boutry M. In vivo evaluation of the context sequence of the translation initiation codon in plants. Plant Sci. 2000;154:89–98.CrossRefPubMedGoogle Scholar
  101. 101.
    Lutcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA. Selection of AUG initiation codons differs in plants and animals. EMBO J. 1987;6:43–8.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Cigan M, Donahue TF. Sequence and structural features associated with translational initiator regions in yeast - a review. Gene. 1987;59:1–18.CrossRefPubMedGoogle Scholar
  103. 103.
    Donahue TF, Cigan M. Sequence and structural requirements for efficient translation in yeast. Meth Enzymol. 1990;185:366–71.CrossRefPubMedGoogle Scholar
  104. 104.
    Cavener DR. Eukaryotic start and stop translation sites. Nucleic Acid Res. 1991;19:3185–92.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Kim Y, Lee G, Jeon E, Sohn EJ, Lee Y, Kang H, Lee Dw, Kim DH, Hwang I. The immediate upstream region of the 5´-UTR from the AUG start codon has a pronounced effect on the translational efficiency in Arabidopsis thaliana. Nucleic Acid Res. 2014;14:485–98.Google Scholar
  106. 106.
    Kawaguchi R, Bailey-Serres J. mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acid Res. 2005;33:955–65.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Nakagawa S, Niimura Y, Gojobori T, Tanaka H, Miura K. Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes. Nucleic Acids Res. 2008;36:861–71.CrossRefPubMedGoogle Scholar
  108. 108.
    Lynch M, Scofield DG, Hong X. The evolution of transcription-initiation sites. Mol Biol Evol. 2005;22:1137–46.CrossRefPubMedGoogle Scholar
  109. 109.
    Mignone F, Gissi C, Liuni S, Pesole L. Untranslated regions of mRNAs. Genome Biol. 2002;3:1–10.CrossRefGoogle Scholar
  110. 110.
    Mazumder B, Seshadri V, Fox PL. Translational control by the 3’-UTR: the ends specify the means. Trends in Biochem Sci. 2003;28:91–8.CrossRefGoogle Scholar
  111. 111.
    Hentze MW, Gebauer F, Preiss T. cis-Regulatory sequences and trans-actin factors in translational control. In: Mathews MB, Sonenberg N, Hershey JWB, editors. Translational control in biology and medicine. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2007. p. 269–96.Google Scholar
  112. 112.
    Pesole G, Mignone F, Gissi C, Grillo G, Licciulli F, Liuni S. Structural and functional features of eukaryotic mRNA untranslated regions. Gene. 2001;276:73–81.CrossRefPubMedGoogle Scholar
  113. 113.
    Svitkin YV, Ovchinnikov LP, Dreyfuss G, Sonenberg N. General RNA binding proteins render translation cap dependent. EMBO J. 1996;15:7147–55.PubMedPubMedCentralGoogle Scholar
  114. 114.
    Araujo PR, Yoon K, Ko D, Smith AD, Qiao M, Suresh U, Burns SC, Penalva LOF. Before it gets started: regulating translation at the 5´-UTR. Comp Funct Genom. 2012;12:1–8.CrossRefGoogle Scholar
  115. 115.
    Alekhina AM, Vassilenko KS. Translation initiation in eukaryotes: versatility of the scanning model. Biochemistry (Moscow). 2012;77:1465–77.CrossRefPubMedGoogle Scholar
  116. 116.
    van der Velden A, Thomas AAM. The role of the 5´untranslated region of an mRNA is translation regulation during development. Int J Biochem Cell Biol. 1999;31:87–106.CrossRefPubMedGoogle Scholar
  117. 117.
    Faye MD, Holcik M. The role of IRES trans-acting factors in carcinogenesis. Biochim Biophys Acta. 2015;1849:887–97.CrossRefPubMedGoogle Scholar
  118. 118.
    Komar AA, Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle. 2011;10:229–40.CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    King HA, Cobbold LC, Willis AE. The role of IRES trans-acting factors in regulating translation initiation. Biochem Soc Trans. 2010;38:1581–6.CrossRefPubMedGoogle Scholar
  120. 120.
    Davuluri RV, Suzuki Y, Sugano S, Zhang MQ. CART Classification of Human 5´UTR Sequences. Genome Res. 2000;10:1807–16.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Resch AM, Ogurstov AY, Rogozin IB, Shabalina SA, Koonin EV. Evolution of alternative and constitutive regions of mammalian 5’UTRs. BMC Genom. 2009;10:162.CrossRefGoogle Scholar
  122. 122.
    Moshonov S, Elfakes R, Golan-Mashiach M, Sinvani H, Dikstein R. Links between core promoter and basic gene features influence gene expression. BMC Genom. 2008;9:92.CrossRefGoogle Scholar
  123. 123.
    Grillo G, Turi A, Licciulli F, Mignone F, Liuni S, Banfi S, Gennarino VA, Horner DS, Pavesi G, Picardi E, Pesole G. UTRdb and UTRsite (RELEASE 2010): a collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acid Res. 2010;38:D75–80.Google Scholar
  124. 124.
    Vogel C, Abreu RS, Ko D, Le SY, Shapiro BA, Burns SC, Sandhu D, Boutz DR, Marcotte EM, Penalva LO. Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol Syst Biol. 2010;6:400.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    de Sousa R, Penalva LO, Marcotte EM, Vogel C. Global signatures of protein and mRNA expression levels. Mol BioSyst. 2009;5:1512–26.Google Scholar
  126. 126.
    Adam RD. The Giardia lamblia genome. Int J Parasitol. 2000;30:475–84.CrossRefPubMedGoogle Scholar
  127. 127.
    Bruchhaus I, Leippe M, Lioutas C, Tannich E. Unusual gene organization in the protozoan parasite Entamoeba histolytica. DNA Cell Biol. 1993;12:925–33.PubMedGoogle Scholar
  128. 128.
    Elfakes R, Dikstein R. A translation initiation element specific to mRNAs with very short 5UTR that Also regulates transcription. PLoS ONE. 2008;3:e3094.CrossRefGoogle Scholar
  129. 129.
    Elfakes R, Sinvani H, Haimov O, Svitkin Y, Sonenberg N, Dikstein R. Unique translation initiation of mRNAs-containing TISU element. Nucleic Acid Res. 2011;39:7598–609.CrossRefGoogle Scholar
  130. 130.
    Sinvani H, Haimov O, Svitkin Y, Sonenberg N, Tamarkin-Ben-Harush A, Viollet B, Dikstein R. Translational tolerance of mitochondrial genes to metabolic energy stress involves TISU and eIF1-eIF4G1 cooperation in start codon selection. Cell Metab. 2015;21:479–92.CrossRefPubMedGoogle Scholar
  131. 131.
    Zhaxybayeva O, Gogarten P. Spliceosomal introns: new insights into their evolution. Curr Biol. 2003;13:R764–6.CrossRefPubMedGoogle Scholar
  132. 132.
    Lambowitz AM, Zimmerly S. Mobile group II introns. Annu Rev Genet. 2004;38:1–35.CrossRefPubMedGoogle Scholar
  133. 133.
    Rogozin IB, Carmel L, Csuros M, Koonin EV. Origin and evolution of spliceosomal introns. Biol Direct. 2012;16:11.CrossRefGoogle Scholar
  134. 134.
    Irimia M. Roy SW (2014) Origin of spliceosomal introns and alternative splicing. In: Keeling PJ, Koonin EV, editors. The origin and evolution of eukaryotes. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2014. p. 295–316.Google Scholar
  135. 135.
    Maone E, Di Stefano M, Berardi A, Benelli D, Marzi S, La Teana A, Londei P. Functional analysis of the translation factor aIF2/5B in the thermophilic archaeon Sulfolobus solfataricus. Mol Microbiol. 2007;65:700–13.CrossRefPubMedPubMedCentralGoogle Scholar
  136. 136.
    Lee JH, Choi SK, Roll-Mecak A, Burley SK, Dever TE. Universal conservation in translation initiation revealed by human and archaeal homologs of bacterial translation initiation factor IF2. Proc Natl Acad Sci USA. 1999;96:4342–7.CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Kyrpides NC, Woese CR. Archaeal translation initiation revisited: the initiation factor 2 and eukaryotic initiation factor 2B a- b-d subunit families. Proc Natl Acad Sci USA. 1998;95:3726–30.CrossRefPubMedPubMedCentralGoogle Scholar
  138. 138.
    Pánek J, Klolár M, Vohradsky J, Valásek LS. An evolutionary conserved pattern of 18S rRNA sequence complementary to mRNA 5´UTRs and its implications for eukaryotic gene translation regulation. Nucleic Acid Res. 2013;41:7625–34.CrossRefPubMedPubMedCentralGoogle Scholar
  139. 139.
    Matveeva OV, Shabalina S. Intermolecular mRNA-rRNA hybridization and the distribution of potential interaction regions in murine 18S rRNA. Nucleic Acid Res. 1993;21:1007–11.CrossRefPubMedPubMedCentralGoogle Scholar
  140. 140.
    Mauro VP, Edelman GM. rRNA-like sequences occur in diverse primary transcripts: implications for the control of gene expression. Proc Natl Acad Sci USA. 1997;94:422–7.CrossRefPubMedPubMedCentralGoogle Scholar
  141. 141.
    Tranque P, Hu MC, Edelman GM, Mauro VP. rRNA complementarity within mRNAs: a possible basis for mRNA-ribosome interactions and translational control. Proc Natl Acad Sci USA. 1998;95:12238–43.CrossRefPubMedPubMedCentralGoogle Scholar
  142. 142.
    Pisarev AV, Kolupaeva VG, Pisareva VP, Merrick WC, Hellen CUT, Pestova T. Specific functional interactions of nucleotides at key −3 and +4 positions flanking the initiation codon with components of the mammalian 48S translation initiation complex. Genes Dev. 2006;20:624–36.CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Jacob F. Evolution and Tinkering. Science. 1977;196:1161–6.CrossRefPubMedGoogle Scholar
  144. 144.
    Gould SJ, Vrba ES. Exaptation - a missing term in the science of form. Paleobiology. 1982;8:4–15.CrossRefGoogle Scholar
  145. 145.
    Nojima T, Hirose T, Kimura H, Hagiwara M. The interaction between cap-binding complex and RNA export factor is required for intronless mRNA export. J Biol Chem. 2007;282:15645–51.CrossRefPubMedGoogle Scholar
  146. 146.
    Vinciguerra P, Stutz F. mRNA export: an assembly line from genes to nuclear pores. Curr Opin Cell Biol. 2004;16:285–92.CrossRefPubMedGoogle Scholar
  147. 147.
    Cougot N, van Dijk E, Babajko S, Séraphin B. Cap-tabolism. Trends Biochem Sci. 2004;29:436–44.CrossRefPubMedGoogle Scholar
  148. 148.
    Ling SH, Qamra R, Song H. Structural and functional insights into eukaryotic mRNA decapping. Wiley Interdiscip Rev RNA. 2011;2:193–208.CrossRefPubMedGoogle Scholar
  149. 149.
    Topisirovic I, Svitkin YV, Sonenberg N, Shatkin AJ. Cap and cap-binding proteins in the control of gene expression. Wiley Interdiscip Rev RNA. 2010;2:277–98.CrossRefPubMedGoogle Scholar
  150. 150.
    Ghosh A, Lima CD. Enzymology of RNA cap synthesis. Wiley Interdiscip Rev RNA. 2010;1:152–72.CrossRefPubMedPubMedCentralGoogle Scholar
  151. 151.
    Martinez-Rucobo FW, Kohler R, van de Waterbeemd M, Heck AJ, Hemann M, Herzog F, Stark H, Cramer P. Molecular basis of transcription-coupled pre-mRNA capping. Mol Cell. 2015;58:1079–89.CrossRefPubMedGoogle Scholar
  152. 152.
    Reed R. Coupling transcription, splicing and mRNA export. Curr Opin Cell Biol. 2003;15:326–31.CrossRefPubMedGoogle Scholar
  153. 153.
    Rhoads RE. eIF4E: new family members, new binding partners, new roles. J Biol Chem. 2009;284:16711–5.CrossRefPubMedPubMedCentralGoogle Scholar
  154. 154.
    Rezende AM, Assis LA, Nunes EC, Lima TD, Marchini FK, Freire ER, Reis CR, de Melo Neto OP. The translation initiation complex eIF3 in trypanosomatids and other pathogenic excavates-identification of conserved and divergent features based on orthologue analysis. BMC Genom. 2014;15:1175.CrossRefGoogle Scholar
  155. 155.
    Hinnebusch AG. eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci. 2006;31:553–60.CrossRefPubMedGoogle Scholar
  156. 156.
    des Georges A, Dhote V, Kuhn L, Hellen CU, Pestova TV, Frank J, Hashem Y. Structure of mammalian eIF3 in the context of the 43S preinitiation complex. Nature. 2015;525:491–5.Google Scholar
  157. 157.
    Querol-Audi J, Sun C, Vogan JM, Smith MD, Gu Y, Cate JH, Nogales E. Architecture of human translation initiation factor 3. Structure. 2013;21:920–8.CrossRefPubMedPubMedCentralGoogle Scholar
  158. 158.
    Pereira RV, de Gomes MS, Jannotti-Passos LK, Borges WC, Guerra-Sá R. Characterisation of the COP9 signalosome in Schistosoma mansoni parasites. Parasitol Res. 2013;112:2245–53.CrossRefPubMedGoogle Scholar
  159. 159.
    Schwechheimer C. The COP9 signalosome (CSN): an evolutionary conserved proteolysis regulator in eukaryotic development. Biochim Biophys Acta. 2004;1695:45–54.CrossRefPubMedGoogle Scholar
  160. 160.
    Scheel H, Hofmann K. Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinformatics. 2005;6:71.CrossRefPubMedPubMedCentralGoogle Scholar
  161. 161.
    Wei N, Serino G, Deng XW. The COP9 signalosome: more than a protease. Trends Biochem Sci. 2008;33:592–600.CrossRefPubMedGoogle Scholar
  162. 162.
    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.CrossRefPubMedGoogle Scholar
  163. 163.
    Marcotrigiano J, Lomakin IB, Sonenberg N, Pestova TV, Hellen CUT, Burley SK. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol Cell. 2001;7:193–203.CrossRefPubMedGoogle Scholar
  164. 164.
    Pontig CP. Novel eIF4G domain homologues linking mRNA translation with nonsense-mediated mRNA decay. Trends Biochem Sci. 2000;25:423–6.CrossRefGoogle Scholar
  165. 165.
    Mendell JT, Medghalchi SM, Lake RG, Noensie EN, Dietz HC. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol Cell Biol. 2000;20:8944–57.CrossRefPubMedPubMedCentralGoogle Scholar
  166. 166.
    Kobe B, Gleichmann T, Horne J, Jennings IG, Scotney PD, Teh T. Turn up the HEAT. Structure. 1999;7:R91–7.CrossRefPubMedGoogle Scholar
  167. 167.
    Andrade MA, Petosa C, O’Donoghue SI, Muller CW, Bork P. Comparison of ARM and HEAT protein repeats. J Mol Biol. 2001;309:1–18.CrossRefPubMedGoogle Scholar
  168. 168.
    Sonenberg N. eIF4E, the mRNA cap-binding protein: from basic discovery to translational research. Biochem Cell Biol. 2008;86:178–83.CrossRefPubMedGoogle Scholar
  169. 169.
    Layana C, Ferrero P, Rivera-Pomar R. Cytoplasmic ribonucleoprotein foci in eukaryotes: hotspots of bio(chemical) diversity. Comp Funct Genom. 2012;2012:504292.CrossRefGoogle Scholar
  170. 170.
    Thomas MG, Loschi M, Desbats MA, Boccaccio GL. RNA granules: the good, the bad and the ugly. Cell Sign. 2011;23:324–34.CrossRefGoogle Scholar
  171. 171.
    Hernández G, Vazquez-Pianzola P. Functional diversity of the eukaryotic translation initiation factors belonging to eIF4 families. Mech Dev. 2005;122:865–76.CrossRefPubMedGoogle Scholar
  172. 172.
    Strudwick S, Borden KLB. The emerging roles of translation factor eIF4E in the nucleus. Differentiation. 2002;70:10–22.CrossRefPubMedGoogle Scholar
  173. 173.
    Osborne MJ, Borden KLB. The eukaryotic translation initiation factor eIF4E in the nucleus: taking the road less traveled. Immunol Rev. 2015;263:210–23.CrossRefPubMedPubMedCentralGoogle Scholar
  174. 174.
    Li L, Wang CC. Identification in the ancient protist Giardia lamblia of two eukaryotic translation initiation factor 4E homologues with distinctive functions. Eukaryot Cell. 2005;4:948–59.CrossRefPubMedPubMedCentralGoogle Scholar
  175. 175.
    Ramirez CV, Vilela C, Berthelot K, McCarthy JE. Modulation of eukaryotic mRNA stability via the cap-binding translation complex eIF4F. J Mol Biol. 2002;318:951–62.CrossRefPubMedGoogle Scholar
  176. 176.
    Deutscher MP, Li Z. Exoribonucleases and their multiple roles in RNA metabolism. Prog Nucleic Acid Res Mol Biol. 2001;66:67–105.CrossRefPubMedGoogle Scholar
  177. 177.
    Shuman S. The mRNA capping apparatus as drug target and guide to eukaryotic phylogeny. Cold Spring Harb Symp Quant Biol. 2001;66:301–12.CrossRefPubMedGoogle Scholar
  178. 178.
    Anantharaman V, Koonin EV, Aravind L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acid Res. 2002;30:1427–64.CrossRefPubMedPubMedCentralGoogle Scholar
  179. 179.
    Muhlemann O. Recognition and elimination of nonsense mRNA. Biochim Biophys Acta. 2008;1779:538–49.CrossRefPubMedGoogle Scholar
  180. 180.
    Eliseeva IA, Lyabin DN, Ovchinnikov LP. Poly(A)-binding proteins: structure, domain organization, and activity regulation. Biochemistry (Moscow). 2013;78:1377–91.CrossRefPubMedGoogle Scholar
  181. 181.
    Derry MC, Yanagiya A, Martineau Y, Sonenberg N. Regulation of poly(A)-binding protein through PABP-interacting proteins. Cold Spring Harb Quant Biol. 2006;71:537–43.CrossRefGoogle Scholar
  182. 182.
    Kuhn U, Wahle E. Structure and function of poly(A) binding proteins. Biochim Biophys Acta. 2004;1678:67–84.CrossRefPubMedGoogle Scholar
  183. 183.
    Vazquez-Pianzola P, Suter B. Conservation of the RNA transport machineries and their coupling to translation control across eukaryotes. Comp Funct Genom. 2012;2012:287852.CrossRefGoogle Scholar
  184. 184.
    Vazquez-Pianzola P, Urlaub H, Suter B. Pabp binds to the osk 3’UTR and specifically contributes to osk mRNA stability and oocyte accumulation. Dev Biol. 2011;357:404–18.CrossRefPubMedGoogle Scholar
  185. 185.
    Maris C, Dominguez C, Allain FH. The RNA recognition motif, a plastic RNA- binding platform to regulate post-transcriptional gene expression. FEBS J. 2005;272:2118–31.CrossRefPubMedGoogle Scholar
  186. 186.
    Lu WT, Wilczynska A, Smith E, Bushell M. The diverse roles of the eIF4A family: you are the company you keep. Biochem Soc Trans. 2014;42:166–72.CrossRefPubMedGoogle Scholar
  187. 187.
    Toone WM, Rudd KE, Friesen JD. deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase, can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J Bacteriol. 1991;173:3291–302.CrossRefPubMedPubMedCentralGoogle Scholar
  188. 188.
    Nishi K, Morel-Deville F, Hershey JW, Leighton T, Schnier J. An eIF-4A-like protein is a suppressor of an Escherichia coli mutant defective in 50S ribosomal subunit assembly. Nature. 1988;336:496–8.CrossRefPubMedGoogle Scholar
  189. 189.
    Lu J, Aoki H, Ganoza MC. Molecular characterization of a prokaryotic translation factor homologous to the eukaryotic initiation factor eIF4A. Int J Biochem Cell Biol. 1999;31:215–29.CrossRefPubMedGoogle Scholar
  190. 190.
    Linder P, Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nature Rev Mol Cell Biol. 2011;12:505–16.CrossRefGoogle Scholar
  191. 191.
    Lüking A, Stahl U, Schmidt U. The protein family of RNA helicases. Crit Rev Biochem Mol Biol. 1998;33:259–96.CrossRefPubMedGoogle Scholar
  192. 192.
    Parsyan A, Svitkin Y, Shahbazian D, Gkogkas C, Lasko P, Merrick WC, Sonenberg N. mRNA helicases: the tacticians of translational control. Nat Rev Mol Cell Biol. 2011;12:235–45.CrossRefPubMedGoogle Scholar
  193. 193.
    Marintchev A. Roles of helicases in translation initiation: a mechanistic view. Biochim Biophys Acta. 2015;1829:799–809.CrossRefGoogle Scholar
  194. 194.
    Takyar S, Hickerson RP, Noller HF. mRNA helicase activity of the ribosome. Cell. 2005;120:49–58.CrossRefPubMedGoogle Scholar
  195. 195.
    Pestova TV, Shatsky IN, Hellen CU. Functional dissection of eukaryotic initiation factor 4F: the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes. Mol Cell Biol. 1996;16:6870–8.CrossRefPubMedPubMedCentralGoogle Scholar
  196. 196.
    Pestova TV, Hellen CU, Shatsky IN. Canonical eukaryotic initiation factors determine translation by internal ribosomal entry. Mol Cell Biol. 1996;16:6859–69.CrossRefPubMedPubMedCentralGoogle Scholar
  197. 197.
    Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 1998;12:67–83.CrossRefPubMedPubMedCentralGoogle Scholar
  198. 198.
    Terenin IM, Dmitriev SE, Andreev DE, Royall E, Belsham GJ, Roberts LO, Shatsky IN. A cross-kingdom internal ribosome entry site reveals a simplified mode of internal ribosome entry. Mol Cell Biol. 2005;25:7879–88.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Greco Hernández
    • 1
    Email author
  • Vincent G. Osnaya
    • 1
  • Alejandra García
    • 1
  • Mitzli X. Velasco
    • 1
  1. 1.Division of Basic ResearchNational Institute of Cancer (INCan)Mexico CityMexico

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