A novel mechanism for translation initiation operates in haloarchaea

Molecular Microbiology

Volumn 71, Issue 6, 2009, Pages 1451-1463

  Hering, Oliver ^a   Brenneis, Mariam ^a   Beer, Jürgen ^a   Suess, Beatrix ^a   Soppa, Jörg ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGION; ARCHAEBACTERIUM; ARTICLE; EUKARYOTE; GENE SEQUENCE; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; PRIORITY JOURNAL; START CODON; TRANSLATION INITIATION;

5' UNTRANSLATED REGIONS; CODON, INITIATOR; GENES, ARCHAEAL; HALOFERAX VOLCANII; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RNA, ARCHAEAL; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); EUKARYOTA; HALOBACTERIA; PROKARYOTA;

EID: 62449324914     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06615.x     Document Type: Article

References (47)

1. Andreev, D.E., Terenin, I.M., Dunaevsky, Y.E., Dmitriev, S.E. Shatsky, I.N. (2006) A leaderless mRNA can bind to mammalian 80S ribosomes and direct polypeptide synthesis in the absence of translation initiation factors. Mol Cell Biol 26 : 3164 3169.
2. Barry, E.R. Bell, S.D. (2006) DNA replication in the archaea. Microbiol Mol Biol Rev 70 : 876 887.
3. Brenneis, M., Hering, O., Lange, C. Soppa, J. (2007) Experimental characterization of Cis-acting elements important for translation and transcription in halophilic archaea. PLoS Genet 3 : e229.
4. Chang, B., Halgamuge, S. Tang, S.L. (2006) Analysis of SD sequences in completed microbial genomes: non-SD-led genes are as common as SD-led genes. Gene 373 : 90 99.
5. Chomczynski, P. Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162 : 156 159.
6. Cline, S.W., Lam, W.L., Charlebois, R.L., Schalkwyk, L.C. Doolittle, W.F. (1989) Transformation methods for halophilic archaebacteria. Can J Microbiol 35 : 148 152.
7. Condo, I., Ciammaruconi, A., Benelli, D., Ruggero, D. Londei, P. (1999) Cis-acting signals controlling translational initiation in the thermophilic archaeon Sulfolobus solfataricus. Mol Microbiol 34 : 377 384.
8. Danner, S. Soppa, J. (1996) Characterization of the distal promoter element of halobacteria in vivo using saturation mutagenesis and selection. Mol Microbiol 19 : 1265 1276.
9. Grill, S., Gualerzi, C.O., Londei, P. Bläsi, U. (2000) Selective stimulation of translation of leaderless mRNA by initiation factor 2: evolutionary implications for translation. EMBO J 19 : 4101 4110.
10. Grill, S., Moll, I., Hasenohrl, D., Gualerzi, C.O. Bläsi, U. (2001) Modulation of ribosomal recruitment to 5′-terminal start codons by translation initiation factors IF2 and IF3. FEBS Lett 495 : 167 171.
11. Grill, S., Moll, I., Giuliodori, A., Gualerzi, C.O. Bläsi, U. (2002) Temperature-dependent translation of leaderless and canonical mRNAs in Escherichia coli. FEMS Microbiol Lett 211 : 161 167.
12. Gualerzi, C.O. Pon, C.L. (1990) Initiation of mRNA translation in prokaryotes. Biochemistry 29 : 5881 5889.
13. Hanson, S., Berthelot, K., Fink, B., McCarthy, J.E. Suess, B. (2003) Tetracycline-aptamer-mediated translational regulation in yeast. Mol Microbiol 49 : 1627 1637.
14. Hasenöhrl, D., Lombo, T., Kaberdin, V., Londei, P. Bläsi, U. (2008) Translation initiation factor a/eIF2(-gamma) counteracts 5′ to 3′ mRNA decay in the archaeon Sulfolobus solfataricus. Proc Natl Acad Sci USA 105 : 2146 2150.
15. Jackson, R.J. (2005) Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem Soc Trans 33 : 1231 1241.
16. Kean, K.M. (2003) The role of mRNA 5′-noncoding and 3′-end sequences on 40S ribosomal subunit recruitment, and how RNA viruses successfully compete with cellular mRNAs to ensure their own protein synthesis. Biol Cell 95 : 129 139.
17. Kozak, M. (1989) Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol Cell Biol 9 : 5073 5080.
18. Kozak, M. (1995) Adherence to the first-AUG rule when a second AUG codon follows closely upon the first. Proc Natl Acad Sci USA 92 : 2662 2666.
19. Kozak, M. (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene 299 : 1 34.
20. Laursen, B.S., Sorensen, H.P., Mortensen, K.K. Sperling-Petersen, H.U. (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69 : 101 123.
21. Liu, L., Dilworth, D., Gao, L., Monzon, J., Summers, A., Lassam, N. Hogg, D. (1999) Mutation of the CDKN2A 5′ UTR creates an aberrant initiation codon and predisposes to melanoma. Nat Genet 21 : 128 132.
22. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 : 402 408.
23. Londei, P. (2005) Evolution of translational initiation: new insights from the archaea. FEMS Microbiol Rev 29 : 185 200.
24. Lopez-Lastra, M., Rivas, A. Barria, M.I. (2005) Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol Res 38 : 121 146.
25. Marintchev, A. Wagner, G. (2004) Translation initiation: structures, mechanisms and evolution. Q Rev Biophys 37 : 197 284.
26. Martinez-Salas, E., Pacheco, A., Serrano, P. Fernandez, N. (2008) New insights into internal ribosome entry site elements relevant for viral gene expression. J Gen Virol 89 : 611 626.
27. Mathews, D.H., Sabina, J., Zuker, M. Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288 : 911 940.
28. Moll, I. Bläsi, U. (2002) Differential inhibition of 30S and 70S translation initiation complexes on leaderless mRNA by kasugamycin. Biochem Biophys Res Commun 297 : 1021 1026.
29. Moll, I., Grill, S., Gualerzi, C.O. Bläsi, U. (2002) Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43 : 239 246.
30. Moll, I., Hirokawa, G., Kiel, M.C., Kaji, A. Bläsi, U. (2004) Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acids Res 32 : 3354 3363.
31. O'Donnell, S.M. Janssen, G.R. (2002) Leaderless mRNAs bind 70S ribosomes more strongly than 30S ribosomal subunits in Escherichia coli. J Bacteriol 184 : 6730 6733.
32. Omer, A.D., Ziesche, S., Decatur, W.A., Fournier, M.J. Dennis, P.P. (2003) RNA-modifying machines in archaea. Mol Microbiol 48 : 617 629.
33. Patenge, N. Soppa, J. (1999) Extensive proteolysis inhibits high-level production of eukaryal G protein-coupled receptors in the archaeon Haloferax volcanii. FEMS Microbiol Lett 171 : 27 35.
34. Peabody, D.S. (1989) Translation initiation at non-AUG triplets in mammalian cells. J Biol Chem 264 : 5031 5035.
35. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I. Helen, C.U. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc Natl Acad Sci USA 98 : 7029 7036.
36. Sambrook, J., Fritsch, E.G. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbour, NY : Cold Spring Harbour Laboratory Press.
37. Sandman, K. Reeve, J.N. (2000) Structure and functional relationships of archaeal and eukaryal histones and nucleosomes. Arch Microbiol 173 : 165 169.
38. Sartorius-Neef, S. Pfeifer, F. (2004) In vivo studies on putative Shine-Dalgarno sequences of the halophilic archaeon Halobacterium salinarum. Mol Microbiol 51 : 579 588.
39. Schluenzen, F., Takemoto, C., Wilson, D.N., Kaminishi, T., Harms, J.M., Hanawa-Suetsugu, K., et al. (2006) The antibiotic kasugamycin mimics mRNA nucleotides to destabalize tRNA binding and inhibit canonical translation initiation. Nat Struct Mol Biol 13 : 871 878.
40. Slupska, M.M., King, A.G., Fitz-Gibbon, S., Besemer, J., Borodovsky, M. Miller, J.H. (2001) Leaderless transcripts of the crenarchaeal hyperthermophile Pyrobaculum aerophilum. J Mol Biol 309 : 347 360.
41. Soppa, J. (2001) Basal and regulated transcription in archaea. Adv Appl Microbiol 50 : 171 217.
42. Spriggs, K.A., Bushell, M., Mitchell, S.A. Willis, A.E. (2005) Internal ribosome entry segment-mediated translation during apoptosis: the role of IRES-trans-acting factors. Cell Death Differ 12 : 585 591.
43. Spriggs, K.A., Stoneley, M., Bushell, M. Willis, A.E. (2008) Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol Cell 100 : 27 38.
44. Tolstrup, N., Sensen, C.W., Garrett, R.A. Clausen, I.G. (2000) Two different and highly organized mechanisms of translation initiation in the archaeon Sulfolobus solfataricus. Extremophiles 4 : 175 179.
45. Udagawa, T., Shimizu, Y. Ueda, T. (2004) Evidence for the translation initiation of leaderless mRNAs by the intact 70S ribosome without its dissociation into subunits in Eubacteria. J Biol Chem 279 : 8539 8546.
46. Van Etten, W.J. Janssen, G.R. (1998) An AUG initiation codon, not codon-anticodon complementarity, is required for the translation of unleadered mRNA in Escherichia coli. Mol Microbiol 27 : 987 1001.
47. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31 : 3406 3415.