Abstract
Insertion sequences (ISs) are small ubiquitous DNA transposable elements coding for one or two proteins that are found in the genome of most bacteria where they play an important role in genetic plasticity. Based on protein similarity, the ISs were grouped in 19 families, the largest being the IS3 family. Interestingly, most of its 418 members possess two overlapping genes and very likely use programmed ribosomal −1 frameshifting (PRF-1) to generate their transposase, the protein required for transposition, as was experimentally demonstrated for a few (e.g., IS3, IS150, IS911, IS3411). A systematic comparison of the IS3 family members was carried out to reveal the main features of the frameshift-programming signals present in their mRNA. The mandatory component is a short sequence where the shift from frame 0 to frame −1 occurs (Z-ZZN or more frequently X-XXZ-ZZN, the 0 frame codons are underlined). In the IS, there is a clear preference for the A-AA[A/G] and U-UU[U/C] tetramers (20%), and for the A-AAA-AA[A/G] heptamers (55%). The slippery motif is accompanied in 87% of the cases by one or two stimulatory elements. Like in eukaryotic viruses, it can be a structure formed by folding of the mRNA downstream of the motif. This is either a stem loop (60%) or a pseudoknot (13%). However, it can also be an upstream Shine–Dalgarno-like sequence (SD) that acts through pairing with 16S ribosomal RNA (in 56% of the IS). The two types of stimulators are both present in 42% of the IS and are both absent in 13% of them. Several lessons can be drawn from this comparative analysis and from more detailed analyses of frameshift signals of a few IS: (i) PRF-1 is a 2 (and perhaps 3) tRNA story and if ISs use a restricted set of frameshift motifs it is because prokaryotic ribosomes are less tolerant to near-cognate tRNA pairing than eukaryotic ribosomes. (ii) ISs have more flexibility in the design of their frameshift regions (use of 0, 1, or 2 stimulators) than eukaryotic viruses. (iii) The nucleotides immediately 3′ to the slippery motif modulate frameshifting and thus must play a role in frame maintenance possibly through yet to identify interactions with the ribosome.
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Agris PF (2008) EMBO Rep 9:629–635
Agris PF, Vendeix FA, Graham WD (2007) J Mol Biol 366:1–13
Aldaz-Carroll L, Tallet B, Dausse E, Yurchenko L, Toulme JJ (2002) Biochemistry 41:5883–5893
Bashan A, Yonath A (2008) Trends Microbiol 16:326–335
Barak Z, Lindsley D, Gallant J (1996) J Mol Biol 256:676–684
Baranov PV, Gesteland RF, Atkins JF (2004) RNA 10:221–230
Baranov PV, Hammer AW, Zhou J, Gesteland RF, Atkins JF (2005) Genome Biol 6:R25
Barry JK, Miller WA (2002) Proc Natl Acad Sci USA 99:11133–11138
Bekaert M, Bidou L, Denise A, Duchateau-Nguyen G, Forest JP, Froidevaux C, Hatin I, Rousset JP, Termier M (2003) Bioinformatics 19:327–335
Berk V, Cate JH (2007) Curr Opin Struct Biol 17:302–309
Bertrand C, Prère MF, Gesteland RF, Atkins JF, Fayet O (2002) RNA 8:16–28
Brierley I, Boursnell ME, Binns MM, Bilimoria B, Blok VC, Brown TD, Inglis SC (1987) EMBO J 6:3779–3785
Brierley I, Jenner AJ, Inglis SC (1992) J Mol Biol 227:463–479
Brierley I, Pennell S (2001) Cold Spring Harbor Symp. Quant Biol 66:233–248
Chandler M, Fayet O (1993) Mol Microbiol 7:497–503
Chandler M, Mahillon J (2002) Insertion Sequences revisited. In Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II, American Society for Microbiology, Washington DC, –pp 305–366
Crick FH (1966) J Mol Biol 19:548–555
Chen X, Chamorro M, Lee SI, Shen LX, Hines JV, Tinoco I Jr, Varmus HE (1995) EMBO J 14:842–852
Chen CC, Hu ST (2006) J Biol Chem 281:21617–21628
Escoubas JM, Prère MF, Fayet O, Salvignol I, Galas D, Zerbib D, Chandler M (1991) EMBO J 10:705–712
Farabaugh PJ (1997) Programmed Alternative Reading of the Genetic Code. Landes Bioscience, Austin, Texas and Springer, Heidelberg, Germany, pp 69–102
Frank J, Gao H, Sengupta J, Gao N, Taylor DJ (2007) Proc Natl Acad Sci USA 104:19671–19678
Gesteland RF, Atkins JF (1996) Annu Rev Biochem 65:741–68Giedroc DP, Cornish PV (2009) Virus Res 139:193–208
Giedroc DP, Theimer CA, Nixon PL (2000) J Mol Biol 298:167–185
Haren L, Normand C, Polard P, Alazard R, Chandler M (2000) J Mol Biol 296:757–768
Harger JW, Meskauskas A, Dinman JD (2002) Trends Biochem Sci 27:448–454
Horsfield JA, Wilson DN, Mannering SA, Adamski FM, Tate WP (1995) Nucleic Acids Res 23:1487–1494
Howard MT, Gesteland RF, Atkins JF (2004) RNA 10:1653–1661
Jacks T, Varmus HE (1985) Science 230:1237–1242
Jacks T, Madhani HD, Masiarz FR, Varmus HE (1988) Cell 55:447–458
Kim YG, Maas S, Rich A (2001) Nucleic Acids Res 29:1125–1131
Kollmus H, Honigman A, Panet A, Hauser H (1994) J Virol 68:6087–6091
Kurland CG (1992) Annu Rev Genet 26:29–50
Larsen B, Wills NM, Gesteland RF, Atkins JF (1994) J Bacteriol 176:6842–6851
Larsen B, Gesteland RF, Atkins JF (1997) J Mol Biol 271:47–60
Larsen B, Wills NM, Nelson C, Atkins JF, Gesteland RF (2000) Proc Natl Acad Sci USA 97:1683–1688
Lee TH, Blanchard SC, Kim HD, Puglisi JD, Chu S (2007) Proc Natl Acad Sci USA 104:13661–13665
Léger M, Dulude D, Steinberg SV, Brakier-Gingras L (2007) Nucleic Acids Res 35:5581–5592
Licznar P, Mejlhede N, Prère MF, Wills N, Gesteland RF, Atkins JF, Fayet O (2003) EMBO J 22:4770–4778
Loot C, Turlan C, Rousseau P, Ton-Hoang B, Chandler M (2002) EMBO J 21:4172–4182
Mazauric MH, Licznar P, Prère MF, Canal I, Fayet O (2008) J Biol Chem 2008 283:20421–20432
Mejlhede N, Atkins JF, Neuhard J (1999) J Bacteriol 181:2930–2937
Murphy FV 4th, Ramakrishnan V, Malkiewicz A, Agris PF (2004) Nat Struct Mol Biol 11:1186–1191
Michiels PJ, Versleijen AA, Verlaan PW, Pleij CW, Hilbers CW, Heus HA(2001) J Mol Biol 310:1109–1112
Namy O, Moran SJ, Stuart DI, Gilbert RJ, Brierley I (2006) Nature 441:244–247
Olsthoorn RC, Laurs, Sohet F, Hilbers CW, Heus HA, Pleij CW (2004) RNA 10:1702–1703
Napthine S, Vidakovic M, Girnary R, Namy O, Brierley I (2003) EMBO J 22:3941–3950
Plant EP, Dinman JD(2005) Nucleic Acids Res 33:1825–1833
Plant EP, Jacobs KL, Harger JW, Meskauskas A, Jacobs JL, Baxter JL, Petrov AN, Dinman JD (2003) RNA 9:168–174
Polard P, Prère MF, Chandler M, Fayet O (1991) J Mol Biol 222:465–477
Prère MF, Chandler M, Fayet O (1990) J Bacteriol 172:4090–4099
Ramakrishnan V (2008) Biochem Soc Trans 36:567–574
Rettberg CC, Prère MF, Gesteland RF, Atkins JF, Fayet O (1999) J Mol Biol 286:1365–1378
Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, Stormo GD, Gold L (1992) Mol Microbiol 6:1219–1229
Rodnina MV, Wintermeyer W (2001) Annu Rev Biochem 70:415–435
Sekine Y, Ohtsubo E (1989) Proc Natl Acad Sci USA 86:4609–4613
Sekine Y, Ohtsubo E (1992) Mol Gen Genet 235:325–332
Sekine Y, Eisaki N, Ohtsubo E (1994) J Mol Biol 235:1406–1420
Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006) Nucleic Acids Res 34(Database issue):D32–36
Stapulionis R, Wang Y, Dempsey GT, Khudaravalli R, Nielsen KM, Cooperman BS, Goldman YE, Knudsen CR (2008) Biol Chem 389:1239–1249
Su L, Chen L, Egli M, Berger JM, Rich A (1999) Nat Struct Biol 6:285–292
Takyar S, Hickerson RP, Noller HF(2005) Cell 120:49–58
Ton-Hoang B, Polard P, Haren L, Turlan C, Chandler M (1999) Mol Microbiol 32:617–627
Tsuchihashi Z, Brown PO(1992) Genes Dev 6:511–519
Yusupova GZ, Yusupov M, Cate JH, Noller HF (2001) Cell 106:233–241
Yusupova G, Jenner L, Rees B, Moras D, Yusupov M (2006) Nature 444:391–394
Vögele K, Schwartz E, Welz C, Schiltz E, Rak B (1991) Nucleic Acids Res 19:4377–4385
Weiss RB, Dunn DM, Atkins JF, Gesteland RF (1987) Cold Spring Harbor Symp Quant Biol 52:687–693
Weiss RB, Dunn DM, Shuh M, Atkins JF, Gesteland RF(1989) New Biol 1:159–169
Wen JD, Lancaster L, Hodges C, Zeri AC, Yoshimura SH, Noller HF, Bustamante C, Tinoco I (2008) Nature 452:598–603
Zheng J, McIntosh MA (1995) Mol Microbiol 16:669–685
Acknowledgments
The help of Mick Chandler and Patricia Siguier with the IS database has been greatly appreciated. This work was funded by the Centre National de la Recherche Scientifique (CNRS), the University of Toulouse, and by a grant to OF from the Agence National pour la Recherche (#ANR-05-BLAN-0048-01)
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Fayet, O., Prère, MF. (2010). Programmed Ribosomal −1 Frameshifting as a Tradition: The Bacterial Transposable Elements of the IS3 Family. In: Atkins, J., Gesteland, R. (eds) Recoding: Expansion of Decoding Rules Enriches Gene Expression. Nucleic Acids and Molecular Biology, vol 24. Springer, New York, NY. https://doi.org/10.1007/978-0-387-89382-2_12
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