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Programmed Ribosomal −1 Frameshifting as a Tradition: The Bacterial Transposable Elements of the IS3 Family

  • Olivier Fayet
  • Marie-Françoise Prère
Chapter
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 24)

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.

Keywords

Insertion Sequence Infectious Bronchitis Virus Stem Loop Site Codon Prokaryotic Ribosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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)

References

  1. Agris PF (2008) EMBO Rep 9:629–635PubMedCrossRefGoogle Scholar
  2. Agris PF, Vendeix FA, Graham WD (2007) J Mol Biol 366:1–13PubMedCrossRefGoogle Scholar
  3. Aldaz-Carroll L, Tallet B, Dausse E, Yurchenko L, Toulme JJ (2002) Biochemistry 41:5883–5893PubMedCrossRefGoogle Scholar
  4. Bashan A, Yonath A (2008) Trends Microbiol 16:326–335PubMedCrossRefGoogle Scholar
  5. Barak Z, Lindsley D, Gallant J (1996) J Mol Biol 256:676–684PubMedCrossRefGoogle Scholar
  6. Baranov PV, Gesteland RF, Atkins JF (2004) RNA 10:221–230PubMedCrossRefGoogle Scholar
  7. Baranov PV, Hammer AW, Zhou J, Gesteland RF, Atkins JF (2005) Genome Biol 6:R25PubMedCrossRefGoogle Scholar
  8. Barry JK, Miller WA (2002) Proc Natl Acad Sci USA 99:11133–11138PubMedCrossRefGoogle Scholar
  9. Bekaert M, Bidou L, Denise A, Duchateau-Nguyen G, Forest JP, Froidevaux C, Hatin I, Rousset JP, Termier M (2003) Bioinformatics 19:327–335PubMedCrossRefGoogle Scholar
  10. Berk V, Cate JH (2007) Curr Opin Struct Biol 17:302–309PubMedCrossRefGoogle Scholar
  11. Bertrand C, Prère MF, Gesteland RF, Atkins JF, Fayet O (2002) RNA 8:16–28PubMedCrossRefGoogle Scholar
  12. Brierley I, Boursnell ME, Binns MM, Bilimoria B, Blok VC, Brown TD, Inglis SC (1987) EMBO J 6:3779–3785PubMedGoogle Scholar
  13. Brierley I, Jenner AJ, Inglis SC (1992) J Mol Biol 227:463–479PubMedCrossRefGoogle Scholar
  14. Brierley I, Pennell S (2001) Cold Spring Harbor Symp. Quant Biol 66:233–248PubMedCrossRefGoogle Scholar
  15. Chandler M, Fayet O (1993) Mol Microbiol 7:497–503PubMedCrossRefGoogle Scholar
  16. 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 305–366Google Scholar
  17. Crick FH (1966) J Mol Biol 19:548–555PubMedCrossRefGoogle Scholar
  18. Chen X, Chamorro M, Lee SI, Shen LX, Hines JV, Tinoco I Jr, Varmus HE (1995) EMBO J 14:842–852PubMedGoogle Scholar
  19. Chen CC, Hu ST (2006) J Biol Chem 281:21617–21628PubMedCrossRefGoogle Scholar
  20. Escoubas JM, Prère MF, Fayet O, Salvignol I, Galas D, Zerbib D, Chandler M (1991) EMBO J 10:705–712PubMedGoogle Scholar
  21. Farabaugh PJ (1997) Programmed Alternative Reading of the Genetic Code. Landes Bioscience, Austin, Texas and Springer, Heidelberg, Germany, pp 69–102CrossRefGoogle Scholar
  22. Frank J, Gao H, Sengupta J, Gao N, Taylor DJ (2007) Proc Natl Acad Sci USA 104:19671–19678PubMedCrossRefGoogle Scholar
  23. Gesteland RF, Atkins JF (1996) Annu Rev Biochem 65:741–68Giedroc DP, Cornish PV (2009) Virus Res 139:193–208PubMedCrossRefGoogle Scholar
  24. Giedroc DP, Theimer CA, Nixon PL (2000) J Mol Biol 298:167–185PubMedCrossRefGoogle Scholar
  25. Haren L, Normand C, Polard P, Alazard R, Chandler M (2000) J Mol Biol 296:757–768PubMedCrossRefGoogle Scholar
  26. Harger JW, Meskauskas A, Dinman JD (2002) Trends Biochem Sci 27:448–454PubMedCrossRefGoogle Scholar
  27. Horsfield JA, Wilson DN, Mannering SA, Adamski FM, Tate WP (1995) Nucleic Acids Res 23:1487–1494PubMedCrossRefGoogle Scholar
  28. Howard MT, Gesteland RF, Atkins JF (2004) RNA 10:1653–1661PubMedCrossRefGoogle Scholar
  29. Jacks T, Varmus HE (1985) Science 230:1237–1242PubMedCrossRefGoogle Scholar
  30. Jacks T, Madhani HD, Masiarz FR, Varmus HE (1988) Cell 55:447–458PubMedCrossRefGoogle Scholar
  31. Kim YG, Maas S, Rich A (2001) Nucleic Acids Res 29:1125–1131PubMedCrossRefGoogle Scholar
  32. Kollmus H, Honigman A, Panet A, Hauser H (1994) J Virol 68:6087–6091PubMedGoogle Scholar
  33. Kurland CG (1992) Annu Rev Genet 26:29–50PubMedCrossRefGoogle Scholar
  34. Larsen B, Wills NM, Gesteland RF, Atkins JF (1994) J Bacteriol 176:6842–6851PubMedGoogle Scholar
  35. Larsen B, Gesteland RF, Atkins JF (1997) J Mol Biol 271:47–60PubMedCrossRefGoogle Scholar
  36. Larsen B, Wills NM, Nelson C, Atkins JF, Gesteland RF (2000) Proc Natl Acad Sci USA 97:1683–1688PubMedCrossRefGoogle Scholar
  37. Lee TH, Blanchard SC, Kim HD, Puglisi JD, Chu S (2007) Proc Natl Acad Sci USA 104:13661–13665PubMedCrossRefGoogle Scholar
  38. Léger M, Dulude D, Steinberg SV, Brakier-Gingras L (2007) Nucleic Acids Res 35:5581–5592PubMedCrossRefGoogle Scholar
  39. Licznar P, Mejlhede N, Prère MF, Wills N, Gesteland RF, Atkins JF, Fayet O (2003) EMBO J 22:4770–4778PubMedCrossRefGoogle Scholar
  40. Loot C, Turlan C, Rousseau P, Ton-Hoang B, Chandler M (2002) EMBO J 21:4172–4182PubMedCrossRefGoogle Scholar
  41. Mazauric MH, Licznar P, Prère MF, Canal I, Fayet O (2008) J Biol Chem 2008 283:20421–20432Google Scholar
  42. Mejlhede N, Atkins JF, Neuhard J (1999) J Bacteriol 181:2930–2937PubMedGoogle Scholar
  43. Murphy FV 4th, Ramakrishnan V, Malkiewicz A, Agris PF (2004) Nat Struct Mol Biol 11:1186–1191PubMedCrossRefGoogle Scholar
  44. Michiels PJ, Versleijen AA, Verlaan PW, Pleij CW, Hilbers CW, Heus HA(2001) J Mol Biol 310:1109–1112PubMedCrossRefGoogle Scholar
  45. Namy O, Moran SJ, Stuart DI, Gilbert RJ, Brierley I (2006) Nature 441:244–247PubMedCrossRefGoogle Scholar
  46. Olsthoorn RC, Laurs, Sohet F, Hilbers CW, Heus HA, Pleij CW (2004) RNA 10:1702–1703PubMedCrossRefGoogle Scholar
  47. Napthine S, Vidakovic M, Girnary R, Namy O, Brierley I (2003) EMBO J 22:3941–3950PubMedCrossRefGoogle Scholar
  48. Plant EP, Dinman JD(2005) Nucleic Acids Res 33:1825–1833PubMedCrossRefGoogle Scholar
  49. Plant EP, Jacobs KL, Harger JW, Meskauskas A, Jacobs JL, Baxter JL, Petrov AN, Dinman JD (2003) RNA 9:168–174PubMedCrossRefGoogle Scholar
  50. Polard P, Prère MF, Chandler M, Fayet O (1991) J Mol Biol 222:465–477PubMedCrossRefGoogle Scholar
  51. Prère MF, Chandler M, Fayet O (1990) J Bacteriol 172:4090–4099PubMedGoogle Scholar
  52. Ramakrishnan V (2008) Biochem Soc Trans 36:567–574PubMedCrossRefGoogle Scholar
  53. Rettberg CC, Prère MF, Gesteland RF, Atkins JF, Fayet O (1999) J Mol Biol 286:1365–1378PubMedCrossRefGoogle Scholar
  54. Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, Stormo GD, Gold L (1992) Mol Microbiol 6:1219–1229PubMedCrossRefGoogle Scholar
  55. Rodnina MV, Wintermeyer W (2001) Annu Rev Biochem 70:415–435PubMedCrossRefGoogle Scholar
  56. Sekine Y, Ohtsubo E (1989) Proc Natl Acad Sci USA 86:4609–4613PubMedCrossRefGoogle Scholar
  57. Sekine Y, Ohtsubo E (1992) Mol Gen Genet 235:325–332PubMedCrossRefGoogle Scholar
  58. Sekine Y, Eisaki N, Ohtsubo E (1994) J Mol Biol 235:1406–1420PubMedCrossRefGoogle Scholar
  59. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006) Nucleic Acids Res 34(Database issue):D32–36PubMedCrossRefGoogle Scholar
  60. Stapulionis R, Wang Y, Dempsey GT, Khudaravalli R, Nielsen KM, Cooperman BS, Goldman YE, Knudsen CR (2008) Biol Chem 389:1239–1249PubMedCrossRefGoogle Scholar
  61. Su L, Chen L, Egli M, Berger JM, Rich A (1999) Nat Struct Biol 6:285–292PubMedCrossRefGoogle Scholar
  62. Takyar S, Hickerson RP, Noller HF(2005) Cell 120:49–58PubMedCrossRefGoogle Scholar
  63. Ton-Hoang B, Polard P, Haren L, Turlan C, Chandler M (1999) Mol Microbiol 32:617–627PubMedCrossRefGoogle Scholar
  64. Tsuchihashi Z, Brown PO(1992) Genes Dev 6:511–519PubMedCrossRefGoogle Scholar
  65. Yusupova GZ, Yusupov M, Cate JH, Noller HF (2001) Cell 106:233–241PubMedCrossRefGoogle Scholar
  66. Yusupova G, Jenner L, Rees B, Moras D, Yusupov M (2006) Nature 444:391–394PubMedCrossRefGoogle Scholar
  67. Vögele K, Schwartz E, Welz C, Schiltz E, Rak B (1991) Nucleic Acids Res 19:4377–4385PubMedCrossRefGoogle Scholar
  68. Weiss RB, Dunn DM, Atkins JF, Gesteland RF (1987) Cold Spring Harbor Symp Quant Biol 52:687–693PubMedCrossRefGoogle Scholar
  69. Weiss RB, Dunn DM, Shuh M, Atkins JF, Gesteland RF(1989) New Biol 1:159–169PubMedGoogle Scholar
  70. Wen JD, Lancaster L, Hodges C, Zeri AC, Yoshimura SH, Noller HF, Bustamante C, Tinoco I (2008) Nature 452:598–603PubMedCrossRefGoogle Scholar
  71. Zheng J, McIntosh MA (1995) Mol Microbiol 16:669–685PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Laboratoire de Microbiologie et Génétique MoléculairesUniversité de ToulouseToulouseFrance
  2. 2.Laboratoire de Microbiologie et Génétique MoléculairesCentre national de la Recherche Scientifique, UMR5100ToulouseFrance

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