Footprinting analysis of BWYV pseudoknot-ribosome complexes

RNA

Volumn 15, Issue 9, 2009, Pages 1775-1786

  Mazauric, Marie Hélène ^a   Leroy, Jean Louis ^a   Visscher, Koen ^b,c   Yoshizawa, Satoko ^a   Fourmy, Dominique ^a  

^a INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

^b University of Arizona   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

BWYV; Frameshifting; mRNA; Translation; Translocation

Indexed keywords

MESSENGER RNA; NUCLEOTIDE; SPACER DNA; TRANSFER RNA;

ARTICLE; BACTERIAL TRANSLOCATION; COMPLEX FORMATION; DNA BINDING; DNA FOOTPRINTING; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; POLEROVIRUS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RIBOSOMAL FRAMESHIFTING; RIBOSOME; RNA BINDING; RNA STRUCTURE; RNA TRANSLATION; RNA TRANSPORT;

BACTERIOPHAGE T4; BASE SEQUENCE; ESCHERICHIA COLI PROTEINS; FRAMESHIFTING, RIBOSOMAL; LUTEOVIRUS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN FOOTPRINTING; RIBOSOMES; RNA, MESSENGER; RNA, VIRAL; SEQUENCE HOMOLOGY, NUCLEIC ACID;

BEET WESTERN YELLOWS VIRUS; ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 69049113945     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1385409     Document Type: Article

References (76)

1. Baranov PV, Gesteland RF, Atkins JF. 2002. Recoding: Translational bifurcations in gene expression. Gene 286: 187-201.
2. Baril M, Dulude D, Steinberg SV, Brakier-Gingras L. 2003. The frameshift stimulatory signal of human immunodeficiency virus type 1 group O is a pseudoknot. J Mol Biol 331: 571-583.
3. Bertrand C, Prere MF, Gesteland RF, Atkins JF, Fayet O. 2002. Influence of the stacking potential of the base 3′ of tandem shift codons on -1 ribosomal frameshifting used for gene expression. RNA 8: 16-28.
4. Blinkowa AL, Walker JR. 1990. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III γ subunit from within the τ subunit reading frame. Nucleic Acids Res 18: 1725-1729.
5. Brierley I, Digard P, Inglis SC. 1989. Characterization of an efficient coronavirus ribosomal frameshifting signal: Requirement for an RNA pseudoknot. Cell 57: 537-547.
6. Brunelle MN, Payant C, Lemay G, Brakier-Gingras L. 1999. Expression of the human immunodeficiency virus frameshift signal in a bacterial cell-free system: Influence of an interaction between the ribosome and a stem-loop structure downstream from the slippery site. Nucleic Acids Res 27: 4783-4791.
7. Chandramouli P, Topf M, Menetret JF, Eswar N, Cannone JJ, Gutell RR, Sali A, Akey CW. 2008. Structure of the mammalian 80S ribosome at 8.7 Å resolution. Structure 16: 535-548.
8. Chen X, Chamorro M, Lee SI, Shen LX, Hines JV, Tinoco I Jr, Varmus HE. 1995. Structural and functional studies of retroviral RNA pseudoknots involved in ribosomal frameshifting: Nucleotides at the junction of the two stems are important for efficient ribosomal frameshifting. EMBO J 14: 842-852.
9. Chen G, Wen JD, Tinoco I Jr. 2007. Single-molecule mechanical unfolding and folding of a pseudoknot in human telomerase RNA. RNA 13: 2175-2188.
10. Cornish PV, Hennig M, Giedroc DP. 2005. A loop 2 cytidine-stem 1 minor groove interaction as a positive determinant for pseudoknot-stimulated -1 ribosomal frameshifting. Proc Natl Acad Sci 102: 12694-12699.
11. Cornish PV, Stammler SN, Giedroc DP. 2006. The global structures of a wild-type and poorly functional plant luteoviral mRNA pseudoknot are essentially identical. RNA 12: 1959-1969.
12. Du Z, Holland JA, Hansen MR, Giedroc DP, Hoffman DW. 1997. Base-pairings within the RNA pseudoknot associated with the simian retrovirus-1 gag-pro frameshift site. J Mol Biol 270: 464-470.
13. Dulude D, Baril M, Brakier-Gingras L. 2002. Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1. Nucleic Acids Res 30: 5094-5102.
14. Egli M, Minasov G, Su L, Rich A. 2002. Metal ions and flexibility in a viral RNA pseudoknot at atomic resolution. Proc Natl Acad Sci 99: 4302-4307.
15. Flower AM, McHenry CS. 1990. The g subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci 87: 3713-3717.
16. Frank J, Agrawal RK. 2000. A ratchet-like intersubunit reorganization of the ribosome during translocation. Nature 406: 318-322.
17. Garcia A, van Duin J, Pleij CW. 1993. Differential response to frameshift signals in eukaryotic and prokaryotic translational systems. Nucleic Acids Res 21: 401-406.
18. Gaudin C, Mazauric MH, Traikia M, Guittet E, Yoshizawa S, Fourmy D. 2005. Structure of the RNA signal essential for translational frameshifting in HIV-1. J Mol Biol 349: 1024-1035.
19. Giedroc DP, Cornish PV. 2009. Frameshifting RNA pseudoknots: Structure and mechanism. Virus Res 139: 193-208.
20. Giedroc DP, Theimer CA, Nixon PL. 2000. Structure, stability, and function of RNA pseudoknots involved in stimulating ribosomal frameshifting. J Mol Biol 298: 167-185.
21. Giedroc DP, Cornish PV, Hennig M. 2003. Detection of scalar couplings involving 2′-hydroxyl protons across hydrogen bonds in a frameshifting mRNA pseudoknot. J AmChem Soc 125: 4676-4677.
22. Green L, Kim CH, Bustamante C, Tinoco I Jr. 2008. Characterization of the mechanical unfolding of RNA pseudoknots. J Mol Biol 375: 511-528.
23. Grentzmann G, Ingram JA, Kelly PJ, Gesteland RF, Atkins JF. 1998. A dual-luciferase reporter system for studying recoding signals. RNA 4: 479-486.
24. Habig WH, Pabst MJ, Jakoby WB. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249: 7130-7139.
25. Hansen TM, Reihani SN, Oddershede LB, Sorensen MA. 2007. Correlation between mechanical strength of messenger RNA pseudoknots and ribosomal frameshifting. Proc Natl Acad Sci 104: 583-585.
26. Hartz D, McPheeters DS, Traut R, Gold L. 1988. Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164: 419-425.
27. Hartz D, McPheeters DS, Gold L. 1989. Selection of the initiator tRNA by Escherichia coli initiation factors. Genes & Dev 3: 1899-1912.
28. Horan LH, Noller HF. 2007. Intersubunit movement is required for ribosomal translocation. Proc Natl Acad Sci 104: 4881-4885.
29. Huttenhofer A, Noller HF. 1994. Footprinting mRNA-ribosome complexes with chemical probes. EMBO J 13: 3892-3901.
30. Jacks T, Power MD, Masiarz FR, Luciw PA, Barr PJ, Varmus HE. 1988. Characterization of ribosomal frameshifting in HIV-1 gagpol expression. Nature 331: 280-283.
31. Jenner L, Rees B, Yusupov M, Yusupova G. 2007. Messenger RNA conformations in the ribosomal E site revealed by X-ray crystallography. EMBO Rep 8: 846-850.
32. Joseph S, Noller HF. 1998. EF-G-catalyzed translocation of anticodon stem-loop analogs of transfer RNA in the ribosome. EMBO J 17: 3478-3483.
33. Kim YG, Su L, Maas S, O'Neill A, Rich A. 1999. Specific mutations in a viral RNA pseudoknot drastically change ribosomal frameshifting efficiency. Proc Natl Acad Sci 96: 14234-14239.
34. Kim YG, Maas S, Wang SC, Rich A. 2000. Mutational study reveals that tertiary interactions are conserved in ribosomal frameshifting pseudoknots of two luteoviruses. RNA 6: 1157-1165.
35. Kim YG, Maas S, Rich A. 2001. Comparative mutational analysis of cis-acting RNA signals for translational frameshifting in HIV-1 and HTLV-2. Nucleic Acids Res 29: 1125-1131.
36. Kollmus H, Honigman A, Panet A, Hauser H. 1994. The sequences of and distance between two cis-acting signals determine the efficiency of ribosomal frameshifting in human immunodeficiency virus type 1 and human T-cell leukemia virus type II in vivo. J Virol 68: 6087-6091.
37. Kontos H, Napthine S, Brierley I. 2001. Ribosomal pausing at a frameshifter RNA pseudoknot is sensitive to reading phase but shows little correlation with frameshift efficiency. Mol Cell Biol 21: 8657-8670.
38. Kurland CG. 1992. Translational accuracy and the fitness of bacteria. Annu Rev Genet 26: 29-50.
39. Marcheschi RJ, Staple DW, Butcher SE. 2007. Programmed ribosomal frameshifting in SIV is induced by a highly structured RNA stem-loop. J Mol Biol 373: 652-663.
40. Marczinke B, Fisher R, Vidakovic M, Bloys AJ, Brierley I. 1998. Secondary structure and mutational analysis of the ribosomal frameshift signal of rous sarcoma virus. J Mol Biol 284: 205-225.
41. Michiels PJ, Versleijen AA, Verlaan PW, Pleij CW, Hilbers CW, Heus HA. 2001. Solution structure of the pseudoknot of SRV-1 RNA, involved in ribosomal frameshifting. J Mol Biol 310: 1109-1123.
42. Namy O, Moran SJ, Stuart DI, Gilbert RJ, Brierley I. 2006. A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature 441: 244-247.
43. Napthine S, Liphardt J, Bloys A, Routledge S, Brierley I. 1999. The role of RNA pseudoknot stem 1 length in the promotion of efficient -1 ribosomal frameshifting. J Mol Biol 288: 305-320.
44. Nixon PL, Rangan A, Kim YG, Rich A, Hoffman DW, Hennig M, Giedroc DP. 2002. Solution structure of a luteoviral P1-P2 frameshifting mRNA pseudoknot. J Mol Biol 322: 621-633.
45. Noller HF, Yusupov MM, Yusupova GZ, Baucom A, Cate JH. 2002. Translocation of tRNA during protein synthesis. FEBS Lett 514: 11-16.
46. Ogle JM, Ramakrishnan V. 2005. Structural insights into translational fidelity. Annu Rev Biochem 74: 129-177.
47. Pallan PS, Marshall WS, Harp J, Jewett FC 3rd, Wawrzak Z, Brown BA 2nd, Rich A, Egli M. 2005. Crystal structure of a luteoviral RNA pseudoknot and model for a minimal ribosomal frameshifting motif. Biochemistry 44: 11315-11322.
48. Philippe C, Eyermann F, Benard L, Portier C, Ehresmann B, Ehresmann C. 1993. Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc Natl Acad Sci 90: 4394-4398.
49. Plant EP, Dinman JD. 2005. Torsional restraint: A new twist on frameshifting pseudoknots. Nucleic Acids Res 33: 1825-1833.
50. Plant EP, Dinman JD. 2006. Comparative study of the effects of heptameric slippery site composition on -1 frameshifting among different eukaryotic systems. RNA 12: 666-673.
51. Plant EP, Jacobs KL, Harger JW, Meskauskas A, Jacobs JL, Baxter JL, Petrov AN, Dinman JD. 2003. The 9-Å solution: How mRNA pseudoknots promote efficient programmed -1 ribosomal frameshifting. RNA 9: 168-174.
52. Pleij CW, Rietveld K, Bosch L. 1985. A new principle of RNA folding based on pseudoknotting. Nucleic Acids Res 13: 1717-1731.
53. Powers T, Noller HF. 1991. A functional pseudoknot in 16S ribosomal RNA. EMBO J 10: 2203-2214.
54. Puglisi JD, Wyatt JR, Tinoco I Jr. 1988. A pseudoknotted RNA oligonucleotide. Nature 331: 283-286.
55. Ringquist S, MacDonald M, Gibson T, Gold L. 1993. Nature of the ribosomal mRNA track: Analysis of ribosome-binding sites containing different sequences and secondary structures. Biochemistry 32: 10254-10262.
56. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310: 827-834.
57. Seol Y, Skinner GM, Visscher K. 2004. Elastic properties of a single-stranded charged homopolymeric ribonucleotide. Phys Rev Lett 93: 118102. doi: 10.1103/PhysRevLett.93.118102.
58. Shen LX, Tinoco I Jr. 1995. The structure of an RNA pseudoknot that causes efficient frameshifting in mouse mammary tumor virus. J Mol Biol 247: 963-978.
59. Snoussi K, Nonin-Lecomte S, Leroy JL. 2001. The RNA i-motif. J Mol Biol 309: 139-153.
60. Spahn CM, Beckmann R, Eswar N, Penczek PA, Sali A, Blobel G, Frank J. 2001. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA- ribosome and subunit-subunit interactions. Cell 107: 373-386.
61. Spedding G, Gluick TC, Draper DE. 1993. Ribosome initiation complex formation with the pseudoknotted alpha operon messenger RNA. J Mol Biol 229: 609-622.
62. Spiegel PC, Ermolenko DN, Noller HF. 2007. Elongation factor G stabilizes the hybrid-state conformation of the 70S ribosome. RNA 13: 1473-1482.
63. Staple DW, Butcher SE. 2005a. Pseudoknots: RNA structures with diverse functions. PLoS Biol 3: e213. doi: 10.1371/journal.pbio. 0030213.
64. Staple DW, Butcher SE. 2005b. Solution structure and thermodynamic investigation of the HIV-1 frameshift inducing element. J Mol Biol 349: 1011-1023.
65. Stern S, Moazed D, Noller HF. 1988. Structural analysis of RNA using chemical and enzymatic probing monitored by primer extension. Methods Enzymol 164: 481-489.
66. Su L, Chen L, Egli M, Berger JM, Rich A. 1999. Minor groove RNA triplex in the crystal structure of a ribosomal frameshifting viral pseudoknot. Nat Struct Biol 6: 285-292.
67. Takyar S, Hickerson RP, Noller HF. 2005. mRNA helicase activity of the ribosome. Cell 120: 49-58.
68. Tsuchihashi Z, Kornberg A. 1990. Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci 87: 2516-2520.
69. Valle M, Zavialov A, Sengupta J, Rawat U, Ehrenberg M, Frank J. 2003. Locking and unlocking of ribosomal motions. Cell 114: 123-134.
70. Weiss RB, Dunn DM, Shuh M, Atkins JF, Gesteland RF. 1989. E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol 1: 159-169.
71. Wen JD, Lancaster L, Hodges C, Zeri AC, Yoshimura SH, Noller HF, Bustamante C, Tinoco I. 2008. Following translation by single ribosomes one codon at a time. Nature 452: 598-603.
72. Wilson KS, Nechifor R. 2004. Interactions of translational factor EF-G with the bacterial ribosome before and after mRNA translocation. J Mol Biol 337: 15-30.
73. Ying BW, Fourmy D, Yoshizawa S. 2007. Substitution of the use of radioactivity by fluorescence for biochemical studies of RNA. RNA 13: 2042-2050.
74. Yoshizawa S, Fourmy D, Puglisi JD. 1999. Recognition of the codon-anticodon helix by ribosomal RNA. Science 285: 1722-1725.
75. Yusupova GZ, Yusupov MM, Cate JH, Noller HF. 2001. The path of messenger RNA through the ribosome. Cell 106: 233-241.
76. Yusupova G, Jenner L, Rees B, Moras D, Yusupov M. 2006. Structural basis for messenger RNA movement on the ribosome. Nature 444: 391-394.