Secondary structure of bacteriophage T4 gene 60 mRNA: Implications for translational bypassing

RNA

Volumn 19, Issue 5, 2013, Pages 685-700

  Todd, Gabrielle C ^a   Walter, Nils G ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Bacterial translation; Discontinuous open reading frame; Frameshift; MRNA structure; SHAPE structure probing; Terbium mediated structure probing

Indexed keywords

CHLORAMPHENICOL ACETYLTRANSFERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); MESSENGER RNA;

ACYLATION; ARTICLE; BACTERIOPHAGE T4; CODON; GENE MUTATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RIBOSOME; RNA ANALYSIS; RNA STRUCTURE; RNA TRANSLATION; WILD TYPE;

BACTERIOPHAGE T4; DNA MUTATIONAL ANALYSIS; DNA TOPOISOMERASES, TYPE II; INTERSPERSED REPETITIVE SEQUENCES; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA FOLDING; RNA, MESSENGER; STRUCTURE-ACTIVITY RELATIONSHIP; TERBIUM;

BACTERIA (MICROORGANISMS);

EID: 84876567617     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.037291.112     Document Type: Article

References (62)

1. Bonocora RP, Zeng Q, Abel EV, Shub DA. 2011. A homing endonucle-ase and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette. Proc Natl Acad Sci 108: 16351-16356.
2. Bucklin DJ, Wills NM, Gesteland RF, Atkins JF. 2005. P-site pairing subtleties revealed by the effects of different tRNAs on programmed translational bypassing where anticodon re-pairing to mRNA is separated from dissociation. J Mol Biol 345: 39-49. (Pubitemid 39572824)
3. Burke-Aguero DH, Hearst JE. 1990. An RNA Holliday junction? Structural and dynamic considerations of the bacteriophage T4 gene 60 interruption. J Mol Biol 213: 199-201. (Pubitemid 20176526)
4. Choi KM, Brimacombe R. 1998. The path of the growing peptide chain through the 23S rRNA in the 50S ribosomal subunit; a comparative cross-linking study with three different peptide families. Nucleic Acids Res 26: 887-895. (Pubitemid 28291638)
5. Choi KM, Atkins JF, Gesteland RF, Brimacombe R. 1998. Flexibility of the nascent polypeptide chain within the ribosome-Contacts from the peptide N-terminus to a specific region of the 30S subunit. Eur J Biochem 255: 409-413. (Pubitemid 28340249)
6. Chou MY, Chang KY. 2010. An intermolecular RNA triplex provides insight into structural determinants for the pseudoknot stimulator of-1 ribosomal frameshifting. Nucleic Acids Res 38: 1676-1685.
7. Chung BY, Firth AE, Atkins JF. 2010. Frameshifting in Alphaviruses: A Diversity of 3' Stimulatory Structures. J Mol Biol 397: 448-456.
8. Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: A bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12: 395.
9. Culver GM. 2001. Meanderings of the mRNA through the ribosome. Structure 9: 751-758. (Pubitemid 32913493)
10. Edgell DR, Gibb EA, Belfort M. 2010. Mobile DNA elements in T4 and related phages. Virol J 7: 290.
11. Ennifar E, Nikulin A, Tishchenko S, Serganov A, Nevskaya N, Garber M, Ehresmann B, Ehresmann C, Nikonov S, Dumas P. 2000. The crystal structure of UUCG tetraloop. J Mol Biol 304: 35-42.
12. Farabaugh PJ. 1996. Programmed translational frameshifting. Microbiol Rev 60: 103-134. (Pubitemid 26087764)
13. Firth AE, Brierley I. 2012. Non-canonical Translation in RNA Viruses. J Gen Virol 93: 1385-1409.
14. Gallant JA, Lindsley D. 1998. Ribosomes can slide over and beyond "hungry" codons, resuming protein chain elongation many nucleotides downstream. Proc Natl Acad Sci 95: 13771-13776.
15. Gherghe CM, Mortimer SA, Krahn JM, Thompson NL, Weeks KM. 2008. Slow conformational dynamics at C2'-endo nucleotides in RNA. J Am Chem Soc 130: 8884-8885. (Pubitemid 352000815)
16. Gherghe C, Lombo T, Leonard CW, Datta SA, Bess JW Jr, Gorelick RJ, Rein A, Weeks KM. 2010. Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome. Proc Natl Acad Sci 107: 19248-19253.
17. Giedroc DP, Cornish PV. 2009. Frameshifting RNA pseudoknots: Structure and mechanism. Virus Res 139: 193-208.
18. Hargittai MR, Musier-Forsyth K. 2000. Use of terbium as a probe of tRNA tertiary structure and folding. RNA 6: 1672-1680.
19. Harris DA, Walter NG. 2003. Probing RNA structure and metal-binding sites using terbium(III) footprinting. Curr Protoc Nucleic Acid Chem Chapter 6: Unit 6.8. doi: 10.1002/0471142700.nc0608s13.
20. Harris DA, Walter NG. 2005. Terbium(III) Footprinting as a probe of RNA structure and metal-binding sites. In Handbook of RNA biochemistry (ed. RK Hartmann, et al.), pp. 205-213. Wiley-VCH, Weinheim.
21. Harris DA, Tinsley RA, Walter NG. 2004. Terbium-mediated footprinting probes a catalytic conformational switch in the antigenomic hepatitis delta virus ribozyme. J Mol Biol 341: 389-403. (Pubitemid 38987777)
22. Hatfull GF. 2008. Bacteriophage genomics. Curr Opin Microbiol 11: 447-453.
23. Herr AJ, Atkins JF, Gesteland RF. 2000a. Coupling of open reading frames by translational bypassing. Annu Rev Biochem 69: 343-372.
24. Herr AJ, Gesteland RF, Atkins JF. 2000b. One protein from two open reading frames: Mechanism of a 50 nt translational bypass. EMBO J 19: 2671-2680. (Pubitemid 30323555)
25. Herr AJ, Wills NM, Nelson CC, Gesteland RF, Atkins JF. 2001. Drop-off during ribosome hopping. J Mol Biol 311: 445-452. (Pubitemid 32816579)
26. Huang WM, Ao SZ, Casjens S, Orlandi R, Zeikus R, Weiss R, Winge D, Fang M. 1988. A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 239: 1005-1012. (Pubitemid 18094166)
27. Jeong S, Sefcikova J, Tinsley RA, Rueda D, Walter NG. 2003. Trans-acting hepatitis delta virus ribozyme: Catalytic core and global structure are dependent on the 5' substrate sequence. Biochemistry 42: 7727-7740. (Pubitemid 36758938)
28. Kigawa T, Yabuki T, Matsuda N, Matsuda T, Nakajima R, Tanaka A, Yokoyama S. 2004. Preparation of Escherichia coli cell extract for highly productive cell-free protein expression. J Struct Funct Genomics 5: 63-68. (Pubitemid 39030621)
29. Kladwang W, VanLang CC, Cordero P, Das R. 2011. Understanding the errors of SHAPE-directed RNA structure modeling. Biochemistry 50: 8049-8056.
30. Kontos H, Napthine S, Brierley I. 2001. Ribosomal pausing at a frame-shifter RNA pseudoknot is sensitive to reading phase but shows little correlation with frameshift efficiency. Mol Cell Biol 21: 8657-8670. (Pubitemid 33108622)
31. Laponogov I, Pan XS, Veselkov DA, McAuley KE, Fisher LM, Sanderson MR. 2010. Structural basis of gate-DNA breakage and reseal-ing by type II topoisomerases. PLoS One 5: e11338.
32. Larsen B, Peden J, Matsufuji S, Matsufuji T, Brady K, Maldonado R, Wills NM, Fayet O, Atkins JF, Gesteland RF. 1995. Upstream stimulators for recoding. Biochem Cell Biol 73: 1123-1129.
33. Le SY, Chen JH, Maizel JV Jr. 1993. Identification of unusual RNA folding patterns encoded by bacteriophage T4 gene 60. Gene 124: 21-28. (Pubitemid 23065963)
34. Legiewicz M, Zolotukhin AS, Pilkington GR, Purzycka KJ, Mitchell M, Uranishi H, Bear J, Pavlakis GN, Le Grice SF, Felber BK. 2010. The RNA Transport Element of the Murine MusD Retrotransposon Requires Long-range Intramolecular Interactions for Function. J Biol Chem 285: 42097-42104.
35. Li GW, Oh E, Weissman JS. 2012. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484: 538-541.
36. Lovett PS. 1994. Nascent peptide regulation of translation. J Bacteriol 176: 6415-6417. (Pubitemid 24338050)
37. Low JT, Weeks KM. 2010. SHAPE-directed RNA secondary structure prediction. Methods 52: 150-158.
38. Maldonado R, Herr AJ. 1998. Efficiency of T4 gene 60 translational bypassing. J Bacteriol 180: 1822-1830. (Pubitemid 28173063)
39. Mazauric MH, Seol Y, Yoshizawa S, Visscher K, Fourmy D. 2009. Interaction of the HIV-1 frameshift signal with the ribosome. Nucleic Acids Res 37: 7654-7664.
40. McGinnis JL, Dunkle JA, Cate JH, Weeks KM. 2012. the Mechanisms of RNA SHAPE Chemistry. J Am Chem Soc 134: 6617-6624.
41. Mortimer SA, Weeks KM. 2007. A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J Am Chem Soc 129: 4144-4145. (Pubitemid 46595421)
42. Mortimer SA, Weeks KM. 2008. Time-resolved RNA SHAPE chemistry. J Am Chem Soc 130: 16178-16180.
43. 2+-induced compaction of single RNA molecules monitored by tethered particle microscopy. Biophys J 90: 3672-3685.
44. Pratt JM. 1984. Coupled transcription-translation in prokaryotic cell-free systems. IRL Press, New York.
45. Repoila F, Tetart F, Bouet JY, Krisch HM. 1994. Genomic polymorphism in the T-even bacteriophages. EMBO J 13: 4181-4192. (Pubitemid 24275875)
46. Reuter JS, Mathews DH. 2010. RNAstructure: Software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 129.
47. Ringquist S, MacDonald M, Gibson T, Gold L. 1993. Nature of the ribo-somal mRNA track: Analysis of ribosome-binding sites containing different sequences and secondary structures. Biochemistry 32: 10254-10262. (Pubitemid 23312458)
48. Sefcikova J, Krasovska MV, Spackova N, Sponer J, Walter NG. 2007a. Impact of an extruded nucleotide on cleavage activity and dynamic catalytic core conformation of the hepatitis delta virus ribozyme. Biopolymers 85: 392-406. (Pubitemid 46649821)
49. Sefcikova J, Krasovska MV, Sponer J, Walter NG. 2007b. The genomic HDV ribozyme utilizes a previously unnoticed U-turn motif to accomplish fast site-specific catalysis. Nucleic Acids Res 35: 1933-1946. (Pubitemid 47064261)
50. Seol Y, Skinner GM, Visscher K, Buhot A, Halperin A. 2007. Stretching of homopolymeric RNA reveals single-stranded helices and base-stacking. Phys Rev Lett 98: 158103.
51. Sissi C, Palumbo M. 2009. Effects of magnesium and related divalent metal ions in topoisomerase structure and function. Nucleic Acids Res 37: 702-711.
52. Steen KA, Rice GM, Weeks KM. 2012. Fingerprinting Noncanonical and Tertiary RNA Structures by Differential SHAPE Reactivity. J Am Chem Soc 134: 13160-13163.
53. Uzan M, Miller ES. 2010. Post-transcriptional control by bacteriophage T4: mRNA decay and inhibition of translation initiation. Virol J 7: 360.
54. Vasa SM, Guex N, Wilkinson KA, Weeks KM, Giddings MC. 2008. ShapeFinder: A software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis. RNA 14: 1979-1990.
55. Walter NG, Yang N, Burke JM. 2000. Probing non-selective cation binding in the hairpin ribozyme with Tb(III). J Mol Biol 298: 539-555.
56. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, Swanstrom R, Burch CL, Weeks KM. 2009. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460: 711-716.
57. Weiss RB, Huang WM, Dunn DM. 1990. A nascent peptide is required for ribosomal bypass of the coding gap in bacteriophage T4 gene 60. Cell 62: 117-126.
58. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, Mathews DH, Giddings MC, Weeks KM. 2008. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 6: e96.
59. ′-hy-droxyl reactivity in RNA. RNA 15: 1314-1321.
60. Wills NM, O'Connor M, Nelson CC, Rettberg CC, Huang WM, Gesteland RF, Atkins JF. 2008. Translational bypassing without pep-tidyl-tRNA anticodon scanning of coding gap mRNA. EMBO J 27: 2533-2544.
61. Woodson SA. 2001. Probing RNA folding pathways by RNA fingerprinting. Curr Protoc Nucleic Acid Chem Chapter 11: Unit 11.4. doi: 10.1002/047114270. nc1104s02.
62. Yusupova GZ, Yusupov MM, Cate JH, Noller HF. 2001. The path of messenger RNA through the ribosome. Cell 106: 233-241. (Pubitemid 32772633)