A homing endonuclease and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 39, 2011, Pages 16351-16356

  Bonocora, Richard P ^a   Zeng, Qinglu ^a,b   Abel, Ethan V ^a,c   Shub, David A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b Massachusetts Institute of Technology   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Bacteriophage gene structure; Group I intron; Horizontal gene transfer; Mobile genetic element; Ribosomal frameshifting

Indexed keywords

DNA; DNA TOPOISOMERASE; ENDONUCLEASE;

ARTICLE; BACTERIOPHAGE T4; CODON; ENZYME ACTIVITY; FRAMESHIFT MUTATION; GENE CASSETTE; GENE INSERTION; INTRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RNA SEQUENCE;

AMINO ACID SEQUENCE; BACTERIOPHAGE T4; BASE SEQUENCE; DNA TOPOISOMERASES, TYPE I; DNA, VIRAL; ENDONUCLEASES; GENE TRANSFER, HORIZONTAL; GENES, VIRAL; HYDROLYSIS; INTRONS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 80053649885     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1107633108     Document Type: Article

References (35)

1. Huang WM, Wei LS, Casjens S (1985) Relationship between bacteriophage T4 and T6 DNA topoisomerases. T6 39-protein subunit is equivalent to the combined T4 39- and 60-protein subunits. J Biol Chem 260:8973-8977. (Pubitemid 15011993)
2. Huang WM, et al. (1988) A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 239:1005-1012. (Pubitemid 18094166)
3. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680. (Pubitemid 24354800)
4. Seasholtz AF, Greenberg GR (1983) Identification of bacteriophage T4 gene 60 product and a role for this protein in DNA topoisomerase. J Biol Chem 258: 1221-1226. (Pubitemid 13139366)
5. Maldonado R, Herr AJ (1998) Efficiency of T4 gene 60 translational bypassing. J Bacteriol 180:1822-1830. (Pubitemid 28173063)
6. 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.
7. Herr AJ, Nelson CC, Wills NM, Gesteland RF, Atkins JF (2001) Analysis of the roles of tRNA structure, ribosomal protein L9, and the bacteriophage T4 gene 60 bypassing signals during ribosome slippage on mRNA. J Mol Biol 309:1029-1048. (Pubitemid 32623306)
8. Wills NM, et al. (2008) Translational bypassing without peptidyl-tRNA anticodon scanning of coding gap mRNA. EMBO J 27:2533-2544.
9. Repoila F, Tétart F, Bouet JY, Krisch HM (1994) Genomic polymorphism in the T-even bacteriophages. EMBO J 13:4181-4192. (Pubitemid 24275875)
10. F. Repoila (1995) Etude du Polymorphisme Genomique Chez les Bacteriophages T-pair. PhD thesis (Paul Sabatier University, Toulouse, France).
11. Petrov VM, Ratnayaka S, Nolan JM, Miller ES, Karam JD (2010) Genomes of the T4-related bacteriophages as windows on microbial genome evolution. Virol J 7:292.
12. Bonocora RP, Shub DA (2009) A likely pathway for formation of mobile group I introns. Curr Biol 19:223-228.
13. Zeng Q, Bonocora RP, Shub DA (2009) A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr Biol 19:218-222.
14. Edgell DR, Gibb EA, Belfort M (2010) Mobile DNA elements in T4 and related phages. Virol J 7:290.
15. Raghavan R, Minnick MF (2009) Group I introns and inteins: Disparate origins but convergent parasitic strategies. J Bacteriol 191:6193-6202.
16. Depew RE, Snopek TJ, Cozzarelli NR (1975) Characterization of a new class of deletions of the D region of the bacteriophage T4 genome. Virology 64:144-145.
17. Belle A, Landthaler M, Shub DA (2002) Intronless homing: Site-specific endonuclease SegF of bacteriophage T4 mediates localized marker exclusion analogous to homing endonucleases of group I introns. Genes Dev 16:351-362. (Pubitemid 34111414)
18. Quirk SM, Bell-Pedersen D, Belfort M (1989) Intron mobility in the T-even phages: High frequency inheritance of group I introns promoted by intron open reading frames. Cell 56:455-465.
19. Landthaler M, Lau NC, Shub DA (2004) Group I intron homing in Bacillus phages SPO1 and SP82: A gene conversion event initiated by a nicking homing endonuclease. J Bacteriol 186:4307-4314. (Pubitemid 38802579)
20. Baranov PV, Fayet O, Hendrix RW, Atkins JF (2006) Recoding in bacteriophages and bacterial IS elements. Trends Genet 22:174-181. (Pubitemid 43290021)
21. Michel F, Westhof E (1990) Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216:585-610. (Pubitemid 120037393)
22. Shub DA, et al. (1988) Structural conservation among three homologous introns of bacteriophage T4 and the group I introns of eukaryotes. Proc Natl Acad Sci USA 85: 1151-1155.
23. Landthaler M, Begley U, Lau NC, Shub DA (2002) Two self-splicing group I introns in the ribonucleotide reductase large subunit gene of Staphylococcus aureus phage Twort. Nucleic Acids Res 30:1935-1943. (Pubitemid 34537588)
24. Lazarevic V (2001) Ribonucleotide reductase genes of Bacillus prophages: A refuge to introns and intein coding sequences. Nucleic Acids Res 29:3212-3218.
25. Swithers KS, Senejani AG, Fournier GP, Gogarten JP (2009) Conservation of intron and intein insertion sites: Implications for life histories of parasitic genetic elements. BMC Evol Biol 9:303.
26. Marchler-Bauer A, et al. (2009) CDD: Specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37(Database issue):D205-D210.
27. Epstein RH, et al. (1963) Physiological studies of conditional lethal mutants of bacteriophage T4D. Cold Spring Harb Symp Quant Biol 28:375-392.
28. Petrov VM, et al. (2006) Plasticity of the gene functions for DNA replication in the T4-like phages. J Mol Biol 361:46-68. (Pubitemid 44043164)
29. Petrov VM, Ratnayaka S, Karam JD (2010) Genetic insertions and diversification of the PolB-type DNA polymerase (gp43) of T4-related phages. J Mol Biol 395:457-474.
30. Friedrich NC, et al. (2007) Insertion of a homing endonuclease creates a genes-in-pieces ribonucleotide reductase that retains function. Proc Natl Acad Sci USA 104: 6176-6181. (Pubitemid 47186068)
31. Crona M, et al. (2011) Assembly of a fragmented ribonucleotide reductase by protein interaction domains derived from a mobile genetic element. Nucleic Acids Res 39: 1381-1389.
32. Dassa B, London N, Stoddard BL, Schueler-Furman O, Pietrokovski S (2009) Fractured genes: A novel genomic arrangement involving new split inteins and a new homing endonuclease family. Nucleic Acids Res 37:2560-2573.
33. Horton RM, Cai ZL, Ho SN, Pease LR (1990) Gene splicing by overlap extension: Tailormade genes using the polymerase chain reaction. Biotechniques 8:528-535. (Pubitemid 20153761)
34. Bonocora RP, Shub DA (2001) A novel group I intron-encoded endonuclease specific for the anticodon region of tRNA(fMet) genes. Mol Microbiol 39:1299-1306. (Pubitemid 32225139)
35. Zeng Q (2008) Collaborative homing directed by site-specific endonucleases in bacteriophages. PhD thesis (University at Albany, State University of New York, Albany, NY).