Phage T4 mobE promotes trans homing of the defunct homing endonuclease I-TevIII

Nucleic Acids Research

Volumn 37, Issue 21, 2009, Pages 7110-7123

  Wilson, Gavin W ^a   Edgell, David R ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE T4 ENDONUCLEASE MOBE; DEOXYRIBONUCLEASE I; DEOXYRIBONUCLEASE I TEVIII; ENDONUCLEASE; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; BACTERIOPHAGE T4; CONTROLLED STUDY; DNA NICK TRANSLATION; DNA SEQUENCE; DNA TRANSCRIPTION; GENE CONVERSION; GENE DELETION; GENETIC POLYMORPHISM; IN VIVO STUDY; INHERITANCE; INTRON; MOLECULAR DYNAMICS; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; BIOSYNTHESIS; CHROMOSOME MAP; ENZYMOLOGY; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; REGULATORY SEQUENCE; TRANSPOSON;

BACTERIOPHAGE T4; CHROMOSOME MAPPING; DNA TRANSPOSABLE ELEMENTS; ENDODEOXYRIBONUCLEASES; INTRONS; RECOMBINATION, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RIBONUCLEOTIDE REDUCTASES; TRANSCRIPTION, GENETIC;

EID: 75349114910     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp769     Document Type: Article

References (50)

1. Belfort, M., Derbyshire, V., Cousineau, B. and Lambowitz, A. (2002) Chapter 31. In Craig, N., Craigie, R., Gellert, M. and Lambowitz, A. (eds), Mobile DNA II. ASM Press, New York, pp. 761-783.
2. Belle, A., Landthaler, M. and Shub, D.A. (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.
3. Goodrich-Blair, H. and Shub, D.A. (1996) Beyond homing: competition between intron endonucleases confers a selective advantage on flanking genetic markers. Cell, 84, 211-221.
4. Russell, R.L. and Huskey, R.J. (1974) Partial exclusion between T-even bacteriophages: an incipient genetic isolation mechanism. Genetics, 78, 989-1014.
5. Edgell, D.R. (2002) Selfish DNA: new abode for homing endonucleases. Curr. Biol., 12, R276-R278.
6. Liu, Q., Belle, A., Shub, D.A., Belfort, M. and Edgell, D.R. (2003) SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. J. Mol. Biol., 334, 13-23.
7. Miller, E.S., Kutter, E., Mosig, G., Arisaka, F., Kunisawa, T. and Ruger, W. (2003) Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev., 67, 86-156.
8. Huang, Y.J., Parker, M.M. and Belfort, M. (1999) Role of exonucleolytic degradation in group I intron homing in phage T4. Genetics, 153, 1501-1512.
9. Mueller, J.E., Clyman, J., Huang, Y.J., Parker, M.M. and Belfort, M. (1996) Intron mobility in phage T4 occurs in the context of recombination-dependent DNA replication by way of multiple pathways. Genes Dev., 10, 351-364.
10. Parker, M.M., Belisle, M. and Belfort, M. (1999) Intron homing with limited exon homology. Illegitimate double-strand-break repair in intron acquisition by phage T4. Genetics, 153, 1513-1523.
11. Bell-Pedersen, D., Quirk, S.M., Aubrey, M. and Belfort, M. (1989) A site-specific endonuclease and co-conversion of flanking exons associated with the mobile td intron of phage T4. Gene, 82, 119-126.
12. Brok-Volchanskaya, V.S., Kadyrov, F.A., Sivogrivov, D.E., Kolosov, P.M., Sokolov, A.S., Shlyapnikov, M.G., Kryukov, V.M. and Granovsky, I.E. (2008) Phage T4 SegB protein is a homing endonuclease required for the preferred inheritance of T4 tRNA gene region occurring in co-infection with a related phage. Nucleic Acids Res., 36, 2094-2105.
13. Kadyrov, F.A., Shlyapnikov, M.G. and Kryukov, V.M. (1997) A phage T4 site-specific endonuclease, SegE, is responsible for a non-reciprocal genetic exchange between T-even-related phages. FEBS Lett., 415, 75-80.
14. Sharma, M., Ellis, R.L. and Hinton, D.M. (1992) Identification of a family of bacteriophage T4 genes encoding proteins similar to those present in group I introns of fungi and phage. Proc. Natl Acad. Sci. USA, 89, 6658-6662.
15. Sharma, M. and Hinton, D.M. (1994) Purification and characterization of the SegA protein of bacteriophage T4, an endonuclease related to proteins encoded by group I introns. J. Bacteriol., 176, 6439-6448.
16. Kutter, E., Gachechiladze, K., Poglazov, A., Marusich, E., Shneider, M., Aronsson, P., Napuli, A., Porter, D. and Mesyanzhinov, V. (1995) Evolution of T4-related phages. Virus Genes, 11, 285-297.
17. Landthaler, M., Shen, B.W., Stoddard, B.L. and Shub, D.A. (2006) I-BasI and I-HmuI: two phage intron-encoded endonucleases with homologous DNA recognition sequences but distinct DNA specificities. J. Mol. Biol., 358, 1137-1151.
18. Landthaler, M. and Shub, D.A. (2003) The nicking homing endonuclease I-BasI is encoded by a group I intron in the DNA polymerase gene of the Bacillus thuringiensis phage Bastille. Nucleic Acids Res., 31, 3071-3077.
19. Landthaler, M., Lau, N.C. and Shub, D.A. (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.
20. Gott, J.M., Zeeh, A., Bell-Pedersen, D., Ehrenman, K., Belfort, M. and Shub, D.A. (1988) Genes within genes: independent expression of phage T4 intron open reading frames and the genes in which they reside. Genes Dev., 2, 1791-1799.
21. Edgell, D.R., Derbyshire, V., Van Roey, P., LaBonne, S., Stanger, M.J., Li, Z., Boyd, T.M., Shub, D.A. and Belfort, M. (2004) Intron-encoded homing endonuclease I-TevI also functions as a transcriptional autorepressor. Nat. Struct. Mol. Biol., 11, 936-944.
22. Sandegren, L., Nord, D. and Sjöberg, B.-M. (2005) SegH and Hef: two novel homing endonucleases whose genes replace the mobC and mobE genes in several T4-related phages. Nucleic Acids Res., 33, 6203-6213.
23. Gott, J.M., Shub, D.A. and Belfort, M. (1986) Multiple self-splicing introns in bacteriophage T4: evidence from autocatalytic GTP labeling of RNA in vitro. Cell, 47, 81-87.
24. Robbins, J.B., Stapleton, M., Stanger, M.J., Smith, D., Dansereau, J.T., Derbyshire, V. and Belfort, M. (2007) Homing endonuclease I-TevIII: dimerization as a means to a double-strand break. Nucleic Acids Res., 35, 1589-1600.
25. Eddy, S.R. and Gold, L. (1991) The phage T4 nrdB intron: a deletion mutant of a version found in the wild. Genes Dev., 5, 1032-1041.
26. Horton, R.M. (1997) In vitro recombination and mutagenesis of DNA. SOEing together tailor-made genes. Methods Mol. Biol., 67, 141-149.
27. Miller, E.S. and Carlson, K. (1994) Chapter 45.1. In Karam, J.D. (ed.), Molecular Biology of Bacteriophage T4. ASM Press, Washington, D.C., pp. 455-456.
28. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
29. Gibb, E.A. and Edgell, D.R. (2007) Multiple controls regulate the expression of mobE, an HNH homing endonuclease gene embedded within a ribonucleotide reductase gene of phage Aeh1. J. Bacteriol., 189, 4648-4661.
30. Crooks, G.E., Hon, G., Chandonia, J.M. and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
31. Tseng, M.J., Hilfinger, J.M., Walsh, A. and Greenberg, G.R. (1988) Total sequence, flanking regions, and transcripts of bacteriophage T4 nrdA gene, coding for alpha chain of ribonucleoside diphosphate reductase. J. Biol. Chem., 263, 16242-16251.
32. Tseng, M.J., He, P., Hilfinger, J.M. and Greenberg, G.R. (1990) Bacteriophage T4 nrdA and nrdB genes, encoding ribonucleotide reductase, are expressed both separately and coordinately: characterization of the nrdB promoter. J. Bacteriol., 172, 6323-6332.
33. Clark, J.M. (1988) Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Res., 16, 9677-9686.
34. Edgell, D.R., Stanger, M.J. and Belfort, M. (2004) Coincidence of cleavage sites of intron endonuclease I-TevI and critical sequences of the host thymidylate synthase gene. J. Mol. Biol., 343, 1231-1241.
35. Scalley-Kim, M., McConnell-Smith, A. and Stoddard, B.L. (2007) Coevolution of a homing endonuclease and its host target sequence. J. Mol. Biol., 372, 1305-1319.
36. Sahlin, M., Lassmann, G., Potsch, S., Slaby, A., Sjoberg, B.M. and Graslund, A. (1994) Tryptophan radicals formed by iron/oxygen reaction with Escherichia coli ribonucleotide reductase protein R2 mutant Y122F. J. Biol. Chem., 269, 11699-11702.
37. Nordlund, P. and Eklund, H. (1993) Structure and function of the Escherichia coli ribonucleotide reductase protein R2. J. Mol. Biol., 232, 123-164.
38. Derbyshire, V., Kowalski, J.C., Dansereau, J.T., Hauer, C.R. and Belfort, M. (1997) Two-domain structure of the td intron-encoded endonuclease I-TevI correlates with the two-domain configuration of the homing site. J. Mol. Biol., 265, 494-506.
39. Shen, B.W., Landthaler, M., Shub, D.A. and Stoddard, B.L. (2004) DNA binding and cleavage by the HNH homing endonuclease I-HmuI. J. Mol. Biol., 342, 43-56.
40. Quirk, S.M., Bell-Pederesen, D. and Belfort, M. (1990) Intron mobility in the T-even phages: high frequency inheritance of group I introns promoted by intron open reading frames. Cell, 56, 455-465.
41. Zeng, Q., Bonocora, R.P. and Shub, D.A. (2009) A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr. Biol., 19, 218-222.
42. Bonocora, R.P. and Shub, D.A. (2009) A likely pathway for formation of mobile group I introns. Curr. Biol., 19, 223-228.
43. Yang, G., Zhang, F., Hancock, C.N. and Wessler, S.R. (2007) Transposition of the rice miniature inverted repeat transposable element mPing in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 104, 10962-10967.
44. Dewannieux, M. and Heidmann, T. (2005) L1-mediated retrotransposition of murine B1 and B2 SINEs recapitulated in cultured cells. J. Mol. Biol., 349, 241-247.
45. Dewannieux, M., Esnault, C. and Heidmann, T. (2003) LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet., 35, 41-48.
46. Landthaler, M. and Shub, D.A. (1999) Unexpected abundance of self-splicing introns in the genome of bacteriophage Twort: introns in multiple genes, a single gene with three introns, and exon skipping by group I ribozymes. Proc. Natl Acad. Sci. USA, 96, 7005-7010.
47. Liu, X.Q., Yang, J. and Meng, Q. (2003) Four inteins and three group II introns encoded in a bacterial ribonucleotide reductase gene. J. Biol. Chem., 278, 46826-46831.
48. Landthaler, M., Begley, U., Lau, N.C. and Shub, D.A. (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.
49. Lazarevic, V., Soldo, B., Dusterhoft, A., Hilbert, H., Mauel, C. and Karamata, D. (1998) Introns and intein coding sequence in the ribonucleotide reductase genes of Bacillus subtilis temperate bacteriophage SPβ. Proc. Natl Acad. Sci. USA, 95, 1692-1697.
50. Nakayama, H., Morinaga, Y., Nomura, N., Nunoura, T., Sako, Y. and Uchida, A. (2003) An archaeal homing endonuclease I-PogI cleaves at the insertion site of the neighboring intron, which has no nested open reading frame. FEBS Lett., 544, 165-170.