Genetic Insertions and Diversification of the PolB-Type DNA Polymerase (gp43) of T4-Related Phages

Journal of Molecular Biology

Volumn 395, Issue 3, 2010, Pages 457-474

  Petrov, Vasiliy M ^a   Ratnayaka, Swarnamala ^a   Karam, Jim D ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

mobile DNA; molecular evolution; PolB family; split DNA polymerase; T4 related phages

Indexed keywords

DEOXYRIBONUCLEASE; DNA DIRECTED DNA POLYMERASE BETA; ENDONUCLEASE; GENE PRODUCT; GENE PRODUCT 43; UNCLASSIFIED DRUG;

AEROMONAS SALMONICIDA; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE T4; CARBOXY TERMINAL SEQUENCE; CISTRON; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE INSERTION; GENE TRANSFER; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA SPLICING; TRANSPOSON; UNTRANSLATED REGION;

AEROMONAS SALMONICIDA; ESCHERICHIA COLI;

EID: 73249128578     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.054     Document Type: Article

References (64)

1. Braithwaite D.K., and Ito J. Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res. 21 (1993) 787-802
2. Villarreal L.P., and DeFilippis V.R. A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J. Virol. 74 (2000) 7079-7084
3. Hubscher U., Nasheuer H.P., and Syvaoja J.E. Eukaryotic DNA polymerases, a growing family. Trends Biochem. Sci. 25 (2000) 143-147
4. Burgers P.M.J. Polymerase dynamics at the eukaryotic DNA replication fork. J. Biol. Chem. 284 (2009) 4041-4045
5. McElhinny S.N., Gordenin D., Stith C., Burgers P., and Kunkel T. Division of labor at the eukaryotic replication fork. Mol. Cell 30 (2008) 137-144
6. Kunkel T.A., and Burgers P.M. Dividing the workload at a eukaryotic replication fork. Trend Cell Biol. 18 (2008) 521-527
7. Barry E.R., and Bell S.D. DNA replication in the archaea. Microbiol. Mol. Biol. Rev. 70 (2006) 876-887
8. Duggin I.G., and Bell S.D. The chromosome replication machinery of the archaeon Sulfolobus solfataricus. J. Biol. Chem. 281 (2006) 15029-15032
9. Lao-Sirieix S.H., Marsh V.L., and Bell S.D. DNA replication and cell cycle. In: Cavicchioli R. (Ed). Archaea: Molecular and Cellular Biology (2007), ASM Press, Washington, DC 93-109
10. Goodman M.F. Coping with replication 'train wrecks' in Escherichia coli using Pol V, Pol II and RecA proteins. Trends Biochem. Sci. 25 (2000) 189-195
11. Sutton M.D., and Walker G.C. Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination. Proc. Natl Acad. Sci. USA 98 (2001) 8342-8349
12. Indiani C., Langston L.D., Yurieva O., Goodman M.F., and O'Donnell M. Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc. Natl Acad. Sci. USA 106 (2009) 6031-6038
13. Karam J.D., and Konigsberg W.H. DNA polymerase of the T4 related bacteriophages. In: Moldave K. (Ed). Progress in Nucleic Acids Research and Molecular Biology 64 (2000), Academic Press, San Diego, CA 65-96
14. Wang T.S., Wong S.W., and Korn D. Human DNA polymerase alpha: predicted functional domains and relationships with viral DNA polymerases. FASEB J. 3 (1989) 14-21
15. Bataille DE.A. Herpes simples virus type 1 replication and recombination. Biochimie 77 (1995) 787-795
16. Cortez D., Forterre P., and Gribaldo S. A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol. 10 (2009) R65
17. Gogarten J.P., Senejani A.G., Zhaxybayeva O., Olendzenski L., and Hilario E. Inteins: structure, function, and evolution. Annu. Rev. Microbiol. 56 (2002) 263-287
18. Perler F.B. InBase: the Intein Database. Nucleic Acids Res. 30 (2002) 383-384
19. Oshige M., Yoshida H., Hirose F., Takata K.I., Inoue Y., Aoyagi N., et al. Molecular cloning and expression during development of the Drosophila gene for the catalytic subunit of DNA polymerase epsilon. Gene 256 (2000) 93-100
20. Petrov V.M., and Karam J.D. Diversity of structure and function of DNA polymerase (gp43) of T4-related bacteriophages. Biochemistry (Moscow) 69 (2004) 1213-1218
21. Petrov V.M., Nolan J.M., Bertrand C., Levy D., Desplats C., Krisch H.M., and Karam J.D. Plasticity of the gene functions for DNA replication in the T4-like phages. J. Mol. Biol. 361 (2006) 46-68
22. Wang J., Sattar A.K., Wang C.C., Karam J.D., Konigsberg W.H., and Steitz T.A. Crystal structure of a Pol alpha family replication DNA polymerase from bacteriophage RB69. Cell 89 (1997) 1087-1099
23. Shamoo Y., and Steitz T.A. Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell 99 (1999) 155-166
24. Franklin M.C., Wang J., and Steitz T.A. Structure of the replicating complex of a pol alpha family DNA polymerase. Cell 105 (2001) 657-667
25. Bebenek A., Dressman H.K., Carver G.T., Ng S., Petrov V., Yang G., et al. Interacting fidelity defects in the replicative DNA polymerase of bacteriophage RB69. J. Biol. Chem. 276 (2001) 10387-10397
26. Hopfner K.P., Eichinger A., Engh R.A., Laue F., Ankenbauer W., Huber R., and Angerer B. Crystal structure of a thermostable type B DNA polymerase from Thermococcus gorgonarius. Proc. Natl Acad. Sci. USA 96 (1999) 3600-3605
27. Rodriguez A.C., Park H.W., Mao C., and Beese L.S. Crystal structure of a pol alpha family DNA polymerase from the hyperthermophilic archaeon Thermococcus sp. 9 degrees N-7. J. Mol. Biol. 299 (2000) 447-462
28. Hashimoto H., Nishioka M., Fujiwara S., Takagi M., Imanaka T., Inoue T., and Kai Y. Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. J. Mol. Biol. 306 (2001) 469-477
29. Zhao Y., Jeruzalmi D., Moarefi I., Leighton L., Lasken R., and Kuriyan J. Crystal structure of an archaebacterial DNA polymerase. Struct. Fold. Des. 7 (1999) 1189-1199
30. Savino C., Federici L., Johnson K.A., Vallone B., Nastopoulos V., Rossi M., et al. Insights into DNA replication: the crystal structure of DNA polymerase B1 from the archaeon Sulfolobus solfataricus. Structure 12 (2004) 2001-2008
31. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
32. Kelman Z., Pietrokovski S., and Hurwitz J. Isolation and characterization of a split B-type DNA polymerase from the archaeon Methanobacterium thermoautotrophicum deltaH. J. Biol. Chem. 274 (1999) 28751-28761
33. Nolan J.M., Petrov V., Bertrand C., Krisch H.M., and Karam J.D. Genetic diversity among five T4-like bacteriophages. Virol. J. 3 (2006) 30
34. Kowalski J.C., Belfort M., Stapleton M.A., Holpert M., Dansereau J.T., Pietrokovski S., et al. Configuration of the catalytic GIY-YIG domain of intron endonuclease I-TevI: coincidence of computational and molecular findings. Nucleic Acids Res. 27 (1999) 2115-2125
35. Landthaler M., and Shub DA. 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 (1999) 7005-7010
36. Michel F., and Westhof E. Modeling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216 (1990) 585-610
37. Sharma M., Ellis R.L., and Hinton D.M. 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 (1992) 6658-6662
38. Kutter E.G.K., Poglazov A., Marusich E., Shneider M., Aronsson P., Napuli A., et al. Evolution of T4-related phages. Virus Genes 11 (1996) 285-297
39. Burke J.M., Belfort M., Cech T.R., Davies R.W., Schweyen R.J., Shub D.A., et al. Structural conventions for group I introns. Nucleic Acids Res. 15 (1987) 7217-7221
40. Shub D.A., Gott J.M., Xu M.Q., Lang B.F., Michel F., Tomaschewski J., et al. Structural conservation among three homologous introns of bacteriophage T4 and the group I introns of eukaryotes. Proc. Natl Acad. Sci. USA 85 (1988) 1151-1155
41. Wang C.C., Yeh L.S., and Karam J.D. Modular organization of T4 DNA polymerase. Evidence from phylogenetics. J. Biol. Chem. 270 (1995) 26558-26564
42. Wang C.C., Pavlov A., and Karam J.D. Evolution of RNA-binding specificity in T4 DNA polymerase. J. Biol. Chem. 272 (1997) 17703-17710
43. Petrov V.M., and Karam J.D. RNA determinants of translational operator recognition by the DNA polymerases of bacteriophages T4 and RB69. Nucleic Acids Res. 30 (2002) 3341-3348
44. Petrov V.M., Ng S.S., and Karam J.D. Protein determinants of RNA binding by DNA polymerase of the T4-related bacteriophage RB69. J. Biol. Chem. 277 (2002) 33041-33048
45. Herr A.J., Atkins J.F., and Gesteland R.F. Coupling of open reading frames by translational bypassing. Annu. Rev. Biochem. 69 (2000) 343-372
46. Huang W.M., Ao S.Z., Casjens S., Orlandi R., Zsikus R., Weiss R., et al. A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 239 (1988) 1005-1012
47. Nichols B. Evolution of genes and enzymes of tryptophan biosynthesis. In: Neidhardt F.C., III Curtiss R., Ingraham J.L., Lin E.C.C., Brooks Low K., Magasanik B., Reznikoff W.S., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd edit. 2 (1996), ASM Press, Washington, DC 2638-2648
48. Miller E.S., Heidelberg J.F., Eisen J.A., Nelson W.C., Durkin A.S., Ciecko A., et al. Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J. Bacteriol. 185 (2003) 5220-5233
49. Friedrich N.C., Torrents E., Gibb E.A., Sahlin M., Sjoberg B.M., and Edgell D.R. Insertion of a homing endonuclease creates a genes-in-pieces ribonucleotide reductase that retains function. Proc. Natl Acad. Sci. USA 104 (2007) 6176-6181
50. Nossal N.G. A new look at old mutants of T4 DNA polymerase. Genetics 148 (1998) 1535-1538
51. Dressman H.K., Wang C.C., Karam J.D., and Drake J.W. Retention of replication fidelity by a DNA polymerase functioning in a distantly related environment. Proc. Natl Acad. Sci. USA 94 (1997) 8042-8046
52. Gibb E.A., and Edgell D.R. An RNA hairpin sequesters the ribosome binding site of the homing endonuclease mobE gene. J. Bacteriol. 191 (2009) 2409-2413
53. Hatfull G.F., Cresawn S.G., and Hendrix R.W. Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution. Res. Microbiol. 159 (2008) 332-339
54. Pedulla M.L., Ford M.E., Houtz J.M., Karthikeyan T., Wadsworth C., Lewis J.A., et al. Origins of highly mosaic mycobacteriophage genomes. Cell 113 (2003) 171-182
55. Belle A., Landthaler M., and Shub D.A. Intronless homing: site-specific endonuclease SegF of bacteriophage T4 mediates localized marker exclusion analogous to homing endonucleases of group I introns. Genes Dev. 16 (2002) 351-362
56. Kadyrov F.A., Shlyapnikov M.G., and Kryukov V.M. A phage T4 site-specific endonuclease, SegE, is responsible for a non-reciprocal genetic exchange between T-even-related phages. FEBS Lett. 415 (1997) 75-80
57. Liu Q., Belle A., Shub D.A., Belfort M., and Edgell D.R. SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. J. Mol. Biol. 334 (2003) 13-23
58. Sandegren L., Nord D., and Sjoberg B.M. SegH and Hef: two novel homing endonucleases whose genes replace the mobC and mobE genes in several T4-related phages. Nucleic Acids Res. 33 (2005) 6203-6213
59. Zeng Q., Bonocora R.P., and Shub D.A. A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr. Biol. 19 (2009) 218-222
60. Roman J., Rubin M.N., and Woodson S.A. Sequence specificity of in vivo reverse splicing of the Tetrahymena group I intron. RNA 5 (1999) 1-13
61. Roy S.W., and Irimia M. Mystery of intron gain: new data and new models. Trends Genet. 25 (2009) 67-73
62. Denou E., Bruttin A., Barretto C., Ngom-Bru C., Brussow H., and Zuber S. T4 phages against Escherichia coli diarrhea: potential and problems. Virology 388 (2009) 21-30
63. Pietrokovski S. Inteins spread and extinction in evolution. Trends Genet. 17 (2001) 465-472
64. Yeh L.S., Hsu T., and Karam J.D. Divergence of a DNA replication gene cluster in the T4-related bacteriophage RB69. J. Bacteriol. 180 (1998) 2005-2013