A single-molecule approach to DNA replication in Escherichia coli cells demonstrated that DNA polymerase III is a major determinant of fork speed

Molecular Microbiology

Volumn 90, Issue 3, 2013, Pages 584-596

  Pham, Tuan Minh ^a   Tan, Kang Wei ^a   Sakumura, Yuichi ^a,b   Okumura, Katsuzumi ^c   Maki, Hisaji ^a   Akiyama, Masahiro Tatsumi ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b AICHI PREFECTURAL UNIVERSITY   (Japan)

^c MIE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA DIRECTED DNA POLYMERASE GAMMA;

ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; CELL LABELING; CELL MOTION; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; RNA TRANSLATION; WILD TYPE;

ESCHERICHIA COLI;

BROMODEOXYURIDINE; CHROMOSOMES, BACTERIAL; DNA POLYMERASE III; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION; THYMIDINE;

EID: 84887111642     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12386     Document Type: Article

References (56)

1. Ahmad, S.I., Kirk, S.H., and Eisenstark, A. (1998) Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu Rev Microbiol 52: 591-625.
2. Akabayov, B., Akabayov, S.R., Lee, S.J., Wagner, G., and Richardson, C.C. (2013) Impact of macromolecular crowding on DNA replication. Nat Commun 4: 1615.
3. Akaike, H. (1973) Information theory and an extension of the maximum likelihood principle. In 2nd International Symposium on Information Theory. Petrov, B.N., and Csáki, F. (eds). Budapest: Akadémiai Kiadó, pp. 267-281.
4. Atkinson, J., Gupta, M.K., Rudolph, C.J., Bell, H., Lloyd, R.G., and McGlynn, P. (2011) Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication. Nucleic Acids Res 39: 949-957.
5. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
6. Bates, D. (2008) The bacterial replisome: back on track? Mol Microbiol 69: 1341-1348.
7. Beacham, I.R., and Pritchard, R.H. (1971) The role of nucleoside phosphorylases in the degradation of deoxyribonucleosides by thymine-requiring mutants of E.coli. Mol Gen Genet 110: 289-298.
8. Bensimon, A., Simon, A., Chiffaudel, A., Croquette, V., Heslot, F., and Bensimon, D. (1994) Alignment and sensitive detection of DNA by a moving interface. Science 265: 2096-2098.
9. Bianco, J.N., Poli, J., Saksouk, J., Bacal, J., Silva, M.J., Yoshida, K., etal. (2012) Analysis of DNA replication profiles in budding yeast and mammalian cells using DNA combing. Methods 57: 149-157.
10. Boubakri, H., de Septenville, A.L., Viguera, E., and Michel, B. (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29: 145-157.
11. Breier, A.M., Weier, H.U., and Cozzarelli, N.R. (2005) Independence of replisomes in Escherichia coli chromosomal replication. Proc Natl Acad Sci USA 102: 3942-3947.
12. Burnham, K.P., and Anderson, D.R. (1998) Model Selection and Inference: A Practical Information-Theoretical Approach. New York: Springer-Verlag.
13. Colasanti, J., and Denhardt, D.T. (1987) The Escherichia coli rep mutation. X. Consequences of increased and decreased Rep protein levels. Mol Gen Genet 209: 382-390.
14. Cooper, S., and Helmstetter, C.E. (1968) Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 31: 519-540.
15. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
16. Funnell, B.E., Baker, T.A., and Kornberg, A. (1986) Complete enzymatic replication of plasmids containing the origin of the Escherichia coli chromosome. J Biol Chem 261: 5616-5624.
17. Guy, C.P., Atkinson, J., Gupta, M.K., Mahdi, A.A., Gwynn, E.J., Rudolph, C.J., etal. (2009) Rep provides a second motor at the replisome to promote duplication of protein-bound DNA. Mol Cell 36: 654-666.
18. Guyer, M.S., Reed, R.R., Steitz, J.A., and Low, K.B. (1981) Identification of a sex-factor-affinity site in E.coli as γδ. Cold Spring Harb Symp Quant Biol 45 (Pt 1): 135-140.
19. Guzmán, E.C., Salguero, I., Martín, C.M., Acedo, E.L., Guarino, E., Sánchez-Romero, A., etal. (2011) Relationship between fork progression and initiation of chromosome replication in E. coli. In DNA Replication-Current Advances. Seligmann, H. (ed.). Croatia: Tech, pp. 203-220.
20. Higuchi, K., Katayama, T., Iwai, S., Hidaka, M., Horiuchi, T., and Maki, H. (2003) Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cell 8: 437-449.
21. Indiani, C., Langston, L.D., Yurieva, O., Goodman, M.F., and O'Donnell, M. (2009) Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc Natl Acad Sci USA 106: 6031-6038.
22. Jergic, S., Horan, N.P., Elshenawy, M.M., Mason, C.E., Urathamakul, T., Ozawa, K., etal. (2013) A direct proofreader-clamp interaction stabilizes the Pol III replicase in the polymerization mode. EMBO J 32: 1322-1333.
23. Johnson, D.S., Bai, L., Smith, B.Y., Patel, S.S., and Wang, M.D. (2007) Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129: 1299-1309.
24. Khodursky, A.B., Peter, B.J., Schmid, M.B., DeRisi, J., Botstein, D., Brown, P.O., and Cozzarelli, N.R. (2000) Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc Natl Acad Sci USA 97: 9419-9424.
25. Kim, S., Dallmann, H.G., McHenry, C.S., and Marians, K.J. (1996) Coupling of a replicative polymerase and helicase: a τ-DnaB interaction mediates rapid replication fork movement. Cell 84: 643-650.
26. Kornberg, A., and Baker, T. (1992) DNA Replication. New York: W. H. Freeman and Company.
27. Lane, H.E.D., and Denhardt, D.T. (1975) The rep mutation IV. Slower movement of replication forks in Escherichia coli rep strain. J Mol Biol 97: 99-112.
28. McHenry, C.S. (2011) DNA replicases from a bacterial perspective. Annu Rev Biochem 80: 403-436.
29. McInerney, P., and O'Donnell, M. (2004) Functional uncoupling of twin polymerases: mechanism of polymerase dissociation from a lagging-strand block. J Biol Chem 279: 21543-21551.
30. McLachlan, G.J., and Basford, K.E. (1988) Mixture Models: Inference and Applications to Clustering. New York: Marcel Dekker.
31. McLachlan, G.J., and Peel, D. (2000) Finite Mixture Models. New York: Wiley.
32. Maki, H., and Furukohri, A. (2013) DNA polymerase III, Bacteral. In The Encyclopedia of Biological Chemistry, Vol. 2. Lennarz, W.J., and Lane, M.D. (eds). Waltham, MA: Academic Press, pp. 92-95.
33. Maki, H., Horiuchi, T., and Kornberg, A. (1985) The polymerase subunit of DNA polymerase III of Escherichia coli. I. Amplification of the dnaE gene product and polymerase activity of the α subunit. J Biol Chem 260: 12982-12986.
34. Maki, H., Mo, J.Y., and Sekiguchi, M. (1991) A strong mutator effect caused by an amino acid change in the α subunit of DNA polymerase III of Escherichia coli. J Biol Chem 266: 5055-5061.
35. Miller, J.H. (1972) Experiments in Molecular Genetics. New York: Cold Spring Harbor Laboratory Press.
36. Mirkin, E.V., and Mirkin, S.M. (2007) Replication fork stalling at natural impediments. Microbiol Mol Biol Rev 71: 13-35.
37. O'Donnell, M. (2006) Replisome architecture and dynamics in Escherichia coli. J Biol Chem 281: 10653-10656.
38. Odsbu, I., Morigen, and Skarstad, K. (2009) A reduction in ribonucleotide reductase activity slows down the chromosome replication fork but does not change its localization. PLoS ONE 4: e7617.
39. van Oijen, A.M., and Loparo, J.J. (2010) Single-molecule studies of the replisome. Annu Rev Biophys 39: 429-448.
40. Patel, S.S., Pandey, M., and Nandakumar, D. (2011) Dynamic coupling between the motors of DNA replication: hexameric helicase, DNA polymerase, and primase. Curr Opin Chem Biol 15: 595-605.
41. Pato, M.L. (1979) Alterations of deoxyribonucleoside triphosphate pools in Escherichia coli: effects on deoxyribonucleic acid replication and evidence for compartmentation. J Bacteriol 140: 518-524.
42. Pennington, J.M., and Rosenberg, S.M. (2007) Spontaneous DNA breakage in single living Escherichia coli cells. Nat Genet 39: 797-802.
43. Rayssiguier, C., Thaler, D.S., and Radman, M. (1989) The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342: 396-401.
44. Renzette, N., Gumlaw, N., Nordman, J.T., Krieger, M., Yeh, S.P., Long, E., etal. (2005) Localization of RecA in Escherichia coli K-12 using RecA-GFP. Mol Microbiol 57: 1074-1085.
45. Roepke, R.R., Libby, R.L., and Small, M.H. (1944) Mutation or variation of Escherichia coli with respect to growth requirements. J Bacteriol 48: 401-412.
46. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning, A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
47. Skarstad, K., and Katayama, T. (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5: a012922.
48. Sugaya, Y., Ihara, K., Masuda, Y., Ohtsubo, E., and Maki, H. (2002) Hyper-processive and slower DNA chain elongation catalysed by DNA polymerase III holoenzyme purified from the dnaE173 mutator mutant of Escherichia coli. Genes Cells 7: 385-399.
49. Sugimura, K., Takebayashi, S., Taguchi, H., Takeda, S., and Okumura, K. (2008) PARP-1 ensures regulation of replication fork progression by homologous recombination on damaged DNA. J Cell Biol 183: 1203-1212.
50. Tanner, N.A., Hamdan, S.M., Jergic, S., Loscha, K.V., Schaeffer, P.M., Dixon, N.E., and van Oijen, A.M. (2008) Single-molecule studies of fork dynamics in Escherichia coli DNA replication. Nat Struct Mol Biol 15: 170-176.
51. Tanner, N.A., Loparo, J.J., Hamdan, S.M., Jergic, S., Dixon, N.E., and van Oijen, A.M. (2009) Real-time single-molecule observation of rolling-circle DNA replication. Nucleic Acids Res 37: e27.
52. Tehranchi, A.K., Blankschien, M.D., Zhang, Y., Halliday, J.A., Srivatsan, A., Peng, J., etal. (2010) The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 141: 595-605.
53. Titz, B., Häuser, R., Engelbrecher, A., and Uetz, P. (2007) The Escherichia coli protein YjjG is a house-cleaning nucleotidase in vivo. FEMS Microbiol Lett 270: 49-57.
54. Willetts, N.S., Clark, A.J., and Low, B. (1969) Genetic location of certain mutations conferring recombination deficiency in Escherichia coli. J Bacteriol 97: 244-249.
55. Wu, C.A., Zechner, E.L., and Marians, K.J. (1992) Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. I. Multiple effectors act to modulate Okazaki fragment size. J Biol Chem 267: 4030-4044.
56. Yao, N.Y., Georgescu, R.E., Finkelstein, J., and O'Donnell, M.E. (2009) Single-molecule analysis reveals that the lagging strand increases replisome processivity but slows replication fork progression. Proc Natl Acad Sci USA 106: 13236-13241.