Insights into okazaki fragment synthesis by the T4 replisome: The fate of lagging-strand holoenzyme components and their influence on okazaki fragment size

Journal of Biological Chemistry

Volumn 288, Issue 29, 2013, Pages 20807-20816

  Chen, Danqi ^a   Yue, Hongjun ^a   Spiering, Michelle M ^a   Benkovic, Stephen J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAMP LOADER; DNA REPLICATIONS; DNA STRANDS; LAGGING-STRAND; OKAZAKI FRAGMENTS; SIGNALING PATHWAYS;

POLYMERS;

COORDINATION REACTIONS;

OKAZAKI FRAGMENT;

ARTICLE; DNA REPLICATION; DNA STRAND; MOLECULAR SIZE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REPLISOME; SIGNAL TRANSDUCTION;

DNA BINDING PROTEIN; DNA ENZYMES; DNA POLYMERASE; DNA REPLICATION; DNA SYNTHESIS; HOLOENZYME; LAGGING-STRAND POLYMERASE RECYCLING; OKAZAKI FRAGMENT; SLIDING CLAMP; T4 REPLISOME;

BACTERIOPHAGE T4; DNA; DNA REPLICATION; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; HOLOENZYMES; MODELS, BIOLOGICAL; MULTIENZYME COMPLEXES; SIGNAL TRANSDUCTION; VIRAL PROTEINS;

EID: 84880524629     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.485961     Document Type: Article

References (45)

1. Benkovic, S. J., Valentine, A. M., and Salinas, F. (2001) Replisome-mediated DNA replication. Annu. Rev. Biochem. 70, 181-208
2. Hamdan, S. M., and Richardson, C. C. (2009) Motors, switches, and contacts in the replisome. Annu. Rev. Biochem. 78, 205-243
3. Lee, S. J., and Richardson, C. C. (2011) Choreography of bacteriophage T7 DNA replication. Curr. Opin. Chem. Biol. 15, 580-586
4. O'Donnell, M. (2006) Replisome architecture and dynamics in Escherichia coli. J. Biol. Chem. 281, 10653-10656
5. Lionnet, T., Spiering, M. M., Benkovic, S. J., Bensimon, D., and Croquette, V. (2007) Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. Proc. Natl. Acad. Sci. U.S.A. 104, 19790-19795
6. Zhang, Z., Spiering, M. M., Trakselis, M. A., Ishmael, F. T., Xi, J., Benkovic, S. J., and Hammes, G. G. (2005) Assembly of the bacteriophage T4 primosome. Single-molecule and ensemble studies. Proc. Natl. Acad. Sci. U.S.A. 102, 3254-3259
7. Arumugam, S. R., Lee, T. H., and Benkovic, S. J. (2009) Investigation of stoichiometry of T4 bacteriophage helicase loader protein (gp59). J. Biol. Chem. 284, 29283-29289
8. Norcum, M. T., Warrington, J. A., Spiering, M. M., Ishmael, F. T., Trakselis, M. A., and Benkovic, S. J. (2005) Architecture of the bacteriophage T4 primosome. Electron microscopy studies of helicase (gp41) and primase (gp61). Proc. Natl. Acad. Sci. U.S.A. 102, 3623-3626
9. Nossal, N. G., Makhov, A. M., Chastain, P. D., 2nd, Jones, C. E., and Griffith, J. D. (2007) Architecture of the bacteriophage T4 replication complex revealed with nanoscale biopointers. J. Biol. Chem. 282, 1098-1108
10. Perumal, S. K., Raney, K. D., and Benkovic, S. J. (2010) Analysis of theDNA translocation and unwinding activities of T4 phage helicases. Methods 51, 277-288
11. Yang, J., Xi, J., Zhuang, Z., and Benkovic, S. J. (2005) The oligomeric T4 primase is the functional form during replication. J. Biol. Chem. 280, 25416-25423
12. Kaboord, B. F., and Benkovic, S. J. (1995) Accessory proteins function as matchmakers in the assembly of the T4 DNA polymerase holoenzyme. Curr. Biol. 5, 149-157
13. Trakselis, M. A., Alley, S. C., Abel-Santos, E., and Benkovic, S. J. (2001) Creating a dynamic picture of the sliding clamp during T4 DNA polymerase holoenzyme assembly by using fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. U.S.A. 98, 8368-8375
14. Manosas, M., Spiering, M. M., Zhuang, Z., Benkovic, S. J., and Croquette, V. (2009) Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome. Nat. Chem. Biol. 5, 904-912
15. Nelson, S. W., Kumar, R., and Benkovic, S. J. (2008)RNAprimer handoff in bacteriophage T4 DNA replication. The role of single-stranded DNAbinding protein and polymerase accessory proteins. J. Biol. Chem. 283, 22838-22846
16. Salinas, F., and Benkovic, S. J. (2000) Characterization of bacteriophage T4-coordinated leading- and lagging-strand synthesis on a minicircle substrate. Proc. Natl. Acad. Sci. U.S.A. 97, 7196-7201
17. Alberts, B. M., Barry, J., Bedinger, P., Formosa, T., Jongeneel, C. V., and Kreuzer, K. N. (1983) Studies onDNAreplication in the bacteriophage T4 in vitro system. Cold Spring Harbor Symp. Quant. Biol. 47, 655-668
18. Debyser, Z., Tabor, S., and Richardson, C. C. (1994) Coordination of leading and lagging strand DNA synthesis at the replication fork of bacteriophage T7. Cell 77, 157-166
19. Yang, J., Trakselis, M. A., Roccasecca, R. M., and Benkovic, S. J. (2003) The application of a minicircle substrate in the study of the coordinated T4 DNA replication. J. Biol. Chem. 278, 49828-49838
20. Lee, J., Chastain, P. D., 2nd, Kusakabe, T., Griffith, J. D., and Richardson, C. C. (1998) Coordinated leading and lagging strand DNA synthesis on a minicircular template. Mol. Cell 1, 1001-1010
21. Wu, C. A., Zechner, E. L., Hughes, A. J., Jr., Franden, M. A., McHenry, C. S., and Marians, K. J. (1992) Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. IV. Reconstitution of an asymmetric, dimericDNApolymerase III holoenzyme. J. Biol. Chem. 267, 4064-4073
22. Kadyrov, F. A., and Drake, J. W. (2001) Conditional coupling of leadingstrand and lagging-strand DNA synthesis at bacteriophage T4 replication forks. J. Biol. Chem. 276, 29559-29566
23. 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. U.S.A. 106, 13236-13241
24. Yang, J., Zhuang, Z., Roccasecca, R. M., Trakselis, M. A., and Benkovic, S. J. (2004) The dynamic processivity of the T4 DNA polymerase during replication. Proc. Natl. Acad. Sci. U.S.A. 101, 8289-8294
25. Ishmael, F. T., Trakselis, M. A., and Benkovic, S. J. (2003) Protein-protein interactions in the bacteriophage T4 replisome. The leading strand holoenzyme is physically linked to the lagging strand holoenzyme and the primosome. J. Biol. Chem. 278, 3145-3152
26. Downey, C. D., and McHenry, C. S. (2010) Chaperoning of a replicative polymerase onto a newly assembled DNA-bound sliding clamp by the clamp loader. Mol. Cell 37, 481-491
27. Trakselis, M. A., Roccasecca, R. M., Yang, J., Valentine, A. M., and Benkovic, S. J. (2003) Dissociative properties of the proteins within the bacteriophage T4 replisome. J. Biol. Chem. 278, 49839-49849
28. Yao, N., Turner, J., Kelman, Z., Stukenberg, P. T., Dean, F., Shechter, D., Pan, Z. Q., Hurwitz, J., and O'Donnell, M. (1996) Clamp loading, unloading and intrinsic stability of the PCNA, β and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells 1, 101-113
29. Su'etsugu, M., and Errington, J. (2011) The replicase sliding clamp dynamically accumulates behind progressing replication forks in Bacillus subtilis cells. Mol. Cell 41, 720-732
30. Yuzhakov, A., Turner, J., and O'Donnell, M. (1996) Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell 86, 877-886
31. Lia, G., Michel, B., and Allemand, J. F. (2012) Polymerase exchange during Okazaki fragment synthesis observed in living cells. Science 335, 328-331
32. Georgescu, R. E., Kurth, I., and O'Donnell, M. E. (2012) Single-molecule studies reveal the function of a third polymerase in the replisome. Nat. Struct. Mol. Biol. 19, 113-116
33. Reyes-Lamothe, R., Sherratt, D. J., and Leake, M. C. (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328, 498-501
34. Tanner, N. A., Tolun, G., Loparo, J. J., Jergic, S., Griffith, J. D., Dixon, N. E., and van Oijen, A. M. (2011) E. coli DNA replication in the absence of free β clamps. EMBO J. 30, 1830-1840
35. Yang, J., Nelson, S. W., and Benkovic, S. J. (2006) The control mechanism for lagging strand polymerase recycling during bacteriophage T4 DNA replication. Mol. Cell 21, 153-164
36. Berdis, A. J., and Benkovic, S. J. (1998) Simultaneous formation of functional leading and lagging strand holoenzyme complexes on a small, defined DNA substrate. Proc. Natl. Acad. Sci. U.S.A. 95, 11128-11133
37. Sexton, D. J., Kaboord, B. F., Berdis, A. J., Carver, T. E., and Benkovic, S. J. (1998) Dissecting the order of bacteriophage T4DNApolymerase holoenzyme assembly. Biochemistry 37, 7749-7756
38. Hamdan, S. M., Loparo, J. J., Takahashi, M., Richardson, C. C., and van Oijen, A. M. (2009) Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis. Nature 457, 336-339
39. Chastain, P. D., 2nd, Makhov, A. M., Nossal, N. G., and Griffith, J. D. (2000) Analysis of the Okazaki fragment distributions along single long DNAs replicated by the bacteriophage T4 proteins. Mol. Cell 6, 803-814
40. Morrical, S. W., Beernink, H. T., Dash, A., and Hempstead, K. (1996) The gene 59 protein of bacteriophage T4. Characterization of protein-protein interactions with gene 32 protein, the T4 single-stranded DNA binding protein. J. Biol. Chem. 271, 20198-20207
41. Burke, R. L., Munn, M., Barry, J., and Alberts, B. M. (1985) Purification and properties of the bacteriophage T4 gene 61 RNA priming protein. J. Biol. Chem. 260, 1711-1722
42. Zhuang, Z., Berdis, A. J., and Benkovic, S. J. (2006) An alternative clamp loading pathway via the T4 clamp loader gp44/62-DNA complex. Biochemistry 45, 7976-7989
43. Perumal, S. K., Ren, W., Lee, T. H., and Benkovic, S. J. (2013) How a holoenzyme for DNA replication is formed. Proc. Natl. Acad. Sci. U.S.A. 110, 99-104
44. Reddy, M. K., Weitzel, S. E., and von Hippel, P. H. (1993) Assembly of a functional replication complex without ATP hydrolysis. A direct interaction of bacteriophage T4 gp45 with T4DNApolymerase. Proc. Natl. Acad. Sci. U.S.A. 90, 3211-3215
45. Kurth, I., Georgescu, R. E., and O'Donnell, M. E. (2013) A solution to release twisted DNA during chromosome replication by coupled DNA polymerases. Nature 496, 119-122