Impact of macromolecular crowding on DNA replication

Nature Communications

Volumn 4, Issue , 2013, Pages

  Akabayov, Barak ^a   Akabayov, Sabine R ^a   Lee, Seung Joo ^a   Wagner, Gerhard ^a   Richardson, Charles C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA POLYMERASE; HELICASE;

BACTERIOPHAGE; CATALYSIS; DIFFUSION; ENZYME ACTIVITY; MITOCHONDRIAL DNA; NUCLEAR MAGNETIC RESONANCE; PROTEIN; X-RAY DIFFRACTION;

ARTICLE; BACTERIOPHAGE T7; DIFFUSION; DNA REPLICATION; ENZYME ACTIVITY; MACROMOLECULAR CROWDING; MACROMOLECULE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN STRUCTURE; X RAY; X RAY CRYSTALLOGRAPHY;

BACTERIOPHAGE T7; BASE SEQUENCE; CATALYSIS; DIFFUSION; DNA REPLICATION; DNA, VIRAL; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

EID: 84875898703     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2620     Document Type: Article

References (51)

1. Zimmerman, S. B. & Minton, A. P. Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu. Rev. Biophys. Biomol. Struct. 22, 27-65 (1993). (Pubitemid 23180316)
2. Zimmerman, S. B. & Trach, S. O. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J. Mol. Biol. 222, 599-620 (1991).
3. Minton, A. P. How can biochemical reactions within cells differ from those in test tubes? J. Cell Sci. 119, 2863-2869 (2006). (Pubitemid 44177864)
4. Ogston, A. G. & Phelps, C. F. Exclusion of inulin from solutions of hyaluronic acid. Nature 187, 1024 (1960).
5. Minton, A. P. Effect of a concentrated 'inert' macromolecular cosolute on the stability of a globular protein with respect to denaturation by heat and by chaotropes: a statistical-thermodynamic model. Biophys. J. 78, 101-109 (2000). (Pubitemid 30207122)
6. Minton, A. P. & Wilf, J. Effect of macromolecular crowding upon the structure and function of an enzyme: glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 20, 4821-4826 (1981).
7. Perham, M., Stagg, L. & Wittung-Stafshede, P. Macromolecular crowding increases structural content of folded proteins. FEBS Lett. 581, 5065-5069 (2007). (Pubitemid 47576087)
8. Strey, H. H., Podgornik, R., Rau, D. C. & Parsegian, V. A. DNA-DNA interactions. Curr. Opin. Struct. Biol. 8, 309-313 (1998). (Pubitemid 28321357)
9. Stagg, L., Zhang, S. Q., Cheung, M. S. & Wittung-Stafshede, P. Molecular crowding enhances native structure and stability of alpha/beta protein flavodoxin. Proc. Natl Acad. Sci. USA 104, 18976-18981 (2007).
10. Fuller, R. S., Kaguni, J. M. & Kornberg, A. Enzymatic replication of the origin of the Escherichia coli chromosome. Proc. Natl Acad. Sci. USA 78, 7370-7374 (1981). (Pubitemid 12186142)
11. Pheiffer, B. H. & Zimmerman, S. B. Polymer-stimulated ligation: enhanced blunt-or cohesive-end ligation of DNA or deoxyribooligonucleotides by T4 DNA ligase in polymer solutions. Nucleic Acids Res. 11, 7853-7871 (1983).
12. Harrison, B. & Zimmerman, S. B. T4 polynucleotide kinase: macromolecular crowding increases the efficiency of reaction at DNA termini. Anal. Biochem. 158, 307-315 (1986).
13. Jarvis, T. C., Ring, D. M., Daube, S. S. & von Hippel, P. H. 'Macromolecular crowding': thermodynamic consequences for protein-protein interactions within the T4 DNA replication complex. J. Biol. Chem. 265, 15160-15167 (1990).
14. Reddy, M. K., Weitzel, S. E. & von Hippel, P. H. Assembly of a functional replication complex without ATP hydrolysis: a direct interaction of bacteriophage T4 gp45 with T4 DNA polymerase. Proc. Natl Acad. Sci. USA 90, 3211-3215 (1993). (Pubitemid 23111335)
15. Reddy, M. K.,Weitzel, S. E., Daube, S. S., Jarvis, T. C. & von Hippel, P. H. Using macromolecular crowding agents to identify weak interactions within DNA replication complexes. Methods Enzymol. 262, 466-476 (1995).
16. Hamdan, S. M. & Richardson, C. C. Motors, switches, and contacts in the replisome. Annu. Rev. Biochem. 78, 205-243 (2009).
17. Bailey, S., Eliason, W. K. & Steitz, T. A. Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 318, 459-463 (2007). (Pubitemid 47614533)
18. Minton, A. P. Excluded volume as a determinant of macromolecular structure and reactivity. Biopolymers 20, 2093-2120 (1981).
19. Levy, Y. & Onuchic, J. N. Water mediation in protein folding and molecular recognition. Annu. Rev. Biophys. Biomol. Struct. 35, 389-415 (2006). (Pubitemid 43877384)
20. Samiotakis, A., Wittung-Stafshede, P. & Cheung, M. S. Folding, stability and shape of proteins in crowded environments: experimental and computational approaches. Int. J. Mol. Sci. 10, 572-588 (2009).
21. Minton, A. P. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J. Biol. Chem. 276, 10577-10580 (2001). (Pubitemid 38089223)
22. Wang, Q., Liang, K. C., Czader, A., Waxham, M. N. & Cheung, M. S. The effect of macromolecular crowding, ionic strength and calcium binding on calmodulin dynamics. PLoS Comput. Biol. 7, e1002114 (2011).
23. van den Berg, B., Wain, R., Dobson, C. M. & Ellis, R. J. Macromolecular crowding perturbs protein refolding kinetics: implications for folding inside the cell. EMBO J. 19, 3870-3875 (2000).
24. Sikorav, J. L. & Church, G. M. Complementary recognition in condensed DNA: accelerated DNA renaturation. J. Mol. Biol. 222, 1085-1108 (1991). (Pubitemid 121003489)
25. Konopka, M. C., Shkel, I. A., Cayley, S., Record, M. T. & Weisshaar, J. C. Crowding and confinement effects on protein diffusion in vivo. J. Bacteriol. 188, 6115-6123 (2006). (Pubitemid 44448553)
26. Huber, H. E., Tabor, S. & Richardson, C. C. Escherichia coli thioredoxin stabilizes complexes of bacteriophage T7 DNA polymerase and primed templates. J. Biol. Chem. 262, 16224-16232 (1987).
27. Akabayov, B. et al. Conformational dynamics of bacteriophage T7 DNA polymerase and its processivity factor, Escherichia coli thioredoxin. Proc. Natl Acad. Sci. USA 107, 15033-15038 (2010).
28. Frick, D. N. & Richardson, C. C. DNA primases. Annu. Rev. Biochem. 70, 39-80 (2001). (Pubitemid 32662205)
29. Kulczyk, A. W. et al. An Interaction between DNA Polymerase and Helicase is Essential for the High Processivity of the Bacteriophage T7 Replisome. J. Biol. Chem. 287, 39050-39060 (2012).
30. Singleton, M. R., Sawaya, M. R., Ellenberger, T. & Wigley, D. B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101, 589-600 (2000).
31. Guo, S., Tabor, S. & Richardson, C. C. The linker region between the helicase and primase domains of the bacteriophage T7 gene 4 protein is critical for hexamer formation. J. Biol. Chem. 274, 30303-30309 (1999).
32. Luna, R. E. et al. The C-terminal domain of eukaryotic initiation factor 5 promotes start codon recognition by its dynamic interplay with eIF1 and eIF2beta. Cell Rep. 1, 689-702 (2012).
33. Svergun, D. I., Barberato, C. & Koch, M. H. J. CRYSOL-a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates. J. Appl. Cryst. 28, 768-773 (1995). (Pubitemid 3014671)
34. Brieba, L. G. et al. Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J. 23, 3452-3461 (2004). (Pubitemid 39265535)
35. Huber, H. E., Russel, M., Model, P. & Richardson, C. C. Interaction of mutant thioredoxins of Escherichia coli with the gene 5 protein of phage T7. The redox capacity of thioredoxin is not required for stimulation of DNA polymerase activity. J. Biol. Chem. 261, 15006-15012 (1986). (Pubitemid 17218065)
36. Lee, S. J., Zhu, B., Hamdan, S. M. & Richardson, C. C. Mechanism of sequence-specific template binding by the DNA primase of bacteriophage T7. Nucleic Acids Res. 38, 4372-4383 (2010).
37. Bertini, I. et al. Solid-state NMR of proteins sedimented by ultracentrifugation. Proc. Natl Acad. Sci. USA 108, 10396-10399 (2011).
38. Harano, Y. & Kinoshita, M. Large gain in translational entropy of water is a major driving force in protein folding. Chem. Phys. Lett. 399, 342-348 (2004). (Pubitemid 40017534)
39. Hamdan, S. M. et al. A unique loop in T7 DNA polymerase mediates the binding of helicase-primase, DNA binding protein, and processivity factor. Proc. Natl Acad. Sci. USA 102, 5096-5101 (2005).
40. Akabayov, B. & Richardson, C. C. Binding of Mn-deoxyribonucleoside triphosphates to the active site of the DNA polymerase of bacteriophage T7. Powder Diffraction 2, 159-163 (2011).
41. Dedmon, M. M., Patel, C. N., Young, G. B. & Pielak, G. J. FlgM gains structure in living cells. Proc. Natl Acad. Sci. USA 99, 12681-12684 (2002).
42. Notarnicola, S. M., Mulcahy, H. L., Lee, J. & Richardson, C. C. The acidic carboxyl terminus of the bacteriophage T7 gene 4 helicase/primase interacts with T7 DNA polymerase. J. Biol. Chem. 272, 18425-18433 (1997). (Pubitemid 27306437)
43. Nakai, H. & Richardson, C. C. Interactions of the DNA polymerase and gene 4 protein of bacteriophage T7. Protein-protein and protein-DNA interactions involved in RNA-primed DNA synthesis. J. Biol. Chem. 261, 15208-15216 (1986).
44. Mendelman, L. V. & Richardson, C. C. Requirements for primer synthesis by bacteriophage T7 63-kDa gene 4 protein. Roles of template sequence and T7 56-kDa gene 4 protein. J. Biol. Chem. 266, 23240-23250 (1991).
45. Allaire, M. & Yang, L. Biomolecular solution X-ray scattering at the National Synchrotron Light Source. J. Synchrotron Radiat. 18, 41-44 (2011).
46. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. & Svergun, D. I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Cryst. 36, 1277-128 (2003).
47. Kuga, S. Pore size distribution analysis of gel substances by size exclusion chromatography. J. Chromatogr. 206, 449-461 (1981).
48. Bereiter-Hahn, J., Anderson, O. R. & Reif, W. E. Cytomechanics: The Mechanical Basis of Cell Form and Structure 3-30 (Springer-Verlag, 1987).
49. Toth, E. A., Li, Y., Sawaya, M. R., Cheng, Y. & Ellenberger, T. The crystal structure of the bifunctional primase-helicase of bacteriophage T7. Mol. Cell 12, 1113-1123 (2003). (Pubitemid 37487922)
50. Kato, M., Ito, T., Wagner, G., Richardson, C. C. & Ellenberger, T. Modular architecture of the bacteriophage T7 primase couples RNA primer synthesis to DNA synthesis. Mol. Cell 11, 1349-1360 (2003). (Pubitemid 36645152)
51. Ilyina, T. V., Gorbalenya, A. E. & Koonin, E. V. Organization and evolution of bacterial and bacteriophage primase-helicase systems. J. Mol. Evol. 34, 351-357 (1992).