Dependence of DNA polymerase replication rate on external forces: A model based on molecular dynamics simulations

Biophysical Journal

Volumn 87, Issue 3, 2004, Pages 1478-1497

  Andricioaei, Ioan ^a,c   Goel, Anita ^a   Herschbach, Dudley ^a   Karplus, Martin ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BASE; NUCLEOTIDE; PRIMER DNA; TAQ DNA POLYMERASE I; TAQ POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CONFORMATIONAL TRANSITION; DNA REPLICATION; DNA STRAND; DNA TEMPLATE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FORCE; MATHEMATICAL ANALYSIS; MODEL; MOLECULAR DYNAMICS; MOTION; NONHUMAN; PARAMETER; REACTION ANALYSIS; SIMULATION; TENSION; THERMUS AQUATICUS;

NEGIBACTERIA; THERMUS; THERMUS AQUATICUS;

EID: 4444318769     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.103.039313     Document Type: Article

References (65)

1. Arndt, J. W., W. Gong, X. Zhong, A. K. Showalter, J. Liu, C. A. Dunlap, Z. Lin, C. Paxson, M.-D. Tsai, and M. K. Chan. (2001). Insight into the catalytic mechanism of DNA polymerase: structures of intermediate complexes. Biochemistry. 40:5368-5375.
2. Beese, L., V. Derbshire, and T. Steitz. 1993. Structure of DNA polymerase I Klenow fragment bound to duplex DNA. Science. 260:352-355.
3. Bell, G. I. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
4. Berg, B. V., W. Wilson, and S. Wilson. 2001. DNA structure and aspartate 276 influence nucleotide binding to human DNA polymerase β. J. Biol. Chem. 276:3408-3416.
5. Brautigam, C., and T. Steitz. 1998. Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr. Opin. Struct. Biol. 8:54-63.
6. Brønsted, N. 1928. Acid and basic catalysis. Chem. Rev. 5:231-338.
7. Brooks III, C. L., and M. Karplus. 1983. Deformable stochastic boundaries in molecular dynamics. J. Chem. Phys. 79:6312-6325.
8. Bryant, F., K. Johnson, and S. Benkovic. 1983. Elementary steps in the DNA polymerase I reaction pathway. Biochemistry. 22:3537-3546.
9. Bueche, F. (1962). Physical Properties of Polymers. Interscience, New York.
10. Carrion-Vazquez, M., A. Oberhauser, S. Fowler, P. Marszalek, S. Broedel, J. Clarke, and J. Fernandez. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA. 96:3694-3699.
11. Cluzel, P., A. Lebrun, C. Heller, R. Lavery, J.-L. Viovy, D. Chatenay, and F. Caron. 1996. DNA: an extensible molecule. Science. 271:792-794.
12. Cocco, S., R. Monasson, and J. Marko. 2001. Force and kinetic barriers to unzipping of the DNA double helix. Proc. Natl. Acad. Sci. USA. 98: 8608-8613.
13. Dahlberg, M., and S. Benkovic. 1991. Kinetic mechanism of DNA-polymerase-I (Klenow fragment): identification of a 2nd conformational change and evaluation of the internal equilibrium-constant. Biochemistry. 30:4835-1843.
14. Dinner, A., G. Blackbum, and M. Karplus. 2001. Uracil-DNA glycosylase acts by substrate autocatalysis. Nature. 413:752-755.
15. Doublié, S., S. Tabor, A. Long, C. Richardson, and T. Ellenberger. 1998. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature. 391:251-258.
16. Eom, S., J. Wang, and T. Steitz. 1996. Structure of Taq polymerase with DNA at the polymerase active site. Nature. 382:278-281.
17. Evans, M., and M. Polanyi. 1938. Inertia and driving force of chemical reactions. Trans. Faraday Soc. 34:11-29.
18. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1572.
19. Franklin, M., J. Wang, and T. Steitz. 2001. Structure of the replicating complex of a pol α family DNA polymerase. Cell. 105:657-667.
20. Goel, A., T. Ellenberger, M. Frank-Kamenetskii, and D. Herschbach. 2002. Unifying themes in DNA replication: reconciling single-molecule kinetic studies with structural data on DNA polymerases. J. Biomol. Struct. Dyn. 19:571-584.
21. Goel, A., M. Frank-Kamenetskii, T. Ellenberger, and D. Herschbach. 2001. Tuning DNA "strings": modulating the rate of DNA replication with mechanical tension. Proc. Natl. Acad. Sci. USA. 98:8485-8489.
22. Grosberg, A., and A. Khokhlov. (1994). Statistical Physics of Macromolecules. American Institute of Physics Press, College Park, MD.
23. Gurrieri, S., S. Smith, and C. Bustamante. 1999. Trapping of megabase-sized DNA molecules during agarose gel electrophoresis. Proc. Natl. Acad. Sci. USA. 96:453-158.
24. Hansen, J. 2002. Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct. 31:361-392.
25. Hatfield, J., and S. Quake. 1998. Dynamic properties of an extended polymer in solution. Phys. Rev. Lett. 82:3548-3551.
26. Hegner, M., S. Smith, and C. Bustamante. 1999. Polymerization and mechanical properties of RecA-DNA filaments. Proc. Natl. Acad. Sci. USA. 96:10109-10114.
27. Hoover, W. G. 1985. Canonical dynamics-equilibrium phase-space distributions. Phys. Rev. A. 31:1695-1697.
28. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.
29. Izrailev, S., S. Stepaniants, M. Balsera, Y. Oono, and K. Schulten. 1997. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72:1568-1581.
30. Joyce, C. 1989. How DNA travels between the separate polymerase and 3′-5′-exonuclease sites of DNA polymerase I (Klenow fragment). J. Biol. Chem. 264:10858-10866.
31. Joyce, C., and T. Steitz. 1994. Function and structure relationships in DNA polymerases. Annu. Rev. Biochem. 63:777-822.
32. Karplus, M., and J. Kushick. 1981. Method for estimating the configurational entropy of macromolecules. Macromolecules. 14:325-332.
33. Kiefer, J., C. Mao, J. Braman, and L. Beese. 1998. Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal. Nature. 391:304-307.
34. Kim, Y., S. Eom, J. Wang, D. Lee, S. Suh, and T. Steitz. (1995). Crystal structures of Thermus aquaticus DNA polymerase. Nature, 376.
35. Konrad, M., and J. Bolonick. 1996. Molecular dynamics simulation of DNA stretching is consistent with the tension observed for extension and strand separation and predicts a novel ladder structure. J. Am. Chem. Soc. 118:10989-10994.
36. Komberg, A., and T. Baker. (1991). DNA Replication. W. H. Freeman, New York.
37. Kunkel, T., and K. Bebenek. 2000. DNA replication fidelity. Annu. Rev. Biochem. 69:497-529.
38. Li, Y., Y. Kong, S. Korolev, and G. Waksman. 1998a. Crystal structures of the Klenow fragment of Thermus aquaticus DNA polymerase I complexed with deoxyribonucleoside triphosphates. Protein Sci. 7: 1116-1123.
39. Li, Y., S. Korolev, and G. Waksman. 1998b. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J. 17:7514-7525.
40. Li, Y., V. Mitaxov, and G. Waksman. 1999. Structure-based design of Taq DNA polymerase with improved properties of dideoxinucleotide incorporation. Proc. Natl. Acad. Sci. USA. 96:9491-9496.
41. Li, Y., and G. Waksman. 2001. Crystal structures of a ddATP-, ddTTP-, ddCTP-, and ddGTP-trapped ternary complex of Klentaq1: insights into nucleotide incorporation and selectivity. Protein Sci. 10:1225-1233.
42. MacKerell, A., Jr., and G. Lee. 1999. Structure, force, and energy of a double-stranded DNA oligonucleotide under tensile loads. Eur. Biophys. J. 28:415-426.
43. Maier, B., D. Bensimon, and V. Croquette. 2000. Replication by a single DNA polymerase of a stretched single-stranded DNA. Proc. Natl. Acad. Sci. USA. 97:12002-12007.
44. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:50-53.
45. Moy, V., E.-L. Florin, and H. Gaub. (1994). Intermolecular forces and energies between ligands and receptors. Science. 266:257-259.
46. Nayal, S. K. M., W. Barnes, E. D. Cera, and G. Waksman. 1995. Crystal structure of the large fragment of Thermus aquaticus DNA polymerase I at 2.5 Å resolution: structural basis for thermostability. Proc. Natl. Acad. Sci. USA. 92:9264-9268.
47. Nosé, S. 1984. A unified formulation of the constant temperature molecular-dynamics methods. J. Chem. Phys. 81:511-519.
48. Ollis, D., P. Brick, R. Hamlin, N. Xuong, and T. Steitz. 1985. Structure of the large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature. 313:762-766.
49. Olmsted, M., C. Anderson, and M. Record, Jr. 1991. Importance of oligoelectrolyte end effects for the thermodynamics of conformational transitions of nucleic acids oligomers: a grand canonical Monte Carlo analysis. Biopolymers. 31:1593-1604.
50. Paci, E., and M. Karplus. 2000. Unfolding proteins by external forces: the importance of topology and energetics. Proc. Natl. Acad. Sci. USA. 97:6521-6526.
51. Patel, P., and L. A. Loeb. 2001. Getting a grip on how DNA polymerases function. Nat. Struct. Biol. 8:656-659.
52. Patel, S., I. Wong, and K. Johnson. 1991. Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry. 30:511-525.
53. Rief, M., H. Clausen-Schaumann, and H. Gaub. 1999. Sequence-dependent mechanics of single DNA molecules. Nat. Struct. Biol. 6:346-349.
54. Roberts, R., and X. Cheng. 1998. Base flipping. Annu. Rev. Biochem. 67:181-198.
55. Rouzina, I., and V. Bloomfield. 2001. Force-induced melting of the DNA double helix. 1. Thermodynamic analysis. Biophys. J. 80:882-893.
56. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
57. Simonson, T., G. Archontis, and M. Karplus. 1997. Continuum treatment of long-range interactions in free energy calculations. Application to protein-ligand binding. J. Phys. Chem. B. 101:8349-8362.
58. Smith, S., Y. Cui, and C. Bustamante. 1996. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science. 271:795-799.
59. Steitz, T. 1998. A mechanism for all polymerases. Nature. 391:231-232.
60. Steitz, T. 1999. DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem. 274:17395-17398.
61. Strick, T., J.-F. Allemand, D. Bensimon, and V. Croquette. 2000. Stress-induced structural transitions in DNA and proteins. Annu. Rev. Biophys. Biomol. Struct. 29:523-543.
62. Turner, R., Jr., N. Grindley, and C. Joyce. 2003. Interaction of DNA polymerase I (Klenow fragment) with the single-stranded template beyond the site of synthesis. Biochemistry. 42: 2373-2385.
63. Wang, M., M. Schnitzer, H. Yin, R. Landick, J. Gelles, and S. Block. 1998. Force and velocity measured for single molecules of RNA polymerase. Science. 282:902-907.
64. Wuite, G., S. Smith, M. Young, D. Keller, and C. Bustamante. 2000. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature. 404:103-106.
65. Yang, L., W. Beard, S. Wilson, S. Broyde, and T. Schlick. 2002. Polymerase β simulations suggest that Arg258 rotation is a slow step rather than large subdomain motions per se. J. Mol. Biol. 317:651-671.