A multiscale dynamic model of DNA supercoil relaxation by topoisomerase IB

Biophysical Journal

Volumn 100, Issue 8, 2011, Pages 2016-2023

  Lillian, Todd D ^a   Taranova, Maryna ^b   Wereszczynski, Jeff ^c   Andricioaei, Ioan ^b   Perkins, N C ^d  

^a Department of Electrical and Computer Engineering   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79959721684     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.03.003     Document Type: Article

References (54)

1. Pruss, G. J., and K. Drlica. 1989. DNA supercoiling and prokaryotic transcription. Cell. 56:521-523. (Pubitemid 19065526)
2. Dorman, C. J. 2006. DNA supercoiling and bacterial gene expression. Sci. Prog. 89:151-166.
3. Drlica, K. 1992. Control of bacterial DNA supercoiling. Mol. Microbiol. 6:425-433.
4. Pommier, Y. 1993. DNA topoisomerase I and II in cancer chemotherapy: update and perspectives. Cancer Chemother. Pharmacol. 32:103-108. (Pubitemid 23131928)
5. Redinbo, M. R., L. Stewart, W. G. Hol. 1998. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science. 279:1504-1513. (Pubitemid 28217069)
6. Been, M. D., R. R. Burgess, and J. J. Champoux. 1984. Nucleotide sequence preference at rat liver and wheat germ type 1 DNA topoisomerase breakage sites in duplex SV40 DNA. Nucleic Acids Res. 12:3097-3114.
7. Champoux, J. J. 2001. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70:369-413. (Pubitemid 32662215)
8. Koster, D. A., V. Croquette, N. H. Dekker. 2005. Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature. 434:671-674. (Pubitemid 40488562)
9. Stewart, L., M. R. Redinbo, J. J. Champoux. 1998. A model for the mechanism of human topoisomerase I. Science. 279:1534-1541. (Pubitemid 28217077)
10. Wereszczynski, J., and I. Andricioaei. 2010. Free energy calculations reveal rotating-ratchet mechanism for DNA supercoil relaxation by topoisomerase IB and its inhibition. Biophys. J. 99:869-878.
11. Smith, S. B., L. Finzi, and C. Bustamante. 1992. Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science. 258:1122-1126.
12. Strick, T. R., J. F. Allemand, V. Croquette. 1996. The elasticity of a single supercoiled DNA molecule. Science. 271:1835-1837. (Pubitemid 26112307)
13. Harada, Y., O. Ohara, K. Kinosita, Jr. 2001. Direct observation of DNA rotation during transcription by Escherichia coli RNA polymerase. Nature. 409:113-115. (Pubitemid 32098636)
14. Bryant, Z., M. D. Stone, C. Bustamante. 2003. Structural transitions and elasticity from torque measurements on DNA. Nature. 424:338-341. (Pubitemid 36899378)
15. Crut, A., D. A. Koster, N. H. Dekker. 2007. Fast dynamics of supercoiled DNA revealed by single-molecule experiments. Proc. Natl. Acad. Sci. USA. 104:11957-11962. (Pubitemid 47185612)
16. Koster, D. A., K. Palle, N. H. Dekker. 2007. Antitumor drugs impede DNA uncoiling by topoisomerase I. Nature. 448:213-217. (Pubitemid 47067371)
17. Koster, D. A., F. Czerwinski, N. H. Dekker. 2008. Single-molecule observations of topotecan-mediated TopIB activity at a unique DNA sequence. Nucleic Acids Res. 36:2301-2310. (Pubitemid 351567003)
18. Lillian, T. D., and N. C. Perkins. 2011. Electrostatics and self-contact in an elastic rod approximation for DNA. J. Comput. Nonlinear Dyn. 6, 011008-6.
19. Clauvelin, N., B. Audoly, and S. Neukirch. 2009. Elasticity and electrostatics of plectonemic DNA. Biophys. J. 96:3716-3723.
20. Purohit, P. K. 2008. Plectoneme formation in twisted fluctuating rods. J. Mech. Phys. Solids. 56:1715-1729.
21. Marko, J. F. 2007. Torque and dynamics of linking number relaxation in stretched supercoiled DNA. Phys. Rev. E. 76:021926.
22. Vologodskii, A. V., and J. F. Marko. 1997. Extension of torsionally stressed DNA by external force. Biophys. J. 73:123-132. (Pubitemid 27274110)
23. Yang, Z., Z. Haijun, and O.-Y. Zhong-Can. 2000. Monte Carlo implementation of supercoiled double-stranded DNA. Biophys. J. 78:1979-1987. (Pubitemid 30183592)
24. Chirico, G., and J. Langowski. 1994. Kinetics of DNA supercoiling studied by Brownian dynamics simulation. Biopolymers. 34:415-433.
25. Huang, J., T. Schlick, and A. Vologodskii. 2001. Dynamics of site juxtaposition in supercoiled DNA. Proc. Natl. Acad. Sci. USA. 98:968-973. (Pubitemid 32121171)
26. Jian, H., T. Schlick, and A. Vologodskii. 1998. Internal motion of supercoiled DNA: Brownian dynamics simulations of site juxtaposition. J. Mol. Biol. 284:287-296. (Pubitemid 28542454)
27. Mielke, S. P., W. H. Fink, C. J. Benham. 2004. Transcription-driven twin supercoiling of a DNA loop: a Brownian dynamics study. J. Chem. Phys. 121:8104-8112.
28. Wada, H., and R. R. Netz. 2009. Plectoneme creation reduces the rotational friction of a polymer. Europhys. Lett. 87:38001.
29. Villa, E., A. Balaeff, K. Schulten. 2004. Multiscale method for simulating protein-DNA complexes. Multiscale Model Simul. 2:527-553.
30. Villa, E., A. Balaeff, and K. Schulten. 2005. Structural dynamics of the lac repressor-DNA complex revealed by a multiscale simulation. Proc. Natl. Acad. Sci. USA. 102:6783-6788. (Pubitemid 40675393)
31. Goyal, S., T. Lillian, N. C. Perkins. 2007. Intrinsic curvature of DNA influences LacR-mediated looping. Biophys. J. 93:4342-4359. (Pubitemid 350294481)
32. Lillian, T. D., N. C. Perkins, and S. Goyal. 2008. Computational elastic rod model applied to DNA looping. Proc. ASME IDETC/CIE 2007. 5:1449-1456.
33. Goyal, S., N. C. Perkins, and C. L. Lee. 2005. Nonlinear dynamics and loop formation in Kirchhoff rods with implications to the mechanics of DNA and cables. J. Comput. Phys. 209:371-389. (Pubitemid 40792371)
34. Strick, T., J. F. Allemand, D. Bensimon. 2000. Twisting and stretching single DNA molecules. Prog. Biophys. Mol. Biol. 74:115-140. (Pubitemid 32011691)
35. Bustamante, C., J. F. Marko, S. Smith. 1994. Entropic elasticity of lambda-phage DNA. Science. 265:1599-1600.
36. Bustamante, C., Z. Bryant, and S. B. Smith. 2003. Ten years of tension: single-molecule DNA mechanics. Nature. 421:423-427. (Pubitemid 36157948)
37. Beveridge, D. L., G. Barreiro, M. A. Young. 2004. Molecular dynamics simulations of the 136 unique tetranucleotide sequences of DNA oligonucleotides. I. Research design and results on d (CpG) steps. Biophys. J. 87:3799-3813. (Pubitemid 39602887)
38. Manning, R. S., J. H. Maddocks, and J. D. Kahn. 1996. A continuum rod model of sequence-dependent DNA structure. J. Chem. Phys. 105:5626-5646. (Pubitemid 126748226)
39. Swigon, D., B. D. Coleman, and W. K. Olson. 2006. Modeling the Lac repressor-operator assembly: the influence of DNA looping on Lac repressor conformation. Proc. Natl. Acad. Sci. USA. 103:9879-9884. (Pubitemid 43993591)
40. Munteanu, M. G., K. Vlahovicek, S. Pongor. 1998. Rod models of DNA: sequence-dependent anisotropic elastic modeling of local bending phenomena. Trends Biochem. Sci. 23:341-347. (Pubitemid 28461866)
41. Schlick, T. 1995. Modeling superhelical DNA: recent analytical and dynamic approaches. Curr. Opin. Struct. Biol. 5:245-262.
42. Balaeff, A., L. Mahadevan, and K. Schulten. 2006. Modeling DNA loops using the theory of elasticity. Phys. Rev. Es. 73:031919.
43. Baumann, C. G., S. B. Smith, C. Bustamante. 1997. Ionic effects on the elasticity of single DNA molecules. Proc. Natl. Acad. Sci. USA. 94:6185-6190. (Pubitemid 27270659)
44. Hagerman, P. J. 1988. Flexibility of DNA. Annu. Rev. Biophys. Biophys. Chem. 17:265-286.
45. Lillian, T. D., S. Goyal, N. C. Perkins. 2008. Computational analysis of looping of a large family of highly bent DNA by LacI. Biophys. J. 95:5832-5842.
46. Goyal, S., and N. C. Perkins. 2008. Looping mechanics of rods and DNA with non-homogeneous and discontinuous stiffness. Int. J. Nonlinear Mech. 43:1121-1129.
47. Vologodskii, A., and N. Cozzarelli. 1995. Modeling of long-range electrostatic interactions in DNA. Biopolymers. 35:289-296.
48. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.
49. Zhu, Q., J. Zeng, D. K. P. Yue. 2006. Direct numerical simulation of single-molecule DNA by cable dynamics. J. Microelectromech. Syst. 15:1078-1087. (Pubitemid 44566925)
50. Chung, J., and G. M. Hulbert. 1993. A time integration algorithm for structural dynamics with improved numerical dissipation: the generalized-a method. J. Appl. Mech. 60:371-375. (Pubitemid 23679960)
51. Goyal, S. 2006. A dynamic rod model to simulate mechanics of cables and DNA. PhD thesis, University of Michigan, Ann Arbor, MI.
52. Goyal, S., N. C. Perkins, and C. L. Lee. 2008. Non-linear dynamic intertwining of rods with self-contact. Int. J. Non-linear Mech. 43:65-73.
53. Rossetto, V., and A. C. Maggs. 2003. Writhing geometry of open DNA. J. Chem. Phys. 118:9864-9874.
54. Wereszczynski, J. M. 2008. Simulations of nucleic acids under stress, in solution, and complexed to proteins. PhD thesis, University of Michigan, Ann Arbor, MI.