Structure, dynamics, and branch migration of a DNA Holliday junction: A single-molecule fluorescence and modeling study

Biophysical Journal

Volumn 95, Issue 9, 2008, Pages 4372-4383

  Karymov, Mikhail A ^a   Chinnaraj, Mathivanan ^b   Bogdanov, Aleksey ^a,c   Srinivasan, Annankoil R ^d   Zheng, Guohui ^d   Olson, Wilma K ^d   Lyubchenko, Yuri L ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRUCIFORM DNA;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; DNA, CRUCIFORM; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MODELS, MOLECULAR;

EID: 58149160374     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.135103     Document Type: Article

References (59)

1. Karymov, M., D. Daniel, O. F. Sankey, and Y. L. Lyubchenko. 2005. Holliday junction dynamics and branch migration: single-molecule analysis. Proc. Natl. Acad. Sci. USA. 102:8186-8191.
2. Holliday, R. 1964. A mechanism for gene conversion in fungi. Genet. Res. 5:282-304.
3. Leach, D. R. F. 1996. Genetic Recombination. Blackwell Science, Oxford, UK; Cambridge, MA.
4. McGlynn, P., and R. G. Lloyd. 2001. Action of RuvAB at replication fork structures. J. Biol. Chem. 276:41938-41944.
5. Postow, L., C. Ullsperger, R. W. Keller, C. Bustamante, A. V. Vologodskii, and N. R. Cozzarelli. 2000. Positive torsional strain causes the formation of a four-way junction at replication forks. J. Biol. Chem. 276:2790-2796.
6. Cromie, G. A., J. C. Connelly, and D. R. Leach. 2001. Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. Mol. Cell. 8:1163-1174.
7. Lilley, D. M. 2000. Structures of helical junctions in nucleic acids. Q. Rev. Biophys. 33:109-159.
8. Hansma, H. G., M. Bezanilla, F. Zenhausern, M. Adrian, and R. L. Sinsheimer. 1993. Atomic force microscopy of DNA in aqueous solutions. Nucleic Acids Res. 21:505-512.
9. Guthold, M., M. Bezanilla, D. A. Erie, B. Jenkins, H. G. Hansma, and C. Bustamante. 1994. Following the assembly of RNA polymerase-DNA complexes in aqueous solutions with the scanning force microscope. Proc. Natl. Acad. Sci. USA. 91:12927-12931.
10. Bustamante, C., M. Guthold, X. Zhu, and G. Yang. 1999. Facilitated target location on DNA by individual Escherichia coli RNA polymerase molecules observed with the scanning force microscope operating in liquid. J. Biol. Chem. 274:16665-16668.
11. Kasas, S., N. H. Thomson, B. L. Smith, H. G. Hansma, X. Zhu, M. Guthold, C. Bustamante, E. T. Kool, M. Kashlev, and P. K. Hansma. 1997. Escherichia coli RNA polymerase activity observed using atomic force microscopy. Biochemistry. 36:461-468.
12. Lyubchenko, Y. L., and L. S. Shlyakhtenko. 1997. Visualization of supercoiled DNA with atomic force microscopy in situ. Proc. Natl. Acad. Sci. USA. 94:496-501.
13. Shlyakhtenko, L. S., V. N. Potaman, R. R. Sinden, and Y. L. Lyubchenko. 1998. Structure and dynamics of supercoil-stabilized DNA cruciforms. J. Mol. Biol. 280:61-72.
14. Shlyakhtenko, L. S., P. Hsieh, M. Grigoriev, V. N. Potaman, R. R. Sinden, and Y. L. Lyubchenko. 2000. A cruciform structural transition provides a molecular switch for chromosome structure and dynamics. J. Mol. Biol. 296:1169-1173.
15. Lyubchenko, Y. L., L. S. Shlyakhtenko, V. N. Potaman, and R. R. Sinden. 2002. Global and local DNA structure and dynamics. Single molecule studies with AFM. Microsc. Microanal. 8:170-171.
16. Ha, T., T. Enderle, D. F. Ogletree, D. S. Chemla, P. R. Selvin, and S. Weiss. 1996. Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA. 93:6264-6268.
17. Weiss, S. 1999. Fluorescence spectroscopy of single biomolecules. Science. 283:1676-1683.
18. Weiss, S. 2000. Measuring conformational dynamics of biomolecules by single molecule fluorescence spectroscopy. Nat. Struct. Biol. 7:724-729.
19. Deniz, A. A., M. Dahan, J. R. Grunwell, T. Ha, A. E. Faulhaber, D. S. Chemla, S. Weiss, and P. G. Schultz. 1999. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: observation of Forster distance dependence and subpopulations. Proc. Natl. Acad. Sci. USA. 96:3670-3675.
20. Deniz, A. A., T. A. Laurence, G. S. Beligere, M. Dahan, A. B. Martin, D. S. Chemla, P. E. Dawson, P. G. Schultz, and S. Weiss. 2000. Single-molecule protein folding: diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc. Natl. Acad. Sci. USA. 97:5179-5184.
21. Ha, T., A. Y. Ting, J. Liang, W. B. Caldwell, A. A. Deniz, D. S. Chemla, P. G. Schultz, and S. Weiss. 1999. Single-molecule fluorescence spectroscopy of enzyme conformational dynamics and cleavage mechanism. Proc. Natl. Acad. Sci. USA. 96:893-898.
22. Tokunaga, M., K. Kitamura, K. Saito, A. H. Iwane, and T. Yanagida. 1997. Single molecule imaging of fluorophores and enzymatic reactions achieved by objective-type total internal reflection fluorescence microscopy. Biochem. Biophys. Res. Commun. 235:47-53.
23. McKinney, S. A., A. C. Declais, D. M. Lilley, and T. Ha. 2003. Structural dynamics of individual Holliday junctions. Nat. Struct. Biol. 10:93-97.
24. Joo, C., S. A. McKinney, D. M. Lilley, and T. Ha. 2004. Exploring rare conformational species and ionic effects in DNA Holliday junctions using single-molecule spectroscopy. J. Mol. Biol. 341:739-751.
25. Hohng, S., R. Zhou, M. K. Nahas, J. Yu, K. Schulten, D. M. Lilley, and T. Ha. 2007. Fluorescence-force spectroscopy maps two-dimensional reaction landscape of the Holliday junction. Science. 318:279-283.
26. Lushnikov, A. Y., A. Bogdanov, and Y. L. Lyubchenko. 2003. DNA recombination: Holliday junctions dynamics and branch migration. J. Biol. Chem. 278:43130-43134.
27. Liu, J., A. C. Declais, S. A. McKinney, T. Ha, D. G. Norman, and D. M. Lilley. 2005. Stereospecific effects determine the structure of a four-way DNA junction. Chem. Biol. 12:217-228.
28. Biswas, I., A. Yamamoto, and P. Hsieh. 1998. Branch migration through DNA sequence heterology. J. Mol. Biol. 279:795-806.
29. Panyutin, I. G., I. Biswas, and P. Hsieh. 1995. A pivotal role for the structure of the Holliday junction in DNA branch migration. EMBO J. 14:1819-1826.
30. Panyutin, I. G., and P. Hsieh. 1994. The kinetics of spontaneous DNA branch migration. Proc. Natl. Acad. Sci. USA. 91:2021-2025.
31. Bruist, M. F., and E. Myers. 2003. Discrete and continuous mathematical models of DNA branch migration. J. Theor. Biol. 220:139-156.
32. Karymov, M. A., A. Bogdanov, and Y. Lyubchenko. 2008. Single molecule fluorescence analysis of branch migration of Holliday junctions: effect of DNA sequence. Biophys. J. 95:1239-1247.
33. Harada, Y., K. Sakurada, T. Aoki, D. D. Thomas, and T. Yanagida. 1990. Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. J. Mol. Biol. 216:49-68.
34. Ha, T. 2001. Single-molecule fluorescence resonance energy transfer. Methods. 25:78-86.
35. Ha, T., I. Rasnik, W. Cheng, H. P. Babcock, G. H. Gauss, T. M. Lohman, and S. Chu. 2002. Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature. 419:638-641.
36. Murphy, M. C., I. Rasnik, W. Cheng, T. M. Lohman, and T. Ha. 2004. Probing single-stranded DNA conformational flexibility using fluorescence spectroscopy. Biophys. J. 86:2530-2537.
37. Mukhopadhyay, J., A. N. Kapanidis, V. Mekler, E. Kortkhonjia, Y. W. Ebright, and R. H. Ebright. 2001. Translocation of sigma(70) with RNA polymerase during transcription: fluorescence resonance energy transfer assay for movement relative to DNA. Cell. 106:453-463.
38. Clegg, R. M. 1992. Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211:353-388.
39. Srinivasan, A. R., and W. K. Olson. 1994. Computer models of DNA four-way junctions. Biochemistry. 33:9389-9404.
40. Ortiz-Lombardia, M., A. Gonzalez, R. Eritja, J. Aymami, F. Azorin, and M. Coll. 1999. Crystal structure of a DNA Holliday junction. Nat. Struct. Biol. 6:913-917.
41. Eichman, B. F., J. M. Vargason, B. H. Mooers, and P. S. Ho. 2000. The Holliday junction in an inverted repeat DNA sequence: sequence effects on the structure of four-way junctions. Proc. Natl. Acad. Sci. USA. 97:3971-3976.
42. Ho, P. S., and B. F. Eichman. 2001. The crystal structures of DNA Holliday junctions. Curr. Opin. Struct. Biol. 11:302-308.
43. Thorpe, J. H., S. C. Teixeira, B. C. Gale, and C. J. Cardin. 2002. Structural characterization of a new crystal form of the four-way Holliday junction formed by the DNA sequence d(CCGGTACCGG)2: sequence versus lattice? Acta Crystallogr. D Biol. Crystallogr. 58: 567-569.
44. Hays, F. A., A. Teegarden, Z. J. Jones, M. Harms, D. Raup, J. Watson, E. Cavaliere, and P. S. Ho. 2005. How sequence defines structure: a crystallographic map of DNA structure and conformation. Proc. Natl. Acad. Sci. USA. 102:7157-7162.
45. Hadden, J. M., A. C. Declais, S. B. Carr, D. M. Lilley, and S. E. Phillips. 2007. The structural basis of Holliday junction resolution by T7 endonuclease I. Nature. 449:621-624.
46. Lu, X. J., and W. K. Olson. 2003. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 31:5108-5121.
47. Srinivasan, A. R., and W. K. Olson. 1987. Nucleic acid model building: the multiple backbone solutions associated with a given base morphology. J. Biomol. Struct. Dyn. 4:895-938.
48. Olson, W. K., M. Bansal, S. K. Burley, R. E. Dickerson, M. Gerstein, S. C. Harvey, U. Heinemann, X. J. Lu, S. Neidle, Z. Shakked, H. Sklenar, M. Suzuki, C. S. Tung, E. Westhof, C. Wolberger, and H. M. Berman. 2001. A standard reference frame for the description of nucleic acid base-pair geometry. J. Mol. Biol. 313:229-237.
49. Ha, T., X. Zhuang, H. D. Kim, J. W. Orr, J. R. Williamson, and S. Chu. 1999. Ligand-induced conformational changes observed in single RNA molecules. Proc. Natl. Acad. Sci. USA. 96:9077-9082.
50. Miick, S. M., R. S. Fee, D. P. Millar, and W. J. Chazin. 1997. Crossover isomer bias is the primary sequence-dependent property of immobilized Holliday junctions. Proc. Natl. Acad. Sci. USA. 94:9080-9084.
51. Hargreaves, D., D. W. Rice, S. E. Sedelnikova, P. J. Artymiuk, R. G. Lloyd, and J. B. Rafferty. 1998. Crystal structure of E. coli RuvA with bound DNA Holliday junction at 6 A resolution. Nat. Struct. Biol. 5:441-446.
52. Ariyoshi, M., T. Nishino, H. Iwasaki, H. Shinagawa, and K. Morikawa. 2000. Crystal structure of the Holliday junction DNA in complex with a single RuvA tetramer. Proc. Natl. Acad. Sci. USA. 97:8257-8262.
53. Gopaul, D. N., F. Guo, and G. D. Van Duyne. 1998. Structure of the Holliday junction intermediate in Cre-loxP site-specific recombination. EMBO J. 17:4175-4187.
54. Chen, Y., U. Narendra, L. E. Iype, M. M. Cox, and P. A. Rice. 2000. Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Mol. Cell. 6:885-897.
55. Martin, S. S., E. Pulido, V. C. Chu, T. S. Lechner, and E. P. Baldwin. 2002. The order of strand exchanges in Cre-LoxP recombination and its basis suggested by the crystal structure of a Cre-LoxP Holliday junction complex. J. Mol. Biol. 319:107-127.
56. Biertumpfel, C., W. Yang, and D. Suck. 2007. Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature. 449:616-620.
57. Olson, W. K., A. A. Gorin, X. J. Lu, L. M. Hock, and V. B. Zhurkin. 1998. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc. Natl. Acad. Sci. USA. 95:11163-11168.
58. Wang, L., B. E. Hingerty, A. R. Srinivasan, W. K. Olson, and S. Broyde. 2002. Accurate representation of B-DNA double helical structure with implicit solvent and counterions. Biophys. J. 83:382-406.
59. Yu, J., T. Ha, and K. Schulten. 2004. Conformational model of the Holliday junction transition deduced from molecular dynamics simulations. Nucleic Acids Res. 32:6683-6695.