Single-molecule views of protein movement on single-stranded DNA

Annual Review of Biophysics

Volumn 41, Issue 1, 2012, Pages 295-319

  Ha, Taekjip ^a,b   Kozlov, Alexander G ^c   Lohman, Timothy M ^c  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FRET; Helicases; Optical tweezers; Rad51; RecA; SSB

Indexed keywords

ADENOSINE TRIPHOSPHATE; HELICASE; RAD51 PROTEIN; RECA PROTEIN; SINGLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN;

ESCHERICHIA COLI; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; DNA HELICASES; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HUMANS; RAD51 RECOMBINASE; REC A RECOMBINASES; RECOMBINASES;

EID: 84861374075     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-042910-155351     Document Type: Review

References (148)

1. Adzuma K. 1998. No sliding during homology search by RecA protein. J. Biol. Chem. 273:31565-73
2. Ali JA, Lohman TM. 1997. Kinetic measurement of the step size of DNA unwinding by Escherichia coli Uvrd helicase. Science 275:377-80
3. Anand SP, Zheng H, Bianco PR, Leuba SH, Khan SA. 2007. DNA helicase activity ofPcrA is not required for the displacement of RecA protein from DNA or inhibition of RecA-mediated strand exchange. J. Bacteriol. 189:4502-9
4. Antony E, Tomko EJ, Xiao Q, Krejci L, Lohman TM, Ellenberger T. 2009. Srs2 disassembles Rad51 filaments bya protein-protein interaction triggering ATP turnover and dissociationofRad51 from DNA. Mol. Cell 35:105-15
5. Arata H, Dupont A, Mine-Hattab J, Disseau L, Renodon-Corniere A, et al. 2009. Direct observation of twisting steps during Rad51 polymerization on DNA. Proc. Natl. Acad. Sci. USA 106:19239-44
6. Arenson TA, Tsodikov OV, Cox MM. 1999. Quantitative analysis of the kinetics of end-dependent disassembly of RecA filaments from ssDNA. J. Mol. Biol. 288:391-401
7. Ashkin A, Dziedzic JM, Bjorkholm JE, Chu S. 1986. Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11:288-90
8. Bell CE. 2005. Structure and mechanism of Escherichia coli RecA ATPase. Mol. Microbiol. 58:358-66
9. Betterton MD, Julicher F. 2003. A motor that makes its own track: helicase unwinding of DNA. Phys. Rev. Lett. 91:258103
10. Bianco PR, Brewer LR, Corzett M, Balhhorn R, Yeh Y, et al. 2001. Processive translocation and DNA unwinding by individual RecBCD enzyme molecules. Nature 409:374-78
11. Bochkarev A, Bochkareva E. 2004. From RPA to BRCA2: lessons from single-stranded DNA binding by the OB-fold. Curr. Opin. Struct. Biol. 14:36-42
12. Bonnet G, Krichevsky O, Libchaber A. 1998. Kinetics of conformational fluctuations in DNA hairpin-loops. Proc. Natl. Acad. Sci. USA 95:8602-6
13. Bujalowski W, Lohman TM. 1986. Escherichia coli single-strand binding protein forms multiple, distinct complexes with single-stranded DNA. Biochemistry 25:7799-802
14. Bujalowski W, Overman LB, Lohman TM. 1988. Binding mode transitions of Escherichia coli single strand binding protein-single-stranded DNA complexes. Cation, anion, pH, and binding density effects. J. Biol. Chem. 263:4629-40
15. Chan KW, Lee YJ, Wang CH, Huang H, Sun YJ. 2009. Single-stranded DNA-binding protein complex from Helicobacter pylori suggests an ssDNA-binding surface. J. Mol. Biol. 388:508-19
16. Chase JW, Williams KR. 1986. Single-stranded DNA binding proteins required for DNA replication. Annu. Rev. Biochem. 55:103-36
17. Chen WS, Chen WH, Chen Z, Gooding AA, Lin KJ, Kiang CH. 2010. Direct observation of multiple pathways of single-stranded DNA stretching. Phys. Rev. Lett. 105:218104
18. Chen Z, Yang H, Pavletich NP. 2008. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453:489-84
19. Cheng W, Dumont S, Tinoco I Jr, Bustamante C. 2007. NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork. Proc. Natl. Acad. Sci. USA 104:13954-59
20. Chrysogelos S, Griffith J. 1982. Escherichia coli single-strand binding protein organizes single-stranded DNA in nucleosome-like units. Proc. Natl. Acad. Sci. USA 79:5803-7
21. Chu JF, Chang TC, Li HW. 2010. Single-molecule TPM studies on the conversion of human telomeric DNA. Biophys. J. 98:1608-16
22. Cisse I, Okumus B, Joo C, Ha T. 2007. Fueling protein DNA interactions inside porous nanocontainers. Proc. Natl. Acad. Sci. USA 104:12646-50
23. Conover AJ, Danilowicz C, Gunaratne R, Coljee VW, Kleckner N, Prentiss M. 2011. Changes in the tension in dsDNA alter the conformation of RecA bound to dsDNA-RecA filaments. Nucleic Acids Res. 39:8833-43
24. De Vlaminck I, Vidic I, van Loenhout MT, Kanaar R, Lebbink JH, Dekker C. 2010. Torsional regulation of hRPA-induced unwinding of double-stranded DNA. Nucleic Acids Res. 38:4133-42
25. Dessinges MN, Lionnet T, Xi XG, Bensimon D, Croquette V. 2004. Single-molecule assay reveals strand switching and enhanced processivity of UvrD. Proc. Natl. Acad. Sci. USA 101:6439-44
26. Dessinges MN, Maier B, Zhang Y, Peliti M, Bensimon D, Croquette V. 2002. Stretching single stranded DNA, a model polyelectrolyte. Phys. Rev. Lett. 89:248102
27. Dillingham MS, Wigley DB, Webb MR. 2000. Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed. Biochemistry 39:205-12
28. Dohoney KM, Gelles J. 2001. Chi-sequence recognition and DNA translocation by single RecBCD helicase/nuclease molecules. Nature 409:370-74
29. Doose S, Barsch H, Sauer M. 2007. Polymer properties of polythymine as revealed by translational diffusion. Biophys. J. 93:1224-34
30. Fields AP, Cohen AE. 2011. Electrokinetic trapping at the one nanometer limit. Proc. Natl. Acad. Sci. USA 108:8937-42
31. Fili N, Mashanov GI, Toseland CP, Batters C, Wallace MI, et al. 2010. Visualizing helicases unwinding DNA at the single molecule level. Nucleic Acids Res. 38:4448-57
32. Finkelstein IJ, Visnapuu ML, Greene EC. 2010. Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468:983-87
33. Finzi L, Gelles J. 1995. Measurement of lactose repressor-mediated loop formation and breakdown in single DNA molecules. Science 267:378-80
34. Frontali C, Dore E, Ferrauto A, Gratton E, Bettini A, et al. 1979. An absolute method for the determination of the persistence length of native DNA from electron micrographs. Biopolymers 18:1353-73
35. Fulconis R, Mine J, Bancaud A, Dutreix M, Viovy JL. 2006. Mechanism of RecA-mediated homologous recombination revisited by single molecule nanomanipulation. EMBO J. 25:4293-304
36. Galletto R, Amitani I, Baskin RJ, Kowalczykowski SC. 2006. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443:875-78
37. Galletto R, Jezewska MJ, Bujalowski W. 2004. Unzipping mechanism of the double-stranded DNA unwinding by a hexameric helicase: the effect of the 3 arm and the stability of the dsDNA on the unwinding activity of the Escherichia coli DnaB helicase. J. Mol. Biol. 343:101-14
38. Graham BW, Schauer GD, Leuba SH, Trakselis MA. 2011. Steric exclusion and wrapping of the excluded DNA strand occurs along discrete external binding paths during MCM helicase unwinding. Nucleic Acids Res. 39:6585-95
39. Grange W, Duckely M, Husale S, Jacob S, Engel A, Hegner M. 2008. VirE2: a unique ssDNA-compacting molecular machine. PLoS Biol. 6:e44
40. Greenleaf WJ, Woodside MT, Block SM. 2007. High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct. 36:171-90
41. Griffith JD, Harris LD, Register J 3rd. 1984. Visualization of SSB-ssDNA complexes active in the assembly of stable RecA-DNA filaments. Cold Spring Harb. Symp. Quant. Biol. 49:553-59
42. Grimme JM, Honda M, Wright R, Okuno Y, Rothenberg E, et al. 2010. Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52-ssDNA complexes. Nucleic Acids Res. 38:2917-30
43. Gyimesi M, Sarlos K, Kovacs M. 2010. Processive translocation mechanism of the human Bloom's syndrome helicase along single-stranded DNA. Nucleic Acids Res. 38:4404-14
44. Ha T, Enderle T, Ogletree DF, Chemla DS, Selvin PR, Weiss S. 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 93:6264-68
45. Ha T, Rasnik I, Cheng W, Babcock HP, Gauss G, et al. 2002. Initiation and reinitiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419:638-41
46. Hatch K, Danilowicz C, Coljee V, Prentiss M. 2007. Direct measurements of the stabilization of single-stranded DNA under tension by single-stranded binding proteins. Phys. Rev. E Stat. Nonlin. Soft. Matter Phys. 76:021916
47. Hatch K, Danilowicz C, Coljee V, Prentiss M. 2008. Measurement of the salt-dependent stabilization of partially open DNA by Escherichia coli SSB protein. Nucleic Acids Res. 36:294-99
48. Hegner M, Smith SB, Bustamante C. 1999. Polymerization and mechanical properties of single RecA-DNA filaments. Proc. Natl. Acad. Sci. USA 96:10109-14
49. Heyer WD. 2007. Biochemistry of eukaryotic homologous recombination. Top. Curr. Genet. 17:95-133
50. Hilario J, Amitani I, Baskin RJ, Kowalczykowski SC. 2009. Direct imaging of human Rad51 nucleoprotein dynamics on individual DNA molecules. Proc. Natl. Acad. Sci. USA 106:361-68
51. Hollis T, Stattel JM, Walther DS, Richardson CC, Ellenberger T. 2001. Structure of the gene 2.5 protein, a single-stranded DNA binding protein encoded by bacteriophage T7. Proc. Natl. Acad. Sci. USA 98:9557-62
52. Honda M, Okuno Y, Yoo J, Ha T, Spies M. 2011. Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding. EMBOJ. 30:3368-82
53. Honda M, Park J, Pugh RA, Ha T, Spies M. 2009. Single-molecule analysis reveals differential effect of ssDNA-binding proteins on DNA translocation by XPD helicase. Mol. Cell 35:694-703
54. Hwang H, Kim H, Myong S. 2011. Protein induced fluorescence enhancement as a single molecule assay with short distance sensitivity. Proc. Natl. Acad. Sci. USA 108:7414-18
55. Iftode C, Daniely Y, Borowiec JA 1999. Replication protein A (RPA): the eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 34:141-80
56. Jankowsky E. 2011. RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 36:19-29
57. Jia H, Korolev S, Niedziela-Majka A, Maluf NK, Gauss GH, et al. 2011. Rotations of the 2B sub-domain of E. coli UvrD helicase/translocase coupled to nucleotide and DNA binding. J. Mol. Biol. 411:633-48
58. Johnson DS, Bai L, Smith BY, Patel SS, Wang MD. 2007. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129:1299-309
59. Joo C, Balci H, Ishitsuka Y, Buranachai C, Ha T. 2008. Advances in single-molecule fluorescence methods for molecular biology. Annu. Rev. Biochem. 77:51-76
60. Joo C, McKinney SA, Nakamura M, Rasnik I, Myong S, Ha T. 2006. Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126:515-27
61. Karpel RL. 1990. T4 bacteriophage gene 32 protein. In The Biology of Non-Specific DNA-Protein Interactions, ed. A Revzin, pp. 103-30. Boca Raton, FL: CRC Press
62. Kasianowicz JJ, Brandin E, Branton D, Deamer DW. 1996. Characterization of individual polynu-cleotide molecules using a membrane channel. Proc. Natl. Acad. Sci. USA 93:13770-73
63. Kim S, Streets AM, Lin RR, Quake SR, Weiss S, Majumdar DS. 2011. High-throughput single-molecule optofluidic analysis. Nat. Methods 8:242-45
64. Kowalczykowski SC. 2000. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25:156-65
65. Kowalczykowski SC, Krupp RA. 1987. Effects of Escherichia coli SSB protein on the single-stranded DNA-dependent ATPase activity of Escherichia coli RecA protein. Evidence that SSB protein facilitates the binding of RecA protein to regions of secondary structure within single-stranded DNA. J. Mol. Biol. 193:97-113
66. Kozlov AG, Lohman TM. 2002. Kinetic mechanism of direct transfer of Escherichia coli SSB tetramers between single-stranded DNA molecules. Biochemistry 41:11611-27
67. Kozlov AG, Lohman TM. 2002. Stopped-flow studies of the kinetics of single-stranded DNA binding and wrapping around the Escherichia coli SSB tetramer. Biochemistry 41:6032-44
68. Kumaran S, Kozlov AG, Lohman TM. 2006. Saccharomyces cerevisiae replication protein A binds to single-stranded DNA in multiple salt-dependent modes. Biochemistry 45:11958-73
69. Kuznetsov SV, Kozlov AG, Lohman TM, Ansari A. 2006. Microsecond dynamics of protein-DNA interactions: direct observation of the wrapping/unwrapping kinetics of single-stranded DNA around the E. coli SSB tetramer. J. Mol. Biol. 359:55-65
70. Lee G, Yoo J, Leslie BJ, Ha T. 2011. Single-molecule analysis reveals three phases of DNA degradation by an exonuclease. Nat. Chem. Biol. 7:367-74
71. Lee J, Lee S, Ragunathan K, Joo C, Ha T, Hohng S. 2010. Single-molecule four-color FRET. Angew. Chem. Int. Ed. Engl. 49:9922-25
72. Lee JB, Hite RK, Hamdan SM, Xie XS, Richardson CC, van Oijen AM. 2006. DNA primase acts as a molecular brake in DNA replication. Nature 439:621-24
73. Lee JY, Okumus B, Kim DS, Ha T. 2005. Extreme conformational diversity in human telomeric DNA. Proc. Natl. Acad. Sci. USA 102:18938-43
74. Lee JY, Yang W. 2006. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127:1349-60
75. Leger JF, Robert J, Bourdieu L, Chatenay D, Marko JF. 1998. RecA binding to a single double-stranded DNA molecule: a possible role of DNA conformational fluctuations. Proc. Natl. Acad. Sci. USA 95:12295-99
76. Lin J, Kolomeisky A, Meller A. 2010. Helix-coil kinetics of individual polyadenylic acid molecules in a protein channel. Phys. Rev. Lett. 104:158101
77. Lionnet T, Spiering MM, Benkovic SJ, Bensimon D, Croquette V. 2007. Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. Proc. Natl. Acad. Sci. USA 104:19790-95
78. Liphardt J, Onoa B, Smith SB, Tinoco I, Bustamante C. 2001. Reversible unfolding of single RNA molecules by mechanical force. Science 292:733-37
79. Liu N, Bu T, Song Y, Zhang W, Li J, et al. 2010. The nature of the force-induced conformation transition of dsDNA studied by using single molecule force spectroscopy. Langmuir 26:9491-96
80. Liu S, Abbondanzieri EA, Rausch JW, Le Grice SF, Zhuang X. 2008. Slide into action: dynamic shuttling of HIV reverse transcriptase on nucleic acid substrates. Science 322:1092-97
81. Lohman TM. 1992. Escherichia coli DNA helicases: mechanisms of DNA unwinding. Mol. Microbiol. 6:5-14
82. Lohman TM, Ferrari ME. 1994. Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem. 63:527-70
83. Lohman TM, Overman LB. 1985. Two binding modes in Escherichia coli single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J. Biol. Chem. 260:3594-603
84. Lohman TM, Tomko EJ, Wu CG. 2008. Non-hexameric DNA helicases and translocases: mechanisms and regulation. Nat. Rev. Mol. Cell. Biol. 9:391-401
85. Maier B, Bensimon D, Croquette V. 2000. Replication by a single DNA polymerase of a stretched single-stranded DNA. Proc. Natl. Acad. Sci. USA 97:12002-7
86. Manosas M, Xi XG, Bensimon D, Croquette V. 2010. Active and passive mechanisms of helicases. Nucleic Acids Res. 38:5518-26
87. McKinney SA, Joo C, Ha T. 2006. Analysis of single-molecule FRET trajectories using hidden Markov modeling. Biophys.J. 91:1941-51
88. Meyer RR, Laine PS. 1990. The single-stranded DNA-binding protein of Escherichia coli. Microbiol. Rev. 54:342-80
89. Mine J, Disseau L, Takahashi M, Cappello G, Dutreix M, Viovy JL. 2007. Real-time measurements of the nucleation, growth and dissociation of single Rad51-DNAnucleoprotein filaments. Nucleic Acids Res. 35:7171-87
90. Murphy MC, Rasnik I, Cheng W, Lohman TM, Ha T. 2004. Probing single stranded DNA conformational flexibility using fluorescence spectroscopy. Biophys.J. 86:2530-37
91. Murzin AG. 1993. OB (oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J. 12:861-67
92. Myong S, Bruno MM, Pyle AM, Ha T. 2007. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 317:513-16
93. Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU, et al. 2009. Cytosolic viral sensor RIG-I is a 5'-triphosphate-dependent translocase on double-stranded RNA Science 323:1070-74
94. Myong S, Ha T. 2010. Stepwise translocation of nucleic acid motors. Curr. Opin. Struct. Biol. 20:121-27
95. Myong S, Rasnik I, Joo C, Lohman TM, Ha T. 2005. Repetitive shuttling of a motor protein on DNA Nature 437:1321-25
96. Niedziela-Majka A, Chesnik MA, Tomko EJ, Lohman TM. 2007. Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro. J. Biol. Chem. 282:27076-85
97. Pant K, Karpel RL, Rouzina I, Williams MC. 2004. Mechanical measurement of single-molecule binding rates: kinetics of DNA helix-destabilization by T4 gene 32 protein. J. Mol. Biol. 336:851-70
98. Pant K, Karpel RL, Rouzina I, Williams MC. 2005. Salt dependent binding of T4 gene 32 protein to single and double-stranded DNA: single molecule force spectroscopy measurements. J. Mol. Biol. 349:317-30
99. Park J, Jeon Y, In D, Fishel R, Ban C, Lee JB. 2010. Single-molecule analysis reveals the kinetics and physiological relevance of MutL-ssDNA binding. PLoS One 5:e15496
100. Park J, Myong S, Niedziela-Majka A, Lee KS, Yu J, et al. 2010. PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell 142:544-55
101. Patel SS, Picha KM. 2000. Structure and function of hexameric helicases. Annu. Rev. Biochem. 69:651-97
102. Perkins TT, Li HW, Dalal RV, Gelles J, Block SM. 2004. Forward and reverse motion of single RecBCD molecules on DNA. Biophys.J. 86:1640-48
103. Raghunathan S, Kozlov AG, Lohman TM, Waksman G. 2000. Structure of the DNA binding domain of E. coli SSB bound to ssDNA Nat. Struct. Biol. 7:648-52
104. Raghunathan S, Ricard CS, Lohman TM, Waksman G. 1997. Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwave-length X-ray diffraction on the selenomethionyl protein at 2.9-angstrom resolution. Proc. Natl. Acad. Sci. USA 94:6652-57
105. Ragunathan K, Joo C, Ha T. 2011. Real-time observation of strand exchange reaction with high spa-tiotemporal resolution. Structure 19:1064-73
106. Record MT Jr, Anderson CF, Lohman TM. 1978. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity. Q. Rev. Biophys. 11:103-78
107. Rivetti C, Walker C, Bustamante C. 1998. Polymer chain statistics and conformational analysis of DNA molecules with bends or sections of different flexibility. J. Mol. Biol. 280:41-59
108. Robertson RB, Moses DN, Kwon Y, Chan P, Chi P, et al. 2009. Structural transitions within human Rad51 nucleoprotein filaments. Proc. Natl. Acad. Sci. USA 106:12688-93
109. Romer R, Schomburg U, Krauss G, Maass G. 1984. Escherichia coli single-stranded DNA binding protein is mobile on DNA: 1H NMR study of its interaction with oligo-and polynucleotides. Biochemistry 23:6132-37
110. Rossi MJ, Mazina OM, Bugreev DV, Mazin AV. 2011. The RecA/RAD51 protein drives migration of Holliday junctions via polymerization on DNA. Proc. Natl. Acad. Sci. USA 108:6432-37
111. Rothenberg E, Grimme JM, Spies M, Ha T. 2008. Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Proc. Natl. Acad. Sci. USA 105:20274-79
112. f-tail.J. Biol. Chem. 282:34229-34
113. Roy R, Kozlov AG, Lohman TM, Ha T. 2007. Dynamic structural rearrangements between DNA binding modes of E. coli SSB protein. J. Mol. Biol. 369:1244-57
114. Roy R, Kozlov AG, Lohman TM, Ha T. 2009. SSB protein diffusion on single-stranded DNA stimulates RecA filament formation. Nature 461:1092-97
115. Saikrishnan K, Jeyakanthan J, Venkatesh J, Acharya N, Sekar K, et al. 2003. Structure of Mycobacterium tuberculosis single-stranded DNA-binding protein. Variability in quaternary structure and its implications. J. Mol. Biol. 331:385-93
116. Saikrishnan K, Manjunath GP, Singh P, Jeyakanthan J, Dauter Z, et al. 2005. Structure ofMycobacterium smegmatis single-stranded DNA-binding protein and a comparative study involving homologous SSBs: biological implications of structural plasticity and variability in quaternary association. Acta Crystallogr. D 61:1140-48
117. Saleh OA, McIntosh DB, Pincus P, Ribeck N. 2009. Nonlinear low-force elasticity of single-stranded DNA molecules. Phys. Rev. Lett. 102:068301
118. Schmidt T, Schutz GJ, Baumgartner W, Gruber HJ, Schindler H. 1996. Imaging of single molecule diffusion. Proc. Natl. Acad. Sci. USA 93:2926-29
119. Seol Y, Skinner GM, Visscher K. 2004. Elastic properties of a single-stranded charged homopolymeric ribonucleotide. Phys. Rev. Lett. 93:118102
120. Shamoo Y, Friedman AM, Parsons MR, Konigsberg WH, Steitz TA 1995. Crystal structure of a replication fork single-stranded DNA binding protein (T4 gp32) complexed to DNA. Nature 376:362-66
121. Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL. 2008. SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43:289-318
122. Shim JW, Tan Q, Gu LQ. 2009. Single-molecule detection of folding and unfolding of the G-quadruplex aptamer in a nanopore nanocavity. Nucleic Acids Res. 37:972-82
123. Shokri L, Marintcheva B, Eldib M, Hanke A, Rouzina I, Williams MC. 2008. Kinetics and thermodynamics of salt-dependent T7 gene 2.5 protein binding to single-and double-stranded DNA. Nucleic Acids Res. 36:5668-77
124. Shokri L, Marintcheva B, Richardson CC, Rouzina I, Williams MC. 2006. Single molecule force spectroscopy of salt-dependent bacteriophage T7 gene 2.5 protein binding to single-stranded DNA. J. Biol. Chem. 281:38689-96
125. Shroff H, Reinhard BM, Siu M, Agarwal H, Spakowitz A, Liphardt J. 2005. Biocompatible force sensor with optical readout and dimensions of 6 nm. Nano Lett. 5:1509-14
126. Singleton MR, Dillingham MS, Wigley DB. 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76:23-50
127. Strick TR, Allemand JF, Bensimon D, Bensimon A, Croquette V. 1996. The elasticity of a single super-coiled DNA molecule. Science 271:1835-37
128. Sun B, Wei KJ, Zhang B, Zhang XH, Dou SX, et al. 2008. Impediment of E. coli UvrD by DNA-destabilizing force reveals a strained-inchworm mechanism of DNA unwinding. EMBOJ. 27:3279-87
129. Theissen B, Karow AR, Kohler J, Gubaev A, Klostermeier D. 2008. Cooperative binding of ATP and RNAinduces a closed conformation in a DEAD box RNAhelicase. Proc. Natl. Acad. Sci. USA 105:548-53
130. Tomko EJ, Fischer CJ, Niedziela-Majka A, Lohman TM. 2007. A nonuniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA. Mol. Cell 26:335-47
131. Tomko EJ, Jia H, Park J, Maluf NK, Ha T, Lohman TM. 2010. 5'-single-stranded/duplexDNAjunctions are loading sites for E. coli UvrD translocase. EMBO J. 29:3826-39
132. van der Heijden T, Modesti M, Hage S, Kanaar R, Wyman C, Dekker C. 2008. Homologous recombination in real time: DNA strand exchange by RecA. Mol. Cell 30:530-38
133. Van Dyck E, Foury F, Stillman B, Brill SJ. 1992. A single-stranded DNA binding protein required for mitochondrial DNA replication in S. cerevisiae is homologous to E. coli SSB. EMBO J. 11:3421-30
134. van Loenhout MT, van der Heijden T, Kanaar R, Wyman C, Dekker C. 2009. Dynamics of RecA filaments on single-stranded DNA. Nucleic Acids Res. 37:4089-99
135. van Mameren J, Modesti M, Kanaar R, Wyman C, Peterman EJ, Wuite GJ. 2009. Counting RAD51 proteins disassembling from nucleoprotein filaments under tension. Nature 457:745-48
136. van Oijen AM, Blainey PC, Crampton DJ, Richardson CC, Ellenberger T, Xie XS. 2003. Single-molecule kinetics of lambda exonuclease reveal base dependence and dynamic disorder. Science 301:1235-38
137. Veaute X, Delmas S, Selva M, Jeusset J, Le Cam E, et al. 2005. UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 24:180-89
138. Walter NG, Huang CY, Manzo AJ, Sobhy MA. 2008. Do-it-yourself guide: how to use the modern single-molecule toolkit. Nat. Methods 5:475-89
139. Wold MS. 1997. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66:61-92
140. Woodside MT, Behnke-Parks WM, Larizadeh K, Travers K, Herschlag D, Block SM. 2006. Nanome-chanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins. Proc. Natl. Acad. Sci. USA 103:6190-95
141. Wuite GJL, Smith SB, Young M, Keller D, Bustamante C. 2000. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404:103-6
142. Yang C, Curth U, Urbanke C, Kang C. 1997. Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 A resolution. Nat. Struct. Biol. 4:153-57
143. Ying L, Green JJ, Li H, Klenerman D, Balasubramanian S. 2003. Studies on the structure and dynamics of the human telomeric G quadruplex by single-molecule fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 100:14629-34
144. Yodh JG, Schlierf M, Ha T. 2010. Insight into helicase mechanism and function revealed through single-molecule approaches. Q. Rev. Biophys. 43:185-217
145. Yodh JG, Stevens BC, Kanagaraj R, Janscak P, Ha T. 2009. BLM helicase measures DNA unwound before switching strands and hRPA promotes unwinding reinitiation. EMBO J. 28:405-16
146. Yu J, Ha T, Schulten K 2007. How directional translocation is regulated in a DNA helicase motor. Biophys. J. 93:3783-97
147. Yu Z, Schonhoft JD, Dhakal S, Bajracharya R, Hegde R, et al. 2009. ILPR G-quadruplexes formed in seconds demonstrate high mechanical stabilities. J. Am. Chem. Soc. 131:1876-82
148. Zhou R, Kozlov AG, Roy R, Zhang J, Korolev S, et al. 2011. SSB functions as a sliding platform that migrates on DNA via reptation. Cell 146:222-32