University of Groningen Dynamics of the bacterial replisome Monachino, Enrico

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University of Groningen

Dynamics of the bacterial replisome

Monachino, Enrico

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Monachino, E. (2018). Dynamics of the bacterial replisome: Biochemical and single-molecule studies of the replicative helicase in Escherichia coli. University of Groningen.

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EFERENCES

Abbondanzieri, E.A., Greenleaf, W.J., Shaevitz, J.W., Landick, R., Block, S.M., 2005. Direct observation of base-pair stepping by RNA polymerase. Nature 438, 460–465. https://doi.org/10.1038/nature04268

Åberg, C., Duderstadt, K.E., van Oijen, A.M., 2016. Stability versus exchange: a paradox in DNA replication. Nucleic Acids Res. 44, 4846–4854.

https://doi.org/10.1093/nar/gkw296

Akyuz, N., Georgieva, E.R., Zhou, Z., Stolzenberg, S., Cuendet, M.A., Khelashvili, G., Altman, R.B., Terry, D.S., Freed, J.H., Weinstein, H., Boudker, O., Blanchard, S.C., 2015. Transport domain unlocking sets the uptake rate of an aspartate transporter. Nature

518, 68–73. https://doi.org/10.1038/nature14158

Alberts, B.M., Barry, J., Bedinger, P., Formosa, T., Jongeneel, C.V., Kreuzer, K.N., 1983. Studies on DNA replication in the bacteriophage T4 in vitro system. Cold Spring Harb.

Symp. Quant. Biol. 47 Pt 2, 655–668. https://doi.org/10.1101/SQB.1983.047.01.077

Alberts, B.M., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P., 2007. Molecular

Biology of the Cell, Fifth edit. ed. Garland Science.

Alegre-Cebollada, J., Kosuri, P., Giganti, D., Eckels, E., Rivas-Pardo, J.A., Hamdani, N., Warren, C.M., Solaro, R.J., Linke, W.A., Fernández, J.M., 2014. S-glutathionylation of cryptic cysteines enhances titin elasticity by blocking protein folding. Cell 156, 1235– 1246. https://doi.org/10.1016/j.cell.2014.01.056

Ali, M.M., Li, F., Zhang, Z., Zhang, K., Kang, D.-K., Ankrum, J.A., Le, X.C., Zhao, W., 2014. Rolling circle amplification: a versatile tool for chemical biology, materials science and medicine. Chem. Soc. Rev. 43, 3324–3341. https://doi.org/10.1039/c3cs60439j Anderson, S.G., Williams, C.R., O’Donnell, M., Bloom, L.B., 2007. A function for the 

subunit in loading the Escherichia coli DNA polymerase sliding clamp. J. Biol. Chem.

282, 7035–7045. https://doi.org/10.1074/jbc.M610136200

Ando, T., 2014. High-speed AFM imaging. Curr. Opin. Struct. Biol. 28, 63–68. https://doi.org/10.1016/j.sbi.2014.07.011

Ando, T., Uchihashi, T., Fukuma, T., 2008. High-speed atomic force microscopy for nano-visualization of dynamic biomolecular processes. Prog. Surf. Sci. 83, 337–437. https://doi.org/10.1016/j.progsurf.2008.09.001

Ando, T., Uchihashi, T., Scheuring, S., 2014. Filming biomolecular processes by high-speed atomic force microscopy. Chem. Rev. 114, 3120–3188.

https://doi.org/10.1021/cr4003837

Arias-Palomo, E., O’Shea, V.L., Hood, I.V., Berger, J.M., 2013. The bacterial DnaC helicase loader is a DnaB ring breaker. Cell 153, 438–448.

https://doi.org/10.1016/j.cell.2013.03.006

Axelrod, D., 2001. Total internal reflection fluorescence microscopy in cell biology. Traffic 2, 764–774. https://doi.org/10.1034/j.1600-0854.2001.21104.x

Axelrod, D., Burghardt, T.P., Thompson, N.L., 1984. Total internal reflection fluorescence.

Annu. Rev. Biophys. Bioeng. 13, 247–268.

https://doi.org/10.1146/annurev.bb.13.060184.001335

Bailey, S., Eliason, W.K., Steitz, T.A., 2007. Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 318, 459–463.

(3)

186

Barry, E.R., Bell, S.D., 2006. DNA replication in the archaea. Microbiol. Mol. Biol. Rev. 70, 876–887. https://doi.org/10.1128/MMBR.00029-06

Baumann, C.G., Smith, S.B., Bloomfield, V.A, Bustamante, C., 1997. Ionic effects on the elasticity of single DNA molecules. Proc. Natl. Acad. Sci. U. S. A. 94, 6185–6190. https://doi.org/10.1073/pnas.94.12.6185

Beattie, T.R., Kapadia, N., Nicolas, E., Uphoff, S., Wollman, A.J., Leake, M.C., Reyes-Lamothe, R., 2017. Frequent exchange of the DNA polymerase during bacterial chromosome replication. eLife 6, e21763. https://doi.org/10.7554/eLife.21763

Beckett, D., Kovaleva, E., Schatz, P.J., 1999. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 8, 921–929. https://doi.org/10.1110/ps.8.4.921

Benkovic, S.J., Valentine, A.M., Salinas, F., 2001. Replisome-mediated DNA replication.

Annu. Rev. Biochem. 70, 181–208.

https://doi.org/10.1146/annurev.biochem.70.1.181

Berghuis, B.A., Köber, M., van Laar, T., Dekker, N.H., 2016. High-throughput, high-force probing of DNA–protein interactions with magnetic tweezers. Methods 105, 90–98. https://doi.org/10.1016/j.ymeth.2016.03.025

Berghuis, B.A., Dulin, D., Xu, Z.-Q., van Laar, T., Cross, B., Janissen, R., Jergic, S., Dixon, N.E., Depken, M., Dekker, N.H., 2015. Strand separation establishes a sustained lock at the Tus–Ter replication fork barrier. Nat. Chem. Biol. 11, 579–585.

https://doi.org/10.1038/nchembio.1857

Bhabha, G., Johnson, G.T., Schroeder, C.M., Vale, R.D., 2016. How dynein moves along microtubules. Trends Biochem. Sci. 41, 94–105.

https://doi.org/10.1016/j.tibs.2015.11.004

Bird, L.E., Pan, H., Soultanas, P., Wigley, D.B., 2000. Mapping protein–protein interactions within a stable complex of DNA primase and DnaB helicase from Bacillus

stearothermophilus. Biochemistry 39, 171–182. https://doi.org/10.1021/bi9918801

Biswas, E.E., Biswas, S.B., 1999. Mechanism of DnaB helicase of Escherichia coli: structural domains involved in ATP hydrolysis, DNA binding, and oligomerization. Biochemistry

38, 10919–10928. https://doi.org/10.1021/bi990048t

Biswas, T., Tsodikov, O.V., 2008. Hexameric ring structure of the N-terminal domain of

Mycobacterium tuberculosis DnaB helicase. FEBS J. 275, 3064–3071.

https://doi.org/10.1111/j.1742-4658.2008.06460.x

Biyani, M., Ichiki, T., 2015. Microintaglio printing for soft lithography-based in situ microarrays. Microarrays 4, 311–323. https://doi.org/10.3390/microarrays4030311 Blehm, B.H., Schroer, T.A., Trybus, K.M., Chemla, Y.R., Selvin, P.R., 2013. In vivo optical

trapping indicates kinesin’s stall force is reduced by dynein during intracellular transport. Proc. Natl. Acad. Sci. U. S. A. 110, 3381–3386.

https://doi.org/10.1073/pnas.1219961110

Blehm, B.H., Selvin, P.R., 2014. Single-molecule fluorescence and in vivo optical traps: how multiple dyneins and kinesins interact. Chem. Rev. 114, 3335–3352.

https://doi.org/10.1021/cr4005555

Blinkova, A., Hervas, C., Stukenberg, P.T., Onrust, R., O’Donnell, M.E., Walker, J.R., 1993. The Escherichia coli DNA polymerase III holoenzyme contains both products of the

dnaX gene,  and , but only  is essential. J. Bacteriol. 175, 6018–6027.

https://doi.org/10.1128/jb.175.18.6018-6027.1993

(4)

187

Escherichia coli DNA polymerase III  subunit from within the  subunit reading frame. Nucleic Acids Res. 18, 1725–1729.

Brown, M.W., Kim, Y., Williams, G.M., Huck, J.D., Surtees, J.A., Finkelstein, I.J., 2016. Dynamic DNA binding licenses a repair factor to bypass roadblocks in search of DNA lesions. Nat. Commun. 7, 10607. https://doi.org/10.1038/ncomms10607

Bujalowski, W., Klonowska, M.M., Jezewska, M.J., 1994. Oligomeric structure of Escherichia

coli primary replicative helicase DnaB protein. J. Biol. Chem. 269, 31350–31358.

Bullard, J.M., Pritchard, A.E., Song, M.-S., Glover, B.P., Wieczorek, A., Chen, J., Janjic, N., McHenry, C.S., 2002. A three-domain structure for the  subunit of the DNA polymerase III holoenzyme  domain III binds ’ and assembles into the DnaX complex. J. Biol. Chem. 277, 13246–13256. https://doi.org/10.1074/jbc.M108708200 Bustamante, C., Marko, J.F., Siggia, E.D., Smith, S., 1994. Entropic elasticity of -phage DNA.

Science 265, 1599–1600. https://doi.org/10.1126/science.8079175

Bustamante, C., Smith, S.B., Liphardt, J., Smith, D., 2000. Single-molecule studies of DNA mechanics. Curr. Opin. Struct. Biol. 10, 279–285.

Cheezum, M.K., Walker, W.F., Guilford, W.H., 2001. Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys. J. 81, 2378–2388.

https://doi.org/10.1016/S0006-3495(01)75884-5

Chen, J., Dalal, R.V., Petrov, A.N., Tsai, A., O’Leary, S.E., Chapin, K., Cheng, J., Ewan, M., Hsiung, P.-L., Lundquist, P., Turner, S.W., Hsu, D.R., Puglisi, J.D., 2014. High-throughput platform for real-time monitoring of biological processes by multicolor single-molecule fluorescence. Proc. Natl. Acad. Sci. U. S. A. 111, 664–669.

Chen, T.-Y., Santiago, A.G., Jung, W., Krzemiński, Ł., Yang, F., Martell, D.J., Helmann, J.D., Chen, P., 2015. Concentration- and chromosome-organization-dependent regulator unbinding from DNA for transcription regulation in living cells. Nat. Commun. 6, 7445. https://doi.org/10.1038/ncomms8445

Cheng, Y., 2015. Single-particle cryo-EM at crystallographic resolution. Cell 161, 450–457. https://doi.org/10.1016/j.cell.2015.03.049

Cho, W.-K., Jergic, S., Kim, D., Dixon, N.E., Lee, J.-B., 2014. Loading dynamics of a sliding DNA clamp. Angew. Chem. Int. Ed. Engl. 53, 6768–6771.

https://doi.org/10.1002/anie.201403063

Cnossen, J.P., Dulin, D., Dekker, N.H., 2014. An optimized software framework for real-time, high-throughput tracking of spherical beads. Rev. Sci. Instrum. 85, 103712.

https://doi.org/10.1063/1.4898178

Collins, B.E., Ye, L.F., Duzdevich, D., Greene, E.C., 2014. DNA curtains: novel tools for imaging protein–nucleic acid interactions at the single-molecule level. Methods Cell

Biol. 123, 217–234. https://doi.org/10.1016/B978-0-12-420138-5.00012-4

Corn, J.E., Pease, P.J., Hura, G.L., Berger, J.M., 2005. Crosstalk between primase subunits can act to regulate primer synthesis in trans. Mol. Cell 20, 391–401.

https://doi.org/10.1016/j.molcel.2005.09.004

Crawford, R., Torella, J.P., Aigrain, L., Plochowietz, A., Gryte, K., Uphoff, S., Kapanidis, A.N., 2013. Long-lived intracellular single-molecule fluorescence using electroporated molecules. Biophys. J. 105, 2439–2450. https://doi.org/10.1016/j.bpj.2013.09.057 Crocker, J.C., Grier, D.G., 1996. When like charges attract: the effects of geometrical

confinement on long-range colloidal interactions. Phys. Rev. Lett. 77, 1897–1900. https://doi.org/10.1103/PhysRevLett.77.1897

(5)

188

Dahm, R., 2008. Discovering DNA: Friedrich Miescher and the early years of nucleic acid research. Hum. Genet. 122, 565–581. https://doi.org/10.1007/s00439-007-0433-0 Dallmann, H.G., Kim, S., Pritchard, A.E., Marians, K.J., McHenry, C.S., 2000. Characterization

of the unique C terminus of the Escherichia coli  DnaX protein. Monomeric C- binds  and DnaB and can partially replace  in reconstituted replication forks. J. Biol. Chem.

275, 15512–15519. https://doi.org/10.1074/jbc.M909257199

Dallmann, H.G., McHenry, C.S., 1995. DnaX complex of Escherichia coli DNA polymerase III holoenzyme. Physical characterization of the DnaX subunits and complexes. J. Biol.

Chem. 270, 29563–29569. https://doi.org/10.1074/jbc.270.49.29563

Dave, R., Terry, D.S., Munro, J.B., Blanchard, S.C., 2009. Mitigating unwanted photophysical processes for improved single-molecule fluorescence imaging. Biophys. J. 96, 2371– 2381. https://doi.org/10.1016/j.bpj.2008.11.061

Dawson, K., Strutwolf, J., Rodgers, K.P., Herzog, G., Arrigan, D.W.M., Quinn, A.J., O’Riordan, A., 2011. Single nanoskived nanowires for electrochemical applications. Anal. Chem.

83, 5535–5540. https://doi.org/10.1021/ac2004086

de Souza, N., 2012. Pulling on single molecules. Nat. Methods 9, 873–877. https://doi.org/10.1038/nmeth.2149

De Vlaminck, I., Henighan, T., van Loenhout, M.T.J., Pfeiffer, I., Huijts, J., Kerssemakers, J.W.J., Katan, A.J., van Langen-Suurling, A., van der Drift, E., Wyman, C., Dekker, C., 2011. Highly parallel magnetic tweezers by targeted DNA tethering. Nano Lett. 11, 5489–5493. https://doi.org/10.1021/nl203299e

de Vries, A.H.B., Krenn, B.E., van Driel, R., Kanger, J.S., 2005. Micro magnetic tweezers for nanomanipulation inside live cells. Biophys. J. 88, 2137–2144.

https://doi.org/10.1529/biophysj.104.052035

Debyser, Z., Tabor, S., Richardson, C.C., 1994. Coordination of leading and lagging strand DNA synthesis at the replication fork of bacteriophage T7. Cell 77, 157–166. https://doi.org/10.1016/0092-8674(94)90243-7

Demidov, V. V, 2002. Rolling-circle amplification in DNA diagnostics: the power of simplicity.

Expert Rev. Mol. Diagn. 2, 542–548. https://doi.org/10.1586/14737159.2.6.542

Dixon, N.E., 2009. DNA replication: prime-time looping. Nature 462, 854–855. https://doi.org/10.1038/462854a

Dohrmann, P.R., Manhart, C.M., Downey, C.D., McHenry, C.S., 2011. The rate of polymerase release upon filling the gap between Okazaki fragments is inadequate to support cycling during lagging strand synthesis. J. Mol. Biol. 414, 15–27.

https://doi.org/10.1016/j.jmb.2011.09.039

Dohrmann, P.R., McHenry, C.S., 2005. A bipartite polymerase-processivity factor

interaction: only the internal  binding site of the  subunit is required for processive replication by the DNA polymerase III holoenzyme. J. Mol. Biol. 350, 228–239. https://doi.org/10.1016/j.jmb.2005.04.065

Duderstadt, K.E., Geertsema, H.J., Stratmann, S.A., Punter, C.M., Kulczyk, A.W., Richardson, C.C., van Oijen, A.M., 2016. Simultaneous real-time imaging of leading and lagging strand synthesis reveals the coordination dynamics of single replisomes. Mol. Cell 64, 1035–1047. https://doi.org/10.1016/j.molcel.2016.10.028

Duderstadt, K.E., Reyes-Lamothe, R., van Oijen, A.M., Sherratt, D.J., 2014. Replication-fork dynamics. Cold Spring Harb. Perspect. Biol. 6, a010157.

https://doi.org/10.1101/cshperspect.a010157

(6)

189

through modern approaches to high-throughput single-molecule force-spectroscopy experiments. Curr. Opin. Struct. Biol. 34, 116–122.

https://doi.org/10.1016/j.sbi.2015.08.007

Dulin, D., Cui, T.J., Cnossen, J., Docter, M.W., Lipfert, J., Dekker, N.H., 2015b. High spatiotemporal-resolution magnetic tweezers: calibration and applications for DNA dynamics. Biophys. J. 109, 2113–2125. https://doi.org/10.1016/j.bpj.2015.10.018 Dulin, D., Lipfert, J., Moolman, M.C., Dekker, N.H., 2013. Studying genomic processes at the

single-molecule level: introducing the tools and applications. Nat. Rev. Genet. 14, 9– 22. https://doi.org/10.1038/nrg3316

Dulin, D., Vilfan, I.D., Berghuis, B.A., Hage, S., Bamford, D.H., Poranen, M.M., Depken, M., Dekker, N.H., 2015c. Elongation-competent pauses govern the fidelity of a viral RNA-dependent RNA polymerase. Cell Rep. 10, 983–992.

https://doi.org/10.1016/j.celrep.2015.01.031

Duzdevich, D., Warner, M.D., Ticau, S., Ivica, N.A., Bell, S.P., Greene, E.C., 2015. The dynamics of eukaryotic replication initiation: origin specificity, licensing, and firing at the single-molecule level. Mol. Cell 58, 483–494.

Eid, J., Fehr, A., Gray, J., Luong, K., Lyle, J., Otto, G., Peluso, P., Rank, D., Baybayan, P., Bettman, B., Bibillo, A., Bjornson, K., Chaudhuri, B., Christians, F., Cicero, R., Clark, S., Dalal, R., DeWinter, A., Dixon, J., Foquet, M., Gaertner, A., Hardenbol, P., Heiner, C., Hester, K., Holden, D., Kearns, G., Kong, X., Kuse, R., Lacroix, Y., Lin, S., Lundquist, P., Ma, C., Marks, P., Maxham, M., Murphy, D., Park, I., Pham, T., Phillips, M., Roy, J., Sebra, R., Shen, G., Sorenson, J., Tomaney, A., Travers, K., Trulson, M., Vieceli, J., Wegener, J., Wu, D., Yang, A., Zaccarin, D., Zhao, P., Zhong, F., Korlach, J., Turner, S., 2009. Real-time DNA sequencing from single polymerase molecules. Science 323, 133–138. https://doi.org/10.1126/science.1162986

Elshenawy, M.M., Jergic, S., Xu, Z.-Q., Sobhy, M.A., Takahashi, M., Oakley, A.J., Dixon, N.E., Hamdan, S.M., 2015. Replisome speed determines the efficiency of the Tus−Ter replication termination barrier. Nature 525, 394–398.

https://doi.org/10.1038/nature14866

Erkens, G.B., Hänelt, I., Goudsmits, J.M.H., Slotboom, D.J., van Oijen, A.M., 2013. Unsynchronised subunit motion in single trimeric sodium-coupled aspartate transporters. Nature 502, 119–123. https://doi.org/10.1038/nature12538

Essmann, C.L., Elmi, M., Shaw, M., Anand, G.M., Pawar, V.M., Srinivasan, M.A., 2017. In-vivo high resolution AFM topographic imaging of Caenorhabditis elegans reveals

previously unreported surface structures of cuticle mutants. Nanomedicine 13, 183– 189. https://doi.org/10.1016/j.nano.2016.09.006

Falkenberg, M., Lehman, I.R., Elias, P., 2000. Leading and lagging strand DNA synthesis in

vitro by a reconstituted herpes simplex virus type 1 replisome. Proc. Natl. Acad. Sci. U. S. A. 97, 3896–3900. https://doi.org/10.1073/pnas.97.8.3896

Fazio, T.A., Lee, J.Y., Wind, S.J., Greene, E.C., 2012. Assembly of DNA curtains using hydrogen silsesquioxane as a barrier to lipid diffusion. Anal. Chem. 84, 7613–7617. https://doi.org/10.1021/ac302149g

Fazio, T.A., Visnapuu, M., Greene, E.C., Wind, S.J., 2009. Fabrication of nanoscale “curtain rods” for DNA curtains using nanoimprint lithography. J. Vac. Sci. Technol. B

Microelectron. Nanom. Struct. 27, 3095–3098. https://doi.org/10.1116/1.3259951

(7)

190

rods: high-throughput tools for single molecule imaging. Langmuir 24, 10524–10531. https://doi.org/10.1021/la801762h

Fernandez-Leiro, R., Conrad, J., Scheres, S.H., Lamers, M.H., 2015. Cryo-EM structures of the

E. coli replicative DNA polymerase reveal its dynamic interactions with the DNA sliding

clamp, exonuclease and τ. eLife 4, e11134. https://doi.org/10.7554/eLife.11134 Fernandez-Leiro, R., Scheres, S.H.W., 2016. Unravelling biological macromolecules with

cryo-electron microscopy. Nature 537, 339–346. https://doi.org/10.1038/nature19948

Fessl, T., Adamec, F., Polívka, T., Foldynová-Trantírková, S., Vácha, F., Trantírek, L., 2012. Towards characterization of DNA structure under physiological conditions in vivo at the single-molecule level using single-pair FRET. Nucleic Acids Res. 40, e121. https://doi.org/10.1093/nar/gks333

Finkelstein, I.J., Greene, E.C., 2011. Supported lipid bilayers and DNA curtains for high-throughput single-molecule studies. Methods Mol. Biol. 745, 447–461.

https://doi.org/10.1007/978-1-61779-129-1_26

Finkelstein, I.J., Visnapuu, M.-L., Greene, E.C., 2010. Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468, 983–987. https://doi.org/10.1038/nature09561

Flower, A.M., McHenry, C.S., 1990. The  subunit of DNA polymerase III holoenzyme of

Escherichia coli is produced by ribosomal frameshifting. Proc. Natl. Acad. Sci. U. S. A.

87, 3713–3717. https://doi.org/10.1073/pnas.87.10.3713

Frick, D.N., Richardson, C.C., 2001. DNA primases. Annu. Rev. Biochem. 70, 39–80. https://doi.org/10.1146/annurev.biochem.70.1.39

Funatsu, T., Harada, Y., Tokunaga, M., Saito, K., Yanagida, T., 1995. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature 374, 555–559. https://doi.org/10.1038/374555a0

Gallardo, I.F., Pasupathy, P., Brown, M., Manhart, C.M., Neikirk, D.P., Alani, E., Finkelstein, I.J., 2015. High-throughput universal DNA curtain arrays for single-molecule

fluorescence imaging. Langmuir 31, 10310–10317. https://doi.org/10.1021/acs.langmuir.5b02416

Galletto, R., Jezewska, M.J., Bujalowski, W., 2003. Interactions of the Escherichia coli DnaB helicase hexamer with the replication factor the DnaC protein. Effect of nucleotide cofactors and the ssDNA on protein–protein interactions and the topology of the complex. J. Mol. Biol. 329, 441–465. https://doi.org/10.1016/S0022-2836(03)00435-2 Gao, D., McHenry, C.S., 2001a.  binds and organizes Escherichia coli replication proteins

through distinct domains. Domain IV, located within the unique C terminus of , binds the replication fork, helicase, DnaB. J. Biol. Chem. 276, 4441–4446.

https://doi.org/10.1074/jbc.M009830200

Gao, D., McHenry, C.S., 2001b.  binds and organizes Escherichia coli replication through distinct domains. Partial proteolysis of terminally tagged  to determine candidate domains and to assign domain V as the  binding domain. J. Biol. Chem. 276, 4433– 4440. https://doi.org/10.1074/jbc.M009828200

Geertsema, H.J., Duderstadt, K.E., van Oijen, A.M., 2015a. Single-molecule observation of prokaryotic DNA replication. Methods Mol. Biol. 1300, 219–238.

https://doi.org/10.1007/978-1-4939-2596-4_14

Geertsema, H.J., Kulczyk, A.W., Richardson, C.C., van Oijen, A.M., 2014. Single-molecule studies of polymerase dynamics and stoichiometry at the bacteriophage T7

(8)

191

replication machinery. Proc. Natl. Acad. Sci. U. S. A. 111, 4073–4078. https://doi.org/10.1073/pnas.1402010111

Geertsema, H.J., Schulte, A.C., Spenkelink, L.M., McGrath, W.J., Morrone, S.R., Sohn, J., Mangel, W.F., Robinson, A., van Oijen, A.M., 2015b. Single-molecule imaging at high fluorophore concentrations by local activation of dye. Biophys. J. 108, 949–956. https://doi.org/10.1016/j.bpj.2014.12.019

Geertsema, H.J., van Oijen, A.M., 2013. A single-molecule view of DNA replication: the dynamic nature of multi-protein complexes revealed. Curr. Opin. Struct. Biol. 23, 788– 793. https://doi.org/10.1016/j.sbi.2013.06.018

Geng, H., Du, C., Chen, S., Salerno, V., Manfredi, C., Hsieh, P., 2011. In vitro studies of DNA mismatch repair proteins. Anal. Biochem. 413, 179–184.

https://doi.org/10.1016/j.ab.2011.02.017

Georgescu, R.E., Kurth, I., O’Donnell, M.E., 2011. Single-molecule studies reveal the function of a third polymerase in the replisome. Nat. Struct. Mol. Biol. 19, 113–116.

https://doi.org/10.1038/nsmb.2179

Georgescu, R.E., Yao, N., Indiani, C., Yurieva, O., O’Donnell, M.E., 2014. Replisome

mechanics: lagging strand events that influence speed and processivity. Nucleic Acids

Res. 42, 6497–6510. https://doi.org/10.1093/nar/gku257

Ghodke, H., Wang, H., Hsieh, C.L., Woldemeskel, S., Watkins, S.C., Rapić-Otrin, V., Van Houten, B., 2014. Single-molecule analysis reveals human UV-damaged DNA-binding protein (UV-DDB) dimerizes on DNA via multiple kinetic intermediates. Proc. Natl.

Acad. Sci. U. S. A. 111, E1862–E1871. https://doi.org/10.1073/pnas.1323856111

Giannone, G., Hosy, E., Levet, F., Constals, A., Schulze, K., Sobolevsky, A.I., Rosconi, M.P., Gouaux, E., Tampé, R., Choquet, D., Cognet, L., 2010. Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density. Biophys. J. 99, 1303–1310. https://doi.org/10.1016/j.bpj.2010.06.005

Gibb, B., Silverstein, T.D., Finkelstein, I.J., Greene, E.C., 2012. Single-stranded DNA curtains for real-time single-molecule visualization of protein–nucleic acid interactions. Anal.

Chem. 84, 7607–7612. https://doi.org/10.1021/ac302117z

Gibb, B., Ye, L.F., Gergoudis, S.C., Kwon, Y., Niu, H., Sung, P., Greene, E.C., 2014.

Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging. PLoS One 9, e87922.

https://doi.org/10.1371/journal.pone.0087922

Glover, B.P., McHenry, C.S., 1998. The  subunits of DNA polymerase III holoenzyme bind to single-stranded DNA-binding protein (SSB) and facilitate replication of an SSB-coated template. J. Biol. Chem. 273, 23476–23484.

https://doi.org/10.1074/jbc.273.36.23476

Gorman, J., Chowdhury, A., Surtees, J.A., Shimada, J., Reichman, D.R., Alani, E., Greene, E.C., 2007. Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2–Msh6. Mol. Cell 28, 359–370.

Gorman, J., Fazio, T., Wang, F., Wind, S., Greene, E.C., 2010a. Nanofabricated racks of aligned and anchored DNA substrates for single-molecule imaging. Langmuir 26, 1372–1379. https://doi.org/10.1021/la902443e

Gorman, J., Greene, E.C., 2013. Target search dynamics during post-replicative mismatch repair. Cell Cycle 12, 537–538. https://doi.org/10.4161/cc.23669

(9)

one-192

dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat.

Struct. Mol. Biol. 17, 932–938. https://doi.org/10.1038/nsmb.1858

Graham, J.E., Marians, K.J., Kowalczykowski, S.C., 2017. Independent and stochastic action of DNA polymerases in the replisome. Cell 169, 1201–1213.e17.

Graham, J.S., Johnson, R.C., Marko, J.F., 2011. Concentration-dependent exchange accelerates turnover of proteins bound to double-stranded DNA. Nucleic Acids Res.

39, 2249–2259. https://doi.org/10.1093/nar/gkq1140

Granéli, A., Yeykal, C.C., Prasad, T.K., Greene, E.C., 2006. Organized arrays of individual DNA molecules tethered to supported lipid bilayers. Langmuir 22, 292–299.

https://doi.org/10.1021/la051944a

Greene, E.C., Wind, S., Fazio, T., Gorman, J., Visnapuu, M.-L., 2010. DNA curtains for high-throughput single-molecule optical imaging. Methods Enzymol. 472, 293–315 https://doi.org/10.1016/S0076-6879(10)72006-1

Greenleaf, W.J., Woodside, M.T., Block, S.M., 2007. High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct. 36, 171– 190. https://doi.org/10.1146/annurev.biophys.36.101106.101451

Gulbis, J.M., Kazmirski, S.L., Finkelstein, J., Kelman, Z., O’Donnell, M., Kuriyan, J., 2004. Crystal structure of the chi:psi sub-assembly of the Escherichia coli DNA polymerase clamp-loader complex. Eur. J. Biochem. 271, 439–449.

https://doi.org/10.1046/j.1432-1033.2003.03944.x

Gulinatti, A., Rech, I., Maccagnani, P., Ghioni, M., 2013. A 48-pixel array of single photon avalanche diodes for multispot single molecule analysis. Proc. SPIE Int. Soc. Opt. Eng. 8631. https://doi.org/10.1117/12.2003984

Ha, T., 2001. Single-molecule fluorescence resonance energy transfer. Methods 25, 78–86. https://doi.org/10.1006/meth.2001.1217

Ha, T., Enderle, T., Ogletree, D.F., Chemla, D.S., Selvin, P.R., 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. U. S. A. 93, 6264– 6268. https://doi.org/10.1073/pnas.93.13.6264

Ha, T., Rasnik, I., Cheng, W., Babcock, H.P., Gauss, G.H., Lohman, T.M., Chu, S., 2002. Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase.

Nature 419, 638–641. https://doi.org/10.1038/nature01083

Ha, T., Tinnefeld, P., 2012. Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu. Rev. Phys. Chem. 63, 595–617. https://doi.org/10.1146/annurev-physchem-032210-103340

Hamdan, S.M., Loparo, J.J., Takahashi, M., Richardson, C.C., van Oijen, A.M., 2009. Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis. Nature

Hamdan, S.M., Richardson, C.C., 2009. Motors, switches, and contacts in the replisome.

Annu. Rev. Biochem. 78, 205–243.

Haraguchi, T., Kojidani, T., Koujin, T., Shimi, T., Osakada, H., Mori, C., Yamamoto, A., Hiraoka, Y., 2008. Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J. Cell Sci. 121, 2540–2554.

https://doi.org/10.1242/jcs.033597

(10)

193

2004. The clamp-loader–helicase interaction in Bacillus. Atomic force microscopy reveals the structural organisation of the DnaB– complex in Bacillus. J. Mol. Biol. 336, 381–393. https://doi.org/10.1016/j.jmb.2003.12.043

Heller, R.C., Marians, K.J., 2005. The disposition of nascent strands at stalled replication forks dictates the pathway of replisome loading during restart. Mol. Cell 17, 733–743. https://doi.org/10.1016/j.molcel.2005.01.019

Henderson, R., Baldwin, J.M., Ceska, T.A., Zemlin, F., Beckmann, E., Downing, K.H., 1990. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213, 899–929.

https://doi.org/10.1016/S0022-2836(05)80271-2

Hendricks, A.G., Holzbaur, E.L.F., Goldman, Y.E., 2012. Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors. Proc. Natl. Acad. Sci. U.

S. A. 109, 18447–18452. https://doi.org/10.1073/pnas.1215462109

Hestand, M.S., Van Houdt, J., Cristofoli, F., Vermeesch, J.R., 2016. Polymerase specific error rates and profiles identified by single molecule sequencing. Mutat. Res. Mol. Mech.

Mutagen. 784–785, 39–45. https://doi.org/10.1016/j.mrfmmm.2016.01.003

Hill, F.R., Monachino, E., van Oijen, A.M., 2017. The more the merrier: high-throughput single-molecule techniques. Biochem. Soc. Trans. 45, 759–769.

https://doi.org/10.1042/BST20160137

Holzbaur, E.L., Goldman, Y.E., 2010. Coordination of molecular motors: from in vitro assays to intracellular dynamics. Curr. Opin. Cell Biol. 22, 4–13.

https://doi.org/10.1016/j.ceb.2009.12.014

Hua, B., Han, K.Y., Zhou, R., Kim, H., Shi, X., Abeysirigunawardena, S.C., Jain, A., Singh, D., Aggarwal, V., Woodson, S.A., Ha, T., 2014. An improved surface passivation method for single-molecule studies. Nat. Methods 11, 1233–1236.

https://doi.org/10.1038/nmeth.3143

Huang, L.C., Wood, E.A., Cox, M.M., 1997. Convenient and reversible site-specific targeting of exogenous DNA into a bacterial chromosome by use of the FLP recombinase: the FLIRT system. J. Bacteriol. 179, 6076–6083. https://doi.org/10.1128/jb.179.19.6076-6083.1997

Jergic, S., Horan, N.P., Elshenawy, M.M., Mason, C.E., Urathamakul, T., Ozawa, K., Robinson, A., Goudsmits, J.M.H., Wang, Y., Pan, X., Beck, J.L., van Oijen, A.M., Huber, T.,

Hamdan, S.M., Dixon, N.E., 2013. A direct proofreader–clamp interaction stabilizes the Pol III replicase in the polymerization mode. EMBO J. 32, 1322–1333.

https://doi.org/10.1038/emboj.2012.347

Jergic, S., Ozawa, K., Williams, N.K., Su, X.-C., Scott, D.D., Hamdan, S.M., Crowther, J.A, Otting, G., Dixon, N.E., 2007. The unstructured C-terminus of the  subunit of

Escherichia coli DNA polymerase III holoenzyme is the site of interaction with the 

subunit. Nucleic Acids Res. 35, 2813–2824. https://doi.org/10.1093/nar/gkm079 Jeruzalmi, D., O’Donnell, M., Kuriyan, J., 2001. Crystal structure of the processivity clamp

loader gamma () complex of E. coli DNA polymerase III. Cell 106, 429–441. https://doi.org/10.1016/S0092-8674(01)00463-9

Jezewska, M.J., Kim, U.S., Bujalowski, W., 1996. Interactions of Escherichia coli primary replicative helicase DnaB protein with nucleotide cofactors. Biophys. J. 71, 2075– 2086. https://doi.org/10.1016/S0006-3495(96)79406-7

Jo, K., Dhingra, D.M., Odijk, T., de Pablo, J.J., Graham, M.D., Runnheim, R., Forrest, D., Schwartz, D.C., 2007. A single-molecule barcoding system using nanoslits for DNA

(11)

194

analysis. Proc. Natl. Acad. Sci. U. S. A. 104, 2673–2678. https://doi.org/10.1073/pnas.0611151104

Johnson, A., O’Donnell, M., 2005. Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 74, 283–315.

Johnson, D.S., Bai, L., Smith, B.Y., Patel, S.S., Wang, M.D., 2007. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129, 1299– 1309. https://doi.org/10.1016/j.cell.2007.04.038

Johnson, S.K., Bhattacharyya, S., Griep, M.A., 2000. DnaB helicase stimulates primer synthesis activity on short oligonucleotide templates. Biochemistry 39, 736–744. https://doi.org/10.1021/bi991554l

Jones, C.E., Green, E.M., Stephens, J.A., Mueser, T.C., Nossal, N.G., 2004. Mutations of bacteriophage T4 59 helicase loader defective in binding fork DNA and in interactions with T4 32 single-stranded DNA-binding protein. J. Biol. Chem. 279, 25721–25728. https://doi.org/10.1074/jbc.M402128200

Joyce, C.M., Benkovic, S.J., 2004. DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry 43, 14317–14324. https://doi.org/10.1021/bi048422z Jun, Y., Tripathy, S.K., Narayanareddy, B.R.J., Mattson-Hoss, M.K., Gross, S.P., 2014.

Calibration of optical tweezers for in vivo force measurements: how do different approaches compare? Biophys. J. 107, 1474–1484.

https://doi.org/10.1016/j.bpj.2014.07.033

Kalkman, G.A., Zhang, Y., Monachino, E., Mathwig, K., Kamminga, M.E., Pourhossein, P., Oomen, P.E., Stratmann, S.A., Zhao, Z., van Oijen, A.M., Verpoorte, E., Chiechi, R.C., 2016. Bisecting microfluidic channels with metallic nanowires fabricated by nanoskiving. ACS Nano 10, 2852–2859. https://doi.org/10.1021/acsnano.5b07996 Kamsma, D., Creyghton, R., Sitters, G., Wuite, G.J.L., Peterman, E.J.G., 2016. Tuning the

music: acoustic force spectroscopy (AFS) 2.0. Methods 105, 26–33. https://doi.org/10.1016/j.ymeth.2016.05.002

Kelman, Z., O’Donnell, M., 1995. DNA polymerase III holoenzyme: structure and function of a chromosomal replicating machine. Annu. Rev. Biochem. 64, 171–200.

https://doi.org/10.1146/annurev.bi.64.070195.001131

Kelman, Z., Yuzhakov, A., Andjelkovic, J., O’Donnell, M., 1998. Devoted to the lagging strand–the  subunit of DNA polymerase III holoenzyme contacts SSB to promote processive elongation and sliding clamp assembly. EMBO J. 17, 2436–2449. https://doi.org/10.1093/emboj/17.8.2436

Kim, S., Blainey, P.C., Schroeder, C.M., Xie, X.S., 2007. Multiplexed single-molecule assay for enzymatic activity on flow-stretched DNA. Nat. Methods 4, 397–399.

https://doi.org/10.1038/nmeth1037

Kim, S., Dallmann, H.G., McHenry, C.S., Marians, K.J., 1996. Coupling of a replicative polymerase and helicase: a –DnaB interaction mediates rapid replication fork movement. Cell 84, 643–650. https://doi.org/10.1016/S0092-8674(00)81039-9 Kobayashi, S., Iwamoto, M., Haraguchi, T., 2016. Live correlative light-electron microscopy

to observe molecular dynamics in high resolution. Reprod. Syst. Sex. Disord. 65, 296– 308. https://doi.org/10.1093/jmicro/dfw024

Kodaira, M., Biswas, S.B., Kornberg, A., 1983. The dnaX gene encodes the DNA polymerase III holoenzyme  subunit, precursor of the  subunit, the dnaZ gene product. Mol.

(12)

195

Kodera, N., Yamamoto, D., Ishikawa, R., Ando, T., 2010. Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468, 72–76.

https://doi.org/10.1038/nature09450

Kong, X.P., Onrust, R., O’Donnell, M., Kuriyan, J., 1992. Three-dimensional structure of the  subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69, 425– 437.

Kornberg, A., Baker, T.A., 1991. DNA replication, second edition. Trends Biochem. Sci. 17, 47. https://doi.org/10.1016/0968-0004(92)90431-8

Kulczyk, A.W., Tanner, N.A., Loparo, J.J., Richardson, C.C., van Oijen, A.M., 2010. Direct observation of enzymes replicating DNA using a single-molecule DNA stretching assay.

J. Vis. Exp. e1689. https://doi.org/10.3791/1689

Kural, C., Kim, H., Syed, S., Goshima, G., Gelfand, V.I., Selvin, P.R., 2005. Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308, 1469–1472. https://doi.org/10.1126/science.1108408

Kurth, I., O’Donnell, M., 2013. New insights into replisome fluidity during chromosome replication. Trends Biochem. Sci. 38, 195–203.

https://doi.org/10.1016/j.tibs.2012.10.003

Langston, L.D., Zhang, D., Yurieva, O., Georgescu, R.E., Finkelstein, J., Yao, N.Y., Indiani, C., O’Donnell, M.E., 2014. CMG helicase and DNA polymerase ε form a functional 15-subunit holoenzyme for eukaryotic leading-strand DNA replication. Proc. Natl. Acad.

Sci. U. S. A. 111, 15390–15395. https://doi.org/10.1073/pnas.1418334111

Lee, J.-B., Hite, R.K., Hamdan, S.M., Xie, X.S., Richardson, C.C., van Oijen, A.M., 2006. DNA primase acts as a molecular brake in DNA replication. Nature 439, 621–624. https://doi.org/10.1038/nature04317

Lee, J., Chastain, P.D., Kusakabe, T., Griffith, J.D., Richardson, C.C., 1998. Coordinated leading and lagging strand DNA synthesis on a minicircular template. Mol. Cell 1, 1001–1010. https://doi.org/10.1016/S1097-2765(00)80100-8

Lee, J.Y., Finkelstein, I.J., Crozat, E., Sherratt, D.J., Greene, E.C., 2012a. Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK. Proc. Natl. Acad. Sci. U. S. A. 109, 6531–6536.

Lee, J.Y., Greene, E.C., 2011. Assembly of recombinant nucleosomes on nanofabricated DNA curtains for single-molecule imaging. Methods Mol. Biol. 778, 243–258.

https://doi.org/10.1007/978-1-61779-261-8_16

Lee, J.Y., Wang, F., Fazio, T., Wind, S., Greene, E.C., 2012b. Measuring intermolecular rupture forces with a combined TIRF-optical trap microscope and DNA curtains.

Biochem. Biophys. Res. Commun. 426, 565–570.

https://doi.org/10.1016/j.bbrc.2012.08.127

Leu, F.P., Georgescu, R., O’Donnell, M., 2003. Mechanism of the E. coli  processivity switch during lagging-strand synthesis. Mol. Cell 11, 315–327.

https://doi.org/10.1016/S1097-2765(03)00042-X

Lewis, J.S., Jergic, S., Dixon, N.E., 2016. The E. coli DNA Replication Fork. Enzym. 39, 31–88. https://doi.org/10.1016/bs.enz.2016.04.001

Lewis, J.S., Spenkelink, L.M., Jergic, S., Wood, E.A., Monachino, E., Horan, N.P., Duderstadt, K.E., Cox, M.M., Robinson, A., Dixon, N.E., van Oijen, A.M., 2017. Single-molecule visualization of fast polymerase turnover in the bacterial replisome. eLife 6, e23932. https://doi.org/10.7554/eLife.23932

(13)

196

Li, H., Linke, W.A., Oberhauser, A.F., Carrion-Vazquez, M., Kerkvliet, J.G., Lu, H., Marszalek, P.E., Fernandez, J.M., 2002. Reverse engineering of the giant muscle protein titin.

Nature 418, 998–1002. https://doi.org/10.1038/nature00938

Lipomi, D.J., Chiechi, R.C., Dickey, M.D., Whitesides, G.M., 2008a. Fabrication of conjugated polymer nanowires by edge lithography. Nano Lett. 8, 2100–2105.

https://doi.org/10.1021/nl8009318

Lipomi, D.J., Chiechi, R.C., Reus, W.F., Whitesides, G.M., 2008b. Laterally ordered bulk heterojunction of conjugated polymers: nanoskiving a jelly roll. Adv. Funct. Mater. 18, 3469–3477. https://doi.org/10.1002/adfm.200800578

Lipomi, D.J., Ilievski, F., Wiley, B.J., Deotare, P.B., Lončar, M., Whitesides, G.M., 2009. Integrated fabrication and magnetic positioning of metallic and polymeric nanowires embedded in thin epoxy slabs. ACS Nano 3, 3315–3325.

https://doi.org/10.1021/nn901002q

Lipomi, D.J., Kats, M.A., Kim, P., Kang, S.H., Aizenberg, J., Capasso, F., Whitesides, G.M., 2010a. Fabrication and replication of arrays of single- or multicomponent nanostructures by replica molding and mechanical sectioning. ACS Nano 4, 4017– 4026. https://doi.org/10.1021/nn100993t

Lipomi, D.J., Martinez, R.V., Rioux, R.M., Cademartiri, L., Reus, W.F., Whitesides, G.M., 2010b. Survey of materials for nanoskiving and influence of the cutting process on the nanostructures produced. ACS Appl. Mater. Interfaces 2, 2503–2514.

https://doi.org/10.1021/am100434g

Lipomi, D.J., Martinez, R.V., Whitesides, G.M., 2011. Use of thin sectioning (nanoskiving) to fabricate nanostructures for electronic and optical applications. Angew. Chemie Int.

Ed. 50, 8566–8583. https://doi.org/10.1002/anie.201101024

Loparo, J.J., Kulczyk, A.W., Richardson, C.C., van Oijen, A.M., 2011. Simultaneous single-molecule measurements of phage T7 replisome composition and function reveal the mechanism of polymerase exchange. Proc. Natl. Acad. Sci. U. S. A. 108, 3584–3589. https://doi.org/10.1073/pnas.1018824108

Loscha, K., Oakley, A.J., Bancia, B., Schaeffer, P.M., Prosselkov, P., Otting, G., Wilce, M.C.J., Dixon, N.E., 2004. Expression, purification, crystallization, and NMR studies of the helicase interaction domain of Escherichia coli DnaG primase. Protein Expr. Purif. 33, 304–310. https://doi.org/10.1016/j.pep.2003.10.001

Love, C.A., Lilley, P.E., Dixon, N.E., 1996. Stable high-copy-number bacteriophage 

promoter vectors for overproduction of proteins in Escherichia coli. Gene 176, 49–53. https://doi.org/10.1016/0378-1119(96)00208-9

Loveland, A.B., Habuchi, S., Walter, J.C., van Oijen, A.M., 2012. A general approach to break the concentration barrier in single-molecule imaging. Nat. Methods 9, 987–992. https://doi.org/10.1038/nmeth.2174

Lyubchenko, Y.L., Shlyakhtenko, L.S., 2016. Imaging of DNA and protein–DNA complexes with atomic force microscopy. Crit. Rev. Eukaryot. Gene Expr. 26, 63–96.

https://doi.org/10.1615/CritRevEukaryotGeneExpr.v26.i1.70

MacLean, R.C., Torres-Barceló, C., Moxon, R., 2013. Evaluating evolutionary models of stress-induced mutagenesis in bacteria. Nat. Rev. Genet. 14, 221–227.

https://doi.org/10.1038/nrg3415

Mahamid, J., Pfeffer, S., Schaffer, M., Villa, E., Danev, R., Cuellar, L.K., Förster, F., Hyman, A.A., Plitzko, J.M., Baumeister, W., 2016. Visualizing the molecular sociology at the HeLa cell nuclear periphery. Science 351, 969–972.

(14)

197

https://doi.org/10.1126/science.aad8857

Maier, B., Bensimon, D., Croquette, V., 2000. Replication by a single DNA polymerase of a stretched single-stranded DNA. Proc. Natl. Acad. Sci. U. S. A. 97, 12002–12007. https://doi.org/10.1073/pnas.97.22.12002

Maki, H., Kornberg, A., 1985. The polymerase subunit of DNA polymerase III of Escherichia

coli. II. Purification of the  subunit, devoid of nuclease activities. J. Biol. Chem. 260,

12987–12992.

Mallik, R., Carter, B.C., Lex, S.A., King, S.J., Gross, S.P., 2004. Cytoplasmic dynein functions as a gear in response to load. Nature 427, 649–52. https://doi.org/10.1038/nature02293 Manhart, C.M., McHenry, C.S., 2013. The PriA replication restart protein blocks replicase

access prior to helicase assembly and directs template specificity through its ATPase activity. J. Biol. Chem. 288, 3989–3999. https://doi.org/10.1074/jbc.M112.435966 Manosas, M., Spiering, M.M., Ding, F., Croquette, V., Benkovic, S.J., 2012. Collaborative

coupling between polymerase and helicase for leading-strand synthesis. Nucleic Acids

Res. 40, 6187–6198. https://doi.org/10.1093/nar/gks254

Manosas, M., Spiering, M.M., Zhuang, Z., Benkovic, S.J., Croquette, V., 2009. Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome. Nat.

Chem. Biol. 5, 904–912. https://doi.org/10.1038/nchembio.236

Marko, J.F., Siggia, E.D., 1995. Stretching DNA. Macromolecules 28, 8759–8770. https://doi.org/10.1021/ma00130a008

Mason, C.E., Jergic, S., Lo, A.T.Y., Wang, Y., Dixon, N.E., Beck, J.L., 2013. Escherichia coli single-stranded DNA-binding protein: nanoESI-MS studies of salt-modulated subunit exchange and DNA binding transactions. J. Am. Soc. Mass Spectrom. 24, 274–285. https://doi.org/10.1007/s13361-012-0552-2

Mays, R.L., Pourhossein, P., Savithri, D., Genzer, J., Chiechi, R.C., Dickey, M.D., 2013. Thiol-containing polymeric embedding materials for nanoskiving. J. Mater. Chem. C 1, 121– 130. https://doi.org/10.1039/C2TC00030J

McHenry, C.S., Crow, W., 1979. DNA polymerase III of Escherichia coli. Purification and identification of subunits. J. Biol. Chem. 254, 1748–1753.

McInerney, P., Johnson, A., Katz, F., O’Donnell, M., 2007. Characterization of a triple DNA polymerase replisome. Mol. Cell 27, 527–538.

McInerney, P., O’Donnell, M., 2004. Functional uncoupling of twin polymerases: mechanism of polymerase dissociation from a lagging-strand block. J. Biol. Chem. 279, 21543– 21551. https://doi.org/10.1074/jbc.M401649200

Mehta, A.D., Rief, M., Spudich, J.A., Smith, D.A., Simmons, R.M., 1999. Single-molecule biomechanics with optical methods. Science 283, 1689–1695.

https://doi.org/10.1126/science.283.5408.1689

Merk, A., Bartesaghi, A., Banerjee, S., Falconieri, V., Rao, P., Davis, M.I., Pragani, R., Boxer, M.B., Earl, L.A., Milne, J.L.S., Subramaniam, S., 2016. Breaking cryo-EM resolution barriers to facilitate drug discovery. Cell 165, 1698–1707.

Miescher, F., 1871. Ueber die chemische Zusammensetzung der Eiterzellen. Mitkova, A. V., Khopde, S.M., Biswas, S.B., 2003. Mechanism and stoichiometry of

interaction of DnaG primase with DnaB helicase of Escherichia coli in RNA primer synthesis. J. Biol. Chem. 278, 52253–52261. https://doi.org/10.1074/jbc.M308956200 Moerner, W.E., Fromm, D.P., 2003. Methods of single-molecule fluorescence spectroscopy

(15)

198

and microscopy. Rev. Sci. Instrum. 74, 3597–3619. https://doi.org/10.1063/1.1589587 Mok, M., Marians, K.J., 1987. The Escherichia coli preprimosome and DNA B helicase can

form replication forks that move at the same rate. J. Biol. Chem. 262, 16644–16654. Monachino, E., Spenkelink, L.M., van Oijen, A.M., 2017. Watching cellular machinery in

action, one molecule at a time. J. Cell Biol. 216, 41–51. https://doi.org/10.1083/jcb.201610025

Monachino, E., Ghodke, H., Spinks, R.R., Hoatson, B.S., Jergic, S., Xu, Z.-Q., Dixon, N.E., van Oijen, A.M., 2018. Design of DNA rolling-circle templates with controlled fork topology to study mechanisms of DNA replication. Anal. Biochem. 557, 42–45. https://doi.org/10.1016/j.ab.2018.07.008

Mori, T., Vale, R.D., Tomishige, M., 2007. How kinesin waits between steps. Nature 450, 750–754. https://doi.org/10.1038/nature06346

Müller, D.J., Dufrêne, Y.F., 2011. Force nanoscopy of living cells. Curr. Biol. 21, R212–R216. https://doi.org/10.1016/j.cub.2011.01.046

Mullin, D.A., Woldringh, C.L., Henson, J.M., Walker, J.R., 1983. Cloning of the Escherichia

coli dnaZX region and identification of its products. Mol. Gen. Genet. 192, 73–79.

Myler, L.R., Gallardo, I.F., Zhou, Y., Gong, F., Yang, S.-H., Wold, M.S., Miller, K.M., Paull, T.T., Finkelstein, I.J., 2016. Single-molecule imaging reveals the mechanism of Exo1 regulation by single-stranded DNA binding proteins. Proc. Natl. Acad. Sci. U. S. A. 113, E1170–E1179. https://doi.org/10.1073/pnas.1516674113

Nakayama, N., Arai, N., Kaziro, Y., Arai, K., 1984. Structural and functional studies of the

dnaB protein using limited proteolysis. Characterization of domains for

DNA-dependent ATP hydrolysis and for protein association in the primosome. J. Biol. Chem.

259, 88–96.

Naktinis, V., Turner, J., O’Donnell, M., 1996. A molecular switch in a replication machine defined by an internal competition for protein rings. Cell 84, 137–145.

https://doi.org/10.1016/S0092-8674(00)81000-4

Nan, X., Sims, P.A., Xie, X.S., 2008. Organelle tracking in a living cell with microsecond time resolution and nanometer spatial precision. ChemPhysChem 9, 707–712.

https://doi.org/10.1002/cphc.200700839

Nelson, D.L., Cox, M.M., 2008. Principles of Biochemistry, V edition. ed. Lehninger. Neuman, K.C., Chadd, E.H., Liou, G.F., Bergman, K., Block, S.M., 1999. Characterization of

photodamage to Escherichia coli in optical traps. Biophys. J. 77, 2856–2863. https://doi.org/10.1016/S0006-3495(99)77117-1

Neuman, K.C., Nagy, A., 2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5, 491–505. https://doi.org/10.1038/nmeth.1218

Neylon, C., Brown, S.E., Kralicek, A.V., Miles, C.S., Love, C.A., Dixon, N.E., 2000. Interaction of the Escherichia coli replication terminator protein (Tus) with DNA: a model derived from DNA-binding studies of mutant proteins by surface plasmon resonance.

Biochemistry 39, 11989–11999. https://doi.org/10.1021/bi001174w

Oakley, A.J., Loscha, K.V., Schaeffer, P.M., Liepinsh, E., Pintacuda, G., Wilce, M.C.J., Otting, G., Dixon, N.E., 2005. Crystal and solution structures of the helicase-binding domain of Escherichia coli primase. J. Biol. Chem. 280, 11495–11504.

https://doi.org/10.1074/jbc.M412645200

Oakley, A.J., Prosselkov, P., Wijffels, G., Beck, J.L., Wilce, M.C.J., Dixon, N.E., 2003. Flexibility revealed by the 1.85 Å crystal structure of the  sliding-clamp subunit of Escherichia

(16)

199

coli DNA polymerase III. Acta Crystallogr. D. Biol. Crystallogr. 59, 1192–1199.

https://doi.org/10.1107/S0907444903009958

Ober, R.J., Ram, S., Ward, E.S., 2004. Localization accuracy in single-molecule microscopy.

Biophys. J. 86, 1185–1200. https://doi.org/10.1016/S0006-3495(04)74193-4

Oesterhelt, F., Oesterhelt, D., Pfeiffer, M., Engel, A., Gaub, H.E., Müller, D.J., 2000. Unfolding pathways of individual bacteriorhodopsins. Science 288, 143–146. https://doi.org/10.1126/science.288.5463.143

Okazaki, R., Okazaki, T., Sakabe, K., Sugimoto, K., Sugino, A., 1968. Mechanism of DNA chain growth. I. Possible discontinuity and unusual secondary structure of newly

synthesized chains. Proc. Natl. Acad. Sci. U. S. A. 59, 598–605. https://doi.org/10.1073/pnas.59.2.598

Olson, M.W., Dallmann, H.G., McHenry, C.S., 1995. DnaX complex of Escherichia coli DNA polymerase III holoenzyme. The  complex functions by increasing the affinity of  and  for ’ to a physiologically relevant range. J. Biol. Chem. 270, 29570–29577. https://doi.org/10.1074/jbc.270.49.29570

Onrust, R., Finkelstein, J., Naktinis, V., Turner, J., Fang, L., O’Donnell, M., 1995a. Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. I. Organization of the clamp loader. J. Biol.

Chem. 270, 13348–13357. https://doi.org/10.1074/jbc.270.22.13348

Onrust, R., Finkelstein, J., Turner, J., Naktinis, V., O’Donnell, M., 1995b. Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. III. Interface between two polymerases and the clamp loader. J. Biol. Chem. 270, 13366–13377.

https://doi.org/10.1074/jbc.270.22.13366

Onuchic, J.N., Luthey-Schulten, Z., Wolynes, P.G., 1997. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48, 545–600.

https://doi.org/10.1146/annurev.physchem.48.1.545

Orrit, M., Bernard, J., 1990. Single pentacene molecules detected by fluorescence excitation in a p-terphenyl crystal. Phys. Rev. Lett. 65, 2716–2719.

https://doi.org/10.1103/PhysRevLett.65.2716

Ozawa, K., Horan, N.P., Robinson, A., Yagi, H., Hill, F.R., Jergic, S., Xu, Z.-Q., Loscha, K.V., Li, N., Tehei, M., Oakley, A.J., Otting, G., Huber, T., Dixon, N.E., 2013. Proofreading exonuclease on a tether: the complex between the E. coli DNA polymerase III subunits , epsilon,  and  reveals a highly flexible arrangement of the proofreading domain.

Nucleic Acids Res. 41, 5354–5367. https://doi.org/10.1093/nar/gkt162

Ozawa, K., Jergic, S., Crowther, J.A., Thompson, P.R., Wijffels, G., Otting, G., Dixon, N.A., 2005. Cell-free protein synthesis in an autoinduction system for NMR studies of protein–protein interactions. J. Biomol. NMR 32, 235–241.

https://doi.org/10.1007/s10858-005-7946-4

Pandey, M., Syed, S., Donmez, I., Patel, G., Ha, T., Patel, S.S., 2009. Coordinating DNA replication by means of priming loop and differential synthesis rate. Nature 462, 940– 943. https://doi.org/10.1038/nature08611

Park, A.Y., Jergic, S., Politis, A., Ruotolo, B.T., Hirshberg, D., Jessop, L.L., Beck, J.L., Barsky, D., O’Donnell, M., Dixon, N.E., Robinson, C.V., 2010. A single subunit directs the assembly of the Escherichia coli DNA sliding clamp loader. Structure 18, 285–292.

https://doi.org/10.1016/j.str.2010.01.009

(17)

200

https://doi.org/10.1074/jbc.R600008200

Peterman, E.J.G., Sosa, H., Moerner, W.E., 2004. Single-molecule fluorescence spectroscopy and microscopy of biomolecular motors. Annu. Rev. Phys. Chem. 55, 79–96.

https://doi.org/10.1146/annurev.physchem.55.091602.094340

Petrov, A., Grosely, R., Chen, J., O’Leary, S.E., Puglisi, J.D., 2016. Multiple parallel pathways of translation initiation on the CrPV IRES. Mol. Cell 62, 92–103.

Pomerantz, R.T., O’Donnell, M., 2010. Direct restart of a replication fork stalled by a head-on RNA polymerase. Science 327, 590–592. https://doi.org/10.1126/science.1179595 Pourhossein, P., Chiechi, R.C., 2013. Fabricating nanogaps by nanoskiving. J. Vis. Exp.

https://doi.org/10.3791/50406

Pourhossein, P., Chiechi, R.C., 2012. Directly addressable bub-3 nm gold nanogaps

fabricated by nanoskiving using self-assembled monolayers as templates. ACS Nano 6, 5566–5573. https://doi.org/10.1021/nn301510x

Prasad, T.K., Yeykal, C.C., Greene, E.C., 2006. Visualizing the assembly of human Rad51 filaments on double-stranded DNA. J. Mol. Biol. 363, 713–728.

https://doi.org/10.1016/j.jmb.2006.08.046

Predki, P.F., Elkin, C., Kapur, H., Jett, J., Lucas, S., Glavina, T., Hawkins, T., 2004. Rolling circle amplification for sequencing templates, in: Zhao, S., Stodolsky, M. (Eds.), Bacterial

Artificial Chromosomes: Volume 1 Library Construction, Physical Mapping, and Sequencing. Springer, Totowa, NJ, pp. 189–196.

https://doi.org/10.1385/1-59259-752-1:189

Pritchard, A.E., Dallmann, H.G., Glover, B.P., McHenry, C.S., 2000. A novel assembly mechanism for the DNA polymerase III holoenzyme DnaX complex: association of ’

with DnaX4 forms DnaX3’. EMBO J. 19, 6536–6545.

https://doi.org/10.1093/emboj/19.23.6536

Qi, Z., Greene, E.C., 2016. Visualizing recombination intermediates with single-stranded DNA curtains. Methods 105, 62–74. https://doi.org/10.1016/j.ymeth.2016.03.027 Rasnik, I., Myong, S., Cheng, W., Lohman, T.M., Ha, T., 2004. DNA-binding orientation and

domain conformation of the E. coli Rep helicase monomer bound to a partial duplex junction: single-molecule studies of fluorescently labeled enzymes. J. Mol. Biol. 336, 395–408. https://doi.org/10.1016/j.jmb.2003.12.031

Renault, J.P., Bernard, A., Bietsch, A., Michel, B., Bosshard, H.R., Delamarche, E., Kreiter, M., Hecht, B., Wild, U.P., 2003. Fabricating arrays of single protein molecules on glass using microcontact printing. J. Phys. Chem. B 107, 703–711.

https://doi.org/10.1021/jp0263424

Reyes-Lamothe, R., Sherratt, D.J., Leake, M.C., 2010. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328, 498–501. https://doi.org/10.1126/science.1185757

Roberts, R.J., Carneiro, M.O., Schatz, M.C., 2013. The advantages of SMRT sequencing.

Genome Biol. 14, 405. https://doi.org/10.1186/gb-2013-14-6-405

Robinson, A., McDonald, J.P., Caldas, V.E.A., Patel, M., Wood, E.A., Punter, C.M., Ghodke, H., Cox, M.M., Woodgate, R., Goodman, M.F., van Oijen, A.M., 2015. Regulation of mutagenic DNA polymerase V activation in space and time. PLoS Genet. 11, e1005482. https://doi.org/10.1371/journal.pgen.1005482

Robinson, A., van Oijen, A.M., 2013. Bacterial replication, transcription and translation: mechanistic insights from single-molecule biochemical studies. Nat. Rev. Microbiol.

(18)

201

11, 303–315. https://doi.org/10.1038/nrmicro2994

Robinson, C.V., Sali, A., Baumeister, W., 2007. The molecular sociology of the cell. Nature

Robison, A.D., Finkelstein, I.J., 2014a. High-throughput single-molecule studies of protein– DNA interactions. FEBS Lett. 588, 3539–3546.

https://doi.org/10.1016/j.febslet.2014.05.021

Robison, A.D., Finkelstein, I.J., 2014b. Rapid prototyping of multichannel microfluidic devices for single-molecule DNA curtain imaging. Anal. Chem. 86, 4157–4163. https://doi.org/10.1021/ac500267v

Rowen, L., Kornberg, A., 1978. Primase, the dnaG protein of Escherichia coli. An enzyme which starts DNA chains. J. Biol. Chem. 253, 758–764.

Sadegh Cheri, M., Latifi, H., Sadeghi, J., Salehi Moghaddam, M., Shahraki, H., Hajghassem, H., 2014. Real-time measurement of flow rate in microfluidic devices using a cantilever-based optofluidic sensor. Analyst 139, 431–438.

https://doi.org/10.1039/C3AN01588B

San Martin, M.C., Stamford, N.P., Dammerova, N., Dixon, N.E., Carazo, J.M., 1995. A structural model for the Escherichia coli DnaB helicase based on electron microscopy data. J. Struct. Biol. 114, 167–176. https://doi.org/10.1006/jsbi.1995.1016

Santos, S., Barcons, V., Christenson, H.K., Billingsley, D.J., Bonass, W.A., Font, J., Thomson, N.H., 2013. Stability, resolution, and ultra-low wear amplitude modulation atomic force microscopy of DNA: small amplitude small set-point imaging. Appl. Phys. Lett.

103, 63702. https://doi.org/10.1063/1.4817906

Sartori, A., Gatz, R., Beck, F., Rigort, A., Baumeister, W., Plitzko, J.M., 2007. Correlative microscopy: bridging the gap between fluorescence light microscopy and cryo-electron tomography. J. Struct. Biol. 160, 135–145.

https://doi.org/10.1016/j.jsb.2007.07.011

Schermerhorn, K.M., Tanner, N., Kelman, Z., Gardner, A.F., 2016. High-temperature single-molecule kinetic analysis of thermophilic archaeal MCM helicases. Nucleic Acids Res.

44, 8764–8771. https://doi.org/10.1093/nar/gkw612

Scheuermann, R.H., Echols, H., 1984. A separate editing exonuclease for DNA replication: the  subunit of Escherichia coli DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci.

U. S. A. 81, 7747–7751. https://doi.org/10.1073/pnas.81.24.7747

Schöler, L., Lange, B., Seibel, K., Schäfer, H., Walder, M., Friedrich, N., Ehrhardt, D., Schönfeld, F., Zech, G., Böhm, M., 2005. Monolithically integrated micro flow sensor for lab-on-chip applications. Microelectron. Eng. 78–79, 164–170.

https://doi.org/10.1016/j.mee.2004.12.022

Schröder, C.H., Erben, E., Kaerner, H.C., 1973. A rolling circle model of the in vivo replication of bacteriophage X174 replicative form DNA: different fate of two types of progeny replicative form. J. Mol. Biol. 79, 599–613.

https://doi.org/10.1016/0022-2836(73)90066-1

Sharonov, A., Hochstrasser, R.M., 2006. Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc. Natl. Acad. Sci. U. S. A. 103, 18911–18916. https://doi.org/10.1073/pnas.0609643104

Shereda, R.D., Kozlov, A.G., Lohman, T.M., Cox, M.M., Keck, J.L., 2008. SSB as an

organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol.

43, 289–318. https://doi.org/10.1080/10409230802341296

(19)

202

single-molecule level using DNA curtains. DNA Repair (Amst). 20, 94–109. https://doi.org/10.1016/j.dnarep.2014.02.004

Simonetta, K.R., Kazmirski, S.L., Goedken, E.R., Cantor, A.J., Kelch, B.A., McNally, R., Seyedin, S.N., Makino, D.L., O’Donnell, M., Kuriyan, J., 2009. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 137, 659–671.

Sims, P.A., Xie, X.S., 2009. Probing dynein and kinesin stepping with mechanical manipulation in a living cell. ChemPhysChem 10, 1511–1516.

Sindelar, C.V., Downing, K.H., 2010. An atomic-level mechanism for activation of the kinesin molecular motors. Proc. Natl. Acad. Sci. U. S. A. 107, 4111–4116.

Sing, C.E., Olvera de la Cruz, M., Marko, J.F., 2014. Multiple-binding-site mechanism explains concentration-dependent unbinding rates of DNA-binding proteins. Nucleic

Acids Res. 42, 3783–3791. https://doi.org/10.1093/nar/gkt1327

Singleton, P., 1999. Bacteria in Biology, Biotechnology and Medicine.

Sinha, N.K., Morris, C.F., Alberts, B.M., 1980. Efficient in vitro replication of double-stranded DNA templates by a purified T4 bacteriophage replication system. J. Biol. Chem. 255, 4290–4293.

Sitters, G., Kamsma, D., Thalhammer, G., Ritsch-Marte, M., Peterman, E.J.G., Wuite, G.J.L., 2015. Acoustic force spectroscopy. Nat. Methods 12, 47–50.

https://doi.org/10.1038/nmeth.3183

Smolina, I.V., Demidov, V.V., Cantor, C.R., Broude, N.E., 2004. Real-time monitoring of branched rolling-circle DNA amplification with peptide nucleic acid beacon. Anal.

Biochem. 335, 326–329. https://doi.org/10.1016/j.ab.2004.07.022

Smolina, I.V., Broude, N.E., 2015. Ultrasensitive detection of DNA and protein markers in cancer cells. Cancer Biol. Med. 12, 143–149. https://doi.org/10.7497/j.issn.2095-3941.2015.0048

Sperling, E., Hohlfeld, M., Mertig, M., 2015. Soft-lithographically fabricated nanofluidic channels for single-DNA measurements. Phys. status solidi 212, 1229–1233. https://doi.org/10.1002/pssa.201431915

Stamford, N.P., Lilley, P.E., Dixon, N.E., 1992. Enriched sources of Escherichia coli replication proteins. The dnaG primase is a zinc metalloprotein. Biochim. Biophys. Acta 1132, 17– 25. https://doi.org/10.1016/0167-4781(92)90047-4

Strycharska, M.S., Arias-Palomo, E., Lyubimov, A.Y., Erzberger, J.P., O’Shea, V.L., Bustamante, C.J., Berger, J.M., 2013. Nucleotide and partner-protein control of bacterial replicative helicase structure and function. Mol. Cell 52, 844–854. https://doi.org/10.1016/j.molcel.2013.11.016

Studier, F.W., Rosenberg, A.H., Dunn, J.J., Dubendorff, J.W., 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60–89. https://doi.org/10.1016/0076-6879(90)85008-C

Studwell-Vaughan, P.S., O’Donnell, M., 1993. DNA polymerase III accessory proteins. V.  encoded by holE. J. Biol. Chem. 268, 11785–11791.

Stukenberg, P.T., Studwell-Vaughan, P.S., O’Donnell, M., 1991. Mechanism of the sliding -clamp of DNA polymerase III holoenzyme. J. Biol. Chem. 266, 11328–11334.

Sustarsic, M., Kapanidis, A.N., 2015. Taking the ruler to the jungle: single-molecule FRET for understanding biomolecular structure and dynamics in live cells. Curr. Opin. Struct.

(20)

203

Biol. 34, 52–59. https://doi.org/10.1016/j.sbi.2015.07.001

Sutton, M.D., 2010. Coordinating DNA polymerase traffic during high and low fidelity synthesis. Biochim. Biophys. Acta 1804, 1167–1179.

https://doi.org/10.1016/j.bbapap.2009.06.010

Svoboda, K., Schmidt, C.F., Schnapp, B.J., Block, S.M., 1993. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365, 721–727.

https://doi.org/10.1038/365721a0

Taft-Benz, S.A., Schaaper, R.M., 2004. The  subunit of Escherichia coli DNA polymerase III: a role in stabilizing the  proofreading subunit. J. Bacteriol. 186, 2774–2780.

https://doi.org/10.1128/JB.186.9.2774-2780.2004

Tafvizi, A., Mirny, L.A., van Oijen, A.M., 2011. Dancing on DNA: kinetic aspects of search processes on DNA. ChemPhysChem 12, 1481–1489.

Tanner, N.A., Hamdan, S.M., Jergic, S., Loscha, K.V., Schaeffer, P.M., Dixon, N.E., van Oijen, A.M., 2008. Single-molecule studies of fork dynamics in Escherichia coli DNA replication. Nat. Struct. Mol. Biol. 15, 170–176. https://doi.org/10.1038/nsmb.1381 Tanner, N.A., Loparo, J.J., Hamdan, S.M., Jergic, S., Dixon, N.E., van Oijen, A.M., 2009.

Real-time single-molecule observation of rolling-circle DNA replication. Nucleic Acids Res.

37, e27. https://doi.org/10.1093/nar/gkp006

Tanner, N.A., Tolun, G., Loparo, J.J., Jergic, S., Griffith, J.D., Dixon, N.E., van Oijen, A.M., 2011. E. coli DNA replication in the absence of free  clamps. EMBO J. 30, 1830–1840. https://doi.org/10.1038/emboj.2011.84

Tanner, N.A., van Oijen, A.M., 2010. Visualizing DNA replication at the single-molecule level, in: Walters, N.G. (Ed.), Single Molecule Tools, Part B: Super-Resolution, Particle

Tracking, Multiparameter, and Force Based Methods, Volume 475. Academic Press,

pp. 259–278. https://doi.org/10.1016/S0076-6879(10)75011-4

Tougu, K., Marians, K.J., 1996. The extreme C terminus of primase is required for interaction with DnaB at the replication fork. J. Biol. Chem. 271, 21391–21397.

https://doi.org/10.1074/jbc.271.35.21391

Tsuchihashi, Z., Kornberg, A., 1990. Translational frameshifting generates the  subunit of DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. U. S. A. 87, 2516–2520. Uemura, S., Aitken, C.E., Korlach, J., Flusberg, B.A., Turner, S.W., Puglisi, J.D., 2010.

Real-time tRNA transit on single translating ribosomes at codon resolution. Nature 464, 1012–1017. https://doi.org/10.1038/nature08925

van der Velde, J.H.M., Oelerich, J., Huang, J., Smit, J.H., Aminian Jazi, A., Galiani, S., Kolmakov, K., Guoridis, G., Eggeling, C., Herrmann, A., Roelfes, G., Cordes, T., 2016. A simple and versatile design concept for fluorophore derivatives with intramolecular photostabilization. Nat. Commun. 7, 10144. https://doi.org/10.1038/ncomms10144 van Oijen, A.M., 2011. Single-molecule approaches to characterizing kinetics of

biomolecular interactions. Curr. Opin. Biotechnol. 22, 75–80. https://doi.org/10.1016/j.copbio.2010.10.002

van Oijen, A.M., Blainey, P.C., Crampton, D.J., Richardson, C.C., Ellenberger, T., Xie, X.S., 2003. Single-molecule kinetics of  exonuclease reveal base dependence and dynamic disorder. Science 301, 1235–1238. https://doi.org/10.1126/science.1084387

van Oijen, A.M., Dixon, N.E., 2015. Probing molecular choreography through single-molecule biochemistry. Nat. Struct. Mol. Biol. 22, 948–952.