1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biophysics
  4. Volume 46, 2017
  5. Article

Annual Review of Biophysics

Volume 46, 2017

Single-Molecule Analysis of Bacterial DNA Repair and Mutagenesis

Abstract

Ubiquitous conserved processes that repair DNA damage are essential for the maintenance and propagation of genomes over generations. Then again, inaccuracies in DNA transactions and failures to remove mutagenic lesions cause heritable genome changes. Building on decades of research using genetics and biochemistry, unprecedented quantitative insight into DNA repair mechanisms has come from the new-found ability to measure single proteins in vitro and inside individual living cells. This has brought together biologists, chemists, engineers, physicists, and mathematicians to solve long-standing questions about the way in which repair enzymes search for DNA lesions and form protein complexes that act in DNA repair pathways. Furthermore, unexpected discoveries have resulted from capabilities to resolve molecular heterogeneity and cell subpopulations, provoking new questions about the role of stochastic processes in DNA repair and mutagenesis. These studies are leading to new technologies that will find widespread use in basic research, biotechnology, and medicine.

Keyword(s): atomic force microscopy, DNA repair, mutagenesis, single-molecule fluorescence, single-molecule force spectroscopy, super-resolution microscopy
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070816-034106
2017-05-22
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biophys/46/1/annurev-biophys-070816-034106.html?itemId=/content/journals/10.1146/annurev-biophys-070816-034106&mimeType=html&fmt=ahah

Literature Cited

  1. Allen DJ, Makhov A, Grilley M, Taylor J, Thresher R. 1.  et al. 1997. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J 16:144467–76 [Google Scholar]
  2. Amit R, Gileadi O, Stavans J. 2.  2004. Direct observation of RuvAB-catalyzed branch migration of single Holliday junctions. PNAS 101:3211605–10 [Google Scholar]
  3. Badrinarayanan A, Le TBK, Laub MT. 3.  2015. Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria. J. Cell Biol. 210:3385–400 [Google Scholar]
  4. Bakshi S, Dalrymple RM, Li W, Choi H, Weisshaar JC. 4.  2013. Partitioning of RNA polymerase activity in live Escherichia coli from analysis of single-molecule diffusive trajectories. Biophys. J. 105:122676–86 [Google Scholar]
  5. Batchelor E, Loewer A, Lahav G. 5.  2009. The ups and downs of p53: understanding protein dynamics in single cells. Nat. Rev. Cancer 9:5371–77 [Google Scholar]
  6. Beaber JW, Hochhut B, Waldor MK. 6.  2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427:696972–74 [Google Scholar]
  7. Belenky P, Ye JD, Porter CBM, Cohen NR, Lobritz MA. 7.  et al. 2015. Bactericidal antibiotics induce toxic metabolic perturbations that lead to cellular damage. Cell Rep 13:5968–80 [Google Scholar]
  8. Bell JC, Kowalczykowski SC. 8.  2016. Mechanics and single-molecule interrogation of DNA recombination. Annu. Rev. Biochem. 85:1193–226 [Google Scholar]
  9. Bell JC, Plank JL, Dombrowski CC, Kowalczykowski SC. 9.  2012. Direct imaging of RecA nucleation and growth on single molecules of SSB-coated ssDNA. Nature 491:7423274–78 [Google Scholar]
  10. Bianco PR, Brewer LR, Corzett M, Balhorn R, Yeh Y. 10.  et al. 2001. Processive translocation and unwinding by individual RecBCD enzyme molecules. Nature 409:6818374–78 [Google Scholar]
  11. Blainey PC, Oijen AMV, Banerjee A, Verdine GL, Xie XS. 11.  2006. A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. PNAS 103:155752–57 [Google Scholar]
  12. Carrasco C, Gilhooly NS, Dillingham MS, Moreno-Herrero F. 12.  2013. On the mechanism of recombination hotspot scanning during double-stranded DNA break resection. PNAS 110:28E2562–71 [Google Scholar]
  13. Chen L, Haushalter KA, Lieber CM, Verdine GL. 13.  2002. Direct visualization of a DNA glycosylase searching for damage. Chem. Biol. 9:3345–50 [Google Scholar]
  14. Christian TD, Romano LJ, Rueda D. 14.  2009. Single-molecule measurements of synthesis by DNA polymerase with base-pair resolution. PNAS 106:5021109–14 [Google Scholar]
  15. Clark TA, Spittle KE, Turner SW, Korlach J. 15.  2011. Direct detection and sequencing of damaged DNA bases. Genome Integr 2:10 [Google Scholar]
  16. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC. 16.  2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. . Genetics 158:141–64 [Google Scholar]
  17. Cox MM, Goodman MF, Kreuzer KN, Sherratt DJ, Sandler SJ, Marians KJ. 17.  2000. The importance of repairing stalled replication forks. Nature 404:677337–41 [Google Scholar]
  18. Crawford R, Torella JP, Aigrain L, Plochowietz A, Gryte K. 18.  et al. 2013. Long-lived intracellular single-molecule fluorescence using electroporated molecules. Biophys. J. 105:112439–50 [Google Scholar]
  19. Cristóvão M, Sisamakis E, Hingorani MM, Marx AD, Jung CP. 19.  et al. 2012. Single-molecule multiparameter fluorescence spectroscopy reveals directional MutS binding to mismatched bases in DNA. Nucleic Acids Res 40:125448–64 [Google Scholar]
  20. Dawid A, Croquette V, Grigoriev M, Heslot F. 20.  2004. Single-molecule study of RuvAB-mediated Holliday-junction migration. PNAS 101:3211611–16 [Google Scholar]
  21. Dessinges M-N, Lionnet T, Xi XG, Bensimon D, Croquette V. 21.  2004. Single-molecule assay reveals strand switching and enhanced processivity of UvrD. PNAS 101:176439–44 [Google Scholar]
  22. De Vlaminck I, van Loenhout MTJ, Zweifel L, den Blanken J, Hooning K. 22.  et al. 2012. Mechanism of homology recognition in DNA recombination from dual-molecule experiments. Mol. Cell 46:5616–24 [Google Scholar]
  23. Dillingham MS, Kowalczykowski SC. 23.  2008. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 72:4642–71 [Google Scholar]
  24. Dulin D, Berghuis BA, Depken M, Dekker NH. 24.  2015. Untangling reaction pathways through modern approaches to high-throughput single-molecule force-spectroscopy experiments. Curr. Opin. Struct. Biol. 34:116–22 [Google Scholar]
  25. Elez M, Murray AW, Bi L-J, Zhang X-E, Matic I, Radman M. 25.  2010. Seeing mutations in living cells. Curr. Biol. 20:161432–37 [Google Scholar]
  26. Elf J, Li G-W, Xie XS. 26.  2007. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316:58281191–94 [Google Scholar]
  27. Epshtein V, Kamarthapu V, McGary K, Svetlov V, Ueberheide B. 27.  et al. 2014. UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 505:7483372–77 [Google Scholar]
  28. Fan J, Leroux-Coyau M, Savery NJ, Strick TR. 28.  2016. Reconstruction of bacterial transcription-coupled repair at single-molecule resolution. Nature 536:7615234–37 [Google Scholar]
  29. Félix M-A, Barkoulas M. 29.  2015. Pervasive robustness in biological systems. Nat. Rev. Genet. 16:8483–96 [Google Scholar]
  30. Finkelstein IJ, Visnapuu M-L, Greene EC. 30.  2010. Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468:7326983–87 [Google Scholar]
  31. Forget AL, Kowalczykowski SC. 31.  2012. Single-molecule imaging of DNA pairing by RecA reveals a 3-dimensional homology search. Nature 482:7385423–27 [Google Scholar]
  32. Friedman N, Vardi S, Ronen M, Alon U, Stavans J. 32.  2005. Precise temporal modulation in the response of the SOS DNA repair network in individual bacteria. PLOS Biol 3:7e238 [Google Scholar]
  33. Fu D, Calvo JA, Samson LD. 33.  2012. Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat. Rev. Cancer 12:2104–20 [Google Scholar]
  34. Gahlmann A, Moerner WE. 34.  2013. Exploring bacterial cell biology with single-molecule tracking and super-resolution imaging. Nat. Rev. Microbiol. 12:19–22 [Google Scholar]
  35. Galhardo RS, Do R, Yamada M, Friedberg EC, Hastings PJ. 35.  et al. 2009. DinB upregulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. . Genetics 182:155–68 [Google Scholar]
  36. Gautier A, Juillerat A, Heinis C, Corrêa IR Jr., Kindermann M. 36.  et al. 2008. An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15:2128–36 [Google Scholar]
  37. Geertsema HJ, Schulte AC, Spenkelink LM, McGrath WJ, Morrone SR. 37.  et al. 2015. Single-molecule imaging at high fluorophore concentrations by local activation of dye. Biophys. J. 108:4949–56 [Google Scholar]
  38. Gorman J, Wang F, Redding S, Plys AJ, Fazio T. 38.  et al. 2012. Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair. PNAS 109:45E3074–83 [Google Scholar]
  39. Greene EC, Wind S, Fazio T, Gorman J, Visnapuu M-L. 39.  2010. DNA curtains for high-throughput single-molecule optical imaging. Methods Enzymol 472:293–315 [Google Scholar]
  40. Griffith J, Huberman JA, Kornberg A. 40.  1971. Electron microscopy of DNA polymerase bound to DNA. J. Mol. Biol. 55:2209–14 [Google Scholar]
  41. Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z. 41.  et al. 2015. A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat. Methods 12:3244–50 [Google Scholar]
  42. Gunawardena J. 42.  2014. Models in biology: “accurate descriptions of our pathetic thinking.”. BMC Biol 12:29 [Google Scholar]
  43. Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A. 43.  et al. 2013. β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat. Commun. 4:1610 [Google Scholar]
  44. Halford SE, Marko JF. 44.  2004. How do site-specific DNA-binding proteins find their targets?. Nucleic Acids Res 32:103040–52 [Google Scholar]
  45. Hammar P, Leroy P, Mahmutovic A, Marklund EG, Berg OG, Elf J. 45.  2012. The lac repressor displays facilitated diffusion in living cells. Science 336:60881595–98 [Google Scholar]
  46. Hinczewski M, Hyeon C, Thirumalai D. 46.  2016. Directly measuring single-molecule heterogeneity using force spectroscopy. PNAS 113:27E3852–61 [Google Scholar]
  47. Hohlbein J, Aigrain L, Craggs TD, Bermek O, Potapova O. 47.  et al. 2013. Conformational landscapes of DNA polymerase I and mutator derivatives establish fidelity checkpoints for nucleotide insertion. Nat. Commun. 4:2131 [Google Scholar]
  48. Howan K, Smith AJ, Westblade LF, Joly N, Grange W. 48.  et al. 2012. Initiation of transcription-coupled repair characterized at single-molecule resolution. Nature 490:7420431–34 [Google Scholar]
  49. Hsu PD, Lander ES, Zhang F. 49.  2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:61262–78 [Google Scholar]
  50. Huang B, Bates M, Zhuang X. 50.  2009. Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 78:1993–1016 [Google Scholar]
  51. Hughes CD, Simons M, Mackenzie CE, Van Houten B, Kad NM. 51.  2014. Single molecule techniques in DNA repair: a primer. DNA Repair 20:2–13 [Google Scholar]
  52. Hughes CD, Wang H, Ghodke H, Simons M, Towheed A. 52.  et al. 2013. Real-time single-molecule imaging reveals a direct interaction between UvrC and UvrB on DNA tightropes. Nucleic Acids Res 41:94901–12 [Google Scholar]
  53. Ibarra B, Chemla YR, Plyasunov S, Smith SB, Lázaro JM. 53.  et al. 2009. Proofreading dynamics of a processive DNA polymerase. EMBO J 28:182794–802 [Google Scholar]
  54. Jee J, Rasouly A, Shamovsky I, Akivis YR, Steinman S. 54.  et al. 2016. Rates and mechanisms of bacterial mutagenesis from maximum-depth sequencing. Nature 534:7609693–96 [Google Scholar]
  55. Jeong C, Cho W-K, Song K-M, Cook C, Yoon T-Y. 55.  et al. 2011. MutS switches between two fundamentally distinct clamps during mismatch repair. Nat. Struct. Mol. Biol. 18:3379–85 [Google Scholar]
  56. Jiang Y, Ke C, Mieczkowski PA, Marszalek PE. 56.  2007. Detecting ultraviolet damage in single DNA molecules by atomic force microscopy. Biophys. J. 93:51758–67 [Google Scholar]
  57. Jiang Y, Marszalek PE. 57.  2011. Atomic force microscopy captures MutS tetramers initiating DNA mismatch repair. EMBO J 30:142881–93 [Google Scholar]
  58. Johnson RP, Fleming AM, Beuth LR, Burrows CJ, White HS. 58.  2016. Base flipping within the α-hemolysin latch allows single-molecule identification of mismatches in DNA. J. Am. Chem. Soc. 138:2594–603 [Google Scholar]
  59. Joo C, McKinney SA, Nakamura M, Rasnik I, Myong S, Ha T. 59.  2006. Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126:3515–27 [Google Scholar]
  60. Josephs EA, Zheng T, Marszalek PE. 60.  2015. Atomic force microscopy captures the initiation of methyl-directed DNA mismatch repair. DNA Repair 35:71–84 [Google Scholar]
  61. Joyce CM, Benkovic SJ. 61.  2004. DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry 43:4514317–24 [Google Scholar]
  62. Kad NM, Wang H, Kennedy GG, Warshaw DM, Van Houten B. 62.  2010. Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single-molecule imaging of quantum-dot-labeled proteins. Mol. Cell 37:5702–13 [Google Scholar]
  63. Kamarthapu V, Epshtein V, Benjamin B, Proshkin S, Mironov A. 63.  et al. 2016. ppGpp couples transcription to DNA repair in E. coli. . Science 352:6288993–96 [Google Scholar]
  64. Kao Y-T, Saxena C, Wang L, Sancar A, Zhong D. 64.  2005. Direct observation of thymine dimer repair in DNA by photolyase. PNAS 102:4516128–32 [Google Scholar]
  65. Karymov M, Daniel D, Sankey OF, Lyubchenko YL. 65.  2005. Holliday junction dynamics and branch migration: single-molecule analysis. PNAS 102:238186–91 [Google Scholar]
  66. Kath JE, Chang S, Scotland MK, Wilbertz JH, Jergic S. 66.  et al. 2016. Exchange between Escherichia coli polymerases II and III on a processivity clamp. Nucleic Acids Res 44:41681–90 [Google Scholar]
  67. Kath JE, Jergic S, Heltzel JMH, Jacob DT, Dixon NE. 67.  et al. 2014. Polymerase exchange on single DNA molecules reveals processivity clamp control of translesion synthesis. PNAS 111:217647–52 [Google Scholar]
  68. Kidane D, Graumann PL. 68.  2005. Dynamic formation of RecA filaments at DNA double strand break repair centers in live cells. J. Cell Biol. 170:3357–66 [Google Scholar]
  69. Kidane D, Sanchez H, Alonso JC, Graumann PL. 69.  2004. Visualization of DNA double-strand break repair in live bacteria reveals dynamic recruitment of Bacillus subtilis RecF, RecO and RecN proteins to distinct sites on the nucleoids. Mol. Microbiol. 52:61627–39 [Google Scholar]
  70. Kisker C, Kuper J, Houten BV. 70.  2013. Prokaryotic nucleotide excision repair. Cold Spring Harb. Perspect. Biol. 5:3a012591 [Google Scholar]
  71. Kunkel TA, Erie DA. 71.  2005. DNA mismatch repair. Annu. Rev. Biochem. 74:681–710 [Google Scholar]
  72. Kuzminov A. 72.  2001. Single-strand interruptions in replicating chromosomes cause double-strand breaks. PNAS 98:158241–46 [Google Scholar]
  73. Lan L, Nakajima S, Wei L, Sun L, Hsieh C-L. 73.  et al. 2014. Novel method for site-specific induction of oxidative DNA damage reveals differences in recruitment of repair proteins to heterochromatin and euchromatin. Nucleic Acids Res 42:42330–45 [Google Scholar]
  74. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J. 74.  2012. Segregation of molecules at cell division reveals native protein localization. Nat. Methods 9:5480–82 [Google Scholar]
  75. Lee KS, Balci H, Jia H, Lohman TM, Ha T. 75.  2013. Direct imaging of single UvrD helicase dynamics on long single-stranded DNA. Nat. Commun. 4:1878 [Google Scholar]
  76. Lee NK, Kapanidis AN, Koh HR, Korlann Y, Ho SO. 76.  et al. 2007. Three-color alternating-laser excitation of single molecules: monitoring multiple interactions and distances. Biophys. J. 92:1303–12 [Google Scholar]
  77. Lenhart JS, Sharma A, Hingorani MM, Simmons LA. 77.  2013. DnaN clamp zones provide a platform for spatiotemporal coupling of mismatch detection to DNA replication. Mol. Microbiol. 87:3553–68 [Google Scholar]
  78. Lestas I, Vinnicombe G, Paulsson J. 78.  2010. Fundamental limits on the suppression of molecular fluctuations. Nature 467:7312174–78 [Google Scholar]
  79. Lesterlin C, Ball G, Schermelleh L, Sherratt DJ. 79.  2014. RecA bundles mediate homology pairing between distant sisters during DNA break repair. Nature 506:7487249–53 [Google Scholar]
  80. Liao Y, Li Y, Schroeder JW, Simmons LA, Biteen JS. 80.  2016. Single-molecule DNA polymerase dynamics at a bacterial replisome in live cells. Biophys. J. 111:122562–69 [Google Scholar]
  81. Liao Y, Schroeder JW, Gao B, Simmons LA, Biteen JS. 81.  2015. Single-molecule motions and interactions in live cells reveal target search dynamics in mismatch repair. PNAS 112:50E6898–906 [Google Scholar]
  82. Lin Y, Zhao T, Jian X, Farooqui Z, Qu X. 82.  et al. 2009. Using the bias from flow to elucidate single DNA repair protein sliding and interactions with DNA. Biophys. J. 96:51911–17 [Google Scholar]
  83. Lindahl T. 83.  1993. Instability and decay of the primary structure of DNA. Nature 362:6422709–15 [Google Scholar]
  84. Lippincott-Schwartz J, Patterson GH. 84.  2009. Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol 19:11555–65 [Google Scholar]
  85. Liu B, Baskin RJ, Kowalczykowski SC. 85.  2013. DNA unwinding heterogeneity by RecBCD results from static molecules able to equilibrate. Nature 500:7463482–85 [Google Scholar]
  86. Liu J, Hanne J, Britton BM, Bennett J, Kim D. 86.  et al. 2016. Cascading MutS and MutL sliding clamps control DNA diffusion to activate mismatch repair. Nature 539:7630583–87 [Google Scholar]
  87. Long H, Miller SF, Strauss C, Zhao C, Cheng L. 87.  et al. 2016. Antibiotic treatment enhances the genome-wide mutation rate of target cells. PNAS 113:18E2498–505 [Google Scholar]
  88. Luijsterburg MS, von Bornstaedt G, Gourdin AM, Politi AZ, Moné MJ. 88.  et al. 2010. Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair. J. Cell Biol. 189:3445–63 [Google Scholar]
  89. Lynch M. 89.  2015. Genetics: feedforward loop for diversity. Nature 523:7561414–16 [Google Scholar]
  90. Malta E, Moolenaar GF, Goosen N. 90.  2007. Dynamics of the UvrABC nucleotide excision repair proteins analyzed by fluorescence resonance energy transfer. Biochemistry 46:319080–88 [Google Scholar]
  91. Manosas M, Perumal SK, Croquette V, Benkovic SJ. 91.  2012. Direct observation of stalled fork restart via fork regression in the T4 replication system. Science 338:61111217–20 [Google Scholar]
  92. Markiewicz RP, Vrtis KB, Rueda D, Romano LJ. 92.  2012. Single-molecule microscopy reveals new insights into nucleotide selection by DNA polymerase I. Nucleic Acids Res 40:167975–84 [Google Scholar]
  93. Matic I, Radman M, Taddei F, Picard B, Doit C. 93.  et al. 1997. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277:53331833–34 [Google Scholar]
  94. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, Sandler SJ. 94.  2004. Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol. Microbiol. 53:51343–57 [Google Scholar]
  95. Mullins EA, Shi R, Parsons ZD, Yuen PK, David SS. 95.  et al. 2015. The DNA glycosylase AlkD uses a non-base-flipping mechanism to excise bulky lesions. Nature 527:7577254–58 [Google Scholar]
  96. Murakami M, Hirokawa H, Hayata I. 96.  2000. Analysis of radiation damage of DNA by atomic force microscopy in comparison with agarose gel electrophoresis studies. J. Biochem. Biophys. Methods 44:1–231–40 [Google Scholar]
  97. Nelson SR, Dunn AR, Kathe SD, Warshaw DM, Wallace SS. 97.  2014. Two glycosylase families diffusively scan DNA using a wedge residue to probe for and identify oxidatively damaged bases. PNAS 111:20E2091–99 [Google Scholar]
  98. Neuman KC, Block SM. 98.  2004. Optical trapping. Rev. Sci. Instrum. 75:92787–809 [Google Scholar]
  99. Okumus B, Landgraf D, Lai GC, Bakhsi S, Arias-Castro JC. 99.  et al. 2016. Mechanical slowing-down of cytoplasmic diffusion allows in vivo counting of proteins in individual cells. Nat. Commun. 7:11641 [Google Scholar]
  100. Paudel BP, Rueda D. 100.  2014. Molecular crowding accelerates ribozyme docking and catalysis. J. Am. Chem. Soc. 136:4816700–3 [Google Scholar]
  101. Pennington JM, Rosenberg SM. 101.  2007. Spontaneous DNA breakage in single living Escherichia coli cells. Nat. Genet. 39:6797–802 [Google Scholar]
  102. Perumal SK, Yue H, Hu Z, Spiering MM, Benkovic SJ. 102.  2010. Single-molecule studies of DNA replisome function. Biochim. Biophys. Acta 1804:51094–112 [Google Scholar]
  103. Petrova V, Chen SH, Molzberger ET, Tomko E, Chitteni-Pattu S. 103.  et al. 2015. Active displacement of RecA filaments by UvrD translocase activity. Nucleic Acids Res 43:84133–49 [Google Scholar]
  104. Pham TM, Tan KW, Sakumura Y, Okumura K, Maki H, Akiyama MT. 104.  2013. A single-molecule approach to DNA replication in Escherichia coli cells demonstrated that DNA polymerase III is a major determinant of fork speed. Mol. Microbiol. 90:3584–96 [Google Scholar]
  105. Possoz C, Filipe SR, Grainge I, Sherratt DJ. 105.  2006. Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. EMBO J 25:112596–604 [Google Scholar]
  106. Pugliese KM, Gul OT, Choi Y, Olsen TJ, Sims PC. 106.  et al. 2015. Processive incorporation of deoxynucleoside triphosphate analogs by single-molecule DNA polymerase I (Klenow fragment) nanocircuits. J. Am. Chem. Soc. 137:309587–94 [Google Scholar]
  107. Qiu R, Sakato M, Sacho EJ, Wilkins H, Zhang X. 107.  et al. 2015. MutL traps MutS at a DNA mismatch. PNAS 112:3510914–19 [Google Scholar]
  108. Radman M. 108.  2001. Fidelity and infidelity. Nature 413:6852115 [Google Scholar]
  109. Ragunathan K, Liu C, Ha T. 109.  2012. RecA filament sliding on DNA facilitates homology search. eLife 1:e00067 [Google Scholar]
  110. Raj A, van Oudenaarden A. 110.  2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:2216–26 [Google Scholar]
  111. Raser JM, O'Shea EK. 111.  2005. Noise in gene expression: origins, consequences, and control. Science 309:57432010–13 [Google Scholar]
  112. Renzette N, Gumlaw N, Nordman JT, Krieger M, Yeh S-P. 112.  et al. 2005. Localization of RecA in Escherichia coli K-12 using RecA–GFP. Mol. Microbiol. 57:41074–85 [Google Scholar]
  113. Reyes-Lamothe R, Sherratt DJ, Leake MC. 113.  2010. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328:5977498–501 [Google Scholar]
  114. Robinson A, McDonald JP, Caldas VEA, Patel M, Wood EA. 114.  et al. 2015. Regulation of mutagenic DNA polymerase V activation in space and time. PLOS Genet 11:8e1005482 [Google Scholar]
  115. Sanchez H, Kidane D, Reed P, Curtis FA, Cozar MC. 115.  et al. 2005. The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilis. Genetics 171:3873–83 [Google Scholar]
  116. Santoso Y, Joyce CM, Potapova O, Le Reste L, Hohlbein J. 116.  et al. 2010. Conformational transitions in DNA polymerase I revealed by single-molecule FRET. PNAS 107:2715–20 [Google Scholar]
  117. Schwartz JJ, Quake SR. 117.  2009. Single molecule measurement of the “speed limit” of DNA polymerase. PNAS 106:4820294–99 [Google Scholar]
  118. Sedgwick B. 118.  2004. Repairing DNA-methylation damage. Nat. Rev. Mol. Cell Biol. 5:2148–57 [Google Scholar]
  119. Selvin PR, Ha T. 119.  2008. Single Molecule Techniques: A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
  120. Shee C, Cox BD, Gu F, Luengas EM, Joshi MC. 120.  et al. 2013. Engineered proteins detect spontaneous DNA breakage in human and bacterial cells. eLife 2:e01222 [Google Scholar]
  121. Simmons LA, Davies BW, Grossman AD, Walker GC. 121.  2008. β clamp directs localization of mismatch repair in Bacillus subtilis. Mol. Cell 29:3291–301 [Google Scholar]
  122. Smith BT, Grossman AD, Walker GC. 122.  2001. Visualization of mismatch repair in bacterial cells. Mol. Cell 8:61197–206 [Google Scholar]
  123. Sokoloski JE, Kozlov AG, Galletto R, Lohman TM. 123.  2016. Chemo-mechanical pushing of proteins along single-stranded DNA. PNAS 113:226194–99 [Google Scholar]
  124. Spies M, Amitani I, Baskin RJ, Kowalczykowski SC. 124.  2007. RecBCD enzyme switches lead motor subunits in response to χ-recognition. Cell 131:4694–705 [Google Scholar]
  125. Stennett EMS, Ciuba MA, Lin S, Levitus M. 125.  2015. Demystifying PIFE: the photophysics behind the protein-induced fluorescence enhancement phenomenon in Cy3. J. Phys. Chem. Lett. 6:101819–23 [Google Scholar]
  126. Stracy M, Jaciuk M, Uphoff S, Kapanidis AN, Nowotny M. 126.  et al. 2016. Single-molecule imaging of UvrA and UvrB recruitment to DNA lesions in living Escherichia coli. . Nat. Commun. 7:12568 [Google Scholar]
  127. Stracy M, Lesterlin C, Garza de Leon F, Uphoff S, Zawadzki P, Kapanidis AN. 127.  2015. Live-cell superresolution microscopy reveals the organization of RNA polymerase in the bacterial nucleoid. PNAS 112:32E4390–99 [Google Scholar]
  128. Sun B, Pandey M, Inman JT, Yang Y, Kashlev M. 128.  et al. 2015. T7 replisome directly overcomes DNA damage. Nat. Commun. 6:10260 [Google Scholar]
  129. Taheri-Araghi S, Brown SD, Sauls JT, McIntosh DB, Jun S. 129.  2015. Single-cell physiology. Annu. Rev. Biophys. 44:1123–42 [Google Scholar]
  130. Tan KW, Pham TM, Furukohri A, Maki H, Akiyama MT. 130.  2015. Recombinase and translesion DNA polymerase decrease the speed of replication fork progression during the DNA damage response in Escherichia coli cells. Nucleic Acids Res 43:31714–25 [Google Scholar]
  131. Tessmer I, Fried MG. 131.  2014. Insight into the cooperative DNA binding of the O6-alkylguanine DNA alkyltransferase. DNA Repair 20:14–22 [Google Scholar]
  132. Tessmer I, Yang Y, Zhai J, Du C, Hsieh P. 132.  et al. 2008. Mechanism of MutS searching for DNA mismatches and signaling repair. J. Biol. Chem. 283:5236646–54 [Google Scholar]
  133. Uphoff S, Holden SJ, Le Reste L, Periz J, van de Linde S. 133.  et al. 2010. Monitoring multiple distances within a single molecule using switchable FRET. Nat. Methods 7:10831–36 [Google Scholar]
  134. Uphoff S, Kapanidis AN. 134.  2014. Studying the organization of DNA repair by single-cell and single-molecule imaging. DNA Repair 20:32–40 [Google Scholar]
  135. Uphoff S, Lord ND, Okumus B, Potvin-Trottier L, Sherratt DJ, Paulsson J. 135.  2016. Stochastic activation of a DNA damage response causes cell-to-cell mutation rate variation. Science 351:62771094–97 [Google Scholar]
  136. Uphoff S, Reyes-Lamothe R, Garza de Leon F, Sherratt DJ, Kapanidis AN. 136.  2013. Single-molecule DNA repair in live bacteria. PNAS 110:208063–68 [Google Scholar]
  137. Uttamapinant C, Howe JD, Lang K, Beránek V, Davis L. 137.  et al. 2015. Genetic code expansion enables live-cell and super-resolution imaging of site-specifically labeled cellular proteins. J. Am. Chem. Soc. 137:144602–5 [Google Scholar]
  138. van de Linde S, Heilemann M, Sauer M. 138.  2012. Live-cell super-resolution imaging with synthetic fluorophores. Annu. Rev. Phys. Chem. 63:519–40 [Google Scholar]
  139. van der Heijden T, Modesti M, Hage S, Kanaar R, Wyman C, Dekker C. 139.  2008. Homologous recombination in real time: DNA strand exchange by RecA. Mol. Cell 30:4530–38 [Google Scholar]
  140. van Gool AJ, Hajibagheri NMA, Stasiak A, West SC. 140.  1999. Assembly of the Escherichia coli RuvABC resolvasome directs the orientation of Holliday junction resolution. Genes Dev 13:141861–70 [Google Scholar]
  141. van Noort SJ, van der Werf KO, Eker AP, Wyman C, de Grooth BG. 141.  et al. 1998. Direct visualization of dynamic protein-DNA interactions with a dedicated atomic force microscope. Biophys. J. 74:62840–49 [Google Scholar]
  142. van Oijen AM, Loparo JJ. 142.  2010. Single-molecule studies of the replisome. Annu. Rev. Biophys. 39:1429–48 [Google Scholar]
  143. Veening J-W, Smits WK, Kuipers OP. 143.  2008. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62:1193–210 [Google Scholar]
  144. Verbruggen P, Heinemann T, Manders E, von Bornstaedt G, van Driel R, Höfer T. 144.  2014. Robustness of DNA repair through collective rate control. PLOS Comput. Biol. 10:1e1003438 [Google Scholar]
  145. Wang H, DellaVecchia MJ, Skorvaga M, Croteau DL, Erie DA, Van Houten B. 145.  2006. UvrB domain 4, an autoinhibitory gate for regulation of DNA binding and ATPase activity. J. Biol. Chem. 281:2215227–37 [Google Scholar]
  146. Wang P, Robert L, Pelletier J, Dang WL, Taddei F. 146.  et al. 2010. Robust growth of Escherichia coli. . Curr. Biol. 20:121099–103 [Google Scholar]
  147. Wu D, Kaur P, Li ZM, Bradford KC, Wang H, Erie DA. 147.  2016. Visualizing the path of DNA through proteins using DREEM imaging. Mol. Cell 61:2315–23 [Google Scholar]
  148. Wuite GJ, Smith SB, Young M, Keller D, Bustamante C. 148.  2000. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404:6773103–6 [Google Scholar]
  149. Yeeles JTP, Marians KJ. 149.  2011. The Escherichia coli replisome is inherently DNA damage tolerant. Science 334:6053235–38 [Google Scholar]
  150. Yokota H, Chujo YA, Harada Y. 150.  2013. Single-molecule imaging of the oligomer formation of the nonhexameric Escherichia coli UvrD helicase. Biophys. J. 104:4924–33 [Google Scholar]
  151. Zieske K, Schwille P. 151.  2013. Reconstitution of pole-to-pole oscillations of Min proteins in microengineered polydimethylsiloxane compartments. Angew. Chem. Int. Ed. 52:1459–62 [Google Scholar]
/content/journals/10.1146/annurev-biophys-070816-034106
Loading
Single-Molecule Analysis of Bacterial DNA Repair and Mutagenesis
Annual Review of Biophysics 46, 411 (2017); https://doi.org/10.1146/annurev-biophys-070816-034106
/content/journals/10.1146/annurev-biophys-070816-034106
/content/journals/10.1146/annurev-biophys-070816-034106
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error