Single-molecule motions and interactions in live cells reveal target search dynamics in mismatch repair

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 50, 2015, Pages E6898-E6906

  Liao, Yi ^a   Schroeder, Jeremy W ^a   Gao, Burke ^a   Simmons, Lyle A ^a   Biteen, Julie S ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Bacillus subtilis; Bacterial cell biology; DNA replication; Single cell analysis; Super resolution microscopy

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTEIN MUTS; BACTERIAL DNA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; CELL MOTION; CELL TRACKING; CONTROLLED STUDY; DNA SYNTHESIS; MICROSCOPY; MISMATCH REPAIR; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REPLISOME; BASE MISPAIRING; DNA REPAIR; DNA REPLICATION; GENETICS; PHYSIOLOGY; SINGLE CELL ANALYSIS;

BACILLUS SUBTILIS; BASE PAIR MISMATCH; DNA REPAIR; DNA REPLICATION; DNA, BACTERIAL; MUTS DNA MISMATCH-BINDING PROTEIN; SINGLE-CELL ANALYSIS;

EID: 84950320307     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1507386112     Document Type: Article

References (66)

1. Jiricny J (2013) Postreplicative mismatch repair. Cold Spring Harb Perspect Biol 5(4):a012633.
2. Lee H, Popodi E, Tang H, Foster PL (2012) Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc Natl Acad Sci USA 109(41):E2774-E2783.
3. Fishel R, et al. (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75(5):1027-1038.
4. Pillon MC, et al. (2010) Structure of the endonuclease domain of MutL: Unlicensed to cut. Mol Cell 39(1):145-151.
5. Kadyrov FA, Dzantiev L, Constantin N, Modrich P (2006) Endonucleolytic function of MutLalpha in human mismatch repair. Cell 126(2):297-308.
6. Tran HT, Gordenin DA, Resnick MA (1999) The 3'→5' exonucleases of DNA polymerases delta and epsilon and the 5'→3' exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol Cell Biol 19(3):2000-2007.
7. Wang H, et al. (2003) DNA bending and unbending by MutS govern mismatch recognition and specificity. Proc Natl Acad Sci USA 100(25):14822-14827.
8. Jeong C, et al. (2011) MutS switches between two fundamentally distinct clamps during mismatch repair. Nat Struct Mol Biol 18(3):379-385.
9. Sass LE, Lanyi C, Weninger K, Erie DA (2010) Single-molecule FRET TACKLE reveals highly dynamic mismatched DNA-MutS complexes. Biochemistry 49(14):3174-3190.
10. Cho WK, et al. (2012) ATP alters the diffusion mechanics of MutS on mismatched DNA. Structure 20(7):1264-1274.
11. Qiu R, et al. (2012) Large conformational changes in MutS during DNA scanning, mismatch recognition and repair signalling. EMBO J 31(11):2528-2540.
12. DeRocco VC, Sass LE, Qiu R, Weninger KR, Erie DA (2014) Dynamics of MutS-mismatched DNA complexes are predictive of their repair phenotypes. Biochemistry 53(12):2043-2052.
13. Gorman J, et al. (2007) Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol Cell 28(3):359-370.
14. Gorman J, Plys AJ, Visnapuu ML, Alani E, Greene EC (2010) Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat Struct Mol Biol 17(8):932-938.
15. Gorman J, et al. (2012) Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair. Proc Natl Acad Sci USA 109(45):E3074-E3083.
16. Smith BT, Grossman AD, Walker GC (2001) Visualization of mismatch repair in bacterial cells. Mol Cell 8(6):1197-1206.
17. Kleczkowska HE, Marra G, Lettieri T, Jiricny J (2001) hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci. Genes Dev 15(6):724-736.
18. Simmons LA, Davies BW, Grossman AD, Walker GC (2008) Beta clamp directs localization of mismatch repair in Bacillus subtilis. Mol Cell 29(3):291-301.
19. Hombauer H, Campbell CS, Smith CE, Desai A, Kolodner RD (2011) Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 147(5):1040-1053.
20. Lenhart JS, Sharma A, Hingorani MM, Simmons LA (2013) DnaN clamp zones provide a platform for spatiotemporal coupling of mismatch detection to DNA replication. Mol Microbiol 87(3):553-568.
21. Klocko AD, et al. (2011) Mismatch repair causes the dynamic release of an essential DNA polymerase from the replication fork. Mol Microbiol 82(3):648-663.
22. Pluciennik A, Burdett V, Lukianova O, O'Donnell M, Modrich P (2009) Involvement of the beta clamp in methyl-directed mismatch repair in vitro. J Biol Chem 284(47):32782-32791.
23. Hombauer H, Srivatsan A, Putnam CD, Kolodner RD (2011) Mismatch repair, but not heteroduplex rejection, is temporally coupled to DNA replication. Science 334(6063):1713-1716.
24. Lenhart JS, Pillon MC, Guarné A, Simmons LA (2013) Trapping and visualizing intermediate steps in the mismatch repair pathway in vivo. Mol Microbiol 90(4):680-698.
25. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793-795.
26. Betzig E, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313(5793):1642-1645.
27. Hess ST, Girirajan TP, Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91(11):4258-4272.
28. Yildiz A, et al. (2003) Myosin V walks hand-over-hand: Single fluorophore imaging with 1.5-nm localization. Science 300(5628):2061-2065.
29. Elmore S, Müller M, Vischer N, Odijk T, Woldringh CL (2005) Single-particle tracking of oriC-GFP fluorescent spots during chromosome segregation in Escherichia coli. J Struct Biol 151(3):275-287.
30. Biteen JS, Moerner WE (2010) Single-molecule and superresolution imaging in live bacteria cells. Cold Spring Harb Perspect Biol 2(3):a000448.
31. Biteen JS, et al. (2008) Super-resolution imaging in live Caulobacter crescentus cells using photoswitchable EYFP. Nat Methods 5(11):947-949.
32. Manley S, et al. (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5(2):155-157.
33. Karunatilaka KS, Cameron EA, Martens EC, Koropatkin NM, Biteen JS (2014) Superresolution imaging captures carbohydrate utilization dynamics in human gut symbionts. MBio 5(6):e02172.
34. Haas BL, Matson JS, Di Rita VJ, Biteen JS (2015) Single-molecule tracking in live Vibrio cholerae reveals that ToxR recruits the membrane-bound virulence regulator TcpP to the toxT promoter. Mol Microbiol 96(1):4-13.
35. Berkmen MB, Grossman AD (2006) Spatial and temporal organization of the Bacillus subtilis replication cycle. Mol Microbiol 62(1):57-71.
36. Lemon KP, Grossman AD (1998) Localization of bacterial DNA polymerase: Evidence for a factory model of replication. Science 282(5393):1516-1519.
37. Reyes-Lamothe R, Sherratt DJ, Leake MC (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328(5977):498-501.
38. Holden SJ, Uphoff S, Kapanidis AN (2011) DAOSTORM: An algorithm for high-density super-resolution microscopy. Nat Methods 8(4):279-280.
39. Zhu L, Zhang W, Elnatan D, Huang B (2012) Faster STORM using compressed sensing. Nat Methods 9(7):721-723.
40. Burnette DT, Sengupta P, Dai Y, Lippincott-Schwartz J, Kachar B (2011) Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules. Proc Natl Acad Sci USA 108(52):21081-21086.
41. Simonson PD, Rothenberg E, Selvin PR (2011) Single-molecule-based super-resolution images in the presence of multiple fluorophores. Nano Lett 11(11):5090-5096.
42. Imai Y, et al. (2000) Subcellular localization of Dna-initiation proteins of Bacillus subtilis: Evidence that chromosome replication begins at either edge of the nucleoids. Mol Microbiol 36(5):1037-1048.
43. Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ (2008) Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133(1):90-102.
44. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X (2003) Visualizing infection of individual influenza viruses. Proc Natl Acad Sci USA 100(16):9280-9285.
45. Wang S, Moffitt JR, Dempsey GT, Xie XS, Zhuang X (2014) Characterization and development of photoactivatable fluorescent proteins for single-molecule-based superresolution imaging. Proc Natl Acad Sci USA 111(23):8452-8457.
46. Durisic N, Laparra-Cuervo L, Sandoval-Álvarez A, Borbely JS, Lakadamyali M (2014) Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate. Nat Methods 11(2):156-162.
47. Wang W, Li GW, Chen C, Xie XS, Zhuang X (2011) Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333(6048):1445-1449.
48. Saxton MJ (1997) Single-particle tracking: The distribution of diffusion coefficients. Biophys J 72(4):1744-1753.
49. Uphoff S, Reyes-Lamothe R, Garza de Leon F, Sherratt DJ, Kapanidis AN (2013) Singlemolecule DNA repair in live bacteria. Proc Natl Acad Sci USA 110(20):8063-8068.
50. Elf J, Li GW, Xie XS (2007) Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316(5828):1191-1194.
51. Gebhardt JC, et al. (2013) Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat Methods 10(5):421-426.
52. Dupes NM, et al. (2010) Mutations in the Bacillus subtilis beta clamp that separate its roles in DNA replication from mismatch repair. J Bacteriol 192(13):3452-3463.
53. Alani E, Sokolsky T, Studamire B, Miret JJ, Lahue RS (1997) Genetic and biochemical analysis of Msh2p-Msh6p: Role of ATP hydrolysis and Msh2p-Msh6p subunit interactions in mismatch base pair recognition. Mol Cell Biol 17(5):2436-2447.
54. Haber LT, Walker GC (1991) Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities. EMBO J 10(9):2707-2715.
55. Sharma A, Doucette C, Biro FN, Hingorani MM (2013) Slow conformational changes in MutS and DNA direct ordered transitions between mismatch search, recognition and signaling of DNA repair. J Mol Biol 425(22):4192-4205.
56. Junop MS, Obmolova G, Rausch K, Hsieh P, Yang W (2001) Composite active site of an ABC ATPase: MutS uses ATP to verify mismatch recognition and authorize DNA repair. Mol Cell 7(1):1-12.
57. Acharya S (2008) Mutations in the signature motif in MutS affect ATP-induced clamp formation and mismatch repair. Mol Microbiol 69(6):1544-1559.
58. Lenhart JS, et al. (2014) RecO and RecR are necessary for RecA loading in response to DNA damage and replication fork stress. J Bacteriol 196(15):2851-2860.
59. Dervyn E, et al. (2001) Two essential DNA polymerases at the bacterial replication fork. Science 294(5547):1716-1719.
60. Sanders GM, Dallmann HG, McHenry CS (2010) Reconstitution of the B. subtilis replisome with 13 proteins including two distinct replicases. Mol Cell 37(2):273-281.
61. Burnett L, Wake RG (1977) Initiation and termination of chromosome replication at 45 degree C in a temperature-sensitive deoxyribonucleic acid initiation mutant of Bacillus subtilis 168, TsB134. J Bacteriol 130(1):538-539.
62. Tabaka M, Kalwarczyk T, Holyst R (2014) Quantitative influence of macromolecular crowding on gene regulation kinetics. Nucleic Acids Res 42(2):727-738.
63. Sekedat MD, et al. (2010) GINS motion reveals replication fork progression is remarkably uniform throughout the yeast genome. Mol Syst Biol 6:353.
64. Tomimatsu N, et al. (2014) Phosphorylation of EXO1 by CDKs 1 and 2 regulates DNA end resection and repair pathway choice. Nat Commun 5:3561.
65. Wang JD, Sanders GM, Grossman AD (2007) Nutritional control of elongation of DNA replication by (p) ppGpp. Cell 128(5):865-875.
66. Lewis JP (1995) Fast normalized cross-correlation. Vis Interface 10(1):120-123.