Chromosomal locus tracking with proper accounting of static and dynamic errors

Physical Review E - Statistical, Nonlinear, and Soft Matter Physics

Volumn 91, Issue 6, 2015, Pages

  Backlund, Mikael P ^a   Joyner, Ryan ^b   Moerner, W E ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROWNIAN MOVEMENT; CHROMOSOMES; DIFFUSION; ERROR STATISTICS;

ANOMALOUS DIFFUSION; COMPLEX ENVIRONMENTS; EXTRACTING PARAMETER; FRACTIONAL BROWNIAN MOTION; MEAN SQUARED DISPLACEMENT; QUANTITATIVE EXTRACTION; STATIC AND DYNAMIC ERRORS; VELOCITY AUTOCORRELATIONS;

ERRORS;

BIOLOGICAL MODEL; CHROMOSOME; GENE LOCUS; GENETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); SACCHAROMYCES CEREVISIAE;

CHROMOSOMES; GENETIC LOCI; MODELS, BIOLOGICAL; MOVEMENT; SACCHAROMYCES CEREVISIAE;

EID: 84936971653     PISSN: 15393755     EISSN: 15502376     Source Type: Journal    
DOI: 10.1103/PhysRevE.91.062716     Document Type: Article

References (58)

1. E. J. Peterman, H. Sosa, and W. E. Moerner, Single-molecule fluorescence spectroscopy and microscopy of biomolecular motors, Annu. Rev. Phys. Chem. 55, 79 (2004). 10.1146/annurev.physchem.55.091602.094340
2. M. J. Saxton and K. Jacobson, Single-particle tracking: Applications to membrane dynamics, Annu. Rev. Biophys. Biomol. Struct. 26, 373 (1997). 10.1146/annurev.biophys.26.1.373
3. K. Ritchie, X. Shan, J. Kondo, K. Iwasawa, T. Fujiwara, and A. Kusumi, Detection of non-brownian diffusion in the cell membrane in single molecule tracking, Biophys. J. 88, 2266 (2005). 10.1529/biophysj.104.054106
4. M. Vrljic, S. Y. Nishimura, S. Brasselet, W. E. Moerner, and H. M. McConnell, Translational diffusion of individual class II MHC membrane proteins in cells, Biophys. J. 83, 2681 (2002). 10.1016/S0006-3495(02)75277-6
5. Y. M. Umemura, M. Vrljic, S. Y. Nishimura, T. K. Fujiwara, K. G. N. Suzuki, and A. Kusumi, Both MHC class II and its GPI-anchored form undergo hop diffusion as observed by single-molecule tracking, Biophys. J. 95, 435 (2008). 10.1529/biophysj.107.123018
6. I. M. Tolić-Nørrelykke, E.-L. Munteanu, G. Thon, L. Oddershede, and K. Berg-Sørensen, Anomalous diffusion in living yeast cells, Phys. Rev. Lett. 93, 078102 (2004). 10.1103/PhysRevLett.93.078102
7. I. Golding and E. C. Cox, Physical nature of bacterial cytoplasm, Phys. Rev. Lett. 96, 098102 (2006). 10.1103/PhysRevLett.96.098102
8. S. C. Weber, A. J. Spakowitz, and J. A. Theriot, Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci, Proc. Natl. Acad. Sci. USA 109, 7338 (2012). 10.1073/pnas.1119505109
9. A. Javer, Z. Long, E. Nugent, M. Grisi, K. Siriwatwetchakul, K. D. Dorfman, P. Cicuta, and M. C. Lagomarsino, Short-time movement of E. Coli chromosomal loci depends on coordinate and subcellular localization, Nat. Commun. 4, 3003 (2013). 10.1038/ncomms3003
10. I. Bronstein, Y. Israel, E. Kepten, S. Mai, Y. Shav-Tal, E. Barkai, and Y. Garini, Transient anomalous diffusion of telomeres in the nucleus of mammalian cells, Phys. Rev. Lett. 103, 018102 (2009). 10.1103/PhysRevLett.103.018102
11. G. G. Cabal, A. Genovesio, S. Rodriguez-Navarro, C. Zimmer, O. Gadal, A. Lesne, H. Buc, F. Feuerbach-Fournier, J. Olivo-Marin, and E. D. Hurt, SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope, Nature 441, 770 (2006). 10.1038/nature04752
12. K. Burnecki, E. Kepten, J. Janczura, I. Bronshtein, Y. Garini, and A. Weron, Universal algorithm for identification of fractional Brownian motion. A case of telomere subdiffusion, Biophys. J. 103, 1839 (2012). 10.1016/j.bpj.2012.09.040
13. A. J. Berglund, Statistics of camera-based single-particle tracking, Phys. Rev. E 82, 011917 (2010). 10.1103/PhysRevE.82.011917
14. C. L. Vestergaard, P. C. Blainey, and H. Flyvbjerg, Optimal estimation of diffusion coefficients from single-particle trajectories, Phys Rev. E 89, 022726 (2014). 10.1103/PhysRevE.89.022726
15. H. Qian, M. P. Sheetz, and E. L. Elson, Single particle tracking. Analysis of diffusion and flow in two dimensional systems, Biophys. J. 60, 910 (1991). 10.1016/S0006-3495(91)82125-7
16. J. Jeon and R. Metzler, Analysis of short subdiffusive time series: Scatter of the time-averaged mean-squared displacement, J. Phys. A: Math. Theor. 43, 252001 (2010). 10.1088/1751-8113/43/25/252001
17. T. Savin and P. S. Doyle, Static and dynamic errors in particle tracking microrheology, Biophys. J. 88, 623 (2005). 10.1529/biophysj.104.042457
18. D. S. Martin, M. B. Forstner, and J. A. Käs, Apparent subdiffusion inherent to single particle tracking, Biophys. J. 83, 2109 (2002). 10.1016/S0006-3495(02)73971-4
19. E. Kepten, I. Bronshtein, and Y. Garini, Improved estimation of anomalous diffusion exponents in single-particle tracking experiments, Phys. Rev. E 87, 052713 (2013). 10.1103/PhysRevE.87.052713
20. M. Hellmann, J. Klafter, D. W. Heermann, and M. Weiss, Challenges in determining anomalous diffusion in crowded fluids, J. Phys.: Condens. Matter 23, 234113 (2011). 10.1088/0953-8984/23/23/234113
21. X. Michalet and A. J. Berglund, Optimal diffusion coefficient estimation in single-particle tracking, Phys. Rev. E 85, 061916 (2012). 10.1103/PhysRevE.85.061916
22. X. Michalet, Mean square displacement analysis of single-particle trajectories with localization error: Brownian motion in an isotropic medium, Phys. Rev. E 82, 041914 (2010). 10.1103/PhysRevE.82.041914
23. H. Deschout, K. Neyts, and K. Braeckmans, The influence of movement on the localization precision of sub-resolution particles in fluorescence microscopy, J. Biophotonics 5, 97 (2012). 10.1002/jbio.201100078
24. M. J. Saxton, Anomalous diffusion due to obstacles: A Monte Carlo study, Biophys. J. 66, 394 (1994). 10.1016/S0006-3495(94)80789-1
25. H. Scher and E. W. Montroll, Anomalous transit-time dispersion in amorphous solids, Phys. Rev. B 12, 2455 (1975). 10.1103/PhysRevB.12.2455
26. B. B. Mandelbrot and J. W. Van Ness, Fractional Brownian motions, fractional noises and applications, SIAM Rev. 10, 422 (1968). 10.1137/1010093
27. D. Ernst, J. Köhler, and M. Weiss, Probing the type of anomalous diffusion with single-particle tracking, Phys. Chem. Chem. Phys. 16, 7686 (2014). 10.1039/C4CP00292J
28. S. C. Weber, M. A. Thompson, W. E. Moerner, A. J. Spakowitz, and J. A. Theriot, Analytical tools to distinguish the effects of localization error, confinement, and medium elasticity on the velocity autocorrelation function, Biophys. J. 102, 2443 (2012). 10.1016/j.bpj.2012.03.062
29. J. Szymanski and M. Weiss, Elucidating the origin of anomalous diffusion in crowded fluids, Phys. Rev. Lett. 103, 038102 (2009). 10.1103/PhysRevLett.103.038102
30. S. Condamin, V. Tejedor, R. Voituriez, O. Bénichou, and J. Klafter, Probing microscopic origins of confined subdiffusion by first-passage observables, Proc. Natl. Acad. Sci. USA 105, 5675 (2008). 10.1073/pnas.0712158105
31. E. Kepten, I. Bronshtein, and Y. Garini, Ergodicity convergence test suggests telomere motion obeys fractional dynamics, Phys. Rev. E 83, 041919 (2011). 10.1103/PhysRevE.83.041919
32. V. Tejedor, O. Bénichou, R. Voituriez, R. Jungmann, F. Simmel, C. Selhuber-Unkel, L. B. Oddershede, and R. Metzler, Quantitative analysis of single particle trajectories: Mean maximal excursion method, Biophys. J. 98, 1364 (2010). 10.1016/j.bpj.2009.12.4282
33. J.-H. Jeon and R. Metzler, Fractional Brownian motion and motion governed by the fractional Langevin equation in confined geometries, Phys. Rev. E 81, 021103 (2010). 10.1103/PhysRevE.81.021103
34. K. Burnecki, M. Muszkieta, G. Sikora, and A. Weron, Statistical modelling of subdiffusive dynamics in the cytoplasm of living cells: A FARIMA approach, Europhys. Lett. 98, 10004 (2012). 10.1209/0295-5075/98/10004
35. M. Magdziarz, A. Weron, K. Burnecki, and J. Klafter, Fractional Brownian motion versus the continuous-time random walk: A simple test for subdiffusive dynamics, Phys. Rev. Lett. 103, 180602 (2009). 10.1103/PhysRevLett.103.180602
36. R. Metzler, J. Jeon, A. G. Cherstvy, and E. Barkai, Anomalous diffusion models and their properties: Non-stationarity, non-ergodicity, and ageing at the centenary of single particle tracking, Phys. Chem. Chem. Phys. 16, 24128 (2014). 10.1039/C4CP03465A
37. J. M. Casolari, C. R. Brown, S. Komili, J. West, H. Hieronymus, and P. A. Silver, Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization, Cell 117, 427 (2004). 10.1016/S0092-8674(04)00448-9
38. A. F. Straight, A. S. Belmont, C. C. Robinett, and A. W. Murray, GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion, Curr. Biol. 6, 1599 (1996). 10.1016/S0960-9822(02)70783-5
39. M. P. Backlund, R. Joyner, K. Weis, and W. E. Moerner, Correlations of three-dimensional motion of chromosomal loci in yeast revealed by the double-helix point spread function microscope, Mol. Biol. Cell 25, 3619 (2014). 10.1091/mbc.E14-06-1127
40. S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function, Proc. Natl. Acad. Sci. USA 106, 2995 (2009). 10.1073/pnas.0900245106
41. M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function, Proc. Natl. Acad. Sci. USA 107, 17864 (2010). 10.1073/pnas.1012868107
42. A. Gahlmann, J. L. Ptacin, G. Grover, S. Quirin, A. R. S. von Diezmann, M. K. Lee, M. P. Backlund, L. Shapiro, R. Piestun, and W. E. Moerner, Quantitative multicolor subdiffraction imaging of bacterial protein ultrastructures in 3D, Nano Lett. 13, 987 (2013). 10.1021/nl304071h
43. A. Gahlmann and W. E. Moerner, Exploring bacterial cell biology with single-molecule tracking and super-resolution imaging, Nat. Rev. Microbiol. 12, 9 (2014). 10.1038/nrmicro3154
44. N. Destainville and L. Salome, Quantification and correction of systematic errors due to detector time-averaging in single-molecule tracking experiments, Biophys. J. 90, L17 (2006). 10.1529/biophysj.105.075176
45. T. Savin and P. S. Doyle, Role of a finite exposure time on measuring an elastic modulus using microrheology, Phys. Rev. E 71, 041106 (2005). 10.1103/PhysRevE.71.041106
46. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevE.91.062716 for derivations of Eqs. (4) and (20-22), as well as all supplemental figures.
47. S. C. Kou and X. S. Xie, Generalized Langevin equation with fractional Gaussian noise: Subdiffusion within a single protein molecule, Phys. Rev. Lett. 93, 180603 (2004). 10.1103/PhysRevLett.93.180603
48. S. C. Weber, A. J. Spakowitz, and J. A. Theriot, Bacterial chromosomal loci move subdiffusively through a viscoelastic cytoplasm, Phys. Rev. Lett. 104, 238102 (2010). 10.1103/PhysRevLett.104.238102
49. J.-H. Jeon, V. Tejedor, S. Burov, E. Barkai, C. Selhuber-Unkel, K. Berg-Sørensen, L. Oddershede, and R. Metzler, In vivo anomalous diffusion and weak ergodicity breaking of lipid granules, Phys. Rev. Lett. 106, 048103 (2011). 10.1103/PhysRevLett.106.048103
50. W. Deng and E. Barkai, Ergodic properties of fractional Brownian-Langevin motion, Phys. Rev. E 79, 011112 (2009). 10.1103/PhysRevE.79.011112
51. D. P. Kroese and Z. I. Botev, in Stochastic Geometry, Spatial Statistics, and Random Fields, Lecture Notes in Mathematics, Vol. 2120 (Springer International Publishing, Switzerland, 2015), pp. 369-404.
52. R. E. Thompson, D. R. Larson, and W. W. Webb, Precise nanometer localization analysis for individual fluorescent probes, Biophys. J. 82, 2775 (2002). 10.1016/S0006-3495(02)75618-X
53. K. I. Mortensen, L. S. Churchman, J. A. Spudich, and H. Flyvbjerg, Optimized localization analysis for single-molecule tracking and super-resolution microscopy, Nat. Methods 7, 377 (2010). 10.1038/nmeth.1447
54. S. C. Weber, J. A. Theriot, and A. J. Spakowitz, Subdiffusive motion of a polymer composed of subdiffusive monomers, Phys. Rev. E 82, 011913 (2010). 10.1103/PhysRevE.82.011913
55. M. Weiss, Single-particle tracking data reveal anticorrelated fractional Brownian motion in crowded fluids, Phys. Rev. E 88, 010101 (2013). 10.1103/PhysRevE.88.010101
56. A. E. Cohen, Trapping and manipulating single molecules in solution, Ph.D. thesis, Stanford University, 2006.
57. J. Kursawe, J. Schulz, and R. Metzler, Transient aging in fractional Brownian and Langevin-equation motion, Phys Rev. E 88, 062124 (2013). 10.1103/PhysRevE.88.062124
58. Y. Meroz, I. M. Sokolov, and J. Klafter, Test for determining a subdiffusive model in ergodic systems from single trajectories, Phys. Rev. Lett. 110, 090601 (2013). 10.1103/PhysRevLett.110.090601