A benchmark for chromatin binding measurements in live cells

Nucleic Acids Research

Volumn 40, Issue 15, 2012, Pages

  Mazza, Davide ^a,b   Abernathy, Alice ^a,c   Golob, Nicole ^a   Morisaki, Tatsuya ^a   McNally, James G ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53;

ANALYTIC METHOD; ARTICLE; BINDING KINETICS; BINDING SITE; CHROMATIN; CONTROLLED STUDY; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; MEASUREMENT; MOLECULAR INTERACTION; MUTANT; PRIORITY JOURNAL; PROTEIN BINDING; SINGLE MOLECULE TRACKING;

CELL LINE, TUMOR; CHROMATIN; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMANS; KINETICS; SPECTROMETRY, FLUORESCENCE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84867294762     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks701     Document Type: Article

References (54)

1. Phair, R. D. and Misteli, T. (2001) Kinetic modelling approaches to in vivo imaging. Nat. Rev. Mol. Cell Biol., 2, 898-907.
2. Elf, J., Li, G.-W. and Xie, X. S. (2007) Probing transcription factor dynamics at the single-molecule level in a living cell. Science, 316, 1191-1194.
3. Hager, G. L., McNally, J. G. and Misteli, T. (2009) Transcription dynamics. Mol. Cell, 35, 741-753.
4. Kang, M., Day, C. A., Di Benedetto, E. and Kenworthy, A. K. (2010) A quantitative approach to analyze binding diffusion kinetics by confocal FRAP. Biophys. J., 99, 2737-2747.
5. Phair, R. D. and Misteli, T. (2000) High mobility of proteins in the mammalian cell nucleus. Nature, 404, 604-609.
6. Mueller, F., Wach, P. and McNally, J. G. (2008) Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophys. J., 94, 3323-3339.
7. Yao, J., Munson, K. M., Webb, W. W. and Lis, J. T. (2006) Dynamics of heat shock factor association with native gene loci in living cells. Nature, 442, 1050-1053.
8. Michelman-Ribeiro, A., Mazza, D., Rosales, T., Stasevich, T. J., Boukari, H., Rishi, V., Vinson, C., Knutson, J. R. and McNally, J. G. (2009) Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. Biophys. J., 97, 337-346.
9. Capoulade, J., Wachsmuth, M., Hufnagel, L. and Knop, M. (2011) Quantitative fluorescence imaging of protein diffusion and interaction in living cells. Nat. Biotechnol., 29, 835-839.
10. Grünwald, D., Spottke, B., Buschmann, V. and Kubitscheck, U. (2006) Intranuclear binding kinetics and mobility of single native U1 snRNP particles in living cells. Mol. Biol. Cell, 17, 5017-5027.
11. Speil, J., Baumgart, E., Siebrasse, J.-P., Veith, R., Vinkemeier, U. and Kubitscheck, U. (2011) Activated STAT1 transcription factors conduct distinct saltatory movements in the cell nucleus. Biophys. J., 101, 2592-2600.
12. Hinow, P., Rogers, C. E., Barbieri, C. E., Pietenpol, J. A., Kenworthy, A. K. and Di Benedetto, E. (2006) The DNA binding activity of p53 displays reaction-diffusion kinetics. Biophys. J., 91, 330-342.
13. Phair, R. D., Scaffidi, P., Elbi, C., Vecerová, J., Dey, A., Ozato, K., Brown, D. T., Hager, G., Bustin, M. and Misteli, T. (2004) Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol., 24, 6393-6402.
14. Dundr, M., Hoffmann-Rohrer, U., Hu, Q., Grummt, I., Rothblum, L. I., Phair, R. D. and Misteli, T. (2002) A kinetic framework for a mammalian RNA polymerase in vivo. Science, 298, 1623-1626.
15. Darzacq, X., Shav-Tal, Y., de Turris, V., Brody, Y., Shenoy, S. M., Phair, R. D. and Singer, R. H. (2007) In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol., 14, 796-806.
16. Kimura, H., Sugaya, K. and Cook, P. R. (2002) The transcription cycle of RNA polymerase II in living cells. J. Cell Biol., 159, 777-782.
17. Maiuri, P., Knezevich, A., De Marco, A., Mazza, D., Kula, A., McNally, J. G. and Marcello, A. (2011) Fast transcription rates of RNA polymerase II in human cells. EMBO Rep., 12, 1280-1285.
18. Larson, D. R., Zenklusen, D., Wu, B., Chao, J. A. and Singer, R. H. (2011) Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science, 332, 475-478.
19. Mueller, F., Mazza, D., Stasevich, T. J. and McNally, J. G. (2010) FRAP and kinetic modeling in the analysis of nuclear protein dynamics: what do we really know? Curr. Opin. Cell Biol., 22, 403-411.
20. Farla, P., Hersmus, R., Trapman, J. and Houtsmuller, A. B. (2005) Antiandrogens prevent stable DNA-binding of the androgen receptor. J. Cell. Sci., 118, 4187-4198.
21. Hendrix, J., Gijsbers, R., De Rijck, J., Voet, A., Hotta, J.-I., McNeely, M., Hofkens, J., Debyser, Z. and Engelborghs, Y. (2010) The transcriptional co-activator LEDGF/p75 displays a dynamic scan-and-lock mechanism for chromatin tethering. Nucleic Acids Res., 10.1093/nar/gkq933.
22. Mikuni, S., Tamura, M. and Kinjo, M. (2007) Analysis of intranuclear binding process of glucocorticoid receptor using fluorescence correlation spectroscopy. FEBS Lett., 581, 389-393.
23. Babcock, H. P., Chen, C. and Zhuang, X. (2004) Using single-particle tracking to study nuclear trafficking of viral genes. Biophys. J., 87, 2749-2758.
24. Tokunaga, M., Imamoto, N. and Sakata-Sogawa, K. (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods, 5, 159-161.
25. Weigel, A. V., Simon, B., Tamkun, M. M. and Krapf, D. (2011) Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking. Proc. Natl Acad. Sci. USA, 108, 6438-6443.
26. Speil, J. and Kubitscheck, U. (2010) Single ovalbumin molecules exploring nucleoplasm and nucleoli of living cell nuclei. Biochim. Biophys. Acta, 1803, 396-404.
27. Bancaud, A., Huet, S., Daigle, N., Mozziconacci, J., Beaudouin, J. and Ellenberg, J. (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J., 28, 3785-3798.
28. Stasevich, T. J., Mueller, F., Michelman-Ribeiro, A., Rosales, T., Knutson, J. R. and McNally, J. G. (2010) Cross-validating FRAP and FCS to quantify the impact of photobleaching on in vivo binding estimates. Biophys. J., 99, 3093-3101.
29. Schröder, J., Benink, H., Dyba, M. and Los, G. V. (2009) In vivo labeling method using a genetic construct for nanoscale resolution microscopy. Biophys. J., 96, L01-03.
30. Selvin, P. R. and Ha, T. (2007) Single-Molecule Techniques: A Laboratory Manual, 1st edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Kimura, H. and Cook, P. R. (2001) Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol., 153, 1341-1353.
32. Marshall, W. F., Straight, A., Marko, J. F., Swedlow, J., Dernburg, A., Belmont, A., Murray, A. W., Agard, D. A. and Sedat, J. W. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr. Biol., 7, 930-939.
33. Neumann, F. R., Dion, V., Gehlen, L. R., Tsai-Pflugfelder, M., Schmid, R., Taddei, A. and Gasser, S. M. (2012) Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev., 26, 369-383.
34. Veith, R., Sorkalla, T., Baumgart, E., Anzt, J., Häberlein, H., Tyagi, S., Siebrasse, J. P. and Kubitscheck, U. (2010) Balbiani ring mRNPs diffuse through and bind to clusters of large intranuclear molecular structures. Biophys. J., 99, 2676-2685.
35. Sprague, B. L., Pego, R. L., Stavreva, D. A. and McNally, J. G. (2004) Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys. J., 86, 3473-3495.
36. Yechiel, E. and Edidin, M. (1987) Micrometer-scale domains in fibroblast plasma membranes. J. Cell Biol., 105, 755-760.
37. Kaeser, M. D. and Iggo, R. D. (2002) Chromatin immunoprecipitation analysis fails to support the latency model for regulation of p53 DNA binding activity in vivo. Proc. Natl Acad. Sci. USA, 99, 95-100.
38. Tafvizi, A., Huang, F., Fersht, A. R., Mirny, L. A. and van Oijen, A. M. (2011) A single-molecule characterization of p53 search on DNA. Proc. Natl Acad. Sci. USA, 108, 563-568.
39. Berkovich, R., Wolfenson, H., Eisenberg, S., Ehrlich, M., Weiss, M., Klafter, J., Henis, Y. I. and Urbakh, M. (2011) Accurate quantification of diffusion and binding kinetics of non-integral membrane proteins by FRAP. Traffic, 12, 1648-1657.
40. Hamard, P.-J., Lukin, D. J. and Manfredi, J. J. (2012) p53 basic C-terminus regulates p53 functions through DNA binding modulation of a subset of target genes. J. Biol. Chem., 287, 22397-22407.
41. Kim, H., Kim, K., Choi, J., Heo, K., Baek, H. J., Roeder, R. G. and An, W. (2012) p53 requires an intact C-terminal domain for DNA binding and transactivation. J. Mol. Biol., 415, 843-854.
42. McNally, J. G., Müller, W. G., Walker, D., Wolford, R. and Hager, G. L. (2000) The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science, 287, 1262-1265.
43. Rayasam, G. V., Elbi, C., Walker, D. A., Wolford, R., Fletcher, T. M., Edwards, D. P. and Hager, G. L. (2005) Ligand-specific dynamics of the progesterone receptor in living cells and during chromatin remodeling in vitro. Mol. Cell. Biol., 25, 2406-2418.
44. Bosisio, D., Marazzi, I., Agresti, A., Shimizu, N., Bianchi, M. E. and Natoli, G. (2006) A hyper-dynamic equilibrium between promoter-bound and nucleoplasmic dimers controls NF-kappaB-dependent gene activity. EMBO J., 25, 798-810.
45. Beck, M., Schmidt, A., Malmstroem, J., Claassen, M., Ori, A., Szymborska, A., Herzog, F., Rinner, O., Ellenberg, J. and Aebersold, R. (2011) The quantitative proteome of a human cell line. Mol. Syst. Biol., 7, 549.
46. Lahav, G., Rosenfeld, N., Sigal, A., Geva-Zatorsky, N., Levine, A. J., Elowitz, M. B. and Alon, U. (2004) Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet., 36, 147-150.
47. Smeenk, L., van Heeringen, S. J., Koeppel, M., Gilbert, B., Janssen-Megens, E., Stunnenberg, H. G. and Lohrum, M. (2011) Role of p53 serine 46 in p53 target gene regulation. PLoS ONE, 6, e17574.
48. Los, G. V. and Wood, K. (2007) The HaloTag: a novel technology for cell imaging and protein analysis. Methods Mol. Biol., 356, 195-208.
49. Rosenke, K., Samuel, M. A., McDowell, E. T., Toerne, M. A. and Fortunato, E. A. (2006) An intact sequence-specific DNA-binding domain is required for human cytomegalovirus-mediated sequestration of p53 and may promote in vivo binding to the viral genome during infection. Virology, 348, 19-34.
50. Crank, J. (1980) The Mathematics of Diffusion, 2nd edn. Oxford University Press, Oxford, UK.
51. Matsuoka, S., Shibata, T. and Ueda, M. (2009) Statistical analysis of lateral diffusion and multistate kinetics in single-molecule imaging. Biophys. J., 97, 1115-1124.
52. Crocker, J. C. and Grier, D. G. (1996) Methods of digital video microscopy for colloidal studies. J. Coll. Int. Sci., 179, 298-310.
53. Yeung, C., Shtrahman, M. and Wu, X. (2007) Stick-and-diffuse and caged diffusion: a comparison of two models of synaptic vesicle dynamics. Biophys. J., 92, 2271-2280.
54. Kues, T. and Kubitscheck, U. (2002) Single molecule motion perpendicular to the focal plane of a microscope: application to splicing factor dynamics within the cell nucleus. Single Mol., 3, 218-224.