Retrieving the intracellular topology from multi-scale protein mobility mapping in living cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Baum, Michael ^a   Erdel, Fabian ^a   Wachsmuth, Malte ^b   Rippe, Karsten ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; GREEN FLUORESCENT PROTEIN; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1 BETA; MONOMER; POLYMER; STAT2 PROTEIN; UNCLASSIFIED DRUG; VIMENTIN; CHROMATIN; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HYBRID PROTEIN; NONHISTONE PROTEIN; PROTEIN; QUANTUM DOT;

ENZYME ACTIVITY; MAPPING; MOLECULAR ANALYSIS; PROTEIN; SPECTROSCOPY;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELL STRUCTURE; CONFOCAL MICROSCOPY; CYTOPLASM; CYTOSKELETON; DATA PROCESSING; DEPOLYMERIZATION; DIFFUSION; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERMEDIATE FILAMENT; INTRACELLULAR SPACE; NUCLEOSOME; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SIGNAL PROCESSING; CELL LINE; CHROMATIN; DEVICES; GENETICS; IMAGE PROCESSING; METABOLISM; PROCEDURES; SPECTROFLUOROMETRY;

CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CYTOPLASM; CYTOSKELETON; DIFFUSION; GREEN FLUORESCENT PROTEINS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; PROTEIN TRANSPORT; PROTEINS; QUANTUM DOTS; RECOMBINANT FUSION PROTEINS; SPECTROMETRY, FLUORESCENCE; STAT2 TRANSCRIPTION FACTOR;

EID: 84905042146     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5494     Document Type: Article

References (69)

1. Benichou, O., Chevalier, C., Klafter, J., Meyer, B. & Voituriez, R. Geometry-controlled kinetics. Nat. Chem. 2, 472-477 (2010).
2. Eltsov, M., Maclellan, K. M., Maeshima, K., Frangakis, A. S. & Dubochet, J. Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc. Natl Acad. Sci. USA 105, 19732-19737 (2008).
3. Wombacher, R. et al. Live-cell super-resolution imaging with trimethoprim conjugates. Nat. Methods 7, 717-719 (2010).
4. Le Bihan, D. Looking into the functional architecture of the brain with diffusion MRI. Nat. Rev. Neurosci. 4, 469-480 (2003). (Pubitemid 37280168)
5. Latour, L. L., Svoboda, K., Mitra, P. P. & Sotak, C. H. Time-dependent diffusion of water in a biological model system. Proc. Natl Acad. Sci. USA 91, 1229-1233 (1994). (Pubitemid 24058983)
6. Mitra, P. P., Sen, P. N. & Schwartz, L. M. Short-time behavior of the diffusion coefficient as a geometrical probe of porous media. Phys. Rev. B Condens. Matter 47, 8565-8574 (1993).
7. Sen, P. N. Time-dependent diffusion coefficient as a probe of geometry. Concept. Magn. Reson. A 23A, 1-21 (2004). (Pubitemid 40646215)
8. Song, Y. Q., Ryu, S. & Sen, P. N. Determining multiple length scales in rocks. Nature 406, 178-181 (2000). (Pubitemid 30468997)
9. Bacia, K., Kim, S. A. & Schwille, P. Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 3, 83-89 (2006). (Pubitemid 43173305)
10. Capoulade, J., Wachsmuth, M., Hufnagel, L. & Knop, M. Quantitative fluorescence imaging of protein diffusion and interaction in living cells. Nat. Biotechnol. 29, 835-839 (2011).
11. Machan, R. & Wohland, T. Recent applications of fluorescence correlation spectroscopy in live systems. FEBS Lett. doi: 10.1016/j.febslet. 2014.03.056 (2014).
12. Heuvelman, G., Erdel, F., Wachsmuth, M. & Rippe, K. Analysis of protein mobilities and interactions in living cells by multifocal fluorescence fluctuation microscopy. Eur. Biophys. J. 38, 813-828 (2009).
13. Digman, M. A. & Gratton, E. Imaging barriers to diffusion by pair correlation functions. Biophys. J. 97, 665-673 (2009).
14. Ruan, Q., Cheng, M. A., Levi, M., Gratton, E. & Mantulin, W. W. Spatial-temporal studies of membrane dynamics: scanning fluorescence correlation spectroscopy (SFCS). Biophys. J. 87, 1260-1267 (2004). (Pubitemid 39095102)
15. Ries, J., Chiantia, S. & Schwille, P. Accurate determination of membrane dynamics with line-scan FCS. Biophys. J. 96, 1999-2008 (2009).
16. Di Rienzo, C., Gratton, E., Beltram, F. & Cardarelli, F. Fast spatiotemporal correlation spectroscopy to determine protein lateral diffusion laws in live cell membranes. Proc. Natl Acad. Sci. USA 110, 12307-12312 (2013).
17. Wachsmuth, M., Waldeck, W. & Langowski, J. Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy. J. Mol. Biol. 298, 677-689 (2000).
18. Weiss, M., Elsner, M., Kartberg, F. & Nilsson, T. Anomalous subdiffusion is a measure for cytoplasmic crowding in living cells. Biophys. J. 87, 3518-3524 (2004). (Pubitemid 40468604)
19. Bunde, A. & Havlin, S. Fractals and Disordered Systems 2nd edn (Springer-Verlag, 1995).
20. McNally, J. G. & Mazza, D. Fractal geometry in the nucleus. EMBO J. 29, 2-3 (2010).
21. Loskutov, V. V. & Sevriugin, V. A. A novel approach to interpretation of the time-dependent self-diffusion coefficient as a probe of porous media geometry. J. Magn. Reson. 230C, 1-9 (2013).
22. Görisch, S. M. et al. Nuclear body movement is determined by chromatin accessibility and dynamics. Proc. Natl Acad. Sci. USA 101, 13221-13226 (2004). (Pubitemid 39209646)
23. Dertinger, T. et al. Two-focus fluorescence correlation spectroscopy: a new tool for accurate and absolute diffusion measurements. Chemphyschem. 8, 433-443 (2007).
24. Braga, J., Desterro, J. M. & Carmo-Fonseca, M. Intracellular macromolecular mobility measured by fluorescence recovery after photobleaching with confocal laser scanning microscopes. Mol. Biol. Cell 15, 4749-4760 (2004). (Pubitemid 39299119)
25. Erdel, F. & Rippe, K. Quantifying transient binding of ISWI chromatin remodelers in living cells by pixel-wise photobleaching profile evolution analysis. Proc. Natl Acad. Sci. USA 109, E3221-E3230 (2012).
26. Hinde, E., Cardarelli, F., Digman, M. A. & Gratton, E. In vivo pair correlation analysis of EGFP intranuclear diffusion reveals DNA-dependent molecular flow. Proc. Natl Acad. Sci. USA 107, 16560-16565 (2010).
27. Dross, N. et al. Mapping eGFP oligomer mobility in living cell nuclei. PLoS ONE 4, e5041 (2009).
28. Pack, C., Saito, K., Tamura, M. & Kinjo, M. Microenvironment and effect of energy depletion in the nucleus analyzed by mobility of multiple oligomeric EGFPs. Biophys. J. 91, 3921-3936 (2006). (Pubitemid 44788334)
29. Moeendarbary, E. et al. The cytoplasm of living cells behaves as a poroelastic material. Nat. Mater. 12, 253-261 (2013).
30. Phillips, R. J. A hydrodynamic model for hindered diffusion of proteins and micelles in hydrogels. Biophys. J. 79, 3350-3353 (2000).
31. Luby-Phelps, K. et al. A novel fluorescence ratiometric method confirms the low solvent viscosity of the cytoplasm. Biophys. J. 65, 236-242 (1993). (Pubitemid 23206057)
32. Swaminathan, R., Hoang, C. P. & Verkman, A. S. Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion. Biophys. J. 72, 1900-1907 (1997). (Pubitemid 27133128)
33. Schliwa, M. Action of cytochalasin D on cytoskeletal networks. J. Cell Biol. 92, 79-91 (1982). (Pubitemid 12138113)
34. Grin, B. et al. Withaferin a alters intermediate filament organization, cell shape and behavior. PLoS ONE 7, e39065 (2012).
35. Wadsworth, P. & McGrail, M. Interphase microtubule dynamics are cell type-specific. J. Cell Sci. 95, 23-32 (1990).
36. Fejes Tóth, K. et al. Trichostatin A induced histone acetylation causes decondensation of interphase chromatin. J. Cell Sci. 117, 4277-4287 (2004). (Pubitemid 39328314)
37. Görisch, S. M., Wachsmuth, M., Fejes Tóth, K., Lichter, P. & Rippe, K. Histone acetylation increases chromatin accessibility. J. Cell Sci. 118, 5825-5834 (2005). (Pubitemid 43079275)
38. Krajewski, W. A. Alterations in the internucleosomal DNA helical twist in chromatin of human erythroleukemia cells in vivo influences the chromatin higher-order folding. FEBS Lett. 361, 149-152 (1995).
39. Ogara, M. F. et al. Chromatin relaxation-mediated induction of p19INK4d increases the ability of cells to repair damaged DNA. PLoS ONE 8, e61143 (2013).
40. Toiber, D. et al. SIRT6 recruits SNF2H to sites of DNA breaks, preventing genomic instability through chromatin remodeling. Mol. Cell 51, 454-468 (2013).
41. Nakamura, K. et al. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol. Cell 41, 515-528 (2011).
42. Frahm, T., Hauser, H. & Köster, M. IFN-type-I-mediated signaling is regulated by modulation of STAT2 nuclear export. J. Cell Sci. 119, 1092-1104 (2006).
43. Levy, D. E. & Darnell, Jr J. E. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3, 651-662 (2002). (Pubitemid 34987786)
44. Vermeulen, M. et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142, 967-980 (2010).
45. Erdel, F., Müller-Ott, K., Baum, M., Wachsmuth, M. & Rippe, K. Dissecting chromatin interactions in living cells from protein mobility maps. Chromosome Res. 19, 99-115 (2011).
46. Bancaud, A. et al. Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J. 28, 3785-3798 (2009).
47. Bancaud, A., Lavelle, C., Huet, S. & Ellenberg, J. A fractal model for nuclear organization: current evidence and biological implications. Nucleic Acids Res. 40, 8783-8792 (2012).
48. Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).
49. Hofling, F. & Franosch, T. Anomalous transport in the crowded world of biological cells. Rep. Prog. Phys. 76, 046602 (2013).
50. Fritsch, C. C. & Langowski, J. Anomalous diffusion in the interphase cell nucleus: the effect of spatial correlations of chromatin. J. Chem. Phys. 133, 025101 (2010).
51. Maeshima, K., Hihara, S. & Eltsov, M. Chromatin structure: does the 30-nm fibre exist in vivo? Curr. Opin. Cell Biol. 22, 291-297 (2010).
52. Fussner, E., Ching, R. W. & Bazett-Jones, D. P. Living without 30 nm chromatin fibers. Trends Biochem. Sci. 36, 1-6 (2011).
53. Rippe, K. Dynamic organization of the cell nucleus. Curr. Opin. Genet. Dev. 17, 373-380 (2007). (Pubitemid 350016898)
54. Yan, Y. & Marriott, G. Analysis of protein interactions using fluorescence technologies. Curr. Opin. Chem. Biol. 7, 635-640 (2003). (Pubitemid 37315801)
55. Guigas, G. & Weiss, M. Sampling the cell with anomalous diffusion-the discovery of slowness. Biophys. J. 94, 90-94 (2008).
56. Cremer, T. & Cremer, M. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2, a003889 (2010).
57. Kind, J. & van Steensel, B. Genome-nuclear lamina interactions and gene regulation. Curr. Opin. Cell Biol. 22, 320-325 (2010).
58. Probst, A. V. & Almouzni, G. Pericentric heterochromatin: dynamic organization during early development in mammals. Differentiation 76, 15-23 (2008).
59. Feuerbach, F. et al. Nuclear architecture and spatial positioning help establish transcriptional states of telomeres in yeast. Nat. Cell Biol. 4, 214-221 (2002). (Pubitemid 34218195)
60. Agmon, N., Liefshitz, B., Zimmer, C., Fabre, E. & Kupiec, M. Effect of nuclear architecture on the efficiency of double-strand break repair. Nat. Cell Biol. 15, 694-699 (2013).
61. Erdel, F., Müller-Ott, K. & Rippe, K. Establishing epigenetic domains via chromatin-bound histone modifiers. Ann. NY Acad. Sci. 1305, 29-43 (2013).
62. Meshorer, E. et al. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10, 105-116 (2006). (Pubitemid 43025681)
63. Gaspar-Maia, A., Alajem, A., Meshorer, E. & Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 12, 36-47 (2011).
64. Slater, A. F. Chloroquine: mechanism of drug action and resistance in Plasmodium falciparum. Pharmacol. Ther. 57, 203-235 (1993).
65. Erdel, F., Krug, J., Längst, G. & Rippe, K. Targeting chromatin remodelers: signals and search mechanisms. Biochim. Biophys. Acta 1809, 497-508 (2011).
66. Pommier, Y., Leo, E., Zhang, H. & Marchand, C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol. 17, 421-433 (2010).
67. Marks, P. A. Histone deacetylase inhibitors: a chemical genetics approach to understanding cellular functions. Biochim. Biophys. Acta 1799, 717-725 (2010).
68. Galassi, M. et al. Gnu Scientific Library: Reference Manual (Network Theory Ltd, 2003).
69. Muller, C. B., Weiss, K., Richtering, W., Loman, A. & Enderlein, J. Calibrating differential interference contrast microscopy with dual-focus fluorescence correlation spectroscopy. Opt. Express 16, 4322-4329 (2008). (Pubitemid 351434402)