Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus

eLife

Volumn 2014, Issue 3, 2014, Pages

  Izeddin, Ignacio ^a,b   Récamier, Vincent ^a,g   Bosanac, Lana ^a,c   Cissé, Ibrahim I ^a,b,h   Boudarene, Lydia ^a,b,d   Dugast Darzacq, Claire ^a,d   Proux, Florence ^a   Bénichou, Olivier ^e   Voituriez, Raphaël ^e   Bensaude, Olivier ^a   Dahan, Maxime ^b,c,f   Darzacq, Xavier ^a,c,i  

^a CNRS   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^f INSTITUT CURIE   (France)

^g Laboratory Imaging   (Czech Republic)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN T1; DENDRA2 PROTEIN; MYC PROTEIN; PEPTIDES AND PROTEINS; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DENDRA2 PROTEIN, DENDRONEPHTHYA; GREEN FLUORESCENT PROTEIN; HISTONE; PHOTOPROTEIN;

ARTICLE; ASSAY; CELL NUCLEUS; CONTROLLED STUDY; DIFFUSION; FLUORESCENCE IMAGING; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE TRANSLOCATION; GENETIC TRANSFECTION; GEOMETRY; HISTOGRAM; HUMAN; HUMAN CELL; INTERMITTENT DIFFUSION; MRNA EXPRESSION ASSAY; PARTICLE DIFFUSION; PHOTOTOXICITY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL NOISE RATIO; SIMULATION; SINGLE MOLECULE TRACKING ASSAY; METABOLISM; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL NUCLEUS; GREEN FLUORESCENT PROTEINS; HISTONES; HUMANS; LUMINESCENT PROTEINS; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTO-ONCOGENE PROTEINS C-MYC; TRANSCRIPTION FACTORS;

EID: 84903392046     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02230     Document Type: Article

References (79)

1. Abraham AV, Ram S, Chao J, Ward ES, Ober RJ. 2009. Quantitative study of single molecule location estimation techniques. Optics Express 17: 23352-23373. doi: 10. 1364/OE. 17. 023352.
2. Bancaud A, Lavelle C, Huet S, Ellenberg J. 2012. A fractal model for nuclear organization: current evidence and biological implications. Nucleic Acids Research 40: 8783-8792. doi: 10. 1093/nar/gks586.
3. Bancaud AEL, Huet SEB, Daigle N, Mozziconacci J, Beaudouin JEL, Ellenberg J. 2009. Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. The EMBO Journal 28: 3785-3798. doi: 10. 1038/emboj. 2009. 340.
4. ben-Avraham D, Havlin S. 2005. Diffusion and reactions in fractals and disordered systems. Cambridge University Press.
5. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642-1645. doi: 10. 1126/science. 1127344.
6. Bénichou O, Chevalier C, Klafter J, Meyer B, Voituriez R. 2010. Geometry-controlled kinetics. Nature Chemistry 2: 472-477. doi: 10. 1038/nchem. 622.
7. Bénichou O, Chevalier C, Meyer B, Voituriez R. 2011. Facilitated diffusion of proteins on chromatin. Physical Review Letters 106: 038102. doi: 10. 1103/PhysRevLett. 106. 038102.
8. Burov S, Tabei SMA, Huynh T, Murrell MP, Philipson LH, Rice SA, Gardel ML, Scherer NF, Dinner AR. 2013. Distribution of directional change as a signature of complex dynamics. Proceedings of the National Academy of Sciences of the United States of America 110: 19689-19694. doi: 10. 1073/pnas. 1319473110.
9. Cheezum MK, Walker WF, Guilford WH. 2001. Quantitative Comparison of algorithms for tracking single fluorescent particles. Biophysical Journal 81: 2378-2388. doi: 10. 1016/S0006-3495(01)75884-5.
10. Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A, Muresan L, Dugast-Darzacq C, Hajj B, Dahan M, Darzacq X. 2013. Real-time dynamics of RNA polymerase ii clustering in live human cells. Science 341: 664-667. doi: 10. 1126/science. 1239053.
11. Condamin S, Bénichou O, Moreau M. 2005. First-passage times for random walks in bounded domains. Physical Review Letters 95: 260601. doi: 10. 1103/PhysRevLett. 95. 260601.
12. Condamin S, Bénichou O, Tejedor V, Voituriez R, Klafter J. 2007. First-passage times in complex scale-invariant media. Nature 450: 77-80. doi: 10. 1038/nature06201.
13. Condamin S, Tejedor V, Voituriez R, Bénichou O, Klafter J. 2008. Probing microscopic origins of confined subdiffusion by first-passage observables. Proceedings of the National Academy of Sciences of the United States of America 105: 5675-5680. doi: 10. 1073/pnas. 0712158105.
14. Darzacq X, Singer RH. 2008. The dynamic range of transcription. Molecular Cell 30: 545-546. doi: 10. 1016/j. molcel. 2008. 05. 009.
15. Darzacq X, Yao J, Larson DR, Causse SZ, Bosanac L, de Turris V, Ruda VM, Lionnet T, Zenklusen D, Guglielmi B, Tjian R, Singer RH. 2009. Imaging transcription in living cells. Annual Review of Biophysics 38: 173-196. doi: 10. 1146/annurev. biophys. 050708. 133728.
16. de Gennes PG. 1982a. Kinetics of diffusion-controlled processes in dense polymer systems. I. Nonentangled regimes. The Journal of Chemical Physics 76: 3316. doi: 10. 1063/1. 443328.
17. de Gennes PG. 1982b. Kinetics of diffusion-controlled processes in dense polymer systems. II. Effects of entanglements. The Journal of Chemical Physics 76: 3322. doi: 10. 1063/1. 443329.
18. Dugast-Darzacq C, Grange T. 2009. MethylQuant: a real-time PCR-based method to quantify DNA methylation at single specific cytosines. Methods in Molecular Biology 507: 281-303. doi: 10. 1007/978-1-59745-522-0_21.
19. Dundr M. 2002. A kinetic framework for a mammalian RNA polymerase in vivo. Science 298: 1623-1626. doi: 10. 1126/science. 1076164.
20. Elf J, Li GW, Xie XS. 2007. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316: 1191-1194. doi: 10. 1126/science. 1141967.
21. English BP, Hauryliuk V, Sanamrad A, Tankov S, Dekker NH, Elf J. 2011. Single-molecule investigations of the stringent response machinery in living bacterial cells. Proceedings of the National Academy of Sciences of the United States of America 108: E365-E373. doi: 10. 1073/pnas. 1102255108.
22. Fong YW, Cattoglio C, Yamaguchi T, Tjian R. 2012. Transcriptional regulation by coactivators in embryonic stem cells. Trends in Cell Biology 22: 292-298. doi: 10. 1016/j. tcb. 2012. 04. 002.
23. Frost NA, Shroff H, Kong H, Betzig E, Blanpied TA. 2010. Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 67: 86-99. doi: 10. 1016/j. neuron. 2010. 05. 026.
24. Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM, Singer RH, Bertrand E. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Current Biology 13: 161-167. doi: 10. 1016/S0960-9822(02)01436-7.
25. Gallant P, Steiger D. 2009. Myc's secret life without Max. Cell Cycle 8: 3848-3853. doi: 10. 4161/cc. 8. 23. 10088.
26. Gebhardt JCM, Suter DM, Roy R, Zhao ZW, Chapman AR, Basu S, Maniatis T, Xie XS. 2013. Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nature Methods 10: 421-426. doi: 10. 1038/nmeth. 2411.
27. Gibcus JH, Dekker J. 2013. The hierarchy of the 3D genome. Molecular Cell 49: 773-782. doi: 10. 1016/j. molcel. 2013. 02. 011.
28. Gorski SA, Snyder SK, John S, Grummt I, Misteli T. 2008. Modulation of RNA polymerase assembly dynamics in transcriptional regulation. Molecular Cell 30: 486-497. doi: 10. 1016/j. molcel. 2008. 04. 021.
29. Grosberg A, Rabin Y, Havlin S, Neer A. 2007. Crumpled globule model of the three-dimensional structure of DNA. Europhysics Letters 23: 373-378. doi: 10. 1209/0295-5075/23/5/012.
30. Grünwald D, Martin RM, Buschmann V, Bazett-Jones DP, Leonhardt H, Kubitscheck U, Cardoso MC. 2008. Probing intranuclear environments at the single-molecule level. Biophysical Journal 94: 2847-2858. doi: 10. 1529/biophysj. 107. 115014.
31. Gurskaya NG, Verkhusha VV, Shcheglov AS, Staroverov DB, Chepurnykh TV, Fradkov AF, Lukyanov S, Lukyanov KA. 2006. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nature Biotechnology 24: 461-465. doi: 10. 1038/nbt1191.
32. Hager GL, McNally JG, Misteli T. 2009. Transcription dynamics. Molecular Cell 35: 741-753. doi: 10. 1016/j. molcel. 2009. 09. 005.
33. Heard E, Bickmore W. 2007. The ins and outs of gene regulation and chromosome territory organisation. Current Opinion in Cell Biology 19: 311-316. doi: 10. 1016/j. ceb. 2007. 04. 016.
34. Hess ST, Girirajan TPK, Mason MD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophysical Journal 91: 4258-4272. doi: 10. 1529/biophysj. 106. 091116.
35. Höfling F, Franosch T. 2013. Anomalous transport in the crowded world of biological cells. Reports on Progress in Physics 76: 046602. doi: 10. 1088/0034-4885/76/4/046602.
36. Itzkovitz S, van Oudenaarden A. 2011. Validating transcripts with probes and imaging technology. Nature Methods 8: S12-S19. doi: 10. 1038/nmeth. 1573.
37. Kopelman R. 1986. Rate-processes on fractals-Theory, simulations, and experiments. Journal of Statistical Physics 42: 185-200. doi: 10. 1007/BF01010846.
38. Kuhlman TE, Cox EC. 2012. Gene location and DNA density determine transcription factor distributions in Escherichia coli. Molecular Systems Biology 8: 1-13. doi: 10. 1038/msb. 2012. 42.
39. Larson DR, Singer RH, Zenklusen D. 2009. A single molecule view of gene expression. Trends in Cell Biology 19: 630-637. doi: 10. 1016/j. tcb. 2009. 08. 008.
40. Liao Y, Yang SK, Koh K, Matzger AJ, Biteen JS. 2012. Heterogeneous single-molecule diffusion in one-, two-, and three-dimensional microporous coordination polymers: directional, trapped, and immobile guests. Nano Letters 12: 3080-3085. doi: 10. 1021/nl300971t.
41. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326: 289-293. doi: 10. 1126/science. 1181369.
42. Lin CY, Lovén J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA. 2012. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151: 56-67. doi: 10. 1016/j. cell. 2012. 08. 026.
43. Lindenberg K, Sheu W-S, Kopelman R. 1991. Scaling properties of diffusion-limited reactions on fractal and euclidean geometries. Journal of Statistical Physics 65: 1269-1283. doi: 10. 1007/BF01049612.
44. Lippincott-Schwartz J, Patterson GH. 2009. Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends in Cell Biology 19: 555-565. doi: 10. 1016/j. tcb. 2009. 09. 003.
45. Lord SJ, Lee H-LD, Moerner WE. 2010. Single-molecule Spectroscopy and imaging of Biomolecules in living cells. Analytical Chemistry 82: 2192-2203. doi: 10. 1021/ac9024889.
46. Malchus N, Weiss M. 2009. Elucidating anomalous protein diffusion in living cells with fluorescence correlation spectroscopy-facts and pitfalls. Journal of Fluorescence 20: 19-26. doi: 10. 1007/s10895-009-0517-4.
47. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, Betzig E, Lippincott-Schwartz J. 2008. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nature Methods 5: 155-157. doi: 10. 1038/nmeth. 1176.
48. Mazza D, Abernathy A, Golob N, Morisaki T, McNally JG. 2012. A benchmark for chromatin binding measurements in live cells. Nucleic Acids Research 40: e119. doi: 10. 1093/nar/gks701.
49. Metzler R, Klafter J. 2000. The Random walk's guide to anomalous diffusion.
50. Meyer B, Bénichou O, Kafri Y, Voituriez R. 2012. Geometry-Induced Bursting dynamics in gene expression. Biophysical Journal 102: 2186-2191. doi: 10. 1016/j. bpj. 2012. 03. 060.
51. Michalet X. 2010. Mean square displacement analysis of single-particle trajectories with localization error: Brownian motion in an isotropic medium. Physical Review E 82: 041914. doi: 10. 1103/PhysRevE. 82. 041914.
52. Misteli T. 2001. Protein Dynamics: Implications for nuclear architecture and gene expression. Science 291: 843-847. doi: 10. 1126/science. 291. 5505. 843.
53. Mueller F, Mazza D, Stasevich TJ, McNally JG. 2010. FRAP and kinetic modeling in the analysis of nuclear protein dynamics: what do we really know? Current Opinion in Cell Biology 22: 403-411. doi: 10. 1016/j. ceb. 2010. 03. 002.
54. Mueller F, Wach P, McNally JG. 2008. Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophysical Journal 94: 3323-3339. doi: 10. 1529/biophysj. 107. 123182.
55. Nasse MJ, Woehl JC. 2010. Realistic modeling of the illumination point spread function in confocal scanning optical microscopy. Journal of the Optical Society of America A, Optics, Image Science, and Vision 27: 295-302. doi: 10. 1364/JOSAA. 27. 000295.
56. Nelson DL, Lehninger AL, Cox MM. 2008. Lehninger principles of Biochemistry.
57. Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W, Wang R, Green DR, Tessarollo L, Casellas R, Zhao K, Levens D. 2012. c-Myc is a universal amplifier of expressed genes in Lymphocytes and embryonic stem cells. Cell 151: 68-79. doi: 10. 1016/j. cell. 2012. 08. 033.
58. Normanno D, Dahan M, Darzacq X. 2012. Intra-nuclear mobility and target search mechanisms of transcription factors: a single-molecule perspective on gene expression. BBA-Gene Regulatory Mechanisms 1819: 482-493. doi: 10. 1016/j. bbagrm. 2012. 02. 001.
59. Parry BR, Surovtsev IV, Cabeen MT, O'Hern CS, Dufresne ER, Jacobs-Wagner C. 2014. The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. Cell 156: 183-194. doi: 10. 1016/j. cell. 2013. 11. 028.
60. Pederson T. 2000. Half a century of "the nuclear matrix". Molecular Biology of the Cell 11: 799-805. doi: 10. 1091/mbc. 11. 3. 799.
61. Phair R, Scaffidi P, Elbi C, Vecerova J, Dey A, Ozato K, Brown D, Hager G, Bustin M, Misteli T. 2004. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Molecular and Cellular Biology 24: 6393-6402. doi: 10. 1128/MCB. 24. 14. 6393-6402. 2004.
62. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. 2008. Imaging individual mRNA molecules using multiple singly labeled probes. Nature Methods 5: 877-879. doi: 10. 1038/nmeth. 1253.
63. Rice S. 1985. Diffusion-limited reactions.
64. Saxton MJ. 2007. A biological interpretation of transient anomalous subdiffusion. I. Qualitative model. Biophysical Journal 92: 1178-1191. doi: 10. 1529/biophysj. 106. 092619.
65. Saxton MJ. 2012. Wanted: a positive control for anomalous subdiffusion. Biophysical Journal 103: 2411-2422. doi: 10. 1016/j. bpj. 2012. 10. 038.
66. Schütz GJ, Schindler H, Schmidt T. 1997. Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophysical Journal 73: 1073-1080. doi: 10. 1016/S0006-3495(97)78139-6.
67. Shav-Tal Y, Darzacq X, Shenoy SM, Fusco D, Janicki SM, SPECTOR DL, Singer RH. 2004. Dynamics of single mRNPs in nuclei of living cells. Science 304: 1797-1800. doi: 10. 1126/science. 1099754.
68. Shlesinger M, Zaslavsky G. 1993. Strange kinetics. Nature.
69. Speil J, Baumgart E, Siebrasse J-P, Veith R, Vinkemeier U, Kubitscheck U. 2011. Activated STAT1 transcription factors conduct distinct saltatory movements in the cell nucleus. Biophysical Journal 101: 2592-2600. doi: 10. 1016/j. bpj. 2011. 10. 006.
70. Sprague BL, Pego RL, Stavreva DA, McNally JG. 2004. Analysis of binding reactions by fluorescence recovery after photobleaching. Biophysical Journal 86: 3473-3495. doi: 10. 1529/biophysj. 103. 026765.
71. Szymanski J, Weiss M. 2009. Elucidating the origin of anomalous diffusion in crowded fluids. Physical Review Letters 103: 038102. doi: 10. 1103/PhysRevLett. 103. 038102.
72. Taube R, Lin X, Irwin D, Fujinaga K, Peterlin BM. 2002. Interaction between p-TEFb and the c-terminal domain of RNA polymerase ii activates transcriptional elongation from sites upstream or downstream of target genes. Molecular and Cellular Biology 22: 321-331. doi: 10. 1128/MCB. 22. 1. 321-331. 2002.
73. Thompson RE, Larson DR, Webb WW. 2002. Precise nanometer localization analysis for individual fluorescent probes. Biophysical Journal 82: 2775-2783. doi: 10. 1016/S0006-3495(02)75618-X.
74. Tokunaga M, Imamoto N, Sakata-Sogawa K. 2008. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nature Methods 5: 159-161. doi: 10. 1038/nmeth1171.
75. Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert F-M, Vandermoere F, Morrice NA, Swift S, Rothbauer U, Leonhardt H, Lamond A. 2008. Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. The Journal of Cell Biology 183: 223-239. doi: 10. 1083/jcb. 200805092.
76. Wada T, Takagi T, Yamaguchi Y, Watanabe D, Handa H. 1998. Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. The EMBO Journal 17: 7395-7403. doi: 10. 1093/emboj/17. 24. 7395.
77. Yao J, Fetter RD, Hu P, Betzig E, Tjian R. 2011. Subnuclear segregation of genes and core promoter factors in myogenesis. Genes & Development 25: 569-580. doi: 10. 1101/gad. 2021411.
78. Zenklusen D, Larson DR, Singer RH. 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nature Structural & Molecular Biology 15: 1263-1271. doi: 10. 1038/nsmb. 1514.
79. Zhou Q, Li T, Price DH. 2012. RNA polymerase ii elongation control. Annual Review of Biochemistry 81: 119-143. doi: 10. 1146/annurev-biochem-052610-095910.