Intra-nuclear mobility and target search mechanisms of transcription factors: A single-molecule perspective on gene expression

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 6, 2012, Pages 482-493

  Normanno, Davide ^a,b,c,d   Dahan, Maxime ^b,c   Darzacq, Xavier ^a,c  

^a PSL RESEARCH UNIVERSITY   (France)

^b LABORATOIRE KASTLER BROSSEL   (France)

^c HHMI Janelia Farm Research Campus   (United States)

^d Fondation Pierre Gilles de Gennes   (France)

Author keywords

Facilitated diffusion; Gene expression regulation; Single molecule analysis; Target search; Transcription factor

Indexed keywords

TRANSCRIPTION FACTOR;

CELL MOTILITY; DIFFUSION; EUKARYOTE; GENE EXPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; CELL SURVIVAL; DNA; EUKARYOTA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HUMANS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EUKARYOTA; PROKARYOTA;

EID: 84860440982     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.02.001     Document Type: Review

References (213)

1. Simon I., Barnett J., Hannett N., Harbison C.T., Rinaldi N.J., Volkert T.L., Wyrick J.J., Zeitlinger J., Gifford D.K., Jaakkola T.S., Young R.A. Serial regulation of transcriptional regulators in the yeast cell cycle. Cell 2001, 106:697-708.
2. Dynlacht B.D. Regulation of transcription by proteins that control the cell cycle. Nature 1997, 389:149-152.
3. Accili D., Arden K.C. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004, 117:421-426.
4. Bain G., Maandag E.C.R., Izon D.J., Amsen D., Kruisbeek A.M., Weintraub B.C., Krop I., Schlissel M.S., Feeney A.J., van Roon M., van der Valk M., te Riele H.P.J., Berns A., Murre C. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 1994, 79:885-892.
5. Furney S., Higgins D., Ouzounis C., Lopez-Bigas N. Structural and functional properties of genes involved in human cancer. BMC Genomics 2006, 7:3.
6. Boyadjiev S., Jabs E. Online Mendelian Inheritance in Man (OMIM) as a knowledgebase for human developmental disorders. Clin. Genet. 2000, 57:253-266.
7. Bustamante C.D., Fledel-Alon A., Williamson S., Nielsen R., Todd Hubisz M., Glanowski S., Tanenbaum D.M., White T.J., Sninsky J.J., Hernandez R.D., Civello D., Adams M.D., Cargill M., Clark A.G. Natural selection on protein-coding genes in the human genome. Nature 2005, 437:1153-1157.
8. De S., Lopez-Bigas N., Teichmann S. Patterns of evolutionary constraints on genes in humans. BMC Evol. Biol. 2008, 8:275.
9. C.Human Genome Sequencing Finishing the euchromatic sequence of the human genome. Nature 2004, 431:931-945.
10. Core L.J., Waterfall J.J., Lis J.T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
11. Jackson D.A., Iborra F.J., Manders E.M.M., Cook P.R. Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei. Mol. Biol. Cell. 1998, 9:1523-1536.
12. Suter D.M., Molina N., Gatfield D., Schneider K., Schibler U., Naef F. Mammalian genes are transcribed with widely different bursting kinetics. Science 2011, 332:472-474.
13. Harper C.V., Finkenstädt B., Woodcock D.J., Friedrichsen S., Semprini S., Ashall L., Spiller D.G., Mullins J.J., Rand D.A., Davis J.R.E., White M.R.H. Dynamic analysis of stochastic transcription cycles. PLoS Biol. 2011, 9:e1000607.
14. Latchman D.S. Eukaryotic Transcription Factors 1998, Academic Press, San Diego.
15. Greive S.J., von Hippel P.H. Thinking quantitatively about transcriptional regulation. Nat. Rev. Mol. Cell Biol. 2005, 6:221-232.
16. Hager G.L., McNally J.G., Misteli T. Transcription dynamics. Mol. Cell 2009, 35:741-753.
17. Darzacq X., Yao J., Larson D.R., Causse S.Z., Bosanac L., de Turris V., Ruda V.M., Lionnet T., Zenklusen D., Guglielmi B., Tjian R., Singer R.H. Imaging transcription in living cells. Annu. Rev. Biophys. 2009, 38:173-196.
18. Cramer P., Bushnell D.A., Kornberg R.D. Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science 2001, 292:1863-1876.
19. Sikorski T.W., Buratowski S. The basal initiation machinery: beyond the general transcription factors. Curr. Opin. Cell Biol. 2009, 21:344-351.
20. Deato M.D.E., Tjian R. Switching of the core transcription machinery during myogenesis. Genes Dev. 2007, 21:2137-2149.
21. Lemon B., Tjian R. Orchestrated response: a symphony of transcription factors for gene control. Genes Dev. 2000, 14:2551-2569.
22. Carter D.R.F., Eskiw C., Cook P.R. Transcription factories. Biochem. Soc. Trans. 2008, 36:585-589.
23. Yu J., Xiao J., Ren X., Lao K., Xie X.S. Probing gene expression in live cells, one protein molecule at a time. Science 2006, 311:1600-1603.
24. Franco E., Friedrichs E., Kim J., Jungmann R., Murray R., Winfree E., Simmel F.C. Timing molecular motion and production with a synthetic transcriptional clock. Proc. Natl. Acad. Sci. 2011, 108:E784-E793.
25. McClintock B. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. 1950, 36:344-355.
26. Jacob F., Monod J. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 1961, 3:318-356.
27. Bourgeois S., Cohn M., Orgel L.E. Suppression of and complementation among mutants of the regulatory gene of the lactose operon of Escherichia coli. J. Mol. Biol. 1965, 14:300-302.
28. Gilbert W., Müller-Hill B. The lac operator is DNA. Proc. Natl. Acad. Sci. 1967, 58:2415-2421.
29. Kania J., Müller-Hill B. Construction, isolation and implications of repressor-galactosidase·ß-galactosidase hybrid molecules. Eur. J. Biochem. 1977, 79:381-386.
30. Krämer H., Niemöller M., Amouyal M., Revet B., von Wilcken-Bergmann B., Müller-Hill B. Lac repressor forms loops with linear DNA carrying two suitably spaced lac operators. EMBO J. 1987, 6:1481-1491.
31. Lewis M., Chang G., Horton N.C., Kercher M.A., Pace H.C., Schumacher M.A., Brennan R.G., Lu P. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 1996, 271:1247-1254.
32. D. Normanno, Biochemistry and mechanics of gene expression regulation by lac repressor at the single-molecule level, Ph.D. thesis - European Laboratory for Non-linear Spectroscopy (LENS) - University of Florence (Italy), 2007, pp. 235.
33. Hsieh W.T., Whitson P.A., Matthews K.S., Wells R.D. Influence of sequence and distance between two operators on interaction with the lac repressor. J. Biol. Chem. 1987, 262:14583-14591.
34. Müller J., Oehler S., Müller-Hill B. Repression of lac promoter as a function of distance, phase and quality of an auxiliary lac operator. J. Mol. Biol. 1996, 257:21-29.
35. Whitson P.A., Hsieh W.T., Wells R.D., Matthews K.S. Supercoiling facilitates lac operator-repressor-pseudooperator interactions. J. Biol. Chem. 1987, 262:4943-4946.
36. Normanno D., Vanzi F., Pavone F.S. Single-molecule manipulation reveals supercoiling-dependent modulation of lac repressor-mediated DNA looping. Nucleic Acids Res. 2008, 36:2505-2513.
37. Lia G., Bensimon D., Croquette V., Allemand J.-F., Dunlap D., Lewis D.E.A., Adhya S., Finzi L. Supercoiling and denaturation in Gal repressor/heat unstable nucleoid protein (HU)-mediated DNA looping. Proc. Natl. Acad. Sci. 2003, 100:11373-11377.
38. Matthews K.S. DNA looping. Microbiol. Mol. Biol. Rev. 1992, 56:123-136.
39. Schleif R. DNA looping. Annu. Rev. Biochem. 1992, 61:199-223.
40. Halford S.E., Welsh A.J., Szczelkun M.D. Enzyme-mediated DNA looping. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:1-24.
41. van den Broek B., Vanzi F., Normanno D., Pavone F.S., Wuite G.J.L. Real-time observation of DNA looping dynamics of type IIE restriction enzymes NaeI and NarI. Nucleic Acids Res. 2006, 34:167-174.
42. Capitanio M., Vanzi F., Broggio C., Cicchi R., Normanno D., Romano G., Sacconi L., Pavone F.S. Exploring molecular motors and switches at the single-molecule level. Microsc. Res. Tech. 2004, 65:194-204.
43. Mossing M.C., Record M.T. Upstream operators enhance repression of the lac promoter. Science 1986, 233:889-892.
44. Blattner F.R., Plunkett G., Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453-1462.
45. Gilbert W., Müller-Hill B. Isolation of the lac repressor. Proc. Natl. Acad. Sci. 1966, 56:1891-1898.
46. Riggs A.D., Bourgeois S., Newby R.F., Cohn M. DNA binding of the lac repressor. J. Mol. Biol. 1968, 34:365-368.
47. Riggs A.D., Bourgeois S., Cohn M. The lac represser-operator interaction: III. Kinetic studies. J. Mol. Biol. 1970, 53:401-417.
48. von Smoluchowski M. Versuch einer mathematischen theorie der koagulationskinetik kolloier lösungen. Z. Phys. Chem. 1917, 92:129-168.
49. Alberty R.A., Hammes G.G. Application of the theory of diffusion-controlled reactions to enzyme kinetics. J. Phys. Chem. 1958, 62:154-159.
50. Berg H. Random Walks in Biology 1993, Princeton University Press.
51. Berg O.G., von Hippel P.H. Diffusion-controlled macromolecular interactions. Annu. Rev. Biophys. Biophys. Chem. 1985, 14:131-158.
52. Riggs A.D., Suzuki H., Bourgeois S. lac repressor-operator interaction: I. Equilibrium studies. J. Mol. Biol. 1970, 48:67-83.
53. Bourgeois S., Riggs A.D. The lac repressor-operator interaction IV. Assay and purification of operator DNA. Biochem. Biophys. Res. Commun. 1970, 38:348-354.
54. Halford S.E. An end to 40 years of mistakes in DNA-protein association kinetics?. Biochem. Soc. Trans. 2009, 37:343-348.
55. Ptashne M. Specific binding of the λ phage repressor to λ DNA. Nature 1967, 214:232-234.
56. Berg O.G., Winter R.B., Von Hippel P.H. Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 1981, 20:6929-6948.
57. Halford S.E., Marko J.F. How do site-specific DNA-binding proteins find their targets?. Nucleic Acids Res. 2004, 32:3040-3052.
58. Mirny L., Slutsky M., Wunderlich Z., Tafvizi A., Leith J., Kosmrlj A. How a protein searches for its site on DNA: the mechanism of facilitated diffusion. J. Phys. A: Math. Theor. 2009, 42:434013.
59. Bénichou O., Loverdo C., Moreau M., Voituriez R. Intermittent search strategies. Rev. Mod. Phys. 2011, 83:81.
60. von Hippel P.H., Berg O.G. Facilitated target location in biological systems. J. Biol. Chem. 1989, 264:675-678.
61. Loverdo C., Bénichou O., Voituriez R., Biebricher A., Bonnet I., Desbiolles P. Quantifying hopping and jumping in facilitated diffusion of DNA-binding proteins. Phys. Rev. Lett. 2009, 102:188101.
62. Díaz de la Rosa M.A., Koslover E.F., Mulligan P.J., Spakowitz A.J. Dynamic strategies for target-site search by DNA-binding proteins. Biophys. J. 2010, 98:2943-2953.
63. Reingruber J., Holcman D. Transcription factor search for a DNA promoter in a three-state model. Phys. Rev. E 2011, 84:020901.
64. Iwahara J., Zweckstetter M., Clore G.M. NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA. Proc. Natl. Acad. Sci. 2006, 103:15062-15067.
65. Doucleff M., Clore G.M. Global jumping and domain-specific intersegment transfer between DNA cognate sites of the multidomain transcription factor Oct-1. Proc. Natl. Acad. Sci. 2008, 105:13871-13876.
66. Vuzman D., Levy Y. DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail. Proc. Natl. Acad. Sci. 2010, 107:21004-21009.
67. Gowers D.M., Halford S.E. Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J. 2003, 22:1410-1418.
68. van den Broek B., Lomholt M.A., Kalisch S.M.J., Metzler R., Wuite G.J.L. How DNA coiling enhances target localization by proteins. Proc. Natl. Acad. Sci. 2008, 105:15738-15742.
69. Lomholt M.A., van den Broek B., Kalisch S.-M.J., Wuite G.J.L., Metzler R. Facilitated diffusion with DNA coiling. Proc. Natl. Acad. Sci. 2009, 106:8204-8208.
70. Hu T., Grosberg A.Y., Shklovskii B.I. How proteins search for their specific sites on DNA: the role of DNA conformation. Biophys. J. 2006, 90:2731-2744.
71. Wunderlich Z., Mirny L.A. Spatial effects on the speed and reliability of protein-DNA search. Nucleic Acids Res. 2008, 36:3570-3578.
72. Coppey M., Bénichou O., Voituriez R., Moreau M. Kinetics of target site localization of a protein on DNA: A stochastic approach. Biophys. J. 2004, 87:1640-1649.
73. Slutsky M., Mirny L.A. Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys. J. 2004, 87:4021-4035.
74. Privalov P.L., Dragan A.I., Crane-Robinson C. Interpreting protein/DNA interactions: distinguishing specific from non-specific and electrostatic from non-electrostatic components. Nucleic Acids Res. 2011, 39:2483-2491.
75. Barkley M.D. Salt dependence of the kinetics of the lac repressor-operator interaction: role of nonoperator deoxyribonucleic acid (DNA) in the association reaction. Biochemistry 1981, 20:3833-3842.
76. Lu P., Vogel C., Wang R., Yao X., Marcotte E.M. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 2007, 25:117-124.
77. Taniguchi Y., Choi P.J., Li G.-W., Chen H., Babu M., Hearn J., Emili A., Xie X.S. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2011, 329:533-538.
78. Ghaemmaghami S., Huh W.-K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
79. Vaquerizas J.M., Kummerfeld S.K., Teichmann S.A., Luscombe N.M. A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 2009, 10:252-263.
80. Charoensawan V., Wilson D., Teichmann S.A. Genomic repertoires of DNA-binding transcription factors across the tree of life. Nucleic Acids Res. 2010, 38:7364-7377.
81. Jolma A., Kivioja T., Toivonen J., Cheng L., Wei G., Enge M., Taipale M., Vaquerizas J.M., Yan J., Sillanpää M.J., Bonke M., Palin K., Talukder S., Hughes T.R., Luscombe N.M., Ukkonen E., Taipale J. Multiplexed massively parallel SELEX for characterization of human transcription factor binding specificities. Genome Res. 2011, 20:861-873.
82. Kalodimos C.G., Biris N., Bonvin A.M.J.J., Levandoski M.M., Guennuegues M., Boelens R., Kaptein R. Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science 2004, 305:386-389.
83. Wilson M.D., Barbosa-Morais N.L., Schmidt D., Conboy C.M., Vanes L., Tybulewicz V.L.J., Fisher E.M.C., Tavaré S., Odom D.T. Species-specific transcription in mice carrying human chromosome 21. Science 2008, 322:434-438.
84. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., Kuznetsov H., Wang C.-F., Coburn D., Newburger D.E., Morris Q., Hughes T.R., Bulyk M.L. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
85. Tuupanen S., Turunen M., Lehtonen R., Hallikas O., Vanharanta S., Kivioja T., Bjorklund M., Wei G., Yan J., Niittymaki I., Mecklin J.-P., Jarvinen H., Ristimaki A., Di-Bernardo M., East P., Carvajal-Carmona L., Houlston R.S., Tomlinson I., Palin K., Ukkonen E., Karhu A., Taipale J., Aaltonen L.A. The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling. Nat. Genet. 2009, 41:885-890.
86. Robertson A.G., Bilenky M., Tam A., Zhao Y., Zeng T., Thiessen N., Cezard T., Fejes A.P., Wederell E.D., Cullum R., Euskirchen G., Krzywinski M., Birol I., Snyder M., Hoodless P.A., Hirst M., Marra M.A., Jones S.J.M. Genome-wide relationship between histone H3 lysine 4 mono- and tri-methylation and transcription factor binding. Genome Res. 2008, 18:1906-1917.
87. Heintzman N.D., Hon G.C., Hawkins R.D., Kheradpour P., Stark A., Harp L.F., Ye Z., Lee L.K., Stuart R.K., Ching C.W., Ching K.A., Antosiewicz-Bourget J.E., Liu H., Zhang X., Green R.D., Lobanenkov V.V., Stewart R., Thomson J.A., Crawford G.E., Kellis M., Ren B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
88. Badis G., Chan E.T., van Bakel H., Pena-Castillo L., Tillo D., Tsui K., Carlson C.D., Gossett A.J., Hasinoff M.J., Warren C.L., Gebbia M., Talukder S., Yang A., Mnaimneh S., Terterov D., Coburn D., Li Yeo A., Yeo Z.X., Clarke N.D., Lieb J.D., Ansari A.Z., Nislow C., Hughes T.R. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 2008, 32:878-887.
89. Chakrabarti J., Chandra N., Raha P., Roy S. High-affinity quasi-specific sites in the genome: How the DNA-binding proteins cope with them. Biophys. J. 2011, 101:1123-1129.
90. Burger A., Walczak A.M., Wolynes P.G. Abduction and asylum in the lives of transcription factors. Proc. Natl. Acad. Sci. 2010, 107:4016-4021.
91. Condamin S., Bénichou O., Tejedor V., Voituriez R., Klafter J. First-passage times in complex scale-invariant media. Nature 2007, 450:77-80.
92. Garcia H.G., Phillips R. Quantitative dissection of the simple repression input-output function. Proc. Natl. Acad. Sci. 2011, 108:12173-12178.
93. Duan Z., Andronescu M., Schutz K., McIlwain S., Kim Y.J., Lee C., Shendure J., Fields S., Blau C.A., Noble W.S. A three-dimensional model of the yeast genome. Nature 2010, 465:363-367.
94. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L.A., Lander E.S., Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
95. Tanizawa H., Iwasaki O., Tanaka A., Capizzi J.R., Wickramasinghe P., Lee M., Fu Z., Noma K. Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation. Nucleic Acids Res. 2010, 38:8164-8177.
96. Hu Z., Killion P.J., Iyer V.R. Genetic reconstruction of a functional transcriptional regulatory network. Nat. Genet. 2007, 39:683-687.
97. Dai Z., Dai X. Nuclear colocalization of transcription factor target genes strengthens coregulation in yeast. Nucleic Acids Res. 2012, 40:27-36.
98. DeSantis M.C., Li J.-L., Wang Y.M. Protein sliding and hopping kinetics on DNA. Phys. Rev. E 2011, 83:021907.
99. Zhou H.-X. Rapid search for specific sites on DNA through conformational switch of nonspecifically bound proteins. Proc. Natl. Acad. Sci. 2011, 108:8651-8656.
100. Thompson R.E., Larson D.R., Webb W.W. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 2002, 82:2775-2783.
101. Yildiz A., Forkey J.N., McKinney S.A., Ha T., Goldman Y.E., Selvin P.R. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 2003, 300:2061-2065.
102. Smith C.S., Joseph N., Rieger B., Lidke K.A. Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat. Methods 2010, 7:373-375.
103. Mortensen K.I., Churchman L.S., Spudich J.A., Flyvbjerg H. Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat. Methods 2010, 7:377-381.
104. van Mameren J., Peterman E.J.G., Wuite G.J.L. See me, feel me: methods to concurrently visualize and manipulate single DNA molecules and associated proteins. Nucleic Acids Res. 2008, 36:4381-4389.
105. Gorman J., Greene E.C. Visualizing one-dimensional diffusion of proteins along DNA. Nat. Struct. Mol. Biol. 2008, 15:768-774.
106. Kabata H., Kurosawa O., Arai I., Washizu M., Margarson S.A., Glass R.E., Shimamoto N. Visualization of single molecules of RNA polymerase sliding along DNA. Science 1993, 262:1561-1563.
107. Harada Y., Funatsu T., Murakami K., Nonoyama Y., Ishihama A., Yanagida T. Single-molecule imaging of RNA polymerase-DNA interactions in real time. Biophys. J. 1999, 76:709-715.
108. Bensimon D., Simon A.J., Croquette V., Bensimon A. Stretching DNA with a receding meniscus: experiments and models. Phys. Rev. Lett. 1995, 74:4754.
109. Crut A., Lasne D., Allemand J.F., Dahan M., Desbiolles P. Transverse fluctuations of single DNA molecules attached at both extremities to a surface. Phys. Rev. E 2003, 67:051910.
110. Michalet X., Ekong R., Fougerousse F.o., Rousseaux S., Schurra C., Hornigold N., Slegtenhorst M.v., Wolfe J., Povey S., Beckmann J.S., Bensimon A. Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science 1997, 277:1518-1523.
111. Blainey P.C., van Oijen A.M., Banerjee A., Verdine G.L., Xie X.S. A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc. Natl. Acad. Sci. 2006, 103:5752-5757.
112. Dunn A.R., Kad N.M., Nelson S.R., Warshaw D.M., Wallace S.S. Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA. Nucleic Acids Res. 2011, 39:7487-7498.
113. Gorman J., Chowdhury A., Surtees J.A., Shimada J., Reichman D.R., Alani E., Greene E.C. Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol. Cell 2007, 28:359-370.
114. Bonnet I., Biebricher A., Porté P.-L., Loverdo C., Bénichou O., Voituriez R.l., Escudé C., Wende W., Pingoud A., Desbiolles P. Sliding and jumping of single EcoRV restriction enzymes on non-cognate DNA. Nucleic Acids Res. 2008, 36:4118-4127.
115. Handa N., Bianco P.R., Baskin R.J., Kowalczykowski S.C. Direct visualization of RecBCD movement reveals cotranslocation of the RecD motor after χ recognition. Mol. Cell 2005, 17:745-750.
116. Granéli A., Yeykal C.C., Robertson R.B., Greene E.C. Long-distance lateral diffusion of human Rad51 on double-stranded DNA. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1221-1226.
117. Wang Y.M., Austin R.H., Cox E.C. Single molecule measurements of repressor protein 1D diffusion on DNA. Phys. Rev. Lett. 2006, 97:048302.
118. Blainey P.C., Luo G., Kou S.C., Mangel W.F., Verdine G.L., Bagchi B., Xie X.S. Nonspecifically bound proteins spin while diffusing along DNA. Nat. Struct. Mol. Biol. 2009, 16:1224-1229.
119. Kim J.H., Larson R.G. Single-molecule analysis of 1D diffusion and transcription elongation of T7 RNA polymerase along individual stretched DNA molecules. Nucleic Acids Res. 2007, 35:3848-3858.
120. Etson C.M., Hamdan S.M., Richardson C.C., van Oijen A.M. Thioredoxin suppresses microscopic hopping of T7 DNA polymerase on duplex DNA. Proc. Natl. Acad. Sci. 2010, 107:1900-1905.
121. Tafvizi A., Huang F., Leith J.S., Fersht A.R., Mirny L.A., van Oijen A.M. Tumor suppressor p53 slides on DNA with low friction and high stability. Biophys. J. 2008, 95:L01-L03.
122. Tafvizi A., Huang F., Fersht A.R., Mirny L.A., van Oijen A.M. A single-molecule characterization of p53 search on DNA. Proc. Natl. Acad. Sci. 2011, 108:563-568.
123. Murugan R. Directional dependent dynamics of protein molecules on DNA. Phys. Rev. E 2009, 79:041913.
124. Graham J.S., Johnson R.C., Marko J.F. Concentration-dependent exchange accelerates turnover of proteins bound to double-stranded DNA. Nucleic Acids Res. 2011, 39:2249-2259.
125. Ali Azam T., Iwata A., Nishimura A., Ueda S., Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 1999, 181:6361-6370.
126. Li G.-W., Berg O.G., Elf J. Effects of macromolecular crowding and DNA looping on gene regulation kinetics. Nat. Phys. 2009, 5:294-297.
127. Gorman J., Plys A.J., Visnapuu M.-L., Alani E., Greene E.C. Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat. Struct. Mol. Biol. 2010, 17:932-938.
128. Elf J., Li G.-W., Xie X.S. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 2007, 316:1191-1194.
129. Xie X.S., Choi P.J., Li G.-W., Lee N.K., Lia G. Single-molecule approach to molecular biology in living bacterial cells. Annu. Rev. Biophys. 2008, 37:417-444.
130. English B.P., Hauryliuk V., Sanamrad A., Tankov S., Dekker N.H., Elf J. Single-molecule investigations of the stringent response machinery in living bacterial cells. Proc. Natl. Acad. Sci. 2011, 108:E365-E373.
131. Qian H., Sheetz M.P., Elson E.L. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 1991, 60:910-921.
132. Li G.-W., Elf J. Single molecule approaches to transcription factor kinetics in living cells. FEBS Lett. 2009, 583:3979-3983.
133. Le T.T., Harlepp S., Guet C.C., Dittmar K., Emonet T., Pan T., Cluzel P. Real-time RNA profiling within a single bacterium. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9160-9164.
134. Li G.-W., Xie X.S. Central dogma at the single-molecule level in living cells. Nature 2011, 475:308-315.
135. Choi P.J., Cai L., Frieda K., Xie X.S. A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 2008, 322:442-446.
136. Larson D.R., Zenklusen D., Wu B., Chao J.A., Singer R.H. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 2011, 332:475-478.
137. Axelrod D., Koppel D.E., Schlessinger J., Elson E., Webb W.W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 1976, 16:1055-1069.
138. Magde D., Elson E., Webb W.W. Thermodynamic fluctuations in a reacting system-measurement by fluorescence correlation spectroscopy. Phys. Rev. Lett. 1972, 29:705.
139. Schwille P., Haupts U., Maiti S., Webb W.W. Molecular dynamics in living cells observed by fluorescence correlation spectroscopy with one- and two-photon excitation. Biophys. J. 1999, 77:2251-2265.
140. Bacia K., Kim S.A., Schwille P. Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 2006, 3:83-89.
141. Haustein E., Schwille P. Fluorescence correlation spectroscopy: novel variations of an established technique. Annu. Rev. Biophys. Biomol. Struct. 2007, 36:151-169.
142. van Royen M.E., Farla P., Mattern K.A., Geverts B., Trapman J., Houtsmuller A.B. Fluorescence recovery after photobleaching (FRAP) to study nuclear protein dynamics in living cells. Methods Mol. Biol. 2009, 464:363-385.
143. Mueller F., Mazza D., Stasevich T.J., McNally J.G. FRAP and kinetic modeling in the analysis of nuclear protein dynamics: what do we really know?. Curr. Opin. Cell Biol. 2011, 22:403-411.
144. Sprague B.L., Pego R.L., Stavreva D.A., McNally J.G. Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys. J. 2004, 86:3473-3495.
145. Beaudouin J., Mora-Bermúdez F., Klee T., Daigle N., Ellenberg J. Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophys. J. 2006, 90:1878-1894.
146. Michelman-Ribeiro A., Mazza D., Rosales T., Stasevich T.J., Boukari H., Rishi V., Vinson C., Knutson J.R., McNally J.G. Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. Biophys. J. 2009, 97:337-346.
147. Sprague B.L., McNally J.G. FRAP analysis of binding: proper and fitting. Trends Cell Biol. 2005, 15:84-91.
148. Kang M., Day C.A., DiBenedetto E., Kenworthy A.K. A quantitative approach to analyze binding diffusion kinetics by confocal FRAP. Biophys. J. 2010, 99:2737-2747.
149. Stasevich T.J., Mueller F., Michelman-Ribeiro A., Rosales T., Knutson J.R., McNally J.G. Cross-validating FRAP and FCS to quantify the impact of photobleaching on in vivo binding estimates. Biophys. J. 2010, 99:3093-3101.
150. Kimura H., Sugaya K., Cook P.R. The transcription cycle of RNA polymerase II in living cells. J. Cell Biol. 2002, 159:777-782.
151. Yao J., Zobeck K.L., Lis J.T., Webb W.W. Imaging transcription dynamics at endogenous genes in living Drosophila tissues. Methods 2008, 45:233-241.
152. Becker M., Baumann C., John S., Walker D.A., Vigneron M., McNally J.G., Hager G.L. Dynamic behavior of transcription factors on a natural promoter in living cells. EMBO Rep. 2002, 3:1188-1194.
153. Yao J., Ardehali M.B., Fecko C.J., Webb W.W., Lis J.T. Intranuclear distribution and local dynamics of RNA polymerase II during transcription activation. Mol. Cell 2007, 28:978-990.
154. Janicki S.M., Tsukamoto T., Salghetti S.E., Tansey W.P., Sachidanandam R., Prasanth K.V., Ried T., Shav-Tal Y., Bertrand E., Singer R.H., Spector D.L. From silencing to gene expression: real-time analysis in single cells. Cell 2004, 116:683-698.
155. Darzacq X., Shav-Tal Y., de Turris V., Brody Y., Shenoy S.M., Phair R.D., Singer R.H. In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 2007, 14:796-806.
156. Karpova T.S., Kim M.J., Spriet C., Nalley K., Stasevich T.J., Kherrouche Z., Heliot L., McNally J.G. Concurrent fast and slow cycling of a transcriptional activator at an endogenous promoter. Science 2008, 319:466-469.
157. Yao J., Munson K.M., Webb W.W., Lis J.T. Dynamics of heat shock factor association with native gene loci in living cells. Nature 2006, 442:1050-1053.
158. Vukojević V., Papadopoulos D.K., Terenius L., Gehring W.J., Rigler R. Quantitative study of synthetic Hox transcription factor-DNA interactions in live cells. Proc. Natl. Acad. Sci. 2010, 107:4093-4098.
159. Papadopoulos D.K., Vukojević V., Adachi Y., Terenius L., Rigler R., Gehring W.J. Function and specificity of synthetic Hox transcription factors in vivo. Proc. Natl. Acad. Sci. 2010, 107:4087-4092.
160. Vukojević V., Heidkamp M., Ming Y., Johansson B., Terenius L., Rigler R. Quantitative single-molecule imaging by confocal laser scanning microscopy. Proc. Natl. Acad. Sci. 2008, 105:18176-18181.
161. Giglia-Mari G., Theil A.F., Mari P.-O., Mourgues S., Nonnekens J., Andrieux L.O., de Wit J., Miquel C., Wijgers N., Maas A., Fousteri M., Hoeijmakers J.H.J., Vermeulen W. Differentiation driven changes in the dynamic organization of basal transcription initiation. PLoS Biol. 2009, 7:e1000220.
162. Hoogstraten D., Nigg A.L., Heath H., Mullenders L.H.F., van Driel R., Hoeijmakers J.H.J., Vermeulen W., Houtsmuller A.B. Rapid switching of THIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol. Cell 2002, 10:1163-1174.
163. Zimmerman S.B., Minton A.P. Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu. Rev. Biophys. Biomol. Struct. 1993, 22:27-65.
164. Zhou H.-X., Rivas G., Minton A.P. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu. Rev. Biophys. 2008, 37:375-397.
165. Ando T., Skolnick J. Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion. Proc. Natl. Acad. Sci. 2010, 107:18457-18462.
166. Dix J.A., Verkman A.S. Crowding effects on diffusion in solutions and cells. Annu. Rev. Biophys. 2008, 37:247-263.
167. Bancaud A., Huet S., Daigle N., Mozziconacci J., Beaudouin J., Ellenberg J. Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J. 2009, 28:3785-3798.
168. Capoulade J., Wachsmuth M., Hufnagel L., Knop M. Quantitative fluorescence imaging of protein diffusion and interaction in living cells. Nat. Biotechnol. 2011, 29:835-839.
169. Grünwald D., Martin R.M., Buschmann V., Bazett-Jones D.P., Leonhardt H., Kubitscheck U., Cardoso M.C. Probing intranuclear environments at the single-molecule level. Biophys. J. 2008, 94:2847-2858.
170. Siebrasse J.P., Veith R., Dobay A., Leonhardt H., Daneholt B., Kubitscheck U. Discontinuous movement of mRNP particles in nucleoplasmic regions devoid of chromatin. Proc. Natl. Acad. Sci. 2008, 105:20291-20296.
171. Goulian M., Simon S.M. Tracking single proteins within cells. Biophys. J. 2000, 79:2188-2198.
172. Bénichou O., Chevalier C., Klafter J., Meyer B., Voituriez R. Geometry-controlled kinetics. Nat. Chem. 2010, 2:472-477.
173. Isaacson S.A., McQueen D.M., Peskin C.S. The influence of volume exclusion by chromatin on the time required to find specific DNA binding sites by diffusion. Proc. Natl. Acad. Sci. 2011, 108:3815-3820.
174. Zink D., Cremer T., Saffrich R., Fischer R., Trendelenburg M.F., Ansorge W., Stelzer E.H.K. Structure and dynamics of human interphase chromosome territories in vivo. Hum. Genet. 1998, 102:241-251.
175. Cremer T., Cremer M., Dietzel S., Müller S., Solovei I., Fakan S. Chromosome territories - a functional nuclear landscape. Curr. Opin. Cell Biol. 2006, 18:307-316.
176. Barrera L.O., Ren B. The transcriptional regulatory code of eukaryotic cells - insights from genome-wide analysis of chromatin organization and transcription factor binding. Curr. Opin. Cell Biol. 2006, 18:291-298.
177. Dorier J., Stasiak A. The role of transcription factories-mediated interchromosomal contacts in the organization of nuclear architecture. Nucleic Acids Res. 2010, 38:7410-7421.
178. Jost K.L., Haase S., Smeets D., Schrode N., Schmiedel J.M., Bertulat B., Herzel H., Cremer M., Cardoso M.C. 3D-Image analysis platform monitoring relocation of pluripotency genes during reprogramming. Nucleic Acids Res. 2011, 39:e113.
179. Hell S.W. Far-field optical nanoscopy. Science 2007, 316:1153-1158.
180. Schermelleh L., Carlton P.M., Haase S., Shao L., Winoto L., Kner P., Burke B., Cardoso M.C., Agard D.A., Gustafsson M.G.L., Leonhardt H., Sedat J.W. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 2008, 320:1332-1336.
181. Bohn M., Diesinger P., Kaufmann R., Weiland Y., Müller P., Gunkel M., von Ketteler A., Lemmer P., Hausmann M., Heermann D.W., Cremer C. Localization microscopy reveals expression-dependent parameters of chromatin nanostructure. Biophys. J. 2010, 99:1358-1367.
182. von Hippel P.H. From "simple" DNA-protein interactions to the macromolecular machines of gene expression. Annu. Rev. Biophys. Biomol. Struct. 2007, 36:79-105.
183. Bintu L., Buchler N.E., Garcia H.G., Gerland U., Hwa T., Kondev J., Phillips R. Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 2005, 15:116-124.
184. Arnosti D.N., Barolo S., Levine M., Small S. The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 1996, 122:205-214.
185. Lin Y.-S., Carey M., Ptashne M., Green M.R. How different eukaryotic transcriptional activators can cooperate promiscuously. Nature 1990, 345:359-361.
186. Mirny L.A. Nucleosome-mediated cooperativity between transcription factors. Proc. Natl. Acad. Sci. 2010, 107:22534-22539.
187. Yao J., Fetter R.D., Hu P., Betzig E., Tjian R. Subnuclear segregation of genes and core promoter factors in myogenesis. Genes Dev. 2011, 25:569-580.
188. Heard E., Bickmore W. The ins and outs of gene regulation and chromosome territory organisation. Curr. Opin. Cell Biol. 2007, 19:311-316.
189. Schneider R., Grosschedl R. Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev. 2007, 21:3027-3043.
190. Shu W., Chen H., Bo X., Wang S. Genome-wide analysis of the relationships between DNaseI HS, histone modifications and gene expression reveals distinct modes of chromatin domains. Nucleic Acids Res. 2011, 39:7428-7443.
191. Barak L.S., Webb W.W. Fluorescent low density lipoprotein for observation of dynamics of individual receptor complexes on cultured human fibroblasts. J. Cell Biol. 1981, 90:595-604.
192. Edidin M., Kuo S.C., Sheetz M.P. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science 1991, 254:1379-1382.
193. Dahan M., Lévi S., Luccardini C., Rostaing P., Riveau B., Triller A. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 2003, 302:442-445.
194. Wieser S., Schütz G.J. Tracking single molecules in the live cell plasma membrane - do's and don'ts. Methods 2008, 46:131-140.
195. Serge A., Bertaux N., Rigneault H., Marguet D. Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes. Nat. Methods 2008, 5:687-694.
196. Diez-Ahedo R., Normanno D., Esteban O., Bakker G.-J., Figdor C.G., Cambi A., García-Parajo M.F. Dynamic re-organization of individual adhesion nanoclusters in living cells by ligand-patterned surfaces. Small 2009, 5:1258-1263.
197. Shav-Tal Y., Darzacq X., Shenoy S.M., Fusco D., Janicki S.M., Spector D.L., Singer R.H. Dynamics of single mRNPs in nuclei of living cells. Science 2004, 304:1797-1800.
198. Grünwald D., Singer R.H. In vivo imaging of labelled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 2011, 467:604-607.
199. Xie X.S., Yu J., Yang W.Y. Living cells as test tubes. Science 2006, 312:228-230.
200. Semrau S., Pezzarossa A., Schmidt T. Microsecond single-molecule tracking (μsSMT). Biophys. J. 2011, 100:L19-L21.
201. Paige J.S., Wu K.Y., Jaffrey S.R. RNA mimics of green fluorescent protein. Science 2011, 333:642-646.
202. Lombardo A., Cesana D., Genovese P., Di Stefano B., Provasi E., Colombo D.F., Neri M., Magnani Z., Cantore A., Lo Riso P., Damo M., Pello O.M., Holmes M.C., Gregory P.D., Gritti A., Broccoli V., Bonini C., Naldini L. Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat. Methods 2011, 8:861-869.
203. Bruckbauer A., James P., Zhou D., Yoon J.W., Excell D., Korchev Y., Jones R., Klenerman D. Nanopipette delivery of individual molecules to cellular compartments for single-molecule fluorescence tracking. Biophys. J. 2007, 93:3120-3131.
204. Manley S., Gillette J.M., Patterson G.H., Shroff H., Hess H.F., Betzig E., Lippincott-Schwartz J. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 2008, 5:155-157.
205. Griffin B.A., Adams S.R., Tsien R.Y. Specific covalent labeling of recombinant protein molecules inside live cells. Science 1998, 281:269-272.
206. Keppler A., Gendreizig S., Gronemeyer T., Pick H., Vogel H., Johnsson K. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 2003, 21:86-89.
207. Wombacher R., Heidbreder M., van de Linde S., Sheetz M.P., Heilemann M., Cornish V.W., Sauer M. Live-cell super-resolution imaging with trimethoprim conjugates. Nat. Methods 2010, 7:717-719.
208. Yang S.K., Shi X., Park S., Doganay S., Ha T., Zimmerman S.C. Monovalent, clickable, uncharged, water-soluble perylenediimide-cored dendrimers for target-specific fluorescent biolabeling. J. Am. Chem. Soc. 2011, 133:9964-9967.
209. Campos C., Kamiya M., Banala S., Johnsson K., González-Gaitán M. Labelling cell structures and tracking cell lineage in zebrafish using SNAP-tag. Dev. Dyn. 2011, 240:820-827.
210. Bojkowska K., Santoni de Sio F., Barde I., Offner S., Verp S., Heinis C., Johnsson K., Trono D. Measuring in vivo protein half-life. Chem. Biol. 2011, 18:805-815.
211. Koyama-Honda I., Ritchie K., Fujiwara T., Iino R., Murakoshi H., Kasai R.S., Kusumi A. Fluorescence imaging for monitoring the colocalization of two single molecules in living cells. Biophys. J. 2005, 88:2126-2136.
212. Douglass A.D., Vale R.D. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 2005, 121:937-950.
213. Schoen I., Krammer H., Braun D. Hybridization kinetics is different inside cells. Proc. Natl. Acad. Sci. 2009, 106:21649-21654.