A fractal model for nuclear organization: Current evidence and biological implications

Nucleic Acids Research

Volumn 40, Issue 18, 2012, Pages 8783-8792

  Bancaud, Aurélien ^a,b   Lavelle, Christophe ^c   Huet, Sébastien ^d,e   Ellenberg, Jan ^f  

^a LAAS CNRS   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

^e UNIVERSITÉ DE RENNES 1   (France)

^f EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME ANALYSIS; CHROMOSOME MAP; CHROMOSOME STRUCTURE; CONFORMATION; DNA REPLICATION; DNA STRUCTURE; FLUORESCENCE IN SITU HYBRIDIZATION; FRACTAL ANALYSIS; HETEROCHROMATIN; IMAGE ANALYSIS; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NEUTRON SCATTERING; PRIORITY JOURNAL; REVIEW; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING;

CELL NUCLEUS; CHROMATIN; CHROMOSOMES; FRACTALS; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, MOLECULAR; NEUTRONS; RHEOLOGY; SCATTERING, RADIATION;

EID: 84867498711     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks586     Document Type: Review

References (101)

1. Luger,K., Mader,A.W., Richmond,R.K., Sargent,D.F. and Richmond,T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389, 251-260. (Pubitemid 27406632)
2. Harp,J.M., Hanson,B.L., Timm,D.E. and Bunick,G.J. (2000) Asymmetries in the nucleosome core particle at 2.5 A resolution. Acta. Crystallogr. D Biol. Cyrstallogr., 56, 1513-1534. (Pubitemid 32040010)
3. van Holde,K.E. (1989) Chromatin. Springer, New York, NY.
4. van Holde,K. and Zlatanova,J. (2007) Chromatin fiber structure: Where is the problem now Semin. Cell. Dev. Biol., 18, 651-658. (Pubitemid 350026429)
5. Woodcock,C.L. and Ghosh,R.P. (2010) Chromatin higher-order structure and dynamics. Cold Spring Harb. Perspect. Biol., 2, a000596.
6. Cook,P.R. (1999) The organization of replication and transcription. Science, 284, 1790-1795.
7. Gondor,A. and Ohlsson,R. (2009) Chromosome crosstalk in three dimensions. Nature, 461, 212-217.
8. Gerlich,D. and Ellenberg,J. (2003) 4D imaging to assay complex dynamics in live specimens. Nat. Cell. Biol., (Suppl), S14-S19. (Pubitemid 37082168)
9. Cremer,T., Cremer,M., Dietzel,S., Muller,S., Solovei,I. and Fakan,S. (2006) Chromosome territories -A functional nuclear landscape. Curr. Opin. Cell. Biol., 18, 307-316.
10. 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. et al. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human chromosome. Science, 326, 289-293.
11. Bancaud,A., Huet,S., Daigle,N., Beaudouin,J., Mozziconacci,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.
12. Goldberger,A.L. (1996) Non-linear dynamics for clinicians: Chaos theory, fractals, and complexity at the bedside. Lancet, 347, 1312-1314. (Pubitemid 26137801)
13. Havlin,S., Buldyrev,S.V., Goldberger,A.L., Mantegna,R.N., Ossadnik,S.M., Peng,C.K., Simons,M. and Stanley,H.E. (1995) Fractals in biology and medicine. Chaos Solitons Fractals, 6, 171-201.
14. Heymans,O., Fissette,J., Vico,P., Blacher,S., Masset,D. and Brouers,F. (2000) Is fractal geometry useful in medicine and biomedical sciences Med. Hypotheses, 54, 360-366. (Pubitemid 30204319)
15. Buldyrev,S.V., Goldberger,A.L., Havlin,S., Peng,C., Simons,M., Sciortino,F. and Stanley,H.E. (1993) Long-range fractal correlations in DNA. Phys. Rev. Lett., 71, 1776.
16. Cristea,P. and Popescu,G. (2003) 1st SouthEast European Symposium on Interdisciplinary Approachees in Fractal Analysis. Bucharest, Romania, pp. 131-134.
17. Garte,S. (2004) Fractal properties of the human genome. J. Theor. Biol., 230, 251-260. (Pubitemid 39078410)
18. Nicolay,S., Brodie Of Brodie,E.B., Touchon,M., Audit,B., d'Aubenton-Carafa,Y., Thermes,C. and Arneodo,A. (2007) Bifractality of human DNA strand-Asymmetry profiles results from transcription. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 75, 032902.
19. Voss,R.F. (1992) Evolution of long-range fractal correlations and 1/f noise in DNA base sequences. Phys. Rev. Lett., 68, 3805-3808.
20. Borovik,A.S., Grosberg,A. and Frank-Kamenetskii,M.D. (1994) Fractality of DNA texts. J Biomol. Struct. Dyn., 12, 655-669.
21. Arneodo,A., Vaillant,C., Audit,B., Argoul,F., d'Aubenton-Carafa,Y. and Thermes,C. (2011) Multi-scale coding of genomic information: From DNA sequence to genome structure and function. Phys. Reports, 498, 45-188.
22. Grosberg,A.Y., Rabin,Y., Havlin,S. and Neer,A. (1993) Crumpled globule model of the three-dimensional structure of DNA. Europhys. Lett., 23, 373-378.
23. Grosberg,A.Y., Nechaev,S.K. and Shakhnovich,E.I. (1988) The role of topological constraints in the kinetics of Collapse of macromolecule. Le J. Phys., 49, 2095-2100.
24. Witten,T.A. (1998) Polymer solutions: A geometric introduction. Rev. Mod. Phys., 70, 1531-1544.
25. McNally,J.G. and Mazza,D. (2010) Fractal geometry in the nucleus. EMBO J., 29, 2-3.
26. Mirny,L.A. (2011) The fractal globule as a model of chromatin architecture in the cell. Chromosome Res., 19, 37-51.
27. Sanyal,A., Bau,D., Marti-Renom,M.A. and Dekker,J. (2011) Chromatin globules: A common motif of higher order chromosome structure Curr. Opin. Cell. Biol., 23, 325-331.
28. Mandelbrot,B.B. (1982) In: Freeman,W.F. (ed.), The Fractal Geometry of Nature, San Francisco.
29. Daban,J.R. (2000) Physical constraints in the condensation of eukaryotic chromosomes. Local concentration of DNA versus linear packing ratio in higher order chromatin structures. Biochemistry, 39, 3861-3866.
30. Bohrmann,B., Haider,M. and Kellenberger,E. (1993) Concentration evaluation of chromatin in unstained resin-embedded sections by means of low-dose ratio-contrast imaging in STEM. Ultramicroscopy, 49, 235-251.
31. Cassi,D. and Regina,S. (1993) Spectral dimension of branched structures: Universality in geometrical disorder. Phys. Rev. Lett., 70, 1647-1649.
32. Beaudouin,J., Mora-Bermudez,F., Klee,T., Daigle,N. and Ellenberg,J. (2006) Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophys. J., 90, 1878-1894.
33. Saxton,M.J. (1994) Anomalous diffusion due to obstacles: A Monte Carlo study. Biophys. J., 66, 394-401. (Pubitemid 24058459)
34. Ben-Avraham,S. and Havlin,S. (2000) Diffusion and Reactions in Fractals and Disordered Systems. Cambridge University Press, Cambridge.
35. Einstein,A.J., Wu,H.-S., Sanchez,M. and Gil,J. (1998) Fractal organization of chromatin appearance for diagnosis in breast cytology. J. Pathol., 185, 366-381. (Pubitemid 28355969)
36. Lebedev,D.V., Filatov,M.V., Kuklin,A.I., Islamov,A.K., Ketzinger,E., Pantina,R., Toperverg,B.P. and Isaev-Ivanov,V.V. (2005) Fractal nature of chromatin organization in interphase chicken erythrocyte nuclei: DNA structure exhibits biphasic fractal properties. FEBS Lett., 579, 1465-1468. (Pubitemid 40289197)
37. Yokota,H., van den Engh,G., Hearst,J.E., Sachs,R.K. and Trask,B.J. (1995) evidence for the organization of chromatin in megabase pair-sized loops arranged along a random walk path in the humand G0/G1 interphase nucleus. J. Cell. Biol., 130, 1239-1249.
38. Sachs,R.K., van den Engh,G., Trask,B., Yokota,H. and Hearst,J.E. (1995) A random-walk/giant-loop model for interphase chromosomes. Proc. Natl Acad. Sci. USA, 92, 2710-2714.
39. Tó th,K.F., Knoch,T.A., Wachsmuth,M., Frank-Stohr,M., Stohr,M., Bacher,C.P., Muller,G. and Rippe,K. (2004) Trichostatin A-induced histone acetylation causes decondensation of interphase chromatin. J. Cell. Sci., 15, 4277-4287. (Pubitemid 39328314)
40. Huisman,A., Ploeger,L.S., Dullens,H.F., Poulin,N., Grizzle,W.E. and van Diest,P.J. (2005) Development of 3D chromatin texture analysis using confocal laser scanning microscopy. Cell Oncol., 27, 335-345. (Pubitemid 41831639)
41. Ferreira,R.C., de Matos,P.S., Adam,R.L., Leite,N.J. and Metze,K. (2006) Application of the Minkowski-Bouligand fractal dimension for the differential diagnosis of thyroid follicular neoplasias. Cell Oncol., 28, 331-333. (Pubitemid 44950104)
42. Mello,M.R., Metze,K., Adam,R.L., Pereira,F.G., Magalhaes,M.G., Machado,C.G. and Lorand-Metze,I. (2008) Phenotypic subtypes of acute lymphoblastic leukemia associated with different nuclear chromatin texture. Anal. Quant. Cytol. Histol., 30, 92-98. (Pubitemid 351501869)
43. Metze,K., Ferreira,R.C., Adam,R.L., Leite,N.J., Ward,L.S. and de Matos,P.S. (2008) Chromatin texture is size dependent in follicular adenomas but not in hyperplastic nodules of the thyroid. World J. Surg., 32, 2744-2746.
44. Castelli,C. and Rosa,G.A. (2001) Ultrastructural complexity of nuclear components during early apoptotic phases in breast cancer cells. Anal. Cell. Pathol., 23, 1-9. (Pubitemid 34014655)
45. Pentland,A.P. (1984) Fractal-based description of natural scenes. IEEE Trans. Pattern Anal. Mach. Intell., 6, 661-674.
46. Lebedev,D.V., Filatov,M.V., Kuklin,A.I., Islamov,A.K., Stellbrink,J., Pantina,R., Denisov,Y.Y., Toperverg,B.P. and Isaev-Ivanov,V.V. (2008) Structural hierarchy of chromatin in chicken erythrocyte nuclei based on small-Angle neutron scattering: Fractal nature of the large-scale chromatin organization. Crystallogr. Reports, 53, 110-115. (Pubitemid 351185526)
47. Dekker,J. (2006) The three 'C's of chromsome conformation capture: Controls, controls, controls. Nat. Methods, 3, 17-21. (Pubitemid 43135343)
48. Weiss,M.,-elsner,M., Kartberg,F. and Nilsson,T. (2004) Anomalous subdiffusion is a measure for cytoplasmic crowding in living cells. Biophys. J., 87, 3518-3524. (Pubitemid 40468604)
49. Saxton,M.J. (1993) Lateral diffusion in an archipelago. Dependence on tracer size. Biophys. J., 64, 1053-1062. (Pubitemid 23143270)
50. Guigas,G. and Weiss,M. (2008) Sampling the cell with anomalous diffusion -The discovery of slowness. Biophys. J., 94, 90-94.
51. Seksek,O., Biwersi,J. and Verkman,A.S. (1997) Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J. Cell. Biol., 138, 131-142. (Pubitemid 27337458)
52. Pack,C., Saito,K., Tamura,M. and Kinjo,M. (2006) Microenvironment and effect of energy depletion in the nucleus analyzed by mobility of multiple oligomeric EGFPs. Biophys. J., 91, 3921-3936. (Pubitemid 44788334)
53. Grunwald,D., Martin,R.M., Buschmann,V., Bazett-Jones,D.P., Leonhardt,H., Kubitscheck,U. and Cardoso,M.C. (2008) Probing intranuclear environments at the single-molecule level. Biophys. J., 94, 2847-2858.
54. Wachsmuth,M., Waldeck,W. and Langowski,J. (2000) Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy. J. Mol. Biol., 298, 677-689.
55. Crawford,J. and Matsui,N. (1996) Heterogeneity of the pore and solid volume of soil: Distinguishing a fractal space from its non-fractal complement. Geoderma, 73, 183-195.
56. Dathe,A. and Thullner,M. (2005) The relationship between fractal properties of solid matrix and pore space in porous media. Geoderma, 129, 279-290. (Pubitemid 41550349)
57. Mc Guffee,S.R. and Elcock,A.H. (2010) Diffusion, crowding & protein stability in a dynamic molecular model of the bacterial cytoplasm. PLoS Comput. Biol., 6,-e1000694.
58. Avnir,D., Biham,O., Lidar,D. and Malcai,O. (1998) Is the geometry of nature fractal Science, 279, 39-40.
59. Schaefer,D.W. and Keefer,K.D. (1986) Structure of random porous materials: Silica aerogel. Phys. Rev. Lett., 56, 2199.
60. Schaeffer,D.W. and Keefer,K.D. (1984) Fractal geometry of silica condensation polymers. Phys. Rev. Lett., 53, 1383-1386.
61. de Gennes,P.-G. (1979) Scaling Concepts in Polymer Physics. Cornell university press, Ithaca.
62. Condamin,S., Tejedor,V., Voituriez,R., Be'nichou,O. and Klafter,J. (2008) Probing microscopic origins of confined subdiffusion by first-passage observables. Proc. Natl Acad. Sci. USA, 105, 5675-5680. (Pubitemid 351758430)
63. Bénichou,O., Chevalie,C., Klafter,J., Meyer,B. and Voituriez,R. (2010) Geometry-controlled kinetics. Nat. Chem., 2, 472-477.
64. Condamin,S., Bénichou,O., Tejedor,V., Voituriez,R. and Klafter,J. (2007) First-passage times in complex scale-invariant media. Nature, 450, 77-80. (Pubitemid 350070561)
65. Rea,S.,-eisenhaber,F., O'Carroll,D., Strahl,B.D., Sun,Z.W., Schmid,M., Opravil,S., Mechtler,K., Ponting,C.P., Allis,C.D. et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature, 406, 593-599. (Pubitemid 30641039)
66. Trojer,P. and Reinberg,D. (2007) Facultative heterochromatin: Is there a distinctive molecular signature Mol. Cell, 28, 1-13. (Pubitemid 47531977)
67. Spinelli,G. (2003) Heterochromatin and complexity: A theoretical approach. Nonlinear Dynamics Psychol. Life Sci., 7, 329-361. (Pubitemid 39056339)
68. Meyer,B., Bénichou,O., Kafri,Y. and Voituriez,R. (2012) Geometry-induced bursting dynamics in gene expression. Biophys. J., 102, 2186-2191.
69. Munkel,C.,-eils,R., Dietzel,S., Zink,D., Mehring,C., Wedeman,G., Cremer,T. and Langowski,J. (1999) Compartmentalization of interphase chromosomes observed in simulation and experiment. J. Mol. Biol., 285, 1053-1065. (Pubitemid 29054316)
70. Mateos-Langerak,J., Bohn,M., de Leeuw,W., Giromus,O., Manders,E.M., Verschure,P.J., Indemans,M.H., Gierman,H.J., Heermann,D.W., van Driel,R. et al. (2009) Spatially confined folding of chromatin in the interphase nucleus. Proc. Natl Acad. Sci. USA, 106, 3812-3817.
71. Solovei,I., Cavallo,A., Schermelleh,L., Jaunin,F., Scasselati,C., Cmarko,D., Cremer,C., Fakan,S. and Cremer,T. (2002) Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp. Cell Res., 276, 10-23. (Pubitemid 34948347)
72. Emanuel,M., Rajda,N.H., Henriksson,A. and Schiessel,H. (2009) The physics behing the larger scale organization of DNA in eukaryotes. Phys. Biol., 6, 025008.
73. Bohn,M. and Heermann,D.W. (2009) Conformational properties of compact polymers. J. Chem. Phys., 130, 174901.
74. Bohn,M. and Heermann,D.W. (2010) Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS One, 5,-e12218.
75. Rosa,A. and Everaers,R. (2008) Structure and dynamics of interphase chromosomes. PLoS Comput, Biol., 4,-e1000153.
76. Metze,K., Adam,R.L., Vido,J.R. and Lorand-Metze,I.G. (2009) The influence of staining characteristics on nuclear texture features in cytology. Anal. Quant. Cytol. Histol., 31, 241-246.
77. Latt,S.A. and Wohlleb,J.C. (1975) Optical studies of the interaction of 33258 Hoechst with DNA, chromatin, and metaphase chromosomes. Chromosoma, 52, 297-316.
78. Martin,R.M., Leonhardt,H. and Cardoso,M.C. (2005) DNA labeling in living cells. Cytometry A, 67, 45-52. (Pubitemid 41318292)
79. Zink,D., Sadoni,N. and Stelzer,E. (2003) Visualizing chromatin and chromosomes in living cells. Methods, 29, 42-50. (Pubitemid 36259911)
80. Monier,K., Armas,J.C.,-etteldorf,S., Ghazal,P. and Sullivan,K.F. (2000) Annexation of the interchromosomal space during viral infection. Nat. Cell. Biol., 2, 661-665.
81. Bazett-Jones,D.P., Li,R., Fussner,E., Nisman,R. and Dehghani,H. (2008) Elucidating chromatin and nuclear domain architecture with electron spectroscopic imaging. Chromosome Res., 16, 397-412. (Pubitemid 351644868)
82. Dellaire,G., Kepkay,R. and Bazett-Jones,D.P. (2009) High resolution imaging of changes in the structure and spatial organization of chromatin, gamma-H2A.X and the MRN complex within etoposide-induced DNA repair foci. Cell Cycle, 8, 3750-3769.
83. Molenaar,C., Wiesmeijer,K., Verwoerd,N.P., Khazen,S.,-eils,R., Tanke,H.J. and Dirks,R.W. (2003) Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J., 22, 6631-6641. (Pubitemid 38009609)
84. Richter,K., Nessling,M. and Lichter,P. (2008) Macromolecular crowding and its potential impact on nuclear function. Biochim. Biophys. Acta., 1783, 2100-2107.
85. Glauert,A.M. and Lewis,P.R. (1998) Biological Specimen Preparation for Transmission Electron Microscopy. Princeton University Press, Princeton.
86. Dubochet,J. (2007) The physics of rapid cooling and its implications for cryoimmobilization of cells. Methods Cell. Biol., 79, 7-21.
87. Dubochet,J., Zuber,B.,-eltsov,M., Bouchet-Marquis,C., Al-Amoudi,A. and Livolant,F. (2007) How to ''read'' a vitreous section. Methods Cell. Biol., 79, 385-406.
88. Betzig,E., Patterson,G.H., Sougrat,R., Lindwasser,O.W., Olenych,S., Bonifacino,J.S., Davidson,M.W., Lippincott-Schwartz,J. and Hess,H.F. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science, 313, 1642-1645. (Pubitemid 44414039)
89. Hell,S.W. (2003) Toward fluorescence nanoscopy. Nat. Biotech., 21, 1347-1355. (Pubitemid 37356621)
90. Rust,M.J., Bates,M. and Zhuang,X. (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods, 3, 793-795. (Pubitemid 44445825)
91. Folling,J., Bossi,M., Bock,H., Medda,R., Wurm,C.A., Hein,B., Jakobs,S.,-eggeling,C. and Hell,S.W. (2008) Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat. Methods, 5, 943-945.
92. Bohn,M., Diesinger,P., Kaufmann,R., Weiland,Y., Muller,P., Gunkel,M., von Ketteler,A., Lemmer,P., Hausmann,M., Heermann,D.W. et al. (2010) Localization Microscopy Reveals Expression-Dependent Parameters of Chromatin Nanostructure. Biophys. J., 99, 1358-1367.
93. Wombacher,R., Heidberder,M., van de Linde,S., Sheetz,M.P., Heilemann,M., Cornish,V.W. and Sauer,M. (2010) Live-cell super-resolution imaging with trimethoprim conjugates. Nat. Methods, 7, 717-719.
94. Hajjoul,H., Kocanova,S., Lassadi,I., Bystricky,K. and Bancaud,A. (2009) Lab-on-chip for fast 3D particle tracking in living cells. Lab. Chip, 9, 3054-3058.
95. Levi,V., Ruan,Q. and Gratton,E. (2005) 3-D particle tracking in a two-photon microscope: Application to the study of molecular dynamics in cells. Biophys. J., 88, 2919-2928. (Pubitemid 40976156)
96. 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. (Pubitemid 46877481)
97. Harke,B., Ullal,C.K., Keller,J. and Hell,S.W. (2008) Three-dimensional nanoscopy of colloidal crystals. Nano. Lett., 8, 1309-1313.
98. Dahan,M., Lé vi,S., Luccardini,C., Rostaing,P., Riveau,B. and Triller,A. (2003) Diffusion dynamics of glycine receptors revealed by single-particle quantum dot tracking. Science, 302, 442-445. (Pubitemid 37296269)
99. Bruckbauer,A., James,P., Zhou,H., Yoon,J.W.,-excell,D., Korchev,Y., Jones,R. and Klenerman,D. (2007) Nanopipette delivery of individual molecules to cellular compartments for single molecule fluorescence tracking. Biophys. J., 93, 3120-3131. (Pubitemid 350097103)
100. Botta,M., Haider,S., Leung,I.X., Lio,P. and Mozziconacci,J. (2010) Intra-And inter-chromosomal interactions correlated with CTCF binding genome wide. Mol. Syst. Biol., 6, 426.
101. Benichou,O., Chevalier,C., Meyer,B. and Voituriez,R. (2011) Facilitated diffusion of proteins on chromatin. Phys. Rev. Lett., 106, 038102.