Large-scale chromatin organization: The good, the surprising, and the still perplexing

Current Opinion in Cell Biology

Volumn 26, Issue 1, 2014, Pages 69-78

  Belmont, Andrew S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

CHROMATIN STRUCTURE; CHROMOSOME; CHROMOSOME STRUCTURE; CYTOLOGY; DROSOPHILA; ENHANCER REGION; GENE CONTROL; GENE INTERACTION; GENOME ANALYSIS; MICROSCOPY; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW;

ANIMALS; CHROMATIN; CYTOPLASM; DNA; GENOMICS; HUMANS; MOLECULAR CONFORMATION;

EID: 84887942741     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.10.002     Document Type: Review

References (62)

1. Bian Q., Belmont A.S. Revisiting higher-order and large-scale chromatin organization. Curr Opin Cell Biol 2012, 24:359-366.
2. Ghirlando R., Felsenfeld G. Chromatin structure outside and inside the nucleus. Biopolymers 2013, 99:225-232.
3. Grigoryev S.A., Woodcock C.L. Chromatin organization-the 30nm fiber. Exp Cell Res 2012, 318:1448-1455.
4. Maeshima K., Hihara S., Eltsov M. Chromatin structure: does the 30-nm fibre exist in vivo?. Curr Opin Cell Biol 2010, 22:291-297.
5. Nishino Y., Eltsov M., Joti Y., Ito K., Takata H., Takahashi Y., Hihara S., Frangakis A.S., Imamoto N., Ishikawa T., et al. Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure. EMBO J 2012, 31:1644-1653.
6. Belmont A.S., Braunfeld M.B., Sedat J.W., Agard D.A. Large-scale chromatin structural domains within mitotic and interphase chromosomes in vivo and in vitro. Chromosoma 1989, 98:129-143.
7. Bohrmann B., Kellenberger E. Immunostaining of DNA in electron microscopy: an amplification and staining procedure for thin sections as alternative to gold labeling. J Histochem Cytochem 1994, 42:635-643.
8. Testillano P.S., Sanchez-Pina M.A., Olmedilla A., Ollacarizqueta M.A., Tandler C.J., Risueno M.C. A specific ultrastructural method to reveal DNA: the NAMA-Ur. J Histochem Cytochem 1991, 39:1427-1438.
9. Olins A.L., Moyer B.A., Kim S.H., Allison D.P. Synthesis of a more stable osmium ammine electron-dense DNA stain. J Histochem Cytochem 1989, 37:395-398.
10. Bazett-Jones D.P., Hendzel M.J. Electron spectroscopic imaging of chromatin. Methods 1999, 17:188-200.
11. Kireev I., Lakonishok M., Liu W., Joshi V.N., Powell R., Belmont A.S. In vivo immunogold labeling confirms large-scale chromatin folding motifs. Nat Methods 2008, 5:311-313.
12. Skaer R.J., Whytock S. The fixation of nuclei and chromosomes. J Cell Sci 1976, 20:221-231.
13. Fakan S., Bernhard W. Localization of rapidly and slowly labeled nuclear RNA as visualized by high resolution autoradiography. Exp Cell Res 1971, 67:129-141.
14. Hu Y., Kireev I., Plutz M.J., Ashourian N., Belmont A.S. Large-scale chromatin structure of inducible genes-transcription on a linear template. J Cell Biol 2009, 185:87-100.
15. Markaki Y., Gunkel M., Schermelleh L., Beichmanis S., Neumann J., Heidemann M., Leonhardt H., Eick D., Cremer C., Cremer T. Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Cold Spring Harb Symp Quant Biol 2010, 75:475-492.
16. Belmont A.S., Bruce K. Visualization of G1 chromosomes: a folded, twisted, supercoiled chromonema model of interphase chromatid structure. J Cell Biol 1994, 127:287-302.
17. Kireeva N., Lakonishok M., Kireev I., Hirano T., Belmont A.S. Visualization of early chromosome condensation: a hierarchical folding, axial glue model of chromosome structure. J Cell Biol 2004, 166:775-785.
18. Rego A., Sinclair P.B., Tao W., Kireev I., Belmont A.S. The facultative heterochromatin of the inactive X chromosome has a distinctive condensed ultrastructure. J Cell Sci 2008, 121:1119-1127.
19. Sparvoli E., Levi M., Rossi E. Replicon clusters may form structurally stable complexes of chromatin and chromosomes. J Cell Sci 1994, 107(Pt 11):3097-3103.
20. Jackson D.A., Pombo A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 1998, 140:1285-1295.
21. Ma H., Samarabandu J., Devdhar R.S., Acharya R., Cheng P-c, Meng C., Berezney R. Spatial and temporal dynamics of DNA replication sites in mammalian cells. J Cell Biol 1998, 143:1415-1425.
22. Belmont A.S., Hu Y., Sinclair P.B., Wu W., Bian Q., Kireev I. Insights into interphase large-scale chromatin structure from analysis of engineered chromosome regions. Cold Spring Harb Symp Quant Biol 2010, 75:453-460.
23. Muller W.G., Walker D., Hager G.L., McNally J.G. Large-scale chromatin decondensation and recondensation regulated by transcription from a natural promoter. J Cell Biol 2001, 154:33-48.
24. Tumbar T., Sudlow G., Belmont A.S. Large-scale chromatin unfolding and remodeling induced by VP16 acidic activation domain. J Cell Biol 1999, 145:1341-1354.
25. Gierman H.J., Indemans M.H., Koster J., Goetze S., Seppen J., Geerts D., van Driel R., Versteeg R. Domain-wide regulation of gene expression in the human genome. Genome Res 2007, 17:1286-1295.
26. Christova R., Jones T., Wu P.J., Bolzer A., Costa-Pereira A.P., Watling D., Kerr I.M., Sheer D. P-STAT1 mediates higher-order chromatin remodelling of the human MHC in response to IFNgamma. J Cell Sci 2007, 120:3262-3270.
27. Chambeyron S., Bickmore W.A. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 2004, 18:1119-1130.
28. Markaki Y., Smeets D., Fiedler S., Schmid V.J., Schermelleh L., Cremer T., Cremer M. The potential of 3D-FISH and super-resolution structured illumination microscopy for studies of 3D nuclear architecture: 3D structured illumination microscopy of defined chromosomal structures visualized by 3D (immuno)-FISH opens new perspectives for studies of nuclear architecture. BioEssays 2012, 34:412-426.
29. Solovei I., Cavallo A., Schermelleh L., Jaunin F., Scasselati C., Cmarko D., Cremer C., Fakan S., Cremer T. Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 2002, 276:10-23.
30. Robinett C.C., Straight A., Li G., Willhelm C., Sudlow G., Murray A., Belmont A.S. In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J Cell Biol 1996, 135:1685-1700.
31. Dostie J., Bickmore W.A. Chromosome organization in the nucleus-charting new territory across the Hi-Cs. Curr Opin Genet Dev 2012, 22:125-131.
32. Tanay A., Cavalli G. Chromosomal domains: epigenetic contexts and functional implications of genomic compartmentalization. Curr Opin Genet Dev 2013, 23:197-203.
33. Dekker J., Marti-Renom M.A., Mirny L.A. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat Rev Genet 2013, 14:390-403.
34. de Wit E., de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev 2012, 26:11-24.
35. Tanizawa H., Noma K. Unravelling global genome organization by 3C-seq. Semin Cell Dev Biol 2012, 23:213-221.
36. Bickmore W.A., van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013, 152:1270-1284.
37. Sexton T., Yaffe E., Kenigsberg E., Bantignies F., Leblanc B., Hoichman M., Parrinello H., Tanay A., Cavalli G. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012, 148:458-472.
38. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
39. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., van Berkum N.L., Meisig J., Sedat J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
40. Hou C., Li L., Qin Z.S., Corces V.G. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol Cell 2012, 48:471-484.
41. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
42. Filion G.J., van Bemmel J.G., Braunschweig U., Talhout W., Kind J., Ward L.D., Brugman W., de Castro I.J., Kerkhoven R.M., Bussemaker H.J., et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 2010, 143:212-224.
43. Kharchenko P.V., Alekseyenko A.A., Schwartz Y.B., Minoda A., Riddle N.C., Ernst J., Sabo P.J., Larschan E., Gorchakov A.A., Gu T., et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 2011, 471:480-485.
44. Yaffe E., Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat Genet 2011, 43:1059-1065.
45. Imakaev M., Fudenberg G., McCord R.P., Naumova N., Goloborodko A., Lajoie B.R., Dekker J., Mirny L.A. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat Methods 2012, 9:999-1003.
46. Hakim O., Sung M.H., Voss T.C., Splinter E., John S., Sabo P.J., Thurman R.E., Stamatoyannopoulos J.A., de Laat W., Hager G.L. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res 2011, 21:697-706.
47. Giresi P.G., Kim J., McDaniell R.M., Iyer V.R., Lieb J.D. FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res 2007, 17:877-885.
48. Simon J.M., Giresi P.G., Davis I.J., Lieb J.D. A detailed protocol for formaldehyde-assisted isolation of regulatory elements (FAIRE). Curr Protoc Mol Biol 2013, edited by Frederick M Ausubel... [et al.], Chapter 21: Unit 21.26.
49. Grigoryev S.A., Arya G., Correll S., Woodcock C.L., Schlick T. Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions. Proc Natl Acad Sci U S A 2009, 106:13317-13322.
50. Gavrilov A.A., Gushchanskaya E.S., Strelkova O., Zhironkina O., Kireev I.I., Iarovaia O.V., Razin S.V. Disclosure of a structural milieu for the proximity ligation reveals the elusive nature of an active chromatin hub. Nucleic Acids Res 2013, 41:3563-3575.
51. Krivega I., Dean A. Enhancer and promoter interactions-long distance calls. Curr Opin Genet Dev 2012, 22:79-85.
52. Deng W., Lee J., Wang H., Miller J., Reik A., Gregory P.D., Dean A., Blobel G.A. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 2012, 149:1233-1244.
53. Schoenfelder S., Sexton T., Chakalova L., Cope N.F., Horton A., Andrews S., Kurukuti S., Mitchell J.A., Umlauf D., Dimitrova D.S., et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 2010, 42:53-61.
54. Song S.H., Kim A., Ragoczy T., Bender M.A., Groudine M., Dean A. Multiple functions of Ldb1 required for beta-globin activation during erythroid differentiation. Blood 2010, 116:2356-2364.
55. Sorsa V. Chromosome Maps of Drosophila 1988, CRC Press, Boca Raton, FL.
56. Hochstrasser M. Chromosome structure in four wild-type polytene tissues of Drosophila melanogaster. The 87A and 87C heat shock loci are induced unequally in the midgut in a manner dependent on growth temperature. Chromosoma 1987, 95:197-208.
57. Hochstrasser M., Sedat J.W. Three-dimensional organization of Drosophila melanogaster interphase nuclei. II. Chromosome spatial organization and gene regulation. J Cell Biol 1987, 104:1471-1483.
58. Wallace H.A., Marques-Kranc F., Richardson M., Luna-Crespo F., Sharpe J.A., Hughes J., Wood W.G., Higgs D.R., Smith A.J. Manipulating the mouse genome to engineer precise functional syntenic replacements with human sequence. Cell 2007, 128:197-209.
59. Clowney E.J., LeGros M.A., Mosley C.P., Clowney F.G., Markenskoff-Papadimitriou E.C., Myllys M., Barnea G., Larabell C.A., Lomvardas S. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 2012, 151:724-737.
60. Amano T., Sagai T., Tanabe H., Mizushina Y., Nakazawa H., Shiroishi T. Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev Cell 2009, 16:47-57.
61. Maass P.G., Rump A., Schulz H., Stricker S., Schulze L., Platzer K., Aydin A., Tinschert S., Goldring M.B., Luft F.C., et al. A misplaced lncRNA causes brachydactyly in humans. J Clin Invest 2012, 122:3990-4002.
62. Heintz N. Analysis of mammalian central nervous system gene expression and function using bacterial artificial chromosome-mediated transgenesis. Human Mol Genet 2000, 9:937-943.