Chromosomes without a 30-nm chromatin fiber

Nucleus (United States)

Volumn 3, Issue 5, 2012, Pages 404-410

  Joti, Yasumasa ^a   Hikima, Takaaki ^b   Nishino, Yoshinori ^b,c   Kamada, Fukumi ^d   Hihara, Saera ^d,e   Takata, Hideaki ^d,f   Ishikawa, Tetsuya ^b   Maeshima, Kazuhiro ^b,d,e  

^a JAPAN SYNCHROTRON RADIATION RESEARCH INSTITUTE   (Japan)

^b Sayo cho ^*  (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^f OSAKA UNIVERSITY   (Japan)

Author keywords

30 nm chromatin fiber; Chromatin; Cryo EM; Fractal nature; Interphase nuclei; Irregular folding; Mitotic chromosomes; X ray scattering

Indexed keywords

HISTONE H2B; HISTONE H3;

ARTICLE; CELL NUCLEUS; CHROMATIN; CHROMOSOME STRUCTURE; CRYOELECTRON MICROSCOPY; DNA STRAND; HELA CELL; HUMAN; HUMAN CELL; INTERPHASE; MITOSIS; NUCLEOSOME; X RAY CRYSTALLOGRAPHY;

EID: 84866165052     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.21222     Document Type: Article

References (64)

1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell, Fifth Edition 2007.
2. Kornberg RD, Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 1999; 98:285-94; PMID:10458604; http://dx.doi.org/10.1016/S0092-8674(00)81958-3.
3. Olins DE, Olins AL. Chromatin history: our view from the bridge. Nat Rev Mol Cell Biol 2003; 4:809-14; PMID:14570061.
4. Robinson PJ, Rhodes D. Structure of the '30 nm' chromatin fibre: a key role for the linker histone. Curr Opin Struct Biol 2006; 16:336-43; PMID:16714106; http://dx.doi.org/10.1016/j.sbi.2006.05.007.
5. Tremethick DJ. Higher-order structures of chromatin: the elusive 30 nm fiber. Cell 2007; 128:651-4; PMID:17320503; http://dx.doi.org/10.1016/j. cell.2007.02.008.
6. Sedat J, Manuelidis L. A direct approach to the structure of eukaryotic chromosomes. Cold Spring Harb Symp Quant Biol 1978; 42:331-50; PMID:98280; http://dx.doi.org/10.1101/SQB.1978.042.01.035.
7. Belmont AS, Sedat JW, Agard DA. A three-dimensional approach to mitotic chromosome structure: evidence for a complex hierarchical organization. J Cell Biol 1987; 105:77-92; PMID:3112167; http://dx.doi.org/10.1083/jcb.105.1.77.
8. Strukov YG, Wang Y, Belmont AS. Engineered chromosome regions with altered sequence composition demonstrate hierarchical large-scale folding within metaphase chromosomes. J Cell Biol 2003; 162:23-35; PMID:12835314; http://dx.doi.org/10.1083/jcb.200303098.
9. Matsuda A, Shao L, Boulanger J, Kervrann C, Carlton PM, Kner P, et al. Condensed mitotic chromosome structure at nanometer resolution using PALM and EGFP-histones. PLoS One 2010; 5:e12768; PMID:20856676; http://dx.doi. org/10.1371/journal.pone.0012768.
10. Belmont AS, Bruce K. Visualization of G1 chromosomes: a folded, twisted, supercoiled chromonema model of interphase chromatid structure. J Cell Biol 1994; 127:287-302; PMID:7929576; http://dx.doi. org/10.1083/jcb.127.2.287.
11. Eltsov M, Maclellan KM, Maeshima K, Frangakis AS, 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 U S A 2008; 105:19732-7; PMID:19064912; http://dx.doi.org/10.1073/pnas.0810057105.
12. McDowall AW, Smith JM, Dubochet J. Cryoelectron microscopy of vitrified chromosomes in situ. EMBO J 1986; 5:1395-402; PMID:3755397.
13. Maeshima K, Eltsov M. Packaging the genome: the structure of mitotic chromosomes. J Biochem 2008; 143:145-53; PMID:17981824; http://dx.doi. org/10.1093/jb/mvm214.
14. Roe R.-J. Methods of X-Ray and Neutron Scattering in Polymer Science. 2000.
15. Nishino Y, Eltsov M, Joti Y, Ito K, Takata H, Takahashi Y, et al. Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure. EMBO J 2012; 31:1644-53; PMID:22343941; http://dx.doi.org/10.1038/emboj.2012.35.
16. Dubochet J, Sartori Blanc N. The cell in absence of aggregation artifacts. Micron 2001; 32:91-9; PMID:10900384; http://dx.doi.org/10.1016/S0968-4328(00)00026-3.
17. Maeshima K, Hihara S, Takata H. New insight into the mitotic chromosome structure: irregular folding of nucleosome fibers without 30-nm chromatin structure. Cold Spring Harb Symp Quant Biol 2010; 75:439-44; PMID:21447821; http://dx.doi. org/10.1101/sqb.2010.75.034.
18. Langmore JP, Paulson JR. Low angle x-ray diffraction studies of chromatin structure in vivo and in isolated nuclei and metaphase chromosomes. J Cell Biol 1983; 96:1120-31; PMID:6682117; http://dx.doi. org/10.1083/jcb.96.4.1120.
19. Paulson JR, Langmore JP. Low angle x-ray diffraction studies of HeLa metaphase chromosomes: effects of histone phosphorylation and chromosome isolation procedure. J Cell Biol 1983; 96:1132-7; PMID:6833394; http://dx.doi.org/10.1083/jcb.96.4.1132.
20. Widom J, Klug A. Structure of the 300A chromatin filament: X-ray diffraction from oriented samples. Cell 1985; 43:207-13; PMID:4075395; http://dx.doi.org/10.1016/0092-8674(85)90025-X.
21. Lewis CD, Laemmli UK. Higher order metaphase chromosome structure: evidence for metalloprotein interactions. Cell 1982; 29:171-81; PMID:7105181; http://dx.doi.org/10.1016/0092-8674(82)90101-5.
22. Maeshima K, Laemmli UK. A two-step scaffolding model for mitotic chromosome assembly. Dev Cell 2003; 4:467-80; PMID:12689587; http://dx.doi. org/10.1016/S1534-5807(03)00092-3.
23. Langmore JP, Schutt C. The higher order structure of chicken erythrocyte chromosomes in vivo. Nature 1980; 288:620-2; PMID:7442809; http://dx.doi. org/10.1038/288620a0.
24. Woodcock CL. Chromatin fibers observed in situ in frozen hydrated sections. Native fiber diameter is not correlated with nucleosome repeat length. J Cell Biol 1994; 125:11-9; PMID:8138565; http://dx.doi. org/10.1083/jcb.125.1.11.
25. Nishino Y, Takahashi Y, Imamoto N, Ishikawa T, Maeshima K. Three-Dimensional Visualization of a Human Chromosome Using Coherent X-ray Diffraction. Physical Review Letters 2009; 102:18101 (4 pages)
26. Hirano T. At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 2006; 7:311-22; PMID:16633335; http://dx.doi.org/10.1038/nrm1909.
27. Wang JC. DNA topoisomerases. Annu Rev Biochem 1996; 65:635-92; PMID:8811192; http://dx.doi. org/10.1146/annurev.bi.65.070196.003223.
28. Laemmli UK, Cheng SM, Adolph KW, Paulson JR, Brown JA, Baumbach WR. Metaphase chromosome structure: the role of nonhistone proteins. Cold Spring Harb Symp Quant Biol 1978; 42:351-60; PMID:277351; http://dx.doi.org/10.1101/SQB.1978.042.01.036.
29. Earnshaw WC, Heck MM. Localization of topoisomerase II in mitotic chromosomes. J Cell Biol 1985; 100:1716-25; PMID:2985626; http://dx.doi. org/10.1083/jcb.100.5.1716.
30. Gasser SM, Laroche T, Falquet J, Boy de la Tour E, Laemmli UK. Metaphase chromosome structure. Involvement of topoisomerase II. J Mol Biol 1986; 188:613-29; PMID:3016287; http://dx.doi. org/10.1016/S0022-2836(86)80010-9.
31. Ono T, Fang Y, Spector DL, Hirano T. Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 2004; 15:3296-308; PMID:15146063; http://dx.doi. org/10.1091/mbc.E04-03-0242.
32. Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM. Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 2004; 117:6435-45; PMID:15572404; http://dx.doi.org/10.1242/jcs.01604.
33. Strukov YG, Belmont AS. Mitotic chromosome structure: reproducibility of folding and symmetry between sister chromatids. Biophys J 2009; 96:1617-28; PMID:19217877; http://dx.doi.org/10.1016/j. bpj.2008.10.051.
34. Bouchet-Marquis C, Dubochet J, Fakan S. Cryoelectron microscopy of vitrified sections: a new challenge for the analysis of functional nuclear architecture. Histochem Cell Biol 2006; 125:43-51; PMID:16328430; http://dx.doi.org/10.1007/s00418-005-0093-x.
35. Fakan S, van Driel R. The perichromatin region: a functional compartment in the nucleus that determines large-scale chromatin folding. Semin Cell Dev Biol 2007; 18:676-81; PMID:17920313; http://dx.doi.org/10.1016/j.semcdb.2007.08.010.
36. Dekker J. Mapping in vivo chromatin interactions in yeast suggests an extended chromatin fiber with regional variation in compaction. J Biol Chem 2008; 283:34532-40; PMID:18930918; http://dx.doi. org/10.1074/jbc.M806479200.
37. Fussner E, Ching RW, Bazett-Jones DP. Living without 30nm chromatin fibers. Trends Biochem Sci 2011; 36:1-6; PMID:20926298; http://dx.doi. org/10.1016/j.tibs.2010.09.002.
38. Fussner E, Djuric U, Strauss M, Hotta A, Perez-Iratxeta C, Lanner F, et al. Constitutive heterochromatin reorganization during somatic cell reprogramming. EMBO J 2011; 30:1778-89; PMID:21468033; http://dx.doi.org/10.1038/emboj.2011.96.
39. Schmidt PW. Use of scattering to determine the fractal dimension. The fractal approach to heterogeneous chemistry (edited by D Avnir) 1989:67-79.
40. 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; 28:3785-98; PMID:19927119; http://dx.doi.org/10.1038/emboj.2009.340.
41. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009; 326:289-93; PMID:19815776; http://dx.doi.org/10.1126/science.1181369.
42. Mirny LA. The fractal globule as a model of chromatin architecture in the cell. Chromosome Res 2011; 19:37-51; PMID:21274616; http://dx.doi. org/10.1007/s10577-010-9177-0.
43. Zhang Y, McCord RP, Ho YJ, Lajoie BR, Hildebrand DG, Simon AC, et al. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 2012; 148:908-21; PMID:22341456; http://dx.doi.org/10.1016/j. cell.2012.02.002.
44. Takahashi M. A fractal model of chromosomes and chromosomal DNA replication. J Theor Biol 1989; 141:117-36; PMID:2699341; http://dx.doi. org/10.1016/S0022-5193(89)80012-8.
45. Rouquette J, Genoud C, Vazquez-Nin GH, Kraus B, Cremer T, Fakan S. Revealing the high-resolution three-dimensional network of chromatin and interchromatin space: a novel electronmicroscopic approach to reconstructing nuclear architecture. Chromosome Res 2009; 17:801-10; PMID:19731052; http://dx.doi.org/10.1007/s10577-009-9070-x.
46. Cremer T, Markaki Y, Hübner B, Zunhammer A, Strickfaden H, Beichmanis S, et al. Chromosome Territory Organization within the Nucleus. Encyclopedia of Molecular Cell Biology and Molecular Medicine 2011.
47. Schermelleh L, Solovei I, Zink D, Cremer T. Twocolor fluorescence labeling of early and mid-to-late replicating chromatin in living cells. Chromosome Res 2001; 9:77-80; PMID:11272795; http://dx.doi. org/10.1023/A:1026799818566.
48. Berezney R, Malyavantham KS, Pliss A, Bhattacharya S, Acharya R. Spatio-temporal dynamics of genomic organization and function in the mammalian cell nucleus. Adv Enzyme Regul 2005; 45:17-26; PMID:16139341; http://dx.doi.org/10.1016/j.advenzreg. 2005.02.013.
49. Albiez H, Cremer M, Tiberi C, Vecchio L, Schermelleh L, Dittrich S, et al. Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks. Chromosome Res 2006; 14:707-33; PMID:17115328; http://dx.doi.org/10.1007/s10577-006-1086-x.
50. Markaki Y, Gunkel M, Schermelleh L, Beichmanis S, Neumann J, Heidemann M, et al. 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; 75:475-92; PMID:21467142; http://dx.doi.org/10.1101/sqb.2010.75.042.
51. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012; 485:376-80; PMID:22495300; http://dx.doi.org/10.1038/nature11082.
52. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M, Zhang J, et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 2010; 20:761-70; PMID:20430782; http://dx.doi. org/10.1101/gr.099655.109.
53. Hansen JC. Human mitotic chromosome structure: what happened to the 30-nm fibre? EMBO J 2012; 31:1621-3; PMID:22415369; http://dx.doi. org/10.1038/emboj.2012.66.
54. Finch JT, Klug A. Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci U S A 1976; 73:1897-901; PMID:1064861; http://dx.doi. org/10.1073/pnas.73.6.1897.
55. Marsden MP, Laemmli UK. Metaphase chromosome structure: evidence for a radial loop model. Cell 1979; 17:849-58; PMID:487432; http://dx.doi. org/10.1016/0092-8674(79)90325-8.
56. Woodcock CL, Frado LL, Rattner JB. The higherorder structure of chromatin: evidence for a helical ribbon arrangement. J Cell Biol 1984; 99:42-52; PMID:6736132; http://dx.doi.org/10.1083/jcb.99.1.42.
57. Widom J. Physicochemical studies of the folding of the 100 A nucleosome filament into the 300 A filament. Cation dependence. J Mol Biol 1986; 190:411-24; PMID:3783706; http://dx.doi. org/10.1016/0022-2836(86)90012-4.
58. Maeshima K, Eltsov M, Laemmli UK. Chromosome structure: improved immunolabeling for electron microscopy. Chromosoma 2005; 114:365-75; PMID:16175370; http://dx.doi.org/10.1007/s00412-005-0023-7.
59. Robinson PJ, Fairall L, Huynh VA, Rhodes D. EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure. Proc Natl Acad Sci U S A 2006; 103:6506-11; PMID:16617109; http://dx.doi. org/10.1073/pnas.0601212103.
60. Maeshima K, Hihara S, Eltsov M. Chromatin structure: does the 30-nm fibre exist in vivo? Curr Opin Cell Biol 2010; 22:291-7; PMID:20346642; http://dx.doi.org/10.1016/j.ceb.2010.03.001.
61. Scheffer MP, Eltsov M, Bednar J, Frangakis AS. Nucleosomes stacked with aligned dyad axes are found in native compact chromatin in vitro. J Struct Biol 2012; 178:207-14; PMID:22138167; http://dx.doi.org/10.1016/j.jsb.2011.11.020.
62. Scheffer MP, Eltsov M, Frangakis AS. Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei. Proc Natl Acad Sci U S A 2011; 108:16992-7; PMID:21969536; http://dx.doi. org/10.1073/pnas.1108268108.
63. Kizilyaprak C, Spehner D, Devys D, Schultz P. In vivo chromatin organization of mouse rod photoreceptors correlates with histone modifications. PLoS One 2010; 5:e11039; PMID:20543957; http://dx.doi.org/10.1371/journal.pone.0011039.
64. Uchiumi T, Traut RR, Kominami R. Monoclonal antibodies against acidic phosphoproteins P0, P1, and P2 of eukaryotic ribosomes as functional probes. J Biol Chem 1990; 265:89-95; PMID:1688437.