The dynamic organization of chromatin plays an essential role in the regulation of genetic activity, interconverting between open and compact forms at the global level. The mechanisms underlying these large-scale changes remain a topic of widespread interest. The simulations of nucleosome-decorated DNA reported herein reveal profound effects of the nucleosome itself on overall chromatin properties. Models that capture the long-range communication between proteins on nucleosome-decorated DNA chains incorporate DNA pathways different from those that were previously proposed based on ultracentrifugation and chemical cross-linking data. New quantitative biochemical assays measuring the rates of communication between interacting proteins bound to a promoter and an enhancer at the ends of saturated, precisely positioned, nucleosome-decorated DNA chains reveal a chromatin architecture with a three-nucleosome repeat, a model inconsistent with the two-start configurations deduced from earlier physical studies. Accompanying computations uncover small differences in the twisting of successive base pairs that seemingly give rise to the observed global properties. These data suggest that the novel state of chromatin determined under physiological conditions differs from that deduced under standard physical conditions, likely reflecting the different salt conditions used in the two types of experiments. This novel chromatin state may be important for a number of DNA transactions that occur in the cell nucleus.
REFERENCES
1.
J. T.
Finch
and A.
Klug
, “Solenoidal model for superstructure in chromatin
,” Proc. Natl. Acad. Sci. U. S. A.
73
(6
), 1897
–1901
(1976
).2.
R. D.
Kornberg
, “Chromatin structure: A repeating unit of histones and DNA
,” Science
184
(4139
), 868
–871
(1974
).3.
C. L. F.
Woodcock
, L.-L. Y.
Frado
, and J. B.
Rattner
, “The higher-order structure of chromatin: Evidence for a helical ribbon arrangement
,” J. Cell Biol.
99
(1
), 42
–52
(1984
).4.
T. J.
Richmond
, J. T.
Finch
, B.
Rushton
, D.
Rhodes
, and A.
Klug
, “Structure of the nucleosome core particle at 7 Å resolution
,” Nature
311
(5986
), 532
–537
(1984
).5.
T.
Schalch
, S.
Duda
, D. F.
Sargent
, and T. J.
Richmond
, “X-ray structure of a tetranucleosome and its implications for the chromatin fibre
,” Nature
436
(7047
), 138
–141
(2005
).6.
T. D.
Frouws
, H.-G.
Patterton
, and B. T.
Sewell
, “Histone octamer helical tubes suggest that an internucleosomal four-helix bundle stabilizes the chromatin fiber
,” Biophys. J.
96
(8
), 3363
–3371
(2009
).7.
B.
Ekundayo
, T. J.
Richmond
, and T.
Schalch
, “Capturing structural heterogeneity in chromatin fibers
,” J. Mol. Biol.
429
(20
), 3031
–3042
(2017
).8.
B.-R.
Zhou
, J.
Jiang
, R.
Ghirlando
, D.
Norouzi
, K.
Sathish Yadav
, H.
Feng
, R.
Wang
, P.
Zhang
, V.
Zhurkin
, and Y.
Bai
, “Revisit of reconstituted 30-nm nucleosome arrays reveals an ensemble of dynamic structures
,” J. Mol. Biol.
430
(18
), 3093
–3110
(2018
).9.
I.
Garcia-Saez
, H.
Menoni
, R.
Boopathi
, M. S.
Shukla
, L.
Soueidan
, M.
Noirclerc-Savoye
, A.
Le Roy
, D. A.
Skoufias
, J.
Bednar
, A.
Hamiche
, D.
Angelov
, C.
Petosa
, and S.
Dimitrov
, “Structure of an H1-bound 6-nucleosome array reveals an untwisted two-start chromatin fiber conformation
,” Mol. Cell
72
(5
), 902
–915.e7
(2018
).10.
Z.
Adhireksan
, D.
Sharma
, P. L.
Lee
, and C. A.
Davey
, “Near-atomic resolution structures of interdigitated nucleosome fibres
,” Nat. Commun.
11
(1
), 4747
(2020
).11.
F.
Song
, P.
Chen
, D.
Sun
, M.
Wang
, L.
Dong
, D.
Liang
, R.-M.
Xu
, P.
Zhu
, and G.
Li
, “Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units
,” Science
344
(6182
), 376
–380
(2014
).12.
C.
Wu
and A.
Travers
, “Modelling and DNA topology of compact 2-start and 1-start chromatin fibres
,” Nucleic Acids Res.
47
(18
), 9902
–9924
(2019
).13.
J. M.
Buckwalter
, D.
Norouzi
, A.
Harutyunyan
, V. B.
Zhurkin
, and S. A.
Grigoryev
, “Regulation of chromatin folding by conformational variations of nucleosome linker DNA
,” Nucleic Acids Res.
45
(16
), 9372
–9387
(2017
).14.
M. V.
Bass
, T.
Nikitina
, D.
Norouzi
, V. B.
Zhurkin
, and S. A.
Grigoryev
, “Nucleosome spacing periodically modulates nucleosome chain folding and DNA topology in circular nucleosome arrays
,” J. Biol. Chem.
294
(11
), 4233
–4246
(2019
).15.
V. B.
Zhurkin
and D.
Norouzi
, “Topological polymorphism of nucleosome fibers and folding of chromatin
,” Biophys. J.
120
, 577
–585
(2021
).16.
S. A.
Grigoryev
, G.
Arya
, S.
Correll
, C. L.
Woodcock
, and T.
Schlick
, “Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions
,” Proc. Natl. Acad. Sci. U. S. A.
106
(32
), 13317
–13322
(2009
).17.
V.
Makarov
, S.
Dimitrov
, V.
Smirnov
, and I.
Pashev
, “A triple helix model for the structure of chromatin fiber
,” FEBS Lett.
181
(2
), 357
–361
(1985
).18.
C. L.
Woodcock
, S. A.
Grigoryev
, R. A.
Horowitz
, and N.
Whitaker
, “A chromatin folding model that incorporates linker variability generates fibers resembling the native structures
,” Proc. Natl. Acad. Sci. U. S. A.
90
(19
), 9021
–9025
(1993
).19.
O. I.
Kulaeva
, G.
Zheng
, Y. S.
Polikanov
, A. V.
Colasanti
, N.
Clauvelin
, S.
Mukhopadhyay
, A. M.
Sengupta
, V. M.
Studitsky
, and W. K.
Olson
, “Internucleosomal interactions mediated by histone tails allow distant communication in chromatin
,” J. Biol. Chem.
287
(24
), 20248
–20257
(2012
).20.
E. V.
Nizovtseva
, N.
Clauvelin
, S.
Todolli
, Y. S.
Polikanov
, O. I.
Kulaeva
, S.
Wengrzynek
, W. K.
Olson
, and V. M.
Studitsky
, “Nucleosome-free DNA regions differentially affect distant communication in chromatin
,” Nucleic Acids Res.
45
(6
), 3059
–3067
(2017
).21.
E. V.
Nizovtseva
, Y. S.
Polikanov
, O. I.
Kulaeva
, N.
Clauvelin
, Y. V.
Postnikov
, W. K.
Olson
, and V. M.
Studitsky
, “Opposite effects of histone H1 and HMGN5 protein on distant interactions in chromatin
,” Mol. Biol.
53
(6
), 912
–921
(2019
).22.
L.
Stryer
and R. P.
Haugland
, “Energy transfer: A spectroscopic ruler
,” Proc. Natl. Acad. Sci. U. S. A.
58
(2
), 719
–726
(1967
).23.
R. M.
Clegg
, A. I. H.
Murchie
, A.
Zechel
, and D. M. J.
Lilley
, “Observing the helical geometry of double-stranded DNA in solution by fluorescence resonance energy transfer
,” Proc. Natl. Acad. Sci. U. S. A.
90
(7
), 2994
–2998
(1993
).24.
N.
Clauvelin
, P.
Lo
, O. I.
Kulaeva
, E. V.
Nizovtseva
, J.
Diaz-Montes
, J.
Zola
, M.
Parashar
, V. M.
Studitsky
, and W. K.
Olson
, “Nucleosome positioning and composition modulate in silico chromatin flexibility
,” J. Phys.: Condens. Matter
27
(6
), 064112
(2015
).25.
D.
Norouzi
and V. B.
Zhurkin
, “Topological polymorphism of the two-start chromatin fiber
,” Biophys. J.
108
(10
), 2591
–2600
(2015
).26.
B.
Dorigo
, T.
Schalch
, A.
Kulangara
, S.
Duda
, R. R.
Schroeder
, and T. J.
Richmond
, “Nucleosome arrays reveal the two-start organization of the chromatin fiber
,” Science
306
(5701
), 1571
–1573
(2004
).27.
A.
Routh
, S.
Sandin
, and D.
Rhodes
, “Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure
,” Proc. Natl. Acad. Sci. U. S. A.
105
(26
), 8872
–8877
(2008
).28.
Y. S.
Polikanov
, M. A.
Rubtsov
, and V. M.
Studitsky
, “Biochemical analysis of enhancer-promoter communication in chromatin
,” Methods
41
(3
), 250
–258
(2007
).29.
H. M.
Berman
, J.
Westbrook
, Z.
Feng
, G. B.
Gilliland
, H.
Weissig
, I. N.
Shindyalov
, and P. E.
Bourne
, “The protein data bank
,” Nucleic Acids Res.
28
(1
), 235
–242
(2000
).30.
S.
Todolli
, R. T.
Young
, A. S.
Watkins
, A.
Bu Sha
, J.
Yager
, and W. K.
Olson
, “Surprising twists in nucleosomal DNA with implication for higher-order folding
,” J. Mol. Biol.
433
(18
), 167121
(2021
).31.
K.
Luger
, A. W.
Mäder
, R. K.
Richmond
, D. F.
Sargent
, and T. J.
Richmond
, “Crystal structure of the nucleosome core particle at 2.8 Å resolution
,” Nature
389
(6648
), 251
–260
(1997
).32.
T. P.
Yang
, S. K.
Hansen
, K. K.
Oishi
, O. A.
Ryder
, and B. A.
Hamkalo
, “Characterization of a cloned repetitive DNA sequence concentrated on the human X chromosome
,” Proc. Natl. Acad. Sci. U. S. A.
79
(21
), 6593
–6597
(1982
).33.
P. T.
Lowary
and J.
Widom
, “New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning
,” J. Mol. Biol.
276
(1
), 19
–42
(1998
).34.
C. A.
Davey
, D. F.
Sargent
, K.
Luger
, A. W.
Maeder
, and T. J.
Richmond
, “Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution
,” J. Mol. Biol.
319
(5
), 1097
–1113
(2002
).35.
X.-J.
Lu
and W. K.
Olson
, “3DNA: A software package for the analysis, rebuilding, and visualization of three-dimensional nucleic acid structures
,” Nucleic Acids Res.
31
(17
), 5108
–5121
(2003
).36.
L.
Britton
, W. K.
Olson
, and I.
Tobias
, “Two perspectives on the twist of DNA
,” J. Chem. Phys.
131
(24
), 245101
(2009
).37.
N.
Clauvelin
, W. K.
Olson
, and I.
Tobias
, “Characterization of the geometry and topology of DNA pictured as a discrete collection of atoms
,” J. Chem. Theory Comput.
8
(3
), 1092
–1107
(2012
).38.
E. V.
Nizovtseva
, S.
Todolli
, W. K.
Olson
, and V. M.
Studitsky
, “Towards quantitative analysis of gene regulation by enhancers
,” Epigenomics
9
(9
), 1219
–1231
(2017
).39.
R. E.
Dickerson
, M.
Bansal
, C. R.
Calladine
, S.
Diekmann
, W. N.
Hunter
, O.
Kennard
, E.
von Kitzing
, R.
Lavery
, H. C. M.
Nelson
, W. K.
Olson
, W.
Saenger
, Z.
Shakked
, H.
Sklenar
, D. M.
Soumpasis
, C.-S.
Tung
, A. H.-J.
Wang
, and V. B.
Zhurkin
, “Definitions and nomenclature of nucleic acid structure parameters
,” Nucleic Acids Res.
17
(5
), 1797
–1803
(1989
).40.
L.
Czapla
, D.
Swigon
, and W. K.
Olson
, “Sequence-dependent effects in the cyclization of short DNA
,” J. Chem. Theory Comput.
2
(3
), 685
–695
(2006
).41.
N.
Metropolis
, A. W.
Rosenbluth
, M. N.
Rosenbluth
, A. H.
Teller
, and E.
Teller
, “Equation of state calculations by fast computing machines
,” J. Chem. Phys.
21
(6
), 1087
–1092
(1953
).42.
W. K.
Hastings
, “Monte Carlo sampling methods using Markov chains and their applications
,” Biometrika
57
(1
), 97
–109
(1970
).43.
R.
Glyde
, F.
Ye
, V. C.
Darbari
, N.
Zhang
, M.
Buck
, and X.
Zhang
, “Structures of RNA polymerase closed and intermediate complexes reveal mechanisms of DNA opening and transcription initiation
,” Mol. Cell
67
(1
), 106
–116.e4
(2017
).44.
J. C.
Hansen
, J.
Ausio
, V. H.
Stanik
, and K. E.
van Holde
, “Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1
,” Biochemistry
28
(23
), 9129
–9136
(1989
).45.
T.
Miyazawa
, “Molecular vibrations and structure of high polymers. II. Helical parameters of infinite polymer chains as functions of bond lengths, bond angles, and internal rotation angles
,” J. Polym. Sci.
55
(161
), 215
–231
(1961
).46.
H.
Sugeta
and T.
Miyazawa
, “General method for calculating helical parameters of polymer chains from bond lengths, bond angles, and internal-rotation angles
,” Biopolymers
5
(7
), 673
–679
(1967
).47.
D.
Norouzi
and V. B.
Zhurkin
, “Dynamics of chromatin fibers: Comparison of Monte Carlo simulations with force spectroscopy
,” Biophys. J.
115
(9
), 1644
–1655
(2018
).48.
M.
Ohno
, T.
Ando
, D. G.
Priest
, V.
Kumar
, Y.
Yoshida
, and Y.
Taniguchi
, “Sub-nucleosomal genome structure reveals distinct nucleosome folding motifs
,” Cell
176
(3
), 520
–534.e25
(2019
).49.
Y. S.
Polikanov
and V. M.
Studitsky
, “Analysis of distant communication on defined chromatin templates in vitro
,” Methods Mol. Biol.
543
, 563
–576
(2009
).50.
Y.
Liu
, V.
Bondarenko
, A.
Ninfa
, and V. M.
Studitsky
, “DNA supercoiling allows enhancer action over a large distance
,” Proc. Natl. Acad. Sci. U. S. A.
98
, 14883
–14888
(2001
).51.
M. A.
Rubtsov
, Y. S.
Polikanov
, V. A.
Bondarenko
, Y.-H.
Wang
, and V. M.
Studitsky
, “Chromatin structure can strongly facilitate enhancer action over a distance
,” Proc. Natl. Acad. Sci. U. S. A.
103
(47
), 17690
–17695
(2006
).52.
O. I.
Kulaeva
, E. V.
Nizovtseva
, Y. S.
Polikanov
, S. V.
Ulianov
, and V. M.
Studitsky
, “Distant activation of transcription: Mechanisms of enhancer action
,” Mol. Cell. Biol.
32
(24
), 4892
–4897
(2012
).53.
Y.
Suzuki
, N.
Horikoshi
, D.
Kato
, and H.
Kurumizaka
, “Crystal structure of the nucleosome containing histone H3 with crotonylated lysine 122
,” Biochem. Biophys. Res. Commun.
469
(3
), 483
–489
(2016
).54.
W. K.
Olson
, N.
Clauvelin
, A. V.
Colasanti
, G.
Singh
, and G.
Zheng
, “Insights into gene expression and packaging from computer simulations
,” Biophys. Rev.
4
(3
), 171
–178
(2012
).55.
S. J.
Correll
, M. H.
Schubert
, and S. A.
Grigoryev
, “Short nucleosome repeats impose rotational modulations on chromatin fibre folding
,” EMBO J.
31
(10
), 2416
–2426
(2012
).56.
R. K.
Suto
, R. S.
Edayathumangalam
, C. L.
White
, C.
Melander
, J. M.
Gottesfeld
, P. B.
Dervan
, and K.
Luger
, “Crystal structures of nucleosome core particles in complex with minor groove DNA-binding ligands
,” J. Mol. Biol.
326
(2
), 371
–380
(2003
).57.
R. S.
Edayathumangalam
, P.
Weyermann
, P. B.
Dervan
, J. M.
Gottesfeld
, and K.
Luger
, “Nucleosomes in solution exist as a mixture of twist-defect states
,” J. Mol. Biol.
345
(1
), 103
–114
(2005
).58.
G. D.
Bowman
and S.
Deindl
, “Remodeling the genome with DNA twists
,” Science
366
(6461
), 35
–36
(2019
).59.
M.
Li
, X.
Xia
, Y.
Tian
, Q.
Jia
, X.
Liu
, Y.
Lu
, M.
Li
, X.
Li
, and Z.
Chen
, “Mechanism of DNA translocation underlying chromatin remodelling by Snf2
,” Nature
567
(7748
), 409
–413
(2019
).60.
L.
Farnung
, M.
Ochmann
, and P.
Cramer
, “Nucleosome-CHD4 chromatin remodeler structure maps human disease mutations
,” eLife
9
, e56178
(2020
).61.
S.
Kilic
, S.
Felekyan
, O.
Doroshenko
, I.
Boichenko
, M.
Dimura
, H.
Vardanyan
, L. C.
Bryan
, G.
Arya
, C. A. M.
Seidel
, and B.
Fierz
, “Single-molecule FRET reveals multiscale chromatin dynamics modulated by HP1α
,” Nat. Commun.
9
(1
), 235
(2018
).62.
B.
Dorigo
, T.
Schalch
, K.
Bystricky
, and T. J.
Richmond
, “Chromatin fiber folding: Requirement for the histone H4 N-terminal tail
,” J. Mol. Biol.
327
(1
), 85
–96
(2003
).63.
N.
Korolev
, “How potassium came to be the dominant biological cation: Of metabolism, chemiosmosis, and cation selectivity since the beginnings of life
,” Bioessays
43
(1
), e2000108
(2021
).64.
A.
Allahverdi
, R.
Yang
, N.
Korolev
, Y.
Fan
, C. A.
Davey
, C.-F.
Liu
, and L.
Nordenskiöld
, “The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association
,” Nucleic Acids Res.
39
(5
), 1680
–1691
(2010
).65.
A.
Allahverdi
, Q.
Chen
, N.
Korolev
, and L.
Nordenskiöld
, “Chromatin compaction under mixed salt conditions: Opposite effects of sodium and potassium ions on nucleosome array folding
,” Sci. Rep.
5
, 8512
(2015
).66.
A. V.
Lyubitelev
, V. M.
Studitsky
, A. V.
Feofanov
, and M. P.
Kirpichnikov
, “Effect of sodium and potassium ions on conformation of linker parts of nucleosomes
,” Moscow Univ. Biol. Sci. Bull.
72
(3
), 146
–150
(2017
).67.
T. V.
Andreeva
, N. V.
Maluchenko
, A. L.
Sivkina
, O. V.
Chertkov
, M. E.
Valieva
, E. Y.
Kotova
, M. P.
Kirpichnikov
, V. M.
Studitsky
, and A. V.
Feofanov
, “Na+ and K+ ions differently affect nucleosome structure, stability, and interactions with proteins
,” Microsc. Microanal.
28
(1
), 243
–253
(2022
).68.
M.
Pasi
, J. H.
Maddocks
, and R.
Lavery
, “Analyzing ion distributions around DNA: Sequence-dependence of potassium ion distributions from microsecond molecular dynamics
,” Nucleic Acids Res.
43
(4
), 2412
–2423
(2015
).69.
A.
Savelyev
and A. D.
MacKerell
, Jr., “Differential deformability of the DNA minor groove and altered BI/BII backbone conformational equilibrium by the monovalent ions Li+, Na+, K+, and Rb+ via water-mediated hydrogen bonding
,” J. Chem. Theory Comput.
11
(9
), 4473
–4485
(2015
).70.
P.
Várnai
and K.
Zakrzewska
, “DNA and its counterions: A molecular dynamics study
,” Nucleic Acids Res.
32
(14
), 4269
–4280
(2004
).71.
Y.
Cheng
, N.
Korolev
, and L.
Nordenskiöld
, “Similarities and differences in interaction of K+ and Na+ with condensed ordered DNA. A molecular dynamics computer simulation study
,” Nucleic Acids Res.
34
(2
), 686
–696
(2006
).72.
A.
Savelyev
and G. A.
Papoian
, “Electrostatic, steric, and hydration interactions favor Na+ condensation around DNA compared with K+
,” J. Am. Chem. Soc.
128
(45
), 14506
–14518
(2006
).73.
J.
Yoo
and A.
Aksimentiev
, “Competitive binding of cations to duplex DNA revealed through molecular dynamics simulations
,” J. Phys. Chem. B
116
(43
), 12946
–12954
(2012
).74.
R.
Lavery
, J. H.
Maddocks
, M.
Pasi
, and K.
Zakrzewska
, “Analyzing ion distributions around DNA
,” Nucleic Acids Res.
42
(12
), 8138
–8149
(2014
).75.
W.
He
, Y.-L.
Chen
, L.
Pollack
, and S.
Kirmizialtin
, “The structural plasticity of nucleic acid duplexes revealed by WAXS and MD
,” Sci. Adv.
7
(17
), eabf6106
(2021
).76.
P. D.
Dans
, L.
Danilāne
, I.
Ivani
, T.
Dršata
, F.
Lankaš
, A.
Hospital
, J.
Walther
, R. I.
Pujagut
, F.
Battistini
, J. L.
Gelpí
, R.
Lavery
, and M.
Orozco
, “Long-timescale dynamics of the Drew-Dickerson dodecamer
,” Nucleic Acids Res.
44
(9
), 4052
–4066
(2016
).77.
W. K.
Olson
and V. B.
Zhurkin
, “Working the kinks out of nucleosomal DNA
,” Curr. Opin. Struct. Biol.
21
(3
), 348
–357
(2011
).78.
R.
Retureau
, N.
Foloppe
, A.
Elbahnsi
, C.
Oguey
, and B.
Hartmann
, “A dynamic view of DNA structure within the nucleosome: Biological implications
,” J. Struct. Biol.
211
(1
), 107511
(2020
).79.
B.
Heddi
, N.
Foloppe
, E.
Hantz
, and B.
Hartmann
, “The DNA structure responds differently to physiological concentrations of K+ or Na+
,” J. Mol. Biol.
368
(5
), 1403
–1411
(2007
).80.
D.
Norouzi
, A.
Katebi
, F.
Cui
, and V. B.
Zhurkin
, “Topological diversity of chromatin fibers: Interplay between nucleosome repeat length, DNA linking number and the level of transcription
,” AIMS Biophys.
2
(4
), 613
–629
(2015
).81.
W.
Alvarado
, J.
Moller
, A. L.
Ferguson
, and J. J.
de Pablo
, “Tetranucleosome interactions drive chromatin folding
,” ACS Cent. Sci.
7
(6
), 1019
–1027
(2021
).82.
T.-H. S.
Hsieh
, A.
Weiner
, B.
Lajoie
, J.
Dekker
, N.
Friedman
, and O. J.
Rando
, “Mapping nucleosome resolution chromosome folding in yeast by Micro-C
,” Cell
162
(1
), 108
–119
(2015
).83.
V. I.
Risca
, S. K.
Denny
, A. F.
Straight
, and W. J.
Greenleaf
, “Variable chromatin structure revealed by in situ spatially correlated DNA cleavage mapping
,” Nature
541
(7636
), 237
–241
(2017
).84.
T.-H. S.
Hsieh
, C.
Cattoglio
, E.
Slobodyanyuk
, A. S.
Hansen
, O. J.
Rando
, R.
Tjian
, and X.
Darzacq
, “Resolving the 3D landscape of transcription-linked mammalian chromatin folding
,” Mol. Cell
78
(3
), 539
–553.e8
(2020
).85.
N.
Krietenstein
, S.
Abraham
, S. V.
Venev
, N.
Abdennur
, J.
Gibcus
, T.-H. S.
Hsieh
, K. M.
Parsi
, L.
Yang
, R.
Maehr
, L. A.
Mirny
, J.
Dekker
, and O. J.
Rando
, “Ultrastructural details of mammalian chromosome architecture
,” Mol. Cell
78
(3
), 554
–565.e7
(2020
).86.
M. A.
Ricci
, C.
Manzo
, M. F.
Garcıa-Parajo
, M.
Lakadamyali
, and M. P.
Cosma
, “Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo
,” Cell
160
(6
), 1145
–1158
(2015
).87.
K.
Maeshima
, R.
Rogge
, S.
Tamura
, Y.
Joti
, T.
Hikima
, H.
Szerlong
, C.
Krause
, J.
Herman
, E.
Seidel
, J.
DeLuca
, T.
Ishikawa
, and J. C.
Hansen
, “Nucleosomal arrays self-assemble into supramolecular globular structures lacking 30-nm fibers
,” EMBO J.
35
(10
), 1115
–1132
(2016
).88.
H. D.
Ou
, S.
Phan
, T. J.
Deerinck
, A.
Thor
, M. H.
Ellisman
, and C. C.
O’Shea
, “ChromEMT: Visualizing 3D chromatin structure and compaction in interphase and mitotic cells
,” Science
357
(6349
), eaag0025
(2017
).89.
D. C.
Woods
, F.
Rodríguez-Ropero
, and J.
Wereszczynski
, “The dynamic influence of linker histone saturation within the poly-nucleosome array
,” J. Mol. Biol.
433
(10
), 166902
(2021
).90.
X.-J.
Lu
, Z.
Shakked
, and W. K.
Olson
, “A-form conformational motifs in ligand-bound DNA structures
,” J. Mol. Biol.
300
(4
), 819
–840
(2000
).© 2024 Author(s). Published under an exclusive license by AIP Publishing.
2024
Author(s)
You do not currently have access to this content.
