Nucleosome Chiral Transition under Positive Torsional Stress in Single Chromatin Fibers

Molecular Cell

Volumn 27, Issue 1, 2007, Pages 135-147

  Bancaud, Aurélien ^a   Wagner, Gaudeline ^a   Conde e Silva, Natalia ^b   Lavelle, Christophe ^b,c,d   Wong, Hua ^c   Mozziconacci, Julien ^c   Barbi, Maria ^c   Sivolob, Andrei ^e   Le Cam, Eric ^d   Mouawad, Liliane ^f   Viovy, Jean Louis ^a   Victor, Jean Marc ^c   Prunell, Ariel ^b  

^a INSTITUT CURIE   (France)

^b INSTITUT JACQUES MONOD   (France)

^c UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

^e TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

^f Centre Universitaire   (France)

Author keywords

DNA

Indexed keywords

DIMER; RNA POLYMERASE;

ARTICLE; CHIRALITY; CHROMATIN STRUCTURE; DNA BINDING; ENERGY TRANSFER; NUCLEOSOME; TORSION;

BIOMECHANICS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NUCLEOSOMES; ROTATION; TIME FACTORS; TORSION;

EID: 34250803868     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.05.037     Document Type: Article

References (53)

1. Alilat M., Sivolob A., Révet B., and Prunell A. Nucleosome dynamics. IV. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA particle. J. Mol. Biol. 291 (1999) 815-841
2. Baer B.W., and Rhodes D. Eukaryotic RNA polymerase II binds to nucleosome cores from transcribed genes. Nature 301 (1983) 482-488
3. Bahar I., and Rader A.J. Coarse-grained normal mode analysis in structural biology. Curr. Opin. Struct. Biol. 15 (2005) 586-592
4. Bancaud A., Conde e Silva N., Barbi M., Wagner G., Allemand J.-F., Mozziconacci J., Lavelle C., Croquette V., Victor J.-M., Prunell A., and Viovy J.-L. Structural plasticity of single chromatin fibers revealed by torsional manipulation. Nat. Struct. Mol. Biol. 13 (2006) 444-450
5. Baneres J.L., Parello J., Zaccai J., and Svergun D. A neutron scattering study of the histone sub-assemblies within the nucleosome protein core. In: Dianoux A.J. (Ed). ILL Millenium Symposium and European User Meeting (2001), I.L.L., Grenoble, France 55-57
6. Bazett-Jones D.P., Mendez E., Czarnota G.J., Ottensmeyer F.P., and Allfrey V.G. Visualization and analysis of unfolded nucleosomes associated with transcribing chromatin. Nucleic Acids Res. 24 (1996) 321-329
7. Benedict R.C., Moudrianakis E.N., and Ackers G.K. Interactions of the nucleosomal core histones: a calorimetric study of octamer assembly. Biochemistry 23 (1984) 1214-1218
8. Bertin A., Leforestier A., Durand D., and Livolant F. Role of histone tails in the conformation and interactions of nucleosome core particles. Biochemistry 43 (2004) 4773-4780
9. Bondarenko V.A., Steele L.M., Ujvari A., Gaykalova D.A., Kulaeva O.I., Polikanov Y.S., Luse D.S., and Studitsky V.M. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol. Cell 24 (2006) 469-479
10. Brooks B., Bruccoleri R., Olafson B., States D., Swaminathan S., and Karplus M. CHARMM: a program for macromolecular energy, minimization and molecular dynamics calculations. J. Comp. Chem. 4 (1983) 187-217
11. Brower-Toland B.D., Smith C.L., Yeh R.C., Lis J.T., Peterson C.L., and Wang M.D. Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. USA 99 (2002) 1960-1965
12. Claudet C., Angelov D., Bouvet P., Dimitrov S., and Bednar J. Histone octamer instability under single molecule experiments conditions. J. Biol. Chem. 280 (2005) 19958-19965
13. Conde e Silva N., Black B.E., Sivolob A., Filipski J., Cleveland D.W., and Prunell A. CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization. J. Mol. Biol. 370 (2007) 555-573
14. Duband-Goulet I., Carot V., Ulyanov A.V., Douc-Rasy S., and Prunell A. Chromatin reconstitution on small DNA rings. IV. DNA supercoiling and nucleosome sequence preference. J. Mol. Biol. 224 (1992) 981-1001
15. Epshtein V., and Nudler E. Cooperation between RNA polymerase molecules in transcription elongation. Science 300 (2003) 801-805
16. Hamiche A., Carot V., Alilat M., De Lucia F., O'Donohue M.F., Révet B., and Prunell A. Interaction of the histone (H3-H4)2 tetramer of the nucleosome with positively supercoiled DNA minicircles: potential flipping of the protein from a left- to a right-handed superhelical form. Proc. Natl. Acad. Sci. USA 93 (1996) 7588-7593
17. Harada Y., Ohara O., Takatsuki A., Itoh H., Shimamoto N., and Kinosita Jr. K. Direct observation of DNA rotation during transcription by Escherichia coli RNA polymerase. Nature 409 (2001) 113-115
18. Huynh V.A., Robinson P.J., and Rhodes D. A method for the in vitro reconstitution of a defined "30 nm" chromatin fiber containing stoichiometric amounts of the linker histone. J. Mol. Biol. 345 (2005) 957-968
19. Ishimi Y., and Kikuchi A. Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J. Biol. Chem. 266 (1991) 7025-7029
20. Ito T., Ikehara T., Nakagawa T., Kraus W.L., and Muramatsu M. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev. 14 (2000) 1899-1907
21. Jackson V. Influence of positive stress on nucleosome assembly. Biochemistry 32 (1993) 5901-5912
22. Kepert J.F., Mazurkiewicz J., Heuvelman G.L., Toth K.F., and Rippe K. NAP1 modulates binding of linker histone H1 to chromatin and induces an extended chromatin fiber conformation. J. Biol. Chem. 280 (2005) 34063-34072
23. Kimura H., and Cook P.R. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 153 (2001) 1341-1353
24. Kireeva M.L., Walter W., Tchernajenko V., Bondarenko V., Kashlev M., and Studitsky V.M. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol. Cell 9 (2002) 541-542
25. Korolev N., Lyubartsev A.P., and Nordenskiold L. Computer modelling demonstrates that electrostatic attraction of nucleosomal DNA is mediated by histone tails. Biophys. J. 90 (2006) 4305-4316
26. Lee M.S., and Garrard W.T. Positive DNA supercoiling generates a chromatin conformation characteristic of highly active genes. Proc. Natl. Acad. Sci. USA 88 (1991) 9675-9679
27. Li G., Levitus M., Bustamante C., and Widom J. Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12 (2005) 46-53
28. Liu L.F., and Wang J.C. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84 (1987) 7024-7027
29. Ljungman M., and Hanawalt P.C. Localized torsional tension in the DNA of human cells. Proc. Natl. Acad. Sci. USA 89 (1992) 6055-6059
30. Louters L., and Chalkley R. Exchange of histones H1, H2A, and H2B in vivo. Biochemistry 24 (1985) 3080-3085
31. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389 (1997) 251-260
32. McKerell Jr. A.D., Brooks B., Brooks C.L.I.I.I., Nilsson L., Roux B., Won Y., and Karplus M. CHARMM: the energy function and its parameterization with an overview of the program. In: Schleyer P.v.R. (Ed). The Encyclopedia of Computational Chemistry (1998), John Wiley and Sons, Chichester, UK 271-277
33. McKerell Jr. A.D., Bashford D., Bellott M., Dunbrack Jr. R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S., et al. All-atom empirical potential for molecular modelling and dynamics studies of proteins. J. Phys. Chem. B 102 (1998) 3586-3616
34. Mihardja S., Spakowitz A.J., Zhang Y., and Bustamante C. Effect of force on mononucleosomal dynamics. Proc. Natl. Acad. Sci. USA 103 (2006) 15871-15876
35. Mouawad L., and Perahia D. Diagonalization in a mixed basis: a method to compute low-frequency normal modes for large macromolecules. Biopolymers 33 (1993) 599-611
36. Mouawad L., and Perahia D. All-atom normal mode calculations of large molecular systems using iterative methods. In: Cui Q., and Bahar I. (Eds). Normal Mode Analysis: Theory and Applications to Biological and Chemical Systems (2006), CRC Press, Boca Raton, FL 17-39
37. Neukirch S., van der Heijden G.H.M., and Thompson J.M.T. Writhing instabilities of twisted rods: from infinite to finite lengths. J. Mech. Phys. Solids 50 (2002) 1175-1191
38. Pfaffle P., Gerlach V., Bunzel L., and Jackson V. In vitro evidence that transcription-induced stress causes nucleosome dissolution and regeneration. J. Biol. Chem. 265 (1990) 16830-16840
39. Protacio R.U., and Widom J. Nucleosome transcription studied in a real-time synchronous system: test of the lexosome model and direct measurement of effects due to histone octamer. J. Mol. Biol. 256 (1996) 458-472
40. Reinberg D., and Sims III R.J. De FACTo nucleosome dynamics. J. Biol. Chem. 281 (2006) 23297-23301
41. Ruiz-Carrillo A., and Jorcano J.L. Nucleohistone assembly: sequential binding of histone H3-H4 tetramer and histone H2A-H2B dimer to DNA. Cold Spring Harb. Symp. Quant. Biol. 42 (1978) 165-170
42. Salceda J., Fernandez X., and Roca J. Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J. 25 (2006) 2575-2583
43. Schwager S., Retief J.D., de Groot P., and von Holt C. Rapide exchange of histones H2A and H2B in sea urchin embryo chromatin. FEBS Lett. 189 (1985) 305-309
44. Sivolob A., and Prunell A. Nucleosome conformational flexibility and implications for chromatin dynamics. Philos. Transact. A Math. Philos. Transact. A Math. Phys. Eng. Sci. 362 (2004) 1519-1547
45. Sivolob A., De Lucia F., Alilat M., and Prunell A. Nucleosome dynamics. VI. Histone tail regulation of tetrasome chiral transition. A relaxation study of tetrasomes on DNA minicircles. J. Mol. Biol. 295 (2000) 55-69
46. Strick T.R., Allemand J.F., Bensimon D., Bensimon A., and Croquette V. The elasticity of a single supercoiled DNA molecule. Science 271 (1996) 1835-1837
47. Studitsky V.M., Kassavetis G.A., Geiduschek E.P., and Felsenfeld G. Mechanism of transcription through the nucleosome by eukaryotic RNA polymerase. Science 278 (1997) 1960-1963
48. Tomschik M., Zheng H., van Holde K., Zlatanova J., and Leuba S.H. Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 102 (2005) 3278-3283
49. van Holde K.E. Chromatin (1988), Springer-Verlag, New York
50. Wilhelm F.X., Wilhelm M.L., Erard M., and Daune M.P. Reconstitution of chromatin: assembly of the nucleosome. Nucleic Acids Res. 5 (1978) 505-521
51. Wilson E.B., Decius J.C., and Cross P.C. Molecular Vibrations: The Theory of Infrared and Raman Vibrational Spectroscopy (1955), Dover Publications Inc., New York
52. Wriggers W., and Schulten K. Protein domain movements: detection of rigid domains and visualization of effective rotations in comparisons of atomic coordinates. Proteins 29 (1997) 1-14
53. Yodh J.G., Woodbury N., Shlyakhtenko L.S., Lyubchenko Y.L., and Lohr D. Mapping nucleosome locations on the 208-12 by AFM provides clear evidence for cooperativity in array occupation. Biochemistry 41 (2002) 3565-3574