Flexible histone tails in a new mesoscopic oligonucleosome model

Biophysical Journal

Volumn 91, Issue 1, 2006, Pages 133-150

  Arya, Gaurav ^a   Zhang, Qing ^a,b   Schlick, Tamar ^a  

^a NEW YORK UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; OLIGONUCLEOTIDE; PROTEIN; SODIUM CHLORIDE;

ARTICLE; CHEMICAL MODEL; CHROMATIN STRUCTURE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DIFFUSION COEFFICIENT; DYNAMICS; ELECTRIC POTENTIAL; ELECTRICITY; GENE EXPRESSION; HYDRODYNAMICS; NUCLEOSOME; PROTEIN INTERACTION; PROTEIN STRUCTURE; SEDIMENTATION; SURFACE CHARGE;

EID: 33745738426     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.083006     Document Type: Article

References (64)

1. Felsenfeld, G., and M. Groudine. 2003. Controlling the double helix. Nature. 421:448-453.
2. Luger, K., A. W. Mader, R. K. Richmond, D. F. Sargent, and T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 389:251-260.
3. Davey, C. A., D. F. Sargent, K. Luger, A. W. Maeder, and T. J. Richmond. 2002. Solvent-mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319:1097-1113.
4. Richmond, T. J., and C. A. Davey. 2003. The structure of DNA in the nucleosome core. Nature. 423:145-150.
5. Widom, J., and A. Klug. 1985. Structure of the 300 Å chromatin filament: x-ray-diffraction from oriented samples. Cell. 43:207-213.
6. McGhee, J. D., J. M. Nickol, G. Felsenfeld, and D. C. Rau. 1983. Higher order structure of chromatin: orientation of nucleosomes within the 30 nm chromatin solenoid is independent of species and spacer length. Cell. 33:831-841.
7. Woodcock, C. L. F., L.-L. Y. Frado, and J. B. Rattner. 1984. The higher-order structure of chromatin: evidence for a helical ribbon arrangement. J. Cell Biol. 99:42-52.
8. Williams, S. P., and J. P. Langmore. 1991. Small-angle x-ray-scattering of chromatin: radius and mass per unit length depend on linker length. Biophys. J. 59:606-618.
9. Woodcock, C. L., S. A. Grigoryev, R. A. Horowitz, and N. Whitaker. 1993. A chromatin folding model that incorporates linker variability generates fibers resembling the native structures. Proc. Natl. Acad. Sci. USA. 90:9021-9025.
10. Bharath, M. M. S., N. R. Chandra, and M. R. S. Rao. 2003. Molecular modeling of the chromatosome particle. Nucleic Acids Res. 31:4264-4274.
11. Hizume, K., S. H. Yoshimura, and K. Takeyasu. 2005. Linker histone H1 per se can induce three-dimensional folding of chromatin fiber. Biochemistry. 44:12978-12989.
12. Tse, C., T. Sera, A. P. Wolffe, and J. C. Hansen. 1998. Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol. Cell. Biol. 18:4629-4638.
13. Wade, P. A., D. Pruss, and A. P. Wolffe. 1997. Histone acetylation: chromatin in action. Trends Bio. Sci. 22:128-132.
14. Davie, J. R. 2004. Histone modifications. In Chromatin Structure and Dynamics: State-of-the-Art. J. Zlatanova and S. H. Leuba, editors. Elsevier B. V., Amsterdam, The Netherlands. 205-240.
15. Ausió , J., and D. W. Abbott. 2004. The role of histone variability in chromatin stability and folding. In Chromatin Structure and Dynamics: State-of-the-Art. J. Zlatanova, and S. H. Leuba, editors. Elsevier B. V., Amsterdam, The Netherlands. 241-290.
16. Tse, C., and J. C. Hansen. 1997. Hybrid trypsinized nucleosomal arrays: identification of multiple functional roles of the H2A/H2B and H3/H4 N-termini in chromatin fiber compaction. Biochemistry. 36:11381-11388.
17. Mangenot, S., E. Raspaud, C. Tribet, L. Belloni, and F. Livolant. 2002. Interactions between isolated nucleosome core particles: a tail-bridging effect. Eur. Phys. J. E. 7:221-231.
18. Zheng, C., X. Lu, J. C. Hansen, and J. J. Hayes. 2005. Salt-dependent intra- and inter-nucleosomal interactions of the H3 tail domain in a model oligonucleosomal array. J. Biol. Chem. 280:33552-33557.
19. Gordon, F., K. Luger, and J. C. Hansen. 2005. The core histone N-terminal tail domains function independently and additively during salt-dependent oligomerization of nucleosomal arrays. J. Biol. Chem. 280:33701-33706.
20. Bednar, J., R. A. Horowitz, S. A. Grigoryev, L. M. Carruthers, J. C. Hansen, A. J. Kostner, and C. L. Woodcock. 1998. Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc. Natl. Acad. Sci. USA. 95:14173-14178.
21. Scheissel, H., W. M. Gelbart, and R. Bruinsma. 2001. DNA folding: structural and mechanical properties of the two-angle model for chromatin. Biophys. J. 80:1940-1956.
22. Katritch, V., C. Bustamante, and W. K. Olson. 2000. Pulling chromatin fibers: computer simulations of direct physical micromanipulations. J. Mol. Biol. 295:29-40.
23. Ben-Haim, E., A. Lesne, and J.-M. Victor. 2001. Chromatin: a tunable spring at work inside chromosomes. Phys. Rev. E. 64:051921.
24. Beard, D. A., and T. Schlick. 2001a. Computational modeling predicts the structure and dynamics of chromatin fiber. Structure. 9:105-114.
25. Beard, D. A., and T. Schlick. 2001b. Modeling salt-mediated electrostatics of macromolecules: the discrete surface charge optimization algorithm and its application to the nucleosome. Biophys. J. 58:106-115.
26. Wedemann, G., and J. Langowski. 2002. Computer simulation of the 30-nanometer chromatin fiber. Biophys. J. 82:2847-2859.
27. Zhang, Q., D. A. Beard, and T. Schlick. 2003. Constructing irregular surfaces to enclose macromolecular complexes for mesoscale modeling using the discrete surface charge optimization (DiSCO) algorithm. J. Comput. Chem. 24:2063-2074.
28. Langowski, J., and H. Schiessel. 2004. Theory and computational modeling of the 30 nm chromatin fiber. In Chromatin Structure and Dynamics: State-of-the-Art. J. Zlatanova and S. H. Leuba, editors. Elsevier B. V., Amsterdam, The Netherlands, 397-420.
29. Mergell, B., R. Everaers, and H. Schiessel. 2004. Nucleosome interactions in chromatin: fiber stiffening and hairpin formation. Phys. Rev. E. 70:011915.
30. Sun, J., Q. Zhang, and T. Schlick. 2005. Electrostatic mechanism of nucleosomal array folding revealed by computer simulation. Proc. Natl. Acad. Sci. USA. 102:8180-8185.
31. Allison, S. A., R. Austin, and M. Hogan. 1989. Bending and twisting dynamics of short linear DNAs: analysis of the triplet anistropy decay of a 209 base pair fragment by Brownian simulation. J. Chem. Phys. 90:3843-3854.
32. Schlick, T., and A. Fogelson. 1992. TNPACK - a truncated Newton minimization package for large-scale problems: I. Algorithm and usage. ACM Trans. Math. Softw. 18:46-70.
33. Schlick, T., and A. Fogelson. 1992. TNPACK - a truncated Newton minimization package for large-scale problems: II. Implementation examples. ACM Trans. Math. Softw. 18:71-111.
34. Xie, D. X., and T. Schlick. 1999. Efficient implementation of the truncated-Newton algorithm for large-scale chemistry applications. SIAM J. Optim. 10:132-154.
35. Gilson, M. K., K. A. Sharp, and B. H. Honig. 1988. Calculating the electrostatic potential of molecules in solution: method and error. J. Comput. Chem. 9:327-335.
36. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:327-332.
37. Sharp, K. A., and B. Honig. 1990. Calculating total electrostatic energies with the nonlinear Poisson Boltzmann equation. J. Phys. Chem. 94:7684-7692.
38. Connolly, M. L. 1983. Solvent-accessible surfaces of proteins and nucleic acids. Science. 221:709-713.
39. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:5179-5197.
40. Heath, P. J., J. A. Gebe, S. A. Allison, and J. M. Schurr. 1996. Comparison of analytical theory with Brownian dynamics simulations for small linear and circular DNA. Macromolecules. 29:3583-3596.
41. Stigter, D. 1977. Interactions of highly charged colloidal cylinders with applications to double-stranded DNA. Biopolymers. 16:1435-1448.
42. Zhang, Q. 2005. Mesoscopic, microscopic, and macroscopic modeling of protein/DNA complexes. PhD thesis. New York University, New York.
43. Levitt, M., and A. Warshel. 1975. Computer simulation of protein folding. Nature. 253:694-698.
44. Levitt, M. 1976. A simplified representation of protein conformations for rapid simulation of protein folding. J. Mol. Biol. 104:59-107.
45. McCammon, J. A., S. H. Northrup, M. Karplus, and R. M. Levy. 1980. Helix-coil transitions in a simple polypeptide model. Biopolymers. 19:2033-2045.
46. Weber, W., H. Demirdjian, R. D. Lins, J. M. Briggs, R. Ferreira, and J. A. McCammon. 1998. Brownian and essential dynamics studies of the HIV-1 integrase catalytic domain. J. Biomol. Struct. Dyn. 16:733-745.
47. Madura, J. D., J. M. Briggs, R. C. Wade, M. E. Davis, B. A. Luty, A. Ilin, J. Antosiewicz, M. K. Gilson, B. Bagheri, L. R. Scott, and J. A. McCammon. 1995. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian dynamics program. Comput. Phys. Commun. 91:57-95.
48. Iniesta, A., and J. G. de la Torre. 1990. A 2nd-order algorithm for the simulation of the Brownian dynamics of macromolecular models. J. Chem. Phys. 92:2015-2018.
49. Ermak, D. L., and J. A. McCammon. 1978. Brownian dynamics with hydrodynamic interactions. J. Chem. Phys. 69:1352-1360.
50. Dahlquist, G., and Å. Björk. 1974. Numerical Methods. Prentice Hall, Englewood Cliffs, NJ.
51. Beard, D. A., and T. Schlick. 2003. Unbiased rotational moves for rigid-body dynamics. Biophys. J. 85:2973-2976.
52. Jian, H., T. Schlick, and A. Vologodskii. 1998. Internal motion of supercoiled DNA: Brownian dynamics simulations of site juxtaposition. J. Mol. Biol. 284:287-296.
53. Rotne, J., and S. Prager. 1969. Variational treatment of hydrodynamic interaction in polymers. J. Chem. Phys. 50:4831-4837.
54. de la Torre, J. G., and V. A. Bloomfield. 1977. Hydrodynamic properties of macromolecular complexes. I. Translation. Biophys. J. 16:1747-1763.
55. Carrasco, B., J. G. de la Torre, and P. Zipper. 1999. Calculation of hydrodynamic properties of macromolecular bead models with overlapping spheres. Eur. Biophys. J. 28:510-515.
56. Bertin, A., A. Leforestier, D. Durand, and F. Livolant. 2004. Role of histone tails in the conformation and interactions of nucleosome core particles. Biochemistry. 43:4773-4780.
57. Yao, J., P. T. Lowary, and J. Widom. 1990. Direct detection of linker DNA bending in defined-length oligomers of chromatin. Proc. Natl. Acad. Sci. USA. 87:7603-7607.
58. Yao, J., P. T. Lowary, and J. Widom. 1991. Linker DNA bending induced by the core histones of chromatin. Biochemistry. 30:8408-8414.
59. Bednar, J., R. A. Horowitz, J. Dubochet, and C. L. Woodcock. 1995. Chromatin conformation and salt-induced compaction: three-dimensional structural information from cryoelectron microscopy. J. Cell Biol. 131:1365-1376.
60. Hansen, J. C., J. Ausio, V. H. Stanik, and K. E. van Holde. 1989. Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. Biochemistry. 28:9129-9136.
61. Kirkwood, J. G. 1954. The general theory of irreversible processes in solutions of macromolecules. J. Polym. Sci. [B]. 12:1-14.
62. Bloomfield, V., W. O. Dalton, and K. E. van Holde. 1967. Frictional coefficients of multisubunit structure. I. Theory. Biopolymers. 5:135-148.
63. Cui, Y., and C. Bustamante. 2000. Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc. Natl. Acad. Sci. USA. 97:127-132.
64. Grigoryev, S. A. 2004. Keeping fingers crossed: heterochromatin spreading through interdigitation of nucleosome arrays. FEBS Lett. 564:4-8.