Nucleosome repositioning via loop formation.

Active (catalyzed) and passive (intrinsic) nucleosome repositioning is known to be a crucial event during the transcriptional activation of certain eukaryotic genes. Here we consider theoretically the intrinsic mechanism and study in detail the energetics and dynamics of DNA-loop-mediated nucleosome repositioning, as previously proposed by earlier works. The surprising outcome of the present study is the inherent nonlocality of nucleosome motion within this model-being a direct physical consequence of the loop mechanism. On long enough DNA templates the longer jumps dominate over the previously predicted local motion, a fact that contrasts simple diffusive mechanisms considered before. The possible experimental outcome resulting from the considered mechanism is predicted, discussed, and compared to existing experimental findings.

[1]  CONFORMATIONS OF LINEAR DNA , 1996, cond-mat/9610126.

[2]  C. Benham.  An elastic model of the large‐scale structure of duplex DNA , 1979, Biopolymers.

[3]  Igor M. Sokolov,et al.  PARADOXAL DIFFUSION IN CHEMICAL SPACE FOR NEAREST-NEIGHBOR WALKS OVER POLYMER CHAINS , 1997 .

[4]  Organized condensation of worm-like chains , 1999, cond-mat/9905289.

[5]  Milton Abramowitz,et al.  Handbook of Mathematical Functions with Formulas, Graphs, and Mathematical Tables , 1964 .

[6]  C. Bustamante,et al.  Evidence of DNA bending in transcription complexes imaged by scanning force microscopy. , 1993, Science.

[7]  M. L. Bret.  Catastrophic variation of twist and writhing of circular DNAs with constraint , 1979 .

[8]  Hiromi Yamakawa,et al.  Statistical Mechanics of Wormlike Chains , 1976 .

[9]  Hiromi Yamakawa,et al.  Helical Wormlike Chains in Polymer Solutions , 1997 .

[10]  B. Fain,et al.  Conformations of closed DNA. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[11]  J. Hearst,et al.  The Kirchhoff elastic rod, the nonlinear Schrödinger equation, and DNA supercoiling , 1994 .

[12]  Alain Goriely,et al.  Towards a classification of Euler–Kirchhoff filaments , 1999 .

[13]  P. Hagerman.  Flexibility of DNA. , 1988, Annual review of biophysics and biophysical chemistry.

[14]  J. Widom,et al.  Polymer reptation and nucleosome repositioning. , 2001, Physical review letters.

[15]  J. Bouchaud,et al.  Anomalous diffusion in disordered media: Statistical mechanisms, models and physical applications , 1990 .

[16]  G. Längst,et al.  ISWI induces nucleosome sliding on nicked DNA. , 2001, Molecular cell.

[17]  E. M. Bradbury,et al.  Mobile nucleosomes‐‐a general behavior. , 1992, The EMBO journal.

[18]  G. J. Fleer,et al.  Polymers in Solution , 1998 .

[19]  C. Bustamante,et al.  Wrapping of DNA around the E.coli RNA polymerase open promoter complex , 1999, The EMBO journal.

[20]  Irene A. Stegun,et al.  Handbook of Mathematical Functions. , 1966 .

[21]  A. Travers.  Chromatin structure and dynamics , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[22]  B. D. Coleman,et al.  Elastic stability of DNA configurations. I. General theory. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[23]  C. Peterson.  ATP‐dependent chromatin remodeling: going mobile , 2000, FEBS letters.

[24]  M. Le Bret,et al.  Twist and writhing in short circular DNAs according to first‐order elasticity , 1984, Biopolymers.

[25]  Jerry L. Workman,et al.  ATP-Dependent Chromatin-Remodeling Complexes , 2000, Molecular and Cellular Biology.

[26]  P. Chambon,et al.  Rearrangement of chromatin structure induced by increasing ionic strength and temperature. , 1979, European journal of biochemistry.

[27]  G. Felsenfeld,et al.  Transcription through nucleosomes. , 2000, Biophysical chemistry.

[28]  J. Widom,et al.  Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. , 2000, Journal of molecular biology.

[29]  J. Langowski,et al.  Scanning force microscopy of Escherichia coli RNA polymerase.sigma54 holoenzyme complexes with DNA in buffer and in air. , 1998, Journal of molecular biology.

[30]  M. Le Bret.  Catastrophic variation of twist and writhing of circular DNAs with constraint? , 1979, Biopolymers.

[31]  Joseph Klafter,et al.  Non-Brownian transport in complex systems , 1993 .

[32]  S. Brenner,et al.  A physical method for deriving the electrostatic interaction between rod-like polyions at all mutual angles. , 1974, Biophysical journal.

[33]  A. G. Greenhill,et al.  Handbook of Mathematical Functions with Formulas, Graphs, , 1971 .

[34]  J. D. Cloizeaux,et al.  Polymers in solution , 1990 .

[35]  J. Workman,et al.  The SWI/SNF Complex Creates Loop Domains in DNA and Polynucleosome Arrays and Can Disrupt DNA-Histone Contacts within These Domains , 1999, Molecular and Cellular Biology.

[36]  C. Benham.  Elastic model of supercoiling. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[37]  David Swigon,et al.  THEORY OF THE INFLUENCE OF END CONDITIONS ON SELF-CONTACT IN DNA LOOPS , 1995 .

[38]  E. Bradbury,et al.  Mobility of positioned nucleosomes on 5 S rDNA. , 1991, Journal of molecular biology.

[39]  J. Widom.  Structure, dynamics, and function of chromatin in vitro. , 1998, Annual review of biophysics and biomolecular structure.

[40]  J. Widom,et al.  Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. , 1995, Journal of molecular biology.

[41]  B. D. Coleman,et al.  The elastic rod model for DNA and its application to the tertiary structure of DNA minicircles in mononucleosomes. , 1998, Biophysical journal.

[42]  P. Beard.  Mobility of histones on the chromosome of simian virus 40 , 1978, Cell.

[43]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[44]  B. D. Coleman,et al.  Elastic stability of DNA configurations. II. Supercoiled plasmids with self-contact. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[45]  R. Kornberg,et al.  Twenty-Five Years of the Nucleosome, Fundamental Particle of the Eukaryote Chromosome , 1999, Cell.