DOI: 10.1073/pnas.0409059102. DNA twisting flexibility and the formation of sharply looped protein

DNA twisting flexibility and the formation of sharply looped protein–DNA complexes

10.1073/pnas.0409059102

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Gene-regulatory complexes often require that pairs of DNA-bound proteins interact by looping-out short (often ≈100-bp) stretches of DNA. The loops can vary in detailed length and sequence and, thus, in total helical twist, which radically alters their geometry. How this variability is accommodated structurally is not known. Here we show that the inherent twistability of 89- to 105-bp DNA circles exceeds theoretical expectation by up to 400-fold. These results can be explained only by greatly enhanced DNA flexibility, not by permanent bends. They invalidate the use of classic theories of flexibility for understanding sharp DNA looping but support predictions of two recent theories. Our findings imply an active role for DNA flexibility in loop formation and suggest that variability in the detailed helical twist of regulatory loops is accommodated naturally by the inherent twistability of the DNA.

Bibliography

Cloutier, T. E., & Widom, J. (2005). DNA twisting flexibility and the formation of sharply looped proteinâDNA complexes. Proceedings of the National Academy of Sciences, 102(10), 3645â3650.

Authors 2

T. E. Cloutier (first)
J. Widom (additional)

References 52 Referenced 181

10.1016/0092-8674(81)90001-5
10.1146/annurev.bi.61.070192.001215
10.1016/S0968-0004(00)89117-3
10.1016/S0022-2836(03)00764-2
10.1126/science.281.5373.60
10.1073/pnas.92.7.2989
10.1101/gad.5.5.820
10.1016/j.jmb.2004.08.070
10.1038/nature01595
10.1002/j.1460-2075.1995.tb00155.x
10.1002/j.1460-2075.1993.tb05674.x
10.1002/j.1460-2075.1989.tb08514.x
10.1006/jmbi.1993.1133
10.1006/jmbi.1996.0143
10.1073/pnas.86.2.476
10.1101/gad.1209404
10.1038/319121a0
10.1038/332856a0
10.1021/ma00134a028
10.1016/S0006-3495(03)74838-3
10.1016/0076-6879(92)12003-9
10.1006/jmbi.2001.5366
10.1073/pnas.78.8.4833
10.1146/annurev.bb.17.060188.001405
10.1016/0022-2836(90)90130-E
10.1016/0022-2836(90)90131-5
10.1021/ma971804a
10.1038/nature01810
10.1016/S0022-2836(83)80198-3
10.1016/S1097-2765(04)00210-2
10.1017/S0033583501003699
10.1103/PhysRevLett.93.108108
Wiggins P. A. Phillips R. & Nelson P. C. (2005) Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top. in press.
Chakrabarti B. & Levine A. J. (2004) e-Print Archive http://xxx.lanl.gov cond-mat/0411358 v1.
Popov Y. O. & Tkachenko A. V. (2004) e-Print Archive http://xxx.lanl.gov cond-mat/0410591 v1.
10.1016/S0076-6879(95)61018-9
10.1073/pnas.85.19.7231
10.1007/978-3-642-77356-3_1
10.1038/255530a0
10.1038/368163a0
10.1093/nar/23.19.3962
10.1038/386563a0
10.1006/jmbi.1996.0687
10.1016/0022-2836(87)90513-4
10.1016/0092-8674(86)90833-0
10.1006/jmbi.1999.3171
10.1016/j.cell.2004.11.030
10.1021/ma991781v
10.1006/jmbi.2000.3921
10.1073/pnas.98.2.427
10.1038/73317
10.1073/pnas.95.19.11163

Dates

Type	When
Created	20 years, 6 months ago (Feb. 17, 2005, 8:23 p.m.)
Deposited	3 years, 4 months ago (April 25, 2022, 10:48 p.m.)
Indexed	11 months, 3 weeks ago (Aug. 29, 2024, 3:43 a.m.)
Issued	20 years, 6 months ago (Feb. 17, 2005)
Published	20 years, 6 months ago (Feb. 17, 2005)
Published Online	20 years, 6 months ago (Feb. 17, 2005)
Published Print	20 years, 5 months ago (March 8, 2005)

Funders 0

None

BibTeX

@article{Cloutier_2005, title={DNA twisting flexibility and the formation of sharply looped protein–DNA complexes}, volume={102}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0409059102}, DOI={10.1073/pnas.0409059102}, number={10}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Cloutier, T. E. and Widom, J.}, year={2005}, month=feb, pages={3645–3650} }

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