Force-driven unbinding of proteins HU and Fis from DNA quantified using a thermodynamic Maxwell relation

Nucleic Acids Research

Volumn 39, Issue 13, 2011, Pages 5568-5577

  Xiao, Botao ^a,b   Zhang, Houyin ^a   Johnson, Reid C ^c,d   Marko, John F ^a,b  

^a Department of Physics and Astronomy ^*  (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CURVED DNA; DNA; FACTOR FOR INVERSION STIMULATION; HU PROTEIN;

ARTICLE; BINDING AND RELATED PHENOMENA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA BINDING; ESCHERICHIA COLI; GENE CONTROL; MATHEMATICAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN UNBINDING; QUANTITATIVE ANALYSIS; STATISTICAL MODEL; THERMODYNAMICS;

DNA; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; MODELS, STATISTICAL; PROTEIN BINDING; THERMODYNAMICS;

BACTERIA (MICROORGANISMS);

EID: 80052258137     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr141     Document Type: Article

References (67)

1. Bustamante, C., Bryant, Z. and Smith, S.B. (2003) Ten years of tension: single-molecule DNA mechanics. Nature, 421, 423-427. (Pubitemid 36157948)
2. Woldringh, C.L. (2002) The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol. Microbiol., 45, 17-29. (Pubitemid 35025930)
3. Yin, H., Wang, M.D., Svoboda, K., Landick, R., Block, S.M. and Gelles, J. (1995) Transcription against an applied force. Science, 270, 1653-1657. (Pubitemid 26002439)
4. Stano, N.M., Jeong, Y.J., Donmez, I., Tummalapalli, P., Levin, M.K. and Patel, S.S. (2005) DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase. Nature, 435, 370-373. (Pubitemid 40745548)
5. Wuite, G.J., Smith, S.B., Young, M., Keller, D. and Bustamante, C. (2000) Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature, 404, 103-106. (Pubitemid 30143142)
6. Kowalczykowski, S.C. (2008) Structural biology: snapshots of DNA repair. Nature, 453, 463-466. (Pubitemid 351733308)
7. Dillingham, M.S. and Kowalczykowski, S.C. (2008) RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev., 72, 642-671.
8. Zhang, H. and Marko, J.F. (2008) Maxwell relations for single-DNA experiments: Monitoring protein binding and double-helix torque with force-extension measurements. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 77, 031916.
9. Yan, J. and Marko, J.F. (2003) Effects of DNA-distorting proteins on DNA elastic response. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 68, 011905.
10. Marko, J.F. and Siggia, E.D. (1997) Driving proteins off DNA using applied tension. Biophys. J., 73, 2173-2178. (Pubitemid 27425748)
11. Skoko, D., Wong, B., Johnson, R.C. and Marko, J.F. (2004) Micromechanical analysis of the binding of DNA-bending proteins HMGB1, NHP6A, and HU reveals their ability to form highly stable DNA-protein complexes. Biochemistry, 43, 13867-13874. (Pubitemid 39431070)
12. van Noort, J., Verbrugge, S., Goosen, N., Dekker, C. and Dame, R.T. (2004) Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc. Natl Acad. Sci. USA, 101, 6969-6974. (Pubitemid 38596427)
13. Xiao, B., Johnson, R.C. and Marko, J.F. (2010) Modulation of HU-DNA interactions by salt concentration and applied force. Nucleic Acids Res., 38, 6176-6185.
14. Schnurr, B., Vorgias, C. and Stavans, J. (2006) Compaction and supercoiling of single, long DNA molecules by HU protein. Biophys. Rev. Lett., 1, 29-44.
15. Skoko, D., Yoo, D., Bai, H., Schnurr, B., Yan, J., McLeod, S.M., Marko, J.F. and Johnson, R.C. (2006) Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J. Mol. Biol., 364, 777-798. (Pubitemid 44737831)
16. Skoko, D., Yan, J., Johnson, R.C. and Marko, J.F. (2005) Low-force DNA condensation and discontinuous high-force decondensation reveal a loop-stabilizing function of the protein Fis. Phys. Rev. Lett., 95, 208101.
17. Ali, B.M., Amit, R., Braslavsky, I., Oppenheim, A.B., Gileadi, O. and Stavans, J. (2001) Compaction of single DNA molecules induced by binding of integration host factor (IHF). Proc. Natl Acad. Sci. USA, 98, 10658-10663. (Pubitemid 32878677)
18. Sugimura, S. and Crothers, D.M. (2006) Stepwise binding and bending of DNA by Escherichia coli integration host factor. Proc. Natl Acad. Sci. USA, 103, 18510-18514. (Pubitemid 44913441)
19. Liu, Y., Chen, H., Kenney, L.J. and Yan, J. (2010) A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev., 24, 339-344.
20. Amit, R., Oppenheim, A.B. and Stavans, J. (2003) Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys. J., 84, 2467-2473. (Pubitemid 36373568)
21. Stavans, J. and Oppenheim, A. (2006) DNA-protein interactions and bacterial chromosome architecture. Phys. Biol., 3, R1-10.
22. Dame, R.T., Noom, M.C. and Wuite, G.J. (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature, 444, 387-390. (Pubitemid 44764116)
23. Dame, R.T., Wyman, C. and Goosen, N. (2000) H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res., 28, 3504-3510.
24. Reck-Peterson, S.L., Derr, N.D. and Stuurman, N. (2010) Imaging single molecules using total internal reflection fluorescence microscopy (TIRFM). Cold Spring Harb. Protoc., 2010, pdb top73.
25. Doyle, P.S., Ladoux, B. and Viovy, J.L. (2000) Dynamics of a tethered polymer in shear flow. Phys. Rev. Lett., 84, 4769-4772.
26. Swinger, K.K. and Rice, P.A. (2007) Structure-based analysis of HU-DNA binding. J. Mol. Biol., 365, 1005-1016. (Pubitemid 46014175)
27. Hodges-Garcia, Y., Hagerman, P.J. and Pettijohn, D.E. (1989) DNA ring closure mediated by protein HU. J. Biol. Chem., 264, 14621-14623.
28. Grove, A. (2010) Functional evolution of bacterial histone-like HU proteins. Curr. Issues Mol. Biol., 13, 1-12.
29. Oberto, J., Nabti, S., Jooste, V., Mignot, H. and Rouviere-Yaniv, J. (2009) The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLoS One, 4, e4367.
30. Johnson, R.C., Johnson, L.M., Schmidt, J.W. and Gardner, J.F. (2005) In Higgins, N.P. (ed.), The Bacterial Chromosome. ASM Press, Washington DC, pp. 65-132.
31. Kamashev, D., Balandina, A. and Rouviere-Yaniv, J. (1999) The binding motif recognized by HU on both nicked and cruciform DNA. EMBO J., 18, 5434-5444. (Pubitemid 29465592)
32. Lavoie, B.D., Shaw, G.S., Millner, A. and Chaconas, G. (1996) Anatomy of a flexer-DNA complex inside a higher-order transposition intermediate. Cell, 85, 761-771. (Pubitemid 26181054)
33. Sagi, D., Friedman, N., Vorgias, C., Oppenheim, A.B. and Stavans, J. (2004) Modulation of DNA conformations through the formation of alternative high-order HU-DNA complexes. J. Mol. Biol., 341, 419-428. (Pubitemid 38987779)
34. Swinger, K.K., Lemberg, K.M., Zhang, Y. and Rice, P.A. (2003) Flexible DNA bending in HU-DNA cocrystal structures. EMBO J., 22, 3749-3760. (Pubitemid 36898351)
35. Wojtuszewski, K. and Mukerji, I. (2003) HU binding to bent DNA: a fluorescence resonance energy transfer and anisotropy study. Biochemistry, 42, 3096-3104. (Pubitemid 36331555)
36. Paull, T.T., Haykinson, M.J. and Johnson, R.C. (1994) HU and functional analogs in eukaryotes promote Hin invertasome assembly. Biochimie, 76, 992-1004.
37. Azam, T.A., Iwata, A., Nishimura, A., Ueda, S. and Ishihama, A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol., 181, 6361-6370. (Pubitemid 29512946)
38. Dixon, N.E. and Kornberg, A. (1984) Protein HU in the enzymatic replication of the chromosomal origin of Escherichia coli. Proc. Natl Acad. Sci. USA, 81, 424-428. (Pubitemid 14185742)
39. Wojtuszewski, K., Hawkins, M.E., Cole, J.L. and Mukerji, I. (2001) HU binding to DNA: evidence for multiple complex formation and DNA bending. Biochemistry, 40, 2588-2598. (Pubitemid 32171734)
40. Koh, J., Saecker, R.M. and Record, M.T. Jr (2008) DNA binding mode transitions of Escherichia coli HU (alphabeta): evidence for formation of a bent DNA-protein complex on intact, linear duplex DNA. J. Mol. Biol., 383, 324-346.
41. Pinson, V., Takahashi, M. and Rouviere-Yaniv, J. (1999) Differential binding of the Escherichia coli HU, homodimeric forms and heterodimeric form to linear, gapped and cruciform DNA. J. Mol. Biol., 287, 485-497. (Pubitemid 29168428)
42. Bonnefoy, E., Takahashi, M. and Rouviere-Yaniv, J. (1994) DNA-binding parameters of the HU protein of Escherichia coli to cruciform DNA. J. Mol. Biol., 242, 116-129. (Pubitemid 24298527)
43. Pan, C.Q., Finkel, S.E., Cramton, S.E., Feng, J.A., Sigman, D.S. and Johnson, R.C. (1996) Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. J. Mol. Biol., 264, 675-695. (Pubitemid 27013553)
44. Perkins-Balding, D., Dias, D.P. and Glasgow, A.C. (1997) Location, degree, and direction of DNA bending associated with the Hin recombinational enhancer sequence and Fis-enhancer complex. J. Bacteriol., 179, 4747-4753. (Pubitemid 27339719)
45. Thompson, J.F. and Landy, A. (1988) Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes. Nucleic Acids Res., 16, 9687-9705.
46. Stella, S., Cascio, D. and Johnson, R.C. (2010) The shape of the DNA minor groove directs binding by the DNA-bending protein Fis. Genes Dev., 24, 814-826.
47. Dorman, C.J. and Deighan, P. (2003) Regulation of gene expression by histone-like proteins in bacteria. Curr. Opin. Genet. Dev., 13, 179-184. (Pubitemid 36369742)
48. Shao, Y., Feldman-Cohen, L.S. and Osuna, R. (2008) Functional characterization of the Escherichia coli Fis-DNA binding sequence. J. Mol. Biol., 376, 771-785.
49. Finkel, S.E. and Johnson, R.C. (1992) The Fis protein: it's not just for DNA inversion anymore. Mol. Microbiol., 6, 3257-3265.
50. Smith, S.B., Finzi, L. and Bustamante, C. (1992) Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science, 258, 1122-1126.
51. Strick, T.R., Allemand, J.F., Bensimon, D. and Croquette, V. (1998) Behavior of supercoiled DNA. Biophys. J., 74, 2016-2028. (Pubitemid 28157936)
52. Skoko, D., Li, M., Huang, Y., Mizuuchi, M., Cai, M., Bradley, C.M., Pease, P.J., Xiao, B., Marko, J.F., Craigie, R. et al. (2009) Barrier-to-autointegration factor (BAF) condenses DNA by looping. Proc. Natl Acad. Sci. USA, 106, 16610-16615.
53. Yan, J., Maresca, T.J., Skoko, D., Adams, C.D., Xiao, B., Christensen, M.O., Heald, R. and Marko, J.F. (2007) Micromanipulation studies of chromatin fibers in Xenopus egg extracts reveal ATP-dependent chromatin assembly dynamics. Mol. Biol. Cell, 18, 464-474. (Pubitemid 46213216)
54. Strick, T.R., Allemand, J.F., Bensimon, D., Bensimon, A. and Croquette, V. (1996) The elasticity of a single supercoiled DNA molecule. Science, 271, 1835-1837. (Pubitemid 26112307)
55. Marko, J.F. and Siggia, E.D. (1995) Stretching DNA. Macromolecules, 28, 8759-8770.
56. Yan, J., Kawamura, R. and Marko, J.F. (2005) Statistics of loop formation along double helix DNAs. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 71, 061905.
57. Zhang, H. and Marko, J.F. (2010) Intrinsic and force-generated cooperativity in a theory of DNA bending proteins. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 82, 051906.
58. Liebesny, P., Goyal, S., Dunlap, D., Family, F. and Finzi, L. (2010) Determination of the number of protein bound non-specifically to DNA. J. Phys. Condens. Matter, 22, 414104.
59. Vladescu, I.D., McCauley, M.J., Nunez, M.E., Rouzina, I. and Williams, M.C. (2007) Quantifying force-dependent and zero-force DNA intercalation by single-molecule stretching. Nat. Methods, 4, 517-522. (Pubitemid 46852078)
60. Hengen, P.N., Bartram, S.L., Stewart, L.E. and Schneider, T.D. (1997) Information analysis of Fis binding sites. Nucleic Acids Res., 25, 4994-5002. (Pubitemid 28022261)
61. Cho, B.K., Knight, E.M., Barrett, C.L. and Palsson, B.O. (2008) Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res., 18, 900-910. (Pubitemid 351793062)
62. Kahramanoglou, C., Seshasayee, A.S., Prieto, A.I., Ibberson, D., Schmidt, S., Zimmermann, J., Benes, V., Fraser, G.M. and Luscombe, N.M. (2010) Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res., Advance Access Published on 21 November 2010; doi: 10.1093/nar/gkq934.
63. dos Remedios, C.G., Chhabra, D., Kekic, M., Dedova, I.V., Tsubakihara, M., Berry, D.A. and Nosworthy, N.J. (2003) Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev., 83, 433-473. (Pubitemid 36378678)
64. Ferrer, J.M., Lee, H., Chen, J., Pelz, B., Nakamura, F., Kamm, R.D. and Lang, M.J. (2008) Measuring molecular rupture forces between single actin filaments and actin-binding proteins. Proc. Natl Acad. Sci. USA, 105, 9221-9226.
65. Doyle, A.D. and Yamada, K.M. (2010) Cell biology: sensing tension. Nature, 466, 192-193.
66. Geisler, M., Netz, R.R. and Hugel, T. (2010) Pulling a single polymer molecule off a substrate reveals the binding thermodynamics of cosolutes. Angew. Chem. Int. Ed. Engl., 49, 4730-4733.
67. Mosconi, F., Allemand, J.F., Bensimon, D. and Croquette, V. (2009) Measurement of the torque on a single stretched and twisted DNA using magnetic tweezers. Phys. Rev. Lett., 102, 078301.