Revealing transient structures of nucleosomes as DNA unwinds

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8767-8776

  Chen, Yujie ^a   Tokuda, Joshua M ^a   Topping, Traci ^b   Sutton, Julie L ^a   Meisburger, Steve P ^a   Pabit, Suzette A ^a   Gloss, Lisa M ^b   Pollack, Lois ^a  

^a School of Operations Research and Industrial Engineering   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE;

5S RIBOSOMAL GENE; ARTICLE; CELL KINETICS; CELLULAR PARAMETERS; CHEMICAL COMPOSITION; DNA CONFORMATION; DNA DENATURATION; DNA DETERMINATION; DNA PROTEIN COMPLEX; DNA TRANSFER; GENE; GENE CONTROL; NUCLEOSOME; NUCLEOSOME CORE PARTICLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SEA URCHIN; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; XENOPUS LAEVIS;

DNA; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; SCATTERING, SMALL ANGLE; SODIUM CHLORIDE; X-RAY DIFFRACTION;

EID: 84905590378     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku562     Document Type: Article

References (42)

1. Luger, K. and Phillips, S.E.V. Luger, K. and Phillips, S.E.V. (2010) Rise of the molecular machines. Curr. Opin. Struct. Biol., 20, 70-72.
2. Yager, T.D., McMurray, C.T., and van Holde, K.E. Yager, T.D., McMurray, C.T., and van Holde, K.E. (1989) Salt-induced release of DNA from nucleosome core particles. Biochemistry, 28, 2271-2281.
3. Killian, J.L., Li, M., Sheinin, M.Y., and Wang, M.D. Killian, J.L., Li, M., Sheinin, M.Y., and Wang, M.D. (2012) Recent advances in single molecule studies of nucleosomes. Curr. Opin. Struct. Biol., 22, 80-87.
4. Gansen, A., Valeri, A., Hauger, F., Felekyan, S., Kalinin, S., Tóth, K., Langowski, J., and Seidal, C.A. Gansen, A., Valeri, A., Hauger, F., Felekyan, S., Kalinin, S., Tóth, K., Langowski, J., and Seidal, C.A. (2009) Nucleosome disassembly intermediates characterized by single-molecule FRET. Proc. Natl. Acad. Sci. U.S.A., 106, 15308-15313.
5. Bohm, V., Hieb, A., Andrews, A.J., Gansen, A., Rocker, A., Tóth, K., Luger, K., and Langowski, J. Bohm, V., Hieb, A., Andrews, A.J., Gansen, A., Rocker, A., Tóth, K., Luger, K., and Langowski, J. (2011) Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res., 39, 3093-3102.
6. Hoch, D.A., Stratton, J.J., and Gloss, L.M. Hoch, D.A., Stratton, J.J., and Gloss, L.M. (2007) Protein-protein forster resonance energy transfer analysis of nucleosome core particles containing H2A and H2A. J. Mol. Biol., 371, 971-988.
7. Koopmans, W.J., Brehm, A., Logie, C., Schmidt, T., and van Noort, J. Koopmans, W.J., Brehm, A., Logie, C., Schmidt, T., and van Noort, J. (2007) Single-pair FRET microscopy reveals mononucleosome dynamics. J. Fluoresc., 17, 785-795.
8. Tomschik, M., van Holde, K., and Zlatanova, J. Tomschik, M., van Holde, K., and Zlatanova, J. (2009) Nucleosome dynamics as studied by single-pair fluorescence resonance energy transfer: a reevaluation. J. Fluoresc., 19, 53-62.
9. Zlatanova, J., Bishop, T.C., Victor, J.M., Jackson, V., and van Holde, K. Zlatanova, J., Bishop, T.C., Victor, J.M., Jackson, V., and van Holde, K. (2009) The nucleosome family: dynamic and growing. Structure, 17, 160-171.
10. Li, G., Levitus, M., Bustamante, C., and Widom, J. Li, G., Levitus, M., Bustamante, C., and Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol., 12, 46-53.
11. Tims, H.S., Gurunathan, K., Levitus, M., and Widom, J. Tims, H.S., Gurunathan, K., Levitus, M., and Widom, J. (2011) Dynamics of nucleosome invasion by DNA binding proteins. J. Mol. Biol., 411, 430-448.
12. Arimura, Y., Tachiwana, H., Oda, T., Sato, M., and Kurumizaka, H. Arimura, Y., Tachiwana, H., Oda, T., Sato, M., and Kurumizaka, H. (2012) Structural analysis of the hexasome, lacking one histone H2A/H2B dimer from the conventional nucleosome. Biochemistry, 51, 3302-3309.
13. Kireeva, M.L., Walter, W., Tchernajenko, V., Bondarenko, V., Kashlev, M., and Studitsky, V. Kireeva, M.L., Walter, W., Tchernajenko, V., Bondarenko, V., Kashlev, M., and Studitsky, V. (2002) Nucleosome remodeling induced by RNA Polymerase II. Loss of the H2A/H2B dimer during transcription. Mol. Cell, 9, 541-552.
14. Miyagi, A., Ando, T., and Lyubchenko, Y.L. Miyagi, A., Ando, T., and Lyubchenko, Y.L. (2011) Dynamics of nucleosomes assessed with time-lapse high-speed atomic force microscopy. Biochemistry, 50, 7901-7908.
15. Andrews, A.J. and Luger, K. Andrews, A.J. and Luger, K. (2011) A coupled equilibrium approach to study nucleosome thermodynamics. Methods Enzymol., 488, 265-285.
16. Andrews, A.J. and Luger, K. Andrews, A.J. and Luger, K. (2011) Nucleosome structure(s) and stability: variations on a theme. Annu. Rev. Biophys., 40, 99-117.
17. Park, Y.J., Dyer, P.N., Tremethick, D.J., and Luger, K. Park, Y.J., Dyer, P.N., Tremethick, D.J., and Luger, K. (2004) A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J. Biol. Chem., 279, 24274-24282.
18. Mazurkiewicz, J., Kepert, J.F., and Rippe, K. Mazurkiewicz, J., Kepert, J.F., and Rippe, K. (2006) On the mechanism of nucleosome assembly by histone chaperone NAP1. J. Biol. Chem., 281, 16462-16472.
19. Lowary, P.T. and Widom, J. Lowary, P.T. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol., 276, 19-42.
20. Simpson, R.T., Thoma, F., and Brubaker, J.M. Simpson, R.T., Thoma, F., and Brubaker, J.M. (1985) Chromatin reconstituted from tandemly repeated cloned DNA fragments and core histones: a model system for study of higher order structure. Cell, 42, 799-808.
21. Svergun, D.I. and Koch, M.H.J. Svergun, D.I. and Koch, M.H.J. (2003) Small-angle scattering studies of biological macromolecules in solution. Rep. Prog. Phys., 66, 1735-1782.
22. Yang, C., van der Woerd, M.J., Muthurajan, U.M., Hansen, J.C., and Luger, K. Yang, C., van derWoerd, M.J., Muthurajan, U.M., Hansen, J.C., and Luger, K. (2011) Biophysical analysis and small-angle X-ray scattering-derived structures of MeCP2-nucleosome complexes. Nucleic Acids Res., 39, 4122-4135.
23. Mangenot, S., Leforestier, A., Vachette, P., Durand, D., and Livolant, F. Mangenot, S., Leforestier, A., Vachette, P., Durand, D., and Livolant, F. (2002) Salt-induced conformation and interaction changes of nucleosome core particles. Biophys. J., 82, 345-356.
24. Bertin, A., Leforestier, A., Durand, D., and Livolant, F. Bertin, A., Leforestier, A., Durand, D., and Livolant, F. (2004) Role of histone tails in the conformation and interactions of nucleosome core particles. Biochemistry, 43, 4773-4780.
25. Bertin, A., Renouard, M., Pedersen, J.S., Livolant, F., and Durand, D. Bertin, A., Renouard, M., Pedersen, J.S., Livolant, F., and Durand, D. (2007) H3 and H4 histone tails play a central role in the interactions of recombinant NCPs. Biophys. J., 92, 2633-2645.
26. Bertin, A., Durand, D., Renouard, M., Livolant, F., and Mangenot, S. Bertin, A., Durand, D., Renouard, M., Livolant, F., and Mangenot, S. (2007) H2A and H2B tails are essential to properly reconstitute nucleosome core particles. Eur. Biophys. J., 36, 1083-1094.
27. Inoko, Y., Yamamoto, M., Fujiwara, S., and Ueki, T. Inoko, Y., Yamamoto, M., Fujiwara, S., and Ueki, T. (1992) X-ray-scattering study of the shape of the DNA region in nucleosome core particle with synchrotron radiation. J. Biochem. (Tokyo), 111, 310-316.
28. Svergun, D.I., Koch, M.H.J., and Serdyuk, I.N. Svergun, D.I., Koch, M.H.J., and Serdyuk, I.N. (1994) Structural model of the 50 S subunit of Escherichia coli ribosomes from solution scattering: I. X-ray synchrotron radiation study. J. Mol. Biol., 240, 66-77.
29. Dyer, P.N., Edayathumangalam, R.S., White, C.L., Bao, Y., Chakravarthy, S., Muthurajan, U.M., and Luger, K. Dyer, P.N., Edayathumangalam, R.S., White, C.L., Bao, Y., Chakravarthy, S., Muthurajan, U.M., and Luger, K. (2004) Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol., 375, 23-44.
30. Thastrom, A., Lowary, P.T., and Widom, J. Thastrom, A., Lowary, P.T., and Widom, J. (2004) Measurement of histone-DNA interaction free energy in nucleosomes. Methods, 33, 33-44.
31. Svergun, D.I. Svergun, D.I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr., 25, 495-503.
32. Russell, R., Millett, I.S., Tate, M.W., Kwok, L.W., Nakatani, B., Gruner, S.M., Mochrie, S.G.J., Pande, V., Doniach, S., Herschlag, D., and Pollack, L. Russell, R., Millett, I.S., Tate, M.W., Kwok, L.W., Nakatani, B., Gruner, S.M., Mochrie, S.G.J., Pande, V., Doniach, S., Herschlag, D., and Pollack, L. (2002) Rapid compaction during RNA folding. Proc. Natl. Acad. Sci. U.S.A., 99, 4266-4271.
33. Macke, T.J. and Case, D.A. Macke, T.J. and Case, D.A. (1998) Modeling unusual nucleic acid structures. ACS Symp. Ser., 682, 379-393.
34. Svergun, D., Barberato, C., and Koch, M.H.J. Svergun, D., Barberato, C., and Koch, M.H.J. (1995) CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr., 28, 768-773.
35. Howell, S.C., Andresen, K., Jimenez-Useche, I., Yuan, C., and Qiu, X. Howell, S.C., Andresen, K., Jimenez-Useche, I., Yuan, C., and Qiu, X. (2013) Elucidating internucleosome interactions and the roles of histone tails. Biophys. J., 105, 194-199.
36. Bernado, P., Mylonas, E., Petoukhov, M.V., Blackledge, M., and Svergun, D.I. Bernado, P., Mylonas, E., Petoukhov, M.V., Blackledge, M., and Svergun, D.I. (2007) Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc., 129, 5656-5664.
37. Chua, E.Y., Vasudevan, D., Davey, G.E., Wu, B., and Davey, C.A. Chua, E.Y., Vasudevan, D., Davey, G.E., Wu, B., and Davey, C.A. (2012) The mechanics behind DNA sequence-dependent properties of the nucleosome. Nucleic Acids Res., 40, 6338-6352.
38. Bao, Y., Konesky, K., Park, Y.J., Rosu, S., Dyer, P.N., Rangasamy, D., Tremethick, D.J., Laybourn, P.J., and Luger, K. Bao, Y., Konesky, K., Park, Y.J., Rosu, S., Dyer, P.N., Rangasamy, D., Tremethick, D.J., Laybourn, P.J., and Luger, K. (2004) Nucleosomes containing the histone variant H2A. Bbd organize only 118 base pairs of DNA. EMBO. J., 23, 3314-3324.
39. Chakravarthy, S., Gundimella, S.K., Caron, C., Perche, P.Y., Pehrson, J.R., Khochbin, S., and Luger, K. Chakravarthy, S., Gundimella, S.K., Caron, C., Perche, P.Y., Pehrson, J.R., Khochbin, S., and Luger, K. (2005) Structural characterization of the histone variant macroH2A. Mol. Cell. Biol., 25, 7616-7624.
40. Luger, K., Rechsteiner, T.J., Flaus, A.J., Waye, M.M.Y., and Richmond, T.J. Luger, K., Rechsteiner, T.J., Flaus, A.J., Waye, M.M.Y., and Richmond, T.J. (1997) Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol., 272, 301-311.
41. Gloss, L.M. and Placek, B.J. Gloss, L.M. and Placek, B.J. (2002) The effect of salts on the stability of the H2A-H2B histone dimer. Biochemistry, 41, 14951-14959.
42. Banks, D.D. and Gloss, L.M. Banks, D.D. and Gloss, L.M. (2003) Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer. Biochemistry, 42, 6827-6839.