Unexpected binding motifs for subnucleosomal particles revealed by atomic force microscopy

Biophysical Journal

Volumn 87, Issue 6, 2004, Pages 4135-4145

  Nikova, Dessy N ^a,c   Pope, Lisa H ^a,d   Bennink, Martin L ^a,b   Van Leijenhorst Groener, Kirsten A ^a   Van Der Werf, Kees ^a   Greve, Jan ^a  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

AIR; ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; DNA BINDING; LIQUID; NONHUMAN; NUCLEOSOME; PROTEIN MOTIF;

ANIMALIA;

EID: 10044275571     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.048983     Document Type: Article

References (47)

1. Alilat, M., A. Sivolob, B. Révet, and A. Prunell. 1999. Nucleosome dynamics. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA Particle. J. Mol. Biol. 291:815-841.
2. Allen, M. J., X. F. Dong, T. E. O'Neill, P. Yau, S. C. Kowalczykowski, J. Gatewood, R. Balhorn, and E. M. Bradbury. 1993. Atomic force microscope measurements of nucleosome cores assembled along defined DNA sequences. Biochemistry. 32:8390-8396.
3. Becker, P. B., and W. Horz. 2002. ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71:247-273.
4. Bennink, M., D. Nikova, K. van der Werf, and J. Greve. 2003. Dynamic imaging of single DNA-protein interactions using atomic force microscopy. Anal. Chim. Acta. 479:3-15.
5. Brower-Toland, B. D., C. L. Smith, R. C. Yeh, J. T. Lis, C. L. Peterson, and M. D. Wang. 2002. Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. USA. 99:1960-1965.
6. 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.
7. d'Erme, M., G. Yang, E. Sheagly, F. Palitti, and C. Bustamante. 2001. Effect of poly(ADP-ribosyl)ation and Mg2+ ions on chromatin structure revealed by scanning force microscopy. Biochemistry. 40:10947-10955.
8. Dong, F., and K. E. van Holde. 1991. Nucleosome positioning is determined by the (H3-H4)2 tetramer. PTOC. Natl. Acad. Sci. USA. 88: 10596-10600.
9. Finch, J. T., and A. Klug. 1976. Solenoidal model for superstructure in chromatin. Proc. Natl. Acad. Sci. USA. 73:1897-1901.
10. Fletcher, T. M., P. Serwer, and J. C. Hansen. 1994. Quantitative analysis of macromolecular conformational changes using agarose gel electrophoresis: application to chromatin folding. Biochemistry. 33:10859-10863.
11. Garcia-Ramirez, M., F. Dong, and J. Ausio. 1992. Role of the histone "tails" in the folding of oligonucleosomes depleted of histone HI. J. Biol. Chem. 267:19587-19595.
12. Gottesfeld, J. M., and K. Luger. 2001. Energetics and affinity of the histone octamer for defined DNA sequences. Biochemistry. 40:10927-10933.
13. Hammermann, M., K. Toth, C. Rodemer, W. Waldeck, R. P. May, and J. Langowski. 2000. Salt-dependent compaction of di- and trinucleosomes studied by small-angle neutron scattering. Biophys. J. 79:584-594.
14. 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 HI. Biochemistry. 28:9129-9136.
15. Hansen, J. C., and A. P. Wolffe. 1994. A role for histones H2A/H2B in chromatin folding and transcriptional repression. Proc. Natl. Acad. Sci. USA. 91:2339-2343.
16. Horn, P. J., and C. L. Peterson. 2002. Molecular biology. Chromatin higher order folding-wrapping up transcription. Science. 297:1824-1827.
17. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science. 293:1074-1080.
18. Kireeva, M. L., W. Walter, V. Tchernajenko, V. Bondarenko, M. Kashlev, and V. M. Studitsky. 2002. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol. Cell. 9:541-552.
19. Kornberg, R. D. 1974. Chromatin structure: a repeating unit of histones and DNA. Science. 184:868-871.
20. Leuba, S. H., G. Yang, C. Robert, B. Samori, K. van Holde, J. Zlatanova, and C. Bustamante. 1994. Three-dimensional structure of extended chromatin fibers as revealed by tapping-mode scanning force microscopy. Proc. Natl. Acad. Sci. USA. 91:11621-11625.
21. Leuba, S. H., C. Bustamante, K. van Holde, and J. Zlatanova. 1998. Linker histone tails and N-tails of histone H3 are redundant: scanning force microscopy studies of reconstituted fibers. Biophys. J. 74:2830-2839.
22. 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 A resolution. Nature. 389:251-260.
23. Luger, K., and T. J. Richmond. 1998. DNA binding within the nucleosome core. Curr. Opin. Struct. Biol. 8:33-40.
24. Martin, L. D., J. P. Vesenka, E. Henderson, and D. L. Dobbs. 1995. Visualization of nucleosomal substructure in native chromatin by atomic force microscopy. Biochemistry. 34:4610-4616.
25. Moreno-Herrero, V., J. Colchero, and A. M. Baro. 2003. DNA height in scanning force microscopy. Ultramicroscopy. 96:167-174.
26. Polach, K. J., and J. Widom. 1995. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254:130-149.
27. Polach, K. J., and J. Widom. 1996. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 258:800-812.
28. Rossell, J. P., S. Allen, M. C. Davies, C. J. Roberts, S. J. B. Tendier, and P. M. Williams. 2003. Electrostatic interactions observed when imaging proteins with the atomic force microscope. Ultramicroscopy. 96:37-46.
29. Sato, M. H., K. Ura, K. I. Hohmura, F. Tokumasu, S. H. Yoshimura, F. Hanaoka, and K. Takeyasu. 1999. Atomic force microscopy sees nucleosome positioning and histone HI-induced compaction in reconstituted chromatin. FEBS Lett. 452:267-271.
30. Schnitzler, G. R., C. L. Cheung, J. H. Hafner, A. J. Saurin, R. E. Kingston, and C. M. Lieber. 2001. Direct imaging of human SWI/SNF-remodeled mono- and polynucleosomes by atomic force microscopy employing carbon nanotube tips. Mol. Cell. Biol. 21:8504-8511.
31. Schwarz, P. M., A. Felthauser, T. M. Fletcher, and J. C. Hansen. 1996. Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains. Biochemistry. 35:4009-4015.
32. Schwarz, P. M., and J. C. Hansen. 1994. Formation and stability of higher order chromatin structures. Contributions of the histone octamer. J. Biol. Chem. 269:16284-16289.
33. Sewell, B., C. Bouloukos, and C. von Holt. 1984. Formaldehyde and glutaraldehyde in the fixation of chromatin for electron microscopy. J. Microsc. 136:103-112.
34. Simon, R. H., and G. Felsenfeld. 1979. A new procedure for purifying histone pairs H2A + H2B and H3 + H4 from chromatin using hydroxylapatite. Nucleic Acids Res. 6:689-696.
35. Simpson, R. T., F. Thoma, and J. M. Brubaker. 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.
36. Smith, D. R., I. J. Jackson, and D. D. Brown. 1984. Domains of the positive transcription factor specific for the Xenopus 5S RNA gene. Cell. 37: 645-652.
37. Tomschik, M., M. A. Karymov, J. Zlatanova, and S. H. Leuba. 2001. The archaeal histone-fold protein HMf organizes DNA into bona fide chromatin fibers. Structure (Camb). 9:1201-1211.
38. van der Werf, K. O., C. Putman, B. G. de Grooth, F. Segerink, E. Schipper, N. F. van Hulst, and J. Greve. 1993. Compact stand-alone atomic force microscope. Rev. Sci. Instrum. 64:2892-2897.
39. van Holde, K., and J. Zlatanova. 1996. What determines the folding of the chromatin fiber? Proc. Natl. Acad. Sci. USA. 93:10548-10555.
40. van Holde, K. E. 1988. In Chromatin. A. Rich, editor. Springer, New York. 111-148.
41. van Noort, J., K. O. van der Werf, B. G. de Grooth, N. F. van Hulst, and J. Greve. 1997. Height anomalies in tapping mode atomic force microscopy in air caused by adhesion. Ultramicroscopy. 69:117-127.
42. Widom, J. 1998. Structure, dynamics, and function of chromatin in vitro. Annu. Rev. Biophys. Biomol. Struct. 27:285-327.
43. Wolffe, A. P. 1994. Transcription: in tune with the histones. Cell. 77: 13-16.
44. Woodcock, C. L., and S. Dimitrov. 2001. Higher-order structure of chromatin and chromosomes. Curr. Opin. Genet. Dev. 11:130-135.
45. Yodh, J. G., Y. L. Lyubchenko, L. S. Shlyakhtenko, N. Woodbury, and D. Lohr. 1999. Evidence for nonrandom behavior in 208-12 subsaturated nucleosomal array populations analyzed by AFM. Biochemistry. 38:15756-15763.
46. Yodh, J. G., N. Woodbury, L. S. Shlyakhtenko, Y. L. Lyubchenko, and D. Lohr. 2002. Mapping nucleosome locations on the 208-12 by AFM provides clear evidence for cooperativity in array occupation. Biochemistry. 41:3565-3574.
47. Zlatanova, J., S. H. Leuba, and K. van Holde. 1998. Chromatin fiber structure: morphology, molecular determinants, structural transitions. Biophys. J. 74:2554-2566.