Nucleosome mobility and the maintenance of nucleosome positioning

Science

Volumn 276, Issue 5313, 1997, Pages 809-812

  Pazin, Michael J ^a   Bhargava, Purnima ^a,b   Geiduschek, E Peter ^a   Kadonaga, James T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA BINDING PROTEIN;

ARTICLE; CHROMATIN; CONTROLLED STUDY; LACTOSE OPERON; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

ADENOSINE TRIPHOSPHATE; APYRASE; BINDING SITES; CHROMATIN; DNA; DNA-BINDING PROTEINS; ISOPROPYL THIOGALACTOSIDE; NUCLEOSOMES; OPERATOR REGIONS (GENETICS); REPRESSOR PROTEINS;

EID: 0030964249     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5313.809     Document Type: Article

References (51)

1. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
2. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
3. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
4. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
5. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
6. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
7. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
8. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
9. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
10. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
11. K. E. van Holde, Chromatin (Springer-Verlag, New York, 1989); R. T. Simpson, Prog. Nucleic Acid Res. Mol. Biol. 40, 143 (1991); M. Grunstein, Sci. Am. 267, 68 (October 1992); J. Svaren and W. Hörz, Curr. Opin. Genet. Dev. 3, 219 (1993); G. L. Hager et al., Cold Spring Harbor Symp. Quant. Biol. 58, 63 (1993); J. L. Workman and A. R. Buchman, Trends Biochem. Sci. 18, 90 (1993); S. M. Paranjape, R. T. Kamakaka, J. T. Kadonaga, Annu. Rev. Biochem. 63, 265 (1994); A. P. Wolffe, Chromatin: Structure and Function (Academic Press, San Diego, CA, ed. 2, 1995); R. D. Kornberg and Y. Lorch, Curr. Opin. Cell Biol. 7, 371 (1995); S. C. R. Elgin, Ed., Chromatin Structure and Gene Expression (Oxford Univ. Press, Oxford, 1995); G. Felsenfeld, Cell 86, 13 (1996).
12. In this work, we examine translational positioning of nucleosomes. Although DNA sequence and structure, such as that of tandemly repeated sequences, can influence nucleosome positioning (1), we did not use tandem repeats in this work.
13. S. Y. Roth, A. Dean, R. T. Simpson, Mol. Cell. Biol. 10, 2247 (1990) S. Y. Roth, M. Shimizu, L. Johnson, M. Grunstein, R. T. Simpson, Genes Dev. 6, 411 (1992).
14. S. Y. Roth, A. Dean, R. T. Simpson, Mol. Cell. Biol. 10, 2247 (1990) S. Y. Roth, M. Shimizu, L. Johnson, M. Grunstein, R. T. Simpson, Genes Dev. 6, 411 (1992).
15. M. Shimizu, S. Y. Roth, C. Szent-Györgyi, R. T. Simpson, EMBO J. 10, 3033 (1991).
16. M. J. Fedor, N. F. Lue, R. D. Komberg, J. Mol. Biol. 204 109 (1988); M. J. Fedor and R. D. Kornberg, Mol. Cell. Biol. 9, 1721 (1989); D. I. Chasman et al., Genes Dev. 4, 503 (1990).
17. M. J. Fedor, N. F. Lue, R. D. Komberg, J. Mol. Biol. 204 109 (1988); M. J. Fedor and R. D. Kornberg, Mol. Cell. Biol. 9, 1721 (1989); D. I. Chasman et al., Genes Dev. 4, 503 (1990).
18. M. J. Fedor, N. F. Lue, R. D. Komberg, J. Mol. Biol. 204 109 (1988); M. J. Fedor and R. D. Kornberg, Mol. Cell. Biol. 9, 1721 (1989); D. I. Chasman et al., Genes Dev. 4, 503 (1990).
19. T. Tsukiyama, P. B. Becker, C. Wu, Nature 367, 525 (1994).
20. G. Wall, P. D. Varga-Weisz, R. Sandaltzopoulos, P. B. Becker, EMBO J. 14, 1727 (1995).
21. J. A. Armstrong and B. M. Emerson, Mol. Cell. Biol. 16, 5634 (1996).
22. M. J. Pazin, R. T. Kamakaka, J. T. Kadonaga, Science 266, 2007 (1994).
23. M. J. Pazin et al., Genes Dev. 10, 37 (1996).
24. S. Alberti, S. Oehler, B. von Wilcken-Bergmann, B. Müller-Hill, EMBO J. 12, 3227 (1993); J. Chen, S. Alberti, K. S. Matthews, J. Biol. Chem. 269, 12482 (1994).
25. S. Alberti, S. Oehler, B. von Wilcken-Bergmann, B. Müller-Hill, EMBO J. 12, 3227 (1993); J. Chen, S. Alberti, K. S. Matthews, J. Biol. Chem. 269, 12482 (1994).
26. The DNA sequence of this plasmid is available upon request. The 183-bp DNA interval was used to represent approximately one nucleosomal repeat.
27. R. T. Kamakaka, M. Bulger, J. T. Kadonaga, Genes Dev. 7, 1779 (1993); M. Bulger and J. T. Kadonaga, Methods Mol. Genet. 5, 241 (1994).
28. R. T. Kamakaka, M. Bulger, J. T. Kadonaga, Genes Dev. 7, 1779 (1993); M. Bulger and J. T. Kadonaga, Methods Mol. Genet. 5, 241 (1994).
29. T. Tsukiyama and C. Wu, Cell 83, 1011 (1995); T. Tsukiyama, C. Daniel, J. Tamkun, C. Wu, ibid., p. 1021.
30. T. Tsukiyama and C. Wu, Cell 83, 1011 (1995); T. Tsukiyama, C. Daniel, J. Tamkun, C. Wu, ibid., p. 1021.
31. P. D. Varga-Weisz, T. A. Blank, P. B. Becker, EMBO J. 14, 2209 (1995).
32. C. Wu, Nature 286, 854 (1980); S. A. Nedospasov and G. P. Georgiev, Biochem. Biophys. Res. Commun. 92, 532 (1980).
33. C. Wu, Nature 286, 854 (1980); S. A. Nedospasov and G. P. Georgiev, Biochem. Biophys. Res. Commun. 92, 532 (1980).
34. The inclusion of R3 protein, IPTG, or apyrase (or all three) did not affect the quality of the chromatin, as determined by micrococcal nuclease digestion analysis (Fig. 3) and by DNA supercoiling analysis (26). In this work, each experimental condition was explored at least twice but more commonly several times, to ensure reproducibility of the data.
35. M. C.-T. Hu and N. Davidson, Cell 48, 555 (1987); M. Brown et al., ibid. 49, 603 (1987); M. Gossen, A. L. Bonin, H. Bujard, Trends Biochem. Sci. 18, 471 (1993).
36. M. C.-T. Hu and N. Davidson, Cell 48, 555 (1987); M. Brown et al., ibid. 49, 603 (1987); M. Gossen, A. L. Bonin, H. Bujard, Trends Biochem. Sci. 18, 471 (1993).
37. M. C.-T. Hu and N. Davidson, Cell 48, 555 (1987); M. Brown et al., ibid. 49, 603 (1987); M. Gossen, A. L. Bonin, H. Bujard, Trends Biochem. Sci. 18, 471 (1993).
38. We did not observe the 10-bp repeating DNase I digestion pattern (1) that is generated with rotationally positioned nucleosomes. Hence, there is no evidence suggesting that the chromatin contains rotationally positioned nucleosomes.
39. C. L. Peterson and J. W. Tamkun, Trends Biochem. Sci. 20, 143 (1995); R. E. Kingston, C. A. Bunker, A. N. Imbalzano, Genes Dev. 10, 905 (1996); T. Krude and S. C. R. Elgin, Curr. Biol. 6, 511 (1996).
40. C. L. Peterson and J. W. Tamkun, Trends Biochem. Sci. 20, 143 (1995); R. E. Kingston, C. A. Bunker, A. N. Imbalzano, Genes Dev. 10, 905 (1996); T. Krude and S. C. R. Elgin, Curr. Biol. 6, 511 (1996).
41. C. L. Peterson and J. W. Tamkun, Trends Biochem. Sci. 20, 143 (1995); R. E. Kingston, C. A. Bunker, A. N. Imbalzano, Genes Dev. 10, 905 (1996); T. Krude and S. C. R. Elgin, Curr. Biol. 6, 511 (1996).
42. P. Beard, Cell 15, 955 (1978); C. Spadafora, P. Oudet, P. Chambon, Eur. J. Biochem. 100, 225 (1979).
43. P. Beard, Cell 15, 955 (1978); C. Spadafora, P. Oudet, P. Chambon, Eur. J. Biochem. 100, 225 (1979).
44. For primer extension footprinting, micrococcal nuclease is more effective than DNase I for the detection of a nucleosome footprint [see, for example, (4)], whereas DNase I is the preferred reagent for detecting sequence-specific DNA-bound factors, such as R3 (compare, for example, Figs. 1B and 2).
45. With other factors and in different contexts, an activation region might be required for binding to the chromatin template, especially in cases of cooperative binding of transcription factors with other proteins that is mediated through interactions with the transcriptional activation domain. In addition, we do not imply that all sequence-specific DNA binding proteins (either prokaryotic or eukaryotic) must necessarily alter chromatin structure.
46. S. N. Ho, S. R. Biggar, D. M. Spencer, S. L. Schreiber, G. R. Crabtree, Nature 382, 822 (1996).
47. A. Reik, G. Schütz, A. F. Stewart, EMBO J. 10, 2569 (1991); A. Schmid, K.-D. Fascher, W. Hörz, Cell 71, 853 (1992); E. Verdin, P. Paras Jr., C. Van Lint, EMBO J. 12, 3249 (1993).
48. A. Reik, G. Schütz, A. F. Stewart, EMBO J. 10, 2569 (1991); A. Schmid, K.-D. Fascher, W. Hörz, Cell 71, 853 (1992); E. Verdin, P. Paras Jr., C. Van Lint, EMBO J. 12, 3249 (1993).
49. A. Reik, G. Schütz, A. F. Stewart, EMBO J. 10, 2569 (1991); A. Schmid, K.-D. Fascher, W. Hörz, Cell 71, 853 (1992); E. Verdin, P. Paras Jr., C. Van Lint, EMBO J. 12, 3249 (1993).
50. P. Bhargava, M. J. Pazin, E. P. Geiduschek, J. T. Kadonaga, unpublished data.
51. We thank J. Newport, A. Wurster, J. Tyler, T. Burke, K. Robinson, M. Levenstein, L. DeVito, and A. Kutach for critical reading of the manuscript; K. Matthews (Rice University) for the generous gift of R3 protein; and M. Ouhammouch (University of California San Diego) for further purification of R3. P.B. held an Overseas Fellowship from the Department of Biotechnology, Government of India. J.T.K. is a Presidential Faculty Fellow. This work was supported by grants to J.T.K. from NSF and the Council for Tobacco Research USA, and to J.T.K and E.P.G. from the National Institute of General Medical Sciences.