Psoralen photocrosslinking, a tool to study the chromatin structure of RNA polymerase I - Transcribed ribosomal genes

Biochemistry and Cell Biology

Volumn 83, Issue 4, 2005, Pages 449-459

  Toussaint, Martin ^a   Levasseur, Geneviève ^a   Tremblay, Maxime ^a   Raquette, Michel ^a   Conconi, Antonio ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Active chromatin; FACT; Lexosome; Photo crosslinking; Psoralen; rDNA; RNA polymerase I

Indexed keywords

BIOCHEMISTRY; CROSSLINKING; DNA; GENES; PHOTOCHEMICAL REACTIONS; RNA;

ACTIVE CHROMATIN; FACT; LEXOSOME; PHOTO-CROSSLINKING; PSORALEN; RDNA; RNA POLYMERASE 1;

ENZYMES;

DNA DIRECTED RNA POLYMERASE; PSORALEN; RIBOSOME DNA; CROSS LINKING REAGENT; FUNGAL DNA; PHOTOSENSITIZING AGENT; TRIOXYSALEN;

CHROMATIN STRUCTURE; CONFERENCE PAPER; DNA REPLICATION; DNA STRUCTURE; DNA TRANSCRIPTION; EUKARYOTE; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOSOME; PLANT; RIBOSOME; SACCHAROMYCES CEREVISIAE; CHEMISTRY; CHROMATIN; DNA REPAIR; FUNGAL GENE; GENETICS; METABOLISM; RADIATION EXPOSURE; REVIEW; ULTRAVIOLET RADIATION;

ANIMALIA; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

CHROMATIN; CROSS-LINKING REAGENTS; DNA REPAIR; DNA, FUNGAL; DNA, RIBOSOMAL; GENES, FUNGAL; PHOTOSENSITIZING AGENTS; RNA POLYMERASE I; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC; TRIOXSALEN; ULTRAVIOLET RAYS;

EID: 27644597191     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-141     Document Type: Conference Paper

References (124)

1. Allfrey, V.G., and Chen, T.A. 1991. Nucleosomes of transcriptionally active chromatin: isolation of template-active nucleosomes by affinity chromatography. Methods Cell Biol. 35: 315-335.
2. Anderson, T.F., and Voorhees, J.J. 1980. Psoralen photochemotherapy of cutaneous disorders. Annu. Rev. Pharmacol. Toxicol. 20: 235-257.
3. Baer, B.W., and Rhodes, D. 1983. Eukaryotic RNA polymerase II binds to nucleosome cores from transcribed genes. Nature (London), 301(5900): 482-488.
4. Banditt, M., Koller, T., and Sogo, J.M. 1999. Transcriptional activity and chromatin structure of enhancer-deleted rRNA genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 19(7): 4953-4960.
5. Bazett-Jones, D.P., Mendez, E., Czarnota, G.J., Ottensmeyer, F.P., and Allfrey, V.G. 1996. Visualization and analysis of unfolded nucleosomes associated with transcribing chromatin. Nucleic Acids Res. 24(2): 321-329.
6. Belotserkovskaya, R., and Reinberg, D. 2004. Facts about FACT and transcript elongation through chromatin. Curr. Opin. Genet. Dev. 14(2): 139-46.
7. Belotserkovskaya, R., Oh, S., Bondarenko, V.A., Orphanides, G., Studitsky, V.M., and Reinberg, D. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science (Wash. D.C.), 301(5636): 1090-1093.
8. Bettler, B., Ness, P.J., Schmidlin, S., and Parish, R.W. 1988. The upstream limit of nuclease-sensitive chromatin in Dictyostelium rRNA genes neighbors a topoisomerase I-like cluster. J. Mol. Biol. 204(3): 549-559.
9. Brewer, B.J., and Fangman, W.L. 1991. Mapping replication origins in yeast chromosomes. BioEssays, 13(7): 317-322.
10. Carrozza, M.J., Utley, R.T., Workman, J.L., and Cote, J. 2003. The diverse functions of histone acetyltransferase complexes. Trends Genet. 19(6): 321-329.
11. Cavalli, G., and Thoma, F. 1993. Chromatin transitions during activation and repression of galactose-regulated genes in yeast. EMBO J. 12(12): 4603-4613.
12. Cech, T., and Pardue, M.L. 1977. Cross-linking of DNA with trimethylpsoralen is a probe for chromatin structure. Cell, 11(3): 631-640.
13. Chakravarthy, S., Park, Y.J., Chodaparambil, J., Edayathumangalam, R.S., and Luger, K. 2005. Structure and dynamic properties of nucleosome core particles. FEBS Lett. 579(4): 895-898.
14. Cohen, R.B., and Sheffery, M. 1985. Nucleosome disruption precedes transcription and is largely limited to the transcribed domain of globin genes in murine erythroleukemia cells. J. Mol. Biol. 182(1): 109-129.
15. Conconi, A. 1987. Correlation between gene activity and chromatin structure in mouse erythroleukemia cells. Ph. D. thesis, Swiss Federal Institute of Technology of Zürich. No. 8448.
16. Conconi, A., and Ryan, C.A. 1993. DNase I and micrococcal nuclease analysis of the tomato proteinase inhibitor I gene in chromatin. J. Biol. Chem. 268(1): 430-435.
17. Conconi, A., Losa, R., Koller, T., and Sogo, J.M. 1984. Psoralen-crosslinking of soluble and of H1-depleted soluble rat liver chromatin. J. Mol. Biol. 178(4): 920-928.
18. Conconi, A., Widmer, R.M., Koller, T., and Sogo, J.M. 1989. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell, 57(5): 753-761.
19. Conconi, A., Sogo, J.M., and Ryan, C.A. 1992. Ribosomal gene clusters are uniquely proportioned between open and closed chromatin structures in both tomato leaf cells and exponentially growing suspension cultures. Proc. Natl. Acad. Sci. U.S.A. 89(12): 5256-5260.
20. Conconi, A., Bespalov, V.A., and Smerdon, M.J. 2002. Transcription- coupled repair in RNA polymerase I-transcribed genes of yeast. Proc. Natl. Acad. Sci. U.S.A. 99(2): 649-654.
21. Conconi, A., Bespalov, V.A., Fahy, D., and Smerdon, M.J. 2005. DNA repair in RNA polymerase I transcribed genes. In DNA photolesions to mutations, skin cancer and cell death. Edited by R. Drouin, E. Sage, M. Rouabhia. RS-C publishers, UK. In press.
22. Culotta, V., and Sollner-Webb, B. 1988. Sites of topoisomerase I action on X. laevis ribosomal chromatin: transcriptionally active rDNA has an approximately 200 bp repeating structure. Cell, 52(4): 585-597.
23. Dammann, R., Lucchini, R., Koller, T., and Sogo, J.M. 1993. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res. 21(10): 2331-2338.
24. Dammann, R., Lucchini, R., Koller, T., and Sogo, J.M. 1995. Transcription in the yeast rRNA gene locus: distribution of the active gene copies and chromatin structure of their flanking regulatory sequences. Mol. Cell. Biol. 15(10): 5294-5303.
25. Davis, A.M., Reudelhuber, T.L., and Garrard, W.T. 1983. Varigated chromatin structures of mouse ribosomal RNA genes. J. Mol. Biol. 167(1): 133-155.
26. De Bernardin, W., Koller, T., and Sogo, J.M. 1986. Structure of in-vivo transcribing chromatin as studied in simian virus 40 minichromosomes. J. Mol. Biol. 191(3): 469-482.
27. De Winter, R.F., and Moss, T. 1986. The ribosomal spacer in Xenopus laevis is transcribed as part of the primary ribosomal RNA. Nucleic Acids Res. 14(15): 6041-6051.
28. Drew, H.R. 1984. Structural specificities of five commonly used DNA nucleases. J. Mol. Biol. 176(4): 535-557.
29. Elgin, S.C., and Weintraub, H. 1975. Chromosomal proteins and chromatin structure. Annu. Rev. Biochem. 44: 725-774.
30. Fahy, D., Conconi, A., and Smerdon, M.J. 2005. Rapid changes in transcription and chromatin structure of ribosomal genes in yeast during phase transitions. Exp. Cell Res. 305(2): 365-373.
31. Fangman, W.L., and Brewer, B.J. 1991. Activation of replication origins within yeast chromosomes. Annu. Rev. Cell Biol. 7: 375-402.
32. Foe, V.E., Wilkinson, L.E., and Laird, C.D. 1976. Comparative organization of active transcription units in Oncopeltus fasciatus. Cell, 9(1): 131-146.
33. Franke, W.W., Scheer, U., Trendelenburg, M.F., Spring, H., and Zentgraf, H. 1976. Absence of nucleosomes in transcriptionally active chromatin. Cytobiologie, 13: 401-434.
34. Fritz, L.K., and Smerdon, M.J. 1995. Repair of UV damage in actively transcribed ribosomal genes. Biochemistry, 34(40): 13117-13124.
35. Gale, J.M., and Smerdon, M.J. 1988. UV-induced pyrimidine dimers and trimethylpsoralen cross-links do not alter chromatin folding in vitro. Biochemistry, 27(19): 7197-7205.
36. Gasser, R., Koller, T., and Sogo, J.M. 1996. The stability of nucleosomes at the replication fork. J. Mol. Biol. 258(2): 224-239.
37. Gottesfeld, J.M., Bagi, G., Berg, B., and Bonner, J. 1976. Sequence composition of the template-active fraction of rat liver chromatin. Biochemistry, 15(11): 2472-2483.
38. Green, C.M., and Almouzni, G. 2002. When repair meets chromatin. First in series on chromatin dynamics. EMBO Rep. 3(1): 28-33.
39. Grummt, I. 1999. Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Prog. Nucleic Acid Res. Mol. Biol. 62: 109-154.
40. Grummt, I., and Pikaard, C.S. 2003. Epigenetic silencing of RNA polymerase I transcription. Nat. Rev. Mol. Cell Biol. 4(8): 641-649.
41. Gruss, C., Wu, J., Koller, T., and Sogo, J.M. 1993. Disruption of the nucleosomes at the replication fork. EMBO J. 12(12): 4533-4545.
42. Haaf, T., Hayman, D.L., and Schmid, M. 1991. Quantitative determination of rDNA transcription units in vertebrate cells. Exp. Cell Res. 193(1): 78-86.
43. Hanawalt, P.C., Ford, J.M., and Lloyd, D.R. 2003. Functional characterization of global genomic DNA repair and its implications for cancer. Mutat. Res. 544(2-3): 107-114.
44. Hanson, C.V., Shen, C.K., and Hearst, J.E. 1976. Cross-linking of DNA in situ as a probe for chromatin structure. Science (Wash. D.C.), 193(4247): 62-64.
45. Hayes, J.J., and Hansen, J.C. 2001. Nucleosomes and the chromatin fiber. Curr. Opin. Genet. Dev. 11(2): 124-129.
46. Higashinakagawa, T., Wahn, H., and Reeder, R.H. 1977. Isolation of ribosomal gene chromatin. Dev. Biol. 55(2): 375-386.
47. Jenuwein, T., and Allis, C.D. 2001. Translating the histone code. Science (Wash. D.C.), 293(5532): 1074-1080.
48. Ju, Q., and Warner, J.R. 1994. Ribosome synthesis during the growth cycle of Saccharomyces cerevisiae. Yeast, 10(2): 151-157;
49. Erratum in Yeast (1994) 10: 979-980.
50. Kasinsky, H.E., Lewis, J.D., Dacks, J.B., and Ausio, J. 2001. Origin of H1 linker histones. FASEB J. 15(1): 34-42.
51. Kramer, P.R., Bat, O., and Sinden, R.R. 1999. Measurement of localized DNA supercoiling and topological domain size in eukaryotic cells. Methods Enzymol. 304: 639-650.
52. Labhart, P., and Koller, T. 1981. Electron microscope specimen preparation of rat liver chromatin by a modified Miller spreading technique. Eur. J. Cell Biol. 24(2): 309-316.
53. Labhart, P., and Koller, T. 1982. Structure of the active nucleolar chromatin of Xenopus laevis oocytes. Cell, 28(2): 279-292.
54. Labhart, P., and Reeder, R.H. 1986. Characterization of three sites of RNA 3′ end formation in the Xenopus ribosomal gene spacer. Cell, 45(3): 431-443.
55. Laird, C.D., Wilkinson, L.E., Foe, V.E., and Chooi, W.Y. 1976. Analysis of chromatin-associated fiber arrays. Chromosoma, 58(2): 169-190.
56. Langst, G., and Becker, P.B. 2004. Nucleosome remodeling: one mechanism, many phenomena? Biochim. Biophys. Acta, 1677(1-3): 58-63.
57. Levy, A., and Noll, M. 1981. Chromatin fine structure of active and repressed genes. Nature (London), 289(5794): 198-203.
58. Long, E.O., and Dawid, I.B. 1980. Repeated genes in eukaryotes. Annu. Rev. Biochem. 49: 727-764.
59. Losa, R., Thoma, F., and Koller, T. 1984. Involvement of the globular domain of histone H1 in the higher order structures of chromatin. J. Mol. Biol. 175(4): 529-551.
60. Lucchini, R., and Sogo, J.M. 1992. Different chromatin structures along the spacers flanking active and inactive Xenopus rRNA genes. Mol. Cell. Biol. 12(10): 4288-4296.
61. Lucchini, R., and Sogo, J.M. 1994. Chromatin structure and transcriptional activity around the replication forks arrested at the 3′ end of the yeast rRNA genes. Mol. Cell. Biol. 14(1): 318-326.
62. Lucchini, R., and Sogo, J.M. 1995. Replication of transcriptionally active chromatin. Nature (London), 374(6519): 276-280.
63. Lucchini, R., and Sogo, J.M. 1998. The dynamic structure of ribosomal RNA gene chromatin. In Transcription of ribosomal genes by eukaryotic RNA polymerase I. Edited by M.R. Paule. Springer-Verlag and R.G. Landes Company, pp. 255-276.
64. Lucchini, R., Pauli, U., Braun, R., Koller, T., and Sogo, J.M. 1987. Structure of the extrachromosomal ribosomal RNA chromatin of Physarum polycephalum. J. Mol. Biol. 196(4): 829-843.
65. Luger, K. 2003. Structure and dynamic behavior of nucleosomes. Curr. Opin. Genet. Dev. 13(2): 127-135.
66. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature (London), 389(6648): 251-260.
67. Macleod, D., and Bird, A. 1982. DNAase I sensitivity and methylation of active versus inactive rRNA genes in Xenopus species hybrids. Cell, 29(1): 211-218.
68. Mathis, D.J., and Gorovsky, M.A. 1976. Subunit structure of rDNA-containing chromatin. Biochemistry, 15(4): 750-755.
69. Matsui, S., and Busch, H. 1977. Isolation and characterization of rDNA-containing chromatin from nucleoli. Exp. Cell Res. 109(1): 151-161.
70. Meier, A., Livingstone-Zatchej, M., and Thoma, F. 2002. Repair of active and silenced rDNA in yeast: the contributions of photolyase and transcription-couples nucleotide excision repair. J. Biol. Chem. 277(14): 11845-11852.
71. Moss, T. 2004. At the crossroads of growth control; making ribosomal RNA. Curr. Opin. Genet. Dev. 14(2): 210-217.
72. Moss, T., and Stefanovsky, V.Y. 2002. At the center of eukaryotic life. Cell, 109(5): 545-548.
73. Muller, M., Lucchini, R., and Sogo, J.M. 2000. Replication of yeast rDNA initiates downstream of transcriptionally active genes. Mol. Cell, 5(5): 767-777.
74. Muscarella, D.E., Vogt, V.M., and Bloom, S.E. 1987. Characterization of ribosomal RNA synthesis in a gene dosage mutant: the relationship of topoisomerase I and chromatin structure to transcriptional activity. J. Cell Biol. 105(4): 1501-1513.
75. Ness, P.J., Labhart, P., Banz, E., Koller, T., and Parish, R.W. 1983. Chromatin structure along the ribosomal DNA of Dictyostelium. Regional differences and changes accompanying cell differentiation. J. Mol. Biol. 166(3): 361-381.
76. Nightingale, K.P., Wellinger, R.E., Sogo, J.M., and Becker, P.B. 1998. Histone acetylation facilitates RNA polymerase II transcription of the Drosophila hsp26 gene in chromatin. EMBO J. 17(10): 2865-2876.
77. Nogi, Y., Yano, R., and Nomura, M. 1991. Synthesis of large rRNAs by RNA polymerase II in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Proc. Natl. Acad. Sci. U.S.A. 88(9): 3962-3966.
78. Noll, M. 1974a. Subunit structure of chromatin. Nature (London), 251(5472): 249-251.
79. Noll, M. 1974b. Internal structure of the chromatin subunit. Nucleic Acids Res. 1(11): 1573-1578.
80. Nomura, M. 2001. Ribosomal RNA genes, RNA polymerases, nucleolar structures, and synthesis of rRNA in the yeast Saccharomyces cerevisiae. Cold Spring Harbor Symp. Quant. Biol. 66: 555-565.
81. Orphanides, G., and Reinberg, D. 2000. RNA polymerase II elongation through chromatin. Nature (London), 407(6803): 471-475.
82. Orphanides, G., LeRoy, G., Chang, C.H., Luse, D.S., and Reinberg, D. 1998. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell, 92(1): 105-116.
83. Orphanides, G., Wu, W.H., Lane, W.S., Hampsey, M., and Reinberg, D. 1999. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature (London), 400(6741): 284-288.
84. Parish, R.W., Banz, E., and Ness, P.J. 1986. Methidiumpropyl-EDTA- iron(II) cleavage of ribosomal DNA chromatin from Dictyostelium discoideum. Nucleic Acids Res. 14(5): 2089-2107.
85. Parsons, B.J. 1980. Psoralen photochemistry. Photochem. Photobiol. 32(6): 813-821.
86. Pasero, P., Bensimon, A., and Schwob, E. 2002. Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev. 16(19): 2459-2464.
87. Peterson, C.L., and Laniel, M.A. 2004. Histones and histone modifications. Curr. Biol. 14(14): R546-R551.
88. Piper, P.W., Celis, J., Kaltoft, K., Leer, J.C., Nielsen, O.F., and Westergaard, O. 1976. Tetrahymena ribosomal RNA gene chromatin is digested by micrococcal nuclease at sites which have the same regular spacing on the DNA as corresponding sites in the bulk nuclear chromatin. Nucleic Acids Res. 3(2): 493-505.
89. Planta, R.J. 1997. Regulation of ribosome synthesis in yeast. Yeast, 13(16): 1505-1518.
90. Prakash, S., and Prakash, L. 2000. Nucleotide excision repair in yeast. Mutat. Res. 451(1-2): 13-24.
91. Prior, C.P., Cantor, C.R., Johnson, E.M., Littau, V.C., and Allfrey, V.G. 1983. Reversible changes in nucleosome structure and histone H3 accessibility in transcriptionally active and inactive states of rDNA chromatin. Cell, 34(3): 1033-1042.
92. Pruitt, S.C., and Grainger, R.M. 1981. A mosaicism in the higher order structure of Xenopus oocyte nucleolar chromatin prior to and during ribosomal gene transcription. Cell, 23(3): 711-720.
93. Reeder, R.H. 1975. The structure of active ribosomal gene chromatin. J. Cell Biol. 62: 357.
94. Reeder, R.H. 1999. Regulation of RNA polymerase I transcription in yeast and vertebrates. Prog. Nucleic Acid Res. Mol. Biol. 62: 293-327.
95. Reeder, R.H., and Roeder, R.G. 1972. Ribosomal RNA synthesis in isolated nuclei. J. Mol. Biol. 67(3): 433-441.
96. Reeves, R. 1976. Ribosomal genes of Xenopus laevis: evidence of nucleosomes in transcriptionally active chromatin. Science (Wash. D.C.), 194(4264): 529-532.
97. Reeves, R. 1977. Analysis and reconstruction of Xenopus ribosomal chromatin nucleosomes. Eur. J. Biochem. 75(2): 545-560.
98. Reeves, R. 1978a. Structure of Xenopus ribosomal gene chromatin during changes in genomic transcription rates. Cold Spring Harbor Symp. Quant. Biol. 42(2): 709-722.
99. Reeves, R. 1978b. Nucleosome structure of Xenopus oocyte amplified ribosomal genes. Biochemistry, 17(23): 4908-4916.
100. Reeves, R., and Jones, A. 1976. Genomic transcriptional activity and the structure of chromatin. Nature (London), 260(5551): 495-500.
101. Sandmeier, J.J., French, S., Osheim, Y., Cheung, W.L., Gallo, C.M., Beyer, A.L., and Smith, J.S. 2002. RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase. EMBO J. 21(18): 4959-4968.
102. Scheer, U. 1980. Structural organization of spacer chromatin between transcribed ribosomal RNA genes in amphibian oocytes. Eur. J. Cell Biol. 23(1): 189-196.
103. Scheer, U., Hugle, B., Hazan, R., and Rose, K.M. 1984. Drug-induced dispersal of transcribed rRNA genes and transcriptional products: immunolocalization and silver staining of different nucleolar components in rat cells treated with 5,6-dichloro-beta-D-ribofuranosylbenzimidazole. J. Cell Biol. 99(2): 672-679.
104. Singer, R.A., and Johnston, G.C. 2004. The FACT chromatin modulator: genetic and structure/function relationships. Biochem. Cell Biol. 82(4): 419-427.
105. Smerdon, M.J., and Conconi, A. 1999. Modulation of DNA damage and DNA repair in chromatin. Prog. Nucleic Acid Res. Mol. Biol. 62: 227-255.
106. Sogo, J.M., and Thoma, F. 2003. The structure of rDNA chromatin. In The nucleolus. Edited by M.O.J. Olson. Kluwer Academic/Plenum publishers, pp. 1-15.
107. Sogo, J.M., Ness, P.J., Widmer, R.M., Parish, R.W., and Koller, T. 1984. Psoralen-crosslinking of DNA as a probe for the structure of active nucleolar chromatin. J. Mol. Biol. 178(4): 897-919.
108. Sogo, J.M., Stahl, H., Koller, T., and Knippers, R. 1986. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J. Mol. Biol. 189(1): 189-204.
109. Sogo, J.M., Widmer, R.M., and Conconi, A. 1989. The use of psoralen-photocrosslinking for the analysis of the chromatin structure during transcription. In Photochemical probes in biochemistry. Edited by P.E. Nielsen. Kluwer Academic Publishers, pp. 179-194.
110. Stancheva, I., Lucchini, R., Koller, T., and Sogo, J.M. 1997. Chromatin structure and methylation of rat rRNA genes studied by formaldehyde fixation and psoralen cross-linking. Nucleic Acids Res. 25(9): 1727-1735.
111. The Merck Index. Merck Publishing Group, Merck and Co., Inc., N.J.
112. Thoma, F. 1991. Structural changes in nucleosomes during transcription: strip, split or flip? Trends Genet. 7(6): 175-177.
113. Van Holde, K.E. 1989. Chromatin. Springer-Verlag, Berlin.
114. Van Holde, K.E., Lohr, D.E., and Robert, C. 1992. What happens to nucleosomes during transcription? J. Biol. Chem. 267(5): 2837-2840.
115. Vogelauer, M., Cioci, F., and Camilloni, G. 1998. DNA protein-interactions at the Saccharomyces cerevisiae 35 S rRNA promoter and in its surrounding region. J. Mol. Biol. 275(2): 197-209.
116. Warner, J.R. 1989. Synthesis of ribosomes in Saccharomyces cerevisiae. Microbiol. Rev. 53(2): 256-271.
117. Weintraub, H., and Groudine, M. 1976. Chromosomal subunits in active genes have an altered conformation. Science (Wash. D.C.), 193(4256): 848-856.
118. Wellinger, R.E., Lucchini, R., Dammann, R., and Sogo, J.M. 1999. In vivo mapping of nucleosomes using psoralen-DNA cross-linking and primer extension. Methods Mol. Biol. 119: 161-173.
119. Widmer, R.M., Lucchini, R., Lezzi, M., Meyer, B., Sogo, J.M., Edstrom, J.E., and Koller, T. 1984. Chromatin structure of a hyperactive secretory protein gene (in Balbiani ring 2) of Chironomus. EMBO J. 3(7): 1635-1641.
120. Widmer, R.M., Koller, T., and Sogo, J.M. 1988. Analysis of the psoralen-crosslinking pattern in chromatin DNA by exonuclease digestion. Nucleic Acids Res. 16(14B): 7013-7024.
121. Wolffe, A. 1998. Chromatin: structure and function. Academic press, New York.
122. Woodcock, C.L., and Dimitrov, S. 2001. Higher-order structure of chromatin and chromosomes. Curr. Opin. Genet. Dev. 11(2): 130-135.
123. Wu, C., Tsukiyama, T., Gdula, D., Georgel, P., Martinez-Balbas, M., Mizuguchi, G. et al. 1998. ATP-dependent remodeling of chromatin. Cold Spring Harbor Symp. Quant. Biol. 63: 525-534.
124. Zylber, E.A., and Penman, S. 1971. Products of RNA polymerases in HeLa cell nuclei. Proc. Natl. Acad. Sci. U.S.A. 68(11): 2861-2865.