5-Bromodeoxyuridine induces transcription of repressed genes with disruption of nucleosome positioning

FEBS Journal

Volumn 277, Issue 21, 2010, Pages 4539-4548

  Miki, Kensuke ^a   Shimizu, Mitsuhiro ^b   Fujii, Michihiko ^a   Takayama, Shinichi ^a   Hossain, Mohammad Nazir ^a   Ayusawa, Dai ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b MEISEI UNIVERSITY   (Japan)

Author keywords

5 bromodeoxyuridine; AT tract; BAR1; Nucleosome positioning; Transcriptional derepression

Indexed keywords

5 BROMOURACIL; BROXURIDINE; GENOMIC DNA; MINICHROMOSOME MAINTENANCE PROTEIN; ANTIMETABOLITE; ASPARTIC PROTEINASE; BAR1 PROTEIN, S CEREVISIAE; FUN80 PROTEIN, S CEREVISIAE; MESSENGER RNA; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; AT RICH SEQUENCE; BAR1 GENE; BINDING SITE; CELL DISRUPTION; CHROMATIN; CHROMOSOME POSITIONING; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VIVO STUDY; MARKER GENE; NONHUMAN; NUCLEOSOME; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; REPRESSOR GENE; TATA BOX; UPREGULATION; YEAST CELL; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NORTHERN BLOTTING; SACCHAROMYCES CEREVISIAE;

ANTIMETABOLITES; ASPARTIC ACID ENDOPEPTIDASES; BLOTTING, NORTHERN; BROMOURACIL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 79952113558     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07868.x     Document Type: Article

References (37)

1. Michishita E, Nakabayashi K, Suzuki T, Kaul SC, Ogino H, Fujii M, Mitsui Y & Ayusawa D (1999) 5-Bromodeoxyuridine induces senescence-like phenomena in mammalian cells regardless of cell type or species. J Biochem (Tokyo) 126, 1052-1059. (Pubitemid 30014451)
2. Fujii M, Ito H, Hasegawa T, Suzuki T, Adachi N & Ayusawa D (2002) 5-Bromo-2′-deoxyuridine efficiently suppresses division potential of the yeast Saccharomyces cerevisiae. Biosci Biotechnol Biochem 66, 906-909. (Pubitemid 39251363)
3. Wilt FH & Anderson M (1972) The action of 5-bromodeoxyuridine on differentiation. Dev Biol 28, 443-447.
4. Weintraub H (1973) Size of the BUdR sensitive targets for differentiation. Nat New Biol 244, 142-143.
5. Goz B (1977) The effects of incorporation of 5-halogenated deoxyuridines into the DNA of eukaryotic cells. Pharmacol Rev 29, 249-272.
6. Suzuki T, Minagawa S, Michishita E, Ogino H, Fujii M, Mitsui Y & Ayusawa D (2001) Induction of senescence-associated genes by 5-bromodeoxyuridine in HeLa cells. Exp Gerontol 36, 465-474. (Pubitemid 32201502)
7. Minagawa S, Nakabayashi K, Fujii M, Scherer SW and Ayusawa D (2005) Early BrdU-responsive genes constitute a novel class of senescence-associated genes in human cells. Exp Cell Res 304, 552-558. (Pubitemid 40321131)
8. Zakharov AF, Baranovskaya LI, Ibraimov AI, Benjusch VA, Demintseva VS & Oblapenko NG (1974) Differential spiralization along mammalian mitotic chromosomes. II. 5-bromodeoxyuridine and 5-bromodeoxycytidine- revealed differentiation in human chromosomes. Chromosoma 44, 343-359.
9. Suzuki T, Yaginuma M, Oishi T, Michishita E, Ogino H, Fujii M & Ayusawa D (2001) 5-Bromodeoxyuridine suppresses position effect variegation of transgenes in HeLa cells. Exp Cell Res 266, 53-63. (Pubitemid 32989042)
10. Fan J, Kodama E, Koh Y, Nakao M & Matsuoka M (2005) Halogenated thymidine analogues restore the expression of silenced genes without demethylation. Cancer Res 65, 6927-6933. (Pubitemid 41060732)
11. Suzuki T, Michishita E, Ogino H, Fujii M & Ayusawa D (2002) Synergistic induction of the senescence-associated genes by 5-bromodeoxyuridine and AT-binding ligands in HeLa cells. Exp Cell Res 276, 174-184. (Pubitemid 34969311)
12. Minagawa S, Nakabayashi K, Fujii M, Scherer SW & Ayusawa D (2004) Functional and chromosomal clustering of genes responsive to 5-bromodeoxyuridine in human cells. Exp Gerontol 39, 1069-1078. (Pubitemid 38952887)
13. Satou W, Suzuki T, Noguchi T, Ogino H, Fujii M & Ayusawa D (2004) AT-hook proteins stimulate induction of senescence markers triggered by 5-bromodeoxyuridine in mammalian cells. Exp Gerontol 39, 173-179. (Pubitemid 38169407)
14. Kingston RE, Bunker CA & Imbalzano AN (1996) Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev 10, 905-920. (Pubitemid 26138703)
15. Wolffe AP & Hayes JJ (1999) Chromatin disruption and modification. Nucleic Acids Res 27, 711-720. (Pubitemid 29209356)
16. Morse RH (2007) Transcription factor access to promoter elements. J Cell Biochem 102, 560-570.
17. Shimizu M, Mori T, Sakurai T & Shindo H (2000) Destabilization of nucleosomes by an unusual DNA conformation adopted by poly(dA)/poly(dT) tracts in vivo. EMBO J 19, 3358-3365. (Pubitemid 30428213)
18. Miki K, Shimizu M, Fujii M, Hossain MN & Ayusawa D (2008) 5-Bromouracil disrupts nucleosome positioning by inducing A-form-like DNA conformation in yeast cells. Biochem Biophys Res Commun 368, 662-669.
19. Lin S, Lin D & Riggs AD (1976) Histones bind more tightly to bromodeoxyuridine-substituted DNA than to normal DNA. Nucleic Acids Res 3, 2183-2191.
20. Fasy TM, Cullen BR, Luk D & Bick MD (1980) Studies on the enhanced interaction of halodeoxyuridine-substituted DNAs with H1 histones and other polypeptides. J Biol Chem 255, 1380-1387.
21. Roth SY, Shimizu M, Johnson L, Grunstein M & Simpson RT (1992) Stable nucleosome positioning and complete repression by the yeast alpha 2 repressor are disrupted by amino-terminal mutations in histone H4. Genes Dev 6, 411-425.
22. Ganter B, Tan S & Richmond TJ (1993) Genomic footprinting of the promoter regions of STE2 and STE3 genes in the yeast Saccharomyces cerevisiae. J Mol Biol 234, 975-987. (Pubitemid 24027229)
23. Cooper JP, Roth SY & Simpson RT (1994) The global transcriptional regulators, SSN6 and TUP1, play distinct roles in the establishment of a repressive chromatin structure. Genes Dev 8, 1400-1410. (Pubitemid 24189807)
24. Davie JK, Trumbly RJ & Dent SY (2002) Histone-dependent association of Tup1-Ssn6 with repressed genes in vivo. Mol Cell Biol 22, 693-703. (Pubitemid 34053051)
25. Ruiz C, Escribano V, Morgado E, Molina M & Mazon MJ (2003) Cell-type-dependent repression of yeast a-specific genes requires Itc1p, a subunit of the Isw2p-Itc1p chromatin remodelling complex. Microbiology 149, 341-351. (Pubitemid 36285191)
26. Shimizu M, Roth SY, Szent-Gyorgyi C & Simpson RT (1991) Nucleosomes are positioned with base pair precision adjacent to the alpha 2 operator in Saccharomyces cerevisiae. EMBO J 10, 3033-3041. (Pubitemid 21905322)
27. Morohashi N, Yamamoto Y, Kuwana S, Morita W, Shindo H, Mitchell AP & Shimizu M (2006) Effect of sequence-directed nucleosome disruption on cell-typespecific repression by alpha2/Mcm1 in the yeast genome. Eukaryot Cell 5, 1925-1933.
28. Zhong H, McCord R & Vershon AK (1999) Identification of target sites of the alpha2-Mcm1 repressor complex in the yeast genome. Genome Res 9, 1040-1047.
29. Goeddel DV, Yansura DG, Winston C & Caruthers MH (1978) Studies on gene control regions. VII. Effect of 5-bromouracil-substituted lac operators on the lac operator-lac repressor interaction. J Mol Biol 123, 661-687. (Pubitemid 9006591)
30. Brennan CA, Van Cleve MD & Gumport RI (1986) The effects of base analogue substitutions on the cleavage by the EcoRI restriction endonuclease of octadeoxyribonucleotides containing modified EcoRI recognition sequences. J Biol Chem 261, 7270-7278. (Pubitemid 17224724)
31. Hayakawa T, Ono A & Ueda T (1988) Synthesis of decadeoxyribonucleotides containing 5-modified uracils and their interactions with restriction endonucleases Bgl II, Sau 3AI and Mbo I (nucleosides and nucleotides 82). Nucleic Acids Res 16, 4761-4776.
32. Risse G, Jooss K, Neuberg M, Bruller HJ & Muller R (1989) Asymmetrical recognition of the palindromic AP1 binding site (TRE) by Fos protein complexes. EMBO J 8, 3825-3832. (Pubitemid 20016064)
33. Balasubramanian B & Morse RH (1999) Binding of Gal4p and bicoid to nucleosomal sites in yeast in the absence of replication. Mol Cell Biol 19, 2977-2985. (Pubitemid 29144543)
34. Takayama S, Fujii M, Kurosawa A, Adachi N & Ayusawa D (2007) Overexpression of HAM1 gene detoxifies 5-bromodeoxyuridine in the yeast Saccharomyces cerevisiae. Curr Genet 52, 203-211. (Pubitemid 350090623)
35. Murphy MR, Shimizu M, Roth SY, Dranginis AM & Simpson RT (1993) DNA-protein interactions at the S. cerevisiae alpha 2 operator in vivo. Nucleic Acids Res 21, 3295-3300. (Pubitemid 23230503)
36. Shimizu M & Mitchell AP (2003) Hap1p photofootprinting as an in vivo assay of repression mechanism in Saccharomyces cerevisiae. Methods Enzymol 370, 479-487. (Pubitemid 37542804)
37. Morohashi N, Nakajima K, Kuwana S, Tachiwana H, Kurumizaka H & Shimizu M (2008) In vivo and in vitro footprinting of nucleosomes and transcriptional activators using an infrared-fluorescence DNA sequencer. Biol Pharm Bull 31, 187-192.