Tup1-Ssn6 and Swi-Snf remodelling activities influence long-range chromatin organization upstream of the yeast SUC2 gene.
The traditional model for chromatin remodelling during transcription has focused upon the remodelling of nucleosomes at gene promoters. However, in this study, we have determined that Tup1-Ssn6 and Swi-Snf chromatin remodelling activities extend far upstream of the SUC2 gene promoter into the intergenic region of the Saccharomyces cerevisiae chromosome. We mapped the nucleosomal array over a 7.5 kb region that encompassed the SUC2 gene promoter and upstream region but was devoid of other transcriptionally active genes. Nucleosome positioning over this region was determined under conditions of glucose repression and derepression, and in snf2, ssn6 and snf2 ssn6 mutant strains. A map detailing remodelling events extending as much as 5 kb upstream of the SUC2 gene promoter underlines the roles of the Tup1-Ssn6 and Swi-Snf complexes in respectively organizing and disrupting nucleosome arrays. The gene specificity of these events suggests a role in gene regulation. We propose that long-range chromatin remodelling activities of Swi-Snf and Tup1-Ssn6 may ultimately influence whether the chromosomal state of the SUC2 gene is proficient for transcription. These data raise the possibility that remodelling of extensive chromatin domains may be a general property of the Swi-Snf and Tup1-Ssn6 complexes.
Fleming
Alastair B
AB
Department of Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK.
Pennings
Sari
S
D000251:Adenosine Triphosphatases; D002843:Chromatin; D042002:Chromatin Assembly and Disassembly; D021901:DNA, Intergenic / Q000737:chemistry; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D015966:Gene Expression Regulation, Fungal; D005947:Glucose / Q000494:pharmacology; D009687:Nuclear Proteins / Q000378:metabolism*; D009707:Nucleosomes / Q000378:metabolism; D011401:Promoter Regions, Genetic; D012097:Repressor Proteins / Q000378:metabolism*; D012441:Saccharomyces cerevisiae / Q000187:drug effects / Q000235:genetics* / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics* / Q000378:metabolism*; D016385:TATA Box; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D014158:Transcription, Genetic / Q000187:drug effects; D043324:beta-Fructofuranosidase / Q000235:genetics*
C065455:CYC8 protein, S cerevisiae; D002843:Chromatin; D021901:DNA, Intergenic; D004268:DNA-Binding Proteins; D009687:Nuclear Proteins; D009707:Nucleosomes; D012097:Repressor Proteins; D029701:Saccharomyces cerevisiae Proteins; C066502:TUP1 protein, S cerevisiae; D014157:Transcription Factors; C468437:SUC2 protein, S cerevisiae; D043324:beta-Fructofuranosidase; D000251:Adenosine Triphosphatases; C499333:SNF2 protein, S cerevisiae; D005947:Glucose
Eukaryot Cell. 2003 Dec;2(6):1288-303
14665463
Genes Dev. 2003 Feb 15;17(4):502-15
12600943
EMBO J. 2004 Jan 14;23(1):127-37
14685262
J Biol Chem. 2004 Feb 27;279(9):7678-84
14670975
EMBO J. 2000 Feb 1;19(3):400-9
10654939
Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3364-9
10725359
Mol Cell Biol. 2000 Sep;20(17):6380-9
10938115
Curr Top Microbiol Immunol. 2001;254:59-78
11190575
Nature. 2001 Jan 25;409(6819):533-8
11206552
Cell. 2000 Dec 22;103(7):1133-42
11163188
EMBO J. 2001 Feb 1;20(3):520-31
11157758
Mol Cell. 2001 Jan;7(1):97-104
11172715
Mol Cell. 2001 Jan;7(1):117-26
11172717
J Biol Chem. 2001 Jan 12;276(2):861-6
11013248
Curr Opin Genet Dev. 2001 Apr;11(2):124-9
11250133
Nat Genet. 2001 Aug;28(4):327-34
11455386
J Biol Chem. 2001 Sep 14;276(37):35209-16
11461917
EMBO J. 2001 Sep 17;20(18):5219-31
11566885
Mol Cell Biol. 2002 Feb;22(3):693-703
11784848
Mol Cell Biol. 2002 Mar;22(6):1615-25
11865042
Nat Struct Biol. 2002 Mar;9(3):167-71
11836537
Annu Rev Biochem. 2002;71:247-73
12045097
Mol Cell. 2002 Jun;9(6):1297-305
12086626
BMC Genet. 2001;2:5
11281938
Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15381-6
12432091
Curr Opin Genet Dev. 2004 Apr;14(2):165-73
15196463
J Biol Chem. 2004 Sep 17;279(38):39240-50
15254041
Cell. 1982 Jan;28(1):145-54
7039847
Mol Cell Biol. 1983 Mar;3(3):351-9
6843548
Genetics. 1984 May;107(1):19-32
6373495
EMBO J. 1986 Oct;5(10):2689-96
3536481
Mol Gen Genet. 1986 Dec;205(3):422-7
3550382
Nucleic Acids Res. 1987 Sep 11;15(17):6937-56
2821486
Mol Cell Biol. 1990 Dec;10(12):6500-11
2247069
Mol Microbiol. 1992 Jan;6(1):15-21
1310793
Mol Gen Genet. 1992 Feb;231(3):395-400
1538695
Genes Dev. 1992 Dec;6(12A):2288-98
1459453
Science. 1994 Jul 1;265(5168):53-60
8016655
Nature. 1994 Aug 11;370(6489):477-81
8047169
Nature. 1994 Aug 11;370(6489):481-5
8047170
Genetics. 1994 May;137(1):49-54
8056322
Genes Dev. 1994 Jun 15;8(12):1400-10
7926740
Mol Cell Biol. 1995 Apr;15(4):1999-2009
7891695
Mol Cell Biol. 1996 May;16(5):1978-88
8628264
Science. 1996 Jul 26;273(5274):513-6
8662543
J Biol Chem. 1997 Apr 25;272(17):11193-7
9111019
Nucleic Acids Res. 1997 Nov 1;25(21):4230-4
9336451
EMBO J. 1997 Oct 15;16(20):6263-71
9321405
EMBO J. 1998 Oct 15;17(20):6028-38
9774346
Mol Cell Biol. 1999 Feb;19(2):1470-8
9891080
Curr Opin Microbiol. 1999 Apr;2(2):202-7
10322167
Methods Enzymol. 1999;304:365-76
10372371
Nature. 1999 Aug 19;400(6746):784-7
10466730
J Biol Chem. 2004 Dec 31;279(53):55520-30
15471882
Mol Cell. 2005 Jun 10;18(6):735-48
15949447
Mol Cell. 2006 Feb 3;21(3):405-16
16455495
Nature. 2006 Aug 17;442(7104):772-8
16862119
Nat Rev Mol Cell Biol. 2006 Sep;7(9):657-66
16912715
Biochem Cell Biol. 2006 Aug;84(4):437-43
16936817
Mol Cell Biol. 2006 Nov;26(22):8607-22
16982689
Annu Rev Genet. 2006;40:107-38
16953792
Nat Genet. 2006 Dec;38(12):1446-51
17099712
Biochemistry. 2007 Feb 27;46(8):2239-48
17269656
Genetics. 2007 Mar;175(3):1127-35
17237508
Mol Cell. 2003 Oct;12(4):983-90
14580348
J Biol Chem. 2003 Dec 12;278(50):50158-62
14525981