Topoisomerase II regulates yeast genes with singular chromatin architectures.
Eukaryotic topoisomerase II (topo II) is the essential decatenase of newly replicated chromosomes and the main relaxase of nucleosomal DNA. Apart from these general tasks, topo II participates in more specialized functions. In mammals, topo IIα interacts with specific RNA polymerases and chromatin-remodeling complexes, whereas topo IIβ regulates developmental genes in conjunction with chromatin remodeling and heterochromatin transitions. Here we show that in budding yeast, topo II regulates the expression of specific gene subsets. To uncover this, we carried out a genomic transcription run-on shortly after the thermal inactivation of topo II. We identified a modest number of genes not involved in the general stress response but strictly dependent on topo II. These genes present distinctive functional and structural traits in comparison with the genome average. Yeast topo II is a positive regulator of genes with well-defined promoter architecture that associates to chromatin remodeling complexes; it is a negative regulator of genes extremely hypo-acetylated with complex promoters and undefined nucleosome positioning, many of which are involved in polyamine transport. These findings indicate that yeast topo II operates on singular chromatin architectures to activate or repress DNA transcription and that this activity produces functional responses to ensure chromatin stability.
Molecular Biology Institute of Barcelona, CSIC, 08028 Barcelona, Spain, Department of Biology, University of Crete, 71409 Heraklion, Greece, Department of Genetics and ERI Biotecmed, University of Valencia, 46100 Burjassot, Spain, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain and Department of Biochemistry and Molecular Biology and ERI Biotecmed, University of Valencia, 46100 Burjassot, Spain.
Christoforos
C
Nikolaou
Ignacio
I
Bermúdez
Chaysavanh
C
Manichanh
José
J
García-Martinez
Roderic
R
Guigó
José E
JE
Pérez-Ortín
Joaquim
J
Roca
D002843:Chromatin / Q000737:chemistry*; D004250:DNA Topoisomerases, Type II / Q000235:genetics / Q000502:physiology*; D004271:DNA, Fungal / Q000737:chemistry; D015966:Gene Expression Regulation, Fungal; D006657:Histones / Q000378:metabolism; D009154:Mutation; D009707:Nucleosomes / Q000737:chemistry; D011401:Promoter Regions, Genetic; D012441:Saccharomyces cerevisiae / Q000201:enzymology / Q000235:genetics*; D014157:Transcription Factors / Q000378:metabolism
D002843:Chromatin; D004271:DNA, Fungal; D006657:Histones; D009707:Nucleosomes; D014157:Transcription Factors; D004250:DNA Topoisomerases, Type II