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Molecular and Cellular Biology, January 2004, p. 217-227, Vol. 24, No. 1
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.1.217-227.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Noncompetitive Counteractions of DNA Polymerase {varepsilon} and ISW2/yCHRAC for Epigenetic Inheritance of Telomere Position Effect in Saccharomyces cerevisiae

Tetsushi Iida1,{dagger} and Hiroyuki Araki1*

Division of Microbial Genetics, National Institute of Genetics, and Department of Genetics, SOKENDAI, Mishima, Shizuoka 411-8540, Japan1

Received 2 July 2003/ Returned for modification 12 August 2003/ Accepted 1 October 2003

Relocation of euchromatic genes near the heterochromatin region often results in mosaic gene silencing. In Saccharomyces cerevisiae, cells with the genes inserted at telomeric heterochromatin-like regions show a phenotypic variegation known as the telomere-position effect, and the epigenetic states are stably passed on to following generations. Here we show that the epigenetic states of the telomere gene are not stably inherited in cells either bearing a mutation in a catalytic subunit (Pol2) of replicative DNA polymerase {varepsilon} (Pol {varepsilon}) or lacking one of the nonessential and histone fold motif-containing subunits of Pol {varepsilon}, Dpb3 and Dpb4. We also report a novel and putative chromatin-remodeling complex, ISW2/yCHRAC, that contains Isw2, Itc1, Dpb3-like subunit (Dls1), and Dpb4. Using the single-cell method developed in this study, we demonstrate that without Pol {varepsilon} and ISW2/yCHRAC, the epigenetic states of the telomere are frequently switched. Furthermore, we reveal that Pol {varepsilon} and ISW2/yCHRAC function independently: Pol {varepsilon} operates for the stable inheritance of a silent state, while ISW2/yCHRAC works for that of an expressed state. We therefore propose that inheritance of specific epigenetic states of a telomere requires at least two counteracting regulators.

* Corresponding author. Mailing address: Division of Microbial Genetics, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan. Phone: (81) 55 981 6754. Fax: (81) 55 981 6762. E-mail: hiaraki{at}lab.nig.ac.jp.

{dagger} Present address: Center for Developmental Biology, RIKEN, Kobe 650-0047, Japan.

Molecular and Cellular Biology, January 2004, p. 217-227, Vol. 24, No. 1
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.1.217-227.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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