Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena

Sean D. Taverna; Robert S. Coyne; C. D. Allis

doi:10.1016/S0092-8674(02)00941-8

Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena

Sean D. Taverna, Robert S. Coyne, C. D. Allis

Research output: Contribution to journal › Article › peer-review

230 Scopus citations

Abstract

Histone H3 lysine 9 methylation [Me(Lys9)H3] is an epigenetic mark for heterochromatin-dependent gene silencing, mediated by direct binding to chromodomain-containing proteins such as Heterochromatin Protein 1. In the ciliate Tetrahymena, two chromodomain proteins, Pdd1p and Pdd3p, are involved in the massive programmed DNA elimination that accompanies macronuclear development. We report that both proteins bind H3(Lys9)Me in vitro. In vivo, H3(Lys9)Me is confined to the time period and location where DNA elimination occurs, and associates with eliminated sequences. Loss of parental Pdd1p expression drastically reduces H3(Lys9)Me. Finally, tethering Pdd1p is sufficient to promote DNA excision. These results extend the range of H3(Lys9)Me involvement in chromatin activities outside transcriptional regulation and also strengthen the link between heterochromatin formation and programmed DNA elimination.

Original language	English (US)
Pages (from-to)	701-711
Number of pages	11
Journal	Cell
Volume	110
Issue number	6
DOIs	https://doi.org/10.1016/S0092-8674(02)00941-8
State	Published - Sep 20 2002
Externally published	Yes

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/S0092-8674(02)00941-8

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title = "Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena",

abstract = "Histone H3 lysine 9 methylation [Me(Lys9)H3] is an epigenetic mark for heterochromatin-dependent gene silencing, mediated by direct binding to chromodomain-containing proteins such as Heterochromatin Protein 1. In the ciliate Tetrahymena, two chromodomain proteins, Pdd1p and Pdd3p, are involved in the massive programmed DNA elimination that accompanies macronuclear development. We report that both proteins bind H3(Lys9)Me in vitro. In vivo, H3(Lys9)Me is confined to the time period and location where DNA elimination occurs, and associates with eliminated sequences. Loss of parental Pdd1p expression drastically reduces H3(Lys9)Me. Finally, tethering Pdd1p is sufficient to promote DNA excision. These results extend the range of H3(Lys9)Me involvement in chromatin activities outside transcriptional regulation and also strengthen the link between heterochromatin formation and programmed DNA elimination.",

author = "Taverna, {Sean D.} and Coyne, {Robert S.} and Allis, {C. D.}",

note = "Funding Information: This work was supported by grants from the National Institutes of Health to C.D.A. (GM-53512) and from the National Science Foundation to R.S.C. (MCB-9808573 and MCB-0096270). We are grateful to Dr. Mikhail Nikiforov for his many helpful suggestions; Drs. Sepideh Khorasanizadeh, Donna Cassidy-Hanley, and Heather McDonald for helpful advice; Joseph Fontana for assistance with the LexA-PDD1 construction; Dr. Wolfgang Fischle for preparation of fluorescein-labeled peptides; and Drs. Meng-Chao Yao and Larry Klobutcher for providing constructs and unpublished sequence information. R.S.C. wishes to gratefully acknowledge Dr. Peter Bruns, in whose laboratory at Cornell University part of this work was conducted.",

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AU - Taverna, Sean D.

AU - Coyne, Robert S.

AU - Allis, C. D.

N1 - Funding Information: This work was supported by grants from the National Institutes of Health to C.D.A. (GM-53512) and from the National Science Foundation to R.S.C. (MCB-9808573 and MCB-0096270). We are grateful to Dr. Mikhail Nikiforov for his many helpful suggestions; Drs. Sepideh Khorasanizadeh, Donna Cassidy-Hanley, and Heather McDonald for helpful advice; Joseph Fontana for assistance with the LexA-PDD1 construction; Dr. Wolfgang Fischle for preparation of fluorescein-labeled peptides; and Drs. Meng-Chao Yao and Larry Klobutcher for providing constructs and unpublished sequence information. R.S.C. wishes to gratefully acknowledge Dr. Peter Bruns, in whose laboratory at Cornell University part of this work was conducted.

PY - 2002/9/20

Y1 - 2002/9/20

N2 - Histone H3 lysine 9 methylation [Me(Lys9)H3] is an epigenetic mark for heterochromatin-dependent gene silencing, mediated by direct binding to chromodomain-containing proteins such as Heterochromatin Protein 1. In the ciliate Tetrahymena, two chromodomain proteins, Pdd1p and Pdd3p, are involved in the massive programmed DNA elimination that accompanies macronuclear development. We report that both proteins bind H3(Lys9)Me in vitro. In vivo, H3(Lys9)Me is confined to the time period and location where DNA elimination occurs, and associates with eliminated sequences. Loss of parental Pdd1p expression drastically reduces H3(Lys9)Me. Finally, tethering Pdd1p is sufficient to promote DNA excision. These results extend the range of H3(Lys9)Me involvement in chromatin activities outside transcriptional regulation and also strengthen the link between heterochromatin formation and programmed DNA elimination.

AB - Histone H3 lysine 9 methylation [Me(Lys9)H3] is an epigenetic mark for heterochromatin-dependent gene silencing, mediated by direct binding to chromodomain-containing proteins such as Heterochromatin Protein 1. In the ciliate Tetrahymena, two chromodomain proteins, Pdd1p and Pdd3p, are involved in the massive programmed DNA elimination that accompanies macronuclear development. We report that both proteins bind H3(Lys9)Me in vitro. In vivo, H3(Lys9)Me is confined to the time period and location where DNA elimination occurs, and associates with eliminated sequences. Loss of parental Pdd1p expression drastically reduces H3(Lys9)Me. Finally, tethering Pdd1p is sufficient to promote DNA excision. These results extend the range of H3(Lys9)Me involvement in chromatin activities outside transcriptional regulation and also strengthen the link between heterochromatin formation and programmed DNA elimination.

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Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena

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