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Molecular and Cellular Biology, November 2002, p. 7459-7472, Vol. 22, No. 21
0270-7306/02/$04.00+0     DOI: 10.1128/MCB.22.21.7459-7472.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Coupling of DNA Synthesis and Histone Synthesis in S Phase Independent of Cyclin/cdk2 Activity

David M. Nelson,1 Xiaofen Ye,1 Caitlin Hall,1 Hidelita Santos,1 Tianlin Ma,2 Gary D. Kao,1 Timothy J. Yen,1 J. Wade Harper,2 and Peter D. Adams1*

Fox Chase Cancer Center, Philadelphia, Pennsylvania,1 Baylor College of Medicine, Houston, Texas2

Received 2 June 2002/ Returned for modification 18 July 2002/ Accepted 30 July 2002

DNA and histone synthesis are both triggered at the beginning of S phase by cyclin/cdk2 activity. Previous studies showed that inhibition of DNA synthesis with hydroxyurea or cytosine arabinoside (AraC) triggers a concerted repression of histone synthesis, indicating that sustained histone synthesis depends on continued DNA synthesis. Here we show that ectopic expression of HIRA, the likely human ortholog of two cell cycle-regulated repressors of histone gene transcription in yeast (Hir1p and Hir2p), represses transcription of histones and that this, in turn, triggers a concerted block of DNA synthesis. Thus, in mammalian cells sustained DNA synthesis and histone synthesis are mutually dependent on each other during S phase. Although cyclin/cdk2 activity drives activation of both DNA and histone synthesis at the G1/S transition of cycling cells, concerted repression of DNA or histone synthesis in response to inhibition of either one of these is not accompanied by prolonged inhibition of cyclin A/cdk2 or E/cdk2 activity. Therefore, during S phase coupling of DNA and histone synthesis occurs, at least in part, through a mechanism that is independent of cyclin/cdk2 activity. Coupling of DNA and histone synthesis in S phase presumably contributes to the prompt and orderly assembly of newly replicated DNA into chromatin.

* Corresponding author. Mailing address: Fox Chase Cancer Center, 7701 Burholme Ave., Philadelphia, PA 19111. Phone: (215) 728-7108. Fax: (215) 728-3616. E-mail: pd_adams{at}fccc.edu.

Molecular and Cellular Biology, November 2002, p. 7459-7472, Vol. 22, No. 21
0022-538X/02/$04.00+0     DOI: 10.1128/MCB.22.21.7459-7472.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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