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Molecular and Cellular Biology, July 2005, p. 6140-6153, Vol. 25, No. 14
0270-7306/05/$08.00+0     doi:10.1128/MCB.25.14.6140-6153.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

HiNF-P Directly Links the Cyclin E/CDK2/p220NPAT Pathway to Histone H4 Gene Regulation at the G1/S Phase Cell Cycle Transition

Angela Miele,1,{dagger} Corey D. Braastad,1,{dagger} William F. Holmes,1,{dagger} Partha Mitra,1,{dagger} Ricardo Medina,1,{dagger} Ronglin Xie,1,{dagger} Sayyed K. Zaidi,1 Xin Ye,2 Yue Wei,3 J. Wade Harper,2 Andre J. van Wijnen,1 Janet L. Stein,1 and Gary S. Stein1*

Department of Cell Biology and Cancer Center, University of Massachusetts Medical School, Worcester, Massachusetts 01655,1 Department of Pathology, Harvard Medical School, Boston, Massachusetts 02115,2 Department of Cell Biology, Baylor College of Medicine, Houston, Texas 770303

Received 18 March 2005/ Accepted 5 April 2005

Genome replication in eukaryotic cells necessitates the stringent coupling of histone biosynthesis with the onset of DNA replication at the G1/S phase transition. A fundamental question is the mechanism that links the restriction (R) point late in G1 with histone gene expression at the onset of S phase. Here we demonstrate that HiNF-P, a transcriptional regulator of replication-dependent histone H4 genes, interacts directly with p220NPAT, a substrate of cyclin E/CDK2, to coactivate histone genes during S phase. HiNF-P and p220 are targeted to, and colocalize at, subnuclear foci (Cajal bodies) in a cell cycle-dependent manner. Genetic or biochemical disruption of the HiNF-P/p220 interaction compromises histone H4 gene activation at the G1/S phase transition and impedes cell cycle progression. Our results show that HiNF-P and p220 form a critical regulatory module that directly links histone H4 gene expression at the G1/S phase transition to the cyclin E/CDK2 signaling pathway at the R point.

* Corresponding author. Mailing address: Department of Cell Biology, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA 01655. Phone: (508) 856-5625. Fax: (508) 856-6800. E-mail: gary.stein{at}umassmed.edu.

{dagger} These authors contributed equally.

Molecular and Cellular Biology, July 2005, p. 6140-6153, Vol. 25, No. 14
0022-538X/05/$08.00+0     doi:10.1128/MCB.25.14.6140-6153.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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