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J. Biol. Chem., Vol. 279, Issue 48, 49857-49867, November 26, 2004

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Nuclear Factor 1 and Octamer Transcription Factor 1 Binding Preset the Chromatin Structure of the Mouse Mammary Tumor Virus Promoter for Hormone Induction^*

Sergey Belikov, Per-Henrik Holmqvist, Carolina Åstrand, and Örjan Wrange

From the Department of Cell and Molecular Biology, The Medical Nobel Institute, P. O. Box 285, Karolinska Institutet, Stockholm SE-17177, Sweden

When the mouse mammary tumor virus (MMTV) is integrated into the genome of a mammalian cell, its long terminal repeat (LTR) harbors six specifically positioned nucleosomes. Transcription from the MMTV promoter is regulated by the glucocorticoid hormone via the glucocorticoid receptor (GR). The mechanism of the apparently constitutive nucleosome arrangement has remained unclear. Previous in vitro reconstitution of nucleosome(s) on small segments of the MMTV LTR suggested that the DNA sequence was decisive for the nucleosome arrangement. However, microinjection of MMTV LTR DNA in Xenopus oocytes rendered randomly distributed nucleosomes. This indicated that oocytes lack factor(s) that induces nucleosome positioning at the MMTV LTR in other cells. Here we demonstrate that specific and concomitant binding of nuclear factor 1 (NF1) and octamer factor 1 (Oct1) to their cognate sites within the MMTV promoter induce a partial nucleosome positioning that is an intermediary state between the randomly organized inactive promoter and the hormone and GR-activated promoter containing distinctly positioned nucleosomes. Oct1 and NF1 reciprocally facilitate each other's binding to the MMTV LTR in vivo. The NF1 and Oct1 binding also facilitate hormone-dependent GR-DNA interaction and result in a faster and stronger hormone response. Since NF1 and Oct1 generate an intermediary state of nucleosome positioning and enhance the hormone-induced response, we refer to this as a preset chromatin structure. We propose that this state of NF1 and Oct1-induced chromatin presetting mimics the early step(s) of chromatin remodeling involved in tissue-specific gene expression.

Received for publication, August 24, 2004 , and in revised form, September 14, 2004.

^* This work was supported by Swedish Cancer Foundation Project 2222-B03-19XCC) and by Knut and Alice Wallenberg's foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains two additional figures.

Supported by the Cell Signaling Program of the Swedish Foundation for Strategic Research.

To whom correspondence should be addressed. Tel.: 46-8-5248-7373; Fax: 46-8-31-35-29; E-mail: orjan.wrange{at}cmb.ki.se.

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