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Molecular and Cellular Biology, July 2000, p. 4666-4679, Vol. 20, No. 13
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Binding of HMG-I(Y) Imparts Architectural Specificity to a Positioned Nucleosome on the Promoter of the Human Interleukin-2 Receptor alpha  Gene

R. Reeves,1,* W. J. Leonard,2 and M. S. Nissen1

Biochemistry/Biophysics, School of Molecular Biosciences, Washington State University, Pullman, Washington 99164,1 and Laboratory of Molecular Immunology, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, Maryland 208922

Received 7 October 1999/Returned for modification 19 November 1999/Accepted 11 April 2000

Transcriptional induction of the interleukin-2 receptor alpha-chain (IL-2Ralpha ) gene is a key event regulating T-cell-mediated immunity in mammals. In vivo, the T-cell-restricted protein Elf-1 and the general architectural transcription factor HMG-I(Y) cooperate in transcriptional regulation of the human IL-2Ralpha gene by binding to a specific positive regulatory region (PRRII) in its proximal promoter. Employing chromatin reconstitution analyses, we demonstrate that the binding sites for both HMG-I(Y) and Elf-1 in the PRRII element are incorporated into a strongly positioned nucleosome in vitro. A variety of analytical techniques was used to determine that a stable core particle is positioned over most of the PRRII element and that this nucleosome exhibits only a limited amount of lateral translational mobility. Regardless of its translational setting, the in vitro position of the nucleosome is such that DNA recognition sequences for both HMG-I(Y) and Elf-1 are located on the surface of the core particle. Restriction nuclease accessibility analyses indicate that a similarly positioned nucleosome also exists on the PRRII element in unstimulated lymphocytes when the IL-2Ralpha gene is silent and suggest that this core particle is remodeled following transcriptional activation of the gene in vivo. In vitro experiments employing the chemical cleavage reagent 1,10-phenanthroline copper (II) covalently attached to its C-terminal end demonstrate that HMG-I(Y) protein binds to the positioned PRRII nucleosome in a direction-specific manner, thus imparting a distinct architectural configuration to the core particle. Together, these findings suggest a role for the HMG-I(Y) protein in assisting the remodeling of a critically positioned nucleosome on the PRRII promoter element during IL-2Ralpha transcriptional activation in lymphocytes in vivo.

* Corresponding author. Mailing address: Biochemistry/Biophysics, School of Molecular Biosciences, Washington State University, Pullman, WA 99164. Phone: (509) 335-1948. Fax: (509) 335-9688. E-mail: reevesr{at}mail.wsu.edu.

Molecular and Cellular Biology, July 2000, p. 4666-4679, Vol. 20, No. 13
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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