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Originally published In Press as doi:10.1074/jbc.M204777200 on August 28, 2002

J. Biol. Chem., Vol. 277, Issue 45, 43481-43494, November 8, 2002
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Novel Combinatorial Interactions of GATA-1, PU.1, and C/EBPepsilon Isoforms Regulate Transcription of the Gene Encoding Eosinophil Granule Major Basic Protein*

Jian DuDagger , Monika J. StankiewiczDagger , Yang LiuDagger , Qing XiDagger , Jonathan E. SchmitzDagger , Julie A. Lekstrom-Himes§, and Steven J. AckermanDagger

From the Dagger  Department of Biochemistry and Molecular Biology, College of Medicine, University of Illinois, Chicago, Illinois 60612 and § Laboratory of Host Defenses, National Institutes of Health, Bethesda, Maryland 20892

GATA-1 and the ets factor PU.1 have been reported to functionally antagonize one another in the regulation of erythroid versus myeloid gene transcription and development. The CCAAT enhancer binding protein epsilon  (C/EBPepsilon ) is expressed as multiple isoforms and has been shown to be essential to myeloid (granulocyte) terminal differentiation. We have defined a novel synergistic, as opposed to antagonistic, combinatorial interaction between GATA-1 and PU.1, and a unique repressor role for certain C/EBPepsilon isoforms in the transcriptional regulation of a model eosinophil granulocyte gene, the major basic protein (MBP). The eosinophil-specific P2 promoter of the MBP gene contains GATA-1, C/EBP, and PU.1 consensus sites that bind these factors in nuclear extracts of the eosinophil myelocyte cell line, AML14.3D10. The promoter is transactivated by GATA-1 alone but is synergistically transactivated by low levels of PU.1 in the context of optimal levels of GATA-1. The C/EBPepsilon 27 isoform strongly represses GATA-1 activity and completely blocks GATA-1/PU.1 synergy. In vitro mutational analyses of the MBP-P2 promoter showed that both the GATA-1/PU.1 synergy, and repressor activity of C/EBPepsilon 27 are mediated via protein-protein interactions through the C/EBP and/or GATA-binding sites but not the PU.1 sites. Co-immunoprecipitations using lysates of AML14.3D10 eosinophils show that both C/EBPepsilon 32/30 and epsilon 27 physically interact in vivo with PU.1 and GATA-1, demonstrating functional interactions among these factors in eosinophil progenitors. Our findings identify novel combinatorial protein-protein interactions for GATA-1, PU.1, and C/EBPepsilon isoforms in eosinophil gene transcription that include GATA-1/PU.1 synergy and repressor activity for C/EBPepsilon 27.

* This work was supported by United States Public Health Service Grant AI33043 (to S. J. A.) from NIAID, National Institutes of Health.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, MC536, A-312 College of Medicine West, University of Illinois, 1819 West Polk St., Chicago, IL 60612. Tel.: 312-996-6149; Fax: 312-996-5623; E-mail: sackerma@uic.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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