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Originally published In Press as doi:10.1074/jbc.M404260200 on January 21, 2005

J. Biol. Chem., Vol. 280, Issue 13, 12262-12270, April 1, 2005
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Regulation of the Transcriptional Activity of the IRF7 Promoter by a Pathway Independent of Interferon Signaling*

Shunbin Ning{ddagger}, Leslie E. Huye{ddagger}§, and Joseph S. Pagano{ddagger}¶||

From the {ddagger}Lineberger Comprehensive Cancer Center and Departments of Medicine and Microbiology, University of North Carolina, Chapel Hill, North Carolina 27599

Genes containing an interferon (IFN)-stimulated response element (ISRE) can be divided into two groups according to their inducibility by IFN and virus infection: one induced only by IFN and the other induced by both IFN and virus infection. Although it is now clear that IFN regulatory factor 7 (IRF7) is a multifunctional gene essential for induction of type I IFNs, regulation of the IRF7 promoter (IRF7p) is poorly understood. The IRF7 gene includes two IFN responsive elements, an IRF-binding element (IRFE) in the promoter region and an ISRE in the first intron, and is induced by the IFN-triggered Jak-STAT pathway by binding of the IFN-stimulated gene factor 3 (ISGF3) complex to the ISRE. In this study, we demonstrate that IRF3 and IRF7, which with the coactivators CREB-binding protein and P300 form the virus-activated factor (VAF) complex upon Sendai virus infection, bind to the IRF7 ISRE and IRFE and can directly activate IRF7 transcription. Promoter reporter assays show that both the ISRE and IRFE are responsive to activation by IRF7 and IRF3. In cells transiently expressing IRF7 or/and IRF3, the VAF level and binding of VAF are clearly increased after Sendai virus infection. Studies with Jak1 kinase inactive 293 cells that were stably transfected with a Jak1 kinase dead dominant negative construct, and the mutant cell lines SAN (IFN{alpha}–/{beta}–), U2A (IRF9–), U4A (Jak1–), and DKO (IRF1–/IRF2–) show that the IRF7 transcription activated directly by VAF is distinct from and independent of the IFN signaling pathway. Thus, IRF7 transcription is autoregulated by binding of the IRF7-containing VAF to its own ISRE and IRFE. The results show two distinct mechanisms for the activation of the IRF7 promoter, by IFN and by virus infection. A regulatory network between type I IFNs and IRF7 is proposed. The distinct pathways may reflect special roles for an efficient antiviral response at different stages of virus infection.

Received for publication, April 16, 2004 , and in revised form, January 18, 2005.

* This work was partially supported by grants from the National Institute of Allergy and Infectious Disease (AI 42372-01) and the National Cancer Institute (CA 19014). 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.

§ Supported by National Cancer Institute Training Grant T32-CA09156-27.

|| To whom correspondence should be addressed: Lineberger Comprehensive Cancer Center, University of North Carolina, Campus Box 7295, Chapel Hill, NC 27599. Tel.: 919-966-5907; Fax: 919-966-9673; E-mail: joseph_pagano{at}med.unc.edu.


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