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Published online on February 14, 2005, 10.1073/pnas.0408707102
PNAS | February 22, 2005 | vol. 102 | no. 8 | 2986-2991


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MICROBIOLOGY
Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling

Eileen Foy *, Kui Li {dagger}, Rhea Sumpter, Jr. *, Yueh-Ming Loo *, Cynthia L. Johnson *, Chunfu Wang *, Penny Mar Fish *, Mitsutoshi Yoneyama {ddagger}, Takashi Fujita {ddagger}, Stanley M. Lemon {dagger}, and Michael Gale, Jr. *, §

*Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, TX 75390; {dagger}Department of Microbiology and Immunology and Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX 77555; and {ddagger}Department of Tumor Cell Biology, Tokyo Metropolitan Institute of Medical Science, Tokyo Metropolitan Organization for Medical Research, Tokyo 113-8613, Japan

Edited by Peter Palese, Mount Sinai School of Medicine, New York, NY and approved January 3, 2005 (received for review November 22, 2004)

Hepatitis C virus (HCV) is a major human pathogen that infects 170 million people. A hallmark of HCV is its ability to establish persistent infections reflecting the evasion of host immunity and interference with {alpha}/{beta}-IFN innate immune defenses. We demonstrate that disruption of retinoic acid-inducible gene I (RIG-I) signaling by the viral NS3/4A protease contributes to the ability of HCV to control innate antiviral defenses. RIG-I was essential for virus or HCV RNA-induced signaling to the IFN-{beta} promoter in human hepatoma cells. This signaling was disrupted by the protease activity of NS3/4A, which ablates RIG-I signaling of downstream IFN regulatory factor 3 and NF-{kappa}B activation, attenuating expression of host antiviral defense genes and interrupting an IFN amplification loop that otherwise suppresses HCV replication. Treatment of cells with an active site inhibitor of the NS3/4A protease relieved this suppression and restored intracellular antiviral defenses. Thus, NS3/4A control of RIG-I supports HCV persistence by preventing IFN regulatory factor 3 and NF-{kappa}B activation. Our results demonstrate that these processes are amenable to restoration through pharmacologic inhibition of viral protease function.

interferon | protease | host response | infection | NF-{kappa}B

This paper was submitted directly (Track II) to the PNAS office.

Abbreviations: RIG-I, retinoic acid-inducible gene I; TLR, Toll-like receptor; HCV, hepatitis C virus; IRF-3, IFN regulatory factor-3; NS, nonstructural; Huh, human hepatoma; SenV, Sendai virus; siRNA, short interfering RNA; TRIF, Toll-IL-1 receptor domain-containing adapter-inducing IFN-{beta}; ISG, IFN-stimulated gene; TBK1, Tank-binding kinase 1; NDV, New Castle disease virus.

§ To whom correspondence should be addressed. E-mail: michael.gale{at}utsouthwestern.edu.

© 2005 by The National Academy of Sciences of the USA


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