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Science 305 (5685): 872-874

Copyright © 2004 by the American Association for the Advancement of Science

HLA and NK Cell Inhibitory Receptor Genes in Resolving Hepatitis C Virus Infection

Salim I. Khakoo,1* Chloe L. Thio,2 Maureen P. Martin,3 Collin R. Brooks,1 Xiaojiang Gao,3 Jacquie Astemborski,2 Jie Cheng,3 James J. Goedert,4 David Vlahov,5 Margaret Hilgartner,6 Steven Cox,7 Ann-Margeret Little,7 Graeme J. Alexander,8 Matthew E. Cramp,9 Stephen J. O'Brien,10 William M. C. Rosenberg,1 David L. Thomas,2 Mary Carrington3*

Abstract: Natural killer (NK) cells provide a central defense against viral infection by using inhibitory and activation receptors for major histocompatibility complex class I molecules as a means of controlling their activity. We show that genes encoding the inhibitory NK cell receptor KIR2DL3 and its human leukocyte antigen C group1 (HLA-C1) ligand directly influence resolution of hepatitis C virus (HCV) infection. This effect was observed in Caucasians and African Americans with expected low infectious doses of HCV but not in those with high-dose exposure, in whom the innate immune response is likely overwhelmed. The data strongly suggest that inhibitory NK cell interactions are important in determining antiviral immunity and that diminished inhibitory responses confer protection against HCV.

1 Liver Group, Division of Infection, Inflammation, and Repair, Southampton University, Southampton 5016 6YD, UK.
2 Department of Medicine, Johns Hopkins Medical Institutions, Baltimore, MD 21231, USA.
3 Basic Research Program, Scientific Applications International Corporation Frederick, Inc., Laboratory of Genomic Diversity, NCI Frederick, Frederick, MD 21702, USA.
4 Viral Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD 20852, USA.
5 New York Academy of Medicine, New York, NY 10029, USA.
6 Department of Pediatrics, New York Presbyterian Hospital–Cornell Medical Center, New York, NY 10021, USA.
7 Anthony Nolan Research Institute, The Royal Free Hospital, London NW3 2PF, UK.
8 Department of Medicine, University of Cambridge, Cambridge CD2 2QQ, UK.
9 Department of Gastroenterology, Derriford Hospital, Plymouth PL6 8DH, UK.
10 Laboratory of Genomic Diversity, National Cancer Institute, Frederick, MD 21702, USA.

* To whom correspondence should be addressed: E-mail: carringt{at}ncifcrf.gov (M.C.); sik{at}soton.ac.uk (S.I.K.)

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CCR5 in T Cell-Mediated Liver Diseases: What's Going On?.
M. N. Ajuebor, J. A. Carey, and M. G. Swain (2006)
J. Immunol. 177, 2039-2045
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Natural Killer Receptors on CD8 T Cells and Natural Killer Cells from Different HLA-C Phenotypes in Melanoma Patients..
J. A. Campillo, J. A. Martinez-Escribano, M. R. Moya-Quiles, L. A. Marin, M. Muro, N. Guerra, A. Parrado, M. Campos, J. F. Frias, A. Minguela, et al. (2006)
Clin. Cancer Res. 12, 4822-4831
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Altered CD45 expression in C77G carriers influences immune function and outcome of hepatitis C infection.
R Dawes, B Hennig, W Irving, S Petrova, S Boxall, V Ward, D Wallace, D C Macallan, M Thursz, A Hill, et al. (2006)
J. Med. Genet. 43, 678-684
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Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C.
J Nattermann, G Feldmann, G Ahlenstiel, B Langhans, T Sauerbruch, and U Spengler (2006)
Gut 55, 869-877
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Association of Transforming Growth Factor-{beta}1 Functional Polymorphisms with Natural Clearance of Hepatitis C Virus.
T. Kimura, T. Saito, M. Yoshimura, S. Yixuan, M. Baba, G. Ji, M. Muramatsu, and S. Kawata (2006)
The Journal of Infectious Disease 193, 1371-1374
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Cmv4, a New Locus Linked to the NK Cell Gene Complex, Controls Innate Resistance to Cytomegalovirus in Wild-Derived Mice.
S. G. Adam, A. Caraux, N. Fodil-Cornu, J. C. Loredo-Osti, S. Lesjean-Pottier, J. Jaubert, I. Bubic, S. Jonjic, J.-L. Guenet, S. M. Vidal, et al. (2006)
J. Immunol. 176, 5478-5485
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Apolipoprotein {varepsilon}3 allele is associated with persistent hepatitis C virus infection.
D A Price, M F Bassendine, S M Norris, C Golding, G L Toms, M L Schmid, C M Morris, A D Burt, and P T Donaldson (2006)
Gut 55, 715-718
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Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function.
M. Yawata, N. Yawata, M. Draghi, A.-M. Little, F. Partheniou, and P. Parham (2006)
J. Exp. Med. 203, 633-645
   Abstract »    Full Text »    PDF »
Genetic Polymorphism of Fc.
J. P. Pandey; and J. M. Woof (2006)
Science 311, 1376d-1377d
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Epidemiological and Genetic Correlates of Severe Acute Respiratory Syndrome Coronavirus Infection in the Hospital with the Highest Nosocomial Infection Rate in Taiwan in 2003.
Y.-M. A. Chen, S.-Y. Liang, Y.-P. Shih, C.-Y. Chen, Y.-M. Lee, L. Chang, S.-Y. Jung, M.-S. Ho, K.-Y. Liang, H.-Y. Chen, et al. (2006)
J. Clin. Microbiol. 44, 359-365
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Donor KIR genotype has a major influence on the rate of cytomegalovirus reactivation following T-cell replete stem cell transplantation.
M. Cook, D. Briggs, C. Craddock, P. Mahendra, D. Milligan, C. Fegan, P. Darbyshire, S. Lawson, E. Boxall, and P. Moss (2006)
Blood 107, 1230-1232
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The Inhibitory Receptor NKG2A Determines Lysis of Vaccinia Virus-Infected Autologous Targets by NK Cells.
C. R. Brooks, T. Elliott, P. Parham, and S. I. Khakoo (2006)
J. Immunol. 176, 1141-1147
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Requisite H2k Role in NK Cell-Mediated Resistance in Acute Murine Cytomegalovirus-Infected MA/My Mice.
A. Dighe, M. Rodriguez, P. Sabastian, X. Xie, M. McVoy, and M. G. Brown (2005)
J. Immunol. 175, 6820-6828
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Killer Cell Ig-Like Receptor-Dependent Signaling by Ig-Like Transcript 2 (ILT2/CD85j/LILRB1/LIR-1).
S. E. Kirwan and D. N. Burshtyn (2005)
J. Immunol. 175, 5006-5015
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Shared Alterations in NK Cell Frequency, Phenotype, and Function in Chronic Human Immunodeficiency Virus and Hepatitis C Virus Infections.
U.-C. Meier, R. E. Owen, E. Taylor, A. Worth, N. Naoumov, C. Willberg, K. Tang, P. Newton, P. Pellegrino, I. Williams, et al. (2005)
J. Virol. 79, 12365-12374
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Natural-killer cells and dendritic cells: "l'union fait la force".
T. Walzer, M. Dalod, S. H. Robbins, L. Zitvogel, and E. Vivier (2005)
Blood 106, 2252-2258
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Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors.
C. A. Stewart, F. Laugier-Anfossi, F. Vely, X. Saulquin, J. Riedmuller, A. Tisserant, L. Gauthier, F. Romagne, G. Ferracci, F. A. Arosa, et al. (2005)
PNAS 102, 13224-13229
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Multiple Cytokines Regulate the NK Gene Complex-Encoded Receptor Repertoire of Mature NK Cells and T Cells.
F. Gays, K. Martin, R. Kenefeck, J. G. Aust, and C. G. Brooks (2005)
J. Immunol. 175, 2938-2947
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Extensive polymorphisms of LILRB1 (ILT2, LIR1) and their association with HLA-DRB1 shared epitope negative rheumatoid arthritis.
K. Kuroki, N. Tsuchiya, M. Shiroishi, L. Rasubala, Y. Yamashita, K. Matsuta, T. Fukazawa, M. Kusaoi, Y. Murakami, M. Takiguchi, et al. (2005)
Hum. Mol. Genet. 14, 2469-2480
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Protective Effect of the HLA-Bw4I80 Epitope and the Killer Cell Immunoglobulin-Like Receptor 3DS1 Gene against the Development of Hepatocellular Carcinoma in Patients with Hepatitis C Virus Infection.
A. Lopez-Vazquez, L. Rodrigo, J. Martinez-Borra, R. Perez, M. Rodriguez, J. L. Fdez-Morera, D. Fuentes, S. Rodriguez-Rodero, S. Gonzalez, and C. Lopez-Larrea (2005)
The Journal of Infectious Disease 192, 162-165
   Abstract »    Full Text »    PDF »
Acute Hepatitis C Virus Infection.
R. T. Chung (2005)
Clinical Infectious Diseases 41, S14-S17
   Abstract »    Full Text »    PDF »

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