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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} (M.C.); sik{at} (S.I.K.)

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J. Immunol. 184, 2057-2064
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PNAS 106, 18692-18697
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Evolution and Survival of Marine Carnivores Did Not Require a Diversity of Killer Cell Ig-Like Receptors or Ly49 NK Cell Receptors.
J. A. Hammond, L. A. Guethlein, L. Abi-Rached, A. K. Moesta, and P. Parham (2009)
J. Immunol. 182, 3618-3627
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The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells.
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Blood 113, 2434-2441
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J. Biol. Chem. 284, 5137-5147
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Complete Characterization of Killer Ig-Like Receptor (KIR) Haplotypes in Mauritian Cynomolgus Macaques: Novel Insights into Nonhuman Primate KIR Gene Content and Organization.
B. N. Bimber, A. J. Moreland, R. W. Wiseman, A. L. Hughes, and D. H. O'Connor (2008)
J. Immunol. 181, 6301-6308
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Regulatory Polymorphisms in the Interleukin-18 Promoter Are Associated with Hepatitis C Virus Clearance.
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The Journal of Infectious Disease 198, 1159-1165
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Altered natural killer cell subset distributions in resolved and persistent hepatitis C virus infection following single source exposure.
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Gut 57, 1121-1128
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Antiviral NK cell responses in HIV infection: I. NK cell receptor genes as determinants of HIV resistance and progression to AIDS.
A. Iannello, O. Debbeche, S. Samarani, and A. Ahmad (2008)
J. Leukoc. Biol. 84, 1-26
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Killer Ig-Like Receptor Expression in Uterine NK Cells Is Biased toward Recognition of HLA-C and Alters with Gestational Age.
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J. Immunol. 181, 39-46
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Synergistic Polymorphism at Two Positions Distal to the Ligand-Binding Site Makes KIR2DL2 a Stronger Receptor for HLA-C Than KIR2DL3.
A. K. Moesta, P. J. Norman, M. Yawata, N. Yawata, M. Gleimer, and P. Parham (2008)
J. Immunol. 180, 3969-3979
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HLA alleles determine differences in human natural killer cell responsiveness and potency.
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PNAS 105, 3053-3058
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Testing Strategy To Identify Cases of Acute Hepatitis C Virus (HCV) Infection and To Project HCV Incidence Rates.
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J. Clin. Microbiol. 46, 499-506
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Differential natural killer cell mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes.
G. Alter, M. P. Martin, N. Teigen, W. H. Carr, T. J. Suscovich, A. Schneidewind, H. Streeck, M. Waring, A. Meier, C. Brander, et al. (2007)
J. Exp. Med. 204, 3027-3036
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Intrahepatic Lymphocyte Expression of Dipeptidyl Peptidase I-Processed Granzyme B and Perforin Induces Hepatocyte Expression of Serine Proteinase Inhibitor 6 (Serpinb9/SPI-6).
H. W. Stout-Delgado, Y. Getachew, B. C. Miller, and D. L. Thiele (2007)
J. Immunol. 179, 6561-6567
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Detection of KIR3DS1 on the Cell Surface of Peripheral Blood NK Cells Facilitates Identification of a Novel Null Allele and Assessment of KIR3DS1 Expression during HIV-1 Infection.
V. Pascal, E. Yamada, M. P. Martin, G. Alter, M. Altfeld, J. A. Metcalf, M. W. Baseler, J. W. Adelsberger, M. Carrington, S. K. Anderson, et al. (2007)
J. Immunol. 179, 1625-1633
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KIR2DS1-Positive NK Cells Mediate Alloresponse against the C2 HLA-KIR Ligand Group In Vitro.
J. H. Chewning, C. N. Gudme, K. C. Hsu, A. Selvakumar, and B. Dupont (2007)
J. Immunol. 179, 854-868
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Protection from Lethal Infection by Adoptive Transfer of CD8 T Cells Genetically Engineered to Express Virus-Specific Innate Immune Receptor.
K. Iizuka, C. Nakajima, Y.-M. Iizuka, M. Takase, T. Kato, S. Noda, K. Tanaka, and O. Kanagawa (2007)
J. Immunol. 179, 1122-1128
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Evolution of Killer Cell Ig-Like Receptor (KIR) Genes: Definition of an Orangutan KIR Haplotype Reveals Expansion of Lineage III KIR Associated with the Emergence of MHC-C.
L. A. Guethlein, A. M. Older Aguilar, L. Abi-Rached, and P. Parham (2007)
J. Immunol. 179, 491-504
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Genetic Susceptibility, HIV Infection, and the Kidney.
K. Kiryluk, J. Martino, and A. G. Gharavi (2007)
Clin. J. Am. Soc. Nephrol. 2, S25-S35
   Abstract »    Full Text »    PDF »
Distinctive NK-cell receptor repertoires sustain high-level constitutive NK-cell activation in HIV-exposed uninfected individuals.
S. Ravet, D. Scott-Algara, E. Bonnet, H. K. Tran, T. Tran, N. Nguyen, L. X. Truong, I. Theodorou, F. Barre-Sinoussi, G. Pancino, et al. (2007)
Blood 109, 4296-4305
   Abstract »    Full Text »    PDF »
Differential NKp30 Inducibility in Chimpanzee NK Cells and Conserved NK Cell Phenotype and Function in Long-Term HIV-1-Infected Animals.
E. Rutjens, S. Mazza, R. Biassoni, G. Koopman, L. Radic, M. Fogli, P. Costa, M. C. Mingari, L. Moretta, J. Heeney, et al. (2007)
J. Immunol. 178, 1702-1712
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Deficient Major Histocompatibility Complex-Linked Innate Murine Cytomegalovirus Immunity in MA/My.L-H2b Mice and Viral Downregulation of H-2k Class I Proteins.
X. Xie, A. Dighe, P. Clark, P. Sabastian, S. Buss, and M. G. Brown (2007)
J. Virol. 81, 229-236
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Cutting Edge: Resistance to HIV-1 Infection among African Female Sex Workers Is Associated with Inhibitory KIR in the Absence of Their HLA Ligands.
W. Jennes, S. Verheyden, C. Demanet, C. A. Adje-Toure, B. Vuylsteke, J. N. Nkengasong, and L. Kestens (2006)
J. Immunol. 177, 6588-6592
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A Single Polymorphism Disrupts the Killer Ig-Like Receptor 2DL2/2DL3 D1 Domain.
C. J. VandenBussche, S. Dakshanamurthy, P. E. Posch, and C. K. Hurley (2006)
J. Immunol. 177, 5347-5357
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Gender Susceptibility to Chronic Hepatitis C Virus Infection Associated with Interleukin 10 Promoter Polymorphism.
N. Paladino, H. Fainboim, G. Theiler, T. Schroder, A. E. Munoz, A. C. Flores, O. Galdame, and L. Fainboim (2006)
J. Virol. 80, 9144-9150
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »

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