Address: office 1410a, 17 Naberezhnaya Severnoy Dviny, Arkhangelsk, 163002, Russian Federation, Northern (Arctic) Federal University named after M.V. Lomonosov

Phone: (818-2) 21-61-21
E-mail: vestnik_est@narfu.ru
http://aer.narfu.ru/en/

ABOUT

Immune Response in Viral Hepatitis C: the Role of Natural Killer Cells. P. 68–78

Версия для печати

Section: Biology

UDC

616-092.19

Authors

Davidovich Nataliya Valer’evna
Northern State Medical University (Arkhangelsk, Russia)
e-mail: nvdavidovich@gmail.com
Solov’eva Nataliya Vladislavovna
Northern State Medical University (Arkhangelsk, Russia)
e-mail: patophiz@yandex.ru

Abstract

The immune response in hepatitis C is polyclonal and multispecific. A large number of studies of humoral and cellular components of immune system functioning in hepatitis C are undertaken. However, to date the most of the focus is on the research of the natural killer cell (NKs) function. NK is a special lymphocyte population of the innate immune system, making a figure in antiviral immunity. This review presents the modern data of national and foreign literature concerning the NK role in each stage of hepatitis C virus (HCV), starting with protection against the introduction of HCV infection and resolution in the acute phase up to the persistent infection. It describes the role of NK as the innate effector cells with an integral role in the immune response in the hepatitis C virus due to the direct cytolytic effect on infected cells, as well as the indirect effect due to the response of cytokines such as IFN-γ. The paper presents data of the main classes of activating and inhibitory receptors and coreceptors of NK, which compound with various ligands presented on the surface of target cells generates the activating or inhibiting NK signals. We present the up-to-date information about the phenotypic subsets of NK (regulatory and effector) and the impact of their redistribution in the peripheral blood to determine the outcome of chronic HCV-infection. The paper also demonstrates bidirectional interaction between NK cells and dendritic cells, required for priming, activation and expansion of T-cell immune response.

Keywords

natural killer cells, immune response, hepatitis C
Download (pdf, 4MB )

References

  1. Ivashkin V.T. Mekhanizmy immunnoy tolerantnosti i patologii pecheni [Mechanisms of Immune Tolerance and Liver Pathology]. Ros. zhurn. gastroentorologii, gepatologii, koloproktologii, 2009, vol. 19, no. 2, pp. 8–13.
  2. Kuznetsov S.D., Makashova V.V., Shabalina S.V. Osobennosti immunnogo otveta bol’nykh khronicheskim gepatitom S [Features of the Immune Response in Chronic Hepatitis C Patients]. Infekts. bolezni, 2011, vol. 9, no. 3, pp. 68–72.
  3. Boonstra A., van der Laan L.J., Vanwolleghem T., Janssen H.L. Experimental Models for Hepatitis C Viral Infection. Hepatology, 2009, vol. 50, no. 5, pp. 1646–1655.
  4. Rosen H.R. Chronic Hepatitis C Infection. N. Engl. J. Med., 2011, no. 364, pp. 2429–2438.
  5. Lanier L.L. Evolutionary Struggles Between NK Cells and Viruses. Nat. Rev. Immunol., 2008, vol. 8, no. 4, pp. 259–268.
  6. Vivier E., Tomasello E., Baratin M., Walzer T., Ugolini S. Functions of Natural Killer Cells. Nat. Rev. Immunol., 2008, vol. 9, no. 5, pp. 503–510.
  7. Raulet D.H. Roles of the NKG2D Immunoreceptor and Its Ligands. Nat. Rev. Immunol., 2003, vol. 3, no. 10, pp. 781–790.
  8. Lanier L.L. NK Cell Recognition. Annu. Rev. Immunol., 2005, no. 23, pp. 225–274.
  9. Farag S.S., Caligiuri M.A. Human Natural Killer Cell Development and Biology. Blood Rev., 2006, vol. 20, no. 3, pp. 123–137.
  10. Fernandez N.C., Flament C., Crepineau F., Angevin E., Vivier E., Zitvogel L. Dendritic Cells (DC) Promote Natural Killer (NK) Cell Functions: Dynamics of the Human DC/NK Cell Cross Talk. Eur. Cytokine Netw., 2002, vol. 13, no. 1, pp. 17–27.
  11. Welsh R.M., Waggoner S.N. NK Cells Controlling Virus-Specific T Cells: Rheostats for Acute vs Persistent Infections. Virology, 2013, vol. 435, no. 1, pp. 37–45.
  12. Golden-Mason L., Rosen H.R. Natural Killer Cells: Primary Target for Hepatitis C Virus Immune Evasion Strategies? Liver Transpl., 2006, vol. 12, no. 3, pp. 363–372.
  13. Vidal S.M., Khakoo S.I., Biron C.A. Natural Killer Cell Responses During Viral Infections: Flexibility and Conditioning of Innate Immunity by Experience. Curr. Opin. Virol., 2011, vol. 1, no. 6, pp. 497–512.
  14. Koch J., Steinle A., Watzl C., Mandelboim O. Activating Natural Cytotoxicity Receptors of Natural Killer Cells in Cancer and Infection. Trends Immunol., 2013, vol. 34, no. 4, pp. 182–191.
  15. Biassoni R. Human Natural Killer Receptors, Co-receptors, and Their Ligands. Curr. Protocol Immunol., 2009, Ch. 14, unit 14.10. doi: 10.1002/0471142735.im1410s84.
  16. Parham P. Influence of KIR Diversity on Human Immunity. Adv. Exp. Med. Biol., 2005, vol. 560, pp. 47–50.
  17. Burgess S.J., Maasho K., Masilamani M., Narayanan S., Borrego F., Coligan J.E. The NKG2D Receptor: Immunobiology and Clinical Implications. Immunol. Res., 2008, vol. 40, no. 1, pp. 18–34.
  18. Brandt C.S., Baratin M., Yi E.C., Kennedy J., Gao Z., Fox B., Haldeman B., Ostrander C.D., Kaifu T., Chabannon C., Moretta A., West R., Xu W., Vivier E., Levin S.D. The B7 Family Member B7-H6 is a Tumor Cell Ligand for the Activating Natural Killer Cell Receptor NKp30 in Humans. J. Exp. Med., 2009, vol. 206, no. 7, pp. 1495–1503.
  19. Jarahian M., Fiedler M., Cohnen A., Djandji D., Hämmerling G.J., Gati C., Cerwenka A., Turner P.C., Moyer R.W., Watzl C., Hengel H., Momburg F. Modulation of NKp30- and NKp46-Mediated Natural Killer Cell Responses by Poxviral Hemagglutinin. PLoS Pathog., 2011, vol. 7, no. 8. doi: 10.1371/journal.ppat.1002195.
  20. Mandelboim O., Lieberman N., Lev M., Paul L., Arnon T.I., Bushkin Y., Davis D.M., Strominger J.L., Yewdell J.W., Porgador A. Recognition of Haemagglutinins on Virus-Infected Cells by NKp46 Activates Lysis by Human NK Cells. Nature, 2001, vol. 409, no. 6823, pp. 1055–1060.
  21. Romero V., Azocar J., Zúñiga J., Clavijo O.P., Terreros D., Gu X., Husain Z., Chung R.T., Amos C., Yunis E.J. Interaction of NK Inhibitory Receptor Genes with HLA-C and MHC Class II Alleles in Hepatitis C Virus Infection Outcome. Mol. Immunol., 2008, vol. 45, no. 9, pp. 2429–2436.
  22. Vivier E., Raulet D.H., Moretta A., Caligiuri M.A., Zitvogel L., Lanier L.L., Yokoyama W.M., Ugolini S. Innate or Adaptive Immunity? The Example of Natural Killer Cells. Science, 2011, vol. 331, no. 6013, pp. 44–49.
  23. Werner J.M., Heller T., Gordon A.M., Sheets A., Sherker A.H., Kessler E., Bean K.S., Stevens M., Schmitt J., Rehermann B. Innate Immune Responses in Hepatitis C Virus Exposed Healthcare Workers Who Do Not Develop Acute Infection. Hepatology, 2013, vol. 58, no. 5, pp. 1621–1631.
  24. Amadei B., Urbani S., Cazaly A., Fisicaro P., Zerbini A., Ahmed P., Missale G., Ferrari C., Khakoo S.I. Activation of Natural Killer Cells During Acute Infection with Hepatitis C Virus. Gastroenterology, 2010, vol. 138, no. 4, pp. 1536–1545.
  25. Alter G., Jost S., Rihn S., Reyor L.L., Nolan B.E., Ghebremichael M., Bosch R., Altfeld M., Lauer G.M. Reduced Frequencies of NKp30+NKp46+, CD161+, and NKG2D+ NK Cells in Acute HCV Infection May Predict Viral Clearance. J. Hepatol., 2011, vol. 55, no. 2, pp. 278–288.
  26. Marras F., Bozzano F., De Maria A. Involvement of Activating NK Cell Receptors and Their Modulation in Pathogen Immunity. J. Biomed. Biotechnol., 2011. Article ID 152430.
  27. Bonorino P., Ramzan M., Camous X., Dufeu-Duchesne T., Thélu M.A., Sturm N., Dariz A., Guillermet C., Pernollet M., Zarski J.P., Marche P.N., Leroy V., Jouvin-Marche E. Fine Characterization of Intrahepatic NK Cells Expressing Natural Killer Receptors in Chronic Hepatitis B and C. J. Hepatol., 2009, vol. 51, no. 3, pp. 458–467.
  28. Cooper M.A., Fehniger T.A., Caligiuri M.A. The Biology of Human Natural Killer-Cell Subsets. Trends Immunol., 2001, vol. 22, no. 11, pp. 633–640.
  29. Crotta S., Stilla A., Wack A., D’Andrea A., Nuti S., D’Oro U., Mosca M., Filliponi F., Brunetto R.M., Bonino F., Abrignani S., Valiante N.M. Inhibition of Natural Killer Cells Through Engagement of CD81 by the Major Hepatitis C Virus Envelope Protein. J. Exp. Med., 2002, vol. 195, no. 1, pp. 35–41.
  30. Wang S.H., Huang C.X., Ye L., Wang X., Song L., Wang Y.J., Liang H., Huang X.Y., Ho W.Z. Natural Killer Cells Suppress Full Cycle HCV Infection of Human Hepatocytes. J. Viral Hepatitis, 2008, vol. 15, no. 12, pp. 855–864.
  31. Lanzavecchia A., Sallusto F. Regulation of T Cell Immunity by Dendritic Cells. Cell, 2001, vol. 106, no. 3, pp. 263–266.
  32. Ferlazzo G., Pack M., Thomas D., Paludan C., Schmid D., Strowig T., Bougras G., Muller W.A., Moretta L., Münz C. Distinct Roles of IL-12 and IL-15 in Human Natural Killer Cell Activation by Dendritic Cells From Secondary Lymphoid Organs. Proc. Nat. Acad. Sci. USA, 2004, vol. 101, no. 47, pp. 16606–16611.
  33. Stone A.E.L., Giugliano S., Schnell G., Cheng L., Leahy K.F., Golden-Mason L., Gale M., Rosen H.R. Hepatitis C Virus Pathogen Associated Molecular Pattern (PAMP) Triggers Production of Lambda-Interferons by Human Plasmacytoid Dendritic Cells. PLoS Pathog., 2013, vol. 49, no. 6. e1003316.
  34. Piccioli D., Sbrana S., Melandri E., Valiante N.M. Contact-Dependent Stimulation and Inhibition of Dendritic Cells by Natural Killer Cells. J. Exp. Med., 2002, vol. 195, no. 3, pp. 335–341.
  35. Wehner R., Dietze K., Bachmann M., Schmitz M. The Bidirectional Crosstalk Between Human Dendritic Cells and Natural Killer Cells. J. Innate Immun., 2011, vol. 3, no. 3, pp. 258–263.
  36. Ryan E.J., O’Farrelly C. The Affect of Chronic Hepatitis C Infection on Dendritic Cell Function: a Summary of the Experimental Evidence. J. Viral Hepatitis, 2011, vol. 18, no. 9, pp. 601–607.
  37. Golden-Mason L., Rosen H.R. Natural Killer Cells: Multi-Faceted Players with Key Roles in Hepatitis C Immunity. Immunol. Rev., 2013, vol. 255, no. 1, pp. 68–81.
  38. Lodoen M.B., Lanier L.L. Viral Modulation of NK Cell Immunity. Nat. Rev. Microbiol., 2005, vol. 3, no. 1, pp. 59–69.