Hepatitis C virus-infected cells downregulate NKp30 and inhibit ex vivo NK cell functions

Journal of Immunology

Volumn 191, Issue 6, 2013, Pages 3308-3318

  Holder, Kayla A ^a   Stapleton, Staci N ^a   Gallant, Maureen E ^a   Russell, Rodney S ^a   Grant, Michael D ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD81 ANTIGEN; GAMMA INTERFERON; HLA E ANTIGEN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR NKG2A; NATURAL KILLER CELL RECEPTOR NKG2D; NKP40 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CELL CONTACT; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EX VIVO STUDY; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; VIRUS CELL INTERACTION;

CELL LINE; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNOLOGIC TECHNIQUES; KILLER CELLS, NATURAL; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3;

EID: 84884273811     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300164     Document Type: Article

References (76)

1. Tellinghuisen, T. L., M. J. Evans, T. von Hahn, S. You, and C. M. Rice. 2007. Studying hepatitis C virus: making the best of a bad virus. J. Virol. 81: 8853-8867.
2. World Health Orgnanization. 2012. Global Alert and Response: Hepatitis C. WHO Press, Geneva, Switzerland. Available at: http://www.who.int/csr/disease/ hepatitis/whocdscsrlyo2003/en/index1.html.
3. Li, K., and S. M. Lemon. 2013. Innate immune responses in hepatitis C virus infection. Semin. Immunopathol. 35: 53-72.
4. Lindenbach, B. D., H. J. Thiel, and C. M. Rice. 2007. Flaviviridae: The Viruses and Their Replication, 5th Ed. Lippincott Williams & Wilkins, Philadelphia.
5. Lindenbach, B. D., M. J. Evans, A. J. Syder, B. Wölk, T. L. Tellinghuisen, C. C. Liu, T. Maruyama, R. O. Hynes, D. R. Burton, J. A. McKeating, and C. M. Rice. 2005. Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
6. Bartosch, B., A. Vitelli, C. Granier, C. Goujon, J. Dubuisson, S. Pascale, E. Scarselli, R. Cortese, A. Nicosia, and F. L. Cosset. 2003. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J. Biol. Chem. 278: 41624-41630.
7. McKeating, J. A., L. Q. Zhang, C. Logvinoff, M. Flint, J. Zhang, J. Yu, D. Butera, D. D. Ho, L. B. Dustin, C. M. Rice, and P. Balfe. 2004. Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J. Virol. 78: 8496-8505.
8. Zhang, J., G. Randall, A. Higginbottom, P. Monk, C. M. Rice, and J. A. McKeating. 2004. CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J. Virol. 78: 1448-1455.
9. Flint, M., C. Maidens, L. D. Loomis-Price, C. Shotton, J. Dubuisson, P. Monk, A. Higginbottom, S. Levy, and J. A. McKeating. 1999. Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J. Virol. 73: 6235-6244.
10. Pileri, P., Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, R. Petracca, A. J.Weiner, M. Houghton, D. Rosa, G. Grandi, and S. Abrignani. 1998. Binding of hepatitis C virus to CD81. Science 282: 938-941.
11. Grove, J., T. Huby, Z. Stamataki, T. Vanwolleghem, P. Meuleman, M. Farquhar, A. Schwarz, M. Moreau, J. S. Owen, G. Leroux-Roels, et al. 2007. Scavenger receptor BI and BII expression levels modulate hepatitis C virus infectivity. J. Virol. 81: 3162-3169.
12. Bartosch, B., G. Verney, M. Dreux, P. Donot, Y. Morice, F. Penin, J. M. Pawlotsky, D. Lavillette, and F. L. Cosset. 2005. An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J. Virol. 79: 8217-8229.
13. Scarselli, E., H. Ansuini, R. Cerino, R. M. Roccasecca, S. Acali, G. Filocamo, C. Traboni, A. Nicosia, R. Cortese, and A. Vitelli. 2002. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21: 5017-5025.
14. Ciesek, S., S. Westhaus, M. Wicht, I. Wappler, S. Henschen, C. Sarrazin, N. Hamdi, A. I. Abdelaziz, C. P. Strassburg, H. Wedemeyer, et al. 2011. Impact of intra-and interspecies variation of occludin on its function as coreceptor for authentic hepatitis C virus particles. J. Virol. 85: 7613-7621.
15. Benedicto, I., F. Molina-Jiménez, B. Bartosch, F. L. Cosset, D. Lavillette, J. Prieto, R. Moreno-Otero, A. Valenzuela-Fernández, R. Aldabe, M. López-Cabrera, and P. L. Majano. 2009. The tight junction-associated protein occludin is required for a postbinding step in hepatitis C virus entry and infection. J. Virol. 83: 8012-8020.
16. Ploss, A., M. J. Evans, V. A. Gaysinskaya, M. Panis, H. You, Y. P. de Jong, and C. M. Rice. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457: 882-886.
17. Meertens, L., C. Bertaux, L. Cukierman, E. Cormier, D. Lavillette, F. L. Cosset, and T. Dragic. 2008. The tight junction proteins claudin-1,-6, and-9 are entry cofactors for hepatitis C virus. J. Virol. 82: 3555-3560.
18. Evans, M. J., T. von Hahn, D. M. Tscherne, A. J. Syder, M. Panis, B. Wö lk, T. Hatziioannou, J. A. McKeating, P. D. Bieniasz, and C. M. Rice. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
19. Roccasecca, R., H. Ansuini, A. Vitelli, A. Meola, E. Scarselli, S. Acali, M. Pezzanera, B. B. Ercole, J. McKeating, A. Yagnik, et al. 2003. Binding of the hepatitis C virus E2 glycoprotein to CD81 is strain specific and is modulated by a complex interplay between hypervariable regions 1 and 2. J. Virol. 77: 1856-1867.
20. Owsianka, A. M., J. M. Timms, A. W. Tarr, R. J. Brown, T. P. Hickling, A. Szwejk, K. Bienkowska-Szewczyk, B. J. Thomson, A. H. Patel, and J. K. Ball. 2006. Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J. Virol. 80: 8695-8704.
21. Li, K., E. Foy, J. C. Ferreon, M. Nakamura, A. C. Ferreon, M. Ikeda, S. C. Ray, M. Gale, Jr., and S. M. Lemon. 2005. Immune evasion by hepatitis C virus NS3/ 4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA 102: 2992-2997.
22. Foy, E., K. Li, C.Wang, R. Sumpter, Jr., M. Ikeda, S. M. Lemon, and M. Gale, Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300: 1145-1148.
23. Lin, W., S. S. Kim, E. Yeung, Y. Kamegaya, J. T. Blackard, K. A. Kim, M. J. Holtzman, and R. T. Chung. 2006. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J. Virol. 80: 9226-9235.
24. Polyak, S. J., K. S. Khabar, D. M. Paschal, H. J. Ezelle, G. Duverlie, G. N. Barber, D. E. Levy, N. Mukaida, and D. R. Gretch. 2001. Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferoninduced antiviral response. J. Virol. 75: 6095-6106.
25. Gale, M. J., Jr., M. J. Korth, N. M. Tang, S. L. Tan, D. A. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230: 217-227.
26. Taylor, D. R., S. T. Shi, P. R. Romano, G. N. Barber, and M. M. Lai. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285: 107-110.
27. Missale, G., R. Bertoni, V. Lamonaca, A. Valli, M. Massari, C. Mori, M. G. Rumi, M. Houghton, F. Fiaccadori, and C. Ferrari. 1996. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J. Clin. Invest. 98: 706-714.
28. Corado, J., F. Toro, H. Rivera, N. E. Bianco, L. Deibis, and J. B. De Sanctis. 1997. Impairment of natural killer (NK) cytotoxic activity in hepatitis C virus (HCV) infection. Clin. Exp. Immunol. 109: 451-457.
29. Kiessling, R., E. Klein, H. Pross, and H. Wigzell. 1975. "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur. J. Immunol. 5: 117-121.
30. Herberman, R. B., M. E. Nunn, and D. H. Lavrin. 1975. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int. J. Cancer 16: 216-229.
31. Mondelli, M. U., S. Varchetta, and B. Oliviero. 2010. Natural killer cells in viral hepatitis: facts and controversies. Eur. J. Clin. Invest. 40: 851-863.
32. Fauci, A. S., D. Mavilio, and S. Kottilil. 2005. NK cells in HIV infection: paradigm for protection or targets for ambush. Nat. Rev. Immunol. 5: 835-843.
33. De Maria, A., F. Bozzano, C. Cantoni, and L. Moretta. 2011. Revisiting human natural killer cell subset function revealed cytolytic CD56dimCD16+ NK cells as rapid producers of abundant IFN-g on activation. Proc. Natl. Acad. Sci. USA 108: 728-732.
34. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
35. Sivori, S., M. Vitale, L. Morelli, L. Sanseverino, R. Augugliaro, C. Bottino, L. Moretta, and A. Moretta. 1997. p46, a novel natural killer cell-specific surface molecule that mediates cell activation. J. Exp. Med. 186: 1129-1136.
36. Pessino, A., S. Sivori, C. Bottino, A. Malaspina, L. Morelli, L. Moretta, R. Biassoni, and A. Moretta. 1998. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J. Exp. Med. 188: 953-960.
37. Vitale, M., C. Bottino, S. Sivori, L. Sanseverino, R. Castriconi, E. Marcenaro R. Augugliaro, L. Moretta, and A. Moretta. 1998. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in nonmajor histocompatibility complex-restricted tumor cell lysis. J. Exp. Med. 187: 2065-2072.
38. Pende, D., S. Parolini, A. Pessino, S. Sivori, R. Augugliaro, L. Morelli, E. Marcenaro, L. Accame, A. Malaspina, R. Biassoni, et al. 1999. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J. Exp. Med. 190: 1505-1516.
39. Wu, J., Y. Song, A. B. Bakker, S. Bauer, T. Spies, L. L. Lanier, and J. H. Phillips. 1999. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285: 730-732.
40. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. López-Botet, and D. E. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95: 5199-5204.
41. Arnon, T. I., H. Achdout, O. Levi, G. Markel, N. Saleh, G. Katz, R. Gazit, T. Gonen-Gross, J. Hanna, E. Nahari, et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat. Immunol. 6: 515-523.
42. Khakoo, S. I., C. L. Thio, M. P. Martin, C. R. Brooks, X. Gao, J. Astemborski, J. Cheng, J. J. Goedert, D. Vlahov, M. Hilgartner, et al. 2004. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305: 872-874.
43. Alter, G., S. Jost, S. Rihn, L. L. Reyor, B. E. Nolan, M. Ghebremichael, R. Bosch, M. Altfeld, and G. M. Lauer. 2011. Reduced frequencies of NKp30+ NKp46+, CD161+, and NKG2D+ NK cells in acute HCV infection may predict viral clearance. J. Hepatol. 55: 278-288.
44. Oliviero, B., S. Varchetta, E. Paudice, G. Michelone, M. Zaramella, D. Mavilio, F. De Filippi, S. Bruno, and M. U. Mondelli. 2009. Natural killer cell functional dichotomy in chronic hepatitis B and chronic hepatitis C virus infections. Gastroenterology 137: 1151-1160.
45. Ahlenstiel, G., R. H. Titerence, C. Koh, B. Edlich, J. J. Feld, Y. Rotman, M. G. Ghany, J. H. Hoofnagle, T. J. Liang, T. Heller, and B. Rehermann. 2010. Natural killer cells are polarized toward cytotoxicity in chronic hepatitis C in an interferon-alfa-dependent manner. Gastroenterology 138: 325-335.
46. Meier, U. C., R. E. Owen, E. Taylor, A. Worth, N. Naoumov, C. Willberg, K. Tang, P. Newton, P. Pellegrino, I. Williams, et al. 2005. Shared alterations in NK cell frequency, phenotype, and function in chronic human immunodeficiency virus and hepatitis C virus infections. J. Virol. 79: 12365-12374.
47. Nattermann, J., G. Feldmann, G. Ahlenstiel, B. Langhans, T. Sauerbruch, and U. Spengler. 2006. Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut 55: 869-877.
48. Crotta, S., A. Stilla, A. Wack, A. D'Andrea, S. Nuti, U. D'Oro, M. Mosca, F. Filliponi, R. M. Brunetto, F. Bonino, et al. 2002. Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J. Exp. Med. 195: 35-41.
49. Tseng, C. T., and G. R. Klimpel. 2002. Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer cell functions. J. Exp. Med. 195: 43-49.
50. Yoon, J. C., M. Shiina, G. Ahlenstiel, and B. Rehermann. 2009. Natural killer cell function is intact after direct exposure to infectious hepatitis C virions. Hepatology 49: 12-21.
51. Varchetta, S., D. Mele, S. Mantovani, B. Oliviero, E. Cremonesi, S. Ludovisi, G. Michelone, M. Alessiani, R. Rosati, M. Montorsi, and M. U. Mondelli. 2012. Impaired intrahepatic natural killer cell cytotoxic function in chronic hepatitis C virus infection. Hepatology 56: 841-849.
52. Yoon, J. C., J. B. Lim, J. H. Park, and J. M. Lee. 2011. Cell-to-cell contact with hepatitis C virus-infected cells reduces functional capacity of natural killer cells. J. Virol. 85: 12557-12569.
53. Wakita, T., T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Kräusslich, M. Mizokami, et al. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11: 791-796.
54. Zhong, J., P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita, and F. V. Chisari. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102: 9294-9299.
55. Russell, R. S., J. C. Meunier, S. Takikawa, K. Faulk, R. E. Engle, J. Bukh, R. H. Purcell, and S. U. Emerson. 2008. Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Proc. Natl. Acad. Sci. USA 105: 4370-4375.
56. Jones, D. M., A. M. Atoom, X. Zhang, S. Kottilil, and R. S. Russell. 2011. A genetic interaction between the core and NS3 proteins of hepatitis C virus is essential for production of infectious virus. J. Virol. 85: 12351-12361.
57. Parsons, M. S., K. Zipperlen, M. Gallant, and M. Grant. 2010. Killer cell immunoglobulin-like receptor 3DL1 licenses CD16-mediated effector functions of natural killer cells. J. Leukoc. Biol. 88: 905-912.
58. Owsianka, A., A. W. Tarr, V. S. Juttla, D. Lavillette, B. Bartosch, F. L. Cosset, J. K. Ball, and A. H. Patel. 2005. Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J. Virol. 79: 11095-11104.
59. Tarr, A. W., A. M. Owsianka, J. M. Timms, C. P. McClure, R. J. Brown, T. P. Hickling, T. Pietschmann, R. Bartenschlager, A. H. Patel, and J. K. Ball. 2006. Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology 43: 592-601.
60. Nattermann, J., H. D. Nischalke, V. Hofmeister, G. Ahlenstiel, H. Zimmermann, L. Leifeld, E. H. Weiss, T. Sauerbruch, and U. Spengler. 2005. The HLA-A2 restricted T cell epitope HCV core 35-44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am. J. Pathol. 166: 443-453.
61. Wang, R., J. J. Jaw, N. C. Stutzman, Z. Zou, and P. D. Sun. 2012. Natural killer cell-produced IFN-g and TNF-a induce target cell cytolysis through upregulation of ICAM-1. J. Leukoc. Biol. 91: 299-309.
62. Bozzano, F., A. Picciotto, P. Costa, F. Marras, V. Fazio, I. Hirsch, D. Olive, L. Moretta, and A. De Maria. 2011. Activating NK cell receptor expression/ function (NKp30, NKp46, DNAM-1) during chronic viraemic HCV infection is associated with the outcome of combined treatment. Eur. J. Immunol. 41: 2905-2914.
63. Ahlenstiel, G., B. Edlich, L. J. Hogdal, Y. Rotman, M. Noureddin, J. J. Feld, L. E. Holz, R. H. Titerence, T. J. Liang, and B. Rehermann. 2011. Early changes in natural killer cell function indicate virologic response to interferon therapy for hepatitis C. Gastroenterology 141: 1231-1239.
64. Mondelli, M. U., B. Oliviero, D. Mele, S. Mantovani, C. Gazzabin, and S. Varchetta. 2012. Natural killer cell functional dichotomy: a feature of chronic viral hepititis? Front. Immunol. 3: 351.
65. Nellore, A., and J. A. Fishman. 2011. NK cells, innate immunity and hepatitis C infection after liver transplantation. Clin. Infect. Dis. 52: 369-377.
66. Dustin, L. B., and C. M. Rice. 2007. Flying under the radar: the immunobiology of hepatitis C. Annu. Rev. Immunol. 25: 71-99.
67. Golden-Mason, L., and H. R. Rosen. 2006. Natural killer cells: primary target for hepatitis C virus immune evasion strategies? Liver Transpl. 12: 363-372.
68. Crotta, S., V. Ronconi, C. Ulivieri, C. T. Baldari, N. M. Valiante, S. Abrignani, and A. Wack. 2006. Cytoskeleton rearrangement induced by tetraspanin engagement modulates the activation of T and NK cells. Eur. J. Immunol. 36: 919-929.
69. Vivier, E., J. A. Nunès, and F. Vély. 2004. Natural killer cell signaling pathways. Science 306: 1517-1519.
70. Stamper, C. C., Y. Zhang, J. F. Tobin, D. V. Erbe, S. Ikemizu, S. J. Davis, M. L. Stahl, J. Seehra, W. S. Somers, and L. Mosyak. 2001. Crystal structure of the B7-1/CTLA-4 complex that inhibits human immune responses. Nature 410: 608-611.
71. Schwartz, J. C., X. Zhang, A. A. Fedorov, S. G. Nathenson, and S. C. Almo. 2001. Structural basis for co-stimulation by the human CTLA-4/B7-2 complex. Nature 410: 604-608.
72. Lin, D. Y., Y. Tanaka, M. Iwasaki, A. G. Gittis, H. P. Su, B. Mikami, T. Okazaki, T. Honjo, N. Minato, and D. N. Garboczi. 2008. The PD-1/PD-L1 complex resembles the antigen-binding Fv domains of antibodies and T cell receptors. Proc. Natl. Acad. Sci. USA 105: 3011-3016.
73. Brandt, C. S., M. Baratin, E. C. Yi, J. Kennedy, Z. Gao, B. Fox, B. Haldeman, C. D. Ostrander, T. Kaifu, C. Chabannon, et al. 2009. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 206: 1495-1503.
74. Joyce, M. G., P. Tran, M. A. Zhuravleva, J. Jaw, M. Colonna, and P. D. Sun. 2011. Crystal structure of human natural cytotoxicity receptor NKp30 and identification of its ligand binding site. Proc. Natl. Acad. Sci. USA 108: 6223-6228.
75. Li, Y., Q. Wang, and R. A. Mariuzza. 2011. Structure of the human activating natural cytotoxicity receptor NKp30 bound to its tumor cell ligand B7-H6. J. Exp. Med. 208: 703-714.
76. Zou, W., and L. Chen. 2008. Inhibitory B7-family molecules in the tumour microenvironment. Nat. Rev. Immunol. 8: 467-477.