Subversion of effector CD8+ T cell differentiation in acute hepatitis C virus infection: The role of the virus

European Journal of Immunology

Volumn 34, Issue 2, 2004, Pages 438-446

  Accapezzato, Daniele ^a   Francavilla, Vittorio ^a   Rawson, Pisana ^a   Cerino, Antonella ^b   Cividini, Agostino ^b   Mondelli, Mario U ^b   Barnaba, Vincenzo ^a,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c Pasteur Institute   (Italy)

Author keywords

CTL; Effector cells; Immune subversion; Memory cells; Virus

Indexed keywords

CD8 ANTIGEN; CORE PROTEIN; INTERLEUKIN 2; CC CHEMOKINE RECEPTOR 7; CHEMOKINE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NUCLEOCAPSID PROTEIN, HEPATITIS C VIRUS;

ADULT; AGED; ARTICLE; CASE REPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; MALE; MEMORY CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIRUS CORE; ACUTE DISEASE; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; VIROLOGY;

ACUTE DISEASE; ADULT; AGED; CELL DIFFERENTIATION; FEMALE; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-2; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHORYLATION; RECEPTORS, CHEMOKINE; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY; VIRAL CORE PROTEINS;

EID: 1642286866     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324540     Document Type: Article

References (52)

1. Sprent, J. and Surh, C. D., T cell memory. Annu. Rev. Immunol. 2002. 20: 551-579.
2. Kaech, S. M., Wherry, E. J. and Ahmed, R., Effector and memory T cell differentiation: implication for vaccine development. Nat. Rev. Immunol. 2002. 2: 251-262.
3. Sallusto, F., Lenig, D., Forster, R., Lipp, M. and Lanzavecchia, A., Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999. 401: 708-712.
4. Badovinac, V. P., Porter, B. B. and Harty, J. T., Programmed contraction of CD8+ T cells after infection. Nat. Immunol. 2002. 3: 619-626.
5. Wherry, E. J., Teichgraber, V., Becker, T. C., Masopust, D., Kaech, S. M., Antia, R., von Andrian, U. H. and Ahmed, R., Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 2003. 4: 225-234.
6. Reinhardt, R. L., Khoruts, A., Merica, R., Zell, T. and Jenkins, M. K., Visualizing the generation of memory CD4 T cells in the whole body. Nature 2001. 410: 101-105.
7. Masopust, D., Vezys, V., Marzo, A. L. and Lefrancois, L., Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001. 291: 2413-2417.
8. Lanzavecchia, A. and Sallusto, F., Dynamics of T lymphocyte responses: intermediates, effectors and memory cells. Science 2000. 290: 92-97.
9. Weninger, W., Crowley, M. A., Manjunath, N. and von Andrian, U. H., Migratory properties of naive, effector, and memory CD8+ T cells. J. Exp. Med. 2001. 194: 953-966.
10. Lanzavecchia, A. and Sallusto, F., Antigen decoding by T lymphocytes: from synapses to fate determination. Nat. Immunol. 2001. 2: 487-492.
11. Manjunath, N., Shankar, P., Wan, J., Weninger, W., Crowley, M. A., Hieshima, K., Springer, T. A., Fan, X., Shen, H., Lieberman, J. and von Andrian, U. H., Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J. Clin. Invest. 2001. 108: 871-878.
12. Lauvau, G., Vijh, S., Kong, P., Horng, T., Kerksiek, K., Serbina, N., Tuma, R. A. and Pamer, E. G., Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science 2001. 294: 1735-1739.
13. Goldrath, A. W., Sivakumar, P. V., Glaccum, M., Kennedy, M. K., Bevan, M. J., Benoist, C., Mathis, D. and Butz, E. A., Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J. Exp. Med. 2002. 195: 1515-1522.
14. Tan, J. T., Ernst, B., Kieper, W. C., LeRoy, E., Sprent, J. and Surh, C. D., Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phentype CD4+ cells. J. Exp. Med. 2002. 195: 1523-1532.
15. Kieper, W. C., Tan, J. T., Bondi-Boyd, B., Gapin, L., Sprent, J., Ceredig, R. and Surh, C. D., Overexpression of interleukin (IL)-7 leads to IL-15-independent generation of memory phenotype CD8+ T cells. J. Exp. Med. 2002. 195: 1533-1539.
16. Becker, T. C., Wherry, E. J., Boone, D., Murali-Krishna, K., Antia, R., Ma, A. and Ahmed, R., Interleukin 15 is required for proliferation renewal of virus-specific memory CD8 T cells. J. Exp. Med. 2002. 195: 1541-1548.
17. Hernandez, J., Aung, S., Marquardt, K. and Sherman, L. A., Uncoupling of proliferative potential and gain of effector function by CD8+ T cells responding to self-antigens. J. Exp. Med. 2002. 3: 323-333.
18. Gett, A. V., Sallusto, F., Lanzavecchia, A. and Geginat, J., T cell fitness determined by signal strength. Nat. Immunol. 2003. 4: 355-360.
19. von Stipdonk, M. J. B., Hardenberg, G., Bijker, M. S., Lemmens, E. E., Droin, N. M., Green, D. R. and Schoenberger, S. P., Dynamic programming of CD8+ T lymphocyte response. Nat. Immunol. 2003. 4: 361-365.
20. Schwartz, R. H., T cell anergy. Annu. Rev. Immunol. 2003. 21: 305-334.
21. Tortorella, D., Gewurz, B. E., Furman, M. H., Schust D. J. and Ploegh, H. L., Viral subversion of the immune system. Annu. Rev. Immunol. 2000. 18: 861-926.
22. Lauer, G. M. and Walker, B. D., Hepatitis C virus infection. N. Engl. J. Med. 2001. 345: 41-52.
23. Cooper, S., Erickson, A. L., Adams, E. J., Kansopon, J., Weiner, A. J., Chien, D. Y., Houghton, M., Parham, P. and Walker, C. M., Analysis of a successful immune response against hepatitis C virus. Immunity 1999. 10: 439-449.
24. Prezzi, C., Casciaro, M. A., Francavilla, V., Schiaffella, E., Finocchi, L., Chircu, L. V., Bruno, G., Sette, A., Abrignani, S. and Barnaba, V., Virus-specific CD8(+) T cells with type 1 or type 2 cytokine profile are related to different disease activity in chronic hepatitis C virus infection. Eur. J. Immunol. 2001. 31: 894-906.
25. He, X. S., Rehermann, B., Lopez-Labrador, F. X., Boisvert, J., Cheung, R., Mumm, J., Wedemeyer, H., Berenguer, M., Wright, T. L., Davis, M. M. and Greenberger, H. B., Quantitative analysis of hepatitis C virus-specific CD8(+) T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA 1999. 96: 5692-5697.
26. Lechner, F., Wong, D. K., Dunbar, P. R., Chapman, R., Chung, R. T., Dohrenwend, P., Robbins, G., Phillips, R., Klenerman, P. and Walker, B. D., Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 2000. 191: 1499-1512.
27. Thimme, R., Oldach, D., Chang, K. M., Steiger, C., Ray, S. C. and Chisari, F. V., Determinants of viral clearance and persistence during acute hepatitis C infection. J. Exp. Med. 2001. 194: 1395-1406.
28. Lechner, F., Gruener, N. H., Urbani, S., Uggeri, J., Santantonio, T., Kammer, A. R., Cerny, A., Phillips, R., Ferrari, C., Pape, G. R. and Klenerman, P., CD8+ T lymphocytes responses are induced during acute hepatitis C virus infection but are not sustained. Eur. J. Immunol. 2000. 30: 2479-2487.
29. Gruener, N. H., Lechner, F., Jung, M.-C., Diepolder, H., Gerlach, T., Lauer, G., Walker, B., Sullivan, J., Phillips, R., Pape, G. R. and Klenerman, P., Sustained, dysfunction of antiviral CD8+ T lymphocytes after infection with hepatitis C virus. J. Virol. 2001. 75: 5550-5558.
30. Lauer, G. M., Ouchi, K., Chung, R. T., Nguyen, T N., Day, C. L., Purkis, D. R., Reiser, M., Kim, A. Y., Lucas, M., Klenerman, P. and Walker, B. D., Comprehensive analysis of CD8+-T cell responses against hepatitis C virus reveals multiple unpredicted specificities. J. Virol. 2002. 76: 6104-6113.
31. Urbani, S., Boni, C., Missale, G., Elia, G., Cavallo, C., Massari, M., Raimondo, G. and Ferrari, C., Virus-specific CD8+ lymphocytes share the same effector-memory phenotype but exhibit functional differences in acute hepatitis B and C. J. Virol. 2002. 76: 12423-12434.
32. Scognamiglio, P., Accapezzato, D., Casciaro, M. A., Cacciani, A., Artini, M., Bruno, G., Chircu, M. L., Sidney, J., Southwood, S., Abrignani, S. and Barnaba, V., Presence of effector CD8+ T cells in hepatitis C virus-exposed healthy seronegative donors. J. Immunol. 1999. 162: 6681-6689.
33. Appay, V., Dunbar, P. R., Callan, M., Klenerman, P., Gillespie, G. M. A., Papagno, L., Ogg, G. S., King, A., Lechner, F., Spina, C. A., Little, S., Havlir, D. V., Richman, D. D., Gruener, N., Pape, G., Waters, A., Easterbrook, P., Salio, M., Cerundolo, V., McMichael, A. J. and Rowland-Jones, S. L., Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 2002. 8: 379-385.
34. Champagne, P., Ogg, G. S., King, A. S., Knabenhans, C., Ellefsen, K., Nobile, M., Appay, V., Rizzardi G. P., Fleury, S., Lipp, M., Forster, R., Rowland-Jones, S., Sekaly, R. P., McMichael, A. J. and Pantaleo, G., Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 2001. 410: 106-111.
35. Kittlesen, D. J., Chianese-Bullick, K. A., Yao, Z. Q., Braciale, T. J. and Hahn, Y. S., Interaction between complement receptor gC1qR and hepatitis C virus core protein inhibits T-lymphocyte proliferation. J. Clin. Invest. 2000. 106: 1239-1249.
36. Yao, Z. Q., Nguyen, D. T., Hiotellis, A. I. and Hahn, Y. S., Hepatitis C virus core protein inhibits human T lymphocyte responses by a complement-dependent regulatory pathway. J. Immunol. 2001. 167: 5264-5272.
37. Maillard, P., Krawczynski, K., Nitkiewicz, J., Bronnert, C., Sidorkiewicz, M., Gounon, P., Dubuisson, J., Faure, G., Crainic, R. and Budkowska, A., Non-enveloped nucleocapsids of hepatitis C virus in the serum of infected patients. J. Virol. 2001. 75: 8240-8250.
38. McLauchlan, J., Properties of the hepatitis C virus core protein: a structural protein that modulates cellular processes. J. Viral Hepat. 2000. 7: 2-14.
39. Matsumoto, M., Hsieh, T.-Y., Zhu, N., VanArsdale, T., Hwang, S. B., Jeng, K.-S., Gorbalenya, A. E., Lo, S.-Y., Ou, J.-H., Ware, C. F. and Lai, M. M. C., Hepatitis C virus core protein interacts with the cytoplasmic tail of lymphotoxin-β receptor. J. Virol. 1997. 71: 1301-1309.
40. Zhu, N., Khoshnan, R., Schneider, R., Matzsumoto, M., Dennert, G., Ware, C. and Lai, M. M. C., Hepatitis C virus core protein binds with the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J. Virol. 1998. 72: 3691-3697.
41. Yoshida, T., Hanada, T., Tokuhisa, T., Kosai, K., Sata, M., Kohara, M. and Yoshimura, A., Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation. J. Exp. Med. 2002. 196: 641-653.
42. Propato, A., Cutrona, G., Francavilla, V., Ulivi, M., Schiaffella, E., Landt, O., Dunbar, R., Cerundolo, V., Ferrarini, M. and Barnaba, V., Apoptotic cells overexpress vinculin and induce vinculin-specific cytotoxic T cell cross-priming. Nat. Med. 2001. 7: 807-813.
43. Kanto, T., Hayashi, N., Takehara, T., Tatsumi, T., Kuzushita, N., Ito, A., Sasaki, Y., Kasahara, A. and Hori, M., Impaired allostimulatory capacity of peripheral blood dendritic cells recovered from hepatitis C virus-infected individuals. J. Immunol. 1999. 162: 5584-5591.
44. Auffermann-Gretzinger, S., Keeffe, E. B. and Levy, S., Impaired dendritic cell maturation in patients with chronic, but not resolved, hepatitis C virus infection. Blood 2001. 97. 3171-3176.
45. Farci, P., Shimoda, A., Coiana, A., Diaz, G., Peddis, G., Melpolder, J. C., Strazzera, A., Chien, D. Y., Munoz, S. J., Balestrieri, A., Purcell, R. H. and Alter, H. J., The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 2000. 288: 339-344.
46. Erickson, A. L., Kimura, Y., Igarashi, S., Eichelberger, J., Houghton, M., Sidney, J., McKinney, D., Sette, A., Hughes, A. L. and Walker, C. M., The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity 2001. 15: 883-895.
47. Cividini, A., Muzzi, A., Furione, M., Rebucci, C., Segagni, L., Gatti, M., Barnaba, V. and Mondelli, M. U., Kinetics and significance of serum hepatitis C virus core antigen in patients with acute hepatitis C. J. Clin. Microbiol. 2003. 41: 2144-2147.
48. Moskophidis, D., Lechner, F., Pircher, H. and Zinkernagel, R. M., Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 1993. 362: 758-761.
49. Zajac, A. J., Blattman, J. N., Murali-Krishna, K., Sourdive, D. J., Suresh, M., Altman, J. D. and Ahmed, R., Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 1998. 188: 2205-2213.
50. Chang, J. and Braciale, T. J., Respiratory syncytial virus infection suppresses lung CD8+ T cell effector activity and peripheral CD8+ T cell memory in the respiratory tract. Nat. Med. 2002. 8: 54-60.
51. Barnaba, V., Franco, A., Alberti, A., Benvenuto, R. and Balsano, F., Selective killing of hepatitis B envelope antigen-specific B cells by class I-restricted, exogenous Antigen-specific T lymphocytes. Nature 1990. 345: 258-260.
52. Cerino, A., Boender, P., La Monica, N., Rosa, C., Habets W. and Mondelli, M. U., A human monoclonal antibody specific for the N terminus of the hepatitis C virus nucleocapsid protein. J. Immunol. 1993. 151: 7005-7015.