Underwhelming the Immune Response: Effect of Slow Virus Growth on CD8 +-T-Lymphocyte Responses

Journal of Virology

Volumn 78, Issue 5, 2004, Pages 2247-2254

  Bocharov, Gennady ^a,d,h   Ludewig, Burkhard ^e,g   Bertoletti, Antonio ^b   Klenerman, Paul ^c   Junt, Tobias ^e   Krebs, Philippe ^e,h   Luzyanina, Tatyana ^f   Fraser, Cristophe ^a   Anderson, Roy M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d INSTITUTE OF NUMERICAL MATHEMATICS   (Russian Federation)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g Research Department   (Switzerland)

^h UNIVERSITY OF CHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CYTOTOXIC T LYMPHOCYTE; FLOW CYTOMETRY; HEPATITIS B VIRUS; IMMUNE RESPONSE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; HEPATITIS B VIRUS; KINETICS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MODELS, IMMUNOLOGICAL; T-LYMPHOCYTES, CYTOTOXIC; VIRUS REPLICATION;

EID: 1242319458     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.5.2247-2254.2004     Document Type: Article

References (46)

1. Altman, J. D., P. A. H. Moss, P. J. R. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94-96.
2. Bartholdy, C., J. P. Christensen, D. Wodarz, and A. R. Thomsen. 2000. Persistent virus infection despite chronic cytotoxic-T-lymphocyte activation in gamma interferon-deficient mice infected with lymphocytic choriomeningitis virus. J. Virol. 74:10304-10311.
3. Battegay, M., S. Cooper, A. Althage, J. Banziger, H. Hengartner, and R. M. Zinkernagel. 1991. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33:191-198.
4. Bell, G. I. 1973. Predator-prey equations simulating an immune response. Math. Biosci. 16:291-314.
5. Bigger, C. B., K. M. Brasky, and R. E. Lanford. 2001. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J. Virol. 75:7059-7066.
6. Brechot, C., V. Thiers, D. Kremsdorf, B. Nalpas, S. Pol, and P. Paterlini-Brechot. 2001. Persistent hepatitis B virus infection in subjects without hepatitis B surface antigen: clinically significant or purely "occult"? Hepatology 34:194-203.
7. Brundler, M. A., P. Aichele, M. Bachmann, D. Kitamura, K. Rajewsky, and R. M. Zinkernagel. 1996. Immunity to viruses in B cell-deficient mice: influence of antibodies on virus persistence and on T cell memory. Eur. J. Immunol. 26:2257-2262.
8. Chisari, F. V. 1997. Cytotoxic T cells and viral hepatitis. J. Clin. Investig. 99:1472-1477.
9. Chisari, F. V., and C. Ferrari. 1995. Hepatitis B virus immunopathogenesis. Annu. Rev. Immunol. 13:29-60.
10. Cooper, S., A. L. Erickson, E. J. Adams, J. Kansopon, A. J. Weiner, D. Y. Chien, M. Houghton, P. Parham, and C. M. Walker. 1999. Analysis of a successful immune response against hepatitis C virus. Immunity 10:439-449.
11. Doherty, P. C., and J. P. Christensen. 2000. Accessing complexity: the dynamics of virus-specific T cell responses. Annu. Rev. Immunol. 18:561-592.
12. Ehl, S., P. Klenerman, R. M. Zinkernagel, and G. Bocharov. 1998. The impact of variation in the number of CD8(+) T-cell precursors on the outcome of virus infection. Cell Immunol. 189:67-73.
13. Farci, P., S. J. Munoz, A. Shimoda, S. Govindarajan, D. C. Wong, A. Coiana, G. Peddis, R. Rubin, and R. H. Purcell. 1999. Experimental transmission of hepatitis C virus-associated fulminant hepatitis to a chimpanzee. J. Infect. Dis. 179:1007-1011.
14. Farci, P., A. Shimoda, A. Coiana, G. Diaz, G. Peddis, J. C. Melpolder, A. Strazzera, D. Y. Chien, S. J. Munoz, A. Balestrieri, R. H. Purcell, and H. J. Alter. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339-344.
15. Forns, X., R. Thimme, S. Govindarajan, S. U. Emerson, R. H. Purcell, F. V. Chisari, and J. Bukh. 2000. Hepatitis C virus lacking the hypervariable region I of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proc. Natl. Acad. Sci. USA 97:13318-13323.
16. Germain, R. N. 2001. The art of the probable: system control in the adaptive immune system. Science 293:240-245.
17. Grossman, Z. 1984. Recognition of self and regulation of specificity at the level of cell populations. Immunol. Rev. 79:119-138.
18. Grossman, Z. 1993. Cellular tolerance as a dynamic state of the adaptable lymphocyte. Immunol. Rev. 133:45-73.
19. Grossman, Z., and G. Berke. 1980. Tumor escape from immune elimination. J. Theor. Biol. 83:267-296.
20. Grossman, Z., and W. E. Paul. 2000. Self-tolerance: context dependent tuning of T cell antigen recognition. Semin. Immunol. 12:197-203.
21. Guidotti, L. G., and F. V. Chisari. 1996. To kill or to cure: options in host defense against viral infection. Curr. Opin. Immunol. 8:478-483.
22. Hassell, M. P. 2000. The spatial and temporal dynamics of host-parasitoid interactions. Oxford University Press, Oxford, United Kingdom.
23. He, X. S., B. Rehermann, F. X. Lopez-Labrador, J. Boisvert, R. Cheung, J. Mumm, H. Wedemeyer, M. Berenguer, T. L. Wright, M. M. Davis, and H. B. Greenberg. 1999. Quantitative analysis of hepatitis C virus-specific CD8(+) T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA 96:5692-5697.
24. Kantzanou, M., M. Lucas, E. Barnes, H. Komatsu, G. Dusheiko, S. Ward, G. Harcourt, and P. Klenerman. 2003. Viral escape and T cell exhaustion in hepatitis C virus infection analysed using Class I peptide tetramers. Immunol. Lett. 85:165-171.
25. Klein, G. 1976. Mechanisms of escape from immune surveillance. Natl. Cancer Inst. Monogr. 44:135-136.
26. Komarova, N. L., E. Barnes, P. Klenerman, and D. Wodarz. 2003. Boosting immunity by antiviral drug therapy: a simple relationship among timing, efficacy, and success. Proc. Natl. Acad. Sci. USA 100:1855-1860.
27. Lechner, F., N. H. Gruener, S. Urbani, J. Uggeri, T. Santantonio, A. R. Kammer, A. Cerny, R. Phillips, C. Ferrari, G. R. Pape, and P. Klenerman. 2000. CD8+ T lymphocyte responses are induced during acute hepatitis C virus infection but are not sustained. Eur. J. Immunol. 30:2479-2487.
28. Lechner, F., D. K. Wong, P. R. Dunbar, R. Chapman, R. T. Chung, P. Dohrenwend, G. Robbins, R. Phillips, P. Klenerman, and B. D. Walker. 2000. Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 191:1499-1512.
29. Maini, M. K., C. Boni, C. K. Lee, J. R. Larrubia, S. Reignat, G. S. Ogg, A. S. King, J. Herberg, R. Gilson, A. Alisa, R. Williams, D. Vergani, N. V. Naoumov, C. Ferrari, and A. Bertoletti. 2000. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191:1269-1280.
30. May, R. M. 2001. Stability and complexity in model ecosystems. Princeton University Press, Princeton, N.J.
31. Moskophidis, D., M. Battegay, M. A. Bruendler, E. Laine, I. Gresser, and R. M. Zinkernagel. 1994. Resistance of lymphocytic choriomeningitis virus to alpha/beta interferon and to gamma interferon. J. Virol. 68:1951-1955.
32. Moskophidis, D., F. Lechner, H. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362:758-761.
33. Nisbet, R. M., and W. S. C. Gurney. 1982. Modelling fluctuating populations. John Wiley & Sons, New York, N.Y.
34. Nowak, M. A., and R. M. May. 2000. Virus dynamics. Oxford University Press, Oxford, United Kingdom.
35. Riviere, Y., R. Ahmed, P. J. Southern, M. J. Buchmeier, and M. B. Oldstone. 1985. Genetic mapping of lymphocytic choriomeningitis virus pathogenicity: virulence in guinea pigs is associated with the L RNA segment. J. Virol. 55:704-709.
36. Seiler, P., M. A. Brundler, C. Zimmermann, D. Weibel, M. Bruns, H. Hengartner, and R. M. Zinkernagel. 1998. Induction of protective cytotoxic T cell responses in the presence of high titers of virus-neutralizing antibodies: implications for passive and active immunization. J. Exp. Med. 187:649-654.
37. Su, A. I., J. P. Pezacki, L. Wodicka, A. D. Brideau, L. Supekova, R. Thimme, S. Wieland, J. Bukh, R. H. Purcell, P. G. Schultz, and F. V. Chisari. 2002. Genomic analysis of the host response to hepatitis C virus infection. Proc. Natl. Acad. Sci. USA 99:15669-15674.
38. Thimme, R., J. Bukh, H. C. Spangenberg, S. Wieland, J. Pemberton, C. Steiger, S. Govindarajan, R. H. Purcell, and F. V. Chisari. 2002. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc. Natl. Acad. Sci. USA 99:15661-15668.
39. Thimme, R., D. Oldach, K. M. Chang, C. Steiger, S. C. Ray, and F. V. Chisari. 2001. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194:1395-1406.
40. Venzon, D. J., and S. H. Moogavkor. 1988. A method for computing profile-likelihood-based confidence intervals. Appl. Statistician 37:87-94.
41. Volterra, V. 1979. Variations and fluctuations in the numbers of co-existing animal species, p. 65-236. In F. M. Scudo and J. R. Ziegler (ed.), The golden age of theoretical biology 1923-1940. Springer, Berlin, Germany.
42. Webster, G. J., S. Reignat, M. K. Maini, S. A. Whalley, G. S. Ogg, A. King, D. Brown, P. L. Amlot, R. Williams, D. Vergani, G. M. Dusheiko, and A. Bertoletti. 2000. Incubation phase of acute hepatitis B in man: dynamic of cellular immune mechanisms. Hepatology 32:1117-1124.
43. Weiner, A. J., X. Paliard, M. J. Selby, A. Medina-Selby, D. Coit, S. Nguyen, J. Kansopon, C. L. Arian, P. Ng, J. Tucker, C. T. Lee, N. K. Polakos, J. Han, S. Wong, H. H. Lu, S. Rosenberg, K. M. Brasky, D. Chien, G. Kuo, and M. Houghton. 2001. Intrahepatic genetic inoculation of hepatitis C virus RNA confers cross-protective immunity. J. Virol. 75:7142-7148.
44. Whalley, S. A., J. M. Murray, D. Brown, G. J. Webster, V. C. Emery, G. M. Dusheiko, and A. S. Perelson. 2001. Kinetics of acute hepatitis B virus infection in humans. J. Exp. Med. 193:847-854.
45. Zinkernagel, R. M. 2000. Localization dose and time of antigens determine immune reactivity. Semin. Immunol. 12:163-171.
46. Zinkernagel, R. M., and H. Hengartner. 2001. Regulation of the immune response by antigen. Science 293:251-253.