Modelling the dynamics of LCMV infection in mice: Conventional and exhaustive CTL responses

Journal of Theoretical Biology

Volumn 192, Issue 3, 1998, Pages 283-308

  Bocharov, G A ^a,b  

^a INSTITUTE OF NUMERICAL MATHEMATICS   (Russian Federation)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIGEN;

APOPTOSIS; ARTICLE; CLONAL ANERGY; CYTOTOXIC T LYMPHOCYTE; DYNAMICS; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MATHEMATICAL MODEL; MODEL; PHENOTYPE; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; SPLEEN; VIRUS CELL INTERACTION; VIRUS INFECTION;

CHORIOMENINGITIS VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; RNA VIRUSES;

EID: 0032493166     PISSN: 00225193     EISSN: None     Source Type: Journal    
DOI: 10.1006/jtbi.1997.0612     Document Type: Article

References (85)

1. AHMED, R., HAHN, C. S., SOMASUNDARAM, T., VILLARETE, L., MATLOUBIAN, M. & STRAUSS, J. H. (1991). Molecular basis of organ-specific selection of viral variants during chronic infection. J. Virol. 65, 4242-4227.
2. AICHELE, P., BRDUSHA-RIEM, K., ZINKERNAGEL, R. M., HENGARTNER, H. & PIRCHER, H. (1995). T cell priming versus T cell tolerance induced by synthetic peptides. J. Exp. Med. 182, 261-266.
3. BACHMAN, M. F., KUNDIG, T. M., KALBERER, C. P., HENGARTNER, H. & ZINKERNAGEL, R. M. (1994). How many specific B cells are needed to protect against a virus? J. Immunol. 152, 4235-4241.
4. BAKER, C. T. H., BOCHAROV, G. A. & PAUL, C. A. H. (1997). Mathematical modelling of the interleukin-2 T-cell system: a comparative study of approaches based on ordinary and delay differential equations. J. Theor. Medicine 2, 117-128.
5. BATTEGAY, M., COOPER, S., ALTHAGE, A., BANZIGER, J., HENGARTNER, H. & ZINKERNAGEL, R. M. (1991). Quantitation of lymphocytic choriomeningitis virus with an immunological focus assay in 24-or 96-well plates. J. Virological Methods 33, 191-198.
6. BELL, G. I. (1970). Mathematical model of clonal selection and antibody production. J. theor. Biol. 29, 191-232.
7. BELL, G. I. (1971). Mathematical model of clonal selection and antibody production. III - The cellular basis of immunological paralysis. J. theor. Biol. 33, 379-398.
8. BELL, G. I. (1978). Lymphocyte traffic patterns and cell-cell interactions. In: Theoretical Immunology (Bell, G. I., Perelson, A. S. & Pimbley, G., eds), pp. 341-375. New York: Marcel Dekker.
9. BISHOP, D. H. L. (1990). Arenaviridae and their replication. In: Virology, 2nd edn (Fields, B. N. & Knipe, D. M., eds), pp. 1231-1243. New York: Raven Press.
10. BOCHAROV, G. A. & ROMANYUKHA, A. A. (1994a). Mathematical model of antiviral immune response. III - Influenza A virus infection. J. theor. Biol. 167, 323-360.
11. BOCHAROV, G. A. & ROMANYUKHA, A. A. (1994b). Numerical treatment of the parameter identification problem for delay-differential equations arising in immune response modelling. Appl. Num. Math. 15, 307-326.
12. COFFIN, J. M. (1995). HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267, 483-489.
13. COHN, M. & LANGMAN, R. E. (1990). The protecton: the unit of humoral immunity selected by evolution. Immun. Rev. 115, 11-142.
14. COLLINS, M. (1995). Potential roles of apoptosis in viral pathogenesis. Am. J. Respir. Crit. Care Med. 152, S20-S24.
15. DE BOER, R. J. & PERELSON, A. S. (1991). Size and connectivity as emergent properties of a developing immune system. J. theor. Biol. 149, 381-424.
16. DE BOER, R. J. & PERELSON, A. S. (1994). T cell repertoires and competitive exclusion. J. theor. Biol. 169, 375-390.
17. DE BOER, R. J. & PERELSON, A. S. (1995). Towards a general function describing T cell proliferation. J. theor. Biol. 175, 567-576.
18. DOHERTY, P. C. (1986). Some problem areas in the interaction between viruses and the immune system. Immun. Cell Biol. 65, 279-286.
19. DOHERTY, P. C. (1995). Immunity to viruses. The Immunologist 3, 231-233.
20. DOHERTY, P. C. & ZINKERNAGEL, R. M. (1974). T-cell mediated immunopathology in viral infections. Transpl. Rev. 19, 89-120.
21. EHL, S., KLENERMAN, P., AICHELE, P., HENGARTNER, H. & ZINKERNAGEL, R. M. (1997). A functional and kinetic comparison of antiviral effector and memory CTL populations in vivo and in vitro. Eur. J. Immunol. 27, 3404-3413.
22. + T cell precursors on the outcome of virus infection. Cellul. Immunol. (submitted).
23. FISHMAN, M. A. & PERELSON, A. S. (1995). Lymphocyte memory and affinity selection. J. theor. Biol. 173, 241-262.
24. FREITAS, A. A. & ROCHA, B. B. (1993). Lymphocyte lifespans: homeostasis, selection and competition. Immunol. Today 14, 25-29.
25. GRAY, D. (1988). Population kinetics of rat peripheral B cells. J. Exp. Med. 167, 805-816.
26. GREEN, D. & SCOTT, D. (1994). Activation-induced apoptosis in lymphocytes. Curr. Opin. Immunol. 6, 476-487.
27. HAYNES, B. F., PANTANLEO, G. & FAUCI, A. S. (1996). Toward an understanding of the correlates of protective immunity to HIV infection. Science 271, 324-328.
28. HERZ, A. V. M., BONHOEFFER, S., ANDERSON, R. M., MAY, R. M. & NOWAK, M. A. (1996). Viral dynamics in vivo: limitations on estimates of intracellular delay and virus decay. Proc. Natl Acad. Sci. USA 93, 7247-7251.
29. JERNE, N. K. (1984). Idiotypic networks and other preconceived ideas. Immun. Rev. 79, 5-24.
30. KABELITZ, D., POHL, T. & PECHHOLD, K. (1993). Activation-induced cell death (apoptosis) of mature peripheral T lymphocytes. Immunol. Today 14, 338-339.
31. KIM, D. T., ROTHBARD, J. B., BLOOM, D. D. & FATHMAN, C. G. (1996). Quantitative analysis of T cell activation. J. Immunol. 156, 2737-2742.
32. KYBURZ, D., AICHELE, P., SPEISER, D. HENGARTNER, H., ZINKERNAGEL, R. M. & PIRCHER, H. (1993). T cell immunity after a viral infection versus T cell tolerance induced by soluble viral peptides. Eur. J. Immunol. 23, 1956-1962.
33. LEHMANN-GRUBE, F. (1971). Lymphocytic Choriomeningitis Virus. New York: Springer-Verlag.
34. LEHMANN-GRUBE, F. (1988). Mechanisms of recovery from acute virus infection. In: Modern Trends in Virology (Bauer, H., Klenk, H.-D. & Scholtissek, Ch., eds), pp. 49-64. Berlin: Springer-Verlag.
35. LEHMANN-GRUBE, F., CIHAK, J., VARHO, M. & TIJERINA, R. (1982). The immune response of the mouse to lymphocytic choriomeningitis virus. II - Active suppresssion of cell-mediated immunity by infection with high virus doses. J. gen. Virol. 58, 223-235.
36. LEONARDO, M. J. (1991). Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis. Nature 353, 858-861.
37. LIBLAU, R. S., TISCH, R., SHOKAT, K., YANG, X., DUMONT, N., GOODNOW, C. C. & MCDEVITT, H. O. (1996). Intravenous injection of soluble antigen induces thymic and peripheral T-cell apoptosis. Proc. Natl. Acad. Sci. USA 93, 3031-3036.
38. MACKAY, C. R. (1993). Immunological memory. Adv. Immunol. 53, 217-265.
39. MARCHUK, G. I. (1997). Mathematical Modelling of Immune Response in Infectious Diseases. Dordrecht: Kluwer Academic Publishers.
40. MARCHUK, G. I., PETROV, R. V., ROMANYUKHA, A. A. & BOCHAROV, G. A. (1991). Mathematical model of antiviral immune response. I. J. theor. Biol. 151, 1-40.
41. MCCORMICK, J. B. (1990). Arenaviruses. In: Virology, 2nd Edn (Fields, B. N. & Knipe, D. M., eds), pp. 1245-1267. New York: Raven Press.
42. MCLEAN, A. R. (1994). Modelling T cell memory. J. theor. Biol. 170, 63-74.
43. MCLEAN, A. R., ROSADO, M. M., AGENES, F., VASCONCELLO, R. & FREITAS, A. A. (1997). Resource competition as a mechanism for B cell homeostasis. Proc. Natl Acad. Sci. USA 94, 5792-5797.
44. MIMS, C. A. (1982). The Pathogenesis of Infectious Diseases, 2nd Edn. New York: Academic Press.
45. + T cells. Eur. J. Immunol. 23, 3306-3311.
46. MOSKOPHIDIS, D., LECHER, F., PIRCHER, H. & ZINKERNAGEL, R. M. (1993b). Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362, 758-761.
47. MOSKOPHIDIS, D., BATTEGAY, M., BRUENDLER, M. A., LAINE, E., GREISSER, I. & ZINKERNAGEL, R. M. (1994a). Resistance of lymphocytic choriomeningitis virus to alpha/beta interferon and to gamma Interferon. J. Virol. 68, 1951-1955.
48. MOSKOPHIDIS, D., LECHER, F., HENGARTNER, H. & ZINKERNAGEL, R. M. (1994b). MHC class I and non-MHC-linked capacity for generating an anti-viral CTL response determines susceptibility to CTL exhaustion and establishment of virus persistence in mice. J. Immunol. 152, 4976-4983.
49. MOSKOPHIDIS, D., BATTEGAY, M., VAN DER BROEK, M., LAINE, E., HOFFMANN-ROHRER, U. & ZINKERNAGEL, R. M. (1995). Role of virus and host variables in virus persistence or immunopathological disease caused by a non-cytolytic virus. J. Gen. Virol. 76, 381-391.
50. NOWAK, M. A., ANDERSON, R. M., MCLEAN, A. R., WOLFS, T. F. W., GOUDSMIT, J. & MAY, R. M. (1991). Antigenic diversity threshold and the development of AIDS. Science 254, 963-969.
51. OHASHI, P. S., HENGARTNER, H., BATTEGAY, M., ZINKERNAGEL, R. M. & PIRCHER, H. (1994). Thymocyte selection and peripheral tolerance using the lymphocytic choriomeningitis virus as a model antigen. In: Transgenesis and Targeted Mutagenesis in Immunology, pp. 113-133. New York: Academic Press.
52. OLDSTONE, M. B. A. (1989). Viral persistence. Cell 56, 517-520.
53. OLDSTONE, M. B. A., AHMED, R., BYRNE, J., BUCHMEIER, M. J., RIVIERE, Y. & SOUTHERN, O. (1985). Virus and immune responses: lymphocytic choriomeningitic virus as a prototype model of viral pathogenesis. Br. Med. Bull. 41, 70-74.
54. PERELSON, A. S. & WEISBUCH, G. (1996). Immunology for physicists. Santa Fe Institute. Working paper/95-06-056 (submitted to the J. Modern Phys.).
55. PERELSON, A. S., NEUMANN, A. U., MARKOWITZ, M., LEONARD, J. M. & HO, D. D. (1996). HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271, 1582-1586.
56. PIRCHER, H., MULLER, K.-P., KYEWSKI, B. A. & HENGARTNER, H. (1992). Thymocytes can tolerize thymocytes by clonal deletion in vitro. Internat. Immunol. 4, 1065-1069.
57. PLANZ, O., SEILER, P., HENGARTNER, H. & ZINKERNAGEL, R. M. (1996). Specific cytotoxic T cells eliminate cells producing neutralizing antibodies. Nature 382, 726-729.
58. RAZVI, E. & WELSH, R. (1993). Programmed cell death of T lymphocytes during acute viral infections: a mechanism for virus-induced immune deficiency. J. Virol. 67, 5754-5765.
59. ROCHA, B., DAUGTIGNY, N. & PEREIRA, P. (1989). Peripheral T lymphocytes: expansion potential and homeostatic regulation of pool sizes and CD4/CD8 ratios in vivo. Eur. J. Immunol. 19, 905-911.
60. ROOST, H., CHARAN, S., GOBET, R., RUEDI, E., HENGARTNER, H., ALTHAGE, A. & ZINKERNAGEL, R. M. (1988). An acquired immune suppression in mice caused by infection with lymphocytic choriomeningitis virus. Eur. J. Immunol. 18, 511-518.
61. RUSSELL, J. H., WHITE, C. L., LOH, D. Y. & MELEEDY-REY, P. (1991). Receptor-stimulated death pathway is opened by antigen in mature T-cells. Proc. Nat. Acad. Sci. USA 88, 2151-2155.
62. SALMON, M., PILLING, D., BORTHWICK, N. J., VINER, N., JANOSSY, G., BACON, P. A. & AKBAR, A. K. (1994). The progressive differentiation of primed T cells is associated with an increasing susceptibility to apoptosis. Eur. J. Immunol. 24, 892-899.
63. SCHWEITZER, A. N., SWINTON, A. N. & ANDERSON, R. M. (1992). Complex outcomes in mouse leishmaniasis: a model for the dynamics of the Th1 response. In: Theoretical and Experimental Insights into Immunology (Perelson, A. S. & Weisbuch, G. eds) pp. 191-202. Berlin: Springer-Verlag.
64. SEBZDA, E., WALLACE, V. A., MAYER, J., YEUNG, R. S. M., MAK, T. W. & OHASHI, P. S. (1994). Positive and negative thymocyte selection induced by different concentrations of a single peptide. Science 263, 1615-1618.
65. SELIN, L. K. & WELSH, R. M. (1994). Specificity and editing by apoptosis of virus-induced cytotoxic T lymphocytes. Curr. Opin. Immunol. 6, 553-559.
66. SPRENT, J. (1995). Immunological memory. The Immunologist 3, 212-215.
67. SPRENT, J. & TOUGH, D. F. (1994). Lymphocyte life-spans and memory. Science 265, 1395-1400.
68. SPRENT, J. & WEBB, S. R. (1995). Intrathymic and extrathymic clonal deletion of T cells. Curr. Opin. Immunol. 7, 196-205.
69. SPRENT, J., GAO, E. K. & TOUGH, D. F. (1990). T cell reactivity to MHC molecules: immunity versus tolerance. Science 248, 1357-1363.
70. STEINMAN, R. M. (1991). The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9, 271-296.
71. STEWART, J. & VARELA, F. J. (1989). Exploring the meaning of connectivity in the immune network. Immunol. Rev. 110, 37-61.
72. SWAIN, S. L. (1995). The activation and differntiation of T cells. The Immunologist 3, 209-211.
73. SWAIN, S. L. & RETH, M. (1994). Lymphocyte activation and effector functions. Curr. Opin. Immun. 6, 355-358.
74. SWINTON, J., SCHWEITZER, A. N. & ANDERSON, R. M. (1994). Two signal activation as an explanation of high zone tolerance: a mathematical exploration of the nature of the second signal. J. theor. Biol. 169, 23-30.
75. THOMPSEN, A. R. & PFAU, C. (1993). Influence of host genes on the outcome of murine lymphocytic choriomeningitis virus infection. A model for studying genetic control of virus-specific immune responses. In: The Arenaviridae (Salvato, M., ed.), Chap. 12, pp. 199-224. New York: Plenum Press.
76. + T cells in an in vivo response. J. Immunol. 155, 3719-3721.
77. WEBB, S., MORRIS, C. & SPRENT, J. (1990). Extrathymic tolerance of mature T cells: clonal elimination as a consequence of immunity. Cell 63, 1249-1256.
78. WODARZ, D., KLENERMAN, P. & NOWAK, M. A. (1998) Dynamics of cytotoxic T-lymphocyte exhaustion. Proc. R. Soc. Lond. 265, 191-203.
79. ZELLER, W., BRUNS, M. & LEHMANN-GRUBE, F. (1988). Lymphocytic choriomeningitis virus. X - Demonstration of nucleoprotein of the surface of infected cells. Virol. 162, 90-97.
80. ZINKERNAGEL, R. M. (1993a). Immunity to viruses. In: Fundamental Immunology, 3rd Edn (Paul, W., ed.), Chap. 34, pp. 1211-1250. New York: Raven Press.
81. ZINKERNAGEL, R. M. (1993b). Virus-induced acquired immunosuppression by T-cell mediated immunopathology and vaccine strategies. In: The Arenaviridae (Salvato, M. ed.), Chap. 14, pp. 247-257. New York: Plenum Press.
82. ZINKERNAGEL, R. M. (1996). Immunology taught by viruses. Science 271, 173-178.
83. ZINKERNAGEL, R. M. & HENGARTNER, H. (1994). T-cell-mediated immunopathology versus direct cytolysis by virus: implications for HIV and AIDS. Immunol. Today 15, 262-268.
84. ZINKERNAGEL, R. M., HENGARTNER, H. & STITZ, L. (1985). On the role of viruses in the evolution of immune responses. Br. Med. Bull. 41(1), 92-97.
85. ZINKERNAGEL, R. M., HAENSELER, E., LEIST, T., CERNY, A., HENGARTNER, H. & ALTHAGE, A. (1986). T cell-mediated hepatitis in mice infected with lymphocytic choriomeningitis virus. J. Exp. Med. 164, 1075-1092.