Visualizing the Viral Burden: Phenotypic and Functional Alterations of T Cells and APCs during Persistent Infection

Journal of Immunology

Volumn 172, Issue 10, 2004, Pages 6239-6250

  Homann, Dirk ^a,b   McGavern, Dorian B ^a   Oldstone, Michael B A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; COMPLEMENT; CYTOKINE; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; BLOOD; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; IMMUNE DEFICIENCY; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PERSISTENT INFECTION; PHENOTYPE; PRIORITY JOURNAL; PUBLIC HEALTH; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VIRUS INFECTION; VIRUS LOAD;

EID: 2442504660     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.10.6239     Document Type: Article

References (73)

1. Homann, D. 2002. Immunocytotherapy. Curr. Top. Microbiol. Immunol. 263:43.
2. Tortorella, D., B. E. Gewurz, M. H. Furman, D. J. Schust, and H. L. Ploegh. 2000. Viral subversion of the immune system. Annu. Rev. Immunol. 18:861.
3. Welsh, R. M. 2001. Assessing CD8 T cell number and dysfunction in the presence of antigen. J. Exp. Med. 193:F19.
4. Lieberman, J., P. Shankar, N. Manjunath, and J. Andersson. 2001. Dressed to kill? A review of why antiviral CD8 T lymphocytes fail to prevent progressive immunodeficiency in HIV-1 infection. Blood 98:1667.
5. Whitton, J. L., and M. B. Oldstone. 2001. The immune response to viruses. In Field's Virology. D. Knipe, P. Howley, D. Griffin, R. Lamb, M. Martin, and S. Strauss, eds. Lippincott Williams & Wilkins, Philadelphia, p. 285.
6. + T cells. Nature 417:95.
7. Borrow, P., and M. B. A. Oldstone. 1997. Lymphocytic choriomeningitis virus. In Viral Pathogenesis. N. Nathanson, R. Ahmed, F. Gonzalez-Scarano, D. E. Griffin, K. V. Holmes, F. A. Murph, and H. L. Robinson, eds. Lippincott-Raven, Philadelphia, p. 593.
8. Tishon, A., P. Borrow, C. Evans, and M. B. Oldstone. 1993. Virus-induced immunosuppression. I. Age at infection relates to a selective or generalized defect. Virology 195:397.
9. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188:2205.
10. Ou, R., S. Zhou, L. Huang, and D. Moskophidis. 2001. Critical role for α/β and γ interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic T cells. J. Virol. 75:8407.
11. Zhou, S., R. Ou, L. Huang, and D. Moskophidis. 2002. Critical role for perforin-, Fas/FasL-, and TNFR1-mediated cytotoxic pathways in down-regulation of antigen-specific T cells during persistent viral infection. J. Virol. 76:829.
12. Wherry, E. J., J. N. Blattman, K. Murali-Krishna, R. van der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77:4911.
13. Leist, T. P., E. Ruedi, and R. M. Zinkernagel. 1988. Virus-triggered immune suppression in mice caused by virus-specific cytotoxic T cells. J. Exp. Med. 167:1749.
14. Sevilla, N., S. Kunz, A. Holz, H. Lewicki, D. Homann, H. Yamada, K. P. Campbell, J. C. de La Torre, and M. B. Oldstone. 2000. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 192:1249.
15. Smelt, S. C., P. Borrow, S. Kunz, W. Cao, A. Tishon, H. Lewicki, K. P. Campbell, and M. B. Oldstone. 2001. Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor α-dystroglycan correlate with viral tropism and disease kinetics. J. Virol. 75:448.
16. Borrow, P., C. F. Evans, and M. B. Oldstone. 1995. Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J. Virol. 69:1059.
17. Sevilla, N., D. B. McGavern, C. Teng, S. Kunz, and M. B. Oldstone. 2004. Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J. Clin. Invest. 113:737.
18. Pircher, H., K. Burki, R. Lang, H. Hengartner, and R. M. Zinkernagel. 1989. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342:559.
19. Traub, E. 1936. Persistence of lymphocytic choriomeningitis virus in immune animals and its relation to immunity. J. Exp. Med. 63:847.
20. Traub, E. 1938. Factors influencing the persistence of LCM virus in the blood of mice after clinical recovery. J. Exp. Med. 68:229.
21. Hotchin, J. E., and M. Cintis. 1958. Lymphocytic choriomeningitis infection of mice as a model for the study of latent virus infection. Can. J. Microbiol. 4:149.
22. Cihak, J., and F. Lehmann-Grube. 1978. Immunological tolerance to lymphocytic choriomeningitis virus in neonatally infected virus carrier mice: evidence supporting a clonal inactivation mechanism. Immunology 34:265.
23. Guttler, F., K. Bro-Jorgensen, and P. N. Jorgensen. 1975. Transient impaired cell-mediated tumor immunity after acute infection with lymphocytic choriomeningitis virus. Scand. J. Immunol. 4:327.
24. Lehmann-Grube, F., I. Niemeyer, and J. Lohler. 1972. Lymphocytic choriomeningitis of the mouse. IV. Depression of the allograft reaction. Med. Microbiol. Immunol. 158:16.
25. Mims, C. A., and S. Wainwright. 1968. The immunodepressive action of lymphocytic choriomeningitis virus in mice. J. Immunol. 101:717.
26. Oldstone, M. B., A. Tishon, J. M. Chiller, W. O. Weigle, and F. J. Dixon. 1973. Effect of chronic viral infection on the immune system. I. Comparison of the immune responsiveness of mice chronically infected with LCM virus with that of noninfected mice. J. Immunol. 110:1268.
27. Buchmeier, M. J., R. M. Welsh, F. J. Dutko, and M. B. Oldstone. 1980. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30:275.
28. Oldstone, M. B., R. Ahmed, J. Byrne, M. J. Buchmeier, Y. Riviere, and P. Southern. 1985. Virus and immune responses: lymphocytic choriomeningitis virus as a prototype model of viral pathogenesis. Br. Med. Bull. 41:70.
29. Mims, C. A., and T. P. Subrahmanyan. 1966. Immunofluorescence study of the mechanism of resistance to superinfection in mice carrying the lymphocytic choriomeningitis virus. J. Pathol. Bacteriol. 91:403.
30. Wagner, R. R., and R. M. Snyder. 1962. Viral interference induced in mice by acute or persistent infection with the virus of lymphocytic choriomeningitis. Nature 196:393.
31. Homann, D., A. Tishon, D. P. Berger, W. O. Weigle, M. G. von Herrath, and M. B. Oldstone. 1998. Evidence for an underlying CD4 helper and CD8 T-cell defect in B-cell-deficient mice: failure to clear persistent virus infection after adoptive immunotherapy with virus-specific memory cells from muMT/muMT mice. J. Virol. 72:9208.
32. + T-cell memory. Nat. Med. 7:913.
33. Homann, D., A. Jahreis, T. Wolfe, A. Hughes, B. Coon, M. J. van Stipdonk, K. R. Prilliman, S. P. Schoenberger, and M. G. von Herrath. 2002. CD40L blockade prevents autoimmune diabetes by induction of bitypic NK/DC regulatory cells. Immunity 16:403.
34. Van Bleek, G. M., and S. G. Nathenson. 1990. Isolation of an endogenously processed immunodominant viral peptide from the class I H-2Kb molecule. Nature 348:213.
35. Burkhart, C., G. Freer, R. Castro, L. Adorini, K. H. Wiesmuller, R. M. Zinkernagel, and H. Hengartner. 1994. Characterization of T-helper epitopes of the glycoprotein of vesicular stomatitis virus. J. Virol. 68:1573.
36. Brehm, M. A., A. K. Pinto, K. A. Daniels, J. P. Schneck, R. M. Welsh, and L. K. Selin. 2002. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3:627.
37. Berger, D. P., D. Homann, and M. B. Oldstone. 2000. Defining parameters for successful immunocytotherapy of persistent viral infection. Virology 266:257.
38. Oldstone, M. B., and M. J. Buchmeier. 1982. Restricted expression of viral glycoprotein in cells of persistently infected mice. Nature 300:360.
39. Ahmed, R., C. C. King, and M. B. Oldstone. 1987. Virus-lymphocyte interaction: T cells of the helper subset are infected with lymphocytic choriomeningitis virus during persistent infection in vivo. J. Virol. 61:1571.
40. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2:151.
41. Maraskovsky, E., K. Brasel, M. Teepe, E. R. Roux, S. D. Lyman, K. Shortman, and H. J. McKenna. 1996. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 184:1953.
42. Pulendran, B., J. Lingappa, M. K. Kennedy, J. Smith, M. Teepe, A. Rudensky, C. R. Maliszewski, and E. Maraskovsky. 1997. Developmental pathways of dendritic cells in vivo: distinct function, phenotype, and localization of dendritic cell subsets in FLT3 ligand-treated mice. J. Immunol. 159:2222.
43. Henri, S., D. Vremec, A. Kamath, J. Waithman, S. Williams, C. Benoist, K. Burnham, S. Saeland, E. Handman, and K. Shortman. 2001. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167:741.
44. Vremec, D., J. Pooley, H. Hochrein, L. Wu, and K. Shortman. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164:2978.
45. Lian, Z. X., T. Okada, X. S. He, H. Kita, Y. J. Liu, A. A. Ansari, K. Kikuchi, S. Ikehara, and M. E. Gershwin. 2003. Heterogeneity of dendritic cells in the mouse liver: identification and characterization of four distinct populations. J. Immunol. 170:2323.
46. + lymphoid-related dendritic cells. J. Immunol. 165:795.
47. + cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J. Exp. Med. 194:1171.
48. Oldstone, M. B. A. 1984. Virus-induced immune complex formation and disease: definition, regulation and importance. In Concepts in Viral Pathogenesis. A. L. Notkins and M. B. A. Oldstone, eds. Springer Verlag, New York, p. 201.
49. Berry, D. M., and J. D. Almeida. 1968. The morphological and biological effects of various antisera on avian infectious bronchitis virus. J. Gen. Virol. 3:97.
50. + regulatory T cells induced by chronic retroviral infection. Proc. Natl. Acad. Sci. USA 98:9226.
51. Akashi, K., M. Kondo, U. von Freden-Jefrry, R. Murray, and I. L. Weissman. 1997. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 89:1033.
52. -/- mice. Cell 89:1011.
53. Nopora, A., and T. Brocker. 2002. Bcl-2 controls dendritic cell longevity in vivo. J. Immunol. 169:3006.
54. Tishon, A., P. J. Southern, and M. B. Oldstone. 1988. Virus-lymphocyte interactions. II. Expression of viral sequences during the course of persistent lymphocytic choriomeningitis virus infection and their localization to the L3T4 lymphocyte subset. J. Immunol. 140:1280.
55. Tishon, A., M. Eddleston, J. C. de la Torre, and M. B. Oldstone. 1993. Cytotoxic T lymphocytes cleanse viral gene products from individually infected neurons and lymphocytes in mice persistently infected with lymphocytic choriomeningitis virus. Virology 197:463.
56. Yewdell, J. W., L. C. Anton, and J. R. Bennink. 1996. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J. Immunol. 157:1823.
57. Khan, S., R. de Giuli, G. Schmidtke, M. Bruns, M. Buchmeier, M. van den Broek, and M. Groettrup. 2001. Cutting edge: neosynthesis is required for the presentation of a T cell epitope from a long-lived viral protein. J. Immunol. 167:4801.
58. Perez, M., R. C. Craven, and J. C. de la Torre. 2003. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc. Natl. Acad. Sci. USA 100:12978.
59. + dendritic cells. J. Immunol. 166:5327.
60. Evans, C. F., P. Borrow, J. C. de la Torre, and M. B. Oldstone. 1994. Virus-induced immunosuppression: kinetic analysis of the selection of a mutation associated with viral persistence. J. Virol. 68:7367.
61. Cao, W., M. D. Henry, P. Borrow, H. Yamada, J. H. Elder, E. V. Ravkov, S. T. Nichol, R. W. Compans, K. P. Campbell, and M. B. Oldstone. 1998. Identification of α-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079.
62. + T cells and subsequently express CD8α and CD205 molecules. J. Exp. Med. 195:1233.
63. Freigang, S., D. Egger, K. Bienz, H. Hengartner, and R. M. Zinkernagel. 2003. Endogenous neosynthesis vs. cross-presentation of viral antigens for cytotoxic T cell priming. Proc. Natl. Acad. Sci. USA 100:13477.
64. Andrews, D. M., C. E. Andoniou, F. Granucci, P. Ricciardi-Castasnoli, and M. A. Degli-Esposti. 2001. Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat. Immunol. 2:1077.
65. Raftery, M. J., M. Schwab, S. M. Eibert, Y. Samstag, H. Walczak, and G. Schonrich. 2001. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 15:997.
66. Silvestri, G., and M. B. Feinberg. 2003. Turnover of lymphocytes and conceptual paradigms in HIV infection. J. Clin. Invest. 112:821.
67. Hellerstein, M. K., R. A. Hoh, M. B. Hanley, D. Cesar, D. Lee, R. A. Neese, and J. M. McCune. 2003. Subpopulations of long-lived and short-lived T cells in advanced HIV-1 infection. J. Clin. Invest. 112:956.
68. + T cell turnover in vivo by IL-12, IL-18, and IFN-γ. J. Immunol. 166:6007.
69. Olson, J. K., J. L. Croxford, and S. D. Miller. 2001. Virus-induced autoimmunity: potential role of viruses in initiation, perpetuation, and progression of T-cell-mediated autoimmune disease. Viral Immunol. 14:227.
70. Gianani, R., and N. Sarvetnick. 1996. Viruses, cytokines, antigens, and autoimmunity. Proc. Natl. Acad. Sci. USA 93:2257.
71. Bach, J. F. 2002. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 347:911.
72. Green, E. L. Biology of the Laboratory Mouse. 1966. Dover Publications, New York.
73. Slifka, M. K., M. Matloubian, and R. Ahmed. 1995. Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 69:1895.