Virally activated CD8 T cells home to Mycobacterium bovis BCG-induced granulomas but enhance antimycobacterial protection only in immunodeficient mice

Infection and Immunity

Volumn 75, Issue 3, 2007, Pages 1154-1166

  Hogan, Laura H ^a   Co, Dominic O ^a,d   Karman, Jozsef ^a,e   Heninger, Erika ^a   Suresh, M ^b   Sandor, Matyas ^a,c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c MSC   (United States)

^d CHILDREN S HOSPITAL OF WISCONSIN   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; OVALBUMIN; T LYMPHOCYTE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GRANULOMA; GRANULOMATOUS INFLAMMATION; IMMUNE DEFICIENCY; IMMUNITY; IMMUNIZATION; LIVER GRANULOMA; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL; SUPERINFECTION; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE; VIRUS INFECTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; GRANULOMA; IMMUNOLOGIC DEFICIENCY SYNDROMES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYCOBACTERIUM BOVIS;

EID: 33847704990     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00943-06     Document Type: Article

References (53)

1. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice: role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160:521-540.
2. Banerjee, K., S. Deshpande, M. Zheng, U. Kumaraguru, S. P. Schoenberger, and B. T. Rouse. 2002. Herpetic stromal keratitis in the absence of viral antigen recognition. Cell. Immunol. 219:108-118.
3. Basu, D., S. Horvath, I. Matsumoto, D. H. Fremont, and P. M. Allen. 2000. Molecular basis for recognition of an arthritic peptide and a foreign epitope on distinct MHC molecules by a single TCR. J. Immunol. 164:5788-5796.
4. Bergmann, C. C, B. Parra, D. R. Hinton, C. Ramakrishna, K. C. Dowdell, and S. A. Stohlman. 2004. Perforin and gamma interferon-mediated control of coronavirus central nervous system infection by CD8 T cells in the absence of CD4 T cells. J. Virol. 78:1739-1750.
5. + T cells during an acute virus infection. Immunity 8:167-175.
6. Cano, M. V., and R. A. Hajjeh. 2001. The epidemiology of histoplasmosis: a review. Semin. Respir. Infect. 16:109-118.
7. Cauley, L. S., E. E. Miller, M. Yen, and S. L. Swain. 2000. Superantigen-induced CD4 T-cell tolerance mediated by myeloid cells and IFN-gamma. J. Immunol. 165:6056-6066.
8. 7a. Co, D. O., L. H. Hogan, J. Karman, E. Heninger, S. Vang, K. Wells, Y. Kawaoka, and M. Sandor. 2006. Interactions between T cells responding to concurrent mycobacterial and influenza infections. J. Immunol. 177:8456-8465.
9. + T-cell immunodominance in primary and secondary influenza virus infections. J. Exp. Med. 198:399-110.
10. -) to TCR/CD8 signaling in response to antigen. J. Immunol. 160: 3236-3243.
11. Dalton, D. K., L. Haynes, C. Q. Chu, S. L. Swain, and S. Wittmer. 2000. Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J. Exp. Med. 192:117-122.
12. Derrick, S. C., C. Repique, P. Snoy, A. L. Yang, and S. Morris. 2004. Immunization with a DNA vaccine cocktail protects mice lacking CD4 cells against an aerogenic infection with Mycobacterium tuberculosis. Infect. Immun. 72:1685-1692.
13. + T lymphocytes. Immunity 20:327-336.
14. Dye, C., S. Scheele, P. Dolin, V. Pathania, and M. C. Raviglione. 1999. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. JAMA 282:677-686.
15. Edwards, M. J., O. Buchatska, M. Ashton, M. Montoya, Q. D. Bickle, and P. Borrow. 2005. Reciprocal immunomodulation in a schistosome and hepatotropic virus coinfection model. J. Immunol. 175:6275-6285.
16. Elliot, D. E. 1996. Methods used to study immunoregulation of schistosome egg granulomas. Methods: Companion Methods Enzymol. 9:255-267.
17. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
18. Flynn, J. L., M. M. Goldstein, J. Chan, K. J. Triebold, K. Pfeffer, C. J. Lowenstein, R. Schreiber, T. W. Mak, and B. R. Bloom. 1995. Tumor necrosis factor-α is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2:561-572.
19. Giulietti, A., L. Overbergh, D. Valckx, B. Decallonne, R. Bouillon, and C. Mathieu. 2001. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25:386-401.
20. Gruener, N. H., M. C. Jung, A. Ulsenheimer, T. J. Gerlach, H. M. Diepolder, C. A. Schirren, R. Hoffmann, M. Wachtler, M. Backmund, and G. R. Pape. 2002. Hepatitis C virus eradication associated with hepatitis B virus superinfection and development of a hepatitis B virus specific T-cell response. J. Hepatol. 37:866-869.
21. Haring, J. S., L. L. Pewe, and S. Perlman. 2002. Bystander CD8 T cell-mediated demyelination after viral infection of the central nervous system. J. Immunol. 169:1550-1555.
22. Heninger, E., L. H. Hogan, J. Karman, S. Macvilay, B. Hill, J. P. Woods, and M. Sandor. 2006. Characterization of the Histoplasma capsulatum-induced granuloma. J. Immunol. 177:3303-3313.
23. Hogan, L. H., K. Macvilay, B. Barger, D. Co, I. Malkovska, G. Fennelly, and M. Sandor. 2001. Mycobacterium bovis strain Bacillus Calmette-Guerin-induced liver granulomas contain a diverse TCR repertoire, but a monoclonal T-cell population is sufficient for protective granuloma formation. J. Immunol. 166:6367-6375.
24. + TCR repertoire heterogeneity in Schistosoma mansoni-induced granulomas. J. Immunol. 169:6386-6393.
25. Hunziker, L., M. Recher, A. Ciurea, M. M. Martinic, B. Odermatt, H. Hengartner, and R. M. Zinkernagel. 2002. Antagonistic variant virus prevents wild-type virus-induced lethal immunopathology. J. Exp. Med. 196: 1039-1046.
26. Jiang, J., L. A. Zenewicz, L. R. San Mateo, L. L. Lau, and H. Shen. 2003. Activation of antigen-specific CD8 T cells results in minimal killing of bystander bacteria. J. Immunol. 171:6032-6038.
27. Kim, S. K., M. A. Brehm, R. M. Welsh, and L. K. Selin. 2002. Dynamics of memory T-cell proliferation under conditions of heterologous immunity and bystander stimulation. J. Immunol. 169:90-98.
28. Kyburz, D., and M. Corr. 2003. The KRN mouse model of inflammatory arthritis. Springer Semin. Immunopathol. 25:79-90.
29. Lawn, S. D., S. T. Butera, and T. M. Shinnick. 2002. Tuberculosis unleashed: the impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes Infect. 4:635-646.
30. McGavern, D. B., and P. Truong. 2004. Rebuilding an immune-mediated central nervous system disease: weighing the pathogenicity of antigen-specific versus bystander T cells. J. Immunol. 173:4779-4790.
31. McNally, J. M., C. C. Zarozinski, M. Y. Lin, M. A. Brehm, H. D. Chen, and R. M. Welsh. 2001. Attrition of bystander CD8 T cells during virus-induced T-cell and interferon responses. J. Virol. 75:5965-5976.
32. Metwali, A., D. Elliott, A. M. Blum, J. Li, M. Sandor, R. G. Lynch, N. Noben-Trauth, and J. V. Weinstock. 1996. The granulomatous response in murine schistomiasis mansoni does not switch to TH1 in IL-4-deficient C57BL/6 mice. J. Immunol. 157:4546-4553.
33. + T cells, during infection with influenza virus. Toxicol. Appl. Pharmacol. 192:275-286.
34. Murali-Krishna, K., J. D. Altman, M. Suresh, D. J. Sourdive, A. J. Zajac, J. D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8:177-187.
35. Ostler, T., H. Pircher, and S. Ehl. 2003. "Bystander" recruitment of systemic memory T cells delays the immune response to respiratory virus infection. Eur. J. Immunol. 33:1839-1848.
36. Perlman, D. C., P. El-Helou, and N. Salomon. 1999. Tuberculosis in patients with human immunodeficiency virus infection. Semin. Respir. Infect. 14:344-352.
37. 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 342:559-561.
38. Qiu, B., K. A. Frait, F. Reich, E. Komuniecki, and S. W. Chensue. 2001. Chemokine expression dynamics in mycobacterial (type-1) and schistosomal (type-2) antigen-elicited pulmonary granuloma formation. Am. J. Pathol. 158:1503-1515.
39. Restifo, N. P., I. Bacik, K. R. Irvine, J. W. Yewdell, B. J. McCabe, R. W. Anderson, L. C. Eisenlohr, S. A. Rosenberg, and J. R. Bennink. 1995. Antigen processing in vivo and the elicitation of primary CTL responses. J. Immunol. 154:4414-4422.
40. Roman, E., E. Miller, A. Harmsen, J. Wiley, U. H. Von Andrian, G. Huston, and S. L. Swain. 2002. CD4 effector T-cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196:957-968.
41. Sandor, M., A. I. Sperling, G. A. Cook, J. V. Weinstock, R. G. Lynch, and J. A. Bluestone. 1995. Two waves of gamma delta T cells expressing different V delta genes are recruited into schistosome-induced liver granulomas. J. Immunol. 155:275-284.
42. Schaible, U. E., F. Winau, P. A. Sieling, K. Fischer, H. L. Collins, K. Hagens, R. L. Modlin, V. Brinkmann, and S. H. Kaufmann. 2003. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-1 and CD1 in tuberculosis. Nat. Med. 9:1039-1046.
43. Sewell, D. L., E. K. Reinke, D. O. Co, L. H. Hogan, R. B. Fritz, M. Sandor, and Z. Fabry. 2003. Infection with Mycobacterium bovis BCG diverts traffic of myelin oligodendroglial glycoprotein autoantigen-specific T cells away from the central nervous system and ameliorates experimental autoimmune encephalomyelitis. Clin. Diagn. Lab. Immunol. 10:564-572.
44. Sourdive, D. J., K. Murali-Krishna, J. D. Altman, A. J. Zajac, J. K. Whitmire, C. Pannetier, P. Kourilsky, B. Evavold, A. Sette, and R. Ahmed. 1998. Conserved T-cell receptor repertoire in primary and memory CD8 T-cell responses to an acute viral infection. J. Exp. Med. 188:71-82.
45. Suresh, M., H. Molina, M. S. Salvato, D. Mastellos, J. D. Lambris, and M. Sandor. 2003. Complement component 3 is required for optimal expansion of CD8 T cells during a systemic viral infection. J. Immunol. 170:788-794.
46. Tewari, K., J. Sacha, X. Gao, and M. Suresh. 2004. Effect of chronic viral infection on epitope selection, cytokine production, and surface phenotype of CD8 T cells and the role of IFN-gamma receptor in immune regulation. J. Immunol. 172:1491-1500.
47. van der Most, R. G., K. Murali-Krishna, J. G. Lanier, E. J. Wherry, M. T. Puglielli, J. N. Blattman, A. Sette, and R. Ahmed. 2003. Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315:93-102.
48. van Pinxteren, L. A., J. P. Cassidy, B. H. Smedegaard, E. M. Agger, and P. Andersen. 2000. Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur. J. Immunol. 30:3689-3698.
49. + T cells during acute infection with lymphocytic choriomeningitis virus. J. Immunol. 161:3215-3218.
50. Villarete, L., R. de Fries, S. Kolhekar, D. Howard, R. Ahmed, and B. Wu-Hsieh. 1995. Impaired responsiveness to gamma interferon of macrophages infected with lymphocytic choriomeningitis virus clone 13: susceptibility to histoplasmosis. Infect. Immun. 63:1468-1472.
51. Wilson, M. E., and J. V. Weinstock. 1996. Hepatic granulomas in murine visceral leishmaniasis chagasi. Methods 9:248.
52. Wu-Hsieh, B., D. H. Howard, and R. Ahmed. 1988. Virus-induced immunosuppression: a murine model of susceptibility to opportunistic infection. J. Infect. Dis. 158:232-235.
53. Wu-Hsieh, B. A., J. K. Whitmire, R. de Fries, J. S. Lin, M. Matloubian, and R. Ahmed. 2001. Distinct CD8 T-cell functions mediate susceptibility to histoplasmosis during chronic viral infection. J. Immunol. 167:4566-4573.