A key role for lung-resident memory lymphocytes in protective immune responses after BCG vaccination

European Journal of Immunology

Volumn 40, Issue 9, 2010, Pages 2482-2492

  Connor, Lisa M ^a   Harvie, Marina C ^a   Rich, Fenella J ^a   Quinn, Kylie M ^a   Brinkmann, Volker ^b   Le Gros, Graham ^a   Kirman, Joanna R ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

BCG; FTY720; IFN ; Tuberculosis

Indexed keywords

BCG VACCINE; FINGOLIMOD; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; HLA ANTIGEN CLASS 2; PROPANEDIOL DERIVATIVE; SPHINGOSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BCG VACCINATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IMMUNE RESPONSE; LUNG ALVEOLUS MACROPHAGE; LUNG TUBERCULOSIS; LYMPHOCYTE MIGRATION; MALE; MEMORY T LYMPHOCYTE; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL COUNT; CELL MOTION; DRUG EFFECTS; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LUNG; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; MYCOBACTERIUM TUBERCULOSIS; PATHOGENICITY; PATHOLOGY; SECRETION (PROCESS); TUBERCULOSIS, PULMONARY; VACCINATION;

ANIMALS; BCG VACCINE; CD4-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELL MOVEMENT; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; LUNG; LYMPHOCYTE ACTIVATION; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; PROPYLENE GLYCOLS; SPHINGOSINE; TUBERCULOSIS, PULMONARY; VACCINATION;

EID: 77956478399     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200940279     Document Type: Article

References (40)

1. Trunz, B. B., Fine, P. and Dye, C., Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet 2006. 367: 1173-1180.
2. Walker, V., Selby, G. and Wacogne, I., Does neonatal BCG vaccination protect against tuberculous meningitis? Arch. Dis. Child 2006. 91: 789-791.
3. Colditz, G. A., Brewer, T. F., Berkey, C. S., Wilson, M. E., Burdick, E., Fineberg, H. V. and Mosteller, F., Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. J. Am. Med. Assoc. 1994. 271: 698-702.
4. Kaufmann, S. H., The contribution of immunology to the rational design of novel antibacterial vaccines. Nat. Rev. Microbiol. 2007. 5: 491-504.
5. Goldsack, L. and Kirman, J. R., Half-truths and selective memory: Interferon gamma, CD4(+) T cells and protective memory against tuberculosis. Tuberculosis (Edinb.) 2007. 87: 465-473.
6. Lefford, M. J., Induction and expression of immunity after BCG immunization. Infect. Immun. 1977. 18: 646-653.
7. Cowley, S. C. and Elkins, K. L., CD4+T cells mediate IFN-gamma- independent control of Mycobacterium tuberculosis infection both in vitro and in vivo. J. Immunol. 2003. 171: 4689-4699.
8. Andersen, P. and Smedegaard, B., CD4(+) T-cell subsets that mediate immunological memory to Mycobacterium tuberculosis infection in mice. Infect. Immun. 2000. 68: 621-629.
9. Kipnis, A., Irwin, S., Izzo, A. A., Basaraba, R. J. and Orme, I. M., Memory T lymphocytes generated by Mycobacterium bovis BCG vaccination reside within a CD4 CD44lo CD62 Ligandhi population. Infect. Immun. 2005. 73: 7759-7764.
10. Dutton, R. W., Bradley, L. M. and Swain, S. L., T cell memory. Annu. Rev. Immunol. 1998. 16: 201-223.
11. Ahmed, R. and Gray, D., Immunological memory and protective immunity: understanding their relation. Science 1996. 272: 54-60.
12. Rogers, P. R., Dubey, C. and Swain, S. L., Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. J. Immunol. 2000. 164: 2338-2346.
13. Jung, Y. J., Ryan, L., LaCourse, R. and North, R. J., Properties and protective value of the secondary versus primary T helper type 1 response to airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 2005. 201: 1915-1924.
14. Goter-Robinson, C., Derrick, S. C., Yang, A. L., Jeon, B. Y. and Morris, S. L., Protection against an aerogenic Mycobacterium tuberculosis infection in BCG-immunized and DNA-vaccinated mice is associated with early type I cytokine responses. Vaccine 2006. 24: 3522-3529.
15. Cooper, A. M., Callahan, J. E., Keen, M., Belisle, J. T. and Orme, I. M., Expression of memory immunity in the lung following re-exposure to Mycobacterium tuberculosis. Tuber. Lung Dis. 1997. 78: 67-73.
16. Khader, S. A., Bell, G. K., Pearl, J. E., Fountain, J. J., Rangel-Moreno, J., Cilley, G. E., Shen, F. et al., IL-23 and IL-17 in the establishment of protective pulmonary CD4+T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 2007. 8: 369-377.
17. Quinn, K. M., Rich, F. J., Goldsack, L. M., de Lisle, G. W., Buddle, B. M., Delahunt, B. and Kirman, J. R., Accelerating the secondary immune response by inactivating CD4(+)CD25(+) T regulatory cells prior to BCG vaccination does not enhance protection against tuberculosis. Eur. J. Immunol. 2008. 38: 695-705.
18. Jeyanathan, M., Mu, J., McCormick, S., Damjanovic, D., Small, C. L., Shaler, C. R., Kugathasan, K. and Xing, Z., Murine airway luminal antituberculosis memory CD8 T cells by mucosal immunization are maintained via antigen-driven in situ proliferation, independent of peripheral T cell recruitment. Am. J. Respir. Crit. Care Med 2010. 181: 862-872. DOI: 200910-1583OCv1
19. Wolf, A. J., Desvignes, L., Linas, B., Banaiee, N., Tamura, T., Takatsu, K. and Ernst, J. D., Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J. Exp. Med. 2008. 205: 105-115.
20. Reiley, W. W., Calayag, M. D., Wittmer, S. T., Huntington, J. L., Pearl, J. E., Fountain, J. J., Martino, C. A. et al., ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc. Natl. Acad. Sci. USA 2008. 105: 10961-10966.
21. Brinkmann, V., Davis, M. D., Heise, C. E., Albert, R., Cottens, S., Hof, R., Bruns, C. et al., The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J. Biol. Chem. 2002. 277: 21453-21457.
22. Matloubian, M., Lo, C. G., Cinamon, G., Lesneski, M. J., Xu, Y., Brinkmann, V., Allende, M. L. et al., Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004. 427: 355-360.
23. Schwab, S. R. and Cyster, J. G., Finding a way out: lymphocyte egress from lymphoid organs. Nat. Immunol. 2007. 8: 1295-1301.
24. Flynn, J. L., Chan, J., Triebold, K. J., Dalton, D. K., Stewart, T. A. and Bloom, B. R., An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 1993. 178: 2249-2254.
25. Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G. and Orme, I. M., Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 1993. 178: 2243-2247.
26. Lindenstrom, T., Agger, E. M., Korsholm, K. S., Darrah, P. A., Aagaard, C., Seder, R. A., Rosenkrands, I. and Andersen, P., Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J. Immunol. 2009. 182: 8047-8055.
27. Gollmann, G., Neuwirt, H., Tripp, C. H., Mueller, H., Konwalinka, G., Heufler, C., Romani, N. and Tiefenthaler, M., Sphingosine-1-phosphate receptor type-1 agonism impairs blood dendritic cell chemotaxis and skin dendritic cell migration to lymph nodes under inflammatory conditions. Int. Immunol. 2008. 20: 911-923.
28. Lan, Y. Y., Tokita, D., Wang, Z., Wang, H. C., Zhan, J., Brinkmann, V. and Thomson, A. W., Sphingosine 1-phosphate receptor agonism impairs skin dendritic cell migration and homing to secondary lymphoid tissue: association with prolonged allograft survival. Transpl. Immunol. 2008. 20: 88-94.
29. Flesch, I. E. and Kaufmann, S. H., Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates. Infect. Immun. 1991. 59: 3213-3218.
30. Kaufmann, S. H. and Flesch, I. E., The role of T cell-macrophage interactions in tuberculosis. Springer Semin. Immunopathol. 1988. 10: 337-358.
31. Fulton, S. A., Martin, T. D., Redline, R. W. and Henry Boom, W., Pulmonary immune responses during primary Mycobacterium bovis-Calmette-Guerin bacillus infection in C57Bl/6 mice. Am. J. Respir. Cell Mol. Biol. 2000. 22: 333-343.
32. Bradley, L. M., Haynes, L. and Swain, S. L., IL-7: maintaining T-cell memory and achieving homeostasis. Trends Immunol. 2005. 26: 172-176.
33. Mehling, M., Brinkmann, V., Antel, J., Bar-Or, A., Goebels, N., Vedrine, C., Kristofic, C. et al., FTY720 therapy exerts differential effects on T cell subsets in multiple sclerosis. Neurology 2008. 71: 1261-1267.
34. Hofmann, M., Brinkmann, V. and Zerwes, H. G., FTY720 preferentially depletes naive T cells from peripheral and lymphoid organs. Int. Immunopharmacol. 2006. 6: 1902-1910.
35. Forbes, E. K., Sander, C., Ronan, E. O., McShane, H., Hill, A. V., Beverley, P. C. and Tchilian, E. Z., Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J. Immunol. 2008. 181: 4955-4964.
36. Darrah, P. A., Patel, D. T., De Luca, P. M., Lindsay, R. W., Davey, D. F., Flynn, B. J., Hoff, S. T. et al., Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 2007. 13: 843-850.
37. Ordway, D., Harton, M., Henao-Tamayo, M., Montoya, R., Orme, I. M. and Gonzalez-Juarrero, M., Enhanced macrophage activity in granulomatous lesions of immune mice challenged with Mycobacterium tuberculosis. J. Immunol. 2006. 176: 4931-4939.
38. Gonzalez-Juarrero, M., Shim, T. S., Kipnis, A., Junqueira-Kipnis, A. P. and Orme, I. M., Dynamics of macrophage cell populations during murine pulmonary tuberculosis. J. Immunol. 2003. 171: 3128-3135.
39. Dalton, D. K., Pitts-Meek, S., Keshav, S., Figari, I. S., Bradley, A. and Stewart, T. A., Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 1993. 259: 1739-1742.
40. Kappos, L., Antel, J., Comi, G., Montalban, X., O'Connor, P., Polman, C. H., Haas, T. et al., Oral fingolimod (FTY720) for relapsing multiple sclerosis. N. Engl. J. Med. 2006. 355: 1124-1140.