Systemic BCG immunization induces persistent lung mucosal multifunctional CD4 TEM cells which expand following virulent mycobacterial challenge

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Kaveh, Daryan A ^a   Bachy, Véronique S ^a   Hewinson, R Glyn ^a   Hogarth, Philip J ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; BCG VACCINE; BETA1 INTEGRIN; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON; HERMES ANTIGEN; INTERLEUKIN 2; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; TUMOR NECROSIS FACTOR ALPHA; LEUKOCYTE ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL VIRULENCE; BCG VACCINATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL HOMING; CELL POPULATION; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG RESPONSE; EFFECTOR CELL; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; LUNG INTERSTITIUM; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PHENOTYPE; RESPIRATORY TRACT MUCOSA; SPLEEN CELL; TUBERCULOSIS; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL PROLIFERATION; CYTOLOGY; HUMAN; IMMUNIZATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; LUNG; MICROBIOLOGY; MUCOSA; PATHOGENICITY; PATHOLOGY; SPLEEN; VIRULENCE;

MURINAE; MUS;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGENS, CD; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; HUMANS; IMMUNIZATION; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKIN-2; LUNG; MICE; MICE, INBRED BALB C; MUCOUS MEMBRANE; MYCOBACTERIUM BOVIS; PHENOTYPE; SPLEEN; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

EID: 79959617632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021566     Document Type: Article

References (55)

1. Ashford DA, Whitney E, Raghunathan P, Cosivi O, (2001) Epidemiology of selected mycobacteria that infect humans and other animals. Rev Sci Tech 20: 325-337.
2. Bloom BH, Fine PEM, (1994) The BCG experience: Implications for future vaccines against tuberculosis. In: Bloom BH, editors. Tuberculosis: Pathogenesis, Protection and Control Washinton, DC ASM Press.
3. Hogarth PJ, Hewinson RG, Vordermeier HM, (2006) Development of vaccines against bovine tuberculosis. J Pharm Pharmacol 58: 749-757.
4. Trunz BB, Fine P, Dye C, (2006) Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet 367: 1173-1180.
5. McShane H, Hill A, (2005) Prime-boost immunisation strategies for tuberculosis. Microbes Infect 7: 962-967.
6. Cooper AM, (2009) Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 27: 393-422.
7. Mittrucker HW, Steinhoff U, Kohler A, Krause M, Lazar D, et al. (2007) Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc Natl Acad Sci U S A 104: 12434-12439.
8. Majlessi L, Simsova M, Jarvis Z, Brodin P, Rojas MJ, et al. (2006) An increase in antimycobacterial Th1-cell responses by prime-boost protocols of immunization does not enhance protection against tuberculosis. Infect Immun 74: 2128-2137.
9. Logan KE, Chambers MA, Hewinson RG, Hogarth PJ, (2005) Frequency of IFN-gamma producing cells correlates with adjuvant enhancement of bacille Calmette-Guerin induced protection against Mycobacterium bovis. Vaccine 23: 5526-5532.
10. Beamer GL, Flaherty DK, Vesosky B, Turner J, (2008) Peripheral blood gamma interferon release assays predict lung responses and Mycobacterium tuberculosis disease outcome in mice. Clin Vaccine Immunol 15: 474-483.
11. Hervas-Stubbs S, Majlessi L, Simsova M, Morova J, Rojas MJ, et al. (2006) High frequency of CD4+ T cells specific for the TB10.4 protein correlates with protection against Mycobacterium tuberculosis infection. Infect Immun 74: 3396-3407.
12. Goldsack L, Kirman JR, (2007) Half-truths and selective memory: Interferon gamma, CD4(+) T cells and protective memory against tuberculosis. Tuberculosis (Edinb) 87: 465-473.
13. Leal IS, Smedegard B, Andersen P, Appelberg R, (2001) Failure to induce enhanced protection against tuberculosis by increasing T-cell-dependent interferon-gamma generation. Immunology 104: 157-161.
14. Skinner MA, Ramsay AJ, Buchan GS, Keen DL, Ranasinghe C, et al. (2003) A DNA prime-live vaccine boost strategy in mice can augment IFN-gamma responses to mycobacterial antigens but does not increase the protective efficacy of two attenuated strains of Mycobacterium bovis against bovine tuberculosis. Immunology 108: 548-555.
15. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, et al. (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
16. Kohlmeier JE, Woodland DL, (2009) Immunity to respiratory viruses. Annu Rev Immunol 27: 61-82.
17. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, et al. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13: 843-850.
18. Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, et al. (2008) 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 181: 4955-4964.
19. Lindenstrom T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, et al. (2009) Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol 182: 8047-8055.
20. Magalhaes I, Sizemore DR, Ahmed RK, Mueller S, Wehlin L, et al. (2008) rBCG induces strong antigen-specific T cell responses in rhesus macaques in a prime-boost setting with an adenovirus 35 tuberculosis vaccine vector. PLoS One 3: e3790.
21. Beveridge NE, Price DA, Casazza JP, Pathan AA, Sander CR, et al. (2007) Immunisation with BCG and recombinant MVA85A induces long-lasting, polyfunctional Mycobacterium tuberculosis-specific CD4+ memory T lymphocyte populations. Eur J Immunol 37: 3089-3100.
22. Young JM, Adetifa IM, Ota MO, Sutherland JS, (2010) Expanded polyfunctional T cell response to mycobacterial antigens in TB disease and contraction post-treatment. PLoS One 5: e11237.
23. Sutherland JS, Adetifa IM, Hill PC, Adegbola RA, Ota MO, (2009) Pattern and diversity of cytokine production differentiates between Mycobacterium tuberculosis infection and disease. Eur J Immunol 39: 723-729.
24. Caccamo N, Guggino G, Joosten SA, Gelsomino G, Di Carlo P, et al. (2010) Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 40: 2211-2220.
25. Logan KE, Gavier-Widen D, Hewinson RG, Hogarth PJ, (2008) Development of a Mycobacterium bovis intranasal challenge model in mice. Tuberculosis (Edinb) 88: 437-443.
26. Vordermeier HM, Chambers MA, Cockle PJ, Whelan AO, Simmons J, et al. (2002) Correlation of ESAT-6-specific gamma interferon production with pathology in cattle following Mycobacterium bovis BCG vaccination against experimental bovine tuberculosis. Infect Immun 70: 3026-3032.
27. Elias D, Akuffo H, Britton S, (2005) PPD induced in vitro interferon gamma production is not a reliable correlate of protection against Mycobacterium tuberculosis. Trans R Soc Trop Med Hyg 99: 363-368.
28. Harari A, Vallelian F, Meylan PR, Pantaleo G, (2005) Functional heterogeneity of memory CD4 T cell responses in different conditions of antigen exposure and persistence. J Immunol 174: 1037-1045.
29. Aagaard C, Hoang T, Dietrich J, Cardona PJ, Izzo A, et al. (2011) A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 17: 189-194.
30. Sander CR, Pathan AA, Beveridge NE, Poulton I, Minassian A, et al. (2009) Safety and immunogenicity of a new tuberculosis vaccine, MVA85A, in Mycobacterium tuberculosis-infected individuals. Am J Respir Crit Care Med 179: 724-733.
31. Abel B, Tameris M, Mansoor N, Gelderbloem S, Hughes J, et al. (2010) The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am J Respir Crit Care Med 181: 1407-1417.
32. Seder RA, Darrah PA, Roederer M, (2008) T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8: 247-258.
33. Henao-Tamayo MI, Ordway DJ, Irwin SM, Shang S, Shanley C, et al. (2010) Phenotypic definition of effector and memory T-lymphocyte subsets in mice chronically infected with Mycobacterium tuberculosis. Clin Vaccine Immunol 17: 618-625.
34. Orme IM, (2010) The Achilles heel of BCG. Tuberculosis (Edinb) 90: 329-332.
35. Orme IM, Collins FM, (1986) Aerogenic vaccination of mice with Mycobacterium bovis BCG. Tubercle 67: 133-140.
36. Olsen AW, Brandt L, Agger EM, van Pinxteren LA, Andersen P, (2004) The influence of remaining live BCG organisms in vaccinated mice on the maintenance of immunity to tuberculosis. Scand J Immunol 60: 273-277.
37. Aldwell FE, Cross ML, Fitzpatrick CE, Lambeth MR, de Lisle GW, et al. (2006) Oral delivery of lipid-encapsulated Mycobacterium bovis BCG extends survival of the bacillus in vivo and induces a long-term protective immune response against tuberculosis. Vaccine 24: 2071-2078.
38. Lyadova IV, Oberdorf S, Kapina MA, Apt AS, Swain SL, et al. (2004) CD4 T cells producing IFN-gamma in the lungs of mice challenged with mycobacteria express a CD27-negative phenotype. Clin Exp Immunol 138: 21-29.
39. Kapina MA, Shepelkova GS, Mischenko VV, Sayles P, Bogacheva P, et al. (2007) CD27low CD4 T lymphocytes that accumulate in the mouse lungs during mycobacterial infection differentiate from CD27high precursors in situ, produce IFN-gamma, and protect the host against tuberculosis infection. J Immunol 178: 976-985.
40. De Jong R, Brouwer M, Hooibrink B, Van der Pouw-Kraan T, Miedema F, et al. (1992) The CD27- subset of peripheral blood memory CD4+ lymphocytes contains functionally differentiated T lymphocytes that develop by persistent antigenic stimulation in vivo. Eur J Immunol 22: 993-999.
41. Schiott A, Lindstedt M, Johansson-Lindbom B, Roggen E, Borrebaeck CA, (2004) CD27- CD4+ memory T cells define a differentiated memory population at both the functional and transcriptional levels. Immunology 113: 363-370.
42. Fritsch RD, Shen X, Sims GP, Hathcock KS, Hodes RJ, et al. (2005) Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J Immunol 175: 6489-6497.
43. Pepper M, Linehan JL, Pagan AJ, Zell T, Dileepan T, et al. (2010) Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat Immunol 11: 83-89.
44. Kolibab K, Yang A, Derrick SC, Waldmann TA, Perera LP, et al. (2010) Highly persistent and effective prime/boost regimens against tuberculosis that use a multivalent modified vaccine virus Ankara-based tuberculosis vaccine with interleukin-15 as a molecular adjuvant. Clin Vaccine Immunol 17: 793-801.
45. Mu J, Jeyanathan M, Shaler CR, Horvath C, Damjanovic D, et al. (2010) Respiratory mucosal immunization with adenovirus gene transfer vector induces helper CD4 T cell-independent protective immunity. J Gene Med 12: 693-704.
46. Walrath JR, Silver RF, (2010) The {alpha}4{beta}1 Integrin in Localization of Mycobacterium Tuberculosis-specific Th1 Cells to the Human Lung. Am J Respir Cell Mol Biol.
47. Pacheco KA, Tarkowski M, Klemm J, Rosenwasser LJ, (1998) CD49d expression and function on allergen-stimulated T cells from blood and airway. Am J Respir Cell Mol Biol 18: 286-293.
48. Xu B, Wagner N, Pham LN, Magno V, Shan Z, et al. (2003) Lymphocyte homing to bronchus-associated lymphoid tissue (BALT) is mediated by L-selectin/PNAd, alpha4beta1 integrin/VCAM-1, and LFA-1 adhesion pathways. J Exp Med 197: 1255-1267.
49. Ghosh S, Chackerian AA, Parker CM, Ballantyne CM, Behar SM, (2006) The LFA-1 adhesion molecule is required for protective immunity during pulmonary Mycobacterium tuberculosis infection. J Immunol 176: 4914-4922.
50. Mikhak Z, Fleming CM, Medoff BD, Thomas SY, Tager AM, et al. (2006) STAT1 in peripheral tissue differentially regulates homing of antigen-specific Th1 and Th2 cells. J Immunol 176: 4959-4967.
51. Fuller CL, Flynn JL, Reinhart TA, (2003) In situ study of abundant expression of proinflammatory chemokines and cytokines in pulmonary granulomas that develop in cynomolgus macaques experimentally infected with Mycobacterium tuberculosis. Infect Immun 71: 7023-7034.
52. Lim J, Derrick SC, Kolibab K, Yang AL, Porcelli S, et al. (2009) Early pulmonary cytokine and chemokine responses in mice immunized with three different vaccines against Mycobacterium tuberculosis determined by PCR array. Clin Vaccine Immunol 16: 122-126.
53. Chen L, Wang J, Zganiacz A, Xing Z, (2004) Single intranasal mucosal Mycobacterium bovis BCG vaccination confers improved protection compared to subcutaneous vaccination against pulmonary tuberculosis. Infect Immun 72: 238-246.
54. Santosuosso M, Zhang X, McCormick S, Wang J, Hitt M, et al. (2005) Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J Immunol 174: 7986-7994.
55. Gallagher J, Horwill DM, (1977) A selective oleic acid albumin agar medium for the cultivation of Mycobacterium bovis. J Hyg (Lond) 79: 155-160.