Oral Vaccination with Lipid-Formulated BCG Induces a Long-lived, Multifunctional CD4+ T Cell Memory Immune Response

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Ancelet, Lindsay R ^a   Aldwell, Frank E ^b   Rich, Fenella J ^a   Kirman, Joanna R ^b  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; HERMES ANTIGEN; L SELECTIN; LIPID; LIPORALE; MYCOBACTERIUM ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BCG VACCINATION; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELLULAR IMMUNITY; CENTRAL MEMORY T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; DOWN REGULATION; DRUG DELIVERY SYSTEM; DRUG DOSAGE FORM COMPARISON; DRUG FORMULATION; EFFECTOR CELL; EFFECTOR MEMORY T LYMPHOCYTE; LUNG; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SPLEEN; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ACYLTRANSFERASES; ADMINISTRATION, ORAL; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BCG VACCINE; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; IMMUNE SYSTEM; INTERFERON-GAMMA; LIPIDS; LUNG; MALE; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; SPLEEN; VACCINES;

BACILLI (CLASS); MUS; MYCOBACTERIUM TUBERCULOSIS;

EID: 84866692076     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045888     Document Type: Article

References (51)

1. Partnership WST (2010) The Global Plan to Stop TB 2011-2015: Transforming the Fight- Towards Elimination of Tuberculosis.
2. Weir RE, Gorak-Stolinska P, Floyd S, Lalor MK, Stenson S, et al. (2008) Persistence of the immune response induced by BCG vaccination. BMC infectious diseases 8: 9.
3. Ozeki Y, Hirayama Y, Takii T, Yamamoto S, Kobayashi K, et al. (2011) Loss of anti-mycobacterial efficacy in mice over time following vaccination with Mycobacterium bovis bacillus Calmette-Guerin. Vaccine 29: 6881-6887.
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. Colditz GA, Brewer TF, Berkey CS, Wilson ME, Burdick E, et al. (1994) Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA: the journal of the American Medical Association 271: 698-702.
6. Fine PE, (1995) Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346: 1339-1345.
7. WHO (2010) The Global Plan to Stop TB 2011-2015: Transforming the Fight- Towards Elimination of Tuberculosis. Geneva: WHO Stop TB Partnership.
8. McShane H, (2011) Tuberculosis vaccines: beyond bacille Calmette-Guerin. Philosophical transactions of the Royal Society of London Series B, Biological sciences 366: 2782-2789.
9. Gheorghiu M, (1994) BCG-induced mucosal immune responses. International journal of immunopharmacology 16: 435-444.
10. Orme IM, (1988) Induction of nonspecific acquired resistance and delayed-type hypersensitivity, but not specific acquired resistance in mice inoculated with killed mycobacterial vaccines. Infection and immunity 56: 3310-3312.
11. Haile M, Schroder U, Hamasur B, Pawlowski A, Jaxmar T, et al. (2004) Immunization with heat-killed Mycobacterium bovis bacille Calmette-Guerin (BCG) in Eurocine L3 adjuvant protects against tuberculosis. Vaccine 22: 1498-1508.
12. Clark S, Cross ML, Nadian A, Vipond J, Court P, et al. (2008) Oral vaccination of guinea pigs with a Mycobacterium bovis bacillus Calmette-Guerin vaccine in a lipid matrix protects against aerosol infection with virulent M. bovis. Infection and immunity 76: 3771-3776.
13. Vipond J, Cross ML, Lambeth MR, Clark S, Aldwell FE, et al. (2008) Immunogenicity of orally-delivered lipid-formulated BCG vaccines and protection against Mycobacterium tuberculosis infection. Microbes and infection/Institut Pasteur 10: 1577-1581.
14. 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.
15. Aldwell FE, Brandt L, Fitzpatrick C, Orme IM, (2005) Mice fed lipid-encapsulated Mycobacterium bovis BCG are protected against aerosol challenge with Mycobacterium tuberculosis. Infection and immunity 73: 1903-1905.
16. Cosgrove CA, Castello-Branco LR, Hussell T, Sexton A, Giemza R, et al. (2006) Boosting of cellular immunity against Mycobacterium tuberculosis and modulation of skin cytokine responses in healthy human volunteers by Mycobacterium bovis BCG substrain Moreau Rio de Janeiro oral vaccine. Infection and immunity 74: 2449-2452.
17. Hoft DF, Brown RM, Belshe RB, (2000) Mucosal bacille calmette-Guerin vaccination of humans inhibits delayed-type hypersensitivity to purified protein derivative but induces mycobacteria-specific interferon-gamma responses. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 30 (Suppl 3): S217-222.
18. Nol P, Palmer MV, Waters WR, Aldwell FE, Buddle BM, et al. (2008) Efficacy of oral and parenteral routes of Mycobacterium bovis bacille Calmette-Guerin vaccination against experimental bovine tuberculosis in white-tailed deer (Odocoileus virginianus): a feasibility study. Journal of wildlife diseases 44: 247-259.
19. Buddle BM, Aldwell FE, Skinner MA, de Lisle GW, Denis M, et al. (2005) Effect of oral vaccination of cattle with lipid-formulated BCG on immune responses and protection against bovine tuberculosis. Vaccine 23: 3581-3589.
20. Tompkins DM, Ramsey DS, Cross ML, Aldwell FE, de Lisle GW, et al. (2009) Oral vaccination reduces the incidence of tuberculosis in free-living brushtail possums. Proceedings Biological sciences/The Royal Society 276: 2987-2995.
21. Corner LA, Costello E, O'Meara D, Lesellier S, Aldwell FE, et al. (2010) Oral vaccination of badgers (Meles meles) with BCG and protective immunity against endobronchial challenge with Mycobacterium bovis. Vaccine 28: 6265-6272.
22. Cooper AM, (2009) T cells in mycobacterial infection and disease. Current opinion in immunology 21: 378-384.
23. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. (1993) Disseminated tuberculosis in interferon gamma gene-disrupted mice. The Journal of experimental medicine 178: 2243-2247.
24. Cooper AM, Magram J, Ferrante J, Orme IM, (1997) Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with mycobacterium tuberculosis. The Journal of experimental medicine 186: 39-45.
25. Scanga CA, Mohan VP, Yu K, Joseph H, Tanaka K, et al. (2000) Depletion of CD4(+) T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon gamma and nitric oxide synthase 2. The Journal of experimental medicine 192: 347-358.
26. Bekker LG, Freeman S, Murray PJ, Ryffel B, Kaplan G, (2001) TNF-alpha controls intracellular mycobacterial growth by both inducible nitric oxide synthase-dependent and inducible nitric oxide synthase-independent pathways. Journal of immunology 166: 6728-6734.
27. Mogues T, Goodrich ME, Ryan L, LaCourse R, North RJ, (2001) The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. The Journal of experimental medicine 193: 271-280.
28. Ancelet L, Kirman JR, (2012) Shaping the CD4 memory immune response against tuberculosis: the role of antigen persistence, location and multi-functionality. BioMol Concepts 3: 13-20.
29. Connor LM, Harvie MC, Rich FJ, Quinn KM, Brinkmann V, et al. (2010) A key role for lung-resident memory lymphocytes in protective immune responses after BCG vaccination. European journal of immunology 40: 2482-2492.
30. Goldsack L, Kirman JR, (2007) Half-truths and selective memory: Interferon gamma, CD4(+) T cells and protective memory against tuberculosis. Tuberculosis 87: 465-473.
31. 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. Proceedings of the National Academy of Sciences of the United States of America 104: 12434-12439.
32. 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. Nature medicine 13: 843-850.
33. Derrick SC, Yabe IM, Yang A, Morris SL, (2011) Vaccine-induced anti-tuberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine 29: 2902-2909.
34. 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. Journal of immunology 182: 8047-8055.
35. 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. Journal of immunology 181: 4955-4964.
36. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A, (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
37. Bingaman AW, Patke DS, Mane VR, Ahmadzadeh M, Ndejembi M, et al. (2005) Novel phenotypes and migratory properties distinguish memory CD4 T cell subsets in lymphoid and lung tissue. European journal of immunology 35: 3173-3186.
38. Zaph C, Uzonna J, Beverley SM, Scott P, (2004) Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nature medicine 10: 1104-1110.
39. Ramsey DS, Aldwell FE, Cross ML, de Lisle GW, Buddle BM, (2009) Protection of free-living and captive possums against pulmonary challenge with Mycobacterium bovis following oral BCG vaccination. Tuberculosis 89: 163-168.
40. Jung YJ, Ryan L, LaCourse R, North RJ, (2005) Properties and protective value of the secondary versus primary T helper type 1 response to airborne Mycobacterium tuberculosis infection in mice. The Journal of experimental medicine 201: 1915-1924.
41. Gallegos AM, Pamer EG, Glickman MS, (2008) Delayed protection by ESAT-6-specific effector CD4+ T cells after airborne M. tuberculosis infection. The Journal of experimental medicine 205: 2359-2368.
42. Kaveh DA, Bachy VS, Hewinson RG, Hogarth PJ, (2011) Systemic BCG immunization induces persistent lung mucosal multifunctional CD4 T(EM) cells which expand following virulent mycobacterial challenge. PloS one 6: e21566.
43. Lee WT, Pelletier WJ, (1998) Visualizing memory phenotype development after in vitro stimulation of CD4(+) T cells. Cellular immunology 188: 1-11.
44. Aldwell FE, Baird MA, Fitzpatrick CE, McLellan AD, Cross ML, et al. (2005) Oral vaccination of mice with lipid-encapsulated Mycobacterium bovis BCG: anatomical sites of bacterial replication and immune activity. Immunology and cell biology 83: 549-553.
45. Butcher EC, Picker LJ, (1996) Lymphocyte homing and homeostasis. Science 272: 60-66.
46. Agace WW, (2006) Tissue-tropic effector T cells: generation and targeting opportunities. Nature reviews Immunology 6: 682-692.
47. Lefrancois L, Puddington L, (2006) Intestinal and pulmonary mucosal T cells: local heroes fight to maintain the status quo. Annual review of immunology 24: 681-704.
48. Campbell DJ, Butcher EC, (2002) Rapid acquisition of tissue-specific homing phenotypes by CD4(+) T cells activated in cutaneous or mucosal lymphoid tissues. The Journal of experimental medicine 195: 135-141.
49. Dorer DE, Czepluch W, Lambeth MR, Dunn AC, Reitinger C, et al. (2007) Lymphatic tracing and T cell responses following oral vaccination with live Mycobacterium bovis (BCG). Cellular microbiology 9: 544-553.
50. Ainslie MP, McNulty CA, Huynh T, Symon FA, Wardlaw AJ, (2002) Characterisation of adhesion receptors mediating lymphocyte adhesion to bronchial endothelium provides evidence for a distinct lung homing pathway. Thorax 57: 1054-1059.
51. Feng CG, Britton WJ, Palendira U, Groat NL, Briscoe H, et al. (2000) Up-regulation of VCAM-1 and differential expansion of beta integrin-expressing T lymphocytes are associated with immunity to pulmonary Mycobacterium tuberculosis infection. Journal of immunology 164: 4853-4860.