Lessons for tuberculosis vaccines from respiratory virus infection

Expert Review of Vaccines

Volumn 7, Issue 8, 2008, Pages 1165-1172

  Beverley, Peter Charles Leonard ^a   Tchilian, Elma Zaven ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Lymphocyte homing; Respiratory virus; T cells; Tuberculosis; Vaccine

Indexed keywords

BCG VACCINE; INFLUENZA VACCINE;

BCG VACCINATION; HUMAN; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY VIRUS; REVIEW; T LYMPHOCYTE; TUBERCULOSIS; TUBERCULOSIS CONTROL; VIRUS INFECTION;

HUMANS; LUNG; MYCOBACTERIUM BOVIS; RESPIRATORY TRACT INFECTIONS; T-LYMPHOCYTES; TUBERCULOSIS VACCINES; VIRUS DISEASES;

EID: 53849128925     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.7.8.1165     Document Type: Review

References (69)

1. WHO. Global Tuberculosis Control - Surveillance, Planning, Financing. WHO/HTM/TB/2008.393 (2008).
2. Friedland G. Tuberculosis, drug resistance, and HIV/AIDS: a triple threat. Curr. Infect. Dis. Rep. 9(3), 252-261 (2007).
3. Fine PE. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346(8986), 1339-1345 (1995).
4. Openshaw P. T cells take the inside track. Nat. Med. 12(6), 614-615 (2006).
5. Liang S, Mozdzanowska K, Palladino G, Gerhard W. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 152(4), 1653-1661 (1994). •• Important article on the time course of decline of lung immunity.
6. Reece ST, Kaufmann SH. Rational design of vaccines against tuberculosis directed by basic immunology. Int. J. Med. Microbiol. 298(1-2), 143-150 (2008).
7. Rook GA, Dheda K, Zumla A. Immune responses to tuberculosis in developing countries: implications for new vaccines. Nat. Rev. Immunol. 5(8), 661-667 (2005).
8. Tedder TF, Steeber DA, Chen A, Engel P. The selectins: vascular adhesion molecules. FASEB J. 9(10), 866-873 (1995).
9. Doerschuk CM. Leukocyte trafficking in alveoli and airway passages. Respir. Res. 1(3), 136-140 (2000).
10. + T cells that persist in the lungs. J. Exp. Med. 193(8), 981-986 (2001).
11. Legge KL, Braciale TJ. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18(2), 265-277 (2003).
12. + T cells during pulmonary influenza virus infection. J. Immunol. 173(2), 1209-1218 (2004).
13. Feng CG, Britton WJ, Palendira U et al. Up-regulation of VCAM-1 and differential expansion of β integrin-expressing T lymphocytes are associated with immunity to pulmonary Mycobacterium tuberculosis infection. J. Immunol. 164(9), 4853-4860 (2000).
14. + T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166(3), 1813-1822 (2001).
15. Ostler T, Hussell T, Surh CD, Openshaw P, Ehl S. Long-term persistence and reactivation of T cell memory in the lung of mice infected with respiratory syncytial virus. Eur. J. Immunol. 31(9), 2574-2582 (2001).
16. Marshall DR, Turner SJ, Belz GT et al. Measuring the diaspora for virus-specific CD8+ T cells. Proc. Natl Acad. Sci. USA 98(11), 6313-6318 (2001).
17. Debes GF, Arnold CN, Young AJ et al. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat. Immunol. 6(9), 889-894 (2005).
18. Bromley SK, Thomas SY, Luster AD. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat. Immunol. 6(9), 895-901 (2005).
19. + T cells in the lung airways depends on proliferation. J. Immunol. 169(9), 4976-4981 (2002).
20. Zammit DJ, Turner DL, Klonowski KD, Lefrancois L, Cauley LS. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24(4), 439-449 (2006). •• Description of the importance of persisting antigen for the maintenance of lung immunity.
21. Julia V, Hessel EM, Malherbe L et al. A restricted subset of dendritic cells captures airborne antigens and remains able to activate specific T cells long after antigen exposure. Immunity 16(2), 271-283 (2002). • Description of the role of persisting antigen in a model of allergy.
22. Mora JR, Cheng G, Picarella D et al. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201(2), 303-316 (2005).
23. Holt PG, Strickland DH, Wikstrom ME, Jahnsen FL. Regulation of immunological homeostasis in the respiratory tract. Nat. Rev. Immunol. 8(2), 142-152 (2008).
24. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 10(9), 927-934 (2004).
25. Xu B, Wagner N, Pham LN et al. Lymphocyte homing to bronchus-associated lymphoid tissue (BALT) is mediated by L-selectin/PNAd, α4β1 integrin/VCAM-1, and LFA-1 adhesion pathways. J. Exp. Med. 197(10), 1255-1267 (2003).
26. + T cells into the interstitium of the normal lung. J. Clin. Invest. 115(12), 3473-3483 (2005).
27. Ray SJ, Franki SN, Pierce RH et al. The collagen binding α1β1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity 20(2), 167-179 (2004).
28. Ainslie MP, McNulty CA, Huynh T, Symon FA, Wardlaw AJ. Characterisation of adhesion receptors mediating lymphocyte adhesion to bronchial endothelium provides evidence for a distinct lung homing pathway. Thorax 57(12), 1054-1059 (2002).
29. Abitorabi MA, Mackay CR, Jerome EH et al. Differential expression of homing molecules on recirculating lymphocytes from sheep gut, peripheral, and lung lymph. J. Immunol. 156(9), 3111-3117 (1996).
30. Zabel BA, Agace WW, Campbell JJ et al. Human G protein-coupled receptor GPR-9-6/CC chemokine receptor 9 is selectively expressed on intestinal homing T lymphocytes, mucosal lymphocytes, and thymocytes and is required for thymus-expressed chemokine-mediated chemotaxis. J. Exp. Med. 190(9), 1241-1256 (1999).
31. Campbell JJ, Bowman EP, Murphy K et al. 6-C-kine (SLC), a lymphocyte adhesion-triggering chemokine expressed by high endothelium, is an agonist for the MIP-3β receptor CCR7. J. Cell Biol. 141(4), 1053-1059 (1998).
32. Campbell JJ, Brightling CE, Symon FA et al. Expression of chemokine receptors by lung T cells from normal and asthmatic subjects. J. Immunol. 166(4), 2842-2848 (2001).
33. Morgan AJ, Guillen C, Symon FA et al. Expression of CXCR6 and its ligand CXCL16 in the lung in health and disease. Clin. Exp. Allergy 35(12), 1572-1580 (2005).
34. Goonetilleke NP, McShane H, Hannan CM et al. Enhanced immunogenicity and protective efficacy against Mycobacterium tuberculosis of bacille Calmette-Guerin vaccine using mucosal administration and boosting with a recombinant modified vaccinia virus Ankara. J. Immunol. 171(3), 1602-1609 (2003).
35. Santosuosso M, McCormick S, Zhang X, Zganiacz A, Xing Z. Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral Mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect. Immun. 74(8), 4634-464 (2006). •• Clear description of the markedly enhanced protection against Mycobacterium tuberculosis, obtained by intranasal immunization.
36. Santosuosso M, Zhang X, McCormick S et al. 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(12), 7986-7994 (2005).
37. Wang J, Thorson L, Stokes RW et al. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J. Immunol. 173(10), 6357-6365 (2004).
38. Marzo AL, Yagita H, Lefrancois L. Cutting edge: migration to nonlymphoid tissues results in functional conversion of central to effector memory CD8 T cells. J. Immunol. 179(1), 36-40 (2007).
39. + T cells but not rested effectors to migrate to non-lymphoid sites in the absence of inflammation. J. Biol. Chem. 282(9), 6106-6115 (2007).
40. Radosevic K, Wieland CW, Rodriguez A et al. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of γ interferon. Infect. Immun. 75(8), 4105-4115 (2007).
41. Santosuosso M, McCormick S, Roediger E et al. Mucosal luminal manipulation of T cell geography switches on protective efficacy by otherwise ineffective parenteral genetic immunization. J. Immunol. 178(4), 2387-2395 (2007).
42. Jung YJ, Ryan L, LaCourse R, North RJ. Properties and protective value of the secondary versus primary T helper type 1 response to airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 201(12), 1915-1924 (2005).
43. Ehrt S, Shiloh MU, Ruan J et al. A novel antioxidant gene from Mycobacterium tuberculosis. J. Exp. Med. 186(11), 1885-1896 (1997).
44. Armstrong JA, Hart PD. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J. Exp. Med. 142(1), 1-16 (1975).
45. van der Wel N, Hava D, Houben D et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129(7), 1287-1298 (2007).
46. Forbes EK, Sander C, Ronan EO et al. 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) (In Press).
47. Minne A, Louahed J, Mehauden S et al. The delivery site of a monovalent influenza vaccine within the respiratory tract impacts on the immune response. Immunology 122(3), 316-325 (2007).
48. Corbett M, Bogers WM, Heeney JL et al. Aerosol immunization with NYVAC and MVA vectored vaccines is safe, simple, and immunogenic. Proc. Natl Acad. Sci. USA 105(6), 2046-2051 (2008).
49. Johnson PR, Feldman S, Thompson JM, Mahoney JD, Wright PF. Immunity to influenza A virus infection in young children: a comparison of natural infection, live cold-adapted vaccine, and inactivated vaccine. J. Infect. Dis. 154(1), 121-127 (1986).
50. Dilraj A, Cutts FT, de Castro JF et al. Response to different measles vaccine strains given by aerosol and subcutaneous routes to schoolchildren: a randomised trial. Lancet 355(9206), 798-803 (2000).
51. Rosenthal SR, McEnery JT, Raisys N. Aerogenic BCG vaccination against tuberculosis in animal and human subjects. J. Asthma Res. 5(4), 309-323 (1968).
52. Garcia-Contreras L, Wong YL, Muttil P et al. Immunization by a bacterial aerosol. Proc. Nat. Acad. Sci. USA 105(12), 4656-4660 (2008).
53. Dietrich J, Andersen C, Rappuoli R et al. Mucosal administration of Ag85B-ESAT-6 protects against infection with Mycobacterium tuberculosis and boosts prior bacillus Calmette-Guerin immunity. J. Immunol. 177(9), 6353-6360 (2006).
54. Taylor JL, Turner OC, Basaraba RJ et al. Pulmonary necrosis resulting from DNA vaccination against tuberculosis. Infect. Immun. 71(4), 2192-2198 (2003).
55. Kim EY, Battaile JT, Patel AC et al. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14(6), 633-640 (2008).
56. Egilmez NK, Kilinc MO, Gu T, Conway TF. Controlled-release particulate cytokine adjuvants for cancer therapy. Endocr. Metab. Immune Disord. Drug Targets 7(4), 266-270 (2007).
57. Liang MT, Davies NM, Blanchfield JT, Toth I. Particulate systems as adjuvants and carriers for peptide and protein antigens. Curr. Drug Deliv. 3(4), 379-388 (2006).
58. Iwata M, Hirakiyama A, Eshima Y et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21(4), 527-538 (2004).
59. Sigmundsdottir H, Pan J, Debes GF et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat. Immunol. 8(3), 285-293 (2007).
60. + T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8(4), 369-377 (2007).
61. + T cell functionality and mucosal homing. Virology 367(1), 156-167 (2007).
62. Karonga Prevention Trial Group. Randomised controlled trial of single BCG, repeated BCG, or combined BCG and killed Mycobacterium leprae vaccine for prevention of leprosy and tuberculosis in Malawi. Lancet 348(9019), 17-24 (1996).
63. Grode L, Kursar M, Fensterle J, Kaufmann SH, Hess J. Cell-mediated immunity induced by recombinant Mycobacterium bovis bacille Calmette-Guerin strains against an intracellular bacterial pathogen: importance of antigen secretion or membrane-targeted antigen display as lipoprotein for vaccine efficacy. J. Immunol. 168(4), 1869-1876 (2002).
64. + T cells are sufficient to mediate protection against Mycobacterium tuberculosis infection. Infect. Immun. 76(5), 2249-2255 (2008).
65. Sambandamurthy VK, Derrick SC, Jalapathy KV et al. Long-term protection against tuberculosis following vaccination with a severely attenuated double lysine and pantothenate auxotroph of Mycobacterium tuberculosis. Infect. Immun. 73(2), 1196-1203 (2005).
66. Olsen AW, Hansen PR, Holm A, Andersen P. Efficient protection against Mycobacterium tuberculosis by vaccination with a single subdominant epitope from the ESAT-6 antigen. Eur. J. Immunol. 30(6), 1724-1732 (2000).
67. Baldwin SL, D'Souza C, Roberts AD et al. Evaluation of new vaccines in the mouse and guinea pig model of tuberculosis. Infect. Immun. 66(6), 2951-2959 (1998).
68. Lin MY, Ottenhoff TH. Not to wake a sleeping giant: new insights into host-pathogen interactions identify new targets for vaccination against latent Mycobacterium tuberculosis infection. Biol. Chem. DOI: 10.1515/BC.2008.057 (2008) (Epub ahead of print).
69. McShane H, Pathan AA, Sander CR et al. Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat. Med. 10(11), 1240-1244 (2004).