A multi-antigenic adenoviral-vectored vaccine improves BCG-induced protection of goats against pulmonary tuberculosis infection and prevents disease progression

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Pérez De Val, Bernat ^a   Vidal, Enric ^a   Villarreal Ramos, Bernardo ^b   Gilbert, Sarah C ^c   Andaluz, Anna ^a   Moll, Xavier ^a   Martín, Maite ^a   Nofrarías, Miquel ^a   McShane, Helen ^c   Vordermeier, H Martin ^b   Domingo, Mariano ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; BCG VACCINE; GAMMA INTERFERON; MYCOBACTERIUM VACCINE; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CELLULAR IMMUNITY; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG EFFICACY; FEMALE; GENETIC IMMUNIZATION; HISTOPATHOLOGY; HUMORAL IMMUNITY; INFECTION PREVENTION; KID (GOAT); LUNG TUBERCULOSIS; MEMORY T LYMPHOCYTE; MYCOBACTERIUM CAPRAE; NONHUMAN; WEIGHT GAIN; ADENOVIRIDAE; ADMINISTRATION AND DOSAGE; ANIMAL; ANIMAL DISEASES; BIOSYNTHESIS; BLOOD; BODY WEIGHT; DISEASE COURSE; GENE VECTOR; GENETICS; GOAT; GRANULOMA; IMMUNIZATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LUNG; MICROBIOLOGY; NECROSIS; PATHOLOGY; T LYMPHOCYTE; VETERINARY;

ADENOVIRIDAE; ANIMAL DISEASES; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL LOAD; BCG VACCINE; BODY WEIGHT; DISEASE PROGRESSION; FEMALE; GENETIC VECTORS; GOATS; GRANULOMA; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; LUNG; NECROSIS; T-LYMPHOCYTES; TUBERCULOSIS, PULMONARY;

EID: 84896690060     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081317     Document Type: Article

References (47)

1. Lienhardt C, Glaziou P, Uplekar M, Lonnroth K, Getahun H, et al. (2012) Global tuberculosis control: Lessons learnt and future prospects. Nat Rev Microbiol 10: 407-416.
2. World Health Organization (2009) Global tuberculosis control: A short update to the 2009 report. Geneva, WHO.
3. Daniel R, Evans H, Rolfe S, de la Rua-Domenech R, Crawshaw T, et al. (2009) Outbreak of tuberculosis caused by mycobacterium bovis in golden guernsey goats in great britain. Vet Rec 165: 335-342.
4. Rodriguez S, Bezos J, Romero B, de Juan L, Alvarez J, et al. (2011) Mycobacterium caprae infection in livestock and wildlife, spain. Emerg Infect Dis 17: 532-535.
5. Shuralev E, Quinn P, Doyle M, Duignan A, Kwok HF, et al. (2012) Application of the enfer chemiluminescent multiplex ELISA system for the detection of mycobacterium bovis infection in goats. Vet Microbiol 154: 292-297.
6. Napp S, Allepuz A, Mercader I, Nofrarías M, López-Soria S, et al. (2013) Evidence of goats acting as domestic reservoirs of bovine tuberculosis. Vet Rec 172: 663-663.
7. Erler W, Martin G, Sachse K, Naumann L, Kahlau D, et al. (2004) Molecular fingerprinting of mycobacterium bovis subsp. caprae isolates from central europe. J Clin Microbiol 42: 2234-2238.
8. Domogalla J, Prodinger WM, Blum H, Krebs S, Gellert S, et al. (2013) Region of difference four (RD4) in alpine mycobacterium caprae isolates indicates three variants. J Clin Microbiol.
9. Kubica T, Rusch-Gerdes S, Niemann S (2003) Mycobacterium bovis subsp. caprae caused one-third of human M. bovis-associated tuberculosis cases reported in germany between 1999 and 2001. J Clin Microbiol 41: 3070-3077.
10. Prodinger WM, Brandstatter A, Naumann L, Pacciarini M, Kubica T, et al. (2005) Characterization of mycobacterium caprae isolates from europe by mycobacterial interspersed repetitive unit genotyping. J Clin Microbiol 43: 4984-4992.
11. Rodríguez E, Sánchez LP, Pérez S, Herrera L, Jiménez MS, et al. (2009) Human tuberculosis due to mycobacterium bovis and M. caprae in spain, 20042007. Int J Tuberc Lung Dis 13: 1536-1541.
12. Krebs JR, The Independent Scientific Review Group (1997) Bovine tuberculosis in cattle and badgers. London, Ministry of Agriculture, Fisheries and Food Publications, London, UK.
13. Fine PE (1995) Variation in protection by BCG: Implications of and for heterologous immunity. Lancet 346: 1339-1345.
14. Buddle BM, de Lisle GW, Pfeffer A, Aldwell FE (1995) Immunological responses and protection against mycobacterium bovis in calves vaccinated with a low dose of BCG. Vaccine 13: 1123-1130.
15. Waters WR, Palmer MV, Buddle BM, Vordermeier HM (2012) Bovine tuberculosis vaccine research: Historical perspectives and recent advances. Vaccine 30: 2611-2622.
16. Skeiky YA, Sadoff JC (2006) Advances in tuberculosis vaccine strategies. Nat Rev Microbiol 4: 469-476.
17. McShane H, Hill A (2005) Prime-boost immunisation strategies for tuberculosis. Microb Infect 7: 962-967.
18. Xing Z, Charters TJ (2007) Heterologous boost vaccines for bacillus calmetteguerin prime immunization against tuberculosis. Expert Review of Vaccines 6: 539-546.
19. Wang J, Thorson L, Stokes RW, Santosuosso M, Huygen K, et al. (2004) Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J Immunol 173: 6357-6365.
20. Santosuosso M, McCormick S, Zhang X, Zganiacz A, Xing Z (2006) Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect Immun 74: 4634-4643.
21. Xing Z, McFarland CT, Sallenave JM, Izzo A, Wang J, et al. (2009) Intranasal mucosal boosting with an adenovirus-vectored vaccine markedly enhances the protection of BCG-primed guinea pigs against pulmonary tuberculosis. PLoS One 4: e5856.
22. Vordermeier HM, Huygen K, Singh M, Hewinson RG, Xing Z (2006) Immune responses induced in cattle by vaccination with a recombinant adenovirus expressing mycobacterial antigen 85A and mycobacterium bovis BCG. Infect Immun 74: 1416-1418.
23. Vordermeier HM, Villarreal-Ramos B, Cockle PJ, McAulay M, Rhodes SG, et al. (2009) Viral booster vaccines improve mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infect Immun 77: 3364-3373.
24. Pérez de Val B, Villarreal-Ramos B, Nofrarías M, López-Soria S, Romera N, et al. (2012) Goats primed with mycobacterium bovis BCG and boosted with a recombinant adenovirus expressing Ag85A show enhanced protection against tuberculosis. Clin Vaccine Immunol 19: 1339-1347.
25. Dean GS, Rhodes SG, Coad M, Whelan AO, Wheeler P, et al. (2008) Isoniazid treatment of mycobacterium bovis in cattle as a model for human tuberculosis. Tuberculosis 88: 586-594.
26. Aranaz A, Liebana E, Gomez-Mampaso E, Galan J, Cousins D, et al. (1999) Mycobacterium tuberculosis subsp. caprae subsp. nov.: A taxonomic study of a new member of the mycobacterium tuberculosis complex isolated from goats in spain. Int J Syst Bacteriol 49: 1263-1273.
27. Pérez de Val B, López-Soria S, Nofrarías M, Martín M, Vordermeier HM, et al. (2011) Experimental model of tuberculosis in the domestic goat after endobronchial infection with mycobacterium caprae. Clin Vaccine Immunol 18: 1872-1881.
28. Wangoo A, Johnson L, Gough J, Ackbar R, Inglut S, et al. (2005) Advanced granulomatous lesions in mycobacterium bovis-infected cattle are associated with increased expression of type I procollagen, γδ (WC1+) T cells and CD 68+ cells. J Comp Pathol 133: 223-234.
29. Garcia-Jimenez WL, Benitez-Medina JM, Fernandez-Llario P, Abecia JA, Garcia-Sanchez A, et al. (2012) Comparative pathology of the natural infections by mycobacterium bovis and by mycobacterium caprae in wild boar (sus scrofa). Transbound Emerg Dis 60:102-109.
30. Vordermeier M, Whelan AO (2012) ELISPOT assays to enumerate bovine IFN-gamma-secreting cells for the development of novel vaccines against bovine tuberculosis. Methods Mol Biol 792: 219-227.
31. Canetti G (1955) The tubercle bacillus in the pulmonary lesion of man. histobacteriology and its bearing on the therapy of pulmonary tuberculosis. New York, Springer Pub Co.
32. Gil O, Díaz I, Vilaplana C, Tapia G, Díaz J, et al. (2010) Granuloma encapsulation is a key factor for containing tuberculosis infection in minipigs. PLoS One 5: e10030.
33. Plopper CG, Harkema JR (2005) The respiratory sytem and its use in research. The laboratory primate Elsevier Academic Press, San Diego 30: 503-526.
34. Domingo M, Gil O, Serrano E, Guirado E, Nofrarias M, et al. (2009) Effectiveness and safety of a treatment regimen based on isoniazid plus vaccination with mycobacterium tuberculosis cells' fragments: Field-study with naturally mycobacterium caprae-infected goats. Scand J Immunol 69: 500-507.
35. Hewinson RG, Vordermeier HM, Buddle BM (2003) Use of the bovine model of tuberculosis for the development of improved vaccines and diagnostics. Tuberculosis 83: 119-130.
36. Buddle B, Skinner M, NeilWedlock D, deLisle G, MartinVordermeier H, et al. (2005) Cattle as a model for development of vaccines against human tuberculosis. Tuberculosis 85: 19-24.
37. Guirado E, Gil O, Cáceres N, Singh M, Vilaplana C, et al. (2008) Induction of a specific strong polyantigenic cellular immune response after short-term chemotherapy controls bacillary reactivation in murine and guinea pig experimental models of tuberculosis. Clin Vaccine Immunol 15: 1229-1237.
38. Keating SM, Bejon P, Berthoud T, Vuola JM, Todryk S, et al. (2005) Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. J Immunol 175: 5675-5680.
39. 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.
40. Lyashchenko K, Whelan AO, Greenwald R, Pollock JM, Andersen P, et al. (2004) Association of tuberculin-boosted antibody responses with pathology and cell-mediated immunity in cattle vaccinated with mycobacterium bovis BCG and infected with M-bovis. Infect Immun 72: 2462-2467.
41. Tameris MD, Hatherill M, Landry BS, Scriba TJ, Snowden MA, et al. (2013) Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: A randomised, placebo-controlled phase 2b trial. Lancet 381:1021-1028.
42. Dietrich J, Andersen C, Rappuoli R, Doherty TM, Jensen CG, et al. (2006) Mucosal administration of Ag85B-ESAT-6 protects against infection with mycobacterium tuberculosis and boosts prior bacillus calmette-guerin immunity. J Immunol 177: 6353-6360.
43. Lin PL, Dietrich J, Tan E, Abalos RM, Burgos J, et al. (2012) The multistage vaccine H56 boosts the effects of BCG to protect cynomolgus macaques against active tuberculosis and reactivation of latent mycobacterium tuberculosis infection. J Clin Invest 122: 303-314.
44. Kyd JM, Foxwell AR, Cripps AW (2001) Mucosal immunity in the lung and upper airway. Vaccine 19: 2527-2533.
45. Ottenhoff TH, Kaufmann SH (2012) Vaccines against tuberculosis: Where are we and where do we need to go? PLoS Pathog 8: e1002607.
46. Kaufmann SH (2010) Future vaccination strategies against tuberculosis: Thinking outside the box. Immunity 33: 567-577.
47. Whelan A, Court P, Xing Z, Clifford D, Hogarth PJ, et al. (2012) Immunogenicity comparison of the intradermal or endobronchial boosting of BCG vaccinates with Ad5-85A. Vaccine 30: 6294-6300.