Lactococcus lactis carrying a DNA vaccine coding for the ESAT-6 antigen increases IL-17 cytokine secretion and boosts the BCG vaccine immune response

Journal of Applied Microbiology

Volumn 122, Issue 6, 2017, Pages 1657-1662

  Pereira, V B ^a   da Cunha, V P ^a   Preisser, T M ^a   Souza, B M ^a   Turk, M Z ^a   De Castro, C P ^a   Azevedo, M S P ^a   Miyoshi, A ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

BCG; DNA vaccine; ESAT 6; Lactococcus lactis; tuberculosis

Indexed keywords

DNA; IMMUNE SYSTEM; IMMUNIZATION; MAMMALS;

BACILLE CALMETTE—GUERIN; CYTOKINE SECRETIONS; DNA VACCINE; ESAT-6; FIBRONECTIN-BINDING PROTEIN; IMMUNE RESPONSE; IMMUNOGENICITY; LACTOCOCCUS LACTIS; PROTEIN A; TUBERCULOSIS;

VACCINES;

BCG VACCINE; DNA VACCINE; EARLY SECRETORY ANTIGENIC TARGET 6; FIBRONECTIN BINDING PROTEIN; FIBRONECTIN BINDING PROTEIN A; GAMMA INTERFERON; IMMUNOGLOBULIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; SECRETORY IMMUNOGLOBULIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CYTOKINE; ESAT-6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS;

ANTIGEN; BACTERIUM; DNA; IMMUNE RESPONSE; PROTEIN; RODENT; SECRETION; TUBERCULOSIS; VACCINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; COLON TISSUE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOGLOBULIN PRODUCTION; LACTOCOCCUS LACTIS; MOUSE; NONHUMAN; SPLEEN CELL; TH1 CELL; TISSUE HOMOGENATE; VACCINATION; ANIMAL; BLOOD; FEMALE; GENETICS; IMMUNOLOGY; METABOLISM; SECRETION (PROCESS);

LACTOCOCCUS LACTIS; MUS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BCG VACCINE; CYTOKINES; FEMALE; INTERLEUKIN-17; INTERLEUKIN-6; LACTOCOCCUS LACTIS; MICE; TUMOR NECROSIS FACTOR-ALPHA; VACCINES, DNA;

EID: 85018772975     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13449     Document Type: Article

References (29)

1. Cervantes-Villagrana, A.R., Hernández-Pando, R., Biragyn, A., Castañeda-Delgado, J., Bodogai, M., Martínez-Fierro, M., Sada, E., Trujillo, V. et al. (2013) Prime-boost BCG vaccination with DNA vaccines based in β-defensin-2 and mycobacterial antigens ESAT6 or Ag85B improve protection in a tuberculosis experimental model. Vaccine 11, 676–684.
2. Chandrashekara, S., Anupama, K.R., Sambarey, A. and Chandra, N. (2016) High IL-6 and low IL-15 levels mark the presence of TB infection: a preliminary study. Cytokine 12, 57–62.
3. Chatel, J.M., Pothelune, L., Ah-Leung, S., Corthier, G., Wal, J.M. and Langella, P. (2008) In vivo transfer of plasmid from food-grade transiting Lactococci to murine epithelial cells. Gene Ther 15, 1184–1190.
4. Chen, H., Cheng, C., Li, M., Gao, S., Li, S. and Sun, H. (2014) Expression of TNF-alpha, IFN-gamma, TGF-beta, and IL-4 in the spinal tuberculous focus and its impact on the disease. Cell Biochem Biophys 70, 1759–1764.
5. Das Gupta, S.K., Jain, S., Kaushal, D. and Tyagi, A.K. (1998) Expression systems for study of mycobacterial gene regulation and development of recombinant BCG vaccines. Biochem Biophys Res Commun 246, 797–804.
6. Dey, B., Jain, R., Khera, A., Rao, V., Dhar, N., Guptad, U.D., Katochd, V.M., Ramanathane, V.D. et al. (2010) Boosting with a DNA vaccine expressing ESAT-6 (DNAE6) obliterates the protection imparted by recombinant BCG (rBCGE6) against aerosol Mycobacterium tuberculosis infection in guinea pigs. Vaccine 28, 63–70.
7. Dhar, N., Rao, V. and Tyagi, A.K. (2000) Recombinant BCG approach for development of vaccines: cloning and expression of immunodominant antigens of M. tuberculosis. FEMS Microbiol Lett 190, 309–316.
8. Dou, J., Wang, Y., Yu, F., Yang, H., Wang, J., He, X., Xu, W., Chen, J. et al. (2012) Protection against Mycobacterium tuberculosis challenge in mice by DNA vaccine Ag85A-ESAT-6-IL-21 priming and BCG boosting. Int J Immunogenet 39, 183–190.
9. Ergun, T., Seckin, D., Baskan, B.E., Onsun, N., Ozgen, Z., Unalan, P., Alpsoy, E. and Karakurt, S. (2015) The risk of tuberculosis in patients with psoriasis treated with anti-tumor necrosis factor agents. Int J Dermatol 54, 594–599.
10. Fan, X., Gao, Q. and Fu, R. (2007) DNA vaccine encoding ESAT-6 enhances the protective efficacy of BCG against Mycobacterium tuberculosis infection in mice. Scand J Immunol 66, 523–528.
11. Green, M.R. and Sambrook, J. (2012) Molecular Cloning: A Laboratory Manual, 4th edn. New York: Cold Spring Harbor Press.
12. Guimarães, V., Innocentin, S., Chatel, J.M., Lefevre, F., Langella, P., Azevedo, V. and Miyoshi, A. (2009) A new plasmid vector for DNA delivery using lactococci. Genet Vaccines Ther 7, 4.
13. Innocentin, S., Guimarães, V., Myoshi, A., Azevedo, V., Langella, P., Chatel, J.M. and Lefèvre, F. (2009) Lactococcus lactis expressing either Staphylococcus aureus fibronectin-binding protein A or Listeria monocytogenes Internalin A can efficiently internalize and deliver DNA in human epithelial cells. Appl Environ Microbiol 75, 4870–4878.
14. Ji, P., Hu, Z.D., Kang, H., Yuan, Q., Ma, H., Wen, H.L., Wu, J., Li, Z.M. et al. (2016) Boosting BCG-primed mice with chimeric DNA vaccine HG856A induces potent multifunctional T cell responses and enhanced protection against Mycobacterium tuberculosis. Immunol Res 64, 64–72.
15. Kim, E.S., Song, G.A., Cho, K.B., Park, K.S., Kim, K.O., Jang, B.I., Kim, E.Y., Jeon, S.W. et al. (2015) Significant risk and associated factors of active tuberculosis infection in Korean patients with inflammatory bowel disease using anti-TNF agents. World J Gastroenterol 21, 3308–3316.
16. Kutzler, M.A. and Weiner, D.B. (2008) DNA vaccines: ready for prime time? Nat Rev Genet 9, 776–788.
17. Ladel, C.H., Blum, C., Dreher, A., Reifenberg, K., Kopf, M. and Kaufmann, S.H. (1997) Lethal tuberculosis in interleukin-6-deficient mutant mice. Infect Immun 65, 4843–4849.
18. Lockhart, E., Green, A. and Flynn, J. (2006) IL-17 production is dominated by gamma-delta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 177, 4662–4669.
19. Lu, J., Wang, C., Zhou, Z., Zhang, Y., Cao, T., Shi, C., Chen, Z., Chen, L. et al. (2011) Immunogenicity and protective efficacy against murine tuberculosis of a prime-boost regimen with BCG and a DNA vaccine expressing ESAT-6 and Ag85A fusion protein. Clin Dev Immunol 2011, 617892.
20. Pereira, V.B., Saraiva, T.D., Souza, B.M., Zurita-Turk, M., Azevedo, M.S., De Castro, C.P., Mancha-Agresti, P., Dos Santos, J.S. et al. (2015) Development of a new DNA vaccine based on mycobacterial ESAT-6 antigen delivered by recombinant invasive Lactococcus lactis FnBPA+. Appl Microbiol Biotechnol 99, 1817–1826.
21. Pontes, D., Innocentin, S., Del Carmen, S., Almeida, J.F., Leblanc, J.G., de Moreno de Leblanc, A., Blugeon, S., Cherbuy, C. et al. (2012) Production of fibronectin binding protein A at the surface of Lactococcus lactis increases plasmid transfer in vitro and in vivo. PLoS ONE 7, e44892.
22. Pym, A.S., Brodin, P., Brosch, R., Huerre, M. and Cole, S.T. (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46, 709–717.
23. Que, Y.A., Francois, P., Haefliger, J.A., Entenza, J.M., Vaudaux, P. and Moreillon, P. (2001) Reassessing the role of Staphylococcus aureus clumping factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect Immun 69, 6296–6302.
24. Tan, K., Liang, J., Teng, X., Wang, X., Zhang, J., Yuan, X. and Fan, X. (2014) Comparison of BCG prime-DNA booster and rBCG regimens for protection against tuberculosis. Hum Vaccin Immunother 10, 391–398.
25. Torrado, E. and Cooper, A.M. (2010) IL-17 and Th17 cells in tuberculosis. Cytokine Growth Factor Rev 21, 455–462.
26. Umemura, M., Yahagi, A., Hamada, S., Begum, M.D., Watanabe, H., Kawakami, K., Suda, T., Sudo, K. et al. (2007) IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis Bacille Calmette-Guerin infection. J Immunol 178, 3786–3796.
27. Wang, Q.L., Pan, Q., Ma, Y., Wang, K., Sun, P., Liu, S. and Zhang, X.L. (2009) An attenuated Salmonella-vectored vaccine elicits protective immunity against Mycobacterium tuberculosis. Vaccine 27, 6712–6722.
28. World Health Organization (2012) Global Tuberculosis Report 2012. Available at: http://apps.who.int/iris/bitstream/10665/75938/1/9789241564502_eng.pdf.
29. Yoshida, Y.O., Umemura, M., Yahagi, A., O'Brien, R., Ikuta, K., Kishihara, K., Hara, H., Nakae, S. et al. (2010) Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J Immunol 184, 4414–4422.