Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Potentiation of Th1-Type Immune Responses to Mycobacterium tuberculosis Antigens in Mice by Cationic Liposomes Combined with De-O-Acylated Lipooligosaccharide

  • Ko, Ara (Department of Bioscience and Biotechnology, Sejong University) ;
  • Wui, Seo Ri (Department of Bioscience and Biotechnology, Sejong University) ;
  • Ryu, Ji In (Department of Bioscience and Biotechnology, Sejong University) ;
  • Lee, Yeon Jeong (Department of Bioscience and Biotechnology, Sejong University) ;
  • Hien, Do Thi Thu (Department of Bioscience and Biotechnology, Sejong University) ;
  • Rhee, Inmoo (Department of Bioscience and Biotechnology, Sejong University) ;
  • Shin, Sung Jae (Department of Microbiology, Institute for Immunology and Immunological Diseases, Yonsei University College of Medicine) ;
  • Park, Shin Ae (R & D Center, EyeGene) ;
  • Kim, Kwang Sung (Department of Bioscience and Biotechnology, Sejong University) ;
  • Cho, Yang Je (R & D Center, EyeGene) ;
  • Lee, Na Gyong (Department of Bioscience and Biotechnology, Sejong University)
  • Received : 2017.09.12
  • Accepted : 2017.10.28
  • Published : 2018.01.28
Download PDF
⟨ Previous Next ⟩

Abstract

Tuberculosis (TB) is an infectious disease caused by Mycobacterium tuberculosis. Bacillus Calmette-$Gu\acute{e}rin$ (BCG) vaccine is the only TB vaccine currently available, but it is not sufficiently effective in preventing active pulmonary TB or adult infection. With the purpose of developing an improved vaccine against TB that can overcome the limitations of the current BCG vaccine, we investigated whether adjuvant formulations containing de-O-acylated lipooligosaccharide (dLOS) are capable of enhancing the immunogenicity and protective efficacy of TB subunit vaccines. The results revealed that the dLOS/dimethyl dioctadecyl ammonium bromide (DDA) adjuvant formulation significantly increased both humoral and Th1-type cellular responses to TB subunit vaccine that are composed of three antigens, Ag85A, ESAT-6, and HspX. The adjuvanted TB vaccine also effectively induced the Th1-type response in a BCG-primed mouse model, suggesting a potential as a booster vaccine. Finally, the dLOS/DDA-adjuvanted TB vaccine showed protective efficacy against M. tuberculosis infection in vitro and in vivo. These data indicate that the dLOS/DDA adjuvant enhances the Th1-type immunity and protective efficacy of the TB subunit vaccine, suggesting that it would be a promising adjuvant candidate for the development of a booster vaccine.

Keywords

References

  1. World Health Organization. 2014. Global tuberculosis report. WHO, Geneva, Switzerland.
  2. Kaufmann SH. 2010. Future vaccination strategies against tuberculosis: thinking outside the box. Immunity 33: 567-577. https://doi.org/10.1016/j.immuni.2010.09.015
  3. Kaufmann SH. 2012. Tuberculosis vaccine development: strength lies in tenacity. Trends Immunol. 33: 373-379. https://doi.org/10.1016/j.it.2012.03.004
  4. Sacksteder KA, Nacy CA. 2002. New tuberculosis vaccine development. Expert Opin. Biol. Ther. 2: 741-749. https://doi.org/10.1517/14712598.2.7.741
  5. Kaufmann SHE, Hussey G, Lambert PH. 2010. New vaccines for tuberculosis. Lancet 375: 2110-2119. https://doi.org/10.1016/S0140-6736(10)60393-5
  6. Brandt L, Skeiky YA, Alderson MR, Lobet Y, Dalemans W, Turner OC, et al. 2004. The protective effect of the Mycobacterium bovis BCG vaccine is increased by coadministration with the Mycobacterium tuberculosis 72-kilodalton fusion polyprotein Mtb72F in M. tuberculosisinfected guinea pigs. Infect. Immun. 72: 6622-6632. https://doi.org/10.1128/IAI.72.11.6622-6632.2004
  7. Garcon N, Chomez P, Van Mechelen M. 2007. GlaxoSmithKline Adjuvant Systems in vaccines: concepts, achievements and perspectives. Expert Rev. Vaccines 6: 723-739. https://doi.org/10.1586/14760584.6.5.723
  8. Harandi AM, Medaglini D, Shattock RJ, Europrise WGC. 2010. Vaccine adjuvants: a priority for vaccine research. Vaccine 28: 2363-2366. https://doi.org/10.1016/j.vaccine.2009.12.084
  9. Skeiky YA, Alderson MR, Ovendale PJ, Guderian JA, Brandt L, Dillon DC, et al. 2004. Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J. Immunol. 172: 7618-7628. https://doi.org/10.4049/jimmunol.172.12.7618
  10. Agger EM, Rosenkrands I, Olsen AW, Hatch G, Williams A, Kritsch C, et al. 2006. Protective immunity to tuberculosis with Ag85B-ESAT-6 in a synthetic cationic adjuvant system IC31. Vaccine 24: 5452-5460.
  11. Lindenstrom T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, Seder RA, et al. 2009. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J. Immunol. 182: 8047-8055. https://doi.org/10.4049/jimmunol.0801592
  12. van Dissel JT, Soonawala D, Joosten SA, Prins C, Arend SM, Bang P, et al. 2011. Ag85B-ESAT-6 adjuvanted with IC31(R) promotes strong and long-lived Mycobacterium tuberculosis specific T cell responses in volunteers with previous BCG vaccination or tuberculosis infection. Vaccine 29: 2100-2109.
  13. Woodworth JS, Cohen SB, Moguche AO, Plumlee CR, Agger EM, Urdahl KB, et al. 2017. Subunit vaccine H56/CAF01 induces a population of circulating CD4 T cells that traffic into the Mycobacterium tuberculosis-infected lung. Mucosal Immunol. 10: 555-564. https://doi.org/10.1038/mi.2016.70
  14. Cho YJ, Ahn B Y, L ee N G, L ee D H, K im DS. 2006. A combination of E. coli DNA fragm ents a nd m odified lipopolysaccharides as a cancer immunotherapy. Vaccine 24: 5862-5871. https://doi.org/10.1016/j.vaccine.2006.04.048
  15. Han J E, Wui SR, K im KS, C ho Y J, C ho WJ, L ee NG. 2 014. Characterization of the structure and immunostimulatory activity of a vaccine adjuvant, de-O-acylated lipooligosaccharide. PLoS One 9: e85838. https://doi.org/10.1371/journal.pone.0085838
  16. Song ES, Park SA, Kim SH, Cho YJ, Ahn BY, Ahn BC, et al. 2007. Adjuvant effect of CIA07, a combination of Escherichia coli DNA fragments and modified lipopolysaccharides, on the immune response to hepatitis B virus surface antigen. FEMS Immunol. Med. Microbiol. 51: 496-504. https://doi.org/10.1111/j.1574-695X.2007.00325.x
  17. Park SA, Song ES, Cho YJ, Ahn BY, Ha SH, Seong BL, et al. 2007. Immune responses of mice to influenza subunit vaccine in combination with CIA07 as an adjuvant. Microbiol. Immunol. 51: 1099-1107. https://doi.org/10.1111/j.1348-0421.2007.tb04005.x
  18. Han JE, Kim HK, P ark SA, Lee SJ, Kim HJ, S on GH, et al. 2010. A nontoxic derivative of lipopolysaccharide increases immune responses to Gardasil (R) HPV vaccine in mice. Int. Immunopharmacol. 10: 169-176. https://doi.org/10.1016/j.intimp.2009.10.012
  19. Wui SR, Kim HK, Han JE, Kim JM, Kim YH, Chun JH, et al. 2011. A com bination of the TLR4 a gonist CIA05 and alum promotes the immune responses to Bacillus anthracis protective antigen in mice. Int. Immunopharmacol. 11: 1195-1204. https://doi.org/10.1016/j.intimp.2011.03.020
  20. Han JE, Wui SR, P ark SA, Lee NG, Kim KS, Cho Y J, et al. 2012. Comparison of the immune responses to the CIA06-adjuvanted human papillomavirus L1 VLP vaccine with those against the licensed HPV vaccine $Cervarix^{TM}$ in mice. Vaccine 30: 4127-4134. https://doi.org/10.1016/j.vaccine.2012.04.079
  21. Wui SR, Han JE, Kim YH, Rhie GE, Lee NG. 2013. Increased long-term immunity to Bacillus anthracis protective antigen in mice immunized with a CIA06B-adjuvanted anthrax vaccine. Arch. Pharm. Res. 36: 464-471.
  22. Ryu JI, Park SA, Wui SR, Ko A, Han JE, Choi JA, et al. 2016. A de-O-acylated lipooligosaccharide-based adjuvant system promotes antibody and Th1-type immune responses to H1N1 pandemic influenza vaccine in mice. Biomed. Res. Int. 2016: 3713656.
  23. Lee CH, Tsai CM. 1999. Quantification of bacterial lipopolysaccharides by the purpald assay: measuring formaldehyde generated from 2-keto-3-deoxyoctonate and heptose at the inner core by periodate oxidation. Anal. Biochem. 267: 161-168. https://doi.org/10.1006/abio.1998.2961
  24. Holten-Andersen L, Doherty TM, Korsholm KS, Andersen P. 2004. Combination of the cationic surfactant dimethyl dioctadecyl ammonium bromide and synthetic mycobacterial cord factor as an efficient adjuvant for tuberculosis subunit vaccines. Infect. Immun. 72: 1608-1617. https://doi.org/10.1128/IAI.72.3.1608-1617.2004
  25. Sable S B, C heruvu M , Nandakum ra S , Sharm a S, Bandyopadhyay K, Kellar KL, et al. 2011. Cellular immune responses to nine Mycobacterium tuberculosis vaccine candidates following intranasal vaccination. PLoS One 6: e22718. https://doi.org/10.1371/journal.pone.0022718
  26. Green AM, Difazio R, Flynn JL. 2013. IFN-gamma from CD4 T cells is essential for host survival and enhances CD8 T cell function during Mycobacterium tuberculosis infection. J. Immunol. 190: 270-277. https://doi.org/10.4049/jimmunol.1200061
  27. Prezzemolo T, Guggino G, La Manna MP, Di Liberto D, Dieli F, Caccamo N. 2014. Functional signatures of human CD4 and CD8 T cell responses to Mycobacterium tuberculosis. Front. Immunol. 5: 180.
  28. Andersson J, Samarina A, Fink J, Rahman S, Grundstrom S. 2007. Impaired expression of perforin and granulysin in CD8+ T cells at the site of infection in human chronic pulmonary tuberculosis. Infect. Immun. 75: 5210-5222.
  29. Jasenosky LD, Scriba TJ, Hanekom WA, Goldfeld AE. 2015. T cells and adaptive immunity to Mycobacterium tuberculosis in humans. Immunol. Rev. 264: 74-87. https://doi.org/10.1111/imr.12274
  30. Behar SM. 2013. Antigen-specific CD8(+) T cells and protective immunity to tuberculosis. Adv. Exp. Med. Biol. 783: 141-163.
  31. Torrado E, Cooper AM. 2010. IL-17 and Th17 cells in tuberculosis. Cytokine Growth Factor Rev. 21: 455-462. https://doi.org/10.1016/j.cytogfr.2010.10.004
  32. Cooper AM. 2009. Cell-mediated immune responses in tuberculosis. Annu. Rev. Immunol. 27: 393-422. https://doi.org/10.1146/annurev.immunol.021908.132703
  33. Ha SJ, Park SH, Kim HJ, Kim SC, Kang HJ, Lee EG, et al. 2006. Enhanced immunogenicity and protective efficacy with the use of interleukin-12-encapsulated microspheres plus AS01B in tuberculosis subunit vaccination. Infect. Immun. 74: 4954-4959.
  34. Geluk A, Lin MY, van Meijgaarden KE, Leyten EM, Franken KL, Ottenhoff TH, et al. 2007. T-cell recognition of the HspX protein of Mycobacterium tuberculosis correlates with latent M. tuberculosis infection but not with M. bovis BCG vaccination. Infect. Immun. 75: 2914-2921. https://doi.org/10.1128/IAI.01990-06
  35. Dalmia N, Ramsay AJ. 2012. Prime-boost approaches to tuberculosis vaccine development. Expert Rev. Vaccines 11: 1221-1233. https://doi.org/10.1586/erv.12.94
  36. Brennan MJ, Clagett B, Fitzgerald H, Chen V, Williams A, Izzo AA, et al. 2012. Preclinical evidence for implementing a prime-boost vaccine strategy for tuberculosis. Vaccine 30: 2811-2823. https://doi.org/10.1016/j.vaccine.2012.02.036

Cited by

  1. Performance of Homologous and Heterologous Prime-Boost Immunization Regimens of Recombinant Adenovirus and Modified Vaccinia Virus Ankara Expressing an Ag85B-TB10.4 Fusion Protein against Mycobacteriu vol.28, pp.6, 2018, https://doi.org/10.4014/jmb.1712.12064
  2. Latest Comprehensive Knowledge of the Crosstalk between TLR Signaling and Mycobacteria and the Antigens Driving the Process vol.29, pp.10, 2019, https://doi.org/10.4014/jmb.1908.08057
  3. Plant-Produced N-glycosylated Ag85A Exhibits Enhanced Vaccine Efficacy Against Mycobacterium tuberculosis HN878 Through Balanced Multifunctional Th1 T Cell Immunity vol.8, pp.2, 2018, https://doi.org/10.3390/vaccines8020189
  4. Cationic Nanostructures for Vaccines Design vol.5, pp.3, 2018, https://doi.org/10.3390/biomimetics5030032
  5. The Effect of a TLR4 Agonist/Cationic Liposome Adjuvant on Varicella-Zoster Virus Glycoprotein E Vaccine Efficacy: Antigen Presentation, Uptake, and Delivery to Lymph Nodes vol.13, pp.3, 2018, https://doi.org/10.3390/pharmaceutics13030390