Enhanced protective efficacy against Mycobacterium tuberculosis afforded by BCG prime-DNA boost regimen in an early challenge mouse model is associated with increased splenic interleukin-2-producing CD4 T-cell frequency post-vaccination

Immunology

Volumn 143, Issue 4, 2014, Pages 661-669

  Kang, Han ^a   Yuan, Qin ^a   Ma, Hui ^a   Hu, Zhi Dong ^a   Han, De Ping ^a   Wu, Kang ^a   Lowrie, Douglas B ^a   Fan, Xiao Yong ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

DNA vaccine; Interleukin 2; Multifunctional T cell; Mycobacterium tuberculosis; Prime boost; Protective immunity

Indexed keywords

AUTACOID; BCG VACCINE; CYTOKINE; INTERLEUKIN 2;

ANIMAL; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; DISEASE MODEL; FEMALE; IMMUNIZATION; IMMUNOLOGY; LUNG; LYMPHOCYTE COUNT; METABOLISM; MICROBIOLOGY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; PATHOLOGY; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TUBERCULOSIS; VACCINATION;

ANIMALS; BCG VACCINE; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; IMMUNIZATION, SECONDARY; INFLAMMATION MEDIATORS; INTERLEUKIN-2; LUNG; LYMPHOCYTE COUNT; MICE; MYCOBACTERIUM TUBERCULOSIS; SPLEEN; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS; VACCINATION;

EID: 84911956303     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12348     Document Type: Article

References (34)

1. World Health Organization (WHO). Global Tuberculosis Control: Surveillance, Planning, Financing. WHO report. Geneva, Switzerland: WHO, 2008.
2. Colditz GA, Brewer TF, Berkey CS, Wilson ME, Burdick E, Fineberg HV, Mosteller F. Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA 1994; 271:698-702.
3. Andersen P. TB vaccines: progress and problems. Trends Immunol 2001; 22:160-8.
4. Caruso AM, Serbina N, Klein E, Triebold K, Bloom BR, Flynn JL. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-γ, yet succumb to tuberculosis. J Immunol 1999; 162:5407-16.
5. Ottenhoff TH, Kaufmann SH. Vaccines against tuberculosis: where are we and where do we need to go? PLoS Pathog 2012; 8:e1002607.
6. Hope JC, Thom ML, McAulay M, Mead E, Vordermeier HM, Clifford D, Hewinson RG, Villarreal-Ramos B. Identification of surrogates and correlates of protection in protective immunity against Mycobacterium bovis infection induced in neonatal calves by vaccination with M. bovis BCG Pasteur and M. bovis BCG Danish. Clin Vaccine Immunol 2011; 18:373-9.
7. Darrah PA, Patel DT, De Luca PM et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13:843-50.
8. + T-cell induction in neutralizing antibody-triggered control of simian immunodeficiency virus infection. J Virol 2009; 83:5514-24.
9. Kannanganat S, Kapogiannis BG, Ibegbu C, Chennareddi L, Goepfert P, Robinson HL, Lennox J, Amara RR. Human immunodeficiency virus type 1 controllers but not noncontrollers maintain CD4 T cells coexpressing three cytokines. J Virol 2007; 81:12071-6.
10. Lindenstrom T, Knudsen NP, Agger EM, Andersen P. Control of chronic Mycobacterium tuberculosis infection by CD4 KLRG1- IL-2-secreting central memory cells. J Immunol 2013; 190:6311-9.
11. Lindenstrom T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, Seder RA, Rosenkrands I, Andersen P. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol 2009; 182:8047-55.
12. + T cells. Eur J Immunol 2010; 40:279-90.
13. + memory T lymphocyte populations. Eur J Immunol 2007; 37:3089-100.
14. Soares AP, Scriba TJ, Joseph S et al. Bacillus Calmette-Guérin vaccination of human newborns induces T cells with complex cytokine and phenotypic profiles. J Immunol 2008; 180:3569-77.
15. Li Z, Song D, Zhang H et al. Improved humoral immunity against tuberculosis ESAT-6 antigen by chimeric DNA prime and protein boost strategy. DNA Cell Biol 2006; 25:25-30.
16. Li Z, Zhang H, Fan X et al. DNA electroporation prime and protein boost strategy enhances humoral immunity of tuberculosis DNA vaccines in mice and non-human primates. Vaccine 2006; 24:4565-8.
17. Wu J, Ma H, Qu Q, Zhou WJ, Luo YP, Thangaraj H, Lowrie DB, Fan XY. Incorporation of immunostimulatory motifs in the transcribed region of a plasmid DNA vaccine enhances Th1 immune responses and therapeutic effect against Mycobacterium tuberculosis in mice. Vaccine 2011; 29:7624-30.
18. + T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 2010; 40:2211-20.
19. Ciuffreda D, Comte D, Cavassini M et al. Polyfunctional HCV-specific T-cell responses are associated with effective control of HCV replication. Eur J Immunol 2008; 38:2665-77.
20. Dey B, Jain R, Gupta UD, Katoch VM, Ramanathan VD, Tyagi AK. A booster vaccine expressing a latency-associated antigen augments BCG induced immunity and confers enhanced protection against tuberculosis. PLoS ONE 2011; 6:e23360.
21. Derrick SC, Yang AL, Morris SL. A polyvalent DNA vaccine expressing an ESAT-6-Ag85B fusion protein protects mice against a primary infection with Mycobacterium tuberculosis and boosts BCG-induced protective efficacy. Vaccine 2004; 23:780-8.
22. Mollenkopf HJ, Grode L, Mattow J et al. Application of mycobacterial proteomics to vaccine design: improved protection by Mycobacterium bovis BCG prime-Rv3407 DNA boost vaccination against tuberculosis. Infect Immun 2004; 72:6471-9.
23. Romano M, D'Souza S, Adnet PY, Laali R, Jurion F, Palfliet K, Huygen K. Priming but not boosting with plasmid DNA encoding mycolyl-transferase Ag85A from Mycobacterium tuberculosis increases the survival time of Mycobacterium bovis BCG vaccinated mice against low dose intravenous challenge with M. tuberculosis H37Rv. Vaccine 2006; 24:3353-64.
24. Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8:247-58.
25. Sweeney KA, Dao DN, Goldberg MF et al. A recombinant Mycobacterium smegmatis induces potent bactericidal immunity against Mycobacterium tuberculosis. Nat Med 2011; 17:1261-8.
26. Derrick SC, Yabe IM, Yang A, Morris SL. Vaccine-induced anti-tuberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine 2011; 29:2902-9.
27. Dooms H, Kahn E, Knoechel B, Abbas AK. IL-2 induces a competitive survival advantage in T lymphocytes. J Immunol 2004; 172:5973-9.
28. + T cell effectors can become memory cells with high efficiency and without further division. Nat Immunol 2001; 2:705-10.
29. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J Virol 2007; 81:8468-76.
30. Kawamura I, Tsukada H, Yoshikawa H, Fujita M, Nomoto K, Mitsuyama M. IFN-γ-producing ability as a possible marker for the protective T cells against Mycobacterium bovis BCG in mice. J Immunol 1992; 148:2887-93.
31. Skinner MA, Ramsay AJ, Buchan GS et al. A DNA prime-live vaccine boost strategy in mice can augment IFN-γ responses to mycobacterial antigens but does not increase the protective efficacy of two attenuated strains of Mycobacterium bovis against bovine tuberculosis. Immunology 2003; 108:548-55.
32. Bekker LG, Freeman S, Murray PJ, Ryffel B, Kaplan G. TNF-α controls intracellular mycobacterial growth by both inducible nitric oxide synthase-dependent and inducible nitric oxide synthase-independent pathways. J Immunol 2001; 166:6728-34.
33. Bogdan C, Moll H, Solbach W, Rollinghoff M. Tumor necrosis factor-α in combination with interferon-γ, but not with interleukin 4 activates murine macrophages for elimination of Leishmania major amastigotes. Eur J Immunol 1990; 20:1131-5.
34. Wille-Reece U, Flynn BJ, Lore K et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 2006; 203:1249-58.