Bacillus calmette-guérin (BCG) revaccination of adults with latent mycobacterium tuberculosis infection induces long-lived BCG-Reactive NK cell responses

Journal of Immunology

Volumn 197, Issue 4, 2016, Pages 1100-1110

  Suliman, Sara ^a   Geldenhuys, Hennie ^a   Johnson, John L ^b   Hughes, Jane E ^a   Smit, Erica ^a   Murphy, Melissa ^a   Toefy, Asma ^a   Lerumo, Lesedi ^a   Hopley, Christiaan ^a   Pienaar, Bernadette ^d   Chheng, Phalkun ^b   Nemes, Elisa ^a   Hoft, Daniel F ^c   Hanekom, Willem A ^a   Boom, W Henry ^b   Hatherill, Mark ^a   Scriba, Thomas J ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c S LOUIS UNIV HLTH SCIENCES CENTER   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMYCOBACTERIAL AGENT; BCG VACCINE; CD56 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 22; ISONIAZID; TUMOR NECROSIS FACTOR; TUBERCULOSTATIC AGENT;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IN VITRO STUDY; MEMORY CELL; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER CELL; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REVACCINATION; SOUTH AFRICAN; TUBERCULIN TEST; TUBERCULOSIS; ADOLESCENT; CLINICAL TRIAL; FEMALE; IMMUNOLOGY; LATENT TUBERCULOSIS; MALE; PROCEDURES; SECONDARY IMMUNIZATION; YOUNG ADULT;

ADOLESCENT; ADULT; ANTITUBERCULAR AGENTS; BCG VACCINE; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNIZATION, SECONDARY; ISONIAZID; KILLER CELLS, NATURAL; LATENT TUBERCULOSIS; MALE; YOUNG ADULT;

EID: 84983735437     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501996     Document Type: Article

References (51)

1. Eurosurveillance Editorial Team. 2013. WHO publishes global tuberculosis report 2013. Euro. Surveill. 18. Available at: http://www.eurosurveillance.org/images/dynamic/EE/V18N43/art20615.pdf.
2. Dye, C., S. Scheele, P. Dolin, V. Pathania, and M. C. Raviglione. 1999. Consensus statement. Global burden of tuberculosis: Estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282: 677-686.
3. Smieja, M. J., C. A. Marchetti, D. J. Cook, and F. M. Smaill. 2000. Isoniazid for preventing tuberculosis in non-HIV infected persons. Cochrane Database Syst. Rev. (2): CD001363.
4. Churchyard, G. J., K. L. Fielding, J. J. Lewis, L. Coetzee, E. L. Corbett, P. Godfrey-Faussett, R. J. Hayes, R. E. Chaisson, and A. D. Grant, Thibela TB Study Team. 2014. A trial of mass isoniazid preventive therapy for tuberculosis control. N. Engl. J. Med. 370: 301-310.
5. Wood, R., and L. G. Bekker. 2014. Isoniazid preventive therapy for tuberculosis in South Africa: An assessment of the local evidence base. S. Afr. Med. J. 104: 174-177.
6. Andrews, J. R., F. Noubary, R. P. Walensky, R. Cerda, E. Losina, and C. R. Horsburgh. 2012. Risk of progression to active tuberculosis following reinfection with Mycobacterium tuberculosis. Clin. Infect. Dis. 54: 784-791.
7. Kaveh, D. A., V. S. Bachy, R. G. Hewinson, and P. J. Hogarth. 2011. Systemic BCG immunization induces persistent lung mucosal multifunctional CD4 T(EM) cells which expand following virulent mycobacterial challenge. PLoS One 6: E21566.
8. Johnson, D. F., L. L. Malone, S. Zalwango, J. Mukisa Oketcho, K. A. Chervenak, B. Thiel, H. Mayanja-Kizza, C. M. Stein, W. H. Boom, and C. L. Lancioni, Tuberculosis Research Unit. 2014. Tuberculin skin test reversion following isoniazid preventive therapy reflects diversity of immune response to primary Mycobacterium tuberculosis infection. PLoS One 9: E96613.
9. Carrara, S., D. Vincenti, N. Petrosillo, M. Amicosante, E. Girardi, and D. Goletti. 2004. Use of a T cell-based assay for monitoring efficacy of antituberculosis therapy. Clin. Infect. Dis. 38: 754-756.
10. Chee, C. B., K. W. KhinMar, S. H. Gan, T. M. Barkham, M. Pushparani, and Y. T. Wang. 2007. Latent tuberculosis infection treatment and T-cell responses to Mycobacterium tuberculosis-specific antigens. Am. J. Respir. Crit. Care Med. 175: 282-287.
11. Ribeiro, S., K. Dooley, J. Hackman, C. Loredo, A. Efron, R. E. Chaisson, M. B. Conde, N. Boechat, and S. E. Dorman. 2009. T-SPOT.TB responses during treatment of pulmonary tuberculosis. BMC Infect. Dis. 9: 23.
12. Chiappini, E., F. Bonsignori, G. Mangone, L. Galli, R. Mazzantini, S. Sollai, C. Azzari, and M. de Martino. 2012. Serial T-SPOT.TB and quantiFERON-TBGold In-Tube assays to monitor response to antitubercular treatment in Italian children with active or latent tuberculosis infection. Pediatr. Infect. Dis. J. 31: 974-977.
13. Chiappini, E., F. Fossi, F. Bonsignori, S. Sollai, L. Galli, and M. de Martino. 2012. Utility of interferon-g release assay results to monitor anti-tubercular treatment in adults and children. Clin. Ther. 34: 1041-1048.
14. Dheda, K., A. Pooran, M. Pai, R. F. Miller, K. Lesley, H. L. Booth, G. M. Scott, A. N. Akbar, A. Zumla, and G. A. Rook. 2007. Interpretation of Mycobacterium tuberculosis antigen-specific IFN-gamma release assays (T-SPOT.TB) and factors that may modulate test results. J. Infect. 55: 169-173.
15. Lee, S. W., C. T. Lee, and J. J. Yim. 2010. Serial interferon-gamma release assays during treatment of active tuberculosis in young adults. BMC Infect. Dis. 10: 300.
16. Lee, S. W., S. H. Lee, and J. J. Yim. 2012. Serial interferon-gamma release assays after chemoprophylaxis in a tuberculosis outbreak cohort. Infection 40: 431-435.
17. Johnson, J. L., H. Geldenhuys, B. A. Thiel, A. Toefy, S. Suliman, B. Pienaar, P. Chheng, T. Scriba, W. H. Boom, W. Hanekom, and M. Hatherill. 2014. Effect of isoniazid therapy for latent TB infection on QuantiFERON-TB gold in-tube responses in adults with positive tuberculin skin test results in a high TB incidence area: A controlled study. Chest 145: 612-617.
18. Hatherill, M., H. Geldenhuys, B. Pienaar, S. Suliman, P. Chheng, S. M. Debanne, D. F. Hoft, W. H. Boom, W. A. Hanekom, and J. L. Johnson. 2014. Safety and reactogenicity of BCG revaccination with isoniazid pretreatment in TST positive adults. Vaccine 32: 3982-3988.
19. Kagina, B. M., N. Mansoor, E. P. Kpamegan, A. Penn-Nicholson, E. Nemes, E. Smit, S. Gelderbloem, A. P. Soares, B. Abel, A. Keyser, et al. 2014. Qualification of a whole blood intracellular cytokine staining assay to measure mycobacteria-specific CD4 and CD8 T cell immunity by flow cytometry. J. Immunol. Methods 417: 22-33.
20. Roederer, M., J. L. Nozzi, and M. C. Nason. 2011. SPICE: Exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A. 79: 167-174.
21. Li, Z., B. Yang, Y. Zhang, J. Ma, X. Chen, S. Lao, B. Li, and C. Wu. 2014. Mycobacterium tuberculosis-specific memory NKT cells in patients with tuberculous pleurisy. J. Clin. Immunol. 34: 979-990.
22. Kleinnijenhuis, J., J. Quintin, F. Preijers, L. A. Joosten, C. Jacobs, R. J. Xavier, J. W. van der Meer, R. van Crevel, and M. G. Netea. 2014. BCG-induced trained immunity in NK cells: Role for non-specific protection to infection. Clin. Immunol. 155: 213-219.
23. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22: 633-640.
24. O'Sullivan, T. E., J. C. Sun, and L. L. Lanier. 2015. Natural killer cell memory. Immunity 43: 634-645.
25. Sun, J. C., J. N. Beilke, and L. L. Lanier. 2009. Adaptive immune features of natural killer cells. Nature 457: 557-561.
26. Horowitz, A., R. H. Behrens, L. Okell, A. R. Fooks, and E. M. Riley. 2010. NK cells as effectors of acquired immune responses: Effector CD4+ T cell-dependent activation of NK cells following vaccination. J. Immunol. 185: 2808-2818.
27. Penn-Nicholson, A., H. Geldenhuys, W. Burny, R. van der Most, C. L. Day, E. Jongert, P. Moris, M. Hatherill, O. Ofori-Anyinam, W. Hanekom, et al; Vaccine Study Team. 2015. Safety and immunogenicity of candidate vaccine M72/AS01E in adolescents in a TB endemic setting. Vaccine 33: 4025-4034.
28. Kupz, A., U. Zedler, M. Staber, C. Perdomo, A. Dorhoi, R. Brosch, and S. H. Kaufmann. 2016. ESAT-6-dependent cytosolic pattern recognition drives noncognate tuberculosis control in vivo. J. Clin. Invest. 126: 2109-2122.
29. Sun, J. C., S. Madera, N. A. Bezman, J. N. Beilke, M. H. Kaplan, and L. L. Lanier. 2012. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209: 947-954.
30. Abu-Raddad, L. J., L. Sabatelli, J. T. Achterberg, J. D. Sugimoto, I. M. Longini Jr., C. Dye, and M. E. Halloran. 2009. Epidemiological benefits of moreeffective tuberculosis vaccines, drugs, and diagnostics. Proc. Natl. Acad. Sci. USA 106: 13980-13985.
31. Scriba, T. J., B. Kalsdorf, D. A. Abrahams, F. Isaacs, J. Hofmeister, G. Black, H. Y. Hassan, R. J. Wilkinson, G. Walzl, S. J. Gelderbloem, et al. 2008. Distinct, specific IL-17- And IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J. Immunol. 180: 1962-1970.
32. Andrews, J. R., M. Hatherill, H. Mahomed, W. A. Hanekom, M. Campo, T. R. Hawn, R. Wood, and T. J. Scriba. 2015. The dynamics of QuantiFERON-TB gold in-tube conversion and reversion in a cohort of South African adolescents. Am. J. Respir. Crit. Care Med. 191: 584-591.
33. Mangtani, P., I. Abubakar, C. Ariti, R. Beynon, L. Pimpin, P. E. Fine, L. C. Rodrigues, P. G. Smith, M. Lipman, P. F. Whiting, and J. A. Sterne. 2014. Protection by BCG vaccine against tuberculosis: A systematic review of randomized controlled trials. Clin. Infect. Dis. 58: 470-480.
34. Barreto, M. L., D. Pilger, S. M. Pereira, B. Genser, A. A. Cruz, S. S. Cunha, C. Sant'Anna, M. A. Hijjar, M. Y. Ichihara, and L. C. Rodrigues. 2014. Causes of variation in BCG vaccine efficacy: Examining evidence from the BCG REVAC cluster randomized trial to explore the masking and the blocking hypotheses. Vaccine 32: 3759-3764.
35. Kagina, B. M., B. Abel, T. J. Scriba, E. J. Hughes, A. Keyser, A. Soares, H. Gamieldien, M. Sidibana, M. Hatherill, S. Gelderbloem, et al; other members of the South African Tuberculosis Vaccine Initiative. 2010. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guérin vaccination of newborns. Am. J. Respir. Crit. Care Med. 182: 1073-1079.
36. Morita, D., Y. Hattori, T. Nakamura, T. Igarashi, H. Harashima, and M. Sugita. 2013. Major T cell response to a mycolyl glycolipid is mediated by CD1c molecules in rhesus macaques. Infect. Immun. 81: 311-316.
37. Van Rhijn, I., A. Kasmar, A. de Jong, S. Gras, M. Bhati, M. E. Doorenspleet, N. de Vries, D. I. Godfrey, J. D. Altman, W. de Jager, et al. 2013. A conserved human T cell population targets mycobacterial antigens presented by CD1b. Nat. Immunol. 14: 706-713.
38. Wheeler, P. R., and P. M. Anderson. 1996. Determination of the primary target for isoniazid in mycobacterial mycolic acid biosynthesis with Mycobacterium aurum A+. Biochem. J. 318: 451-457.
39. Kasmar, A. G., I. van Rhijn, T. Y. Cheng, M. Turner, C. Seshadri, A. Schiefner, R. C. Kalathur, J. W. Annand, A. de Jong, J. Shires, et al. 2011. CD1b tetramers bind ab T cell receptors to identify a mycobacterial glycolipid-reactive T cell repertoire in humans. J. Exp. Med. 208: 1741-1747.
40. Schlums, H., F. Cichocki, B. Tesi, J. Theorell, V. Beziat, T. D. Holmes, H. Han, S. C. Chiang, B. Foley, K. Mattsson, et al. 2015. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity 42: 443-456.
41. Lee, J., T. Zhang, I. Hwang, A. Kim, L. Nitschke, M. Kim, J. M. Scott, Y. Kamimura, L. L. Lanier, and S. Kim. 2015. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity 42: 431-442.
42. Merle, C. S., S. S. Cunha, and L. C. Rodrigues. 2010. BCG vaccination and leprosy protection: Review of current evidence and status of BCG in leprosy control. Expert Rev. Vaccines 9: 209-222.
43. Kleinnijenhuis, J., J. Quintin, F. Preijers, L. A. Joosten, D. C. Ifrim, S. Saeed, C. Jacobs, J. van Loenhout, D. de Jong, H. G. Stunnenberg, et al. 2012. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc. Natl. Acad. Sci. USA 109: 17537-17542.
44. Lauwerys, B. R., J. C. Renauld, and F. A. Houssiau. 1999. Synergistic proliferation and activation of natural killer cells by interleukin 12 and interleukin 18. Cytokine 11: 822-830.
45. Soares, A. P., T. J. Scriba, S. Joseph, R. Harbacheuski, R. A. Murray, S. J. Gelderbloem, A. Hawkridge, G. D. Hussey, H. Maecker, G. Kaplan, and W. A. Hanekom. 2008. Bacillus Calmette-Guérin vaccination of human newborns induces T cells with complex cytokine and phenotypic profiles. J. Immunol. 180: 3569-3577.
46. Zufferey, C., S. Germano, B. Dutta, N. Ritz, and N. Curtis. 2013. The contribution of non-conventional T cells and NK cells in the mycobacterial-specific IFNg response in Bacille Calmette-Guérin (BCG)-immunized infants. PLoS One 8: E77334.
47. Soares, A. P., C. K. Kwong Chung, T. Choice, E. J. Hughes, G. Jacobs, E. J. van Rensburg, G. Khomba, M. de Kock, L. Lerumo, L. Makhethe, et al. 2013. Longitudinal changes in CD4(+) T-cell memory responses induced by BCG vaccination of newborns. J. Infect. Dis. 207: 1084-1094.
48. Montaldo, E., C. Vitale, F. Cottalasso, R. Conte, T. Glatzer, P. Ambrosini, L. Moretta, and M. C. Mingari. 2012. Human NK cells at early stages of differentiation produce CXCL8 and express CD161 molecule that functions as an activating receptor. Blood 119: 3987-3996.
49. Ji, H. F., J. Wang, L. Yu, J. Q. Niu, D. A. Ayana, and Y. F. Jiang. 2013. High frequencies of CD158b+ NK cells are associated with persistent hepatitis C virus infections. Ann. Hepatol. 12: 539-547.
50. Nielsen, C. M., M. J. White, M. R. Goodier, and E. M. Riley. 2013. Functional significance of CD57 expression on human NK cells and relevance to disease. Front. Immunol. 4: 422.
51. World Health Organization. 2015. Guidelines on the Management of Latent Tuberculosis Infection. Available at: http://apps.who.int/iris/bitstream/10665/136471/1/9789241548908-eng.pdf?ua=1&ua=1.