The recombinant BCG ΔureC::hly vaccine targets the AIM2 inflammasome to induce autophagy and inflammation

Journal of Infectious Diseases

Volumn 211, Issue 11, 2015, Pages 1831-1841

  Saiga, Hiroyuki ^a   Nieuwenhuizen, Natalie ^a   Gengenbacher, Martin ^a,b   Koehler, Anne Britta ^a   Schuerer, Stefanie ^a   Moura Alves, Pedro ^a   Wagner, Ina ^a   Mollenkopf, Hans Joachim ^a   Dorhoi, Anca ^a   Kaufmann, Stefan H E ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

autophagy; inflammasome; innate immunity; macrophages; recombinant BCG ureC::hly; tuberculosis; vaccination

Indexed keywords

ABSENT IN MELANOMA 2 PROTEIN; BCG VACCINE; CASPASE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; MEMBRANE PROTEIN; RECOMBINANT VACCINE; TRANSMEMBRANE PROTEIN 173; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BCG VACCINATION; CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; DNA DETERMINATION; DRUG EFFICACY; DRUG TARGETING; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IL 18 GENE; IL 1BETA GENE; INFLAMMATION; LYMPHATIC DRAINAGE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; THP 1 CELL LINE; TMEM173 GENE; TUBERCULOSIS; ANIMAL; C57BL MOUSE; CHEMISTRY; IMMUNOLOGY; LYMPH NODE;

ANIMALS; AUTOPHAGY; BCG VACCINE; CELL LINE; FEMALE; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-18; INTERLEUKIN-1BETA; LYMPH NODES; MICE; MICE, INBRED C57BL; TUBERCULOSIS; VACCINES, SYNTHETIC;

EID: 84930446416     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu675     Document Type: Article

References (50)

1. World Health Organization. Global tuberculosis report 2014. Geneva: WHO Press, 2014.
2. Kaufmann SH. Envisioning future strategies for vaccination against tuberculosis. Nat Rev Immunol 2006; 6:699-704.
3. Colditz GA, Brewer TF, Berkey CS, et al. Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA 1994; 271:698-702.
4. Colditz GA, Berkey CS, Mosteller F, et al. The efficacy of bacillus Calmette- Guérin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics 1995; 96:29-35.
5. Pieters J. Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 2008; 3:399-407.
6. Killick KE, Ní Cheallaigh C, O'Farrelly C, Hokamp K, MacHugh DE, Harris J. Receptor-mediated recognition of mycobacterial pathogens. Cell Microbiol 2013; 15:1484-95.
7. Moura-Alves P, Faé K, Houthuys E, et al. AhR sensing of bacterial pigments regulates antibacterial defence. Nature 2014; 512:387-92.
8. Kaufmann SH, Dorhoi A. Inflammation in tuberculosis: interactions, imbalances and interventions. Curr Opin Immunol 2013; 25:441-9.
9. Cooper AM, Mayer-Barber KD, Sher A. Role of innate cytokines in mycobacterial infection. Mucosal Immunol 2011; 4:252-60.
10. Schaible UE, Winau F, Sieling PA, et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 2003; 9:1039-46.
11. Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol 2009; 27:229-65.
12. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009; 458:509-13.
13. Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009; 458:514-8.
14. Rathinam VA, Jiang Z, Waggoner SN, et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 2010; 11:395-402.
15. Tsuchiya K, Hara H, Kawamura I, et al. Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. J Immunol 2010; 185:1186-95.
16. Saiga H, Kitada S, Shimada Y, et al. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int Immunol 2012; 24:637-44.
17. Shi CS, Shenderov K, Huang NN, et al. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012; 13:255-63.
18. Shintani T, Klionsky DJ. Autophagy in health and disease: a doubleedged sword. Science 2004; 306:990-5.
19. Deretic V. Autophagy in tuberculosis. Cold Spring Harb Perspect Med 2014; 4:a018481.
20. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66.
21. Liu PT, Modlin RL. Human macrophage host defense against Mycobacterium tuberculosis. Curr Opin Immunol 2008; 20:371-6.
22. Jagannath C, Lindsey DR, Dhandayuthapani S, Xu Y, Hunter RL Jr, Eissa NT. Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 2009; 15:267-76.
23. Grode L, Seiler P, Baumann S, et al. Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette- Guérin mutants that secrete listeriolysin. J Clin Invest 2005; 115:2472-9.
24. Grode L, Ganoza CA, Brohm C, Weiner J III, Eisele B, Kaufmann SH. Safety and immunogenicity of the recombinant BCG vaccine VPM1002 in a phase 1 open-label randomized clinical trial. Vaccine 2013; 31:1340-8.
25. Kaufmann SH, Cotton MF, Eisele B, et al. The BCG replacement vaccine VPM1002: from drawing board to clinical trial. Expert Rev Vaccines 2014; 13:619-30.
26. Vogelzang A, Perdomo C, Zedler U, et al. Central memory CD4+ T cells are responsible for the recombinant Bacillus Calmette-Guérin ΔureC:: hly vaccine's superior protection against tuberculosis. J Infect Dis 2014; 210:1928-37.
27. Desel C, Dorhoi A, Bandermann S, Grode L, Eisele B, Kaufmann SH. Recombinant BCG ΔureC hly+ induces superior protection over parental BCG by stimulating a balanced combination of type 1 and type 17 cytokine responses. J Infect Dis 2011; 204:1573-84.
28. Farinacci M, Weber S, Kaufmann SH. The recombinant tuberculosis vaccine rBCG ΔureC::hly(+) induces apoptotic vesicles for improved priming of CD4(+) and CD8(+) T cells. Vaccine 2012; 30:7608-14.
29. Hess J, Miko D, Catic A, Lehmensiek V, Russell DG, Kaufmann SH. Mycobacterium bovis bacille Calmette-Guérin strains secreting listeriolysin of Listeria monocytogenes. Proc Natl Acad Sci U S A 1998; 95:5299-304.
30. Stover CK, de la Cruz VF, Fuerst TR, et al. New use of BCG for recombinant vaccines. Nature 1991; 351:456-60.
31. Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol 2008; 445:77-88.
32. McIlwain DR, Berger T, Mak TW. Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 2013; 5:a008656.
33. Tschopp J, Martinon F, Burns K. NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 2003; 4:95-104.
34. Portnoy DA, Auerbuch V, Glomski IJ. The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cellmediated immunity. J Cell Biol 2002; 158:409-14.
35. van der Wel N, Hava D, Houben D, et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007; 129:1287-98.
36. Stamm LM, Morisaki JH, Gao LY, et al. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J Exp Med 2003; 198:1361-8.
37. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 2012; 11:469-80.
38. Lee H, Park HJ, Cho SN, Bai GH, Kim SJ. Species identification of mycobacteria by PCR-restriction fragment length polymorphism of the rpoB gene. J Clin Microbiol 2000; 38:2966-71.
39. Watson RO, Manzanillo PS, Cox JS. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 2012; 150:803-15.
40. Adachi O, Kawai T, Takeda K, et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998; 9:143-50.
41. Brunette RL, Young JM, Whitley DG, Brodsky IE, Malik HS, Stetson DB. Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J Exp Med 2012; 209:1969-83.
42. Van de Craen M, DeclercqW, Van den brande I, FiersW, Vandenabeele P. The proteolytic procaspase activation network: an in vitro analysis. Cell Death Differ 1999; 6:1117-24.
43. Akhter A, Gavrilin MA, Frantz L, et al. Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog 2009; 5:e1000361.
44. Russell DG. Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol Rev 2011; 240:252-68.
45. Müller I, Cobbold SP, Waldmann H, Kaufmann SH. Impaired resistance to Mycobacterium tuberculosis infection after selective in vivo depletion of L3T4+ and Lyt-2+ T cells. Infect Immun 1987; 55:2037-41.
46. Smith J, Manoranjan J, PanM, et al. Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect Immun 2008; 76:5478-87.
47. Behr MA, Wilson MA, Gill WP, et al. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 1999; 284:1520-3.
48. Meunier E, Dick MS, Dreier RF, et al. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 2014; 509:366-70.
49. Weiner J III, Kaufmann SH. Recent advances towards tuberculosis control: vaccines and biomarkers. J Intern Med 2014; 275:467-80.
50. Kaufmann SH. Tuberculosis vaccines: time to think about the next generation. Semin Immunol 2013; 25:172-81.