Deletion of nuoG from the vaccine candidate Mycobacterium bovis BCG ΔureC:: Hly improves protection against tuberculosis

mBio

Volumn 7, Issue 3, 2016, Pages

  Gengenbacher, Martin ^a,b   Nieuwenhuizen, Natalie ^a   Vogelzang, Alexis ^a   Liu, Haipeng ^a   Kaiser, Peggy ^a   Schuerer, Stefanie ^a   Lazar, Doris ^a   Wagner, Ina ^a   Mollenkopf, Hans Joachim ^a   Kaufmann, Stefan H E ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CELL PROTEIN; GUANOSINE TRIPHOSPHATASE; IMMUNOGLOBULIN G; INFLAMMASOME; INTERLEUKIN 18; LC3 PROTEIN; TRANSCRIPTOME; UBIQUILIN PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BACTERIAL GENE; BACTERIAL LOAD; BCG VACCINATION; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; GBPS GENE; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HELPER CELL; IFI204 GENE; IL 18 GENE; IL 1BETA GENE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INFLAMMATION; LUNG TUBERCULOSIS; MOUSE; NONHUMAN; NUOG GENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TRANSCRIPTOME ANALYSIS; TUBERCULOSIS; UPREGULATION; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; LUNG; LYMPH NODE; MICROBIOLOGY; MYCOBACTERIUM BOVIS; PATHOLOGY; TUBERCULOSIS, PULMONARY; VACCINATION;

ANIMALS; BACTERIAL LOAD; BACTERIAL PROTEINS; BCG VACCINE; ELECTRON TRANSPORT COMPLEX I; GENE DELETION; GENE EXPRESSION PROFILING; INFLAMMASOMES; LUNG; LYMPH NODES; MICE; MYCOBACTERIUM BOVIS; TUBERCULOSIS, PULMONARY; VACCINATION;

EID: 84979009162     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00679-16     Document Type: Article

References (44)

1. WHO. 2015. Global tuberculosis report 2015. WHO Press, Geneva, Switzerland.
2. Calmette A. 1927. Sur la vaccination préventive des enfants nouveau-nés contre la tuberculose par le BCG. Ann Inst Pasteur 41:201-232.
3. Kaufmann SH, Gengenbacher M. 2012. Recombinant live vaccine candidates against tuberculosis. Curr Opin Biotechnol 23:900-907. http://dx.doi.org/10.1016/j.copbio.2012.03.007.
4. Hesseling A, Cotton M, Jennings T, Whitelaw A, Johnson L, Eley B, Roux P, Godfrey-Faussett P, Schaaf H. 2009. High incidence of tuberculosis among HIV-infected infants: evidence from a South African population-based study highlights the need for improved tuberculosis control strategies. Clin Infect Dis 48:108-114. http://dx.doi.org/10.1086/595012.
5. Grode L, Seiler P, Baumann S, Hess J, Brinkmann V, Nasser EA, Mann P, Goosmann C, Bandermann S, Smith D, Bancroft GJ, Reyrat JM, van Soolingen D, Raupach B, Kaufmann SH. 2005. Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis Bacille Calmette-Guerin mutants that secrete listeriolysin. J Clin Invest 115: 2472-2479. http://dx.doi.org/10.1172/JCI24617.
6. + T cells are responsible for the recombinant Bacillus Calmette-Guerin DeltaureC::hly vaccine’s superior protection against tuberculosis. J Infect Dis 210: 1928-1937. http://dx.doi.org/10.1093/infdis/jiu347.
7. Saiga H, Nieuwenhuizen N, Gengenbacher M, Koehler A, Schuerer S, Moura-Alves P, Wagner I, Mollenkopf H, Dorhoi A, Kaufmann SHE. 2015. The recombinant BCG deltaureC::hly vaccine targets the AIM2 inflammasome to induce autophagy and inflammation. J Infect Dis 211: 1831-1841. http://dx.doi.org/10.1093/infdis/jiu675.
8. Grode L, Ganoza CA, Brohm C, Weiner J III, Eisele B, Kaufmann SHE. 2013. Safety and immunogenicity of the recombinant BCG vaccine VPM1002 in a phase 1 open-label randomized clinical trial. Vaccine 31: 1340-1348. http://dx.doi.org/10.1016/j.vaccine.2012.12.053.
9. Kaufmann SH, Cotton MF, Eisele B, Gengenbacher M, Grode L, Hesseling AC, Walzl G. 2014. The BCG replacement vaccine VPM1002: from drawing board to clinical trial. Expert Rev Vaccines 13:619-630. http://dx.doi.org/10.1586/14760584.2014.905746.
10. Deretic V, Saitoh T, Akira S. 2013. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13:722-737. http://dx.doi.org/10.1038/nri3532.
11. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753-766. http://dx.doi.org/10.1016/j.cell.2004.11.038.
12. Watson R, Manzanillo P, Cox J. 2012. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803-815. http://dx.doi.org/10.1016/j.cell.2012.06.040.
13. Sakowski ET, Koster S, Portal Celhay C, Park HS, Shrestha E, Hetzenecker SE, Maurer K, Cadwell K, Philips JA. 2015. Ubiquilin 1 promotes IFN-gamma-induced xenophagy of Mycobacterium tuberculosis. PLoS Pathog 11:e1005076. http://dx.doi.org/10.1371/journal.ppat.1005076.
14. Jagannath C, Lindsey DR, Dhandayuthapani S, Xu Y, Hunter RL, Jr, Eissa NT. 2009. Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 15: 267-276. http://dx.doi.org/10.1038/nm.1928.
15. Simeone R, Sayes F, Song O, Gröschel MI, Brodin P, Brosch R, Majlessi L. 2015. Cytosolic access of Mycobacterium tuberculosis: critical impact of phagosomal acidification control and demonstration of occurrence in vivo. PLoS Pathog 11:e1004650. http://dx.doi.org/10.1371/journal.ppat.1004650.
16. Behar SM, Martin CJ, Booty MG, Nishimura T, Zhao X, Gan H, Divangahi M, Remold HG. 2011. Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis. Mucosal Immunol 4:279-287. http://dx.doi.org/10.1038/mi.2011.3.
17. Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, Hagens K, Modlin RL, Brinkmann V, Kaufmann SHE. 2003. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 9:1039-1046. http://dx.doi.org/10.1038/nm906.
18. Miller JL, Velmurugan K, Cowan MJ, Briken V. 2010. The type I Nadh dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-alpha-mediated host cell apoptosis. PLoS Pathog 6:e1000864. http://dx.doi.org/10.1371/journal.ppat.1000864.
19. Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, Hsu T, Glickman M, Jacobs WR, Jr., Porcelli SA, Briken V. 2007. Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3:e110. http://dx.doi.org/10.1371/journal.ppat.0030110.
20. Tzelepis F, Verway M, Daoud J, Gillard J, Hassani-Ardakani K, Dunn J, Downey J, Gentile ME, Jaworska J, Sanchez AMJ, Nédélec Y, Vali H, Tabrizian M, Kristof AS, King IL, Barreiro LB, Divangahi M. 2015. Annexin1 regulates DC efferocytosis and cross-presentation during Mycobacterium tuberculosis infection. J Clin Invest 125:752-768. http://dx.doi.org/10.1172/JCI77014.
21. Winau F, Weber S, Sad S, de Diego J, Hoops SL, Breiden B, Sandhoff K, Brinkmann V, Kaufmann SHE, Schaible UE. 2006. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 24: 105-117. http://dx.doi.org/10.1016/j.immuni.2005.12.001.
22. Martinez J, Malireddi RKS, Lu Q, Cunha LD, Pelletier S, Gingras S, Orchard R, Guan J, Tan H, Peng J, Kanneganti T, Virgin HW, Green DR. 2015. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol 17:893-906. http://dx.doi.org/10.1038/ncb3192.
23. Boyle KB, Randow F. 2015. Rubicon swaps autophagy for LAP. Nat Cell Biol 17:843-845. http://dx.doi.org/10.1038/ncb3197.
24. + Mycobacterium bovis BCG and modified vaccinia virus Ankara expressing M. tuberculosis antigen 85A against murine tuberculosis. Infect Immun 77: 622-631. http://dx.doi.org/10.1128/IAI.00685-08.
25. Finethy R, Jorgensen I, Haldar AK, de Zoete MR, Strowig T, Flavell RA, Yamamoto M, Nagarajan UM, Miao EA, Coers J. 2015. Guanylatebinding proteins enable rapid activation of canonical and noncanonical inflammasomes in Chlamydia-infected macrophages. Infect Immun 83: 4740-4749. http://dx.doi.org/10.1128/IAI.00856-15.
26. Kim B, Shenoy A, Kumar P, Bradfield C, MacMicking J. 2012. IFNinducible GTPases in host cell defense. Cell Host Microbe 12:432-444. http://dx.doi.org/10.1016/j.chom.2012.09.007.
27. Meunier E, Wallet P, Dreier RF, Costanzo S, Anton L, Rühl S, Dussurgey S, Dick MS, Kistner A, Rigard M, Degrandi D, Pfeffer K, Yamamoto M, Henry T, Broz P. 2015. Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nat Immunol 16:476-484. http://dx.doi.org/10.1038/ni.3119.
28. MacMicking JD. 2012. Interferon-inducible effector mechanisms in cellautonomous immunity. Nat Rev Immunol 12:367-382. http://dx.doi.org/10.1038/nri3210.
29. Roy A, Eisenhut M, Harris RJ, Rodrigues LC, Sridhar S, Habermann S, Snell L, Mangtani P, Adetifa I, Lalvani A, Abubakar I. 2014. Effect of BCG vaccination against Mycobacterium tuberculosis infection in children: systematic review and meta-analysis. BMJ 349:g4643. http://dx.doi.org/10.1136/bmj.g4643.
30. Chevalier N, Jarrossay D, Ho E, Avery DT, Ma CS, Yu D, Sallusto F, Tangye SG, Mackay CR. 2011. CXCR5 expressing human central memory CD4 T cells and their relevance for humoral immune responses. J Immunol 186:5556-5568. http://dx.doi.org/10.4049/jimmunol.1002828.
31. Knudsen NPH, Olsen A, Buonsanti C, Follmann F, Zhang Y, Coler RN, Fox CB, Meinke A, D’Oro D, Casini D, Bonci A, Billeskov R, De Gregorio GE, Rappuoli R, Harandi AM, Andersen P, Agger EM. 2016. Different human vaccine adjuvants promote distinct antigenindependent immunological signatures tailored to different pathogens. Sci Rep 6:19570. http://dx.doi.org/10.1038/srep19570.
32. Gopal R, Rangel-Moreno J, Slight S, Lin Y, Nawar HF, Fallert Junecko BA, Reinhart TA, Kolls J, Randall TD, Connell TD, Khader SA. 2013. Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 6:972-984. http://dx.doi.org/10.1038/mi.2012.135.
33. Liu SM, King C. 2013. IL-21-producing Th cells in immunity and autoimmunity. J Immunol 191:3501-3506. http://dx.doi.org/10.4049/jimmunol.1301454.
34. Kaufmann SHE. 2013. Tuberculosis vaccines: time to think about the next generation. Semin Immunol 25:172-181. http://dx.doi.org/10.1016/j.smim.2013.04.006.
35. Fazilleau N, McHeyzer-Williams LJ, Rosen H, McHeyzer-Williams MG. 2009. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat Immunol 10:375-384. http://dx.doi.org/10.1038/ni.1704.
36. Riendeau CJ, Kornfeld H. 2003. THP-1 cell apoptosis in response to mycobacterial infection. Infect Immun 71:254-259. http://dx.doi.org/10.1128/IAI.71.1.254-259.2003.
37. Huang J, Brumell JH. 2014. Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol 12:101-114. http://dx.doi.org/10.1038/nrmicro3160.
38. Mantegazza AR, Savina A, Vermeulen M, Perez L, Geffner J, Hermine O, Rosenzweig SD, Faure F, Amigorena S. 2008. NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 112:4712-4722. http://dx.doi.org/10.1182/blood-2008-01-134791.
39. Divangahi M, Desjardins D, Nunes-Alves C, Remold HG, Behar SM. 2010. Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol 11:751-758. http://dx.doi.org/10.1038/ni.1904.
40. Bardarov S, Bardarov S, Jr, Pavelka MS, Jr, Sambandamurthy V, Larsen M, Tufariello J, Chan J, Hatfull G, Jacobs WR, Jr. 2002. Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148:3007-3017. http://dx.doi.org/10.1099/00221287-148-10-3007.
41. Malaga W, Perez E, Guilhot C. 2003. Production of unmarked mutations in mycobacteria using site-specific recombination. FEMS Microbiol Lett 219:261-268. http://dx.doi.org/10.1016/S0378-1097(03)00003-X.
42. Pepper M, Pagán A, Igyártó B, Taylor J, Jenkins M. 2011. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 35: 583-595. http://dx.doi.org/10.1016/j.immuni.2011.09.009.
43. Rozen S, Skaletsky HJ. 2000. Primer3 on theWWWfor general users and for biologist programmers. Methods Mol Biol 132:365-386.
44. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. http://dx.doi.org/10.1038/nprot.2008.73.