Immunogenicity and protective efficacy of DMT liposome-adjuvanted tuberculosis subunit CTT3H vaccine

References

• WHO. Global tuberculosis report 2013. Geneva: WHO; 23 Oct 2013. Available from: http://apps.who.int/iris/bitstream/10665/91355/1/9789241564656_eng.pdf
   Google Scholar
• Kaufmann SH. Tuberculosis vaccine development at a divide. Curr Opin Pulm Med 2014; 20:294–300; PMID:24626237; http://dx.doi.org/10.1097/MCP.0000000000000041
   PubMed Web of Science ®Google Scholar
• Weinrich OA, van Pinxteren LA, Meng OL, Birk RP, Andersen P. Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85b and esat-6. Infect Immun 2001; 69:2773-8; PMID:11292688; http://dx.doi.org/10.1128/IAI.69.5.2773-2778.2001
   PubMedGoogle Scholar
• Dietrich J, Aagaard C, Leah R, Olsen AW, Stryhn A, Doherty TM, Andersen P. Exchanging ESAT6 with TB10.4 in an Ag85B fusion molecule-based tuberculosis subunit vaccine: efficient protection and ESAT6-based sensitive monitoring of vaccine efficacy. J Immunol 2005; 174:6332-9; PMID:15879133; http://dx.doi.org/10.4049/jimmunol.174.10.6332
   PubMed Web of Science ®Google Scholar
• Aagaard C, Hoang T, Dietrich J, Cardona PJ, Izzo A, Dolganov G, Schoolnik GK, Cassidy JP, Billeskov R, Andersen P. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 2011; 17:189-94; PMID:21258338; http://dx.doi.org/10.1038/nm.2285
   PubMed Web of Science ®Google Scholar
• Bertholet S, Ireton GC, Ordway DJ, Windish HP, Pine SO, Kahn M, Phan T, Orme IM, Vedvick TS, Baldwin SL, et al. A defined tuberculosis vaccine candidate boosts BCG and protects against multidrug-resistant Mycobacterium tuberculosis. Sci Transl Med 2010; 2:53r-74r; http://dx.doi.org/10.1126/scitranslmed.3001094
   Web of Science ®Google Scholar
• Cooper AM. Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 2009; 27:393-422; PMID:19302046; http://dx.doi.org/10.1146/annurev.immunol.021908.132703
   PubMed Web of Science ®Google Scholar
• O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MP. The immune response in tuberculosis. Annu Rev Immunol 2013; 31:475-527; PMID:23516984; http://dx.doi.org/10.1146/annurev-immunol-032712-095939
   PubMed Web of Science ®Google Scholar
• Geldmacher C, Zumla A, Hoelscher M. Interaction between HIV and Mycobacterium tuberculosis: HIV-1-induced CD4 T-cell depletion and the development of active tuberculosis. Curr Opin HIV AIDS 2012; 7:268-75; PMID:22495739
   PubMedGoogle Scholar
• Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, Siegel JN, Braun MM. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 2001; 345:1098-104; PMID:11596589; http://dx.doi.org/10.1056/NEJMoa011110
   PubMed Web of Science ®Google Scholar
• Davids V, Hanekom WA, Mansoor N, Gamieldien H, Gelderbloem SJ, Hawkridge A, Hussey GD, Hughes EJ, Soler J, Murray RA, et al. The effect of bacille Calmette-Guerin vaccine strain and route of administration on induced immune responses in vaccinated infants. J Infect Dis 2006; 193:531-6; PMID:16425132; http://dx.doi.org/10.1086/499825
   PubMed Web of Science ®Google Scholar
• Mangtani P, Abubakar I, Ariti C, Beynon R, Pimpin L, Fine PE, Rodrigues LC, Smith PG, Lipman M, Whiting PF, et al. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Clin Infect Dis 2014; 58:470-80; PMID:24336911; http://dx.doi.org/10.1093/cid/cit790
   PubMed Web of Science ®Google Scholar
• Woodworth JS, Behar SM. Mycobacterium tuberculosis-specific CD8+ T cells and their role in immunity. Crit Rev Immunol 2006; 26:317-52; PMID:17073557; http://dx.doi.org/10.1615/CritRevImmunol.v26.i4.30
   PubMed Web of Science ®Google Scholar
• Behar SM, Woodworth JS, Wu Y. Next generation: tuberculosis vaccines that elicit protective CD8+ T cells. Expert Rev Vaccines 2007; 6:441-56; PMID:17542758; http://dx.doi.org/10.1586/14760584.6.3.441
   PubMed Web of Science ®Google Scholar
• Sousa AO, Mazzaccaro RJ, Russell RG, Lee FK, Turner OC, Hong S, Van Kaer L, Bloom BR. Relative contributions of distinct MHC class I-dependent cell populations in protection to tuberculosis infection in mice. Proc Natl Acad Sci U S A 2000; 97:4204-8; PMID:10760288; http://dx.doi.org/10.1073/pnas.97.8.4204
   PubMed Web of Science ®Google Scholar
• van Pinxteren LA, Cassidy JP, Smedegaard BH, Agger EM, Andersen P. Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur J Immunol 2000; 30:3689-98; PMID:11169412; http://dx.doi.org/10.1002/1521-4141(200012)30:12%3c3689::AID-IMMU3689%3e3.0.CO;2-4
   PubMed Web of Science ®Google Scholar
• Flynn JL, Goldstein MM, Triebold KJ, Koller B, Bloom BR. Major histocompatibility complex class I-restricted T cells are required for resistance to Mycobacterium tuberculosis infection. Proc Natl Acad Sci U S A 1992; 89:12013-7; PMID:1465432; http://dx.doi.org/10.1073/pnas.89.24.12013
   PubMed Web of Science ®Google Scholar
• Zvi A, Ariel N, Fulkerson J, Sadoff JC, Shafferman A. Whole genome identification of Mycobacterium tuberculosis vaccine candidates by comprehensive data mining and bioinformatic analyses. BMC Med Genomics 2008; 1:18; PMID:18505592; http://dx.doi.org/10.1186/1755-8794-1-18
   PubMed Web of Science ®Google Scholar
• Geluk A, van Meijgaarden KE, Joosten SA, Commandeur S, Ottenhoff TH. Innovative Strategies to Identify M. tuberculosis Antigens and Epitopes Using Genome-Wide Analyses. Front Immunol 2014; 5:256; PMID:25009541; http://dx.doi.org/10.3389/fimmu.2014.00256
   PubMed Web of Science ®Google Scholar
• D'Souza S, Rosseels V, Romano M, Tanghe A, Denis O, Jurion F, Castiglione N, Vanonckelen A, Palfliet K, Huygen K. Mapping of murine Th1 helper T-Cell epitopes of mycolyl transferases Ag85A, Ag85B, and Ag85C from Mycobacterium tuberculosis. Infect Immun 2003; 71:483-93; PMID:12496199; http://dx.doi.org/10.1128/IAI.71.1.483-493.2003
   PubMed Web of Science ®Google Scholar
• Billeskov R, Vingsbo-Lundberg C, Andersen P, Dietrich J. Induction of CD8 T cells against a novel epitope in TB10.4: correlation with mycobacterial virulence and the presence of a functional region of difference-1. J Immunol 2007; 179:3973-81; PMID:17785835; http://dx.doi.org/10.4049/jimmunol.179.6.3973
   PubMed Web of Science ®Google Scholar
• Caccamo N, Milano S, Di Sano C, Cigna D, Ivanyi J, Krensky AM, Dieli F, Salerno A. Identification of epitopes of Mycobacterium tuberculosis 16-kDa protein recognized by human leukocyte antigen-A*0201 CD8(+) T lymphocytes. J Infect Dis 2002; 186:991-8; PMID:12232840; http://dx.doi.org/10.1086/344174
   PubMedGoogle Scholar
• Shi C, Chen L, Chen Z, Zhang Y, Zhou Z, Lu J, Fu R, Wang C, Fang Z, Fan X. Enhanced protection against tuberculosis by vaccination with recombinant BCG over-expressing HspX protein. Vaccine 2010; 28:5237-44; PMID:20538090; http://dx.doi.org/10.1016/j.vaccine.2010.05.063
   PubMed Web of Science ®Google Scholar
• Skeiky YA, Alderson MR, Ovendale PJ, Guderian JA, Brandt L, Dillon DC, Campos-Neto A, Lobet Y, Dalemans W, Orme IM, et al. Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J Immunol 2004; 172:7618-28; PMID:15187142; http://dx.doi.org/10.4049/jimmunol.172.12.7618
   PubMed Web of Science ®Google Scholar
• Kamath AB, Woodworth J, Xiong X, Taylor C, Weng Y, Behar SM. Cytolytic CD8+ T cells recognizing CFP10 are recruited to the lung after Mycobacterium tuberculosis infection. J Exp Med 2004; 200:1479-89; PMID:15557351; http://dx.doi.org/10.1084/jem.20041690
   PubMed Web of Science ®Google Scholar
• Wu Y, Woodworth JS, Shin DS, Morris S, Behar SM. Vaccine-elicited 10-kilodalton culture filtrate protein-specific CD8+ T cells are sufficient to mediate protection against Mycobacterium tuberculosis infection. Infect Immun 2008; 76:2249-55; PMID:18332205; http://dx.doi.org/10.1128/IAI.00024-08
   PubMed Web of Science ®Google Scholar
• Temmerman ST, Place S, Debrie AS, Locht C, Mascart F. Effector functions of heparin-binding hemagglutinin-specific CD8+ T lymphocytes in latent human tuberculosis. J Infect Dis 2005; 192:226-32; PMID:15962217; http://dx.doi.org/10.1086/430930
   PubMed Web of Science ®Google Scholar
• Parra M, Pickett T, Delogu G, Dheenadhayalan V, Debrie AS, Locht C, Brennan MJ. The mycobacterial heparin-binding hemagglutinin is a protective antigen in the mouse aerosol challenge model of tuberculosis. Infect Immun 2004; 72:6799-805; PMID:15557600; http://dx.doi.org/10.1128/IAI.72.12.6799-6805.2004
   PubMed Web of Science ®Google Scholar
• Millington KA, Fortune SM, Low J, Garces A, Hingley-Wilson SM, Wickremasinghe M, Kon OM, Lalvani A. Rv3615c is a highly immunodominant RD1 (Region of Difference 1)-dependent secreted antigen specific for Mycobacterium tuberculosis infection. Proc Natl Acad Sci U S A 2011; 108:5730-5; PMID:21427227; http://dx.doi.org/10.1073/pnas.1015153108
   PubMed Web of Science ®Google Scholar
• Kong H, Dong C, Xiong S. A novel vaccine p846 encoding Rv3615c, Mtb10.4, and Rv2660c elicits robust immune response and alleviates lung injury induced by Mycobacterium infection. Hum Vaccin Immunother 2014; 10:378-90; PMID:24280763; http://dx.doi.org/10.4161/hv.27121
   PubMed Web of Science ®Google Scholar
• Coler RN, Skeiky YA, Vedvick T, Bement T, Ovendale P, Campos-Neto A, Alderson MR, Reed SG. Molecular cloning and immunologic reactivity of a novel low molecular mass antigen of Mycobacterium tuberculosis. J Immunol 1998; 161:2356-64; PMID:9725231.
   PubMed Web of Science ®Google Scholar
• Coler RN, Campos-Neto A, Ovendale P, Day FH, Fling SP, Zhu L, Serbina N, Flynn JL, Reed SG, Alderson MR. Vaccination with the T cell antigen Mtb 8.4 protects against challenge with Mycobacterium tuberculosis. J Immunol 2001; 166:6227-35; PMID:11342645; http://dx.doi.org/10.4049/jimmunol.166.10.6227
   PubMed Web of Science ®Google Scholar
• Skjot RL, Brock I, Arend SM, Munk ME, Theisen M, Ottenhoff TH, Andersen P. Epitope mapping of the immunodominant antigen TB10.4 and the two homologous proteins TB10.3 and TB12.9, which constitute a subfamily of the esat-6 gene family. Infect Immun 2002; 70:5446-53; PMID:12228269; http://dx.doi.org/10.1128/IAI.70.10.5446-5453.2002
   PubMedGoogle Scholar
• P Stop TB Partnership | Working Group on new TB Vaccines; EB/OL.; 2014-3-9. Available from:http://www.stoptb.org/wg/new_vaccines/documents.asp
   Google Scholar
• Tameris MD, Hatherill M, Landry BS, Scriba TJ, Snowden MA, Lockhart S, Shea JE, McClain JB, Hussey GD, Hanekom WA, et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 2013; 381:1021-8; PMID:23391465; http://dx.doi.org/10.1016/S0140-6736(13)60177-4
   PubMed Web of Science ®Google Scholar
• van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007; 129:1287-98; PMID:17604718; http://dx.doi.org/10.1016/j.cell.2007.05.059
   PubMed Web of Science ®Google Scholar
• Hervas-Stubbs S, Majlessi L, Simsova M, Morova J, Rojas MJ, Nouze C, Brodin P, Sebo P, Leclerc C. High frequency of CD4+ T cells specific for the TB10.4 protein correlates with protection against Mycobacterium tuberculosis infection. Infect Immun 2006; 74:3396-407; PMID:16714570; http://dx.doi.org/10.1128/IAI.02086-05
   PubMed Web of Science ®Google Scholar
• Menozzi FD, Rouse JH, Alavi M, Laude-Sharp M, Muller J, Bischoff R, Brennan MJ, Locht C. Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 1996; 184:993-1001; PMID:9064359; http://dx.doi.org/10.1084/jem.184.3.993
   PubMed Web of Science ®Google Scholar
• Menozzi FD, Bischoff R, Fort E, Brennan MJ, Locht C. Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc Natl Acad Sci U S A 1998; 95:12625-30; PMID:9770536; http://dx.doi.org/10.1073/pnas.95.21.12625
   PubMed Web of Science ®Google Scholar
• Pethe K, Alonso S, Biet F, Delogu G, Brennan MJ, Locht C, Menozzi FD. The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 2001; 412:190-4; PMID:11449276; http://dx.doi.org/10.1038/35084083
   PubMed Web of Science ®Google Scholar
• Masungi C, Temmerman S, Van Vooren JP, Drowart A, Pethe K, Menozzi FD, Locht C, Mascart F. Differential T and B cell responses against Mycobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J Infect Dis 2002; 185:513-20; PMID:11865404; http://dx.doi.org/10.1086/338833
   PubMed Web of Science ®Google Scholar
• Guerrero GG, Locht C. Recombinant HBHA boosting effect on BCG-induced immunity against Mycobacterium tuberculosis infection. Clin Dev Immunol 2011; 2011:730702; PMID:21647410; http://dx.doi.org/10.1155/2011/730702
   PubMedGoogle Scholar
• Panas MW, Sixsmith JD, White K, Korioth-Schmitz B, Shields ST, Moy BT, Lee S, Schmitz JE, Jacobs WJ, Porcelli SA, et al. Gene deletions in Mycobacterium bovis BCG stimulate increased CD8+ T cell responses. Infect Immun 2014; 82:5317-26; PMID:25287928; http://dx.doi.org/10.1128/IAI.02100-14
   PubMed Web of Science ®Google Scholar
• Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, Hagens K, Modlin RL, Brinkmann V, Kaufmann SH. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 2003; 9:1039-46; PMID:12872166; http://dx.doi.org/10.1038/nm906
   PubMed Web of Science ®Google Scholar
• Farinacci M, Weber S, Kaufmann SH. The recombinant tuberculosis vaccine rBCG DeltaureC::hly(+) induces apoptotic vesicles for improved priming of CD4(+) and CD8(+) T cells. Vaccine 2012; 30:7608-14; PMID:23088886; http://dx.doi.org/10.1016/j.vaccine.2012.10.031
   PubMed Web of Science ®Google Scholar
• Billeskov R, Grandal MV, Poulsen C, Christensen JP, Winther N, Vingsbo-Lundberg C, Hoang TT, van Deurs B, Song YH, Aagaard C, et al. Difference in TB10.4 T-cell epitope recognition following immunization with recombinant TB10.4, BCG or infection with Mycobacterium tuberculosis. Eur J Immunol 2010; 40:1342-54; PMID:20186878; http://dx.doi.org/10.1002/eji.200939830
   PubMedGoogle Scholar
• Bruffaerts N, Huygen K, Romano M. DNA vaccines against tuberculosis. Expert Opin Biol Ther 2014; 14:1801-13; PMID:25145964; http://dx.doi.org/10.1517/14712598.2014.951630
   PubMed Web of Science ®Google Scholar
• Xing Z, Lichty BD. Use of recombinant virus-vectored tuberculosis vaccines for respiratory mucosal immunization. Tuberculosis (Edinb) 2006; 86:211-7; PMID:16504584
   PubMed Web of Science ®Google Scholar
• Stenger S, Hanson DA, Teitelbaum R, Dewan P, Niazi KR, Froelich CJ, Ganz T, Thoma-Uszynski S, Melian A, Bogdan C, et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998; 282:121-5; PMID:9756476; http://dx.doi.org/10.1126/science.282.5386.121
   PubMed Web of Science ®Google Scholar
• Endsley JJ, Furrer JL, Endsley MA, McIntosh MA, Maue AC, Waters WR, Lee DR, Estes DM. Characterization of bovine homologues of granulysin and NK-lysin. J Immunol 2004; 173:2607-14; PMID:15294977; http://dx.doi.org/10.4049/jimmunol.173.4.2607
   PubMed Web of Science ®Google Scholar
• Mata-Haro V, Cekic C, Martin M, Chilton PM, Casella CR, Mitchell TC. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007; 316:1628-32; PMID:17569868; http://dx.doi.org/10.1126/science.1138963
   PubMed Web of Science ®Google Scholar
• Mbow ML, De Gregorio E, Valiante NM, Rappuoli R. New adjuvants for human vaccines. Curr Opin Immunol 2010; 22:411-6; PMID:20466528; http://dx.doi.org/10.1016/j.coi.2010.04.004
   PubMed Web of Science ®Google Scholar
• Schoenen H, Bodendorfer B, Hitchens K, Manzanero S, Werninghaus K, Nimmerjahn F, Agger EM, Stenger S, Andersen P, Ruland J, et al. Cutting edge: Mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol 2010; 184:2756-60; PMID:20164423; http://dx.doi.org/10.4049/jimmunol.0904013
   PubMed Web of Science ®Google Scholar
• Werninghaus K, Babiak A, Gross O, Holscher C, Dietrich H, Agger EM, Mages J, Mocsai A, Schoenen H, Finger K, et al. Adjuvanticity of a synthetic cord factor analogue for subunit Mycobacterium tuberculosis vaccination requires FcRgamma-Syk-Card9-dependent innate immune activation. J Exp Med 2009; 206:89-97; PMID:19139169; http://dx.doi.org/10.1084/jem.20081445
   PubMed Web of Science ®Google Scholar
• Christensen D, Agger EM, Andreasen LV, Kirby D, Andersen P, Perrie Y. Liposome-based cationic adjuvant formulations (CAF): past, present, and future. J Liposome Res 2009; 19:2-11; PMID:19515003; http://dx.doi.org/10.1080/08982100902726820
   PubMed Web of Science ®Google Scholar
• Gram GJ, Karlsson I, Agger EM, Andersen P, Fomsgaard A. A novel liposome-based adjuvant CAF01 for induction of CD8(+) cytotoxic T-lymphocytes (CTL) to HIV-1 minimal CTL peptides in HLA-A*0201 transgenic mice. PLoS One 2009; 4:e6950; PMID:19759892; http://dx.doi.org/10.1371/journal.pone.0006950
   PubMed Web of Science ®Google Scholar
• Nordly P, Agger EM, Andersen P, Nielsen HM, Foged C. Incorporation of the TLR4 agonist monophosphoryl lipid A into the bilayer of DDA/TDB liposomes: physico-chemical characterization and induction of CD8+ T-cell responses in vivo. Pharm Res 2011; 28:553-62; PMID:21042837; http://dx.doi.org/10.1007/s11095-010-0301-9
   PubMed Web of Science ®Google Scholar
• Winau F, Weber S, Sad S, de Diego J, Hoops SL, Breiden B, Sandhoff K, Brinkmann V, Kaufmann SH, Schaible UE. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 2006; 24:105-17; PMID:16413927; http://dx.doi.org/10.1016/j.immuni.2005.12.001
   PubMed Web of Science ®Google Scholar
• Tascon RE, Stavropoulos E, Lukacs KV, Colston MJ. Protection against Mycobacterium tuberculosis infection by CD8+ T cells requires the production of gamma interferon. Infect Immun 1998; 66:830-4; PMID:9453650
   PubMed Web of Science ®Google Scholar
• Fu R, Wang C, Shi C, Lu M, Fang Z, Lu J, Wang F, Fan X. An improved whole-blood gamma interferon assay based on the CFP21-MPT64 fusion protein. Clin Vaccine Immunol 2009; 16:686-91; PMID:19279170; http://dx.doi.org/10.1128/CVI.00486-08
   PubMedGoogle Scholar