Effects of the fusion design and immunization route on the immunogenicity of Ag85A-Mtb32 in adenoviral vectored tuberculosis vaccine

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 7, 2015, Pages 1803-1813

  Zhang, Yiling ^a   Feng, Liqiang ^b   Li, Liang ^a   Wang, Dimin ^c   Li, Chufang ^a   Sun, Caijun ^b   Li, Pingchao ^b   Zheng, Xuehua ^b   Liu, Yichu ^b   Yang, Wei ^a   Niu, Xuefeng ^a   Zhong, Nanshan ^a   Chen, Ling ^a,b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^c ANHUI UNIVERSITY   (China)

Author keywords

Fusion strategies; Immunization routes; Immunogenicity; Multiple antigens; Mycobacterium tuberculosis

Indexed keywords

ADENOVIRUS VECTOR; AG85A; ANTIGEN; BCG VACCINE; GAMMA INTERFERON; INTERLEUKIN 2; MTB32; SIGNAL PEPTIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE; RECOMBINANT VACCINE;

ADENO ASSOCIATED VIRUS 5; ADMINISTRATION OF DRUGS, FOOD AND CHEMICALS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DSAM GENE; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE FUSION; GSGAM GENE; IMMUNIZATION; IMMUNOGENICITY; LUNG; LYMPHOCYTE; MOUSE; MYCOBACTERIUM BOVIS BCG; NONHUMAN; OPTAM GENE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; SPLEEN CELL; WESTERN BLOTTING; WTAM GENE; ADENOVIRIDAE; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; GENE VECTOR; GENETICS; IMMUNOLOGY; METABOLISM; ORAL DRUG ADMINISTRATION; SPLEEN;

ADENOVIRIDAE; ADMINISTRATION, ORAL; ANIMALS; BCG VACCINE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; FEMALE; GENETIC VECTORS; IMMUNITY, CELLULAR; LUNG; MICE; MICE, INBRED C57BL; SPLEEN; TUBERCULOSIS VACCINES; VACCINES, SYNTHETIC;

EID: 84938801542     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1042193     Document Type: Article

References (55)

1. Organization WH. Global Tuberculosis Report 2013. http://www. who. int/tb/publications/global_report/en/ 2013.
2. Montagnani C, Chiappini E, Galli L, de Martino M. Vaccine against tuberculosis: what's new? BMC Infect Dis 2014; 14 Suppl 1:S2; PMID:24564340; http://dx. doi. org/10. 1186/1471-2334-14-S1-S2
3. Mittrucker HW, Steinhoff U, Kohler A, Krause M, Lazar D, Mex P, Miekley D, Kaufmann SH. Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. P Natl Acad Sci USA 2007; 104:12434-9; http://dx. doi. org/ 10. 1073/pnas. 0703510104
4. Smaill F, Jeyanathan M, Smieja M, Medina MF, Thanthrige- Don N, Zganiacz A, Yin C, Heriazon A, Damjanovic D, Puri L, et al. A Human Type 5 Adenovirus- Based Tuberculosis Vaccine Induces Robust T Cell Responses in Humans Despite Preexisting Anti-Adenovirus Immunity. Sci Transl Med 2013; 5:205ra134
5. Abel B, Tameris M, Mansoor N, Gelderbloem S, Hughes J, Abrahams D, Makhethe L, Erasmus M, de Kock M, van der Merwe L, et al. The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am J Respir Crit Care Med 2010; 181:1407-17; PMID:20167847; http://dx. doi. org/10. 1164/rccm. 200910-1484OC
6. Scriba TJ, Tameris M, Mansoor N, Smit E, van der Merwe L, Isaacs F, Keyser A, Moyo S, Brittain N, Lawrie A, et al. Modified vaccinia Ankara-expressing Ag85A, a novel tuberculosis vaccine, is safe in adolescents and children, and induces polyfunctional CD4+ T cells. Eur J Immunol 2010; 40:279-90; PMID:20017188; http://dx. doi. org/10. 1002/eji. 200939754
7. Mu J, Jeyanathan M, Small CL, Zhang X, Roediger E, Feng X, Chong D, Gauldie J, Xing Z. Immunization with a bivalent adenovirus-vectored tuberculosis vaccine provides markedly improved protection over its monovalent counterpart against pulmonary tuberculosis. Mol Ther 2009; 17:1093-100; PMID:19319120; http://dx. doi. org/10. 1038/mt. 2009. 60
8. 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, placebocontrolled phase 2b trial. Lancet 2013; 381:1021-8; http://dx. doi. org/10. 1016/S0140-6736(13)60177-4
9. Havenga M, Vogels R, Zuijdgeest D, Radosevic K, Mueller S, Sieuwerts M, Weichold F, Damen I, Kaspers J, Lemckert A, et al. Novel replication-incompetent adenoviral B-group vectors: high vector stability and yield in PER. C6 cells. J Gen Virol 2006; 87:2135-43; PMID:16847108; http://dx. doi. org/10. 1099/vir. 0. 81956-0
10. Mir FA, Kaufmann SH, Eddine AN. A multicistronic DNA vaccine induces significant protection against tuberculosis in mice and offers flexibility in the expressed antigen repertoire. Clin Vaccine Immunol 2009; 16:1467-75; PMID:19656992; http://dx. doi. org/10. 1128/CVI. 00237-09
11. Yuan W, Dong N, Zhang L, Liu J, Lin S, Xiang Z, Qiao H, Tong W, Qin C. Immunogenicity and protective efficacy of a tuberculosis DNA vaccine expressing a fusion protein of Ag85B-Esat6-HspX in mice. Vaccine 2012; 30:2490-7; PMID:21704108; http://dx. doi. org/ 10. 1016/j. vaccine. 2011. 06. 029
12. Perez de Val B, Vidal E, Villarreal-Ramos B, Gilbert SC, Andaluz A, Moll X, Martín M, Nofrarías M, McShane H, Vordermeier HM, et al. A multi-antigenic adenoviral-vectored vaccine improves BCG-induced protection of goats against pulmonary tuberculosis infection and prevents disease progression. PloS one 2013; 8:e81317; PMID:24278420; http://dx. doi. org/ 10. 1371/journal. pone. 0081317
13. Whelan A, Court P, Xing Z, Clifford D, Hogarth PJ, Vordermeier M, Villarreal-Ramos B. Immunogenicity comparison of the intradermal or endobronchial boosting of BCG vaccinates with Ad5-85A. Vaccine 2012; 30:6294-300; PMID:22885013; http://dx. doi. org/ 10. 1016/j. vaccine. 2012. 07. 086
14. McCluskie MJ, Brazolot Millan CL, Gramzinski RA, Robinson HL, Santoro JC, Fuller JT, Widera G, Haynes JR, Purcell RH, Davis HL. Route and method of delivery of DNA vaccine influence immune responses in mice and non-human primates. Mol Med 1999; 5:287-300; PMID:10390545; http://dx. doi. org/ 10. 1007/s0089490050287
15. Wang J, Thorson L, Stokes RW, Santosuosso M, Huygen K, Zganiacz A, Hitt M, Xing Z. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J Immunol 2004; 173:6357-65; http://dx. doi. org/10. 4049/jimmunol. 173. 10. 6357
16. Xing Z, McFarland CT, Sallenave JM, Izzo A, Wang J, McMurray DN. Intranasal mucosal boosting with an adenovirus-vectored vaccine markedly enhances the protection of BCG-primed guinea pigs against pulmonary tuberculosis. PloS one 2009; 4:e5856; PMID:19516906; http://dx. doi. org/10. 1371/journal. pone. 0005856
17. Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, Beverley PC, Tchilian EZ. Multifunctional, highlevel cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J Immunol 2008; 181:4955-64; http://dx. doi. org/10. 4049/ jimmunol. 181. 7. 4955
18. Santosuosso M, Zhang X, McCormick S, Wang J, Hitt M, Xing Z. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J Immunol 2005; 174:7986- 94; http://dx. doi. org/10. 4049/jimmunol. 174. 12. 7986
19. Santosuosso M, McCormick S, Roediger E, Zhang X, Zganiacz A, Lichty BD, Xing Z. Mucosal luminal manipulation of T cell geography switches on protective efficacy by otherwise ineffective parenteral genetic immunization. J Immunol 2007; 178:2387-95; http:// dx. doi. org/10. 4049/jimmunol. 178. 4. 2387
20. Vordermeier HM, Villarreal-Ramos B, Cockle PJ, McAulay M, Rhodes SG, Thacker T, Gilbert SC, McShane H, Hill AV, Xing Z, et al. Viral booster vaccines improve Mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infect Immun 2009; 77:3364-73; PMID:19487476; http://dx. doi. org/10. 1128/IAI. 00287-09
21. Ahn SS, Jeon BY, Kim KS, Kwack JY, Lee EG, Park KS, Sung YC, Cho SN. Mtb32 is a promising tuberculosis antigen for DNA vaccination in pre- and postexposure mouse models. Gene Ther 2012; 19:570-5; PMID:21956689; http://dx. doi. org/10. 1038/gt. 2011. 140
22. Cooper AM, Mayer-Barber KD, Sher A. Role of innate cytokines in mycobacterial infection. Mucosal Immunol 2011; 4:252-60; PMID:21430655; http://dx. doi. org/10. 1038/mi. 2011. 13
23. Redford PS, Boonstra A, Read S, Pitt J, Graham C, Stavropoulos E, Bancroft GJ, O'Garra A. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur J Immunol 2010; 40:2200-10; PMID:20518032; http://dx. doi. org/10. 1002/eji. 201040433
24. Derrick SC, Yabe IM, Yang A, Morris SL. Vaccineinduced anti-tuberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine 2011; 29:2902-9; PMID:21338678; http://dx. doi. org/10. 1016/j. vaccine. 2011. 02. 010
25. Caccamo N, Meraviglia S, La Mendola C, Guggino G, Dieli F, Salerno A. Phenotypical and functional analysis of memory and effector human CD8 T cells specific for mycobacterial antigens. J Immunol 2006; 177:1780-5; http://dx. doi. org/10. 4049/jimmunol. 177. 3. 1780
26. Caccamo N, Guggino G, Meraviglia S, Gelsomino G, Di Carlo P, Titone L, Bocchino M, Galati D, Matarese A, Nouta J, et al. Analysis of Mycobacterium tuberculosis- specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection. PloS one 2009; 4:e5528; PMID:19436760; http://dx. doi. org/10. 1371/journal. pone. 0005528
27. Cid-Arregui A, Juarez V, zur Hausen H. A synthetic E7 gene of human papillomavirus type 16 that yields enhanced expression of the protein in mammalian cells and is useful for DNA immunization studies. J Virol 2003; 77:4928-37; PMID:12663798; http://dx. doi. org/10. 1128/JVI. 77. 8. 4928-4937. 2003
28. Ramakrishna L, Anand KK, Mohankumar KM, Ranga U. Codon optimization of the tat antigen of human immunodeficiency virus type 1 generates strong immune responses in mice following genetic immunization. J Virol 2004; 78:9174-89; PMID:15308713; http://dx. doi. org/10. 1128/JVI. 78. 17. 9174-9189. 2004
29. Ko HJ, Ko SY, Kim YJ, Lee EG, Cho SN, Kang CY. Optimization of codon usage enhances the immunogenicity of a DNA vaccine encoding mycobacterial antigen Ag85B. Infect Immun 2005; 73:5666-74; PMID:16113284; http://dx. doi. org/10. 1128/IAI. 73. 9. 5666-5674. 2005
30. Wen B, Deng Y, Guan J, Yan W, Wang Y, Tan W, Gao J. Signal peptide replacements enhance expression and secretion of hepatitis C virus envelope glycoproteins. Acta biochimica et biophysica Sinica 2011; 43:96-102; PMID:21196448; http://dx. doi. org/ 10. 1093/abbs/gmq117
31. de Felipe P, Luke GA, Brown JD, Ryan MD. Inhibition of 2A-mediated 'cleavage' of certain artificial polyproteins bearing N-terminal signal sequences. Biotechnol J 2010; 5:213-23; PMID:19946875; http:// dx. doi. org/10. 1002/biot. 200900134
32. Chia MY, Hsiao SH, Chan HT, Do YY, Huang PL, Chang HW, Tsai YC, Lin CM, Pang VF, Jeng CR. The immunogenicity of DNA constructs co-expressing GP5 and M proteins of porcine reproductive and respiratory syndrome virus conjugated by GPGP linker in pigs. Veterinary Microbiol 2010; 146:189-99; PMID:20570063; http://dx. doi. org/10. 1016/j. vetmic. 2010. 05. 007
33. Chen X, Zaro JL, Shen WC. Fusion protein linkers: property, design and functionality. Adv Drug Deliv Rev 2013; 65:1357-69; PMID:23026637; http://dx. doi. org/10. 1016/j. addr. 2012. 09. 039
34. Radosevic K, Wieland CW, Rodriguez A, Weverling GJ, Mintardjo R, Gillissen G, Vogels R, Skeiky YA, Hone DM, Sadoff JC, et al. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 Tcell epitope mapping and role of gamma interferon. Infection and immunity 2007; 75:4105-15; PMID:17526747; http://dx. doi. org/10. 1128/IAI. 00004-07
35. 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; http://dx. doi. org/ 10. 4049/jimmunol. 172. 12. 7618
36. Irwin SM, Izzo AA, Dow SW, Skeiky YA, Reed SG, Alderson MR, Orme IM. Tracking antigen-specific CD8 T lymphocytes in the lungs of mice vaccinated with the Mtb72F polyprotein. Infect Immun 2005; 73:5809-16; PMID:16113299; http://dx. doi. org/ 10. 1128/IAI. 73. 9. 5809-5816. 2005
37. Hel Z, Tsai WP, Tryniszewska E, Nacsa J, Markham PD, Lewis MG, Pavlakis GN, Felber BK, Tartaglia J, Franchini G. Improved vaccine protection from simian AIDS by the addition of nonstructural simian immunodeficiency virus genes. J Immunol 2006; 176:85-96; http://dx. doi. org/10. 4049/ jimmunol. 176. 1. 85
38. Zhang Y, Sun C, Feng L, Xiao L, Chen L. Enhancement of Gag-specific but reduction of Env- and Polspecific CD8+ T cell responses by simian immunodeficiency virus nonstructural proteins in mice. AIDS Res hum Retroviruses 2012; 28:374-83; PMID:21736424; http://dx. doi. org/10. 1089/aid. 2011. 0061
39. Beverley PC, Sridhar S, Lalvani A, Tchilian EZ. Harnessing local and systemic immunity for vaccines against tuberculosis. Mucosal Immunol 2014; 7:20-6; PMID:24253104; http://dx. doi. org/10. 1038/mi. 2013. 99
40. Santosuosso M, McCormick S, Zhang X, Zganiacz A, Xing Z. Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral Mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect Immun 2006; 74:4634- 43; PMID:16861651; http://dx. doi. org/10. 1128/IAI. 00517-06
41. Koblin BA, Casapia M, Morgan C, Qin L, Wang ZM, Defawe OD, Baden L, Goepfert P, Tomaras GD, Montefiori DC, et al. Safety and immunogenicity of an HIV adenoviral vector boost after DNA plasmid vaccine prime by route of administration: a randomized clinical trial. PloS one 2011; 6:e24517; PMID:21931737; http://dx. doi. org/10. 1371/journal. pone. 0024517
42. Ma C, Li Y, Wang L, Zhao G, Tao X, Tseng CT, Zhou Y, Du L, Jiang S. Intranasal vaccination with recombinant receptor-binding domain of MERS-CoV spike protein induces much stronger local mucosal immune responses than subcutaneous immunization: Implication for designing novel mucosal MERS vaccines. Vaccine 2014; 32:2100-8; PMID:24560617; http://dx. doi. org/10. 1016/j. vaccine. 2014. 02. 004
43. Richardson JS, Pillet S, Bello AJ, Kobinger GP. Airway delivery of an adenovirus-based Ebola virus vaccine bypasses existing immunity to homologous adenovirus in nonhuman primates. JVirol 2013; 87:3668-77; PMID:23302894; http://dx. doi. org/10. 1128/JVI. 02864-12
44. Xiang ZQ, Gao GP, Reyes-Sandoval A, Li Y, Wilson JM, Ertl HC. Oral vaccination of mice with adenoviral vectors is not impaired by preexisting immunity to the vaccine carrier. J Virol 2003; 77:10780-9; PMID:14512528; http://dx. doi. org/10. 1128/JVI. 77. 20. 10780-10789. 2003
45. Appledorn DM, Aldhamen YA, Godbehere S, Seregin SS, Amalfitano A. Sublingual administration of an adenovirus serotype 5 (Ad5)-based vaccine confirms Tolllike receptor agonist activity in the oral cavity and elicits improved mucosal and systemic cell-mediated responses against HIV antigens despite preexisting Ad5 immunity. Clin Vaccine Immunol 2011; 18:150-60; PMID:21084461; http://dx. doi. org/10. 1128/CVI. 00341-10
46. Hovav AH. Dendritic cells of the oral mucosa. Mucosal Immunol 2014; 7:27-37; PMID:23757304; http://dx. doi. org/10. 1038/mi. 2013. 42
47. Skeiky YA, Lodes MJ, Guderian JA, Mohamath R, Bement T, Alderson MR, Reed SG. Cloning, expression, and immunological evaluation of two putative secreted serine protease antigens of Mycobacterium tuberculosis. Infect Immun 1999; 67:3998-4007.; PMID:10417166
48. Armitige LY, Jagannath C, Wanger AR, Norris SJ. Disruption of the genes encoding antigen 85A and antigen 85B of Mycobacterium tuberculosis H37Rv: effect on growth in culture and in macrophages. Infect Immun 2000; 68:767-78; PMID:10639445; http://dx. doi. org/ 10. 1128/IAI. 68. 2. 767-778. 2000
49. Ahn SS, Jeon BY, Park SJ, Choi DH, Ku SH, Cho SN, Sung YC. Nonlytic Fc-fused IL-7 synergizes with Mtb32 DNA vaccine to enhance antigen-specific T cell responses in a therapeutic model of tuberculosis. Vaccine 2013; 31:2884-90; PMID:23624092; http://dx. doi. org/10. 1016/j. vaccine. 2013. 04. 029
50. Romano M, Roupie V, Wang XM, Denis O, Jurion F, Adnet PY, Laali R, Huygen K. Immunogenicity and protective efficacy of tuberculosis DNA vaccines combining mycolyl-transferase Ag85A and phosphate transport receptor PstS-3. Immunology 2006; 118:321-32; PMID:16827893; http://dx. doi. org/ 10. 1111/j. 1365-2567. 2006. 02373. x
51. Tzelepis F, Verway M, Daoud J, Gillard J, Hassani-Ardakani K, Dunn J, Downey J, GentileME, Jaworska J, Sanchez AM, et al. Annexin1 regulates DC efferocytosis and cross-presentation during Mycobacterium tuberculosis infection. J Clin Investig 2015; 125:752-68; PMID:25562320; http://dx. doi. org/10. 1172/JCI77014
52. Chen CY, Huang D, Wang RC, Shen L, Zeng G, Yao S, Shen Y, Halliday L, Fortman J, McAllister M, et al. A critical role for CD8 T cells in a nonhuman primate model of tuberculosis. PLoS Pathogens 2009; 5: e1000392; PMID:19381260; http://dx. doi. org/ 10. 1371/journal. ppat. 1000392
53. Qiu Z, Zhang M, Zhu Y, Zheng F, Lu P, Liu H, Graner MW, Zhou B, Chen X. Multifunctional CD4 T cell responses in patients with active tuberculosis. Sci Rep 2012; 2:216.; PMID:22355730
54. Caccamo N, Guggino G, Joosten SA, Gelsomino G, Di Carlo P, Titone L, Galati D, Bocchino M, Matarese A, Salerno A, et al. Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 2010; 40:2211-20; PMID:20540114; http://dx. doi. org/10. 1002/eji. 201040455
55. Prezzemolo T, Guggino G, La Manna MP, Di Liberto D, Dieli F, Caccamo N. Functional Signatures of Human CD4 and CD8 T Cell Responses to Mycobacterium tuberculosis. Front Immunol 2014; 5:180; PMID:24795723; http://dx. doi. org/10. 3389/fimmu. 2014. 00180