Strategies to enhance immunogenicity of cDNA vaccine encoded antigens by modulation of antigen processing

Vaccine

Volumn 34, Issue 42, 2016, Pages 5132-5140

  Platteel, Anouk C M ^a   Marit de Groot, A ^a   Keller, Christin ^b,c   Andersen, Peter ^d   Ovaa, Huib ^e   Kloetzel, Peter M ^b,c   Mishto, Michele ^b,c   Sijts, Alice J A M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c BERLIN INSTITUTE OF HEALTH   (Germany)

^d STATENS SERUM INSTITUT   (Denmark)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antigen presentation; CD8 T cell; Dermal DNA tattoo immunization; Flanking residue optimization; MHC class I restricted epitopes; Proteasome

Indexed keywords

CELL ANTIGEN; COMPLEMENTARY DNA; DNA VACCINE; EARLY SECRETORY ANTIGENIC TARGET 6; EPITOPE; GLUTAMIC ACID; MYCOBACTERIUM ANTIGEN; PROTEASOME; BACTERIAL ANTIGEN; BCG VACCINE; HLA ANTIGEN CLASS 1; MYCOBACTERIUM TUBERCULOSIS ANTIGENS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ANTIGENIC MODULATION; ARTICLE; CD8+ T LYMPHOCYTE; CELL ASSAY; COMPUTER MODEL; CONTROLLED STUDY; DNA FLANKING REGION; DNA IMMUNIZATION; EX VIVO STUDY; GENE FUSION; HYDROPHOBICITY; IMMUNOGENICITY; MOLECULAR DYNAMICS; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SPLEEN CELL; ANIMAL; COMPUTER SIMULATION; GENETICS; IMMUNIZATION; IMMUNOLOGY; METABOLISM; VACCINE IMMUNOGENICITY;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, BACTERIAL; CD8-POSITIVE T-LYMPHOCYTES; COMPUTER SIMULATION; DNA, COMPLEMENTARY; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNIZATION; IMMUNOGENICITY, VACCINE; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; TUBERCULOSIS VACCINES; VACCINES, DNA;

EID: 84991020719     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.08.039     Document Type: Article

References (57)

1. [1] Kloetzel, P., Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2:3 (2001), 179–187.
2. [2] Rock, K.L., York, I.A., Saric, T., Goldberg, A.L., Protein degradation and the generation of MHC class I-presented peptides. Adv Immunol 80 (2002), 1–70.
3. [3] Sijts, E.J.A.M., Kloetzel, P., The role of the proteasome in the generation of MHC class I ligands and immune responses. Cell Mol Life Sci 68:9 (2011), 1491–1502.
4. [4] Aki, M., Shimbara, N., Takashina, M., Akiyama, K., Kagawa, S., Tamura, T., et al. Interferon-γ induces different subunit organizations and functional diversity of proteasomes. J Biochem 115:2 (1994), 257–269.
5. [5] Liepe, J., Holzhütter, H.G., Bellavista, E., Kloetzel, P.M., Stumpf, M.P.H., Mishto, M., Quantitative time-resolved analysis reveals intricate, differential regulation of standard- and immuno-proteasomes. eLife, 4, 2015, e07545 2015.
6. [6] Mishto, M., Bellavista, E., Ligorio, C., Textoris-Taube, K., Santoro, A., Giordano, M., et al. Immunoproteasome LMP2 60HH variant alters MBP epitope generation and reduces the risk to develop multiple sclerosis in Italian female population. PLoS ONE, 5(2), 2010.
7. [7] Platteel, A.C.M., Mishto, M., Textoris-Taube, K., Keller, C., Liepe, J., Busch, D.H., et al. CD8+ T cells of Listeria monocytogenes-infected mice recognize both linear and spliced proteasome products. Eur J Immunol 46:5 (2016), 1109–1118.
8. [8] Mishto, M., Liepe, J., Textoris-Taube, K., Keller, C., Henklein, P., Weberruß, M., et al. Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur J Immunol 44:12 (2014), 3508–3521.
9. [9] Arciniega, M., Beck, P., Lange, O.F., Groll, M., Huber, R., Differential global structural changes in the core particle of yeast and mouse proteasome induced by ligand binding. Proc Natl Acad Sci USA 111:26 (2014), 9479–9484.
10. [10] Ruschak, A.M., Kay, L.E., Proteasome allostery as a population shift between interchanging conformers. Proc Natl Acad Sci USA, 109(50), 2012.
11. [11] Tregoning, J.S., Kinnear, E., Using plasmids as DNA vaccines for infectious diseases. Microbiol Spectr, 2(6), 2014.
12. [12] Le Gall, S., Stamegna, P., Walker, B.D., Portable flanking sequences modulate CTL epitope processing. J Clin Invest 117:11 (2007), 3563–3575.
13. [13] Mo, A.X.Y., Van Lelyveld, S.F.L., Craiu, A., Rock, K.L., Sequences that flank subdominant and cryptic epitopes influence the proteolytic generation of MHC class I-presented peptides. J Immunol 164:8 (2000), 4003–4010.
14. [14] Beekman, N.J., Van Veelen, P.A., Van Hall, T., Neisig, A., Sijts, A., Camps, M., et al. Abrogation of CTL epitope processing by single amino acid substitution flanking the C-terminal proteasome cleavage site. J Immunol 164:4 (2000), 1898–1905.
15. [15] Ossendorp, F., Eggers, M., Neisig, A., Ruppert, T., Groettrup, M., Sijts, A., et al. A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity 5:2 (1996), 115–124.
16. [16] Del Val, M., Schlicht, H., Ruppert, T., Reddehase, M.J., Koszinowski, U.H., Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell 66:6 (1991), 1145–1153.
17. [17] Seifert, U., Liermann, H., Racanelli, V., Halenius, A., Wiese, M., Wedemeyer, H., et al. Hepatitis C virus mutation affects proteasomal epitope processing. J Clin Invest 114:2 (2004), 250–259.
18. [18] Qazi, K.R., Wikman, M., Vasconcelos, N., Berzins, K., Ståhl, S., Fernández, C., Enhancement of DNA vaccine potency by linkage of Plasmodium falciparum malarial antigen gene fused with a fragment of HSP70 gene. Vaccine 23:9 (2005), 1114–1125.
19. [19] Karwacz, K., Mukherjee, S., Apolonia, L., Blundell, M.P., Bouma, G., Escors, D., et al. Nonintegrating lentivector vaccines stimulate prolonged T-cell and antibody responses and are effective in tumor therapy. J Virol 83:7 (2009), 3094–3103.
20. [20] Šmahel, M., Pokorná, D., Macková, J., Vlasák, J., Enhancement of immunogenicity of HPV16 E7 oncogene by fusion with E. coli ß-glucuronidase. J Gene Med 6:10 (2004), 1092–1101.
21. [21] Aagaard, C., Hoang, T., Dietrich, J., Cardona, P.-J., Izzo, A., Dolganov, G., et al. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 17:2 (2011), 189–195.
22. [22] Bins, A.D., Jorritsma, A., Wolkers, M.C., Hung, C., Wu, T., Schumacher, T.N.M., et al. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat Med 11:8 (2005), 899–904.
23. [23] Lundegaard, C., Lamberth, K., Harndahl, M., Buus, S., Lund, O., Nielsen, M., NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8–11. Nucleic Acids Res 36:Web Server issue (2008), W509–W512.
24. [24] Mishto, M., Goede, A., Taube, K.T., Keller, C., Janek, K., Henklein, P., et al. Driving forces of proteasome-catalyzed peptide splicing in yeast and humans. Mol Cell Proteomics 11:10 (2012), 1008–1023.
25. [25] Liepe, J., Mishto, M., Textoris-Taube, K., Janek, K., Keller, C., Henklein, P., et al. The 20S proteasome splicing activity discovered by SpliceMet. PLoS Comput Biol, 6(6), 2010.
26. [26] Textoris-Taube, K., Keller, C., Liepe, J., Henklein, P., Sidney, J., Sette, A., et al. The T210M substitution in the HLA-A∗02:01 gp100 epitope strongly affects overall proteasomal cleavage site usage and antigen processing. J Biol Chem 290:51 (2015), 30417–30428.
27. [27] Oosterhuis, K., Hlschläger, P., Van Den Berg, J.H., Toebes, M., Gomez, R., Schumacher, T.N., et al. Preclinical development of highly effective and safe DNA vaccines directed against HPV 16 E6 and E7. Int J Cancer 129:2 (2011), 397–406.
28. [28] Oosterhuis, K., Aleyd, E., Vrijland, K., Schumacher, T.N., Haanen, J.B., Rational design of DNA vaccines for the induction of human papillomavirus type 16 E6- and E7-specific cytotoxic T-cell responses. Hum Gene Ther 23:12 (2012), 1301–1312.
29. [29] Ebstein, F., Lehmann, A., Kloetzel, P., The FAT10- and ubiquitin-dependent degradation machineries exhibit common and distinct requirements for MHC class I antigen presentation. Cell Mol Life Sci 69:14 (2012), 2443–2454.
30. [30] Rowe, H.M., Lopes, L., Ikeda, Y., Bailey, R., Barde, I., Zenke, M., et al. Immunization with a lentiviral vector stimulates both CD4 and CD8 T cell responses to an ovalbumin transgene. Mol Ther 13:2 (2006), 310–319.
31. [31] Radoševic, K., Wieland, C.W., Rodriguez, A., Weverling, G.J., Mintardjo, R., Gillissen, G., et al. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of gamma interferon. Infect Immun 75:8 (2007), 4105–4115.
32. [32] Denis, O., Tanghe, A., Palfliet, K., Jurion, F., Van Den Berg, T.-P., Vanonckelen, A., et al. Vaccination with plasmid DNA encoding mycobacterial antigen 85A stimulates a CD4+ and CD8+ T-cell epitopic repertoire broader than that stimulated by mycobacterium tuberculosis H37Rv infection. Infect Immun 66:4 (1998), 1527–1533.
33. [33] D'Souza, S., Denis, O., Scorza, T., Nzabintwali, F., Verschueren, H., Huygen, K., CD4+ T cells contain mycobacterium tuberculosis infection in the absence of CD8+ T cells in mice vaccinated with DNA encoding Ag85A. Eur J Immunol 30:9 (2000), 2455–2459.
34. [34] Stevenson, F.K., Rice, J., Ottensmeier, C.H., Thirdborough, S.M., Zhu, D., DNA fusion gene vaccines against cancer: From the laboratory to the clinic. Immunol Rev 199 (2004), 156–180.
35. [35] Brulet, J., Maudoux, F., Thomas, S., Thielemans, K., Burny, A., Leo, O., et al. DNA vaccine encoding endosome-targeted human papillomavirus type 16 E7 protein generates CD4+ T cell-dependent protection. Eur J Immunol 37:2 (2007), 376–384.
36. [36] Rodriguez, F., Zhang, J., Whitton, J.L., DNA immunization: ubiquitination of a viral protein enhances cytotoxic T-lymphocyte induction and antiviral protection but abrogates antibody induction. J Virol 71:11 (1997), 8497–8503.
37. [37] Brandt, L., Oettinger, T., Holm, A., Andersen, Å.B., Andersen, P., Key epitopes on the ESAT-6 antigen recognized in mice during the recall of protective immunity to mycobacterium tuberculosis. J Immunol 157:8 (1996), 3527–3533.
38. [38] Huygen, K., Lozes, E., Gilles, B., Drowart, A., Palfliet, K., Jurion, F., et al. Mapping of TH1 helper T-cell epitopes on major secreted mycobacterial antigen 85A in mice infected with live mycobacterium bovis BCG. Infect Immun 62:2 (1994), 363–370.
39. [39] Basler, M., Buerger, S., Groettrup, M., The ubiquitin-like modifier FAT10 in antigen processing and antimicrobial defense. Mol Immunol 68 (2015), 129–132.
40. [40] Chapiro, J., Claverol, S., Piette, F., Ma, W., Stroobant, V., Guillaume, B., et al. Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 176:2 (2006), 1053–1061.
41. [41] Ebstein, F., Textoris-Taube, K., Keller, C., Golnik, R., Vigneron, N., Van den Eynde, B.J., et al. Proteasomes generate spliced epitopes by two different mechanisms and as efficiently as non-spliced epitopes. Sci Rep, 6, 2016, 24032.
42. [42] Tenzer, S., Wee, E., Burgevin, A., Stewart-Jones, G., Friis, L., Lamberth, K., et al. Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nat Immunol 10:6 (2009), 636–646.
43. [43] Weichold, F.F., Mueller, S., Kortsik, C., Hitzler, W.E., Wulf, M.J., Hone, D.M., et al. Impact of MHC class I alleles on the M. tuberculosis antigen-specific CD8+ T-cell response in patients with pulmonary tuberculosis. Genes Immun 8:4 (2007), 334–343.
44. [44] Kutzler, M.A., Kraynyak, K.A., Nagle, S.J., Parkinson, R.M., Zharikova, D., Chattergoon, M., et al. Plasmids encoding the mucosal chemokines CCL27 and CCL28 are effective adjuvants in eliciting antigen-specific immunity in vivo. Gene Ther 17:1 (2010), 72–82.
45. [45] Schneeberger, A., Wagner, C., Zemann, A., Lührs, P., Kutil, R., Goos, M., et al. CpG motifs are efficient adjuvants for DNA cancer vaccines. J Invest Dermatol 123:2 (2004), 371–379.
46. [46] Iwasaki, A., Stiernholm, B.J.N., Chan, A.K., Berinstein, N.L., Barber, B.H., Enhanced CTL responses mediated by plasmid DNA immunogens encoding costimulatory molecules and cytokines. J Immunol 158:10 (1997), 4591–4601.
47. [47] Oosterhuis, K., Van Den Berg, J.H., Schumacher, T.N., Haanen, J.B.A.G., DNA vaccines and intradermal vaccination by DNA tattooing. Curr Top Microbiol Immunol 351:1 (2012), 221–250.
48. [48] Panina-Bordignon, P., Tan, A., Termijtelen, A., Demotz, S., Corradin, G., Lanzavecchia, A., Universally immunogenic T cell epitopes: promiscuous binding to human MHC class II and promiscuous recognition by T cells. Eur J Immunol 19:12 (1989), 2237–2242.
49. [49] Wolkers, M.C., Toebes, M., Okabe, M., Haanen, J.B.A.G., Schumacher, T.N.M., Optimizing the efficacy of epitope-directed DNA vaccination. J Immunol 168:10 (2002), 4998–5004.
50. [50] Deol, P., Zaiss, D.M.W., Monaco, J.J., Sijts, A.J.A.M., Rates of processing determine the immunogenicity of immunoproteasome- generated epitopes. J Immunol 178:12 (2007), 7557–7562.
51. [51] Coscolla, M., Copin, R., Sutherland, J., Gehre, F., De Jong, B., Owolabi, O., et al. M. tuberculosis T cell epitope analysis reveals paucity of antigenic variation and identifies rare variable TB antigens. Cell Host Microbe 18:5 (2015), 538–548.
52. [52] Dorhoi, A., Kaufmann, S.H.E., Pathology and immune reactivity: understanding multidimensionality in pulmonary tuberculosis. Semin Immunopathol 38:2 (2016), 153–166.
53. [53] Woodworth, J.S., Andersen, P., Reprogramming the T cell response to tuberculosis. Trends Immunol 37:2 (2016), 81–83.
54. [54] Orr, M.T., Ireton, G.C., Beebe, E.A., Huang, P.-D., Reese, V.A., Argilla, D., et al. Immune subdominant antigens as vaccine candidates against Mycobacterium tuberculosis. J Immunol 193:6 (2014), 2911–2918.
55. [55] Burman, W.J., Jones, B.E., Clinical and radiographic features of HIV-related tuberculosis. Semin Respir Infect 18:4 (2003), 263–271.
56. [56] Geldmacher, C., Ngwenyama, N., Schuetz, A., Petrovas, C., Reither, K., Heeregrave, E.J., et al. Preferential infection and depletion of Mycobacterium tuberculosis-specific CD4 T cells after HIV-1 infection. J Exp Med 207:13 (2010), 2869–2881.
57. [57] Peters, B., Sette, A., Integrating epitope data into the emerging web of biomedical knowledge resources. Nat Rev Immunol 7:6 (2007), 485–490.