Plant-derived recombinant immune complexes as self-adjuvanting TB immunogens for mucosal boosting of BCG

Plant Biotechnology Journal

Volumn 12, Issue 7, 2014, Pages 840-850

  Pepponi, Ilaria ^a,b   Diogo, Gil R ^a   Stylianou, Elena ^a,b   van Dolleweerd, Craig J ^a   Drake, Pascal M W ^a   Paul, Matthew J ^a   Sibley, Laura ^c   Ma, Julian K C ^a   Reljic, Rajko ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Immune complexes; Infection; Plants; Tuberculosis; Vaccine

Indexed keywords

MUS; MYCOBACTERIUM TUBERCULOSIS; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

ANTIGEN ANTIBODY COMPLEX; BCG VACCINE; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; GENETICS; HUMAN; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; METABOLISM; MOLECULAR CLONING; MOUSE; MYCOBACTERIUM TUBERCULOSIS; TOBACCO; TRANSGENIC PLANT;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODY FORMATION; ANTIGEN-ANTIBODY COMPLEX; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CLONING, MOLECULAR; HUMANS; INTERLEUKIN-2; MICE; MYCOBACTERIUM TUBERCULOSIS; PLANTS, GENETICALLY MODIFIED; TOBACCO; TUBERCULOSIS VACCINES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84906221356     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12185     Document Type: Article

References (52)

1. Agger, E.M., Rosenkrands, I., Olsen, A.W., Hatch, G., Williams, A., Kritsch, C., Lingnau, K., von Gabain, A., Andersen, C.S., Korsholm, K.S. and Andersen, P. (2006) Protective immunity to tuberculosis with Ag85B-ESAT-6 in a synthetic cationic adjuvant system IC31. Vaccine, 24, 5452-5460.
2. Agger, E.M., Rosenkrands, I., Hansen, J., Brahimi, K., Vandahl, B.S., Aagaard, C., Werninghaus, K., Kirschning, C., Lang, R., Christensen, D., Theisen, M., Follmann, F. and Andersen, P. (2008) Cationic liposomes formulated with synthetic mycobacterial cordfactor (CAF01): a versatile adjuvant for vaccines with different immunological requirements. PLoS ONE, 3, e3116.
3. Andersen, P., Andersen, A.B., Sorensen, A.L. and Nagai, S. (1995) Recall of long-lived immunity to Mycobacterium tuberculosis infection in mice. J. Immunol. 154, 3359-3372.
4. Antoniou, A.N. and Watts, C. (2002) Antibody modulation of antigen presentation: positive and negative effects on presentation of the tetanus toxin antigen via the murine B cell isoform of FcgammaRII. Eur. J. Immunol. 32, 530-540.
5. Boesen, H., Jensen, B.N., Wilcke, T. and Andersen, P. (1995) Human T-cell responses to secreted antigen fractions of Mycobacterium tuberculosis. Infect. Immun. 63, 1491-1497.
6. Brennan, M.J., Clagett, B., Fitzgerald, H., Chen, V., Williams, A., Izzo, A.A. and Barker, L.F. (2012) Preclinical evidence for implementing a prime-boost vaccine strategy for tuberculosis. Vaccine, 30, 2811-2823.
7. Caccamo, N., Meraviglia, S., La Mendola, C., Bosze, S., Hudecz, F., Ivanyi, J., Dieli, F. and Salerno, A. (2004) Characterization of HLA-DR- and TCR-binding residues of an immunodominant and genetically permissive peptide of the 16-kDa protein of Mycobacterium tuberculosis. Eur. J. Immunol. 34, 2220-2229.
8. Chang, Z., Primm, T.P., Jakana, J., Lee, I.H., Serysheva, I., Chiu, W., Gilbert, H.F. and Quiocho, F.A. (1996) Mycobacterium tuberculosis 16-kDa antigen (Hsp16.3) functions as an oligomeric structure in vitro to suppress thermal aggregation. J. Biol. Chem. 271, 7218-7223.
9. Chargelegue, D., Drake, P.M., Obregon, P., Prada, A., Fairweather, N. and Ma, J.K. (2005) Highly immunogenic and protective recombinant vaccine candidate expressed in transgenic plants. Infect. Immun. 73, 5915-5922.
10. Chen, Y., Inobe, J., Marks, R., Gonnella, P., Kuchroo, V.K. and Weiner, H.L. (1995) Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature, 376, 177-180.
11. Darrah, P.A., Patel, D.T., De Luca, P.M., Lindsay, R.W., Davey, D.F., Flynn, B.J., Hoff, S.T., Andersen, P., Reed, S.G., Morris, S.L., Roederer, M. and Seder, R.A. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13, 843-850.
12. De Muynck, B., Navarre, C. and Boutry, M. (2010) Production of antibodies in plants: status after twenty years. Plant Biotechnol. J. 8, 529-563.
13. Desel, C., Dorhoi, A., Bandermann, S., Grode, L., Eisele, B. and Kaufmann, S.H. (2011) Recombinant BCG DeltaureC hly+ induces superior protection over parental BCG by stimulating a balanced combination of type 1 and type 17 cytokine responses. J. Infect. Dis. 204, 1573-1584.
14. Dorokhov, Y.L., Sheveleva, A.A., Frolova, O.Y., Komarova, T.V., Zvereva, A.S., Ivanov, P.A. and Atabekov, J.G. (2007) Superexpression of tuberculosis antigens in plant leaves. Tuberculosis (Edinb), 87, 218-224.
15. Falero-Diaz, G., Challacombe, S., Rahman, D., Mistry, M., Douce, G., Dougan, G., Acosta, A. and Ivanyi, J. (2000) Transmission of IgA and IgG monoclonal antibodies to mucosal fluids following intranasal or parenteral delivery. Int. Arch. Allergy Immunol. 122, 143-150.
16. Frutos, R., Denise, H., Vivares, C., Neuhaus, J.M., Vitale, S., Pedrazzini, E., Ma, J., Dix, P., Gray, J., Pezzotti, M., Conrad, U. and Robinson, D. (2008) Pharmaceutical proteins in plants. A strategic genetic engineering approach for the production of tuberculosis antigens. Ann. N. Y. Acad. Sci. 1149, 275-280.
17. Giri, P.K., Verma, I. and Khuller, G.K. (2006) Enhanced immunoprotective potential of Mycobacterium tuberculosis Ag85 complex protein based vaccine against airway Mycobacterium tuberculosis challenge following intranasal administration. FEMS Immunol. Med. Microbiol. 47, 233-241.
18. Heyman, B. (1990) The immune complex: possible ways of regulating the antibody response. Immunol. Today 11, 310-313.
19. Horwitz, M.A. and Harth, G. (2003) A new vaccine against tuberculosis affords greater survival after challenge than the current vaccine in the guinea pig model of pulmonary tuberculosis. Infect. Immun. 71, 1672-1679.
20. Kaufmann, S.H. (2012) Tuberculosis vaccine development: strength lies in tenacity. Trends Immunol. 33, 373-379.
21. Klaus, G.G. (1978) The generation of memory cells. II. Generation of B memory cells with preformed antigen-antibody complexes. Immunology, 34, 643-652.
22. Kostense, S., Koudstaal, W., Sprangers, M., Weverling, G.J., Penders, G., Helmus, N., Vogels, R., Bakker, M., Berkhout, B., Havenga, M. and Goudsmit, J. (2004) Adenovirus types 5 and 35 seroprevalence in AIDS risk groups supports type 35 as a vaccine vector. AIDS, 18, 1213-1216.
23. Langermans, J.A., Doherty, T.M., Vervenne, R.A., van der Laan, T., Lyashchenko, K., Greenwald, R., Agger, E.M., Aagaard, C., Weiler, H., van Soolingen, D., Dalemans, W., Thomas, A.W. and Andersen, P. (2005) Protection of macaques against Mycobacterium tuberculosis infection by a subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Vaccine, 23, 2740-2750.
24. Lindenstrom, T., Agger, E.M., Korsholm, K.S., Darrah, P.A., Aagaard, C., Seder, R.A., Rosenkrands, I. and Andersen, P. (2009) Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J. Immunol. 182, 8047-8055.
25. Marusic-Galesic, S., Marusic, M. and Pokric, B. (1992) Cellular immune response to the antigen administered as an immune complex in vivo. Immunology, 75, 325-329.
26. McShane, H., Pathan, A.A., Sander, C.R., Keating, S.M., Gilbert, S.C., Huygen, K., Fletcher, H.A. and Hill, A.V. (2004) Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat. Med. 10, 1240-1244.
27. Mustafa, A.S., Amoudy, H.A., Wiker, H.G., Abal, A.T., Ravn, P., Oftung, F. and Andersen, P. (1998) Comparison of antigen-specific T-cell responses of tuberculosis patients using complex or single antigens of Mycobacterium tuberculosis. Scand. J. Immunol. 48, 535-543.
28. Olsen, A.W., Williams, A., Okkels, L.M., Hatch, G. and Andersen, P. (2004) Protective effect of a tuberculosis subunit vaccine based on a fusion of antigen 85B and ESAT-6 in the aerosol guinea pig model. Infect. Immun. 72, 6148-6150.
29. Park, H.D., Guinn, K.M., Harrell, M.I., Liao, R., Voskuil, M.I., Tompa, M., Schoolnik, G.K. and Sherman, D.R. (2003) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 48, 833-843.
30. Pepponi, I., Stylianou, E., van Dolleweerd, C., Diogo, G.R., Paul, M.J., Drake, P.M., Ma, J.K. and Reljic, R. (2013) Immune-complex mimics as a molecular platform for adjuvant-free vaccine delivery. PLoS ONE, 8, e60855.
31. Phoolcharoen, W., Bhoo, S.H., Lai, H., Ma, J., Arntzen, C.J., Chen, Q. and Mason, H.S. (2011a) Expression of an immunogenic Ebola immune complex in Nicotiana benthamiana. Plant Biotechnol. J. 9, 807-816.
32. Phoolcharoen, W., Dye, J.M., Kilbourne, J., Piensook, K., Pratt, W.D., Arntzen, C.J., Chen, Q., Mason, H.S. and Herbst-Kralovetz, M.M. (2011b) A nonreplicating subunit vaccine protects mice against lethal Ebola virus challenge. Proc. Natl Acad. Sci. USA, 108, 20695-20700.
33. Reljic, R., Clark, S.O., Williams, A., Falero-Diaz, G., Singh, M., Challacombe, S., Marsh, P.D. and Ivanyi, J. (2006a) Intranasal IFNgamma extends passive IgA antibody protection of mice against Mycobacterium tuberculosis lung infection. Clin. Exp. Immunol. 143, 467-473.
34. Reljic, R., Williams, A. and Ivanyi, J. (2006b) Mucosal immunotherapy of tuberculosis: is there a value in passive IgA? Tuberculosis (Edinb), 86, 179-190.
35. Rogerson, B.J., Jung, Y.J., LaCourse, R., Ryan, L., Enright, N. and North, R.J. (2006) Expression levels of Mycobacterium tuberculosis antigen-encoding genes versus production levels of antigen-specific T cells during stationary level lung infection in mice. Immunology, 118, 195-201.
36. Roosnek, E. and Lanzavecchia, A. (1991) Efficient and selective presentation of antigen-antibody complexes by rheumatoid factor B cells. J. Exp. Med. 173, 487-489.
37. Roupie, V., Romano, M., Zhang, L., Korf, H., Lin, M.Y., Franken, K.L., Ottenhoff, T.H., Klein, M.R. and Huygen, K. (2007) Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice. Infect. Immun. 75, 941-949.
38. Santosuosso, M., McCormick, S., Zhang, X., Zganiacz, A. and Xing, Z. (2006) Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral Mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect. Immun. 74, 4634-4643.
39. Simitsek, P.D., Campbell, D.G., Lanzavecchia, A., Fairweather, N. and Watts, C. (1995) Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J. Exp. Med. 181, 1957-1963.
40. Studier, F.W. (1991) Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J. Mol. Biol. 219, 37-44.
41. Sun, R., Skeiky, Y.A., Izzo, A., Dheenadhayalan, V., Imam, Z., Penn, E., Stagliano, K., Haddock, S., Mueller, S., Fulkerson, J., Scanga, C., Grover, A., Derrick, S.C., Morris, S., Hone, D.M., Horwitz, M.A., Kaufmann, S.H. and Sadoff, J.C. (2009) Novel recombinant BCG expressing perfringolysin O and the over-expression of key immunodominant antigens; pre-clinical characterization, safety and protection against challenge with Mycobacterium tuberculosis. Vaccine, 27, 4412-4423.
42. Tameris, M.D., Hatherill, M., Landry, B.S., Scriba, T.J., Snowden, M.A., Lockhart, S., Shea, J.E., McClain, J.B., Hussey, G.D., Hanekom, W.A., Mahomed, H. and McShane, H. (2013) Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet, 381, 1021-1028.
43. Teh, A.Y., Maresch, D., Klein, K. and Ma, J.K. (2013) Characterization of VRC01, a potent and broadly neutralizing anti-HIV mAb, produced in transiently and stably transformed tobacco. Plant Biotechnol. J. doi: 10.1111/pbi.12137. [Epub ahead of print].
44. Von Eschen, K., Morrison, R., Braun, M., Ofori-Anyinam, O., De Kock, E., Pavithran, P., Koutsoukos, M., Moris, P., Cain, D., Dubois, M.C., Cohen, J. and Ballou, W.R. (2009) The candidate tuberculosis vaccine Mtb72F/AS02A: tolerability and immunogenicity in humans. Hum. Vaccin. 5, 475-482.
45. Wiersma, E.J., Coulie, P.G. and Heyman, B. (1989) Dual immunoregulatory effects of monoclonal IgG-antibodies: suppression and enhancement of the antibody response. Scand. J. Immunol. 29, 439-448.
46. Wiker, H.G. and Harboe, M. (1992) The antigen 85 complex: a major secretion product of Mycobacterium tuberculosis. Microbiol. Rev. 56, 648-661.
47. Wilkinson, R.J., Wilkinson, K.A., De Smet, K.A., Haslov, K., Pasvol, G., Singh, M., Svarcova, I. and Ivanyi, J. (1998) Human T- and B-cell reactivity to the 16 kDa alpha-crystallin protein of Mycobacterium tuberculosis. Scand. J. Immunol. 48, 403-409.
48. Williams, A., Reljic, R., Naylor, I., Clark, S.O., Falero-Diaz, G., Singh, M., Challacombe, S., Marsh, P.D. and Ivanyi, J. (2004) Passive protection with immunoglobulin A antibodies against tuberculous early infection of the lungs. Immunology, 111, 328-333.
49. Yuan, Y., Crane, D.D. and Barry, C.E. 3rd. (1996) Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial alpha-crystallin homolog. J. Bacteriol. 178, 4484-4492.
50. Yuan, Y., Crane, D.D., Simpson, R.M., Zhu, Y.Q., Hickey, M.J., Sherman, D.R. and Barry, C.E. 3rd. (1998) The 16-kDa alpha-crystallin (Acr) protein of Mycobacterium tuberculosis is required for growth in macrophages. Proc. Natl Acad. Sci. USA, 95, 9578-9583.
51. Yusibov, V., Streatfield, S.J. and Kushnir, N. (2011) Clinical development of plant-produced recombinant pharmaceuticals: vaccines, antibodies and beyond. Hum. Vaccin. 7, 313-321.
52. Zelada, A.M., Calamante, G., de la Paz Santangelo, M., Bigi, F., Verna, F., Mentaberry, A. and Cataldi, A. (2006) Expression of tuberculosis antigen ESAT-6 in Nicotiana tabacum using a potato virus X-based vector. Tuberculosis (Edinb), 86, 263-267.