Oral delivery of Acid Alpha Glucosidase epitopes expressed in plant chloroplasts suppresses antibody formation in treatment of Pompe mice

Plant Biotechnology Journal

Volumn 13, Issue 8, 2015, Pages 1023-1032

  Su, Jin ^a   Sherman, Alexandra ^b   Doerfler, Phillip A ^b   Byrne, Barry J ^b   Herzog, Roland W ^b   Daniell, Henry ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Bioencapsulation; Enzyme replacement therapy; Lysosomal storage disorder; Molecular farming; Oral tolerance; Pompe disease

Indexed keywords

ALPHA GLUCOSIDASE; CHOLERA TOXIN; EPITOPE; GAA PROTEIN, HUMAN; HYBRID PROTEIN;

ANIMAL; ANTIBODY PRODUCTION; CHLOROPLAST; DISEASE MODEL; ENZYME REPLACEMENT; GENE EXPRESSION; GENE VECTOR; GENETICS; GLYCOGEN STORAGE DISEASE TYPE II; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; ORAL DRUG ADMINISTRATION; PHENOTYPE; TOBACCO; TRANSGENIC PLANT;

ADMINISTRATION, ORAL; ALPHA-GLUCOSIDASES; ANIMALS; ANTIBODY FORMATION; CHLOROPLASTS; CHOLERA TOXIN; DISEASE MODELS, ANIMAL; ENZYME REPLACEMENT THERAPY; EPITOPES; GENE EXPRESSION; GENETIC VECTORS; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; MICE; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; TOBACCO;

EID: 84942194703     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12413     Document Type: Article

References (64)

1. Arakawa, T., Yu, J., Chong, D.K., Hough, J., Engen, P.C. and Langridge, W.H. (1998) A plant-based cholera toxin B subunit-insulin fusion protein protects against the development of autoimmune diabetes. Nat. Biotechnol. 16, 934-938.
2. Bergerot, I., Ploix, C., Petersen, J., Moulin, V., Rask, C., Fabien, N., Lindblad, M., Mayer, A., Czerkinsky, C., Holmgren, J. and Thivolet, C. (1997) A cholera toxoid-insulin conjugate as an oral vaccine against spontaneous autoimmune diabetes. Proc. Natl Acad. Sci. USA, 94, 4610-4614.
3. Boyhan, D. and Daniell, H. (2011) Low-cost production of proinsulin in tobacco and lettuce chloroplasts for injectable or oral delivery of functional insulin and C-peptide. Plant Biotechnol. J. 9, 585-598.
4. Brooks, D.A., Kakavanos, R. and Hopwood, J.J. (2003) Significance of immune response to enzyme-replacement therapy for patients with a lysosomal storage disorder. Trends Mol. Med. 9, 450-453.
5. Byrne, B.J., Falk, D.J., Pacak, C.A., Nayak, S., Herzog, R.W., Elder, M.E., Collins, S.W., Conlon, T.J., Clement, N., Cleaver, B.D., Cloutier, D.A., Porvasnik, S.L., Islam, S., Elmallah, M.K., Martin, A., Smith, B.K., Fuller, D.D., Lawson, L.A. and Mah, C.S. (2011) Pompe disease gene therapy. Hum. Mol. Genet. 20, R61-R68.
6. Chen, S., Hajirezaei, M. and Börnke, F. (2005) Differential expression of sucrose-phosphate synthase isoenzymes in tobacco reflects their functional specialization during dark-governed starch mobilization in source leaves. Plant Physiol. 139, 1163-1174.
7. Daniell, H. (2002) Molecular strategies for gene containment in transgenic crops. Nat. Biotechnol. 20, 581-586.
8. Daniell, H. (2007) Transgene containment by maternal inheritance: effective or elusive? Proc. Natl Acad. Sci. USA, 104, 6879-6880.
9. Daniell, H., Datta, R., Varma, S., Gray, S. and Lee, S.B. (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat. Biotechnol. 16, 345-348.
10. Daniell, H., Lee, S.B., Panchal, T. and Wiebe, P.O. (2001) Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J. Mol. Biol. 31, 1001-1009.
11. Daniell, H., Ruiz, O.N. and Dhingra, A. (2004) Chloroplast genetic engineering to improve agronomic traits. Methods Mol. Biol. 286, 111-137.
12. Daniell, H., Ruiz, G., Denes, B., Sandberg, L. and Langridge, W. (2009a) Optimization of codon composition and regulatory elements for expression of human insulin like growth factor-1 in transgenic chloroplasts and evaluation of structural identity and function. BMC Biotechnol. 9, 33, doi:10.1186/1472-6750-9-33.
13. Daniell, H., Singh, N.D., Mason, H. and Streatfield, S.J. (2009b) Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci. 14, 669-679.
14. De Cosa, B., Moar, W., Lee, S.B., Miller, M. and Daniell, H. (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat. Biotechnol. 19, 71-74.
15. Dénes, B., Fodor, I. and Langridge, W.H.R. (2013) Persistent suppression of Type 1 Diabetes by a multicomponent vaccine containing a cholera toxin B subunit-autoantigen fusion protein and Complete Freund's Adjuvant. Clin. Dev. Immunol. Article ID 578786. doi:10.1155/2013/578786.
16. DeRuisseau, L.R., Fuller, D.D., Qiu, K., DeRuisseau, K.C., Donnelly, W.H., Mah, C., Reier, P.J. and Byrne, B.J. (2009) Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc. Natl Acad. Sci. USA, 106, 9419-9424.
17. Dolgin, E. (2014) Immunology-Oral solutions. Nature, 515, S166-S167.
18. Elder, M.E., Sushrusha, N.S., Collins, S.W., Lawson, L.A., Kelley, J.S., Herzog, R.W., Modica, R.F., Lew, J., Lawrence, R.M. and Byrne, B.J. (2013) B-Cell depletion and immunomodulation before initiation of enzyme replacement therapy blocks the immune response to acid alpha-glucosidase in Infantile-Onset Pompe disease. J. Pediatr. 163, 847-854.
19. Eriksson, K., Fredriksson, M., Nordström, I. and Holmgren, J. (2003) Cholera toxin and its B subunit Promote dendritic cell vaccination with different influences on Th1 and Th2 development. Infect. Immun. 71, 1740-1747.
20. Falk, D.J., Todd, A.G., Lee, S., Soustek, M.S., ElMallah, M.K., Fuller, D.D., Notterpek, L. and Byrne, B.J. (2015) Peripheral nerve and neuromuscular junction pathology in Pompe disease. Hum. Mol. Genet. 24, 625-636.
21. van Gelder, C.M., Hoogeveen-Westerveld, M., Kroos, M.A., Plug, I., van der Ploeg, A.T. and Reuser, A.J.J. (2015) Enzyme therapy and immune response in relation to CRIM status: the Dutch experience in classic infantile Pompe disease. J. Inherit. Metab. Dis. 38, 305-314. doi: 10.1007/s10545-014-9707-6
22. Heckman, K.L. and Pease, L. (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2, 924-932.
23. Hermans, M.M.P., Marian, A., Kroos, M.A., van Beeurnens, J., Ben, A., Oostra, B.A. and Reuser, A.J.J. (1991) Human Lysosomal a-Glucosidase - characterization of the catalytic site. J. Biol. Chem. 266, 13507-13512.
24. Hermans, M.M.P., Wisselaar, H.A., Kroos, M.A., Oostra, B.A. and Reuser, A.J.J. (1993) Human lysosomal a-glucosidase: functional characterization of the glycosylation sites. Biochem. J. 289, 681-686.
25. Hoefsloot, L.H., Hoogeveen-Westerveld, M., Kroos, M.A., van Beeumen, J., Reuser, J.A. and Oostra, B.A. (1988) Primary structure and processing of lysosomal a-glucosidase; homology with the intestinal sucrase isomaltase complex. EMBO J. 7, 1697-1704.
26. Jansen, R.K., Raubeson, L.A., Boore, J.L., dePamphilis, C.W., Chumley, T.W., Haberle, R.C., Wyman, S.K., Alverson, A.J., Peery, R., Herman, S.J., Fourcade, H.M., Kuehl, J.V., McNeal, J.R., Leebens-Mack, J. and Cui, L. (2005) Methods for obtaining and analyzing chloroplast genome sequences. Methods Enzymol. 395, 348-384.
27. Kim, Y.C., Zhang, A.H., Su, Y., Rieder, S.A., Rossi, R.J., Ettinger, R.A., Pratt, K.P., Shevach, E.M. and Scott, D.W. (2015) Engineered antigen-specific human regulatory T cel ls: immunosuppression of FVIII-specific T- and B-cell responses. Blood, 125, 1107-1115. doi: 10.1182/blood-2014-04-566786.
28. Kishnani, P.S., Corzo, D., Nicolino, M., Byrne, B., Mandel, H., Hwu, W.L., Leslie, N., Levine, J., Spencer, C., Mcdonald, M., Li, J., Dumontier, J., Halberthal, M., Chien, Y.H., Hopkin, R., Vijayaraghavan, S., Gruskin, D., Bartholomew, D., Van Der, P.A., Clancy, J.P., Parini, R., Morin, G., Beck, M., De La Gastine, G.S., Jokic, M., Thurberg, B., Richards, S., Bali, D., Davison, M., Worden, M.A., Chen, Y.T. and Wraith, J.E. (2007) Recombinant human acid alpha-glucosidase: major clinical benefits in infantile-onset Pompe disease. Neurology, 68, 99-109.
29. Kishnani, P.S., Goldenberg, P.C., Dearmey, S.L., Heller, J., Benjamin, D., Young, S., Bali, D., Smith, S.A., Li, J.S., Mandel, H., Koeberl, D., Rosenberg, A. and Chen, Y.T. (2010) Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol. Genet. Metab. 99, 26-33.
30. Kohli, N., Westerveld, D.R., Ayache, A.C., Verma, A., Shil, P., Prasad, T., Zhu, P., Chan, S.L., Li, Q. and Daniell, H. (2014) Oral delivery of bioencapsulated proteins across blood-brain and blood-retinal barriers. Mol. Ther. 22, 535-546.
31. Koya, V., Moayeri, M., Leppla, S.H. and Daniell, H. (2005) Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect. Immun. 73, 8266-8274.
32. Kraehenbuhl, J.P., Hopkins, S.A., Kernéis, S. and Pringault, E. (1997) Antigen sampling by epithelial tissues: implication for vaccine design. Behring Inst. Mitt. 98, 24-32.
33. Kumar, S., Hahn, F.M., Baidoo, E., Kahlon, T.S., Wood, D.F., McMahan, C.M., Cornish, K., Keasling, J.D., Daniell, H. and Whalen, M.C. (2012) Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts. Metab. Eng. 14, 19-28.
34. Kumar, S. and Daniell, H. (2004) Engineering the chloroplast genome for hyperexpression of human therapeutic proteins and vaccine antigens. Methods Mol. Biol. 267, 365-383.
35. Kwon, K.-C., Verma, D., Singh, N.D., Herzog, R. and Daniell, H. (2013a) Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv. Drug Deliv. Rev. 65, 782-799.
36. Kwon, K.-C., Nityanandam, R., James, S., New, J.S. and Daniell, H. (2013b) Oral delivery of bioencapsulated exendin-4 expressed in chloroplasts lowers blood glucose level in mice and stimulates insulin secretion in beta-TC6 cells. Plant Biotechnol. J. 11, 77-86.
37. Limaye, A., Koya, V., Samsam, M. and Daniell, H. (2006) Receptor-mediated oral delivery of a bioencapsulated green fluorescent protein expressed in transgenic chloroplasts into the mouse circulatory system. FASEB J. 20, 959-961.
38. Lobo, A.K.M., Martins, M.O., Neto, M.C.L., Machado, E.C., Ribeiro, R.V. and Silveira, J.A.G. (2015) Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity. J. Plant Physiol. 179, 113-121.
39. Ma, S., Huang, Y., Yin, Z., Menassa, R., Brandle, J.E. and Jevnikar, A.M. (2004) Induction of oral tolerance to prevent diabetes with transgenic plants requires glutamic acid decarboxylase (GAD) and IL-4. Proc. Natl Acad. Sci. USA, 101, 5680-5685.
40. Maga, J.A., Zhou, J., Kambampati, R., Peng, S., Wang, X., Bohnsack, R.N., Thomm, A., Golata, S., Tom, P., Dahms, N.M., Byrne, B.J. and LeBowitz, J.H. (2013) Glycosylation-independent lysosomal targeting of acid α-glucosidase enhances muscle glycogen clearance in Pompe mice. J. Biol. Chem. 288, 1428-1438.
41. Messinger, Y.H., Mendelsohn, N.J., Rhead, W., Dimmock, D., Hershkovitz, E., Michael Champion, M., Jones, S.A., Olson, R., White, A., Wells, C., Bali, D., Case, L.E., Young, S.P., Rosenberg, A.S. and Kishnani, P.S. (2012) Successful immune tolerance induction to enzyme replacement therapy in CRIM-negative infantile Pompe disease. Genet. Med. 14, 135-142.
42. Nashar, T.O. and Hirst, T.R. (1995) Immunoregulatory role of H-2 and intra-H-2 alleles on antibody responses to recombinant preparations of B-subunits of Escherichia coli heat-labile enterotoxin (rEtxB) and cholera toxin (rCtxB). Vaccine, 13, 803-810.
43. Nayak, S., Sivakumar, R., Cao, O., Daniell, H., Byrne, B.J. and Herzog, R.W. (2012) Mapping the T helper cell response to acid α-glucosidase in Pompe mice. Mol. Genet. Metab. 106, 189-195.
44. Nayak, S., Doerfler, P.A., Porvasnik, S.L., Cloutier, D.D., Khanna, R., Valenzano, K.J., Herzog, R.W. and Byrne, B.J. (2014) Immune responses and hypercoagulation in ERT for Pompe disease are mutation and rhGAA dose dependent. PLoS One, 9, e98336. doi:10.1371/journal.pone.0098336.
45. Ohashi, T., Iizuka, S., Shimada, Y., Eto, Y., Ida, H., Hachimura, S. and Kobayashi, H. (2011) Oral administration of recombinant human acid α-glucosidase reduces specific antibody formation against enzyme in mouse. Mol. Genet. Metab. 103, 98-100.
46. Oshima, A., Nolan, C.M., Kyle, J.W., Grubb, J.H. and Sly, W.S. (1988) The human cation-independent mannose 6-phosphate receptor. Cloning and sequence of the full-length cDNA and expression of functional receptor in COS cells. J. Biol. Chem. 263, 2553-2562.
47. Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J.P. and Ricciardi-Castagnoli, P. (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367.
48. Rogers, G.L. and Herzog, R.W. (2015) Gene therapy for hemophilia. Front Biosci. (Landmark Ed.) 20, 556-603.
49. Ruhlman, T., Ahangari, R., Devine, A., Samsam, M. and Daniell, H. (2007) Expression of cholera toxin B-proinsulin fusion protein in lettuce and tobacco chloroplasts-oral administration protects against development of insulitis in non-obese diabetic mice. Plant Biotechnol. J. 5, 495-510.
50. Ruhlman, T., Verma, D., Samson, N. and Daniell, H. (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol. 152, 2088-2104.
51. Sack, B.K., Herzog, R.W., Terhorst, C. and Markusic, D.M. (2014) Development of gene transfer for induction of antigen-specific tolerance. Mol Ther Methods Clin. Dev. 1, 14013.
52. Saski, C., Lee, S.B., Fjellheim, S., Guda, C., Jansen, R.K., Luo, H., Tomkins, J., Rognli, O.A., Daniell, H. and Clarke, J.L. (2007) Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor. Appl. Genet. 115, 571-590.
53. Shaaltiel, Y., Bartfeld, D., Hashmueli, S., Baum, G., Brill-Almon, E., Galili, G., Dym, O., Boldin-Adamsky, S.A., Israel Silman, I., Sussman, J.L., Futerman, A.H. and Aviezer, D. (2007) Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol. J. 5, 579-590.
54. Shenoy, V., Kwon, K.-C., Rathinasabapathy, A., Lin, S., Jin, G., Song, C., Shil, P., Nair, A., Qi, Y., Li, Q., Francis, J., Katovich, M.J., Daniell, H. and Raizad, M.K. (2014) Oral delivery of Angiotensin-Converting Enzyme 2 and Angiotensin-(1-7) bioencapsulated in plant cells attenuates pulmonary hypertension. Hypertension, 64, 1248-1259. doi:10.1161/HYPERTENSIONAHA.114.03871.
55. Sherman, A., Su, J., Lin, S., Wang, X., Herzog, R.W. and Daniell, H. (2014) Suppression of inhibitor formation against FVIII in a murine model of hemophilia A by oral delivery of antigens bioencapsulated in plant cells. Blood, 124, 1659-1668.
56. Shil, P.K., Kwon, K.-C., Zhu, P., Verma, A., Daniell, H. and Li, Q. (2014) Oral Delivery of ACE2/Ang-(1-7) bioencapsulated in plant cells protects against experimental uveitis and autoimmune uveoretinitis. Mol. Ther. 22, 2069-2082. doi:10.1038/mt.2014.179.
57. Sun, J.B., Holmgren, J. and Czerkinsky, C. (1994) Cholera toxin B subunit: an efficient transmucosal carrier-delivery system for induction of peripheral immunological tolerance. Proc. Natl Acad. Sci. USA, 91, 10795-10799.
58. Sun, B., Bird, A., Young, S.P., Kishnani, P.S., Chen, Y.T. and Koeberl, D.D. (2007) Enhanced response to enzyme replacement therapy in Pompe disease after the induction of immune tolerance. Am. J. Hum. Genet. 81, 1042-1049.
59. Tsuji, T., Watanabe, K. and Miyama, A. (1995) Monomer of the B subunit of heat-labile enterotoxin from enterotoxigenic Escherichia coli has little ability to bind to GM1 ganglioside compared to its coligenoid. Microbiol. Immunol. 39, 817-819.
60. Verma, D., Samson, N.P., Koya, V. and Daniell, H. (2008) A protocol for expression of foreign genes in chloroplasts. Nat. Protoc. 3, 739-758.
61. Verma, D., Moghimi, B., LoDuca, P.A., Singh, H.D., Hoffman, B.E., Herzog, R.W. and Daniell, H. (2010) Oral delivery of bioencapsulated coagulation factor IX prevents inhibitor formation and fatal anaphylaxis in hemophilia B mice. Proc. Natl Acad. Sci. USA, 107, 7101-7106.
62. Walsh, G. (2014) Biopharmaceutical benchmarks. Nat. Biotechnol. 32, 992-1000.
63. Wang, X., Sherman, A., Liao, G., Kam, W., Leong, K.W., Daniell, H., Terhorst, C. and Herzog, R.W. (2013) Mechanism of oral tolerance induction to therapeutic proteins. Adv. Drug Deliv. Rev. 65, 759-773.
64. + T cells. Blood, 125, 2418-2427.