Plant-based oral delivery of β-glucocerebrosidase as an enzyme replacement therapy for Gaucher's disease

Plant Biotechnology Journal

Volumn 13, Issue 8, 2015, Pages 1033-1040

  Shaaltiel, Yoseph ^a   Gingis Velitski, Svetlana ^a   Tzaban, Salit ^a,b   Fiks, Nadia ^a   Tekoah, Yoram ^a   Aviezer, David ^a,c  

^a Protalix Biotherapeutics   (Israel)

^b Enzymotec Ltd   (Israel)

^c BAR ILAN UNIVERSITY   (Israel)

Author keywords

Enzyme replacement therapy; Gaucher's disease; Lysosomal storage disorder; Oral delivery; Plant cells; glucocerebrosidase

Indexed keywords

GLUCOSYLCERAMIDASE; RECOMBINANT PROTEIN;

ANIMAL; ANTIBODY SPECIFICITY; BODY FLUID; CACO 2 CELL LINE; ENZYME REPLACEMENT; ENZYME STABILITY; GAUCHER DISEASE; HUMAN; INTESTINE MUCOSA; METABOLISM; ORAL DRUG ADMINISTRATION; PIG; PLANT CELL; RAT; TISSUE DISTRIBUTION; TOBACCO; TRANSCYTOSIS;

ADMINISTRATION, ORAL; ANIMALS; BODY FLUIDS; CACO-2 CELLS; ENZYME REPLACEMENT THERAPY; ENZYME STABILITY; GAUCHER DISEASE; GLUCOSYLCERAMIDASE; HUMANS; INTESTINAL MUCOSA; ORGAN SPECIFICITY; PLANT CELLS; RATS; RECOMBINANT PROTEINS; SUS SCROFA; TISSUE DISTRIBUTION; TOBACCO; TRANSCYTOSIS;

EID: 84942196886     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12366     Document Type: Article

References (44)

1. Alvarez, M.L., Pinyerd, H.L., Crisantes, J.D., Rigano, M.M., Pinkhasov, J., Walmsley, A.M., Mason, H.S. and Cardineau, G.A. (2006) Plant-made subunit vaccine against pneumonic and bubonic plague is orally immunogenic in mice. Vaccine, 24, 2477-2490.
2. 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.
3. Arlen, P.A., Singleton, M., Adamovicz, J.J., Ding, Y., Davoodi-Semiromi, A. and Daniell, H. (2008) Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infect. Immun. 76, 3640-3650.
4. Artursson, P. and Karlsson, J. (1991) Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem. Biophys. Res. Commun. 175, 880-885.
5. Aviezer, D., Brill-Almon, E., Shaaltiel, Y., Hashmueli, S., Bartfeld, D., Mizrachi, S., Liberman, Y., Freeman, A., Zimran, A. and Galun, E. (2009) A plant-derived recombinant human glucocerebrosidase enzyme - A preclinical and phase I investigation. PLoS ONE, 4, e4792.
6. Bennett, L.L. and Mohan, D. (2013) Gaucher disease and its treatment options. Ann. Pharmacother. 47, 1182-1193.
7. 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.
8. Brannon, P.M. (1990) Adaptation of the exocrine pancreas to diet. Annu. Rev. Nutr. 10, 85-105.
9. Carino, G.P. and Mathiowitz, E. (1999) Oral insulin delivery. Adv. Drug Deliv. Rev. 35, 249-257.
10. Chirino, A.J., Ary, M.L. and Marshall, S.A. (2004) Minimizing the immunogenicity of protein therapeutics. Drug Discov. Today, 9, 82-90.
11. Choi, J., Diao, H., Feng, Z.-C., Lau, A., Wang, R., Jevnikar, A.M. and Ma, S. (2014) A fusion protein derived from plants holds promising potential as a new oral therapy for type 2 diabetes. Plant Biotechnol. J. 12, 425-435.
12. Choonara, B.F., Choonara, Y.E., Kumar, P., Bijukumar, D., du Toit, L.C. and Pillay, V. (2014) A review of advanced oral drug delivery technologies facilitating the protection and absorption of protein and peptide molecules. Biotechnol. Adv. 32, 1269-1282.
13. Daniell, H., Chebolu, S., Kumar, S., Singleton, M. and Falconer, R. (2005) Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine, 23, 1779-1783.
14. Daniell, H., Singh, N.D., Mason, H. and Streatfield, S.J. (2009) Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci. 14, 669-679.
15. Devriendt, B., De Geest, B.G., Goddeeris, B.M. and Cox, E. (2012) Crossing the barrier: targeting epithelial receptors for enhanced oral vaccine delivery. J. Control. Release, 160, 431-439.
16. Dressman, J.B., Amidon, G.L., Reppas, C. and Shah, V.P. (1998) Dissolution testing as a prognostic tool for oral drug absorption: immediate release dosage forms. Pharm. Res. 15, 11-22.
17. Fischer, R., Stoger, E., Schillberg, S., Christou, P. and Twyman, R.M. (2004) Plant-based production of biopharmaceuticals. Curr. Opin. Plant Biol. 7, 152-158.
18. Fossati, L., Dechaume, R., Hardillier, E., Chevillon, D., Prevost, C., Sb, B. and Maubon, N. (2008) Use of simulated intestinal fluid for Caco-2 permeability assay of lipophilic drugs. Int. J. Pharm. 360, 148-155.
19. Grabowski, G.A., Golembo, M. and Shaaltiel, Y. (2014) Taliglucerase alfa: an enzyme replacement therapy using plant cell expression technology. Mol. Genet. Metab. 112, 1-8.
20. Gupta, S., Jain, A., Chakraborty, M., Sahni, J.K., Ali, J. and Dang, S. (2013) Oral delivery of therapeutic proteins and peptides: a review on recent developments. Drug Deliv. 20, 237-246.
21. Jahan-Mihan, A., Luhovyy, B.L., El Khoury, D. and Anderson, G.H. (2011) Dietary proteins as determinants of metabolic and physiologic functions of the gastrointestinal tract. Nutrients, 3, 574-603.
22. Kapusta, J., Modelska, A., Figlerowicz, M., Pniewski, T., Letellier, M., Lisowa, O., Yusibov, V., Koprowski, H., Plucienniczak, A. and Legocki, A.B. (1999) A plant-derived edible vaccine against hepatitis B virus. FASEB J, 13, 1796-1799.
23. Kwon, K.C., Nityanandam, R., New, J.S. and Daniell, H. (2013a) 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.
24. Kwon, K.C., Verma, D., Singh, N.D., Herzog, R. and Daniell, H. (2013b) Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv. Drug Deliv. Rev. 65, 782-799.
25. Lee, H.J. (2002) Protein drug oral delivery: the recent progress. Arch. Pharm. Res. 25, 572-584.
26. 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.
27. 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.
28. Morishita, M. and Peppas, N.A. (2006) Is the oral route possible for peptide and protein drug delivery? Drug Discov. Today, 11, 905-910.
29. Müller, G. (2010) Oral protein therapy for the future - transport of glycolipid-modified proteins: vision or fiction. Pharmacology, 86, 92-116.
30. Muller, C.P., Marquet-Blouin, E., Fack, F., Damien, B., Steinmetz, A. and Bouche, F.B. (2003) Immunogenic measles antigens expressed in plants: role as an edible vaccine for adults. Vaccine, 21, 816-819.
31. Park, K., Kwon, I.C. and Park, K. (2011) Oral protein delivery: current status and future prospect. React. Funct. Polym. 71, 280-287.
32. Patel, N., Forbes, B., Eskola, S. and Murray, J. (2006) Use of simulated intestinal fluids with Caco-2 cells and rat ileum. Drug Dev. Ind. Pharm. 32, 151-161.
33. Pinto Reis, C., Silva, C., Martinho, N. and Rosado, C. (2013) Drug carriers for oral delivery of peptides and proteins: accomplishments and future perspectives. Ther. Deliv. 4, 251-265.
34. Rosenbloom, B.E. and Weinreb, N.J. (2013) Gaucher disease: a comprehensive review. Crit. Rev. Oncog. 18, 163-175.
35. 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.
36. Shaaltiel, Y., Bartfeld, D., Hashmueli, S., Baum, G., Brill-Almon, E., Galili, G., Dym, O., Boldin-Adamsky, S.A., 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.
37. Sherman, A., Su, J., Lin, S., Wang, X., Herzog, R.W. and Daniell, H. (2014) Suppression of inhibitor formation against factor VIII in hemophilia A mice by oral delivery of antigens bioencapsulated in plant cells. Blood, 124, 1659-1668.
38. Tekoah, Y., Tzaban, S., Kizhner, T., Hainrichson, M., Gantman, A., Golembo, M., Aviezer, D. and Shaaltiel, Y. (2013) Glycosylation and functionality of recombinant β-Glucocerebrosidase from various production systems. Biosci. Rep. 33, 771-781. art:e00071.doi:10.1042/BSR20130081.
39. Tremblay, R., Wang, D., Jevnikar, A.M. and Ma, S. (2010) Tobacco, a highly efficient green bioreactor for production of therapeutic proteins. Biotechnol. Adv. 28, 214-221.
40. Urban, D.J., Zheng, W., Goker-Alpan, O., Jadhav, A., Lamarca, M.E., Inglese, J., Sidransky, E. and Austin, C.P. (2008) Optimization and validation of two miniaturized glucocerebrosidase enzyme assays for high throughput screening. Comb. Chem. High Throughput Screen. 11, 817-824.
41. 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.
42. Xie, T., Qiu, Q., Zhang, W., Ning, T., Yang, W., Zheng, C., Wang, C., Zhu, Y. and Yang, D. (2008) A biologically active rhIGF-1 fusion accumulated in transgenic rice seeds can reduce blood glucose in diabetic mice via oral delivery. Peptides, 29, 1862-1870.
43. Zimran, A. (2011) How I treat Gaucher disease. Blood, 118, 1463-1471.
44. Ziv, E., Lior, O. and Kidron, M. (1987) Absorption of protein via the intestinal wall. A quantitative model. Biochem. Pharmacol. 36, 1035-1039.