The production of human glucocerebrosidase in glyco-engineered Nicotiana benthamiana plants

Plant Biotechnology Journal

Volumn 14, Issue 8, 2016, Pages 1682-1694

  Limkul, Juthamard ^a   Iizuka, Sayoko ^b   Sato, Yohei ^b   Misaki, Ryo ^a   Ohashi, Takao ^a   Ohashi, Toya ^b   Fujiyama, Kazuhito ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

glyco engineered plant; human glucocerebrosidase; N acetylglucosaminyltransferase I; Nicotiana benthamiana; plant made pharmaceuticals

Indexed keywords

ALPHA-1,3-MANNOSYL-GLYCOPROTEIN BETA-1,2-N-ACETYLGLUCOSAMINYLTRANSFERASE I; CELL SURFACE RECEPTOR; GLUCOSYLCERAMIDASE; LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR; N ACETYLGLUCOSAMINYLTRANSFERASE; POLYSACCHARIDE; RECOMBINANT PROTEIN;

ANIMAL; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; GENETICS; GLYCOSYLATION; HUMAN; ISOLATION AND PURIFICATION; MACROPHAGE; METABOLISM; POLLINATION; RNA INTERFERENCE; TISSUE DISTRIBUTION; TOBACCO; TRANSGENIC PLANT;

ANIMALS; GLUCOSYLCERAMIDASE; GLYCOSYLATION; HUMANS; LECTINS, C-TYPE; MACROPHAGES; MANNOSE-BINDING LECTINS; MICE, INBRED C57BL; N-ACETYLGLUCOSAMINYLTRANSFERASES; PLANTS, GENETICALLY MODIFIED; POLLINATION; POLYSACCHARIDES; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; RNA INTERFERENCE; TISSUE DISTRIBUTION; TOBACCO;

EID: 84958259501     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12529     Document Type: Article

References (48)

1. Altmann, F. (2007) The role of protein glycosylation in allergy. Int. Arch. Allergy Immunol. 142, 99–115.
2. Becker, D., Kemper, E., Schell, J. and Masterson, R. (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20, 1195–1197.
3. Bencurova, M., Hemmer, W., Focke, T., Wilson, I. and Altmann, F. (2004) Specificity of IgG and IgE antibodies against plant and insect glycoprotein glycans determined with artificial glycoforms of human transferrin. Glycobiology, 14, 457–466.
4. Bosch, D., Castilho, A., Loos, A., Schots, A. and Steinkellner, H. (2013) N-glycosylation of plant-produced recombinant proteins. Curr. Pharm. Des. 19, 5503–5512.
5. Brumshtein, B., Peterson, B., Chan, V., Silman, I., Sussman, J.L., Savickas, P.J., Robinson, G.S. and Futerman, A.H. (2010) Characterization of gene-activated human acid- glucosidase: Crystal structure, glycan composition, and internalization into macrophages. Glycobiol. 20, 24–32.
6. Dohi, K., Ishoyama-Tanaka, J., Tokuda, T. and Fujiyama, K. (2010) Recombinant expression and characterization of N-acetylglucosaminyltransferase I derived from Nicotiana tabacum. J. Biosci. Bioeng. 109, 388–391.
7. Ernst, O. and Zor, T. (2010) Linearization of the bradford protein assay. J. Vis. Exp. 38, 1918.
8. Fanata, W.I., Lee, K.H., Son, B.H., Yoo, J.Y., Harmoko, R., Ko, K.S., Ramasamy, N.K. et al. (2013) N-glycan maturation is crucial for cytokinin-mediated development and cellulose synthesis in Oryza sativa. Plant J. 73, 966–979.
9. Fitchette-Laine, A., Gomord, V., Chekkafi, A. and Faye, L. (1994) Distribution of xylosylation and fucosylation in the plant Golgi apparatus. Plant J. 5, 673–682.
10. Friedman, B. and Hayes, M. (1996) Enhanced in vivo uptake of glucocerebrosidase. US Patent 5549892.
11. Ginns, E.I., Choudary, P.V., Tsuji, S., Martin, B., Stubblefield, B., Sawyert, J., Hoziert, J. et al. (1985) Gene mapping and leader polypeptide sequence of human glucocerebrosidase: implications for Gaucher disease. Proc. Natl Acad. Sci. USA, 82, 7101–7105.
12. Grace, M.E. and Grabowski, G.A. (1990) Human acid beta-glucosidase: glycosylation is required for catalytic activity. Biochem. Biophys. Res. Commun. 168, 771–777.
13. Gregory, S.H. (1988) Substratum-dependent proliferation and survival of bone marrow-derived mononuclear phagocytes. J. Leukoc. Biol. 43, 67–79.
14. He, X., Galpin, J.D., Tropak, M.B., Mahuran, D., Haselhorst, T., von Itzstein, M., Kolarich, D. et al. (2012) Production of active human glucocerebrosidase in seeds of arabidopsis thaliana complex glycan-deficient (cgl) plants. Glycobiology, 22, 492–503.
15. He, X., Pierce, O., Haselhorst, T., von Itzstein, M., Kolarich, D., Packer, N.H., Gloster, T.M. et al. (2013) Characterization and downstream mannose phosphorylation of human recombinant α-l-iduronidase produced in Arabidopsis complex glycan-deficient (cgl) seeds. Plant Biotechnol. J. 11, 1034–1043.
16. Kermode, A.R. (2012) Seed expression systems for molecular farming. In Molecular Farming in Plants: Recent Advances and Future Prospects (Wang, A. and Ma, S., eds), pp. 89–123. New York: Springer Science Business Media.
17. Klimyuk, V., Pogue, G., Herz, S., Butler, J. and Haydon, H. (2014) Production of recombinant antigens and antibodies in Nicotiana benthamiana using ‘magnifection’ technology: GMP-compliant facilities for small- and large-scale manufacturing. Curr. Top. Microbiol. Immunol. 375, 127–154.
18. Lauriere, M., Lauriere, C., Chrispeels, M.J., Johnson, K.D. and Sturm, A. (1989) Characterization of a xylose-specific antiserum that reacts with the complex asparagine-linked glycans of extracellular and vacuolar glycoproteins. Plant Physiol. 90, 1182–1188.
19. Li, J., Stoddard, T.J., Demorest, Z.L., Lavoie, P.O., Luo, S., Clasen, B.M., Cedrone, F. et al. (2015) Multiplexed, targeted gene editing in Nicotiana benthamiana for glyco-engineering and monoclonal antibody production. Plant Biotechnol. J. doi: 10.1111/pbi.12403.
20. Liebminger, E., Veit, C., Pabst, C., Batoux, M., Zipfel, C., Altmann, F., Mach, L. et al. (2011) β-N-Acetylhexosaminidases HEXO1 and HEXO3 are responsible for the formation of paucimannosidic N-glycans in Arabidopsis thaliana. J. Biol. Chem. 286, 10793–10802.
21. Limkul, J., Misaki, R., Kato, K. and Fujiyama, K. (2015) The combination of plant translational enhancers and terminator increase the expression of human glucocerebrosidase in Nicotiana benthamiana plants. Plant Sci. 240, 41–49.
22. Liu, D., Raghothama, K.G., Hasegawa, P.M. and Bressan, R.A. (1994) Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad. Sci. USA 91, 1888–1892.
23. Marillonnet, S., Thoeringer, C., Kandzia, R., Klimyuk, V. and Gleba, Y. (2005) Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nat. Biotechnol. 23, 718–723.
24. Misaki, R., Kimura, Y., Fujiyama, K. and Seki, T. (2001) Glycoproteins secreted from suspension-cultured tobacco BY2 cells have distinct glycan structures from intracellular glycoproteins. Biosci. Biotechnol. Biochem. 65, 2482–2488.
25. Morelle, W. and Michalski, J.C. (2007) Analysis of protein glycosylation by mass spectrometry. Nat. Protoc. 2, 1585–1602.
26. O'Keefe, B.R., Vojdani, F., Buffa, V., Shattock, R.J., Montefiori, D.C., Bakke, J., Mirsalis, J. et al. (2009) Scaleable manufacture of HIV-1 entry in hibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc. Natl Acad. Sci. USA, 106, 6099–6104.
27. van Patten, S.M., Hughes, H., Huff, M.R., Piepenhagen, P.A., Waire, J., Qiu, H., Ganesa, C. et al. (2007) Effect of mannose chain length on targeting of glucocerebrosidase for enzyme replacement therapy of Gaucher disease. Glycobiology, 17, 467–478.
28. Ramírez, N., Ayala, M., Lorenzo, D., Palenzuela, D., Herrera, L., Doreste, V., Pérez, M. et al. (2002) Expression of a single-chain Fv antibody fragment specific for the hepatitis B surface antigen in transgenic tobacco plants. Transgenic Res. 11, 61–64.
29. Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V. and Scott, D.A. (2013) Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281–2308.
30. van Ree, R., Cabanes-Macheteau, M., Akkerdaas, J., Milazzo, J.P., Loutelier-Bourhis, C., Rayon, C., Villalba, M. et al. (2000) β(1,2)-Xylose and α(1,3)-Fucose residues have a strong contribution in IgE binding to plant glycoallergens. J. Biol. Chem. 275, 11451–11458.
31. von Schaewen, A., Sturm, A., O'Neill, J. and Chrispeels, M.J. (1993) Isolation of a mutant Arabidopsis plant that lacks N-acetylglucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiol. 102, 1109–1118.
32. Shaaltiel, Y., Bartfield, D., Hashmueli, S., Baum, G., Brill-Almon, E., Galili, G., Dym, O. et al. (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.
33. Shimizu, Y., Nakata, M., Kuroda, Y., Tsutsumi, F., Kojima, N. and Mizuochi, T. (2001) Rapid and simple preparation of N-linked oligosaccharides by cellulose-column chromatography. Carbohydr. Res. 332, 381–388.
34. Strasser, R. (2014) Biological significance of complex N-glycans in plants and their impact on plant physiology. Front. Plant Sci. 363, 1–6.
35. Strasser, R., Altmann, F., Glössl, J. and Steinkellner, H. (2004) Unaltered complex N-glycan profiles in Nicotiana benthamiana despite drastic reduction of beta1,2-N-acetylglucosaminyltransferase I activity. Glycoconj. J. 21, 275–282.
36. Strasser, R., Stadlmann, J., Svoboda, B., Altmann, F., Glössl, J. and Mach, L. (2005) Molecular basis of N-acetylglucosaminyltransferase I deficiency in Arabidopsis thaliana plants lacking complex N-glycans. Biochem. J. 387, 385–391.
37. Strasser, R., Bondili, J.S., Schoberer, J., Svoboda, B., Liebminger, E., Glössl, J., Altmann, F. et al. (2007) Enzymatic properties and subcellular localization of Arabidopsis beta-N-acetylhexosaminidases. Plant Physiol. 145, 5–16.
38. Strasser, R., Stadlmann, J., Schähs, M., Stiegler, G., Quendler, H., Mach, L., Glössl, J. et al. (2008) Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol. J. 6, 392–402.
39. Takasaki, S., Murray, G.J., Furbish, F.S., Brady, R.O., Barranger, J.A. and Kobata, A. (1984) Structure of the N-asparagine-linked oligosaccharide units of human placental beta-glucocerebrosidase. J. Biol. Chem. 259, 10112–10117.
40. Tekoah, Y., Tzaban, S., Kizhner, T., Hainrichson, M., Gantman, A., Golembo, M., Aviezer, D. et al. (2013) Glycosylation and functionality of recombinant β-glucocerebrosidase from various production systems. Biosci. Rep. 33, 771–781.
41. Tretter, V., Altmann, F. and März, L. (1991) Peptide-N4-(N-acetyl-beta-glucosaminyl)asparagine amidase F cannot release glycans with fucose attached alpha 1–3 to the asparagine-linked N-acetylglucosamine residue. Eur. J. Biochem. 199, 647–652.
42. Tretter, V., Altmann, F., Kubelka, V., März, L. and Becker, W.M. (1993) Fucose α1,3-linked to the core region of glycoprotein N-glycans creates an important epitope for IgE from honeybee venom allergic individuals. Int. Arch. Allergy Immunol. 102, 259–266.
43. Vitale, A. and Chrispeels, M.J. (1984) Transient N-acetylglucosamine in the biosynthesis of phytohemagglutinin: attachment in the Golgi apparatus and removal in protein bodies. J. Cell Biol. 99, 133–140.
44. Webster, D.E., Wang, L., Mulcair, M., Ma, C., Santi, L., Mason, H.S., Wesselingh, S.L. et al. (2009) Production and characterization of an orally immunogenic Plasmodium antigen in plants using a virus-based expression system. Plant Biotechnol. J. 7, 846–855.
45. Wenderoth, I. and von Schaewen, A. (2000) Isolation and characterization of plant N-acetylglucosaminyltransferase I (GntI) cDNA sequences: functional analyses in the Arabidopsis cgl mutant and in antisense plants. Plant Physiol. 123, 1097–1108.
46. Wood, J., Sames, J., Moore, A. and Ekins, S. (2013) Multifaceted roles of ultra-rare and rare disease patients/parents in drug discovery. Drug Discov. Today, 18, 1043–1051.
47. Yoo, J.Y., Ko, K.S., Lee, S.Y. and Lee, K.O. (2014) Glycoengineering in plants for the development of N-glycan structures compatible with biopharmaceuticals. Plant Biotechnol. Rep. 8, 357–376.
48. Zor, T. and Selinger, Z. (1996) Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal. Biochem. 236, 302–308.