Glyco-engineering of biotherapeutic proteins in plants

Molecules and Cells

Volumn 25, Issue 4, 2008, Pages 494-503

  Ko, Kisung ^a   Ahn, Mi Hyun ^a   Song, Mira ^a   Choo, Young Kug ^a   Kim, Hyun Soon ^b   Ko, Kinarm ^c   Joung, Hyouk ^b  

^a Wonkwang University   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

Glycoprotein; Glycosylation; Molecular biopharming; Monoclonal antibody; Recombinant protein; Transgenic plant

Indexed keywords

GLYCOSYLTRANSFERASE; MONOCLONAL ANTIBODY; N GLYCOLOYLNEURAMINIC ACID; RABIES VACCINE; RECOMBINANT ANTIBODY; RECOMBINANT GLYCOPROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ACTIVE IMMUNIZATION; ANTINEOPLASTIC ACTIVITY; BIOENGINEERING; BIOLOGICAL ACTIVITY; BIOTECHNOLOGICAL PRODUCTION; CYTOTOXICITY; DRUG HALF LIFE; DRUG SYNTHESIS; ENZYME SPECIFICITY; GENE EXPRESSION SYSTEM; HUMAN; IMMUNOGENICITY; IMMUNOTHERAPY; NONHUMAN; PASSIVE IMMUNIZATION; PHARMACEUTICAL ENGINEERING; PLANT CELL; PROTEIN ENGINEERING; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SYSTEMS BIOLOGY;

BIOPHARMACEUTICS; ENDOPLASMIC RETICULUM; GLYCOPROTEINS; GLYCOSYLATION; GOLGI APPARATUS; HUMANS; PLANTS, GENETICALLY MODIFIED; PROTEIN ENGINEERING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS;

EID: 56049113736     PISSN: 10168478     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (73)

1. AS Insights (2005). Monoclonal antibody therapeutics-current market dynamics & future outlook. pp. 42.
2. Bakker, H., Bardor, M., Molthoff, J.W., Gomord, V, Elbers, I., Stevens, L.H., Jordi, W., Lommen, A., Faye, L., Lerouge, P., et al. (2001a). Galactose-extended glycans of antibodies produced by transgenic plants. Proc. Natl. Acad. Sci. USA 98, 2899-2904.
3. Bakker, H., Schijlen, E., de Vries, T., Schiphorst, W.E., Jordi, W., Lommen, A., Bosch, D., and van Die, I. (2001b). Plant members of the alphal → 3/4-fucosyltransferase gene family encode an alphal → 4-fucosyltransferase, potentially involved in Lewis (a) biosynthesis, and two core alphal → 3-fucosyltransferases. FEBS Lett. 507, 307-312.
4. Bardor, M., Loutelier-Bourhis, C., Paccalet, T., Cosette, P., Fitchette, A.C., Vézina, L.P., Trépanier, S., Dargis, M., Lemieux, R., Lange, C., et al. (2003). Monoclonal C5-1 antibody produced in transgenic alfalfa plants exhibits a N-glycosylation that is homogenous and suitable for glyco-engineering into human-compatible structures. Plant Biotechnol. J. 1, 451-462.
5. Bardor, M., Cabrera, G., Rudd, P.M., Dwek, R.A., Cremata, J.A., and Lerouge, P. (2006). Analytical strategies to investigate plant N-glycan profiles in the context of plant-made pharmaceuticals. Curr. Opin. Struct. Biol. 16, 576-583.
6. Brodzik, R., Glogowska, M., Bandurska, K., Okulicz, M., Deka, D., Ko, K., van der Linden, J., Leusen, J.H.W., Pogrebnyak, N., Golovkin, M., et al. (2006). Plant-derived anti-Lewis Y mAb exhibits biological activities for efficient immunotherapy against human cancer cells. Proc. Natl. Acad. Sci. USA 103, 8804-8809.
7. Cabanes-Macheteau, M., Fitchette-Lainé, A.C., Loutelier-Bourhis, C., Lange, C., Vine, N.D., Ma, J.K., Lerouge, P., and Faye, L. (1999). N-glycosylation of a mouse IgG expressed in transgenic tobacco plants. Glycobiology 9, 365-372.
8. Chargeleque, D., Vine, N.D., van Dolleweerd, C.J., Drake, P.M.W., and Ma, J.K. (2000). A murine monoclonal antibody produced in transgenic plants with plant-specific glycans is not immunogenic in mice. Transgenic Res. 9, 187-194.
9. Conrad, U., and Fiedler, U. (1998). Compartment-specific accumulation of recombinant immunoglobulins in plant cells: an essential tool for antibody production and immunomodulation of physiological functions and pathogen activity. Plant Mol. Biol. 38, 101-109.
10. Deisenhofer, J. (1981). Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-A resolution. Biochemistry 20, 2361-2370.
11. Dorai, H., Mueller, B.M., Reisfeld, R.A., and Gillies, S.D. (1991). Aglycosylated chimeric mouse/human IgG1 antibody retains some effector function. Hybridoma 10, 211-217.
12. Elbers, I.J., Stoopen, G.M., Bakker, H., Stevens, L.H., Bardor, M., Molthoff, J.W., Jordi, W.J., Bosch, D., and Lommen, A. (2001). Influence of growth conditions and developmental stage on N-glycan heterogeneity of transgenic immunoglobulin G and endogenous proteins in tobacco leaves. Plant Physiol. 126, 1314-1322.
13. Faye, L., Johnson, K.D., and Chrispeels, M.J. (1986a). Oligosaccharide side chains of glycoproteins that remain in the high-mannose form are not accessible to glycosidases. Plant Physiol. 81, 206-211.
14. Faye, L., Sturm, A., Bollini, R., Vitale, A., and Chrispeels, M.J. (1986b). The position of the oligosaccharide side-chains of phytohemaglutinin and their accessibility to glycosidases determines their subsequent processing in the Golgi. Eur. J. Biochem. 158, 655-661.
15. Faye, L., Gomord, V., Fitchette-Lainé, A.C., and Chrispeels, M.J. (1993). Affinity purification of antibodies specific for Asn-linked glycans containing alpha 1 → 3 fucose or beta 1 → 2 xylose, Anal. Biochem. 209, 104-108.
16. Faye, L., Boulaflous, A., Benchabane, M., Gomord, V., and Michaud, D. (2005). Protein modifications in the plant secretory pathway: current status and practical implications in molecular pharming. Vaccine 23, 1770-1778.
17. Fitchette-Lainé, A.C., Gomord, V., Cabanes, M., Michalski, J.C., Saint Macary, M., Foucher, B., Cavelier, B., Hawes, C., Lerouge, P., and Faye, L. (1997). N-glycans harboring the Lewis a epitope are expressed at the surface of plant tells. Plant J. 12, 1411-1417.
18. Fitchette, A.C., Cabanes-Macheteau, M., Marvin, L., Martin, B., Satiat-Jeunemaitre, B., Gomord, V., Crooks, K., Lerouge, P., Faye, L., and Hawes, C. (1999). Biosynthesis and immunolocalization of Lewis a-containing N-glycans in the plant cell. Plant Physiol. 121, 333-344.
19. Freeze, H.H., and Aebi, M. (2005). Altered glycan structures: the molecular basis of congenital disorders of glycosylation. Curr. Opin. Struct. Biol. 15, 490-498.
20. Gomord, V., and Faye, L. (2004). Posttraiislational modification of therapeutic protein in plants. Curr. Opin. Plant Biol. 7, 171-181.
21. Gomord, V., Sourrouille, C., Fitchette, A.C., Bardor, M., Pagny, S., Lerouge, P., and Faye, L. (2004). Production and glycosylation of plant-made pharmaceuticals: the antibodies as a challenge. Plant Biotechnol. J. 2, 83-100.
22. Gomord, V., Chamberlain, P., Jefferis, R., and Faye, L. (2005). Biopharmaceutical production in plants: problems, solutions and opportunities. Trends Biotechnol. 23, 559-565.
23. Helenius, A., and Aebi, M. (2001). Intracellular f1unctions of N- linked glycans. Science 291, 2364-2369.
24. Hiatt, A., Cafferkey, R., and Bowdish, K. (1989). Production of antibodies in transgenic plants. Nature 342, 76-78.
25. Jobling, S.A., Jarman, C., Teh, M.M., Holmberg, N., Blake, C., and Verhoeyen, M.E. (2003). Immunomodulation of enzyme function in plants by single-domain antibody fragments. Nat. Biotechnol. 21, 77-80.
26. Kaneko, M., and Nighorn, A. (2003). Interaxonal Eph-ephrin signaling may mediate sorting of olfactory sensory axons in Manduca sexta. J. Neurosci. 23, 11523-11538.
27. Kanwar, Y.S., Hascall, V.C., JakubowskL, M.L., and Gibbons, J.T. (1984). Effect of beta-D-xyloside on the glomerular proteoglycans. I. Biochemical studies. J. Cell Biol. 99, 715-722.
28. Kelm, S., and Schauer, R. (1997). Sialic acids in molecular and cellular interactions. Int. Rev. Cytol. 175, 137-240.
29. Kim, S.M., Lee, J.S., Lee, Y.H., Kim, W.J., Do, S.I., Choo, Y.K., and Park, Y.I. (2007). Increased α(2,3)-Sialylation and, hyperglycosylation of N-glycans in embryonic rat cortical neurons during Camptothecin-induced apoptosis. Mol. Cells 24, 416-423.
30. Ko, K., and Koprowski, H. (2005). Plant biopharming of monoclonal antibodies. Virus Res. 111, 93-100.
31. Ko, K., Tekoah, Y., Rudd, P.M., Harvey, D.J., Dwek, R.A., Spitsin, S., Hanlon, C.A., Rupprecht, C., Dietzschold, B., Golovkin, M., et al. (2003). Function and glycosylation of plant-derived antiviral monoclonal antibody. Proc. Nall. Acad. Sci. USA 100, 8013-8018.
32. Ko, K., Steplewski, Z., Glogowska, M., and Koprowski, H. (2005). Inhibition of tumor growth by plant-derived mAb. Proc. Natl. Acad. Sci. USA 102, 7026-7030.
33. Koprivova, A., Stemmer, C., Altmann, F., Hoffmann, A., Kopriva, S., Gorr, G., Reski, R., and Decker, E.L. (2004). Targeted knockouts of Physcomitrella lacking plant specific immunogenic N-glycans. Plant Biotech. J. 2, 517-523.
34. Koprowski, H., and Croce, C. (1980). Hybridomas revisited. Science 210, 248.
35. Kurosaka, A., Yano, A., Itoh, N., Kuroda, Y., Nakagawa, T., and Kawasaki, T. (1991). The structure of a neural specific carbohydrate epitope of horseradish peroxidase recognized by antihorseradish peroxidase antiserum. J. Biol. Chem. 266, 4168-4172.
36. Li, L., Yan, J., and Zhao, M.P. (2006). Improvement of the performance of an immunoaffinity extraction method via regionspecific immobilization of IgG J. Chromatogr. A. 1103, 350-355.
37. Ma, J.K., Hikmat, B.Y., Wycoff, K., Vine, N.D., Chargelegue, D., Yu, L., Hein, M.B., and Lehner, T. (1998). Characterization of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. Nat. Med. 4, 601-606.
38. Ma, J.K., Drake, P.M., and Christou, P. (2003). The production of recombinant pharmaceutical proteins in plants. Nat. Rev. Genet. 4, 794-805.
39. Mason, H.S., Lam, D.M., and Arntzen, C.J. (1992). Expression of hepatitis B surface antigen in trnsgenic plants. Proc. Natl. Acad. Sci. USA 89, 11745-11749.
40. Mayfield, S.P., Franklin, S.E., and Lerner, R.A. (2003). Expression and assembly of a fully active antibody in algae. Proc. Natl. Acad. Sci. USA 100, 438-442.
41. Misaki, R., Fujiyama, K., and Seki, T. (2006). Expression of human CMP-N-acetylneuraminic acid synthetase and CMP-sialic acid transporter in tobacco suspension-cultured cell. Biochem. Biophys. Res. Commun. 339, 1184-1189.
42. Niwa, R., Hatanaka, S., Shoji-Hosaka, E., Sakurada, M., Kobayashi, Y., Uehara, A., Yokoi, H., Nakamura, K., and Shitara, K. (2004). Enhancement of the antibody-dependent cellular cytotoxicity of low-fucose IgG1 Is independent of Fcgamma RIIIa functional polymorphism. Clin. Cancer Res. 10, 6248-6255.
43. Okazaki, A., Shoji-Hosaka, E., Nakamura, K., Wakitani, M., Uchida, K., Kakita, S., Tsumoto, K., Kumagai, I., and Shitara, K. (2004). Fucose depletion from human IgG1 oligosaccharide enhances binding enthalpy and association rate between IgG1 and FcgammaRIIIa. J. Mol. Biol. 336, 1239-1249.
44. Paccalet, T., Bardor, M., Rihoucy, C., Delmas, F., Chevalier, C., D'Aoust, M.A., Faye, L., Vézina, L., Gomord, V., and Lerouge, P. (2007). Engineering of a sialic acid synthesis pathway in transgenic plants by expression of bacterial Neu5Ac-synthesizing enzymes. Plant Biotechnol. J. 5, 16-25.
45. Pagny, S., Cabanes-Macheteau, M., Gillikin, J.W., Leborgne-Castel, N., Lerouge, P., Boston, R.S., Faye, L., and Gomord, V. (2000). Protein recycling from the Golgi apparatus to the endoplasmic reticulum in plants and its minor contribution to calreticulin retention. Plant Cell 12, 739-756.
46. Peeters, K., De Wilde, C., and Depicker, A. (2001). Highly efficient targeting and accumulation of a F(ab) fragment within the secretory pathway and apoplast of Arabidopsis thaliana Eur. J. Biochem. 268, 4251-4260.
47. Perlman, S., van den Hazel, B., Christiansen, J., Gram-Nielsen, S., Jeppesen, C.B., Andersen, K.V., Halkier, T., Okkels, S., and Schambye, H.T. (2003). Glycosylation of an N-terminal extension prolongs the half-life and increases the in vivo activity of follicle stimulating hormone. J. Clin. Endocrinol. Metab. 88, 3227-3235.
48. Petruccelli, S., Otegui, M.S., Lareu, F., Tran Dinh, O., Fitchette, A.C., Circosta, A., Rumbo, M., Bardor, M., Carcamo, R., Gomord, V., et al. (2006). A KDEL-tagged monoclonal antibody is efficiently retained in the endoplasmic reticulum in leaves, but is both partially secreted and sorted to protein storage vacuoles in seeds. Plant Biotechnol. J. 4, 511-527.
49. Rayon, C., Cabanes-Macheteau, M., Loutelier-Bourhis, C., Salliot-Maire, I., Lemoine, J., Reiter, W.D., Lerouge, P., and Faye, L. (1999). Characterization of N-glycans from Arabi-dopsis. Application to a fucose-deficient mutant. Plant Physiol. 119, 725-734.
50. Rudd, P.M., Wormald, M.R., and Dwek, R.A. (2004). Sugar-mediated ligand-receptor interactions in the immune system. Trends Biotechnol. 22, 524-530.
51. Schähs, M., Strasser, R., Stadlmann, J., Kunert, R., Rademacher, T., and Steinkellner, H. (2007). Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol. J. 5, 657-663.
52. Schouten, A., Roosien, J., van Engelen, F.A., de Jong, G.A., Borst-Vrenssen, A.W., Zilverentant, J.F., Bosch, D., Stiekema, W.J., Gommers, F.J., Schots, A., et al. (1996). The C-terminal KDEL sequence increases the expression level of a single-chain antibody designed to be targeted to both the cytosol and the secretory pathway in transgenic tobacco. Plant Mol. Biol. 30, 781-793.
53. Séveno, M., Bardor, M., Paccalet, T., Gomord, V., Lerouge, P., Faye, L. (2004). Glycoprotein sialylation in plants? Nat. Biotechnol. 22, 1351-1352.
54. Shah, N., Kuntz, D.A., and Rose, D.R. (2003). Comparison of kifunensine and 1-deoxymannojirimycin binding to class I and II alpha-mannosidases demonstrates different saccharide distortions in inverting and retaining catalytic mechanisms. Biochemistry 42, 13812-13816.
55. Sharp, J.M., and Doran, P.M. (2001). Characterization of monoclonal antibody fragments produced by plant cells. Biotechnol. Bioeng. 73, 338-346.
56. Shields, R.L., Lai, J., Keck, R., O'Connell, L.Y., Hong, K., Meng, Y.G., Weikert, S.H., and Presta, L.G. (2002). Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 277, 26733-26740.
57. Shin, D.J., Kang, J.Y., Kim, Y.U., Yoon, J.S., Choy, H.E., Maeda, Y., Kinoshita, T., and Hong, Y. (2006). Isolation of new CHO cell mutants defective in CMP-Sialic Acid biosynthesis and transport. Mol. Cells 22, 343-352.
58. Shinkawa, T., Nakamura, K., Yamane, N., Shoji-Hosaka, E., Kanda, Y., Sakurada, M., Uchida, K., Anazawa, H., Satoh, M., Yamasaki, M., et al. (2003). The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical iirole of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. 278, 3466-3473.
59. Sriraman, R., Bardor, M., Sack, M., Vaquero, C., Faye, L., Fischer, R., Finnern, R., and Lerouge, P. (2004). Recombinant anti-hCG antibodies retained in the endoplasmic reticulum of transformed plants lack core-xylose and core-alpha(1,3)-fucose residues. Plant Biotechnol. J. 2, 279-287.
60. Tekoah, Y., Ko, K., Koprowski, H., Harvey, D.J., Wormald, M.R., Dwek, R.A., and Rudd, P.M. (2004). Controlled glycosylation of therapeutic antibodies in plants. Arch. Biochem. Biophys. 426, 266-278.
61. Umaña, P., Jean-Mairet, J., and Bailey, J.E. (1999). Tetracycline-regulated overexpression of glycosyltransferases in Chinese hamster ovary cells. Biotechnol. Bioeng. 65, 542-549.
62. van Ree, R., Cabanes-Macheteau, M., Akkerdaas, J., Milazzo, J.P., Loutelier-Bourhis, C., Rayon, C., Villalba, M., Koppelman, S., Aalberse, R., Rodriguez, R., et al. (2000). Beta(1,2)-xylose and alpha(1,3)-fucose residues have a strong contribution in IgE binding to plant glycoallergens. J. Biol. Chem. 275, 11451-11458.
63. 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(1 Pt 1), 133-140.
64. Walker, M.R., Lund, J., Thompson, K.M., and Jefferis, R. (1989). A glycosylation of human IgG1 and IgG3 monoclonal antibodies can eliminate recognition by human cells expressing Fc gamma RI and/or Fc gamma RII receptors. Biochem. J. 259, 347-353.
65. Wee, E.G., Sherrier, D.J., Prime, T.A., and Dupree, P. (1998). Targeting of active sialyltransferase to the plant Golgi apparatus. Plant Cell 10, 1759-1768.
66. Wenderoth, I., and von Schaewen, A. (2000). Isolation and characterization of plant- N-acetyl glucosaminyltransferase I (Gntl) cDNA sequences. Functional analyses in the Arabidopsis cgl mutant and in antisense plants. Plant Physiol. 123, 1097-1108.
67. Werner, R.G., Kopp, K., and Schlueter, M. (2007). Glycosylation of therapeutic proteins in different production systems. Acta Paediatr. Suppl. 96, 17-22.
68. Wide, L. (1986). The regulation of metabolic clearance rate of human FSH in mice by variation of the molecular structure of the hormone. Acta Endocrinologica 112, 519-529.
69. Wright A., and Morrison, S.L. (1997). Effect of glycosylation on antibody function: implications for genetic engineering. Trends Biotechnol. 15, 26-32.
70. Wright, K.E., Prior, F., Sardana, R., Altosaar, I., Dudani, A.K., Ganz, P.R., and Tackaberry, E.S. (2001). Sorting of glycoprotein B from human cytomegalovirus to protein storage vesicles in seeds of transgenic tobacco. Transgenic Res. 10, 177-181.
71. Zeitlin, L., Olmsted, S.S., Moench, T.R., Co, M.S., Martinell, B.J., Paradkar, V.M., Russell, D.R., Queen, C., Cone, R.A., and Whaley, K.J. (1998). A humanized monoclonal antibody produced in transgenic plants for immunoprotection of the vagina against genital herpes. Nat. Biotechnol. 16, 1361-1364.
72. Zeleny, R., Kolarich, D., Strasser, R., and Altmann, F. (2006a). Sialic acid concentrations in plants are in the range of inadvertent contamination. Planta 224, 222-227.
73. Zeleny, R., Leonard, R., Dorfner, G., Dalik, T., Kolarich, D., and Altmann, F. (2006b). Molecular cloning and characterization of a plant alpha1, 3/4-fucosidase based on sequence tags from almond fucosidase I. Phytochemistry 67, 641-648.