Oligomerization status influences subcellular deposition and glycosylation of recombinant butyrylcholinesterase in Nicotiana benthamiana

Plant Biotechnology Journal

Volumn 12, Issue 7, 2014, Pages 832-839

  Schneider, Jeannine D ^a   Marillonnet, Sylvestre ^b   Castilho, Alexandra ^a   Gruber, Clemens ^a   Werner, Stefan ^b   Mach, Lukas ^a   Klimyuk, Victor ^b   Mor, Tsafrir S ^c   Steinkellner, Herta ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b Icon Genetics GmbH   (Germany)

^c Arizona State University   (United States)

Author keywords

Butyrylcholinesterase; Glycoengineering; Plants; Sialic acid; Subcellular targeting

Indexed keywords

MAMMALIA; NICOTIANA BENTHAMIANA;

CHOLINESTERASE; RECOMBINANT PROTEIN;

GENE VECTOR; GENETICS; GLYCOSYLATION; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN ENGINEERING; PROTEIN PROCESSING; PROTEIN TRANSPORT; TOBACCO; TRANSGENIC PLANT;

BUTYRYLCHOLINESTERASE; GENETIC VECTORS; GLYCOSYLATION; HUMANS; PLANTS, GENETICALLY MODIFIED; PROTEIN ENGINEERING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; TOBACCO;

EID: 84906270407     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12184     Document Type: Article

References (54)

1. 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.
2. Bakker, H., Bardor, M., Molthoff, J.W., Gomord, V., Elbers, I., Stevens, L.H., Jordi, W., Lommen, A., Faye, L., Lerouge, P. and Bosch, D. (2001) Galactose-extended glycans of antibodies produced by transgenic plants. Proc. Natl. Acad. Sci. USA, 98, 2899-2904.
3. Biberoglu, K., Schopfer, L.M., Tacal, O. and Lockridge, O. (2012) The proline-rich tetramerization peptides in equine serum butyrylcholinesterase. FEBS J. 279, 3844-3858.
4. Bock, R. (2013) Strategies for metabolic pathway engineering with multiple transgenes. Plant Mol. Biol. 83, 21-31.
5. 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.
6. Both, L., van Dolleweerd, C., Wright, E., Banyard, A.C., Bulmer-Thomas, B., Selden, D., Altmann, F., Fooks, A.R. and Ma, J.K.-C. (2013) Production, characterization, and antigen specificity of recombinant 62-71-3, a candidate monoclonal antibody for rabies prophylaxis in humans. FASEB J. 27, 2055-2065.
7. Brandizzi, F. and Barlowe, C. (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat. Rev. Mol. Cell Biol. 14, 382-392.
8. Castilho, A. and Steinkellner, H. (2012) Glyco-engineering in plants to produce human-like N-glycan structures. Biotechnol. J. 7, 1088-1098.
9. Castilho, A., Pabst, M., Leonard, R., Veit, C., Altmann, F., Mach, L., Gloessl, J., Strasser, R. and Steinkellner, H. (2008) Construction of a functional CMP-sialic acid biosynthesis pathway in Arabidopsis. Plant Physiol. 147, 331-339.
10. Castilho, A., Strasser, R., Stadlmann, J., Grass, J., Jez, J., Gattinger, P., Kunert, R., Quendler, H., Pabst, M., Leonard, R., Altmann, F. and Steinkellner, H. (2010) In planta protein sialylation through overexpression of the respective mammalian pathway. J. Biol. Chem. 285, 15923-15930.
11. Castilho, A., Gattinger, P., Grass, J., Jez, J., Pabst, M., Altmann, F., Gorfer, M., Strasser, R. and Steinkellner, H. (2011) N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology, 21, 813-823.
12. Castilho, A., Neumann, L., Daskalova, S., Mason, H.S., Steinkellner, H., Altmann, F. and Strasser, R. (2012) Engineering of sialylated mucin-type O-Glycosylation in plants. J. Biol. Chem. 287, 36518-36526.
13. Castilho, A., Neumann, L., Gattinger, P., Strasser, R., Vorauer-Uhl, K., Sterovsky, T., Altmann, F. and Steinkellner, H. (2013) Generation of biologically active multi-sialylated recombinant human EPOFc in plants. PLoS ONE, 8, e54836.
14. Cox, K.M., Sterling, J.D., Regan, J.T., Gasdaska, J.R., Frantz, K.K., Peele, C.G., Black, A., Passmore, D., Moldovan-Loomis, C., Srinivasan, M., Cuison, S., Cardarelli, P.M. and Dickey, L.F. (2006) Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat. Biotechnol. 24, 1591-1597.
15. Denecke, J., Aniento, F., Frigerio, L., Hawes, C., Hwang, I., Mathur, J., Neuhaus, J.-M. and Robinson, D.G. (2012) Secretory pathway research: the more experimental systems the better. Plant Cell, 24, 1316-1326.
16. Engler, C. and Marillonnet, S. (2013) Combinatorial DNA Assembly using Golden Gate Cloning. In: Methods Mol. Biol., Vol. 1073 (Polizzi, K.M. and Kontoravdi, C., eds), pp. 141-156. New York, NY: Humana Press.
17. Farid, A., Pabst, M., Schoberer, J., Altmann, F., Glossl, J. and Strasser, R. (2011) Arabidopsis thaliana alpha1, 2-glucosyltransferase (ALG10) is required for efficient N-glycosylation and leaf growth. Plant J. 68, 314-325.
18. Feige, M.J., Groscurth, S., Marcinowski, M., Shimizu, Y., Kessler, H., Hendershot, L.M. and Buchner, J. (2009) An unfolded CH1 domain controls the assembly and secretion of IgG antibodies. Mol. Cell, 34, 569-579.
19. Feige, M.J., Hendershot, L.M. and Buchner, J. (2010) How antibodies fold. Trends Biochem. Sci. 35, 189-198.
20. Geyer, B.C., Kannan, L., Cherni, I., Woods, R.R., Soreq, H. and Mor, T.S. (2010a) Transgenic plants as a source for the bioscavenging enzyme, human butyrylcholinesterase. Plant Biotechnol. J. 8, 873-886.
21. Geyer, B.C., Kannan, L., Garnaud, P.E., Broomfield, C.A., Cadieux, C.L., Cherni, I., Hodgins, S.M., Kasten, S.A., Kelley, K., Kilbourne, J., Oliver, Z.P., Otto, T.C., Puffenberger, I., Reeves, T.E., Robbins, N. 2nd, Woods, R.R., Soreq, H., Lenz, D.E., Cerasoli, D.M. and Mor, T.S. (2010b) Plant-derived human butyrylcholinesterase, but not an organophosphorous-compound hydrolyzing variant thereof, protects rodents against nerve agents. Proc. Natl. Acad. Sci. USA, 107, 20251-20256.
22. Hossler, P., Khattak, S.F. and Li, Z.J. (2009) Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology, 19, 936-949.
23. Huang, Y.J., Huang, Y., Baldassarre, H., Wang, B., Lazaris, A., Leduc, M., Bilodeau, A.S., Bellemare, A., Cote, M., Herskovits, P., Touati, M., Turcotte, C., Valeanu, L., Lemee, N., Wilgus, H., Begin, I., Bhatia, B., Rao, K., Neveu, N., Brochu, E., Pierson, J., Hockley, D.K., Cerasoli, D.M., Lenz, D.E., Karatzas, C.N. and Langermann, S. (2007) Recombinant human butyrylcholinesterase from milk of transgenic animals to protect against organophosphate poisoning. Proc. Natl. Acad. Sci. USA, 104, 13603-13608.
24. Ilyushin, D.G., Smirnov, I.V., Belogurov, A.A. Jr, Dyachenko, I.A., Zharmukhamedova, T., Novozhilova, T.I., Bychikhin, E.A., Serebryakova, M.V., Kharybin, O.N., Murashev, A.N., Anikienko, K.A., Nikolaev, E.N., Ponomarenko, N.A., Genkin, D.D., Blackburn, G.M., Masson, P. and Gabibov, A.G. (2013) Chemical polysialylation of human recombinant butyrylcholinesterase delivers a long-acting bioscavenger for nerve agents in vivo. Proc. Natl. Acad. Sci. USA, 110, 1243-1248.
25. Klimyuk, V., Pogue, G., Herz, S., Butler, J. and Haydon, H. (2012) Production of Recombinant Antigens and Antibodies in Nicotiana Benthamiana Using 'Magnifection' Technology: GMP-Compliant Facilities for Small- and Large-Scale Manufacturing. In: Curr. Top. Microbiol. Immunol., Vol. 375 (Palmer, K.E. and Gleba, Y., eds), pp. 1-28. Heidelberg: Springer Berlin.
26. Kolarich, D., Weber, A., Pabst, M., Stadlmann, J., Teschner, W., Ehrlich, H., Schwarz, H.P. and Altmann, F. (2008) Glycoproteomic characterization of butyrylcholinesterase from human plasma. Proteomics, 8, 254-263.
27. Li, H., Schopfer, L.M., Masson, P. and Lockridge, O. (2008) Lamellipodin proline rich peptides associated with native plasma butyrylcholinesterase tetramers. Biochem. J. 411, 425-432.
28. Liu, J.-X. and Howell, S.H. (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell, 22, 2930-2942.
29. Loos, A. and Steinkellner, H. (2012) IgG-Fc glycoengineering in non-mammalian expression hosts. Arch. Biochem. Biophys. 526, 167-173.
30. Loos, A., Van Droogenbroeck, B., Hillmer, S., Grass, J., Kunert, R., Cao, J., Robinson, D.G., Depicker, A. and Steinkellner, H. (2011a) Production of monoclonal antibodies with a controlled N-glycosylation pattern in seeds of Arabidopsis thaliana. Plant Biotechnol. J. 9, 179-192.
31. Loos, A., Van Droogenbroeck, B., Hillmer, S., Grass, J., Pabst, M., Castilho, A., Kunert, R., Liang, M., Arcalis, E., Robinson, D.G., Depicker, A. and Steinkellner, H. (2011b) Expression of antibody fragments with a controlled N-Glycosylation pattern and induction of endoplasmic reticulum-derived vesicles in seeds of Arabidopsis. Plant Physiol. 155, 2036-2048.
32. Marillonnet, S., Giritch, A., Gils, M., Kandzia, R., Klimyuk, V. and Gleba, Y. (2004) In planta engineering of viral RNA replicons: efficient assembly by recombination of DNA modules delivered by Agrobacterium. Proc. Natl. Acad. Sci. USA, 101, 6852-6857.
33. 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.
34. Melnik, S. and Stoger, E. (2013) Green factories for biopharmaceuticals. Curr. Med. Chem. 20, 1038-1046.
35. Miller, E.A. and Schekman, R. (2013) COPII - a flexible vesicle formation system. Curr. Opin. Cell Biol. 25, 420-427.
36. Nuttall, J., Vine, N., Hadlington, J.L., Drake, P., Frigerio, L. and Ma, J.K.C. (2002) ER-resident chaperone interactions with recombinant antibodies in transgenic plants. Eur. J. Biochem. 269, 6042-6051.
37. Pabst, M., Chang, M., Stadlmann, J. and Altmann, F. (2012) Glycan profiles of the 27 N-glycosylation sites of the HIV envelope protein CN54gp140. Biol. Chem. 393, 719-730.
38. Palacpac, N.Q., Yoshida, S., Sakai, H., Kimura, Y., Fujiyama, K., Yoshida, T. and Seki, T. (1999) Stable expression of human β1, 4-galactosyltransferase in plant cells modifies N-linked glycosylation patterns. Proc. Natl. Acad. Sci. USA, 96, 4692-4697.
39. Rademacher, T., Sack, M., Arcalis, E., Stadlmann, J., Balzer, S., Altmann, F., Quendler, H., Stiegler, G., Kunert, R., Fischer, R. and Stoger, E. (2008) Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnol. J. 6, 189-201.
40. Rosenberg, Y.J., Saxena, A., Sun, W., Jiang, X., Chilukuri, N., Luo, C., Doctor, B.P. and Lee, K.D. (2010) Demonstration of in vivo stability and lack of immunogenicity of a polyethyleneglycol-conjugated recombinant CHO-derived butyrylcholinesterase bioscavenger using a homologous macaque model. Chem. Biol. Interact. 187, 279-286.
41. Saxena, A., Ashani, Y., Raveh, L., Stevenson, D., Patel, T. and Doctor, B.P. (1998) Role of oligosaccharides in the pharmacokinetics of tissue-derived and genetically engineered cholinesterases. Mol. Pharmacol. 53, 112-122.
42. Schillberg, S., Raven, N., Fischer, R., Twyman, R.M. and Schiermeyer, A. (2013) Molecular farming of pharmaceutical proteins using plant suspension cell and tissue cultures. Curr. Pharm. Des. 19, 5531-5542.
43. Schoberer, J., Vavra, U., Stadlmann, J., Hawes, C., Mach, L., Steinkellner, H. and Strasser, R. (2009) Arginine/lysine residues in the cytoplasmic tail promote ER export of plant glycosylation enzymes. Traffic, 10, 101-115.
44. 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.
45. Stadlmann, J., Pabst, M., Kolarich, D., Kunert, R. and Altmann, F. (2008) Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics, 8, 2858-2871.
46. Strasser, R., Stadlmann, J., Schahs, M., Stiegler, G., Quendler, H., Mach, L., Glossl, J., Weterings, K., Pabst, M. and Steinkellner, H. (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.
47. Strasser, R., Castilho, A., Stadlmann, J., Kunert, R., Quendler, H., Gattinger, P., Jez, J., Rademacher, T., Altmann, F., Mach, L. and Steinkellner, H. (2009) Improved virus neutralization by plant-produced Anti-HIV Antibodies with a homogeneous β1, 4-Galactosylated N-Glycan profile. J. Biol. Chem. 284, 20479-20485.
48. Taschwer, M., Hackl, M., Hernández Bort, J.A., Leitner, C., Kumar, N., Puc, U., Grass, J., Papst, M., Kunert, R., Altmann, F. and Borth, N. (2012) Growth, productivity and protein glycosylation in a CHO EpoFc producer cell line adapted to glutamine-free growth. J. Biotechnol. 157, 295-303.
49. Trummer, E., Fauland, K., Seidinger, S., Schriebl, K., Lattenmayer, C., Kunert, R., Vorauer-Uhl, K., Weik, R., Borth, N., Katinger, H. and Müller, D. (2006) Process parameter shifting: Part II. Biphasic cultivation-A tool for enhancing the volumetric productivity of batch processes using Epo-Fc expressing CHO cells. Biotechnol. Bioeng. 94, 1045-1052.
50. Van Patten, S.M., Hughes, H., Huff, M.R., Piepenhagen, P.A., Waire, J., Qiu, H., Ganesa, C., Reczek, D., Ward, P.V., Kutzko, J.P. and Edmunds, T. (2007) Effect of mannose chain length on targeting of glucocerebrosidase for enzyme replacement therapy of Gaucher disease. Glycobiology, 17, 467-478.
51. Weber, A., Butterweck, H., Mais-Paul, U., Teschner, W., Lei, L., Muchitsch, E.M., Kolarich, D., Altmann, F., Ehrlich, H.J. and Schwarz, H.P. (2011a) Biochemical, molecular and preclinical characterization of a double-virus-reduced human butyrylcholinesterase preparation designed for clinical use. Vox Sang. 100, 285-297.
52. Weber, E., Engler, C., Gruetzner, R., Werner, S. and Marillonnet, S. (2011b) A modular cloning system for standardized assembly of multigene constructs. PLoS ONE, 6, e16765.
53. Werner, S., Engler, C., Weber, E., Gruetzner, R. and Marillonnet, S. (2012) Fast track assembly of multigene constructs using Golden Gate cloning and the MoClo system. Bioeng. Bugs, 3, 38-43.
54. Wolfson, W. (2013) Grow your own: Protalix BioTherapeutics produces drugs in carrot cells. Chem. Biol. 20, 969-970.