Reduced paucimannosidic N-glycan formation by suppression of a specific β-hexosaminidase from Nicotiana benthamiana

Plant Biotechnology Journal

Volumn 15, Issue 2, 2017, Pages 197-206

  Shin, Yun Ji ^a   Castilho, Alexandra ^a   Dicker, Martina ^a   Sádio, Flavio ^a   Vavra, Ulrike ^a   Grünwald Gruber, Clemens ^a   Kwon, Tae Ho ^b   Altmann, Friedrich ^a   Steinkellner, Herta ^a   Strasser, Richard ^a  

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

^b NBM Inc   (South Korea)

Author keywords

glyco engineering; N glycosylation; Nicotiana benthamiana; plant made pharmaceuticals; 1 antitrypsin

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; PLANT PROTEIN; POLYSACCHARIDE; RECOMBINANT PROTEIN;

ANTAGONISTS AND INHIBITORS; ARABIDOPSIS; BIOSYNTHESIS; CELL MEMBRANE; CELL VACUOLE; ENZYMOLOGY; GENETICS; GLYCOSYLATION; METABOLISM; NUCLEOTIDE SEQUENCE; PLANT GENE; PLANT LEAF; TOBACCO; TRANSGENIC PLANT;

ARABIDOPSIS; BASE SEQUENCE; BETA-N-ACETYLHEXOSAMINIDASES; CELL MEMBRANE; GENES, PLANT; GLYCOSYLATION; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES; RECOMBINANT PROTEINS; TOBACCO; VACUOLES;

EID: 84981541252     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12602     Document Type: Article

References (43)

1. Altmann, F., Schwihla, H., Staudacher, E., Glössl, J. and März, L. (1995) Insect cells contain an unusual, membrane-bound beta-N-acetylglucosaminidase probably involved in the processing of protein N-glycans. J. Biol. Chem. 270, 17344–17349.
2. Castilho, A., Gattinger, P., Grass, J., Jez, J., Pabst, M., Altmann, F., Gorfer, M. et al. (2011) N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology, 21, 813–823.
3. Castilho, A., Windwarder, M., Gattinger, P., Mach, L., Strasser, R., Altmann, F. and Steinkellner, H. (2014) Proteolytic and N-glycan processing of human α1-antitrypsin expressed in Nicotiana benthamiana. Plant Physiol. 166, 1839–1851.
4. Castilho, A., Gruber, C., Thader, A., Oostenbrink, C., Pechlaner, M., Steinkellner, H. and Altmann, F. (2015) Processing of complex N-glycans in IgG Fc-region is affected by core fucosylation. MAbs, 7, 863–870.
5. Dicker, M., Tschofen, M., Maresch, D., König, J., Juarez, P., Orzaez, D., Altmann, F. et al. (2016) Transient glyco-engineering to produce recombinant IgA1 with defined N- and O-glycans in plants. Front. Plant Sci. 7, 18.
6. Dirnberger, D., Steinkellner, H., Abdennebi, L., Remy, J. and van de Wiel, D. (2001) Secretion of biologically active glycoforms of bovine follicle stimulating hormone in plants. Eur. J. Biochem. 268, 4570–4579.
7. Grabowski, G.A., Barton, N.W., Pastores, G., Dambrosia, J.M., Banerjee, T.K., McKee, M.A., Parker, C. et al. (1995) Enzyme therapy in type 1 Gaucher disease: comparative efficacy of mannose-terminated glucocerebrosidase from natural and recombinant sources. Ann. Intern. Med. 122, 33–39.
8. 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.
9. Humair, D., Hernández Felipe, D., Neuhaus, J. and Paris, N. (2001) Demonstration in yeast of the function of BP-80, a putative plant vacuolar sorting receptor. Plant Cell, 13, 781–792.
10. Hüttner, S., Veit, C., Vavra, U., Schoberer, J., Liebminger, E., Maresch, D., Grass, J. et al. (2014) Arabidopsis class I α-mannosidases MNS4 and MNS5 are involved in endoplasmic reticulum-associated degradation of misfolded glycoproteins. Plant Cell, 26, 1712–1728.
11. Jez, J., Castilho, A., Grass, J., Vorauer-Uhl, K., Sterovsky, T., Altmann, F. and Steinkellner, H. (2013) Expression of functionally active sialylated human erythropoietin in plants. Biotechnol. J. 8, 371–382.
12. Kurup, S., Runions, J., Köhler, U., Laplaze, L., Hodge, S. and Haseloff, J. (2005) Marking cell lineages in living tissues. Plant J. 42, 444–453.
13. Léonard, R., Rendic, D., Rabouille, C., Wilson, I., Préat, T. and Altmann, F. (2006) The Drosophila fused lobes gene encodes an N-acetylglucosaminidase involved in N-glycan processing. J. Biol. Chem. 281, 4867–4875.
14. Liebminger, E., Veit, C., Pabst, M., 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.
15. Limkul, J., Iizuka, S., Sato, Y., Misaki, R., Ohashi, T. and Fujiyama, K. (2016) The production of human glucocerebrosidase in glyco-engineered Nicotiana benthamiana plants. Plant Biotechnol. J. 14, 1682–1694.
16. Loos, A., Gruber, C., Altmann, F., Mehofer, U., Hensel, F., Grandits, M., Oostenbrink, C. et al. (2014) Expression and glycoengineering of functionally active heteromultimeric IgM in plants. Proc. Natl. Acad. Sci. USA, 111, 6263–6268.
17. Loos, A., Gach, J.S., Hackl, T., Maresch, D., Henkel, T., Porodko, A., Bui-Minh, D. et al. (2015) Glycan modulation and sulfoengineering of anti-HIV-1 monoclonal antibody PG9 in plants. Proc. Natl. Acad. Sci. USA, 112, 12675–12680.
18. Qiu, X., Wong, G., Audet, J., Bello, A., Fernando, L., Alimonti, J.B., Fausther-Bovendo, H. et al. (2014) Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature, 514, 47–53.
19. Reusch, D. and Tejada, M.L. (2015) Fc glycans of therapeutic antibodies as critical quality attributes. Glycobiology, 25, 1325–1334.
20. Samyn-Petit, B., Wajda Dubos, J.P., Chirat, F., Coddeville, B., Demaizieres, G., Farrer, S., Slomianny, M.C. et al. (2003) Comparative analysis of the site-specific N-glycosylation of human lactoferrin produced in maize and tobacco plants. Eur. J. Biochem. 270, 3235–3242.
21. Schachter, H. (2009) Paucimannose N-glycans in Caenorhabditis elegans and Drosophila melanogaster. Carbohydr. Res. 344, 1391–1396.
22. Schneider, J.D., Castilho, A., Neumann, L., Altmann, F., Loos, A., Kannan, L., Mor, T.S. et al. (2014) Expression of human butyrylcholinesterase with an engineered glycosylation profile resembling the plasma-derived orthologue. Biotechnol. J. 9, 501–510.
23. 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.
24. Schoberer, J., Liebminger, E., Botchway, S.W., Strasser, R. and Hawes, C. (2013) Time-resolved fluorescence imaging reveals differential interactions of N-glycan processing enzymes across the Golgi stack in planta. Plant Physiol. 161, 1737–1754.
25. Schoberer, J., Liebminger, E., Vavra, U., Veit, C., Castilho, A., Dicker, M., Maresch, D. et al. (2014) The transmembrane domain of N-acetylglucosaminyltransferase I is the key determinant for its Golgi subcompartmentation. Plant J. 80, 809–822.
26. Sethi, M.K., Kim, H., Park, C.K., Baker, M.S., Paik, Y.K., Packer, N.H., Hancock, W.S. et al. (2015) In-depth N-glycome profiling of paired colorectal cancer and non-tumorigenic tissues reveals cancer-, stage- and EGFR-specific protein N-glycosylation. Glycobiology, 25, 1064–1078.
27. Shaaltiel, Y., Bartfeld, 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.
28. Shen, J.S., Busch, A., Day, T.S., Meng, X.L., Yu, C.I., Dabrowska-Schlepp, P., Fode, B. et al. (2016) Mannose receptor-mediated delivery of moss-made α-galactosidase A efficiently corrects enzyme deficiency in Fabry mice. J. Inherit. Metab. Dis. 39, 293–303.
29. 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.
30. Steinkellner, H. and Castilho, A. (2015) N-glyco-engineering in plants: update on strategies and major achievements. Methods Mol. Biol. 1321, 195–212.
31. Stoger, E., Fischer, R., Moloney, M. and Ma, J.K. (2014) Plant molecular pharming for the treatment of chronic and infectious diseases. Annu. Rev. Plant Biol. 65, 743–768.
32. Strasser, R. (2016) Plant protein glycosylation. Glycobiology, doi:10.1093/glycob/cww023
33. Strasser, R., Mucha, J., Schwihla, H., Altmann, F., Glössl, J. and Steinkellner, H. (1999) Molecular cloning and characterization of cDNA coding for beta1,2N-acetylglucosaminyltransferase I (GlcNAc-TI) from Nicotiana tabacum. Glycobiology, 9, 779–785.
34. Strasser, R., Altmann, F., Mach, L., Glössl, J. and Steinkellner, H. (2004) Generation of Arabidopsis thaliana plants with complex N-glycans lacking beta1,2-linked xylose and core alpha1,3-linked fucose. FEBS Lett. 561, 132–136.
35. Strasser, R., Bondili, J., 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.
36. 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.
37. Strasser, R., Castilho, A., Stadlmann, J., Kunert, R., Quendler, H., Gattinger, P., Jez, J. et al. (2009) Improved virus neutralization by plant-produced anti-HIV antibodies with a homogeneous ,4-galactosylated N-glycan profile. J. Biol. Chem. 284, 20479–20485.
38. Strasser, R., Altmann, F. and Steinkellner, H. (2014) Controlled glycosylation of plant-produced recombinant proteins. Curr. Opin. Biotechnol. 30C, 95–100.
39. 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.
40. Wilbers, R.H., Westerhof, L.B., Reuter, L.J., Castilho, A., van Raaij, D.R., Nguyen, D.L., Lozano-Torres, J.L. et al. (2016) The N-glycan on Asn54 affects the atypical N-glycan composition of plant-produced interleukin-22, but does not influence its activity. Plant Biotechnol. J. 14, 670–681.
41. Yang, Z., Wang, S., Halim, A., Schulz, M.A., Frodin, M., Rahman, S.H., Vester-Christensen, M.B. et al. (2015a) Engineered CHO cells for production of diverse, homogeneous glycoproteins. Nat. Biotechnol. 33, 842–844.
42. Yang, W.H., Aziz, P.V., Heithoff, D.M., Mahan, M.J., Smith, J.W. and Marth, J.D. (2015b) An intrinsic mechanism of secreted protein aging and turnover. Proc. Natl. Acad. Sci. USA, 112, 13657–13662.
43. Zeitlin, L., Geisbert, J.B., Deer, D.J., Fenton, K.A., Bohorov, O., Bohorova, N., Goodman, C. et al. (2016) Monoclonal antibody therapy for Junin virus infection. Proc. Natl. Acad. Sci. USA, 113, 4458–4463.