Expression of functionally active sialylated human erythropoietin in plants

Biotechnology Journal

Volumn 8, Issue 3, 2013, Pages 371-382

  Jez, Jakub ^a   Castilho, Alexandra ^a   Grass, Josephine ^a   Vorauer Uhl, Karola ^a   Sterovsky, Thomas ^b   Altmann, Friedrich ^a   Steinkellner, Herta ^a  

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

^b Polymun Scientific   (Austria)

Author keywords

Erythropoietin; Glycoengineering; Plants; Purification; Sialylation

Indexed keywords

BIOPHARMACEUTICAL PRODUCTS; CELL-BASED; CO-EXPRESSION; ERYTHROPOIETIN (EPO); EXPRESSION LEVELS; EXPRESSION SYSTEM; GLYCOENGINEERING; GLYCOFORMS; HUMAN ERYTHROPOIETIN; IMMUNOAFFINITY; LECTIN CHROMATOGRAPHY; MAMMALIAN CELLS; MAMMALIAN GENES; N-GLYCANS; NICOTIANA BENTHAMIANA; PLANTS; PRODUCTION OF; RECEPTOR-BINDING ASSAYS; RECOMBINANT HORMONES; RECOMBINANT HUMAN ERYTHROPOIETIN (RHEPO); SIALYLATION;

ANTIGEN-ANTIBODY REACTIONS; BIOACTIVITY; ESTERIFICATION; GLYCOSYLATION; MAMMALS; MEDICAL APPLICATIONS; PLANTS (BOTANY); PURIFICATION;

GENE EXPRESSION;

GLYCAN; PEPTIDE DERIVATIVE; RECOMBINANT ERYTHROPOIETIN; RECOMBINANT HORMONE;

ANEMIA; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; GLYCOSYLATION; IMMUNOAFFINITY CHROMATOGRAPHY; MAMMALIAN GENETICS; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT LEAF; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; RECEPTOR BINDING; SIALYLATION;

CHROMATOGRAPHY, AFFINITY; ERYTHROPOIETIN; HUMANS; PLANTS; RECOMBINANT PROTEINS;

EID: 84874556555     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201200363     Document Type: Article

References (46)

1. Krantz, S. B., Erythropoietin. Blood 1991, 77, 419-434.
2. Jelkmann, W., Erythropoietin: Structure, control of production, and function. Physiol. Rev. 1992, 72, 449-489.
3. Brines, M., Patel, N. S., Villa, P., Brines, C. et al., Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proc. Natl. Acad. Sci. USA 2008, 105, 10925-10930.
4. Chateauvieux, S., Grigorakaki, C., Morceau, F., Dicato, M. et al., Erythropoietin, erythropoiesis and beyond. Biochem. Pharmacol. 2011, 82, 1291-1303.
5. Jacobs, K., Schoemaker, C., Rudersdorf, R., Neill, S. D. et al., Isolation and characterization of genomic and cDNA clones of human erythropoietin. Nature 1985, 313, 806-810.
6. Lin, F. K., Suggs, S., Lin, C. H., Browne, J. K. et al., Cloning and expression of the human erythropoietin gene. Proc. Natl. Acad. Sci. USA 1985, 82, 7580-7584.
7. Thevis, M., Schänzer, W., Emerging drugs-potential for misuse in sport and doping control detection strategies. Mini Rev. Med. Chem. 2007, 7, 531-537.
8. Jelkmann, W., Biosimilar epoetins and other "follow-on" biologics: Update on the European experiences. Am. J. Hematol. 2010, 85, 771-780.
9. Takeuchi, M., Takasaki, S., Miyazaki, H., Kato, T. et al., Comparative study of the asparagine-linked sugar chains of human erythropoietins purified from urine and the culture medium of recombinant Chinese hamster ovary cells. J. Biol. Chem. 1988, 263, 3657-3663.
10. Tsuda, E., Goto, M., Murakami, A., Akai, K. et al., Comparative structural study of N-linked oligosaccharides of urinary and recombinant erythropoietins. Biochemistry 1988, 27, 5646-5654.
11. Hokke, C. H., Bergwerff, A. A., Van Dedem, G. W., Kamerling, J. P. et al., Structural analysis of the sialylated N- and O-linked carbohydrate chains of recombinant human erythropoietin expressed in Chinese hamster ovary cells. Sialylation patterns and branch location of dimeric N-acetyllactosamine units. Eur. J. Biochem. 1995, 228, 981-1008.
12. Egrie, J. C., Browne, J. K., Development and characterization of novel erythropoiesis stimulating protein (NESP). Nephrol. Dial Transplant. 2001, 16, 3-13.
13. Skibeli, V., Nissen-Lie, G., Torjesen, P., Sugar profiling proves that human serum erythropoietin differs from recombinant human erythropoietin. Blood 2001, 98, 3626-3634.
14. Sytkowski, A. J., Feldman, L., Zurbuch, D. J., Biological activity and structural stability of N-deglycosylated recombinant human erythropoietin. Biochem. Biophys. Res. Commun. 1991, 176, 698-704.
15. Takeuchi, M., Inoue, N., Strickland, T. W., Kubota, M. et al., Relationship between sugar chain structure and biological activity of recombinant human erythropoietin produced in Chinese hamster ovary cells. Proc. Natl. Acad. Sci. USA 1989, 86, 7819-7822.
16. Yuen, C. T., Storring, P. L., Tiplady, R. J., Izquierdo, M. et al., Relationships between the N-glycan structures and biological activities of recombinant human erythropoietins produced using different culture conditions and purification procedures. Br. J. Haematol. 2003, 121, 511-526.
17. Bragonzi, A., Distefano, G., Buckberry, L. D., Acerbis, G. et al., A new Chinese hamster ovary cell line expressing alpha 2, 6-sialyltransferase used as universal host for the production of human-like sialylated recombinant glycoproteins. Biochim. Biophys. Acta. 2000, 1474, 273-282.
18. Wang, Z., Park, J. H., Park, H. H., Tan, W. et al., Enhancement of recombinant human EPO production and sialylation in chinese hamster ovary cells through Bombyx mori 30Kc19 gene expression. Biotechnol. Bioeng. 2011, 108, 1634-1642.
19. Loos, A., Steinkellner, H., IgG-Fc glycoengineering in non-mammalian expression hosts. Arch. Biochem. Biophys. 2012, 526, 167-173.
20. Castilho, A., Steinkellner, H., Glyco-engineering in plants towards human like structures. Biotechnol. J. 2012, 7, 1088-1098.
21. Conley, A. J., Mohib, K., Jevnikar, A. M., Brandle, J. E., Plant recombinant erythropoietin attenuates inflammatory kidney cell injury. Plant Biotechnol. J. 2009, 7, 183-199.
22. Musa, T. A., Hung, C. Y., Darlington, D. E., Sane, D. C. et al., Overexpression of human erythropoietin in tobacco does not affect plant fertility or morphology. Plant Biotechnol. Rep. 2009, 3, 157-165.
23. Kittur, F. S., Hung, C. Y., Darlington, D. E., Sane, D. C. et al., N-Glycosylation engineering of tobacco plants to produce asialoerythropoietin. Plant Cell Rep. 2012, 31, 1233-1243.
24. Parsons, J., Altmann, F., Arrenberg, C. K., Koprivova, A. et al., Moss-based production of asialo-erythropoietin devoid of Lewis A and other plant-typical carbohydrate determinants. Plant Biotechnol. J. 2012, 10, 851-861.
25. Weise, A., Altmann, F., Rodriguez-Franco, M., Sjoberg, E. R. et al., High-level expression of secreted complex glycosylated recombinant human erythropoietin in the Physcomitrella Delta-fuc-t Delta-xyl-t mutant. Plant Biotechnol. J. 2007, 5, 389-401.
26. Matsumoto, S., Ikura, K., Ueda, M., Sasaki, R., Characterization of a human glycoprotein (erythropoietin) produced in cultured tobacco cells. Plant Mol. Biol. 1995, 27, 1163-1172.
27. Marillonnet, S., Thoeringer, C., Kandzia, R., Klimyuk, V. et al., Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nat. Biotechnol. 2005, 23, 718-723.
28. Strasser, R., Stadlmann, J., Schähs, M., Stiegler, G. et al., Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol. J. 2008, 6, 392-402.
29. Castilho, A., Strasser, R., Stadlmann, J., Grass, J. et al., In planta protein sialylation through overexpression of the respective mammalian pathway. J. Biol. Chem. 2010, 285, 15923-15930.
30. Strasser, R., Castilho, A., Stadlmann, J., Kunert, R. et al., Improved virus neutralization by plant-produced anti-HIV antibodies with a homogeneous beta1, 4-galactosylated N-glycan profile. J. Biol. Chem. 2009, 284, 20479-20485.
31. Marchetti-Deschmann, M., Kemptner, J., Reichel, C., Allmaier, G., Comparing standard and microwave assisted staining protocols for SDS-PAGE of glycoproteins followed by subsequent PMF with MALDI MS. J. Proteomics 2009, 72, 628-639.
32. Stadlmann, J., Pabst, M., Kolarich, D., Kunert, R. et al., Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 2008, 8, 2858-2871.
33. Komatsu, N., Nakauchi, H., Miwa, A., Ishihara, T. et al., Establishment and characterization of a human leukemic cell line with megakaryocytic features: Dependency on granulocyte-macrophage colony-stimulating factor, interleukin 3, or erythropoietin for growth and survival. Cancer Res. 1991, 51, 341-348.
34. Muster, T., Steindl, F., Purtscher, M., Trkola, A. et al., A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 1993, 67, 6642-6647.
35. Castilho, A., Gattinger, P., Grass, J., Jez, J. et al., N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology 2011, 21, 813-823.
36. Nagels, B., Van Damme, E. J., Callewaert, N., Zabeau, L. et al., Biologically active, magnICON® expressed EPO-Fc from stably transformed Nicotiana benthamiana plants presenting tetra-antennary N-glycan structures. J. Biotechnol. 2012, 160, 242-250.
37. Conley, A. J., Zhum, H., Le, L. C., Jevnikar, A. M. et al., Recombinant protein production in a variety of Nicotiana hosts: A comparative analysis. Plant Biotechnol. J. 2011, 9, 434-444.
38. Giritch, A., Marillonnet, S., Engler, C., van Eldik, G. et al., Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 14701-14706.
39. Castilho, A., Bohorova, N., Grass, J., Bohorov, O. et al., Rapid high yield production of different glycoforms of ebola virus monoclonal antibody. PLoS One 2011, 6, e26040.
40. Bendandi, M., Marillonnet, S., Kandzia, R., Thieme, F. et al., Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin's lymphoma. Ann. Oncol. 2010, 21, 2420-2427.
41. Pogue, G. P., Vojdani, F., Palmer, K. E., Hiatt, E. et al., Production of pharmaceutical-grade recombinant aprotinin and a monoclonal antibody product using plant-based transient expression systems. Plant Biotechnol. J. 2010, 8, 638-654.
42. Loos, A., Van Droogenbroeck, B., Hillmer, S., Grass, J. et al., Expression of antibody fragments with a controlled N-glycosylation pattern and induction of endoplasmic reticulum-derived vesicles in seeds of Arabidopsis. Plant Physiol. 2011, 155, 2036-2048.
43. Loos, A., Van Droogenbroeck, B., Hillmer, S., Grass, J. et al., Production of monoclonal antibodies with a controlled N-glycosylation pattern in seeds of Arabidopsis thaliana. Plant Biotechnol. J. 2011, 9, 179-192.
44. Kunert, R., Steinfellner, W., Purtscher, M., Assadian, A. et al., Stable recombinant expression of the anti HIV-1 monoclonal antibody 2F5 after IgG3/IgG1 subclass switch in CHO cells. Biotechnol. Bioeng. 2000, 67, 97-103.
45. Reisinger, H., Steinfellner, W., Stern, B., Katinger, H. et al., The absence of effect of gene copy number and mRNA level on the amount of mAb secretion from mammalian cells. Appl. Microbiol. Biotechnol. 2008, 81, 701-710.
46. Darling, R. J., Kuchibhotla, U., Glaesner, W., Micanovic, R. et al., Glycosylation of erythropoietin affects receptor binding kinetics: Role of electrostatic interactions. Biochemistry 2002, 41, 14524-14531.