Plant species and organ influence the structure and subcellular localization of recombinant glycoproteins

Plant Molecular Biology

Volumn 83, Issue 1-2, 2013, Pages 105-117

  Arcalis, Elsa ^a   Stadlmann, Johannes ^a   Rademacher, Thomas ^b   Marcel, Sylvain ^c   Sack, Markus ^d   Altmann, Friedrich ^a   Stoger, Eva ^a  

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

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^c Caliber Biotherapeutics   (United States)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Glycoprotein production; Molecular farming; Plant made pharmaceuticals; Protein trafficking; Subcellular deposition

Indexed keywords

2G12 MONOCLONAL ANTIBODY; FUNGAL PROTEIN; GLYCOPROTEIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MONOCLONAL ANTIBODY; PHYTASE; POLYSACCHARIDE; RECOMBINANT PROTEIN;

ARABIDOPSIS; ARTICLE; ASPERGILLUS NIGER; GENETICS; GLYCOSYLATION; METABOLISM; PLANT LEAF; PLANT SEED; PROTEIN STABILITY; PROTEIN TRANSPORT; SPECIES DIFFERENCE; TOBACCO; TRANSGENIC PLANT;

6-PHYTASE; ANTIBODIES, MONOCLONAL; ARABIDOPSIS; ASPERGILLUS NIGER; FUNGAL PROTEINS; GLYCOPROTEINS; GLYCOSYLATION; HIV ANTIBODIES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES; PROTEIN STABILITY; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SEEDS; SPECIES SPECIFICITY; TOBACCO;

ARABIDOPSIS; ASPERGILLUS NIGER; HUMAN IMMUNODEFICIENCY VIRUS; NICOTIANA TABACUM;

EID: 84883241122     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0049-9     Document Type: Article

References (60)

1. Abranches R, Marcel S, Arcalis E, Altmann F, Fevereiro P, Stoger E (2005) Plants as bioreactors: a comparative study suggests that Medicago truncatula is a promising production system. J Biotechnol 120(1): 121-134. doi: 10. 1016/j. jbiotec. 2005. 04. 026.
2. Abranches R, Arcalis E, Marcel S, Altmann F, Ribeiro-Pedro M, Rodriguez J, Stoger E (2008) Functional specialization of Medicago truncatula leaves and seeds does not affect the subcellular localization of a recombinant protein. Planta 227(3): 649-658. doi: 10. 1007/s00425-007-0647-3.
3. Arcalis E, Marcel S, Altmann F, Kolarich D, Drakakaki G, Fischer R, Christou P, Stoger E (2004) Unexpected deposition patterns of recombinant proteins in post-endoplasmic reticulum compartments of wheat endosperm. Plant Physiol 136(3): 3457-3466. doi: 10. 1104/pp. 104. 050153.
4. Arcalis E, Stadlmann J, Marcel S, Drakakaki G, Winter V, Rodriguez J, Fischer R, Altmann F, Stoger E (2010) The changing fate of a secretory glycoprotein in developing maize endosperm. Plant Physiol 153(2): 693-702. doi: 10. 1104/pp. 109. 152363.
5. Brinch-Pedersen H, Hatzack F, Stoger E, Arcalis E, Pontopidan K, Holm PB (2006) Heat-stable phytases in transgenic wheat (Triticum aestivum L.): deposition pattern, thermostability, and phytate hydrolysis. J Agric Food Chem 54(13): 4624-4632. doi: 10. 1021/jf0600152.
6. Brown RC, Lemmon BE (2007) The developmental biology of cereal endosperm. Plant Cell Monogr 8: 1-20.
7. Castilho A, Strasser R, Stadlmann J, Grass J, Jez J, Gattinger P, Kunert R, Quendler H, Pabst M, Leonard R, Altmann F, Steinkellner H (2010) In planta protein sialylation through overexpression of the respective mammalian pathway. J Biol Chem 285(21): 15923-15930. doi: 10. 1074/jbc. M109. 088401.
8. Chen F, Bradford KJ (2000) Expression of an expansion is associated with endosperm weakening during tomato seed germination. Plant Physiol 124(3): 1265-1274.
9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6): 735-743.
10. Denecke J, Botterman J, Deblaere R (1990) Protein secretion in plant cells can occur via a default pathway. Plant cell 2(1): 51-59. doi: 10. 1105/tpc. 2. 1. 51.
11. Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol 59(6): 869-880. doi: 10. 1007/s11103-005-1537-3.
12. Drakakaki G, Marcel S, Arcalis E, Altmann F, Gonzalez-Melendi P, Fischer R, Christou P, Stoger E (2006) The intracellular fate of a recombinant protein is tissue dependent. Plant Physiol 141(2): 578-586. doi: 10. 1104/pp. 106. 076661.
13. Elbers IJ, Stoopen GM, Bakker H, Stevens LH, Bardor M, Molthoff JW, Jordi WJ, Bosch D, 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(3): 1314-1322.
14. FDA (2012) NDA approval letter for new drug application number 022458, Reference ID: 3124792.
15. Fischer R, Emans N (2000) Molecular farming of pharmaceutical proteins. Transgenic Res 9(4-5): 279-299.
16. Fischer R, Schillberg S, Hellwig S, Twyman RM, Drossard J (2012) GMP issues for recombinant plant-derived pharmaceutical proteins. Biotechnol Adv 30(2): 434-439. doi: 10. 1016/j. biotechadv. 2011. 08. 007.
17. Fischl RM, Stadlmann J, Grass J, Altmann F, Leonard R (2011) The two endo-beta-N-acetylglucosaminidase genes from Arabidopsis thaliana encode cytoplasmic enzymes controlling free N-glycan levels. Plant Mol Biol 77(3): 275-284. doi: 10. 1007/s11103-011-9808-7.
18. Fitchette AC, Cabanes-Macheteau M, Marvin L, Martin B, Satiat-Jeunemaitre B, Gomord V, Crooks K, Lerouge P, Faye L, Hawes C (1999) Biosynthesis and immunolocalization of Lewis a-containing N-glycans in the plant cell. Plant Physiol 121(2): 333-344.
19. Floss DM, Sack M, Arcalis E, Stadlmann J, Quendler H, Rademacher T, Stoger E, Scheller J, Fischer R, Conrad U (2009) Influence of elastin-like peptide fusions on the quantity and quality of a tobacco-derived human immunodeficiency virus-neutralizing antibody. Plant Biotechnol J 7(9): 899-913. doi: 10. 1111/j. 1467-7652. 2009. 00452. x.
20. Goetze AM, Liu YD, Zhang Z, Shah B, Lee E, Bondarenko PV, Flynn GC (2011) High-mannose glycans on the Fc region of therapeutic IgG antibodies increase serum clearance in humans. Glycobiology 21(7): 949-959. doi: 10. 1093/glycob/cwr027.
21. Gomord V, Fitchette AC, Menu-Bouaouiche L, Saint-Jore-Dupas C, Plasson C, Michaud D, Faye L (2010) Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 8(5): 564-587. doi: 10. 1111/j. 1467-7652. 2009. 00497. x.
22. Haddley K (2012) Taliglucerase alfa for the treatment of Gaucher's disease. Drugs Today 48(8): 525-532. doi: 10. 1358/dot. 2012. 48. 8. 1844808.
23. Hiatt A, Cafferkey R, Bowdish K (1989) Production of antibodies in transgenic plants. Nature 342(6245): 76-78. doi: 10. 1038/342076a0.
24. Hoja U, Sonnewald U (2012) Molecular farming in plants In: eLS. Wiley: Chichester. doi: 10. 1002/9780470015902. a0003365. pub2.
25. Hollak CE (2012) An evidence-based review of the potential benefits of taliglucerase alfa in the treatment of patients with Gaucher disease. Core Evid 7: 15-20. doi: 10. 2147/CE. S20201.
26. Holland T, Sack M, Rademacher T, Schmale K, Altmann F, Stadlmann J, Fischer R, Hellwig S (2010) Optimal nitrogen supply as a key to increased and sustained production of a monoclonal full-size antibody in BY-2 suspension culture. Biotechnol Bioeng 107(2): 278-289. doi: 10. 1002/bit. 22800.
27. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231.
28. Jefferis R (2009) Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov 8(3): 226-234. doi: 10. 1038/nrd2804.
29. Katayama H, Nagasu T, Oda Y (2001) Improvement of in-gel digestion protocol for peptide mass fingerprinting by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 15(16): 1416-1421. doi: 10. 1002/rcm. 379.
30. Ko K, Tekoah Y, Rudd PM, Harvey DJ, Dwek RA, Spitsin S, Hanlon CA, Rupprecht C, Dietzschold B, Golovkin M, Koprowski H (2003) Function and glycosylation of plant-derived antiviral monoclonal antibody. Proc Natl Acad Sci USA 100(13): 8013-8018. doi: 10. 1073/pnas. 0832472100.
31. Kolarich D, Altmann F (2000) N-Glycan analysis by matrix-assisted laser desorption/ionization mass spectrometry of electrophoretically separated nonmammalian proteins: application to peanut allergen Ara h 1 and olive pollen allergen Ole e 1. Anal Biochem 285(1): 64-75. doi: 10. 1006/abio. 2000. 4737.
32. Lerouge P, Cabanes-Macheteau M, Rayon C, Fischette-Laine AC, Gomord V, Faye L (1998) N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol Biol 38(1-2): 31-48.
33. Leubner-Metzger G, Frundt C, Vogeli-Lange R, Meins F Jr (1995) Class I [beta]-1, 3-glucanases in the endosperm of tobacco during germination. Plant Physiol 109(3): 751-759.
34. Levanony H, Rubin R, Altschuler Y, Galili G (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol 119(5): 1117-1128.
35. Loos A, van Droogenbroeck B, Hillmer S, Grass J, Kunert R, Cao J, Robinson DG, Depicker A, Steinkellner H (2011a) Production of monoclonal antibodies with a controlled N-glycosylation pattern in seeds of Arabidopsis thaliana. Plant Biotechnol J 9(2): 179-192. doi: 10. 1111/j. 1467-7652. 2010. 00540. x.
36. Loos A, van Droogenbroeck B, Hillmer S, Grass J, Pabst M, Castilho A, Kunert R, Liang M, Arcalis E, Robinson DG, Depicker A, 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(4): 2036-2048. doi: 10. 1104/pp. 110. 171330.
37. Lössl AG, Waheed MT (2011) Chloroplast-derived vaccines against human diseases: achievements, challenges and scopes. Plant Biotechnol J 9(5): 527-539. doi: 10. 1111/j. 1467-7652. 2011. 00615. x.
38. Ma JK, Drake PM, Christou P (2003) The production of recombinant pharmaceutical proteins in plants. Nat Rev Genet 4(10): 794-805. doi: 10. 1038/nrg1177.
39. Morandini F, Avesani L, Bortesi L, van Droogenbroeck B, De Wilde K, Arcalis E, Bazzoni F, Santi L, Brozzetti A, Falorni A, Stoger E, Depicker A, Pezzotti M (2011) Non-food/feed seeds as biofactories for the high-yield production of recombinant pharmaceuticals. Plant Biotechnol J 9(8): 911-921. doi: 10. 1111/j. 1467-7652. 2011. 00605. x.
40. Muntz K (1998) Deposition of storage proteins. Plant Mol Biol 38(1-2): 77-99.
41. Nonogaki H, Morohashi Y (1996) An endo-beta-mannanase develops exclusively in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiol 110(2): 555-559.
42. Okamoto T, Shimada T, Hara-Nishimura I, Nishimura M, Minamikawa T (2003) C-terminal KDEL sequence of a KDEL-tailed cysteine proteinase (sulfhydryl-endopeptidase) is involved in formation of KDEL vesicle and in efficient vacuolar transport of sulfhydryl-endopeptidase. Plant Physiol 132(4): 1892-1900.
43. Paul MJ, Teh AY-H, Twyman RM, Ma JK-C. (2013) Target product selection-where can Molecular Pharming make the difference? Curr Pharm Des [Epub ahead of print].
44. Peters J, Stoger E (2011) Transgenic crops for the production of recombinant vaccines and anti-microbial antibodies. Hum vaccin 7(3): 367-374.
45. Petruccelli S, Otegui MS, Lareu F, Tran Dinh O, Fitchette AC, Circosta A, Rumbo M, Bardor M, Carcamo R, Gomord V, Beachy RN (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(5): 511-527. doi: 10. 1111/j. 1467-7652. 2006. 00200. x.
46. Rademacher T, Sack M, Arcalis E, Stadlmann J, Balzer S, Altmann F, Quendler H, Stiegler G, Kunert R, Fischer R, 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(2): 189-201. doi: 10. 1111/j. 1467-7652. 2007. 00306. x.
47. Ramessar K, Rademacher T, Sack M, Stadlmann J, Platis D, Stiegler G, Labrou N, Altmann F, Ma J, Stoger E, Capell T, Christou P (2008) Cost-effective production of a vaginal protein microbicide to prevent HIV transmission. Proc Natl Acad Sci U S A 105(10): 3727-3732. doi: 10. 1073/pnas. 0708841104.
48. Ramirez N, Rodriguez M, Ayala M, Cremata J, Perez M, Martinez A, Linares M, Hevia Y, Paez R, Valdes R, Gavilondo JV, Selman-Housein G (2003) Expression and characterization of an anti-hepatitis B surface antigenglycosylated mouse antibody in transgenic tobacco (Nicotiana tabacum) plants and its use in the immunopurification of its target antigen. Biotechnol Appl Biochem 38: 223-230. doi: 10. 1042/Ba20030028.
49. Schahs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H (2007) Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol J 5(5): 657-663. doi: 10. 1111/j. 1467-7652. 2007. 00273. x.
50. Shaaltiel Y, Bartfeld D, Hashmueli S, Baum G, Brill-Almon E, Galili G, Dym O, Boldin-Adamsky SA, Silman I, Sussman JL, Futerman AH, 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(5): 579-590. doi: 10. 1111/j. 1467-7652. 2007. 00263. x.
51. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, Weikert SH, Presta LG (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(30): 26733-26740. doi: 10. 1074/jbc. M202069200.
52. Sitrit Y, Hadfield KA, Bennett AB, Bradford KJ, Downie AB (1999) Expression of a polygalacturonase associated with tomato seed germination. Plant Physiol 121(2): 419-428. doi: 10. 1104/Pp. 121. 2. 419.
53. Sriraman R, Bardor M, Sack M, Vaquero C, Faye L, Fischer R, Finnern R, 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(4): 279-287. doi: 10. 1111/j. 1467-7652. 2004. 00078. x.
54. Strasser R, Altmann F, Mach L, Glossl J, 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(1-3): 132-136. doi: 10. 1016/S0014-5793(04)00150-4.
55. Strasser R, Stadlmann J, Schahs M, Stiegler G, Quendler H, Mach L, Glossl J, Weterings K, Pabst M, 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(4): 392-402. doi: 10. 1111/j. 1467-7652. 2008. 00330. x.
56. Takagi H, Hiroi T, Hirose S, Yang L, Takaiwa F (2010) Rice seed ER-derived protein body as an efficient delivery vehicle for oral tolerogenic peptides. Peptides 31(8): 1421-1425. doi: 10. 1016/j. peptides. 2010. 04. 032.
57. Toyooka K, Okamoto T, Minamikawa T (2000) Mass transport of proform of a KDEL-tailed cysteine proteinase (SH-EP) to protein storage vacuoles by endoplasmic reticulum-derived vesicle is involved in protein mobilization in germinating seeds. J Cell Biol 148(3): 453-464.
58. Twyman RM, Stoger E, Schillberg S, Christou P, Fischer R (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol 21(12): 570-578. doi: 10. 1016/j. tibtech. 2003. 10. 002.
59. Verwoerd TC, van Paridon PA, van Ooyen AJ, van Lent JW, Hoekema A, Pen J (1995) Stable accumulation of Aspergillus niger phytase in transgenic tobacco leaves. Plant Physiol 109(4): 1199-1205.
60. Wright A, Morrison SL (1998) Effect of C2-associated carbohydrate structure on Ig effector function: studies with chimeric mouse-human IgG1 antibodies in glycosylation mutants of Chinese hamster ovary cells. J Immunol 160(7): 3393-3402.