Fusion of an Fc chain to a VHH boosts the accumulation levels in arabidopsis seeds

Plant Biotechnology Journal

Volumn 11, Issue 8, 2013, Pages 1006-1016

  De Buck, Sylvie ^a,b   Nolf, Jonah ^a,b   De Meyer, Thomas ^a,b   Virdi, Vikram ^a,b   De Wilde, Kirsten ^a,b   Van Lerberge, Els ^a,b   Van Droogenbroeck, Bart ^a,b,c   Depicker, Ann ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c INSTITUTE FOR AGRICULTURAL AND FISHERIES RESEARCH ILVO   (Belgium)

Author keywords

Arabidopsis thaliana; Molecular farming; Prostate cancer; Seed specific expression; Transgene expression; VHH Fc fusion protein

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; ESCHERICHIA COLI; SUIDAE;

HYBRID PROTEIN; IMMUNOGLOBULIN FC FRAGMENT; NANOBODY;

AMINO ACID SEQUENCE; ANIMAL; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BIOSYNTHESIS; CAMEL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR FARMING; MOLECULAR GENETICS; MOUSE; PROSTATE CANCER; PROTEIN DEGRADATION; SEED-SPECIFIC EXPRESSION; SWINE; TRANSGENE EXPRESSION; TRANSGENIC PLANT; VHH-FC FUSION PROTEIN;

ARABIDOPSIS THALIANA; MOLECULAR FARMING; PROSTATE CANCER; SEED-SPECIFIC EXPRESSION; TRANSGENE EXPRESSION; VHH-FC FUSION PROTEIN;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; CAMELS; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; MICE; MOLECULAR SEQUENCE DATA; PLANTS, GENETICALLY MODIFIED; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SINGLE-DOMAIN ANTIBODIES; SUS SCROFA;

EID: 84884418296     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12094     Document Type: Article

References (81)

1. Andrianov, V., Brodzik, R., Spitsin, S., Bandurska, K., McManus, H., Koprowski, H. and Golovkin, M. (2010) Production of recombinant anthrax toxin receptor (ATR/CMG2) fused with human Fc in planta. Protein Expr. Purif. 70, 158-162.
2. Arakawa, T., Chong, D.K.X., Merritt, J.L. and Langridge, W.H.R. (1997) Expression of cholera toxin B subunit oligomers in transgenic potato plants. Transgenic Res. 6, 403-413.
3. Arbabi Ghahroudi, M., Desmyter, A., Wyns, L., Hamers, R. and Muyldermans, S. (1997) Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett. 414, 521-526.
4. Asano, R., Ikoma, K., Kawaguchi, H., Ishiyama, Y., Nakanishi, T., Umetsu, M., Hayashi, H., Katayose, Y., Unno, M., Kudo, T. and Kumagai, I. (2010) Application of the Fc fusion format to generate tag-free bi-specific diabodies. FEBS J. 277, 477-487.
5. Baud, S., Guyon, V., Kronenberger, J., Wuillème, S., Miquel, M., Caboche, M., Lepiniec, L. and Rochat, C. (2003) Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant J. 33, 75-86.
6. Benchabane, M., Goulet, C., Rivard, D., Faye, L., Gomord, V. and Michaud, D. (2008) Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol. J. 6, 633-648.
7. Bitonti, A.J., Dumont, J.A., Low, S.C., Peters, R.T., Kropp, K.E., Palombella, V.J., Stattel, J.M., Lu, Y., Tan, C.A., Song, J.J., Garcia, A.M., Simister, N.E., Spiekermann, G.M., Lencer, W.I. and Blumberg, R.S. (2004) Pulmonary delivery of an erythropoietin Fc fusion protein in non-human primates through an immunoglobulin transport pathway. Proc. Natl Acad. Sci. USA, 101, 9763-9768.
8. Bok, R.A. and Small, E.J. (2002) Bloodborne biomolecular markers in prostate cancer development and progression. Nat. Rev. Cancer, 2, 918-926.
9. 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.
10. Conley, A.J., Joensuu, J.J., Richman, A. and Menassa, R. (2011) Protein body-inducing fusions for high-level production and purification of recombinant proteins in plants. Plant Biotechnol. J. 9, 419-433.
11. Conrad, U., Plagmann, I., Malchow, S., Sack, M., Floss, D.M., Kruglov, A.A., Nedospasov, S.A., Rose-John, S. and Scheller, J. (2011) ELPylated anti-human TNF therapeutic single-domain antibodies for prevention of lethal septic shock. Plant Biotechnol. J. 9, 22-31.
12. De Buck, S., Virdi, V., De Meyer, T., De Wilde, K., Piron, R., Nolf, J., Van Lerberge, E., De Paepe, A. and Depicker, A. (2012) Production of camel-like antibodies in plants. In Single Domain Antibodies: Methods and Protocols (Muyldermans, S. and Saerens, D., eds), pp. 305-324. New York: Humana Press.
13. De Jaeger, G., Scheffer, S., Jacobs, A., Zambre, M., Zobell, O., Goossens, A., Depicker, A. and Angenon, G. (2002) Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat. Biotechnol. 20, 1265-1268.
14. De Muynck, B., Navarre, C., Nizet, Y., Stadlmann, J. and Boutry, M. (2009) Different subcellular localization and glycosylation for a functional antibody expressed in Nicotiana tabacum plants and suspension cells. Transgenic Res. 18, 467-482.
15. De Muynck, B., Navarre, C. and Boutry, M. (2010) Production of antibodies in plants: status after twenty years. Plant Biotechnol. J. 8, 529-563.
16. De Wilde, K., De Buck, S., Vanneste, K. and Depicker, A. (2013) Recombinant antibody production in Arabidopsis seeds triggers an unfolded protein response. Plant Physiol. 161, 1021-1033.
17. Düring, K., Hippe, S., Kreuzaler, F. and Schell, J. (1990) Synthesis and self-assembly of a functional monoclonal antibody in transgenic Nicotiana tabacum. Plant Mol. Biol. 15, 281-293.
18. Fallahi, H., Scofield, G.N., Badger, M.R., Chow, W.S., Furbank, R.T. and Ruan, Y-L. (2008) Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J. Exp. Bot. 59, 3283-3295.
19. Fischer, R., Schillberg, S., Hellwig, S., Twyman, R.M. and Drossard, J. (2012) GMP issues for recombinant plant-derived pharmaceutical proteins. Biotechnol. Adv. 30, 434-439.
20. Frenken, L.G.J., van der Linden, R.H.J., Hermans, P.W.J.J., Bos, J.W., Ruuls, R.C., de Geus, B. and Verrips, C.T. (2000) Isolation of antigen specific Llama V-HH antibody fragments and their high level secretion by Saccharomyces cerevisiae. J. Biotechnol. 78, 11-21.
21. Gething, M-J. (1999) Role and regulation of the ER chaperone BiP. Semin. Cell Dev. Biol. 10, 465-472.
22. Giersberg, M., Floss, D.M., Kipriyanov, S., Conrad, U. and Scheller, J. (2010) Covalent dimerization of camelidae anti-human TNF-alpha single domain antibodies by the constant kappa light chain domain improves neutralizing activity. Biotechnol. Bioeng. 106, 161-166.
23. Goossens, A., Dillen, W., De Clercq, J., Van Montagu, M. and Angenon, G. (1999) The arcelin-5 gene of Phaseolus vulgaris directs high seed-specific expression in transgenic Phaseolus acutifolius and Arabidopsis plants. Plant Physiol. 120, 1095-1104.
24. Hamers-Casterman, C., Atarhouch, T., Muyldermans, S., Robinson, G., Hammers, C., Songa, E.B., Bendahman, N. and Hammers, R. (1993) Naturally occurring antibodies devoid of light chains. Nature, 363, 446-448.
25. Harmsen, M.M. and De Haard, H.J. (2007) Properties, production, and applications of camelid single-domain antibody fragments. Appl. Microbiol. Biotechnol. 77, 13-22.
26. Hein, M.B., Tang, Y., McLeod, D.A., Janda, K.D. and Hiatt, A. (1991) Evaluation of immunoglobulins from plant-cells. Biotechnol. Prog. 7, 455-461.
27. Hiatt, A., Cafferkey, R. and Bowdish, K. (1989) Production of antibodies in transgenic plants. Nature, 342, 76-78.
28. Hondred, D., Walker, J.M., Mathews, D.E. and Vierstra, R.D. (1999) Use of ubiquitin fusions to augment protein expression in transgenic plants. Plant Physiol. 119, 713-724.
29. Huang, L., Reekmans, G., Saerens, D., Friedt, J-M., Frederix, F., Francis, L., Muyldermans, S., Campitelli, A. and Van Hoof, C. (2005) Prostate-specific antigen immunosensing based on mixed self-assembled monolayers, camel antibodies and colloidal gold enhanced sandwich assays. Biosens. Bioelectron. 21, 483-490.
30. Ismaili, A., Jalali-Javaran, M., Rasaee, M.J., Rahbarizadeh, F., Forouzandeh-Moghadam, M. and Memari, H.R. (2007) Production and characterization of anti-(mucin MUCI) single-domain antibody in tobacco (Nicotiana tabacum cultivar Xanthi). Biotechnol. Appl. Biochem. 47, 11-19.
31. 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.
32. Joensuu, J.J., Conley, A.J., Lienemann, M., Brandle, J.E., Linder, M.B. and Menassa, R. (2010) Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiol. 152, 622-633.
33. HHs) by Aspergillus awamori. Appl. Microbiol. Biotechnol. 66, 384-392.
34. Karg, S.R. and Kallio, P.T. (2009) The production of biopharmaceuticals in plant systems. Biotechnol. Adv. 27, 879-894.
35. Koncz, C. and Schell, J. (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
36. Korouzhdehy, B., Dadmehr, M., Piri, I., Rahbarizadeh, F. and Solouki, M. (2011) Expression of biological active VHH camelid single domain antibody in transgenic tobacco. Afr. J. Biotechnol. 10, 4234-4241.
37. Lau, O.S. and Sun, S.S.M. (2009) Plant seeds as bioreactors for recombinant protein production. Biotechnol. Adv. 27, 1015-1022.
38. Lentz, E.M., Garaicoechea, L., Alfano, E.F., Parreño, V., Wigdorovitz, A. and Bravo-Almonacid, F.F. (2012) Translational fusion and redirection to thylakoid lumen as strategies to improve the accumulation of a camelid antibody fragment in transplastomic tobacco. Planta, 236, 703-714.
39. van der Linden, R.H.J., de Geus, B., Frenken, L.G.J., Peters, H. and Verrips, C.T. (2000) Improved production and function of llama heavy chain antibody fragments by molecular evolution. J. Biotechnol. 80, 261-270.
40. -{increment}{increment}CT method. Methods, 25, 402-408.
41. Logan, G.J., Wang, L., Zheng, M., Ginn, S.L., Coppel, R.L. and Alexander, I.E. (2009) Antigen-specific humoral tolerance or immune augmentation induced by intramuscular delivery of adeno-associated viruses encoding CTLA4-Ig-antigen fusion molecules. Gene Ther. 16, 200-210.
42. 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.
43. 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.
44. Ma, J.K-C., Drake, P.M.W., Chargelegue, D., Obregon, P. and Prada, A. (2005) Antibody processing and engineering in plants, and new strategies for vaccine production. Vaccine, 23, 1814-1818.
45. Magee, A.M., Coyne, S., Murphy, D., Horvath, E.M., Medgyesy, P. and Kavanagh, T.A. (2004) T7 RNA polymerase-directed expression of an antibody fragment transgene in plastids causes a semi-lethal pale-green seedling phenotype. Transgenic Res. 13, 325-337.
46. Mainieri, D., Rossi, M., Archinti, M., Bellucci, M., De Marchis, F., Vavassori, S., Pompa, A., Arcioni, S. and Vitale, A. (2004) Zeolin. A new recombinant storage protein constructed using maize γ-zein and bean phaseolin. Plant Physiol. 136, 3447-3456.
47. 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. and Pezzotti, M. (2011) Non-food/feed seeds as biofactories for the high-yield production of recombinant pharmaceuticals. Plant Biotechnol. J. 9, 911-921.
48. Muyldermans, S. (2001) Single domain camel antibodies: current status. J. Biotechnol. 74, 277-302.
49. ®-expressed EPO-Fc from stably transformed Nicotiana benthamiana plants presenting tetra-antennary N-glycan structures. J. Biotechnol. 160, 242-250.
50. Nguyen, V.K., Muyldermans, S. and Hamers, R. (1998) The specific variable domain of camel heavy-chain antibodies is encoded in the germline. J. Mol. Biol. 275, 413-418.
51. 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.
52. Obregon, P., Chargelegue, D., Drake, P.M.W., Prada, A., Nuttall, J., Frigerio, L. and Ma, J.K-C. (2006) HIV-1 p24-immunoglobulin fusion molecule: a new strategy for plant-based protein production. Plant Biotechnol. J. 4, 195-207.
53. Oesterling, J.E., Moyad, M.A., Wright, G.L. Jr and Beck, G.R. (1995) An analytical comparison of the three most commonly used prostate-specific antigen assays: Tandem-R, Tandem-E, and IMx. Urology, 46, 524-532.
54. Patel, J., Zhu, H., Menassa, R., Gyenis, L., Richman, A. and Brandle, J. (2007) Elastin-like polypeptide fusions enhance the accumulation of recombinant proteins in tobacco leaves. Transgenic Res. 16, 239-249.
55. Paul, M. and Ma, J.K-C. (2011) Plant-made pharmaceuticals: leading products and production platforms. Biotechnol. Appl. Biochem. 58, 58-67.
56. Peters, J. and Stoger, E. (2011) Transgenic crops for the production of recombinant vaccines and anti-microbial antibodies. Hum. Vaccin. 7, 367-374.
57. Phan, H.T. and Conrad, U. (2011) Membrane-based inverse transition cycling: an improved means for purifying plant-derived recombinant protein-elastin-like polypeptide fusions. Int. J. Mol. Sci. 12, 2808-2821.
58. Rahbarizadeh, F., Rasaee, M.J., Forouzandeh, M. and Allameh, A-A. (2006) Over expression of anti-MUC1 single-domain antibody fragments in the yeast Pichia pastoris. Mol. Immunol. 43, 426-435.
59. Saerens, D., Kinne, J., Bosmans, E., Wernery, U., Muyldermans, S. and Conrath, K. (2004) Single domain antibodies derived from dromedary lymph node and peripheral blood lymphocytes sensing conformational variants of prostate-specific antigen. J. Biol. Chem. 279, 51965-51972.
60. Saerens, D., Frederix, F., Reekmans, G., Conrath, K., Jans, K., Brys, L., Huang, L., Bosmans, E., Maes, G., Borghs, G. and Muyldermans, S. (2005) Engineering camel single-domain antibodies and immobilization chemistry for human prostate-specific antigen sensing. Anal. Chem. 77, 7547-7555.
61. Saerens, D., Ghassabeh, G.H. and Muyldermans, S. (2008) Single-domain antibodies as building blocks for novel therapeutics. Curr. Opin. Pharmacol. 8, 600-608.
62. Schaaf, A., Tintelnot, S., Baur, A., Reski, R., Gorr, G. and Decker, E.L. (2005) Use of endogenous signal sequences for transient production and efficient secretion by moss (Physcomitrella patens) cells. BMC Biotechnol. 5, 30.
63. Scheller, J., Henggeler, D., Viviani, A. and Conrad, U. (2004) Purification of spider silk-elastin from transgenic plants and application for human chondrocyte proliferation. Transgenic Res. 13, 51-57.
64. Scheller, J., Leps, M. and Conrad, U. (2006) Forcing single-chain variable fragment production in tobacco seeds by fusion to elastin-like polypeptides. Plant Biotechnol. J. 4, 243-249.
65. T method. Nat. Protoc. 3, 1101-1108.
66. Shapiro, R.I., Wen, D., Levesque, M., Hronowski, X., Gill, A., Garber, E.A., Galdes, A., Strauch, K.L. and Taylor, F.R. (2003) Expression of Sonic hedgehog-Fc fusion protein in Pichia pastoris. Identification and control of post-translational, chemical, and proteolytic modifications. Protein Expr. Purif. 29, 272-283.
67. Spitsin, S., Andrianov, V., Pogrebnyak, N., Smirnov, Y., Borisjuk, N., Portocarrero, C., Veguilla, V., Koprowski, H. and Golovkin, M. (2009) Immunological assessment of plant-derived avian flu H5/HA1 variants. Vaccine, 27, 1289-1292.
68. Streatfield, S.J. (2007) Approaches to achieve high-level heterologous protein production in plants. Plant Biotechnol. J. 5, 2-15.
69. Teh, Y-H.A. and Kavanagh, T.A. (2010) High-level expression of Camelid nanobodies in Nicotiana benthamiana. Transgenic Res. 19, 575-586.
70. Twyman, R.M., Stoger, E., Schillberg, S., Christou, P. and Fischer, R. (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol. 21, 570-578.
71. Van Droogenbroeck, B., Cao, J., Stadlmann, J., Altmann, F., Colanesi, S., Hillmer, S., Robinson, D.G., Van Lerberge, E., Terryn, N., Van Montagu, M., Liang, M., Depicker, A. and De Jaeger, G. (2007) Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc. Natl Acad. Sci. USA, 104, 1430-1435.
72. ®: new ammunition to battle viruses. Antiviral Res. 92, 389-407.
73. Villani, M.E., Morgun, B., Brunetti, P., Marusic, C., Lombardi, R., Pisoni, I., Bacci, C., Desiderio, A., Benvenuto, E. and Donini, M. (2009) Plant pharming of a full-sized, tumour-targeting antibody using different expression strategies. Plant Biotechnol. J. 7, 59-72.
74. Virdi, V., Coddens, A., De Buck, S., Millet, S., Goddeeris, B.M., Cox, E., De Greve, H. and Depicker, A. (2013) Orally fed seeds producing designer IgAs protect weaned piglets against enterotoxigenic Escherichia coli infection. Proc. Natl. Acad. Sci. USA, 110. doi: 10.1073/pnas.1301975110.
75. Vitale, L., Blanset, D., Lowy, I., O'Neill, T., Goldstein, J., Little, S.F., Andrews, G.P., Dorough, G., Taylor, R.K. and Keler, T. (2006) Prophylaxis and therapy of inhalational anthrax by a novel monoclonal antibody to protective antigen that mimics vaccine-induced immunity. Infect. Immun. 74, 5840-5847.
76. Whitlow, M., Bell, B.A., Feng, S-L., Filpula, D., Hardman, K.D., Hubert, S.L., Rollence, M.L., Wood, J.F., Schott, M.E., Milenic, D.E., Yokota, T. and Schlom, J. (1993) An improved linker for single-chain Fv with reduced aggregation and enhanced proteolytic stability. Protein Eng. 6, 989-995.
77. Winichayakul, S., Pernthaner, A., Scott, R., Vlaming, R. and Roberts, N. (2009) Head-to-tail fusions of camelid antibodies can be expressed in planta and bind in rumen fluid. Biotechnol. Appl. Biochem. 53, 111-122.
78. Wycoff, K.L., Belle, A., Deppe, D., Schaefer, L., Maclean, J.M., Haase, S., Trilling, A.K., Liu, S., Leppla, S.H., Geren, I.N., Pawlik, J. and Peterson, J.W. (2011) Recombinant anthrax toxin receptor-Fc fusion proteins produced in plants protect rabbits against inhalational anthrax. Antimicrob. Agents Chemother. 55, 132-139.
79. Yewdell, J.W., Lacsina, J.R., Rechsteiner, M.C. and Nicchitta, C.V. (2011) Out with the old, in with the new? Comparing methods for measuring protein degradation. Cell Biol. Int. 35, 457-462.
80. Yoshida, K., Matsui, T. and Shinmyo, A. (2004) The plant vesicular transport engineering for production of useful recombinant proteins. J. Mol. Catal. B Enzym. 28, 167-171.
81. Zhou, J.X., Tressel, T., Yang, X. and Seewoester, T. (2008) Implementation of advanced technologies in commercial monoclonal antibody production. Biotechnol. J. 3, 1185-1200.