Recombinant antibody production in arabidopsis seeds triggers an unfolded protein response

Plant Physiology

Volumn 161, Issue 2, 2013, Pages 1021-1033

  De Wilde, Kirsten ^a,b   De Buck, Sylvie ^a,b   Vanneste, Kevin ^a,b   Depicker, Ann ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873254593     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.209718     Document Type: Article

References (96)

1. Anelli T, Sitia R (2008) Protein quality control in the early secretory pathway. EMBO J 27: 315-327
2. Baud S, Boutin J-P, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40: 151-160
3. Baud S, Wuillème S, Dubreucq B, de Almeida A, Vuagnat C, Lepiniec L, Miquel M, Rochat C (2007) Function of plastidial pyruvate kinases in seeds of Arabidopsis thaliana. Plant J 52: 405-419
4. Benchabane M, Goulet C, Rivard D, Faye L, Gomord V, Michaud D (2008) Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol J 6: 633-648
5. Boothe J, Nykiforuk C, Shen Y, Zaplachinski S, Szarka S, Kuhlman P, Murray E, Morck D, Moloney MM (2010) Seed-based expression systems for plant molecular farming. Plant Biotechnol J 8: 588-606
6. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25: 288-289
7. Carvalho NDSP, Arentshorst M, Kooistra R, Stam H, Sagt CM, van den Hondel CAMJJ, Ram AFJ (2011) Effects of a defective ERAD pathway on growth and heterologous protein production in Aspergillus niger. Appl Microbiol Biotechnol 89: 357-373
8. Chandrasekharan MB, Bishop KJ, Hall TC (2003) Module-specific regulation of the beta-phaseolin promoter during embryogenesis. Plant J 33: 853-866
9. Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 46: 521-529
10. Day RC, Herridge RP, Ambrose BA, Macknight RC (2008) Transcriptome analysis of proliferating Arabidopsis endosperm reveals biological implications for the control of syncytial division, cytokinin signaling, and gene expression regulation. Plant Physiol 148: 1964-1984 De
11. De Buck S, Virdi V, De Meyer T, De Wilde K, Piron R, Nolf J, Van Lerberge E, De Paepe A, Depicker A (2012) Production of camel like antibodies in plants. In S Muyldermans, D Saerens, eds, Single Domain Antibodies: Methods and Protocols. Methods in Molecular Biology, Vol 911. Springer, New York, pp 305-324 De
12. Jaeger G, Scheffer S, Jacobs A, Zambre M, Zobell O, Goossens A, Depicker A, Angenon G (2002) Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat Biotechnol 20: 1265-1268
13. Ellgaard L, Helenius A (2001) ER quality control: towards an understanding at the molecular level. Curr Opin Cell Biol 13: 431-437
14. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191
15. Ellgaard L, Molinari M, Helenius A (1999) Setting the standards: quality control in the secretory pathway. Science 286: 1882-1888
16. Ernst HA, Olsen AN, Larsen S, Lo Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5: 297-303
17. Feige MJ, Groscurth S, Marcinowski M, Shimizu Y, Kessler H, Hendershot LM, Buchner J (2009) An unfolded CH1 domain controls the assembly and secretion of IgG antibodies. Mol Cell 34: 569-579
18. Fewell SW, Travers KJ, Weissman JS, Brodsky JL (2001) The action of molecular chaperones in the early secretory pathway. Annu Rev Genet 35: 149-191
19. Fischer R, Stoger E, Schillberg S, Christou P, Twyman RM (2004) Plantbased production of biopharmaceuticals. Curr Opin Plant Biol 7: 152-158
20. Focks N, Benning C (1998) wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol 118: 91-101
21. Fomenko DE, Gladyshev VN (2003) Genomics perspective on disulfide bond formation. Antioxid Redox Signal 5: 397-402
22. Fujiwara T, Nambara E, Yamagishi K, Goto DB, Naito S (2002) Storage proteins. The Arabidopsis Book 1: e0020, doi/10.1199/tab.0020
23. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy: analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315
24. Gilbert HF (1998) Protein disulfide isomerase. Methods Enzymol 290: 26-50
25. Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J (2000) Microarray analysis of developing Arabidopsis seeds. Plant Physiol 124: 1570-1581
26. Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266: 605-614
27. Guerfal M, Ryckaert S, Jacobs PP, Ameloot P, Van Craenenbroeck K, Derycke R, Callewaert N (2010) The HAC1 gene from Pichia pastoris: characterization and effect of its overexpression on the production of secreted, surface displayed and membrane proteins. Microb Cell Fact 9: 49
28. Hall TC, Chandrasekharan MB, Li G (1999) Phaseolin: its past, properties, regulation and future. In PR Shewry, R Casey, eds, Seed Proteins. Kluwer, Dordrecht, The Netherlands, pp 209-240
29. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, et al (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619-633
30. Hendershot L, Wei J, Gaut J, Melnick J, Aviel S, Argon Y (1996) Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proc Natl Acad Sci USA 93: 5269-5274
31. Herman EM, Larkins BA (1999) Protein storage bodies and vacuoles. Plant Cell 11: 601-614
32. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264
33. Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysisactivated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20: 3107-3121
34. Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102: 5280-5285
35. Kamauchi S, Nakatani H, Nakano C, Urade R (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J 272: 3461-3476
36. Kauffman KJ, Pridgen EM, Doyle FJ III, Dhurjati PS, Robinson AS (2002) Decreased protein expression and intermittent recoveries in BiP levels result from cellular stress during heterologous protein expression in Saccharomyces cerevisiae. Biotechnol Prog 18: 942-950
37. Kimata Y, Oikawa D, Shimizu Y, Ishiwata-Kimata Y, Kohno K (2004) A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J Cell Biol 167: 445-456
38. Kirst ME, Meyer DJ, Gibbon BC, Jung R, Boston RS (2005) Identification and characterization of endoplasmic reticulum-associated degradation proteins differentially affected by endoplasmic reticulum stress. Plant Physiol 138: 218-231
39. Koizumi N, Martinez IM, Kimata Y, Kohno K, Sano H, Chrispeels MJ (2001) Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. Plant Physiol 127: 949-962
40. Lau OS, Sun SSM (2009) Plant seeds as bioreactors for recombinant protein production. Biotechnol Adv 27: 1015-1022
41. Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, et al (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107: 8063-8070 Lee A-H
42. Lee A-H, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-7459
43. Li Q, Wang B-C, Xu Y, Zhu Y-X (2007) Systematic studies of 12S seed storage protein accumulation and degradation patterns during Arabidopsis seed maturation and early seedling germination stages. J Biochem Mol Biol 40: 373-381
44. Liebrand TWH, Smit P, Abd-El-Haliem A, de Jonge R, Cordewener JHG, America AHP, Sklenar J, Jones AME, Robatzek S, Thomma BPHJ, et al (2012) Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiol 159: 1819-1833
45. Lisbona F, Rojas-Rivera D, Thielen P, Zamorano S, Todd D, Martinon F, Glavic A, Kress C, Lin JH, Walter P, et al (2009) BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1a. Mol Cell 33: 679-691 Liu J-X
46. Liu J-X, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22: 2930-2942
47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408
48. 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: 179-192
49. Loos A, Van Droogenbroeck B, Hillmer S, Grass J, Pabst M, Castilho A, Kunert R, LiangM, Arcalis E, Robinson DG, et al (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
50. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275 Lu D-P
51. Lu D-P, Christopher DA (2008) Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol Genet Genomics 280: 199-210 Ma JK-C
52. Ma JK-C, Barros E, Bock R, Christou P, Dale PJ, Dix PJ, Fischer R, Irwin J, Mahoney R, Pezzotti M, et al (2005) Molecular farming for new drugs and vaccines: current perspectives on the production of pharmaceuticals in transgenic plants. EMBO Rep 6: 593-599
53. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449
54. Martínez IM, Chrispeels MJ (2003) Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15: 561-576
55. Morandini F, Avesani L, Bortesi L, Van Droogenbroeck B, De Wilde K, Arcalis E, Bazzoni F, Santi L, Brozzetti A, Falorni A, et al (2011) Nonfood/ feed seeds as biofactories for the high-yield production of recombinant pharmaceuticals. Plant Biotechnol J 9: 911-921
56. Moreno AA, Orellana A (2011) The physiological role of the unfolded protein response in plants. Biol Res 44: 75-80
57. Nagashima Y, Mishiba K-i, Suzuki E, Shimada Y, Iwata Y, Koizumi N (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1: 29
58. Nakatsukasa K, Brodsky JL (2008) The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 9: 861-870
59. Naouar N, Vandepoele K, Lammens T, Casneuf T, Zeller G, van Hummelen P, Weigel D, Rätsch G, Inzé D, Kuiper M, et al (2009) Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant J 57: 184-194
60. Ng DTW, Spear ED, Walter P (2000) The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J Cell Biol 150: 77-88 Nishikawa S-i
61. Nishikawa S-i, Brodsky JL, Nakatsukasa K (2005) Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD). J Biochem 137: 551-555 Noh S-J
62. Noh S-J, Kwon CS, Oh D-H, Moon JS, Chung W-I (2003) Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene 311: 81-91
63. Okada T, Yoshida H, Akazawa R, Negishi M, Mori K (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNAactivated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366: 585-594
64. Oono Y, Wakasa Y, Hirose S, Yang L, Sakuta C, Takaiwa F (2010) Analysis of ER stress in developing rice endosperm accumulating b-amyloid peptide. Plant Biotechnol J 8: 691-718
65. Pagnussat GC, Yu H-J, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie L-F, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132: 603-614
66. Peters J, Stoger E (2011) Transgenic crops for the production of recombinant vaccines and anti-microbial antibodies. Hum Vaccin 7: 367-374
67. Petruccelli S, OteguiMS, Lareu F, Tran Dinh O, Fitchette A-C, Circosta A, Rumbo M, Bardor M, Carcamo R, Gomord V, et al (2006) A KDELtagged 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: 511-527
68. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45
69. Pilon M, Schekman R, Römisch K (1997) Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J 16: 4540-4548
70. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, et al (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31: 224-228
71. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110
72. Ruuska SA, Girke T, Benning C, Ohlrogge JB (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14: 1191-1206
73. Ruuska SA, Ohlrogge JB (2001) Protocol for small-scale RNA isolation and transcriptional profiling of developing Arabidopsis seeds. Biotechniques 31: 752-758
74. Saerens D, Kinne J, Bosmans E, Wernery U, Muyldermans S, 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
75. Sanchez P, de Torres Zabala M, GrantM(2000) AtBI-1, a plant homologue of Bax inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J 21: 393-399
76. Scheuner D, Song BB, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7: 1165-1176
77. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101-1108
78. Sharma AK, Sharma MK (2009) Plants as bioreactors: recent developments and emerging opportunities. Biotechnol Adv 27: 811-832
79. Simons JF, Ferro-Novick S, RoseMD, Helenius A (1995) BiP/Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast. J Cell Biol 130: 41-49
80. Sitia R, Braakman I (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426: 891-894
81. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3
82. Smyth GK (2005) Limma: linear models for microarray data. In RC Gentleman, VJ Carey, S Dudoit, R Irizarry, W Huber, eds, Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Springer, New York, pp 397-420
83. Spencer MWB, Casson SA, Lindsey K (2007) Transcriptional profiling of the Arabidopsis embryo. Plant Physiol 143: 924-940
84. Stoger E, Ma JK-C, Fischer R, Christou P (2005) Sowing the seeds of success: pharmaceutical proteins from plants. Curr Opin Biotechnol 16: 167-173
85. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258
86. Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274: 1152-1171
87. Urade R (2009) The endoplasmic reticulum stress signaling pathways in plants. Biofactors 35: 326-331 van
88. Anken E, Braakman I (2005) Versatility of the endoplasmic reticulum protein folding factory. Crit Rev Biochem Mol Biol 40: 191-228 Van
89. Van Droogenbroeck B, Cao JY, Stadlmann J, Altmann F, Colanesi S, Hillmer S, Robinson DG, Van Lerberge E, Terryn N, Van Montagu M, et al (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 Van
90. Van Droogenbroeck B, De Wilde K, Depicker A (2009) Production of antibody fragments in Arabidopsis seeds. In L Faye, V Gomord, eds, Recombinant Proteins from Plants. Humana Press, New York, pp 89-101
91. Vitale A, Boston RS (2008) Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9: 1581-1588
92. White JA, Todd J, Newman T, Focks N, Girke T, de Ilárduya OM, Jaworski JG, Ohlrogge JB, Benning C (2000) A new set of Arabidopsis expressed sequence tags from developing seeds: the metabolic pathway from carbohydrates to seed oil. Plant Physiol 124: 1582-1594
93. Xu P, Raden D, Doyle FJ III, Robinson AS (2005) Analysis of unfolded protein response during single-chain antibody expression in Saccharomyces cerevisiae reveals different roles for BiP and PDI in folding. Metab Eng 7: 269-279
94. Xu P, Robinson AS (2009) Decreased secretion and unfolded protein response up-regulation are correlated with intracellular retention for single-chain antibody variants produced in yeast. Biotechnol Bioeng 104: 20-29
95. Yamamoto M, Maruyama D, Endo T, Nishikawa S-i (2008) Arabidopsis thaliana has a set of J proteins in the endoplasmic reticulum that are conserved from yeast to animals and plants. Plant Cell Physiol 49: 1547-1562
96. Yoshida H, Haze K, Yanagi H, Yura T, Mori K (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins: involvement of basic leucine zipper transcription factors. J Biol Chem 273: 33741-33749